The Yin and Yang Effect of the Apelinergic System in Oxidative Stress
Abstract
:1. Physiology of the Apelin/APJ System
2. Apelin/APJ System and Oxidative Stress
2.1. Oxidative Stress-Linked Hypertension, Atherosclerosis, and Pre-Eclampsia
2.2. Oxidative Stress and Diabetic Microvascular Complications
2.3. Oxidative Stress and Cardiac Function
2.4. Oxidative Stress and Ischemia/Reperfusion Injury
2.5. Oxidative Stress, Obesity, and Insulin Resistance
2.6. Oxidative Stress and Aging
2.7. Oxidative Stress in the Central Nervous System
2.8. Oxidative Stress and Osteoporosis
2.9. Drug-Induced Oxidative Stress
2.10. Oxidative Stress and Cancer
3. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Tatemoto, K.; Hosoya, M.; Habata, Y.; Fujii, R.; Kakegawa, T.; Zou, M.X.; Kawamata, Y.; Fukusumi, S.; Hinuma, S.; Kitada, C.; et al. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem. Biophys. Res.Commun. 1998, 251, 471–476. [Google Scholar] [CrossRef]
- Lee, D.K.; Cheng, R.; Nguyen, T.; Fan, T.; Kariyawasam, A.P.; Liu, Y.; Osmond, D.H.; George, S.R.; O’Dowd, B.F. Characterization of apelin, the ligand for the APJ receptor. J. Neurochem. 2000, 74, 34–41. [Google Scholar] [CrossRef]
- O’Dowd, B.F.; Heiber, M.; Chan, A.; Heng, H.H.; Tsui, L.C.; Kennedy, J.L.; Shi, X.; Petronis, A.; George, S.R.; Nguyen, T. A human gene that shows identity with the gene encoding the angiotensin receptor is located on chromosome 11. Gene 1993, 136, 355–360. [Google Scholar] [CrossRef]
- Durham, A.L.; Speer, M.Y.; Scatena, M.; Giachelli, C.M.; Shanahan, C.M. Role of smooth muscle cells in vascular calcification: Implications in atherosclerosis and arterial stiffness. Cardiovasc. Res. 2018, 114, 590–600. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, X.L.; Liu, J.Q.; Zhou, H.; Chen, L.X. Apelin/APJ system: A critical regulator of vascular smooth muscle cell. J. Cell Physiol. 2018, 233, 5180–5188. [Google Scholar] [CrossRef] [PubMed]
- Antushevich, H.; Wojcik, M. Apelin in disease. Clin. Chim. Acta 2018, 483, 241–248. [Google Scholar] [CrossRef] [PubMed]
- Mughal, A.; O’Rourke, S.T. Vascular effects of apelin: Mechanisms and therapeutic potential. Pharmacol. Ther. 2018, 190, 139–147. [Google Scholar] [CrossRef]
- Pouresmaeili-Babaki, E.; Esmaeili-Mahani, S.; Abbasnejad, M.; Ravan, H. Protective effect of neuropeptide apelin-13 on 6-hydroxydopamine-induced neurotoxicity in SH-SY5Y dopaminergic cells: Involvement of its antioxidant and antiapoptotic properties. Rejuv. Res. 2018, 21, 162–167. [Google Scholar] [CrossRef]
- Kurowska, P.; Barbe, A.; Rozycka, M.; Chmielinska, J.; Dupont, J.; Rak, A. Apelin in reproductive physiology and pathology of different species: A critical review. Int. J. Endocrinol. 2018, 2018, 9170480. [Google Scholar] [CrossRef] [Green Version]
- Tian, Y.; Chen, R.; Jiang, Y.; Bai, B.; Yang, T.; Liu, H. The protective effects and mechanisms of Apelin/APJ system on ischemic stroke: A promising therapeutic target. Front. Neurol. 2020, 11, 75. [Google Scholar] [CrossRef]
- Wu, Y.; Wang, X.; Zhou, X.; Cheng, B.; Li, G.; Bai, B. Temporal expression of apelin/apelin receptor in ischemic stroke and its therapeutic potential. Front. Mol. Neurosc. 2017, 10, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kang, Y.; Kim, J.; Anderson, J.P.; Wu, J.; Gleim, S.R.; Kundu, R.K.; McLean, D.L.; Kim, J.D.; Park, H.; Jin, S.W.; et al. Apelin-APJ signaling is a critical regulator of endothelial MEF2 activation in cardiovascular development. Circ. Res. 2013, 113, 22–31. [Google Scholar] [CrossRef] [Green Version]
- Medhurst, A.D.; Jennings, C.A.; Robbins, M.J.; Davis, R.P.; Ellis, C.; Winborn, K.Y.; Lawrie, K.W.M.; Hervieu, G.; Riley, G.; Bolaky, J.E.; et al. Pharmacological and immunohistochemical characterization of the APJ receptor and its endogenous ligand apelin. J. Neurochem. 2003, 84, 1162–1172. [Google Scholar] [CrossRef] [PubMed]
- Bennett, M.R.; Sinha, S.; Owens, G.K. Vascular smooth muscle cells in atherosclerosis. Circ. Res. 2016, 118, 692–702. [Google Scholar] [CrossRef] [Green Version]
- Cheng, X.; Cheng, X.S.; Pang, C.C. Venous dilator effect of apelin, an endogenous peptide ligand for the orphan APJ receptor, in conscious rats. Eur. J. Pharmacol. 2003, 470, 171–175. [Google Scholar] [CrossRef]
- Reaux, A.; De Mota, N.; Skultetyova, I.; Lenkei, Z.; El Messari, S.; Gallatz, K.; Corvol, P.; Palkovits, M.; Llorens-Cortès, C. Physiological role of a novel neuropeptide, apelin, and its receptor in the rat brain. J. Neurochem. 2001, 77, 1085–1096. [Google Scholar] [CrossRef]
- Taheri, S.; Murphy, K.; Cohen, M.; Sujkovic, E.; Kennedy, A.; Dhillo, W.; Dakin, C.; Sajedi, A.; Ghatei, M.; Bloom, S. The effects of centrally administered apelin-13 on food intake, water intake and pituitary hormone release in rats. Biochem. Biophys. Res. Commun. 2002, 291, 1208–1212. [Google Scholar] [CrossRef]
- O’Carroll, A.; Lolait, S.J.; Harris, L.E.; Pope, G.R. The apelin receptor APJ: Journey from an orphan to a multifaceted regulator of homeostasis. J. Endocrinol. 2013, 219, R13–R35. [Google Scholar] [CrossRef] [PubMed]
- O’Shea, M.; Hansen, M.J.; Tatemoto, K.; Morris, M.J. Inhibitory effect of apelin-12 on nocturnal food intake in the rat. Nutr. Neurosci. 2003, 6, 163–167. [Google Scholar] [CrossRef]
- Kazemi, F.; Zahedias, S. Effects of exercise training on adipose tissue apelin expression in streptozotocin-nicotinamide induced diabetic rats. Gene 2018, 662, 97–102. [Google Scholar] [CrossRef] [PubMed]
- Wang, G.; Anini, Y.; Wei, W.; Qi, X.; O’Carroll, A.; Mochizuki, T.; Wang, H.; Hellmich, M.R.; Englander, E.W.; Greeley, G.H., Jr. Apelin, a new enteric peptide: Localization in the gastrointestinal tract, ontogeny, and stimulation of gastric cell proliferation and of cholecystokinin secretion. Endocrinology 2004, 145, 1342–1348. [Google Scholar] [CrossRef] [Green Version]
- Chen, P.; Wang, Y.; Chen, L.; Song, N.; Xie, J. Apelin-13 protects dopaminergic neurons against rotenone-induced neurotoxicity through the AMPK/mTOR/ULK1 mediated autophagy activation. Int. J. Mol. Sci. 2020, 21, 8376. [Google Scholar] [CrossRef] [PubMed]
- Chapman, N.A.; Dupre, D.J.; Rainey, J.K. The apelin receptor: Physiology, pathology, cell signaling, and ligand modulation of a peptide-activated class A GPCR. Biochem. Cell Biol. 2014, 92, 431–440. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, N.; Zhang, X.; Fan, X.; Argyris, E.; Fang, J.; Acheampong, E.; DuBois, G.C.; Pomerantz, R.J. The N-terminal domain of APJ, a CNS-based coreceptor for HIV-1, is essential for its receptor function and coreceptor activity. Virology 2003, 317, 84–94. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, D.K.; Ferguson, S.S.; George, S.R.; O’Dowd, B.F. The fate of the internalized apelin receptor is determined by different isoforms of apelin mediating differential interaction with beta-arrestin. Biochem. Biophys. Res. Commun. 2010, 395, 185–189. [Google Scholar] [CrossRef]
- Sharma, M.; Prabhavalkar, K.S.; Bhatt, L.K. Elabela peptide: An emerging target in therapeutics. Curr. Drug Targets 2022, 23, 1304–1318. [Google Scholar]
- Wu, J.Q.; Kosten, T.R.; Zhang, X.Y. Free radicals, antioxidant defense system, and schizophrenia. Prog.Neuropsychopharmacol. Biol. Psychiatry 2013, 46, 200–206. [Google Scholar] [CrossRef] [PubMed]
- Rajendran, P.; Nandakumar, N.; Rengarajan, T.; Palaniswami, R.; Gnanadhas, E.N.; Lakshminarasaiah, U. Antioxidants and human diseases. Clin. Chim. Acta. 2014, 436, 332–347. [Google Scholar] [CrossRef]
- Taniyama, Y.; Griendling, K.K. Reactive oxygen species in the vasculature. Hypertension 2003, 42, 1075–1081. [Google Scholar] [CrossRef] [Green Version]
