Cordyceps militaris Immunomodulatory Protein Promotes the Phagocytic Ability of Macrophages through the TLR4-NF-κB Pathway
Abstract
:1. Introduction
2. Results and Discussion
2.1. CMIMP Enhanced Phagocytic and Bactericidal Activity of Macrophages
2.2. CMIMP Enlarged the Size and F-Actin Expression of Macrophages
2.3. Role of TLR4 in CMIMP-Mediated Cell Phagocytosis
2.4. Role of the NF-κB Pathway in CMIMP-Mediated Cell Phagocytosis
3. Materials and Methods
3.1. Materials
3.2. Measurement of the Phagocytic Activity
3.3. Measurement of Cell Size
3.4. Measurement of F-Actin Expression
3.5. Assessing the Role of TLR4-NF-κB Pathway in Cell Phagocytosis
3.6. Statistical Analysis
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Motta, F.; Gershwin, M.E.; Selmi, C. Mushrooms and immunity. J. Autoimmun. 2021, 117, 102576. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.; Yan, H.; Chen, J.; Zhang, X. Bioactive proteins from mushrooms. Biotechnol. Adv. 2011, 29, 667–674. [Google Scholar] [CrossRef] [PubMed]
- Yang, A.; Fan, H.; Zhao, Y.; Chen, X.; Zhu, Z.; Zha, X.; Zhao, Y.; Chai, X.; Li, J.; Tu, P.; et al. An immune-stimulating proteoglycan from the medicinal mushroom Huaier up-regulates NF-κB and MAPK signaling via Toll-like receptor 4. J. Biol. Chem. 2019, 294, 2628–5268. [Google Scholar] [CrossRef] [Green Version]
- Kino, K.; Yamashita, A.; Yamaoka, K.; Watanabe, J.; Tanaka, S.; Ko, K.; Shimizu, K.; Tsunoo, H. Isolation and characterization of a new immunomodulatory protein, ling zhi-8 (LZ-8), from Ganoderma lucidium. J. Biol. Chem. 1989, 264, 472–478. [Google Scholar] [CrossRef]
- Wu, G.G.; Sun, Y.; Deng, T.S.; Song, L.L.; Li, P.; Zeng, H.J.; Tang, X.M. Identification and functional characterization of a novel immunomodulatory protein from Morchella conica SH. Front. Immunol. 2020, 11, 559770. [Google Scholar] [CrossRef]
- Parra, D.; Rieger, A.M.; Li, J.; Zhang, Y.A.; Randall, L.M.; Hunter, C.A.; Barreda, D.R.; Sunyer, J.O. Pivotal Advance: Peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4(+) T cells. J. Leukocyte Biol. 2012, 91, 525–536. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stuart, L.M.; Ezekowitz, R.A.B. Phagocytosis: Elegant complexity. Immunity 2005, 22, 539–550. [Google Scholar] [CrossRef] [Green Version]
- Jaumouille, V.; Grinstein, S. Receptor mobility, the cytoskeleton, and particle binding during phagocytosis. Curr. Opin. Cell Biol. 2011, 23, 22–29. [Google Scholar] [CrossRef]
- Rana, T.; Bera, A.K.; Das, S.; Bhattacharya, D.; Pan, D.; Bandyopadhyay, S.; De, S.; Das, S.K. Mushroom lectin protects arsenic induced apoptosis in hepatocytes of rodents. Hum. Exp. Toxicol. 2011, 30, 307–317. [Google Scholar] [CrossRef]
- Wang, Y.; Zhang, Y.; Shao, J.; Wu, B.; Li, B. Potential immunomodulatory activities of a lectin from the mushroom Latiporus sulphureus. Int. J. Biol. Macromol. 2019, 130, 399–406. [Google Scholar] [CrossRef] [PubMed]
- Sheu, F.; Chien, P.J.; Hsieh, K.Y.; Chin, K.L.; Huang, W.T.; Tsao, C.Y.; Chen, Y.F.; Cheng, H.C.; Chang, H.H. Purification, cloning, and functional characterization of a novel immunomodulatory protein from Antrodia camphorata (bitter mushroom) that exhibits TLR2-dependent NF-κB activation and M1 polarization within murine macrophages. J. Agric. Food Chem. 2009, 57, 4130–4141. [Google Scholar] [CrossRef] [PubMed]
