Evaluating the Effect of Hypoxia on Human Adult Mesenchymal Stromal Cell Chondrogenesis In Vitro: A Systematic Review
Abstract
:1. Introduction
2. Results
2.1. Tissue Source of MSCs Used
2.2. MSC Markers Assessed
2.3. Stage of Exposure to Hypoxia
2.4. Effect of Hypoxia on Chondrogenic Differentiation: Expansion Stage Only
2.5. Effect of Hypoxia on Chondrogenic Differentiation: Differentiation Stage Only
2.6. Effect of Hypoxia on Chondrogenic Differentiation: During Both Expansion and Differentiation Phase
2.7. Effect of Sequential Exposure to Hypoxia in Both the Expansion Phase and Then the Differentiation Phase
3. Discussion
3.1. Donor Variability of MSCs
3.2. Different Stage and Time of Exposure in Experiments to Hypoxia
3.3. Differing Conditions Used in Both Culture Stage and Differentiation Stage
3.4. Different Characterisation of MSCs
3.5. Risk of Bias
3.6. Possible Biochemical Mechanisms of the Effect of Hypoxia on Chondrogenesis
3.7. The Effect of Hypoxia on Chondrocyte Maturation and Function
3.8. Future Implications
4. Methods
Author Contributions
Funding
Conflicts of Interest
References
- Akkiraju, H.; Nohe, A. Role of Chondrocytes in Cartilage Formation, Progression of Osteoarthritis and Cartilage Regeneration. J. Dev. Biol. 2015, 3, 177–192. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4916494/ (accessed on 17 November 2022). [CrossRef] [PubMed] [Green Version]
- Luo, Y.; Sinkeviciute, D.; He, Y.; Karsdal, M.; Henrotin, Y.; Mobasheri, A.; Önnerfjord, P.; Bay-Jensen, A. The minor collagens in articular cartilage. Protein Cell 2017, 8, 560–572. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alcaide-Ruggiero, L.; Molina-Hernández, V.; Granados, M.M.; Domínguez, J.M. Main and Minor Types of Collagens in the Articular Cartilage: The Role of Collagens in Repair Tissue Evaluation in Chondral Defects. Int. J. Mol. Sci. 2021, 22, 13329. Available online: https://www.mdpi.com/1422-0067/22/24/13329 (accessed on 17 November 2022). [CrossRef] [PubMed]
- Poole, A.R.; Kobayashi, M.; Yasuda, T.; Laverty, S.; Mwale, F.; Kojima, T.; Sakai, T.; Wahl, C.; El-Maadawy, S.; Webb, G.; et al. Type II collagen degradation and its regulation in articular cartilage in osteoarthritis. Ann. Rheum. Dis. 2002, 61 (Suppl. S2), ii78–ii81. Available online: https://ard.bmj.com/content/61/suppl_2/ii78 (accessed on 17 November 2022). [CrossRef] [Green Version]
- Rim, Y.A.; Nam, Y.; Ju, J.H. The Role of Chondrocyte Hypertrophy and Senescence in Osteoarthritis Initiation and Progression. Int. J. Mol. Sci. 2020, 21, 2358. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7177949/ (accessed on 17 November 2022). [CrossRef] [Green Version]
- Zheng, L.; Zhang, Z.; Sheng, P.; Mobasheri, A. The role of metabolism in chondrocyte dysfunction and the progression of osteoarthritis. Ageing Res. Rev. 2021, 66, 101249. Available online: https://www.sciencedirect.com/science/article/pii/S1568163720303846/pdfft?md5=ec0ccabf4979584cfdf8197ce7457fbb&pid=1-s2.0-S1568163720303846-main.pdf&isDTMRedir=Y (accessed on 17 November 2022). [CrossRef]
- Brew, C.J.; Clegg, P.D.; Boot-Handford, R.P.; Andrew, J.G.; Hardingham, T. Gene expression in human chondrocytes in late osteoarthritis is changed in both fibrillated and intact cartilage without evidence of generalised chondrocyte hypertrophy. Ann. Rheum. Dis. 2008, 69, 234–240. [Google Scholar] [CrossRef]