- Orrenius, S. Reactive oxygen species in mitochondria-mediated cell death. Drug Metab. Rev. 2007, 39, 443–455. [Google Scholar] [CrossRef]
- Pizzino, G.; Irrera, N.; Cucinotta, M.; Pallio, G.; Mannino, F.; Arcoraci, V.; Squadrito, F.; Altavilla, D.; Bitto, A. Oxidative Stress: Harms and Benefits for Human Health. Oxid. Med. Cell Longev. 2017, 2017, 8416763. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kinjo, T.; Higashi, H.; Uno, K.; Kuramoto, N. Apelin/Apelin Receptor System: Molecular Characteristics, Physiological Roles, and Prospects as a Target for Disease Prevention and Pharmacotherapy. Curr. Mol. Pharmacol. 2021, 14, 210–219. [Google Scholar] [CrossRef]
- Ronkainen, V.; Ronkainen, J.J.; Hänninen, S.L.; Leskinen, H.; Ruas, J.L.; Pereira, T.; Poellinger, L.; Vuolteenaho, O.; Tavi, P. Hypoxia inducible factor regulates the cardiac expression and secretion of apelin. FASEB J. 2007, 21, 1821–1830. [Google Scholar] [CrossRef] [Green Version]
- Kleinz, M.J.; Davenport, A.P. Emerging roles of apelin in biology and medicine. Pharmacol. Ther. 2005, 107, 198–211. [Google Scholar] [CrossRef]
- Ishida, J.; Hashimoto, T.; Hashimoto, Y.; Nishiwaki, S.; Iguchi, T.; Harada, S.; Sugaya, T.; Matsuzaki, H.; Yamamoto, R.; Shiota, N.; et al. Regulatory roles for APJ, a seven-transmembrane receptor related to angiotensin-type 1 receptor in blood pressure in vivo. J. Biol. Chem. 2004, 279, 26274–26279. [Google Scholar] [CrossRef] [Green Version]
- Zhong, J.C.; Huang, D.Y.; Liu, G.F.; Jin, H.Y.; Yang, Y.M.; Li, Y.F.; Song, X.H.; Du, K. Effects of all-trans retinoic acid on orphan receptor APJ signaling in spontaneously hypertensive rats. Cardiovasc. Res. 2005, 65, 743–750. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhong, J.C.; Yu, X.Y.; Huang, Y.; Yung, L.M.; Lau, C.W.; Lin, S.G. Apelin modulates aortic vascular tone via endothelial nitric oxidase phosphorylation pathway in diabetic mice. Cardiovasc. Res. 2007, 74, 388–395. [Google Scholar] [CrossRef]
- Gurzu, B.; Petrescu, B.C.; Costuleanu, M.; Petrescu, G. Interactions between apelin and angiotensin II on rat portal vein. J. Renin. Angiotensin. Aldosterone. Syst. 2006, 7, 212–216. [Google Scholar] [CrossRef] [PubMed]
- Sato, T.; Suzuki, T.; Watanabe, H.; Kadowaki, A.; Fukamizu, A.; Liu, P.P.; Kimura, A.; Ito, H.; Penninger, J.M.; Imai, Y.; et al. Apelin is a positive regulator of ACE2 in failing hearts. J. Clin. Investig. 2013, 123, 5203–5211. [Google Scholar] [CrossRef] [Green Version]
- Sabry, M.M.; Mahmoud, M.M.; Shoukry, H.S.; Rashed, L.; Kamar, S.S.; Ahmed, M.M. Interactive effects of apelin, renin-angiotensin system and nitric oxide in treatment of obesity-induced type 2 diabetes mellitus in male albino rats. Arch. Physiol. Biochem. 2019, 125, 244–254. [Google Scholar] [CrossRef] [PubMed]
- Sinha, N.; Dabla, P. Oxidative stress and antioxidants in hypertension-a current review. Curr. Hypertens. Rev. 2015, 11, 132–142. [Google Scholar] [CrossRef]
- Yoshida, K.; Kobayashi, N.; Ohno, T.; Fukushima, H.; Matsuoka, H. Cardioprotective effect of angiotensin II type 1 receptor antagonist associated with bradykinin-endothelial nitric oxide synthase and oxidative stress in dahl salt-sensitive hypertensive rats. J. Hypertens. 2007, 25, 1633–1642. [Google Scholar] [CrossRef]
- Oidor-Chan, V.H.; Hong, E.; Pérez-Severiano, F.; Montes, S.; Torres-Narváez, J.C.; Del Valle-Mondragón, L.; Pastelín-Hernández, G.; Sánchez-Mendoza, A. Fenofibrate plus metformin produces cardioprotection in a type 2 diabetes and acute myocardial infarction model. PPAR Res. 2016, 2016, 8237264. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sowers, J.R. Insulin resistance and hypertension. Am. J. Physiol. Heart Circ. Physiol. 2004, 286, H1597–H1602. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Q.; Cao, J.; Chen, L. Apelin/APJ system: A novel therapeutic target for oxidative stress-related inflammatory diseases. Int. J. Mol. Med. 2016, 37, 1159–1169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wassmann, S.; Nickenig, G. Pathophysiological regulation of the AT1-receptor and implications for vascular disease. J. Hypertens. Suppl. 2006, 24, S15–S21. [Google Scholar] [CrossRef]
- Grootaert, M.O.J.; Bennett, M.R. Vascular smooth muscle cells in atherosclerosis: Time for a re-assessment. Cardiovasc. Res. 2021, 117, 2326–2339. [Google Scholar] [CrossRef]
- Sato, K.; Kihara, M.; Hashimoto, T.; Matsushita, K.; Koide, Y.; Tamura, K.; Hirawa, N.; Toya, Y.; Fukamizu, A.; Umemura, S. Alterations in renal endothelial nitric oxide synthase expression by salt diet in angiotensin type-1a receptor gene knockout mice. J. Am. Soc. Nephrol. 2004, 15, 1756–1763. [Google Scholar] [CrossRef] [Green Version]
- Pueyo, M.E.; Arnal, J.F.; Rami, J.; Michel, J.B. Angiotensin II stimulates the production of NO and peroxynitrite in endothelial cells. Am. J. Physiol. 1998, 274, C214–C220. [Google Scholar] [CrossRef]
- Kihara, M.; Sato, K.; Hashimoto, T.; Imai, N.; Toya, Y.; Umemura, S. Expression of endothelial nitric oxide synthase is suppressed in the renal vasculature of angiotensinogen-gene knockout mice. Cell Tissue Res. 2006, 323, 313–320. [Google Scholar] [CrossRef]
- Ramchandran, R.; Takezako, T.; Saad, Y.; Stull, L.; Fink, B.; Yamada, H.; Dikalov, S.; Harrison, D.G.; Moravec, C.; Karnik, S.S. Angiotensinergic stimulation of vascular endothelium in mice causes hypotension, bradycardia, and attenuated angiotensin response. Proc. Natl. Acad. Sci. USA 2006, 103, 19087–19092. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, L.; Li, L.; Xie, F.; Zhang, Z.; Guo, Y.; Tang, G.; Lv, D.; Lu, Q.; Chen, L.; Li, J. Jagged-1/Notch3 signaling transduction pathway is involved in apelin-13-induced vascular smooth muscle cells proliferation. Acta Biochim. Biophys. Sin. 2013, 45, 875–881. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hashimoto, T.; Kihara, M.; Imai, N.; Yoshida, S.; Shimoyamada, H.; Yasuzaki, H.; Ishida, J.; Toya, Y.; Kiuchi, Y.; Hirawa, N.; et al. Requirement of Apelin-Apelin Receptor System for Oxidative Stress-Linked Atherosclerosis. AJP 2007, 171, 1705–1712. [Google Scholar] [CrossRef] [Green Version]
- Lv, D.; Li, H.; Chen, L. Apelin and APJ, a novel critical factor and therapeutic target for atherosclerosis. Acta Biochim. Biophys. Sin. 2013, 45, 527–533. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mao, X.H.; Tao, S.; Zhang, X.H.; Li, F.; Qin, X.P.; Liao, D.F.; Li, L.F.; Chen, L.X. Apelin-13 promotes monocyte adhesion to human umbilical vein endothelial cell mediated by phosphatidylinositol 3-kinase signaling pathway. Prog. Biochem. Biophys. 2011, 38, 1162–1170. [Google Scholar] [CrossRef]
- Lu, Y.; Zhu, X.; Liang, G.; Cui, R.; Liu, Y.; Wu, S.; Liang, Q.; Liu, G.; Jiang, Y.; Liao, X.; et al. Apelin-APJ induces ICAM-1, VCAM-1 and MCP-1 expression via NF-κB/JNK signal pathway in human umbilical vein endothelial cells. Amino Acids 2012, 43, 2125–2136. [Google Scholar] [CrossRef]
- Ruiz, E.; Gordillo-Moscoso, A.; Padilla, E.; Redondo, S.; Rodriguez, E.; Reguillo, F.; Briones, A.M.; van Breemen, C.; Okon, E.; Tejerina, T. Human vascular smooth muscle cells from diabetic patients are resistant to induced apoptosis due to high Bcl-2 expression. Diabetes 2006, 55, 1243–1251. [Google Scholar] [CrossRef] [Green Version]
- Ruiz, E.; Redondo, S.; Gordillo-Moscoso, A.; Tejerina, T. Pioglitazone induces apoptosis in human vascular smooth muscle cells from diabetic patients involving the transforming growth factor-beta/activin receptor-like kinase-4/5/7/Smad2signaling pathway. J. Pharmacol. Exp. Ther. 2007, 321, 431–438. [Google Scholar] [CrossRef]