- Bai, K.C.; Sheu, F. A novel protein from edible fungi Cordyceps militaris that induces apoptosis. J. Food Drug Anal. 2018, 26, 21–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ng, T.B.; Wang, H.X. Pharmacological actions of Cordyceps, a prized folk medicine. J. Pharm. Pharmacol. 2005, 57, 1509–1519. [Google Scholar] [CrossRef]
- Zhu, S.J.; Pan, J.; Zhao, B.; Liang, J.; Wu, Z.Y.; Yang, J.J. Comparisons on enhancing the immunity of fresh and dry Cordyceps militaris in vivo and in vitro. J. Ethnopharmacol. 2013, 149, 713–719. [Google Scholar] [CrossRef]
- Byung Tae, P.; Kwang Heum, N.; Eui Cha, J.; Jae Wan, P.; Ha Hyung, K. Antifungal and anticancer activities of a protein from the mushroom Cordyceps militaris. Korean J. Physiol. Pharmacol. 2009, 13, 49–54. [Google Scholar]
- Jung, E.C.; Kim, K.D.; Chan, H.B.; Ju, C.K.; Kim, D.K.; Kim, H.H. A mushroom lectin from ascomycete Cordyceps militaris. Biochim. Biophis. Acta (BBA)-Gen. Subj. 2007, 1770, 833–838. [Google Scholar] [CrossRef]
- Wong, J.H.; Ng, T.B.; Wang, H.; Sze, S.C.; Zhang, K.Y.; Li, Q.; Lu, X. Cordymin, an antifungal peptide from the medicinal fungus Cordyceps militaris. Phytomedicine 2011, 18, 387–392. [Google Scholar] [CrossRef]
- Wong, J.H.; Wang, H.; Ng, T.B. A haemagglutinin from the medicinal fungus Cordyceps militaris. Biosci. Rep. 2009, 29, 321–327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fan, H.B.; Zheng, Q.W.; Han, Q.; Zou, Y.; Liu, Y.L.; Guo, L.Q.; Lin, J.F. Effect and mechanism of a novel Cordyceps militaris immunomodulatory protein on the differentiation of macrophages. Food Biosci. 2021, 43, 101268. [Google Scholar] [CrossRef]
- Das, R.; Ganapathy, S.; Settle, M.; Plow, E.F. Plasminogen promotes macrophage phagocytosis in mice. Blood 2014, 124, 679. [Google Scholar] [CrossRef] [Green Version]
- De Melo, R.H.; do Amaral, A.E.; Menolli, R.A.; Ayala, T.S.; de Cassia Garcia Simao, R.; de Santana-Filho, A.P.; Sassaki, G.L.; Kadowaki, M.K.; da Conceicao Silva, J.L. β-(1-->3)-Glucan of the southern bracket mushroom, Ganoderma australe (Agaricomycetes), stimulates phagocytosis and interleukin-6 production in mouse peritoneal macrophages. Int. J. Med. Mushrooms 2016, 18, 313–320. [Google Scholar] [CrossRef] [PubMed]
- Ni, W.Y.; Wu, M.F.; Liao, N.C.; Yeh, M.Y.; Lu, H.F.; Hsueh, S.C.; Liu, J.Y.; Huang, Y.P.; Chang, C.H.; Chung, J.G. Extract of medicinal mushroom Agaricus blazei Murill enhances the non-specific and adaptive immune activities in BALB/c mice. In Vivo 2013, 27, 779–786. [Google Scholar]
- Evans, E. Kinetics of granulocyte phagocytosis: Rate limited by cytoplasmic viscosity and constrained by cell size. Cell Motil. Cytoskelet. 1989, 14, 544–551. [Google Scholar] [CrossRef]
- Kim, K.A.; Choi, S.K.; Choi, H.S. Corn silk induces nitric oxide synthase in murine macrophages. Exp. Mol. Med. 2004, 36, 545–550. [Google Scholar] [CrossRef] [Green Version]
- Howard, T.; Oresajo, C. The kinetics of chemotactic peptide-induced change in F-actin content, F-actin distribution, and the shape of neutrophils. J. Cell Biol. 1985, 101, 1078–1085. [Google Scholar] [CrossRef] [Green Version]