- Liberman, M. Oxidant generation predominates around calcifying foci and enhances progression of aortic valve calcification. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 463–470. [Google Scholar] [CrossRef] [Green Version]
- Nakagawa, Y.; Ikeda, K.; Akakabe, Y.; Koide, M.; Uraoka, M. Paracrine osteogenic signals via bone morphogenetic protein-2 accelerate the atheroscle-rotic intimal calcification in vivo. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 1908–1915. [Google Scholar] [CrossRef] [Green Version]
- Newby, A.C.; Zaltsman, A.B. Fibrous cap formation or destruction–the critical importance of vascular smooth muscle cell proliferation, migration and matrix formation. Cardiovasc. Res. 1999, 41, 345–360. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, P.; Wang, A.; Yang, H.; Ai, L.; Zhang, H.; Wang, Y.; Bi, Y.; Fan, H.; Gao, J.; Zhang, H.; et al. Apelin-13 attenuates high glucose-induced calcification of MOVAS cells by regulating MAPKs and PI3K/AKT pathways and ROS-mediated signals. Biomed. Pharmacother. 2020, 128, 110271. [Google Scholar] [CrossRef] [PubMed]
- Chun, H.J.; Ali, Z.A.; Kojima, Y.; Kundu, R.K.; Sheikh, A.Y.; Agrawal, R.; Zheng, L.; Leeper, N.J.; Pearl, N.E.; Patterson, A.J.; et al. Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis. J. Clin. Investig. 2008, 118, 3343–3354. [Google Scholar] [CrossRef] [Green Version]
- Staff, A.C. The two-stage placental model of preeclampsia: An update. J. Reprod. Immunol. 2019, 134–135, 1–10. [Google Scholar] [CrossRef]
- Daskalakis, G.; Papapanagiotou, A. Serum markers for the prediction of preeclampsia. J. Neurol. Neurophysiol. 2015, 6, 264. [Google Scholar]
- Cobellis, L.; De Falco, M.; Mastrogiacomo, A.; Giraldi, D.; Dattilo, D.; Scaffa, C.; Colacurci, N.; De Luca, A. Modulation of apelin and APJ receptor in normal and preeclampsia-complicated placentas. Histol. Histopathol. 2007, 22, 1–8. [Google Scholar] [PubMed]
- Deniz, R.; Baykus, Y.; Ustebay, S.; Ugur, K.; Yavuzkir, S.; Aydin, S. Evaluation of elabela, apelin and nitric oxide findings in maternal blood of normal pregnant women, pregnant women with pre-eclampsia, severe pre-eclampsia and umbilical arteries and venules of newborns. J. Obstet. Gynaecol. Res. 2019, 39, 907–912. [Google Scholar] [CrossRef]
- Gürlek, B.; Yılmaz, A.; Durakoğlugil, M.E.; Karakaş, S.; Kazaz, I.M.; Önal, Ö.; Şatıroğlu, Ö. Evaluation of serum apelin-13 and apelin-36 concentrations in preeclamptic pregnancies. J. Obstet. Gynaecol. Res. 2020, 46, 58–65. [Google Scholar] [CrossRef]
- Inuzuka, H.; Nishizawa, H.; Inagaki, A.; Suzuki, M.; Ota, S.; Miyamura, H.; Miyazaki, J.; Sekiya, T.; Kurahashi, H.; Udagawa, Y. Decreased expression of apelin in placentas from severe pre-eclampsia patients. Hypertens. Pregnancy 2013, 32, 410–421. [Google Scholar] [CrossRef]
- Bortoff, K.D.; Qiu, C.; Runyon, S.; Williams, M.A.; Maitra, R. Decreased maternal plasma apelin concentrations in preeclampsia. Hypertens. Pregnancy 2012, 31, 398–404. [Google Scholar] [CrossRef]
- Van Mieghem, T.; Doherty, A.; Baczyk, D.; Drewlo, S.; Baud, D.; Carvalho, J. Apelin in normal pregnancy and pregnancies complicated by placental insufficiency. Reprod. Sci. 2016, 23, 1037–1043. [Google Scholar] [CrossRef]
- Hamza, R.Z.; Diab, A.A.A.; Zahra, M.H.; Asalah, A.K.; Moursi, S.M.M.; Al-Baqami, N.M.; Al-Salmi, F.A.; Attia, M.S. Correlation between Apelin and Some Angiogenic Factors in the Pathogenesis of Preeclampsia: Apelin-13 as Novel Drug for Treating Preeclampsia and Its Physiological Effects on Placenta. Int. J. Endocrinol. 2021, 15, 5017362. [Google Scholar] [CrossRef] [PubMed]
- Murthi, P.; Pinar, A.A.; Dimitriadis, E.; Samuel, C.S. Inflammasomes—A molecular link for altered immunoregulation and inflammation mediated vascular dysfunction in Preeclampsia. Int. J. Mol. Sci. 2020, 21, 1406. [Google Scholar] [CrossRef] [Green Version]
- Armistead, B.; Kadam, L.; Drewlo, S.; Kohan-Ghadr, H. The role of NFκB in healthy and preeclamptic placenta: Trophoblasts in the spotlight. Int. J. Mol. Sci. 2020, 21, 1775. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ryu, S.; Ornoy, A.; Samuni, A.; Zangen, S.; Kohen, R. Oxidative stress in Cohen diabetic rat model by high-sucrose, low-copper diet: Inducing pancreatic damage and diabetes. Metabolism 2008, 57, 1253–1261. [Google Scholar] [CrossRef] [PubMed]
- Nishida, M.; Okumura, Y.; Oka, T.; Toiyama, K.; Ozawa, S.; Itoi, T.; Hamaoka, K. The role of apelin on the alleviative effect of Angiotensin receptor blocker in unilateral ureteral obstruction-induced renal fibrosis. Nephron. Extra 2012, 2, 39–47. [Google Scholar] [CrossRef] [PubMed]
- Day, R.T.; Cavaglieri, R.C.; Feliers, D. Apelin retards the progression of diabetic nephropathy. Am. J. Physiol. Renal. Physiol. 2013, 304, F788–F800. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zeng, X.J.; Yu, S.P.; Zhang, L.; Wei, L. Neuroprotective effect of the endogenous neural peptide apelin in cultured mouse cortical neurons. Exp. Cell Res. 2010, 316, 1773–1783. [Google Scholar] [CrossRef] [Green Version]
- Tao, Y.; Lu, Q.; Jiang, Y.R.; Qian, J.; Wang, J.Y.; Gao, L.; Jonas, J.B. Apelin in plasma and vitreous and in fibrovascular retinal membranes of patients with proliferative diabetic retinopathy. Investig. Ophthalmol. Vis. Sci. 2010, 51, 4237–4242. [Google Scholar] [CrossRef] [Green Version]
- Lu, Q.; Feng, J.; Jiang, Y.R. The role of apelin in the retina of diabetic rats. PLoS ONE 2013, 8, e69703. [Google Scholar] [CrossRef]
- Saint-Geniez, M.; Masri, B.; Malecaze, F.; Knibiehler, B.; Audigier, Y. Expression of the murine msr/apj receptor and its ligand apelin is upregulated during formation of the retinal vessels. Mech. Dev. 2002, 110, 183–186. [Google Scholar] [CrossRef] [PubMed]
- Foussal, C.; Lairez, O.; Calise, D.; Pathak, A.; Guilbeau-Frugier, C.; Valet, P.; Parini, A.; Kunduzova, O. Activation of catalase by apelin prevents oxidative stress-linked cardiac hypertrophy. FEBS Lett. 2010, 584, 2363–2370. [Google Scholar] [CrossRef] [PubMed]
- Ceylan-Isik, A.F.; Kandadi, M.R.; Xu, X.; Hua, Y.; Chicco, A.J.; Ren, J.; Nair, S. Apelin administration ameliorates high fat diet-induced cardiac hypertrophy and contractile dysfunction. J. Mol. Cell Cardiol. 2013, 63, 4–13. [Google Scholar] [CrossRef] [PubMed]
- Zhong, S.; Guo, H.; Wang, H.; Xing, D.; Lu, T.; Yang, J.; Wang, C. Apelin-13 alleviated cardiac fibrosis via inhibiting the PI3K/Akt pathway to attenuate oxidative stress in rats with myocardial infarction-induced heart failure. Biosci. Rep. 2020, 40, BSR20200040. [Google Scholar] [CrossRef] [Green Version]
- Japp, A.; Cruden, N.; Barnes, G.; Van Gemeren, N.; Mathews, J.; Adamson, J.; Johnston, N.; Denvir, M.; Megson, I.; Flapan, A. Acute cardiovascular effects of apelin in humans: Potential role in patients with chronic heart failure. Circulation 2010, 121, 1818–1827. [Google Scholar] [CrossRef]
- Zhang, F.; Sun, H.J.; Xiong, X.Q.; Chen, Q.; Li, Y.; Kang, Y.; Wang, J.; Gao, X.; Zhu, G. Apelin-13 and APJ in paraventricular nucleus contribute to hypertension via sympathetic activation and vasopressin release in spontaneously hypertensive rats. Acta Physiol. 2014, 212, 17–27. [Google Scholar] [CrossRef]
- Cowled, P.; Fitridge, R. Pathophysiology of Reperfusion Injury. In Mechanisms of Vascular Disease: A Reference Book for Vascular Specialists; University of Adelaide Press: Adelaide, Australia, 2011; ISBN -13 978-0-9871718-2-5. [Google Scholar]
- Lakhan, S.E.; Kirchgessner, A.; Tepper, D.; Aidan, L. Matrix metalloproteinases and blood-brain barrier disruption in acute ischemic stroke. Front. Neurol. 2013, 4, 32. [Google Scholar] [CrossRef] [Green Version]
- Zeng, X.J.; Zhang, L.K.; Wang, H.X.; Lu, L.Q.; Ma, L.Q.; Tang, C.S. Apelin protects heart against ischemia/reperfusion injury in rat. Peptides 2009, 30, 1144–1152. [Google Scholar] [CrossRef]
- Simpkin, J.C.; Yellon, D.M.; Davidson, S.M.; Lim, S.Y.; Wynne, A.M.; Smith, C.C. Apelin-13 and apelin-36 exhibit direct cardioprotective activity against ischemia-reperfusion injury. Basic Res. Cardiol. 2007, 102, 518–528. [Google Scholar] [CrossRef]
- Ashley, E.A.; Powers, J.; Chen, M.; Kundu, R.; Finsterbach, T.; Caffarelli, A.; Deng, A.; Eichhorn, J.; Mahajan, R.; Agrawal, R. The endogenous peptide apelin potently improves cardiac contractility and reduces cardiac loading in vivo. Cardiovasc. Res. 2005, 65, 73–82. [Google Scholar] [CrossRef]
- Xu, W.; Yu, H.; Ma, R.; Ma, L.; Liu, Q.; Shan, H.; Wu, C.; Zhang, R.; Zhou, Y.; Shan, H. Apelin protects against myocardial ischemic injury by inhibiting dynamin-related protein 1. Oncotarget 2017, 8, 100034. [Google Scholar] [CrossRef] [Green Version]
- Li, L.; Zeng, H.; Chen, J.X. Apelin-13 increases myocardial progenitor cells and improves repair post-myocardial infarction. Am. J. Phys. Heart Circ. Phys. 2012, 303, H605–H618. [Google Scholar]
- Kupai, K.; Szabó, R.; Veszelka, M.; Awar, A.A.; Török, S.; Csonka, A.; Baráth, Z.; Pósa, A.; Varga, C. Consequences of exercising on ischemia-reperfusion injury in type 2 diabetic Goto-Kakizaki rat hearts: Role of the HO/NOS system. Diabetol. Metab. Syndr. 2015, 7, 85. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- An, S.; Wang, X.; Shi, H.; Zhang, X.; Meng, H.; Li, W.; Chen, D.; Ge, J. Apelin protects against ischemia-reperfusion injury in diabetic myocardium via inhibiting apoptosis and oxidative stress through PI3K and p38-MAPK signaling pathways. Aging 2020, 12, 25120–25137. [Google Scholar] [CrossRef] [PubMed]
- Robinson, E.; Grieve, D.J. Significance of peroxisome proliferator-activated receptors in the cardiovascular system in health and disease. Pharmacol. Ther. 2009, 122, 246–263. [Google Scholar] [CrossRef] [PubMed]
- Kim, T.; Yang, Q. Peroxisome-proliferator-activated receptors regulate redox signaling in the cardiovascular system. World J. Cardiol. 2013, 5, 164–174. [Google Scholar] [CrossRef] [PubMed]
- Weyker, P.D.; Webb, C.A.; Kiamanesh, D.; Flynn, B.C. Lung ischemia reperfusion injury: A bench-to-bedside review. Semin. Cardiothorac. Vasc. Anesth. 2013, 17, 28–43. [Google Scholar] [CrossRef] [PubMed]
- Xia, F.; Chen, H.; Jin, Z.; Fu, Z. Apelin-13 protects the lungs from ischemia-reperfusion injury by attenuating inflammatory and oxidative stress. Hum. Exp. Toxicol. 2021, 40, 685–694. [Google Scholar] [CrossRef]
- Singh, P.K.; Gari, M.; Choudhury, S.; Shukla, A.; Gangwar, N.; Garg, S.K. Oleic acid prevents isoprenaline-induced cardiac injury: Effects on cellular oxidative stress, inflammation and histopathological alterations. Cardiovasc. Toxicol. 2020, 20, 28–48. [Google Scholar] [CrossRef]
- Beckman, J.S.; Beckman, T.W.; Chen, J.; Marshall, P.A.; Freeman, B.A. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 1990, 87, 1620–1624. [Google Scholar] [CrossRef] [Green Version]
- Gu, Z.; Kaul, M.; Yan, B.; Kridel, S.J.; Cui, J.; Strongin, A.; Smith, J.W.; Liddington, R.C.; Lipton, S.A. S-nitrosylation of matrix metalloproteinases: Signaling pathway to neuronal cell death. Science 2002, 297, 1186–1190. [Google Scholar] [CrossRef]
- Chen, H.; Yoshioka, H.; Kim, G.S.; Jung, J.E.; Okami, N.; Sakata, H.; Maier, C.M.; Narasimhan, P.; Goeders, C.E.; Chan, P.H. Oxidative stress in ischemic brain damage: Mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid. Redox. Signal. 2011, 14, 1505–1517. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chan, P.H. Reactive oxygen radicals in signaling and damage in the ischemic brain. J. Cereb. Blood Flow Metab. 2002, 21, 2–14. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.; Ko, A.R.; Hyun, H.W.; Kang, T.C. ETB receptor-mediated MMP-9 activation induces vasogenic edema via ZO-1 protein degradation following status epilepticus. Neuroscience 2015, 304, 355–367. [Google Scholar] [CrossRef] [PubMed]
- Lochhead, J.J.; McCaffrey, G.; Quigley, C.E.; Finch, J.; DeMarco, K.M.; Nametz, N.; Davis, T.P. Oxidative stress increases blood–brain barrier permeability and induces alterations in occludin during hypoxia–reoxygenation. J. Cereb. Blood Flow Metab. 2010, 30, 1625–1636. [Google Scholar] [CrossRef] [Green Version]
- Thor´en, M.; Azevedo, E.; Dawson, J.; Egido, J.A.; Falcou, A.; Ford, G.A.; Holmin, S.; Mikulik, R.; Ollikainen, J.; Wahlgren, N. Predictors for cerebral edema in acute ischemic stroke treated with intravenous thrombolysis. Stroke 2017, 48, 2464–2471. [Google Scholar] [CrossRef] [Green Version]
- Amani, H.; Habibey, R.; Shokri, F.; Hajmiresmail, S.J.; Akhavan, O.; Mashaghi, A.; Pazoki-Toroudi, H. Selenium nanoparticles for targeted stroke therapy through modulation of inflammatory and metabolic signaling. Sci. Rep. 2019, 9, 6044. [Google Scholar] [CrossRef] [Green Version]
- Yang, Y.; Thompson, J.F.; Taheri, S.; Salayandia, V.M.; McAvoy, T.A.; Hill, J.W.; Yang, Y.; Estrada, E.Y.; Rosenberg, G.A. Early inhibition of MMP activity in ischemic rat brain promotes expression of tight junction proteins and angiogenesis during recovery. J. Cereb. Blood Flow Metab. 2013, 33, 1104–1114. [Google Scholar] [CrossRef] [Green Version]
- Michinaga, S.; Nagase, M.; Matsuyama, E.; Yamanaka, D.; Seno, N.; Fuka, M.; Yamamoto, Y.; Koyama, Y. Amelioration of cold injury-induced cortical brain edema formation by selective endothelin ETB receptor antagonists in mice. PLoS ONE 2014, 9, e102009. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chu, H.; Yang, X.; Huang, C.; Gao, Z.; Tang, Y.; Dong, Q. Apelin-13 protects against ischemic blood-brain barrier damage through the effects of aquaporin-4. Cerebrovasc. Dis. 2017, 44, 10–25. [Google Scholar] [CrossRef]
- Yuan, M.; Ge, M.; Yin, J.; Dai, Z.; Xie, L.; Li, Y.; Liu, X.; Peng, L.; Zhang, G.; Si, J. Isoflurane post-conditioning down-regulates expression of aquaporin 4 in rats with cerebral ischemia/reperfusion injury and is possibly related to bone morphogenetic protein 4/Smad1/5/8 signaling pathway. Biomed. Pharm. 2018, 97, 429–438. [Google Scholar] [CrossRef]
- Gholamzadeh, R.; Ramezani, F.; Tehrani, P.M.; Aboutaleb, N. Apelin-13 attenuates injury following ischemic stroke by targeting matrix metalloproteinases (MMP), endothelin- B receptor, occludin/claudin-5 and oxidative stress. J. Chem. Neuroanat. 2021, 118, 102015. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.E.; Ryu, H.; Kang, T. Status epilepticus induces vasogenic edema via tumor necrosis factor-α/endothelin-1-mediated two different pathways. PLoS ONE 2013, 8, e74458. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, G.; Li, L.; Liao, D.; Wang, Z. Protective effect of Apelin-13 on focal cerebral ischemia-reperfusion injury in rats. Nan Fang Yi Ke Da Xue Xue Bao 2015, 35, 1335–1339. [Google Scholar] [PubMed]
- Duan, J.; Cui, J.; Yang, Z.; Guo, C.; Cao, J.; Xi, M.; Weng, Y.; Yin, Y.; Wang, Y.; Wei, G.; et al. Neuroprotective effect of Apelin 13 on ischemic stroke by activating AMPK/GSK-3beta/Nrf2 signaling. J. Neuroinflammation 2019, 16, 24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, Y.; Zhang, X.J.; Li, L.T.; Cui, H.Y.; Zhang, C.; Zhu, C.H.; Miao, J.Y. Apelin-13 protects against apoptosis by activating AMP-activated protein kinase pathway in ischemia stroke. Peptides 2016, 75, 96–100. [Google Scholar] [CrossRef]