- Zhuang, Z.; Zhang, Y.; Sun, S.; Li, Q.; Chen, K.; An, C.; Wang, L.; van den Beucken, J.J.J.P.; Wang, H. Control of matrix stiffness using methacrylate–gelatin hydrogels for a macrophage-mediated inflammatory response. ACS Biomater. Sci. Eng. 2020, 6, 3091–3102. [Google Scholar] [CrossRef] [PubMed]
- Sanjuan, M.A.; Dillon, C.P.; Tait, S.W.G.; Moshiach, S.; Dorsey, F.; Connell, S.; Komatsu, M.; Tanaka, K.; Cleveland, J.L.; Withoff, S.; et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 2007, 450, 1253–1257. [Google Scholar] [CrossRef] [PubMed]
- Blander, J.M.; Medzhitov, R. Regulation of phagosome maturation by signals from Toll-like receptors. Science 2004, 304, 1014–1018. [Google Scholar] [CrossRef]
- Zang, L.H.; Wang, J.; Ren, Y.L.; Liu, W.W.; Yu, Y.; Zhao, S.Y.; Otkur, W.; Zhao, Y.X.; Hayashi, T.; Tashiro, S.; et al. Activated toll-like receptor 4 is involved in oridonin-induced phagocytosis via promotion of migration and autophagy-lysosome pathway in RAW264.7 macrophages. Int. Immunopharmacol. 2019, 66, 99–108. [Google Scholar] [CrossRef]
- Cui, S.N.; Wu, Q.Q.; Wang, J.; Li, M.; Qian, J.; Li, S.H. Quercetin inhibits LPS-induced macrophage migration by suppressing the iNOS/FAK/paxillin pathway and modulating the cytoskeleton. Cell Adhes. Migr. 2019, 13, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akira, S.; Uematsu, S.; Takeuchi, O. Pathogen recognition and innate immunity. Cell 2006, 124, 783–801. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Franchi, N.; Schiavon, F.; Betti, M.; Canesi, L.; Ballarin, L. Insight on signal transduction pathways involved in phagocytosis in the colonial ascidian Botryllus schlosseri. J. Invertebr. Pathol. 2013, 112, 260–266. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.J.; Xu, Z.M.; Zhang, C.M.; Dai, H.Y.; Ji, X.Q.; Wang, X.F.; Li, C. Pyrrolidine dithiocarbamate inhibits nuclear factor-kappa B pathway activation, and regulates adhesion, migration, invasion and apoptosis of endometriotic stromal cells. Mol. Human Reprod. 2011, 17, 175–181. [Google Scholar] [CrossRef] [PubMed]
- Qiao, J.; Xu, L.H.; He, J.; Ouyang, D.Y.; He, X.H. Cucurbitacin E exhibits anti-inflammatory effect in RAW 264.7 cells via suppression of NF-kappa B nuclear translocation. Inflamm. Res. 2013, 62, 461–469. [Google Scholar] [CrossRef] [PubMed]
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Fan, H.-B.; Zou, Y.; Han, Q.; Zheng, Q.-W.; Liu, Y.-L.; Guo, L.-Q.; Lin, J.-F. Cordyceps militaris Immunomodulatory Protein Promotes the Phagocytic Ability of Macrophages through the TLR4-NF-κB Pathway. Int. J. Mol. Sci. 2021, 22, 12188. https://doi.org/10.3390/ijms222212188
Fan H-B, Zou Y, Han Q, Zheng Q-W, Liu Y-L, Guo L-Q, Lin J-F. Cordyceps militaris Immunomodulatory Protein Promotes the Phagocytic Ability of Macrophages through the TLR4-NF-κB Pathway. International Journal of Molecular Sciences. 2021; 22(22):12188. https://doi.org/10.3390/ijms222212188
Chicago/Turabian StyleFan, Hong-Bo, Yuan Zou, Qing Han, Qian-Wang Zheng, Ying-Li Liu, Li-Qiong Guo, and Jun-Fang Lin. 2021. "Cordyceps militaris Immunomodulatory Protein Promotes the Phagocytic Ability of Macrophages through the TLR4-NF-κB Pathway" International Journal of Molecular Sciences 22, no. 22: 12188. https://doi.org/10.3390/ijms222212188