- Gu, Q.; Zhai, L.; Feng, X.; Chen, J.; Miao, Z.; Ren, L.; Qian, X.; Yu, J.; Li, Y.; Xu, X.; et al. Apelin-36, a potent peptide, protects against ischemic brain injury by activating the PI3K/Akt pathway. Neurochem. Int. 2013, 63, 535–540. [Google Scholar] [CrossRef]
- Qiu, J.; Wang, X.; Wu, F.; Wan, L.; Cheng, B.; Wu, Y.; Bai, B. Low dose of Apelin-36 attenuates ER stress-associated apoptosis in rats with Ischemic stroke. Front. Neurol. 2017, 8, 556. [Google Scholar] [CrossRef]
- Zhu, J.; Gao, W.; Shan, X.; Wang, C.; Wang, H.; Shao, Z.; Dou, S.; Jiang, Y.; Wang, C.; Cheng, B. Apelin-36 mediates neuroprotective effects by regulating oxidative stress, autophagy and apoptosis in MPTP-induced Parkinson’s disease model mice. Brain Res. 2020, 1726, 146493. [Google Scholar] [CrossRef]
- Liu, D.R.; Hu, W.; Chen, G.Z. Apelin-12 exerts neuroprotective effect against ischemia-reperfusion injury by inhibiting JNK and P38MAPK signaling pathway in mouse. Eur. Rev. Med. Pharmacol. Sci. 2018, 22, 3888–3895. [Google Scholar]
- Curry, D.W.; Stutz, B.; Andrews, Z.B.; Elsworth, J.D. Targeting AMPK signaling as a neuroprotective strategy in Parkinson’s disease. J. Park. Dis. 2018, 8, 161–181. [Google Scholar] [CrossRef] [Green Version]
- Bao, H.J.; Zhang, L.; Han, W.C.; Dai, D.K. Apelin-13 attenuates traumatic brain injury-induced damage by suppressing autophagy. Neurochem. Res. 2015, 40, 89–97. [Google Scholar] [CrossRef]
- Bircan, B.; Cakir, M.; Kirbag, S.; Gul, H.F. Effect of apelin hormone on renal ischemia/reperfusion induced oxidative damage in rats. Ren. Fail. 2016, 38, 1122–1128. [Google Scholar] [CrossRef] [Green Version]
- Boucher, J.; Masri, B.; Daviaud, D.; Gesta, S.; Guigné, C.; Mazzucotelli, A.; Castan-Laurell, I.; Tack, I.; Knibiehler, B.; Carpéné, C.; et al. Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology 2005, 146, 1764–1771. [Google Scholar] [CrossRef]
- SorhedeWinzell, M.; Magnusson, C.; Ahren, B. The APJ receptor is expressed in pancreatic islets and its ligand, apelin, inhibits insulin secretion in mice. Regul. Pept. 2005, 131, 12–17. [Google Scholar] [CrossRef] [Green Version]
- Wei, L.; Hou, X.; Tatemoto, K. Regulation of apelin mRNA expression by insulin and glucocorticoids in mouse 3T3-L1 adipocytes. Regul. Pept. 2005, 132, 27–32. [Google Scholar] [CrossRef]
- Daviaud, D.; Boucher, J.; Gesta, S.; Dray, C.; Guigne, C.; Quilliot, D.; Ayav, A.; Ziegler, O.; Carpene, C.; Saulnier-Blache, J.; et al. TNF alpha up-regulates apelin expression in human and mouse adipose tissue. FASEB J. 2006, 20, 1528–1530. [Google Scholar] [CrossRef] [PubMed]
- Frier, B.C.; Williams, D.B.; Wright, D.C. The effects of apelin treatment on skeletal muscle mitochondrial content. Am. J. Physiol. -Regul. Integr. Comp. Physiol. 2009, 297, R1761–R1768. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Attané, C.; Foussal, C.; Le Gonidec, S.; Benani, A.; Daviaud, D.; Wanecq, E.; Guzmán-Ruiz, R.; Dray, C.; Bezaire, V.; Rancoule, C. Apelin treatment increases complete fatty acid oxidation, mitochondrial oxidative capacity, and biogenesis in muscle of insulin-resistant mice. Diabetes 2012, 61, 310–320. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Than, A.; Zhang, X.; Leow, M.K.; Poh, C.L.; Chong, S.K.; Chen, P. Apelin attenuates oxidative stress in human adipocytes. J. Biol. Chem. 2014, 289, 3763–3774. [Google Scholar] [CrossRef] [Green Version]
- Milagro, F.I.; Campion, J.; Martinez, J.A. Weight gain induced by high-fat feeding involves increased liver oxidative stress. Obesity 2006, 14, 1118–1123. [Google Scholar] [CrossRef] [PubMed]
- Dray, C.; Knauf, C.; Daviaud, D.; Waget, A.; Boucher, J.; Buléon, M.; Cani, P.D.; Attané, C.; Guigné, C.; Carpéné, C. Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab. 2008, 8, 437–445. [Google Scholar] [CrossRef] [PubMed]
- Rai, R.; Ghosh, A.K.; Eren, M.; Mackie, A.R.; Levine, D.C.; Kim, S.; Cedernaes, J.; Ramirez, V.; Procissi, D.; Smith, L.H.; et al. Downregulation of the apelinergic axis accelerates aging, whereas its systemic restoration improves the mammalian healthspan. Cell Rep. 2017, 21, 1471–1480. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yao, F.; Lv, Y.; Zhang, M.; Xie, W.; Tan, Y.; Gong, D.; Cheng, H.; Liu, D.; Li, L.; Liu, X.; et al. Apelin-13 impedes foam cell formation by activating Class III PI3K/Beclin-1-mediated autophagic pathway. Biochem. Biophys. Res. Comm. 2015, 466, 637–643. [Google Scholar] [CrossRef]
- Xie, F.; Liu, W.; Feng, F.; Li, X.; He, L.; Lv, D.; Qin, X.; Li, L.; Li, L.; Chen, L. Apelin-13 promotes cardiomyocyte hypertrophy via PI3K-Akt-ERK1/2-p70S6K and PI3K-induced autophagy. Acta Biochim. Biophys. Sin. 2015, 47, 969–980. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Busch, R.; Strohbach, A.; Pennewitz, M.; Lorenz, F.; Bahls, M.; Busch, M.C.; Felix, S.B. Regulation of the endothelial apelin/APJ system by hemodynamic fluid flow. Cell. Signal. 2015, 27, 1286–1296. [Google Scholar] [CrossRef]
- Cheng, B.; Chen, J.; Bai, B.; Xin, Q. Neuroprotection of apelin and its signaling pathway. Peptides 2012, 37, 171–173. [Google Scholar] [CrossRef]
- O’Donnell, L.A.; Agrawal, A.; Sabnekar, P.; Dichter, M.A.; Lynch, D.R.; Kolson, D.L. Apelin, an endogenous neuronal peptide, protects hippocampal neurons against excitotoxic injury. J. Neurochem. 2007, 102, 1905–1917. [Google Scholar] [CrossRef]
- Mohseni, F.; Garmabi, B.; Khaksari, M. Apelin-13 attenuates spatial memory impairment by anti-oxidative, anti-apoptosis, and anti-inflammatory mechanism against ethanol neurotoxicity in the neonatal rat hippocampus. Neuropeptides 2021, 87, 102130. [Google Scholar] [CrossRef]
- Xin, Q.; Cheng, B.; Pan, Y.; Liu, H.; Yang, C.; Chen, J.; Bai, B. Neuroprotective effects of apelin-13 on experimental ischemic stroke through suppression of inflammation. Peptides 2015, 63, 55–62. [Google Scholar] [CrossRef]
- Xu, W.; Li, T.; Gao, L.; Zheng, J.; Yan, J.; Zhang, J.; Shao, A. Apelin-13/APJ system attenuates early brain injury via suppression of endoplasmic reticulum stress-associated TXNIP/NLRP3 inflammasome activation and oxidative stress in a AMPK-dependent manner after subarachnoid hemorrhage in rats. J. Neuroinflammation 2019, 16, 247. [Google Scholar] [CrossRef] [PubMed]
- Cherry, J.D.; Olschowka, J.A.; O’Banion, M.K. Neuroinflammation and M2 microglia: The good, the bad, and the inflamed. J. Neuroinflammation 2014, 11, 98. [Google Scholar] [CrossRef] [Green Version]
- Chen, D.; Lee, J.; Gu, X.; Wei, L.; Yu, S.P. Intranasal delivery of Apelin-13 is neuroprotective and promotes angiogenesis after ischemic stroke in mice. ASN Neuro 2015, 7, 1759091415605114. [Google Scholar] [CrossRef] [PubMed]
- Zhou, S.; Guo, X.; Chen, S.; Xu, Z.; Duan, W.; Zeng, B. Apelin-13 regulates LPS-induced N9 microglia polarization involving STAT3 signaling pathway. Neuropeptides 2019, 76, 101938. [Google Scholar] [CrossRef]
- Luo, H.; Xiang, Y.; Qu, X.; Liu, H.; Liu, C.; Li, G.; Han, L.; Qin, X. Apelin-13 suppresses neuroinflammation against cognitive deficit in a streptozotocin-induced rat model of Alzheimer’s disease through activation of BDNF-TrkB signaling pathway. Front. Pharmacol. 2019, 10, 395. [Google Scholar] [CrossRef]
- Zhang, Z.X.; Li, E.; Yan, J.P.; Fu, W.; Shen, P.; Tian, S.W.; You, Y. Apelin attenuates depressive-like behaviour and neuroinflammation in rats co-treated with chronic stress and lipopolysaccharide. Neuropeptides 2019, 77, 101959. [Google Scholar] [CrossRef] [PubMed]
- Keep, R.F.; Hua, Y.; Xi, G. Intracerebral haemorrhage: Mechanisms of injury and therapeutic targets. Lancet Neurol. 2012, 11, 720–731. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, Y.; Guo, H.; Wang, L.; Xu, L.; Zhang, X.; Yu, L.; Liu, Q.; Li, Y.; Zhao, N.; Zhao, N.; et al. Human albumin attenuates excessive innate immunity via inhibition of microglial Mincle/Syk signaling in subarachnoid hemorrhage. Brain Behav. Immun. 2017, 60, 346–360. [Google Scholar] [CrossRef]
- Li, Y.; Li, J.; Li, S.; Li, Y.; Wang, X.; Liu, B.; Fu, Q.; Ma, S. Curcumin attenuates glutamate neurotoxicity in the hippocampus by suppression of ER stress-associated TXNIP/NLRP3 inflammasome activation in a manner dependent on AMPK. Toxicol. Appl. Pharmacol. 2015, 286, 53–63. [Google Scholar] [CrossRef]
- Jaiswal, M.K.; Zech, W.D.; Goos, M.; Leutbecher, C.; Ferri, A.; Zippelius, A.; Carrì, M.T.; Nau, R.; Keller, B.U. Impairment of mitochondrial calcium handling in a mtSOD1 cell culture model of motoneuron disease. BMC Neurosci. 2009, 10, 64. [Google Scholar] [CrossRef] [Green Version]
- Manev, H.; Favaron, M.; Guidotti, A.; Costa, E. Delayed increase of Ca2+ influx elicited by glutamate: Role in neuronal death. Mol. Pharmacol. 1989, 36, 106–112. [Google Scholar] [PubMed]
- Cook, D.R.; Gleichman, A.J.; Cross, S.A.; Doshi, S.; Ho, W.; Jordan-Sciutto, K.L.; Lynch, D.R.; Kolson, D.L. NMDA receptor modulation by the neuropeptide apelin: Implications for excitotoxic injury. J. Neurochem. 2011, 118, 1113–1123. [Google Scholar] [CrossRef] [Green Version]
- Khaksari, M.; Aboutaleb, N.; Nasirinezhad, F.; Vakili, A.; Madjd, Z. Apelin-13 protects the brain against ischemic reperfusion injury and cerebral edema in a transient model of focal cerebral ischemia. J. Mol. Neurosci. 2012, 48, 201–208. [Google Scholar] [CrossRef]
- Ishimaru, Y.; Sumino, A.; Kajioka, D.; Shibagaki, F.; Yamamuro, A.; Yoshioka, Y.; Maeda, S. Apelin protects against NMDA-induced retinal neuronal death via an APJ receptor by activating Akt and ERK1/2, and suppressing TNF-alpha expression in mice. J. Pharmacol. Sci. 2017, 133, 34–41. [Google Scholar] [CrossRef] [PubMed]
- Shibagaki, F.; Ishimaru, Y.; Sumino, A.; Yamamuro, A.; Yoshioka, Y.; Maeda, S. Systemic administration of an apelin receptor agonist prevents NMDA-induced loss of retinal neuronal cells in mice. Neurochem. Res. 2020, 45, 752–759. [Google Scholar] [CrossRef]
- Song, W.; Sun, J.; Su, B.; Yang, R.; Dong, H.; Xiong, L. Ischemic post-conditioning protects the spinal cord from ischemia–reperfusion injury via modulation of redox signaling. J. Thoracic. Cardiovasc. Surg. 2013, 146, 688–695. [Google Scholar] [CrossRef] [Green Version]
- Xu, Z.; Li, Z. Experimental Study on the Role of Apelin-13 in Alleviating Spinal Cord Ischemia Reperfusion Injury Through Suppressing Autophagy. Drug Des. Devel. Ther. 2020, 14, 1571–1581. [Google Scholar] [CrossRef] [Green Version]
- Şişli, H.B.; Hayal, T.B.; Şenkal, S.; Kıratlı, B.; Sağraç, D.; Seçkin, S.; Özpolat, M.; Şahin, F.; Yılmaz, B.; Doğan, A. Apelin Receptor Signaling Protects GT1-7 GnRH Neurons Against Oxidative Stress In Vitro. Cell. Mol. Neurobiol. 2022, 42, 753–775. [Google Scholar] [CrossRef]
- Selkoe, D.J. The molecular pathology of Alzheimer’s disease. Neuron 1991, 6, 487–498. [Google Scholar] [CrossRef]
- Gilgun-Sherki, Y.; Melamed, E.; Offen, D. Oxidative stress induced-neurodegenerative diseases: The need for antioxidants that penetrate the blood brain barrier. Neuropharmacol 2001, 40, 959–975. [Google Scholar] [CrossRef]
- Nunomura, A.; Perry, G.; Aliev, G.; Hirai, K.; Takeda, A.; Balraj, E.K.; Jones, P.K.; Ghanbari, H.; Wataya, T.; Shimohama, S. Oxidative damage is the earliest event in Alzheimer disease. J. Neuropathol. Exp. Neurol. 2001, 60, 759–767. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lovell, M.A.; Xiong, S.; Xie, C.; Davies, P.; Markesbery, W.R. Induction of hyperphosphorylated tau in primary rat cortical neuron cultures mediated by oxidative stress and glycogen synthase kinase-3. J. Alzheimer’s Dis. 2004, 6, 659–671. [Google Scholar] [CrossRef] [PubMed]
- Sahara, N.; Murayama, M.; Lee, B.; Park, J.M.; Lagalwar, S.; Binder, L.I.; Takashima, A. Active c-Jun N-terminal kinase induces caspase cleavage of tau and additional phosphorylation by GSK-3β is required for tau aggregation. Eur. J. Neurosci. 2008, 27, 2897–2906. [Google Scholar] [CrossRef] [PubMed]
- Tamagno, E.; Parola, M.; Bardini, P.; Piccini, A.; Borghi, R.; Guglielmotto, M.; Santoro, G.; Davit, A.; Danni, O.; Smith, M. β-Site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J. Neurochem. 2005, 92, 628–636. [Google Scholar] [CrossRef] [PubMed]
- Supnet, C.; Bezprozvanny, I. The dysregulation of intracellular calcium in Alzheimer disease. Cell Calcium 2010, 47, 183–189. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eren, N.; Deni, Z.; Yildiz, Z.; Mu, F.; Go, N.; Gu, L.; Karabiyik, T. P200-Levels of apelin-13 and total oxidant/antioxidant status in sera of Alzheimer patients. Turk. J. Biochem. 2012, 4, 201–205. [Google Scholar]
- Aminyavari, S.; Zahmatkesh, M.; Farahmandfar, M.; Khodagholi, F.; Dargahi, L.; Zarrindast, M.R. Protective role of Apelin-13 on amyloid beta25-35-induced memory deficit; Involvement of autophagy and apoptosis process. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2018, 89, 322–334. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.; Li, X.; Gao, W.; Wang, Q.; Zhang, L.; Li, Y.; Li, L.; Zhang, L. Cornel Iridoid Glycoside Inhibits Tau Hyperphosphorylation via Regulating Cross-Talk Between GSK-3beta and PP2A Signaling. Front. Pharmacol. 2018, 9, 682. [Google Scholar] [CrossRef] [PubMed]
- Masoumi, J.; Abbasloui, M.; Parvan, R.; Mohammadnejad, D.; Pavon-Djavid, G.; Barzegari, A.; Abdolalizadeh, J. Apelin, a promising target for Alzheimer disease prevention and treatment. Neuropeptides 2018, 70, 76–86. [Google Scholar] [CrossRef]
- Samandari-Bahraseman, M.R.; Elyasi, L. Apelin-13 protects human neuroblastoma SH-SY5Y cells against amyloid-beta induced neurotoxicity: Involvement of antioxidant and antiapoptotic properties. J. Basic Clin. Physiol. Pharmacol. 2022, 33, 599–605. [Google Scholar] [CrossRef]
- Pollanen, M.S.; Bergeron, C.; Weyer, L. Deposition of detergent resistant neurofilaments into Lewy body fibrils. Brain Res. 1992, 603, 121–124. [Google Scholar] [CrossRef]
- Riess, O.; Jakes, R.; Kruger, R. Genetic dissection of familial Parkinson’s disease. Mol. Med. Today 1998, 4, 438–444. [Google Scholar] [CrossRef] [PubMed]
- Yang, F.; Jiang, Q.; Zhao, J.; Ren, Y.; Sutton, M.D.; Feng, J. Parkin stabilizes microtubules through strong binding mediated by three independent domains. J. Biol. Chem. 2005, 280, 17154–17162. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jha, S.K.; Jha, N.K.; Kar, R.; Ambasta, R.K.; Kumar, P. p38 MAPK and PI3K/AKT signalling cascades in Parkinson’s disease. Int. J. Mol. Cell. Med. 2015, 4, 67–86. [Google Scholar] [PubMed]
- Jiang, Y.; Liu, H.; Ji, B.; Wang, Z.; Wang, C.; Yang, C.; Pan, Y.; Chen, J.; Cheng, B.; Bai, B.O. Apelin13 attenuates ER stress-associated apoptosis induced by MPP+ in SHSY5Y cells. Int. J. Mol. Med. 2018, 42, 1732–1740. [Google Scholar] [PubMed] [Green Version]
- Haghparast, E.; Esmaeili-Mahani, S.; Abbasnejad, M.; Sheibani, V. Apelin-13 ameliorates cognitive impairments in 6-hydroxydopamineinduced substantia nigra lesion in rats. Neuropeptides 2018, 68, 28–35. [Google Scholar] [CrossRef]
- Cai, W.J.; Chen, Y.; Shi, L.X.; Cheng, H.R.; Banda, I.; Ji, Y.H.; Wang, Y.T.; Li, X.M.; Mao, Y.X.; Zhang, D.F.; et al. AKT-GSK3β signaling pathway regulates mitochondrial dysfunction-associated OPA1 cleavage contributing to osteoblast apoptosis: Preventative effects of hydroxytyrosol. Oxidative Med. Cell. Longev. 2019, 2019, 4101738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Manolagas, S.C. From estrogen-centric to aging and oxidative stress: A revised perspective of the pathogenesis of osteoporosis. Endocr. Rev. 2010, 31, 266–300. [Google Scholar] [CrossRef] [Green Version]
- Banfi, G.; Iorio, E.L.; Corsi, M.M. Oxidative stress, free radicals and bone remodeling. Clin. Chem. Lab. Med. 2008, 46, 1550–1555. [Google Scholar] [CrossRef]
- Domazetovic, V.; Marcucci, G.; Falsetti, I.; Bilia, A.R.; Vincenzini, M.T.; Brandi, M.L.; Iantomasi, T. Blueberry juice antioxidants protect osteogenic activity against oxidative stress and improve long-term activation of the mineralization process in human osteoblast-like SaOS-2 cells: Involvement of SIRT1. Antioxidants 2020, 9, 125. [Google Scholar] [CrossRef] [Green Version]
- Zhen, Y.F.; Wang, G.D.; Zhu, L.Q.; Tan, S.P.; Zhang, F.Y.; Zhou, X.Z.; Wang, X.D. P53 dependent mitochondrial permeability transition pore opening is required for dexamethasone-induced death of osteoblasts. J. Cell. Physiol. 2014, 229, 1475–1483. [Google Scholar] [CrossRef] [PubMed]
- Menale, C.; Robinson, L.J.; Palagano, E.; Rigoni, R.; Erreni, M.; Almarza, A.J.; Strina, D.; Mantero, S.; Lizier, M.; Forlino, A.; et al. Absence of dipeptidyl peptidase 3 increases oxidative stress and causes bone loss. J. Bone Miner. Res. 2019, 34, 2133–2148. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Qi, H.; Tang, Y.; Shen, H.M. Post-translational modifications of key machinery in the control of mitophagy. Trends Biochem. Sci. 2020, 45, 58–75. [Google Scholar] [CrossRef]
- Zhang, F.; Peng, W.; Zhang, Y.; Dong, W.; Wu, J.; Wang, T.; Xie, Z. P53 and Parkin coregulate mitophagy in bone marrow mesenchymal stem cells to promote the repair of early steroid-induced osteonecrosis of the femoral head. Cell Death Dis. 2020, 11, 42. [Google Scholar] [CrossRef] [Green Version]
- Fan, P.; Yu, X.Y.; Xie, X.H.; Chen, C.H.; Zhang, P.; Yang, C.; Peng, X.; Wang, Y.T. Mitophagy is a protective response against oxidative damage in bone marrow mesenchymal stem cells. Life Sci. 2019, 229, 36–45. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Gao, Z.; Chen, Y.; Guan, M.X. The role of mitochondria in osteogenic, adipogenic and chondrogenic differentiation of mesenchymal stem cells. Protein Cell 2017, 8, 439–445. [Google Scholar] [CrossRef] [Green Version]
- Shen, Y.; Wu, L.; Qin, D.; Xia, Y.; Zhou, Z.; Zhang, X.; Wu, X. Carbon black suppresses the osteogenesis of mesenchymal stem cells: The role of mitochondria. Part. Fibre Toxicol. 2018, 15, 16. [Google Scholar] [CrossRef]
- Jing, X.; Du, T.; Yang, X.; Zhang, W.; Wang, G.; Liu, X.; Li, T.; Jiang, Z. Desferoxamine protects against glucocorticoid-induced osteonecrosis of the femoral head via activating HIF-1α expression. J. Cell. Physiol. 2020, 235, 9864–9875. [Google Scholar] [CrossRef]
- Feng, X.; Yin, W.; Wang, J.; Feng, L.; Kang, Y.J. Mitophagy promotes the stemness of bone marrow-derived mesenchymal stem cells. Exp. Biol. Med. 2020, 246, 97–105. [Google Scholar] [CrossRef]
- Hang, K.; Ye, C.; Xu, J.; Chen, E.; Wang, C.; Zhang, W.; Ni, L.; Kuang, Z.; Ying, L.; Xue, D.; et al. Apelin enhances the osteogenic differentiation of human bone marrow mesenchymal stem cells partly through Wnt/β-catenin signaling pathway. Stem Cell Res. Ther. 2019, 10, 189. [Google Scholar] [CrossRef] [Green Version]
- Chen, L.; Shi, X.; Xie, J.; Weng, S.; Xie, Z.; Tang, J.; Yan, D.; Wang, B.; Fang, K.; Hong, C.; et al. Apelin-13 induces mitophagy in bone marrow mesenchymal stem cells to suppress intracellular oxidative stress and ameliorate osteoporosis by activation of AMPK signaling pathway. Free Radical. Biol. Med. 2021, 163, 356–368. [Google Scholar] [CrossRef] [PubMed]
- Liu, S.; Wang, W.; Yin, L.; Zhu, Y. Influence of Apelin-13 on osteoporosis in Type-2 diabetes mellitus: A clinical study. Pak. J. Med. Sci. 2018, 34, 159–163. [Google Scholar] [CrossRef] [PubMed]
- Tang, S.Y.; Xie, H.; Yuan, L.Q.; Luo, X.H.; Huang, J.; Cui, R.R.; Zhou, H.D.; Wu, X.P.; Liao, E.Y. Apelin stimulates proliferation and suppresses apoptosis of mouse osteoblastic cell line MC3T3-E1 via JNK and PI3-K/Akt signaling pathways. Peptides 2007, 28, 708–718. [Google Scholar] [CrossRef]
- Zeng, X.; Yu, S.P.; Taylor, T.; Ogle, M.; Wei, L. Protective effect of apelin on cultured rat bone marrow mesenchymal stem cells against apoptosis. Stem Cell Res. 2012, 8, 357–367. [Google Scholar] [CrossRef] [Green Version]
- Yan, J.; Wang, A.; Cao, J.; Chen, L. Apelin/APJ system: An emerging therapeutic target for respiratory diseases. Cell. Mol. Life Sci. 2020, 77, 2919–2930. [Google Scholar] [CrossRef] [PubMed]
- Patane, S. Cardiotoxicity: Cisplatin and long-term cancer survivors. Int. J. Cardiol. 2014, 175, 201–202. [Google Scholar] [CrossRef]
- Paken, C.D.; Govender, M.; Pillay, V.; Sewram, A. Review of Cisplatin-Associated Ototoxicity. Semin. Hear. 2019, 40, 108–121. [Google Scholar] [CrossRef]
- El-Awady, S.E.; Moustafa, Y.M.; Abo-Elmatty, D.M.; Radwan, A. Cisplatin-induced cardiotoxicity: Mechanisms and cardioprotective strategies. Eur. J. Pharmacol. 2011, 650, 335–341. [Google Scholar] [CrossRef]
- Ferroni, P.; Della-Morte, D.; Palmirotta, R.; McClendon, M.; Testa, G.; Abete, P. Platinum-based compounds and risk for cardiovascular toxicity in the elderly: Role of the antioxidants in chemoprevention. Rejuvenation Res. 2011, 14, 293–308. [Google Scholar] [CrossRef]
- Zhang, P.; Yi, L.; Meng, G.; Zhang, H.; Sun, H.; Cui, L. Apelin-13 attenuates cisplatin-induced cardiotoxicity through inhibition of ROSmediated DNA damage and regulation of MAPKs and AKT pathways. Free Radical. Res. 2017, 51, 449–459. [Google Scholar] [CrossRef]
- Kamogashira, T.; Fujimoto, C.; Yamasoba, T. Reactive oxygen species, apoptosis, and mitochondrial dysfunction in hearing loss. Biomed. Res. Int. 2015, 2015, 617207. [Google Scholar] [CrossRef] [Green Version]
- Callejo, A.; Sedo-Cabezon, L.; Juan, I.D.; Llorens, J. Cisplatin-Induced Ototoxicity: Effects, Mechanisms and Protection Strategies. Toxics 2015, 3, 268–293. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Majumder, P.; Duchen, M.R.; Gale, J.E. Cellular glutathione content in the organ of Corti and its role during ototoxicity. Front. Cell. Neurosci. 2015, 9, 143. [Google Scholar] [CrossRef] [Green Version]
- Yin, H.; Zhang, H.; Kong, Y.; Wang, C.; Guo, Y.; Gao, Y.; Yuan, L.; Yang, X.; Chen, J. Apelin protects auditory cells from cisplatin-induced toxicity in vitro by inhibiting ROS and apoptosis. Neurosci. Lett. 2020, 728, 134948. [Google Scholar] [CrossRef]
- Topcu, A.; Saral, S.; Mercantepe, T.; Akyildiz, K.; Tumkaya, L.; Yilmaz, A. The effects of apelin-13 against cisplatin-induced nephrotoxicity in rats. Drug Chem. Toxicol. 2023, 46, 47. [Google Scholar] [CrossRef]
- Fettiplace, M.R.; Kowal, K.; Ripper, R.; Young, A.; Lis, K.; Rubinstein, I.; Bonini, M.; Minshall, R.; Weinberg, G. Insulin signaling in bupivacaine-induced cardiac toxicity: Sensitization during recovery and potentiation by lipid emulsion. Anesthesiology 2016, 124, 428–442. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cela, O.; Piccoli, C.; Scrima, R.; Quarato, G.; Marolla, A.; Cinnella, G.; Dambrosio, M.; Capitanio, N. Bupivacaine uncouples the mitochondrial oxidative phosphorylation, inhibits respiratory chain complexes I and III and enhances ROS production: Results of a study on cell cultures. Mitochondrion 2010, 10, 487–496. [Google Scholar] [CrossRef] [PubMed]
- Weinberg, G.L.; Palmer, J.W.; Vade Boncouer, T.R.; Zuechner, M.B.; Edelman, G.; Hoppel, C.L. Bupivacaine inhibits acylcarnitine exchange in cardiac mitochondria. Anesthesiology 2000, 92, 523–528. [Google Scholar] [CrossRef]
- Ye, Y.; Cai, Y.; Xia, E.; Shi, K.; Jin, Z.; Chen, H.; Xia, F.; Xia, Y.; Papadimos, T.J.; Xu, X.; et al. Apelin-13 Reverses Bupivacaine-Induced Cardiotoxicity via the Adenosine Monophosphate–Activated Protein Kinase Pathway. Anesth. Analg. 2021, 133, 1048–1059. [Google Scholar] [CrossRef]
- Gorrini, C.; Harris, I.S.; Mak, T.W. Modulation of oxidative stress as an anticancer strategy. Nat. Rev. Drug Discov. 2013, 12, 931–947. [Google Scholar] [CrossRef]
- Diehn, M.; Cho, R.W.; Lobo, N.A.; Kalisky, T.; Dorie, M.J.; Kulp, A.N.; Qian, D.; Lam, J.S.; Ailles, L.E.; Wong, M.; et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458, 780–783. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, H.M.; Haraguchi, N.; Ishii, H.; Ohkuma, M.; Okano, M.; Mimori, K.; Eguchi, H.; Yamamoto, H.; Nagano, H.; Sekimoto, M.; et al. Increased CD13 expression reduces reactive oxygen species, promoting survival of liver cancer stem cells via an epithelial-mesenchymal transition-like phenomenon. Ann. Surg. Oncol. 2012, 19, 539–548. [Google Scholar] [CrossRef] [PubMed]
- Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zelenka, J.; Koncosova, M.; Ruml, T. Targeting of stress response pathways in the prevention and treatment of cancer. Biotechnol. Adv. 2018, 36, 583–602. [Google Scholar] [CrossRef] [PubMed]
- Marnett, L.J. Oxyradicals and DNA damage. Carcinogenesis 2000, 21, 361–370. [Google Scholar] [CrossRef] [Green Version]
- Panieri, E.; Santoro, M.M. ROS homeostasis and metabolism: A dangerousliason in cancer cells. Cell Death Dis. 2016, 7, e2253. [Google Scholar] [CrossRef] [Green Version]
- Yang, Y.; Lv, S.Y.; Ye, W.; Zhang, L. Apelin/APJ system and cancer. Clin. Chim. Acta 2016, 457, 112–116. [Google Scholar] [CrossRef]
- Berta, J.; Hoda, M.A.; Laszlo, V.; Rozsas, A.; Garay, T.; Torok, S.; Grusch, M.; Berger, W.; Paku, S.; Renyi-Vamos, F.; et al. Apelin promotes lymphangiogenesis and lymph node metastasis. Oncotarget 2014, 5, 4426–4437. [Google Scholar] [CrossRef] [Green Version]
- Hall, C.; Ehrlich, L.; Venter, J.; O’Brien, A.; White, T.; Zhou, T.; Dang, T.; Meng, F.; Invernizzi, P.; Bernuzzi, F.; et al. Inhibition of the apelin/apelin receptor axis decreases cholangiocarcinoma growth. Cancer Lett. 2017, 386, 179–188. [Google Scholar] [CrossRef] [Green Version]
- Diakowska, D.; Markocka-Maczka, K.; Nienartowicz, M.; Rosińczuk, J.; Krzystek-Korpacka, M. Assessment of apelin, apelin receptor, resistin, and adiponectin levels in the primary tumor and serum of patients with esophageal squamous cell carcinoma. Adv. Clin. Exp. Med. 2019, 28, 671–678. [Google Scholar] [CrossRef]
- Masoumi, J.; Jafarzadeh, A.; Khorramdelazad, H.; Abbasloui, M.; Abdolalizadeh, J.; Jamali, N. Role of Apelin/APJ axis in cancer development and progression. Adv. Med. Sci. 2020, 65, 202–213. [Google Scholar] [CrossRef] [PubMed]
- Sorli, S.C.; Le Gonidec, S.; Knibiehler, B.; Audigier, Y. Apelin is a potent activator of tumourneoangiogenesis. Oncogene 2007, 26, 7692–7699. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Han, S.; Wang, G.; Qi, X.; Lee, H.M.; Englander, E.W.; Greeley, G.H., Jr. A possible role for hypoxia-induced apelin expression in enteric cell proliferation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294, R1832–R1839. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.; Wang, Z. Increased oxidative stress as a selective anti cancer therapy. Oxidative Med. Cell. Longev. 2015, 2015, 294303. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Picault, F.X.; Chaves-Almagro, C.; Projetti, F.; Prats, H.; Masri, B.; Audigier, Y. Tumour co-expression of apelin and its receptor is the basis of an autocrine loop involved in the growth of colon adenocarcinomas. Eur. J. Cancer 2014, 50, 663–674. [Google Scholar] [CrossRef]
- Harford-Wright, E.; Andre-Gregoire, G.; Jacobs, K.A.; Treps, L.; Le Gonidec, S.; Leclair, H.M.; Gonzalez-Diest, S.; Roux, Q.; Guillonneau, F.; Loussouarn, D.; et al. Pharmacological targeting of apelin impairs glioblastoma growth. Brain 2017, 140, 2939–2954. [Google Scholar] [CrossRef] [Green Version]
- Grupinska, J.; Budzyn, M.; Brezinski, J.J.; Gryszczynska, B.; Kasprzak, M.P.; Kycler, W.; Leporowska, E.; Iskra, M. Association between clinicopathological features of breast cancer with adipocytokine levels and oxidative stress markers before and after chemotherapy. Biomed. Rep. 2021, 14, 30. [Google Scholar] [CrossRef]
- Muto, J.; Shirabe, K.; Yoshizumi, T.; Ikegami, T.; Aishima, S.; Ishigami, K.; Yonemitsu, Y.; Ikeda, T.; Soejima, Y.; Maehara, Y. The apelin-APJ system induces tumor arteriogenesis in hepato- cellular carcinoma. Anticancer Res. 2014, 34, 5313–5320. [Google Scholar]
- Yoshiya, S.; Shirabe, K.; Imai, D.; Toshima, T.; Yamashita, Y.; Ikegami, T.; Okano, S.; Yoshizumi, T.; Kawanaka, H.; Maehara, Y. Blockade of the apelin-APJ system promotes mouse liver regeneration by activating Kupffer cells after partial hepatectomy. J. Gastroenterol. 2015, 50, 573–582. [Google Scholar] [CrossRef]
Oxidative Stress-Related Effects the Apelinergic System in Different Organs and Tissues | |
---|---|
Cardiovascular system | |
Vasodilation and blood pressure lowering [35,36,37,38,39,40,45] |
|
Promotion of early atherogenesis [48,49,50,51,52,53,54,55,56] |
|
Suppression of vascular calcification processes [62,63] |
|
Prevention of diabetic microvascular complications [75,76,77,78,79,80,81] |
|
Improvement of cardiac function [82,83,84,85] |
|
Protection of myocardiocytes against IRI and reduction of infarct size in diabetic and non-diabetic patients [89,90,91,92,93,95,96,97] |
|
Protection of myocardiocytes against cisplatin-induced injury [201] |
|
Protection of myocardiocytes against bupivacaine-induced injury [210] |
|
Lung | |
Restrainment of IRI-associated damage after pulmonary oedema or acute respiratory distress syndrome [99,100] |
|
Placenta | |
Low apelin levels correlate with the etiopathogenesis of pre-eclampsia by inducing placental ischemia and endothelial dysfunction [67,68,69,70,71,72] |
|
Central nervous system | |
Protection of neurons and BBB against IRI [113,114,115,116,117,118,119,120,121,122,123] |
|
Neuroprotection [45,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177] |
|
Kidney | |
Protection of renal cells against IRI [124] |
|
Protection of renal cells against cisplatin-induced toxicity [206] |
|
Adipose tissue, skeletal muscle, and liver | |
Amelioration of insulin sensitivity [125,126,127,128,129,130,131,132,133] |
|
Bone | |
Maintenance of bone health [192,194,195,196] |
|
Inner ear | |
Protection of cochlear cells against cisplatin-induced injury [205] |
|
Cancer cells | |
Increased serum apelin levels correlate with shorter survival, higher incidence of cancer recurrence, and resistance to anticancer drugs [160,218,219,220,221,222,223,224,225,226,227,228,229,230] |
|
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Fibbi, B.; Marroncini, G.; Naldi, L.; Peri, A. The Yin and Yang Effect of the Apelinergic System in Oxidative Stress. Int. J. Mol. Sci. 2023, 24, 4745. https://doi.org/10.3390/ijms24054745
Fibbi B, Marroncini G, Naldi L, Peri A. The Yin and Yang Effect of the Apelinergic System in Oxidative Stress. International Journal of Molecular Sciences. 2023; 24(5):4745. https://doi.org/10.3390/ijms24054745
Chicago/Turabian StyleFibbi, Benedetta, Giada Marroncini, Laura Naldi, and Alessandro Peri. 2023. "The Yin and Yang Effect of the Apelinergic System in Oxidative Stress" International Journal of Molecular Sciences 24, no. 5: 4745. https://doi.org/10.3390/ijms24054745