- van der Kraan, P.M.; van den Berg, W.B. Chondrocyte hypertrophy and osteoarthritis: Role in initiation and progression of cartilage degeneration? Osteoarthr. Cartil. 2012, 20, 223–322. Available online: https://www.oarsijournal.com/article/S1063458411003323/pdf (accessed on 17 November 2022). [CrossRef] [Green Version]
- Wang, M.; Shen, J.; Jin, H.; Im, H.-J.; Sandy, J.; Chen, D. Recent progress in understanding molecular mechanisms of cartilage degeneration during osteoarthritis. Ann. N. Y. Acad. Sci. 2011, 1240, 61–69. Available online: https://europepmc.org/articles/pmc3671949?pdf=render (accessed on 17 November 2022). [CrossRef] [Green Version]
- Li, B.; Guan, G.; Mei, L.; Jiao, K.; Li, H. Pathological mechanism of chondrocytes and the surrounding environment during osteoarthritis of temporomandibular joint. J. Cell. Mol. Med. 2021, 25, 4902–4911. Available online: https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/jcmm.16514 (accessed on 17 November 2022). [CrossRef]
- Maumus, M.; Pers, Y.M.; Ruiz, M.; Jorgensen, C.; Noël, D. Mesenchymal stem cells and regenerative medicine: Future perspectives in osteoarthritis. Med. Sci. 2018, 34, 1092–1099. Available online: https://www.medecinesciences.org/articles/medsci/pdf/2018/13/msc170210.pdf (accessed on 17 November 2022).
- Yang, Y.-H.K.; Ogando, C.R.; See, C.W.; Chang, T.-Y.; Barabino, G.A. Changes in phenotype and differentiation potential of human mesenchymal stem cells aging in vitro. Stem Cell Res. Ther. 2018, 9, 131. Available online: https://stemcellres.biomedcentral.com/counter/pdf/10.1186/s13287-018-0876-3 (accessed on 17 November 2022). [CrossRef] [PubMed] [Green Version]
- Pattappa, G.; Zellner, J.; Johnstone, B.; Docheva, D.; Angele, P. Cells under pressure–the relationship between hydrostatic pressure and mesenchymal stem cell chondrogenesis. Eur. Cells Mater. 2019, 36, 360–381. [Google Scholar] [CrossRef] [PubMed]
- Scotti, C.; Gobbi, A.; Nakamura, N.; Peretti, G.M. Stem Cells for Cartilage Regeneration: A Roadmap to the Clinic. Stem Cells Int. 2018, 2018, 7348560. Available online: https://downloads.hindawi.com/journals/sci/2018/7348560.pdf (accessed on 17 November 2022). [CrossRef] [Green Version]
- Yamagata, K.; Nakayamada, S.; Tanaka, Y. Use of mesenchymal stem cells seeded on the scaffold in articular cartilage repair. Inflamm. Regen. 2018, 38, 4. Available online: https://inflammregen.biomedcentral.com/counter/pdf/10.1186/s41232-018-0061-1 (accessed on 17 November 2022). [CrossRef] [PubMed] [Green Version]
- Shen, B.; Wei, A.; Whittaker, S.; Williams, L.A.; Tao, H.; Ma, D.D.; Diwan, A. The role of BMP-7 in chondrogenic and osteogenic differentiation of human bone marrow multipotent mesenchymal stromal cells in vitro. J. Cell. Biochem. 2009, 109, 406–416. Available online: http://www.ncbi.nlm.nih.gov/pubmed/19950204 (accessed on 17 November 2022). [CrossRef]
- Le, H.; Xu, W.; Zhuang, X.; Chang, F.; Wang, Y.; Ding, J. Mesenchymal stem cells for cartilage regeneration. J. Tissue Eng. 2020, 11, 2041731420943839. Available online: https://journals.sagepub.com/doi/pdf/10.1177/2041731420943839 (accessed on 17 November 2022). [CrossRef]
- Solchaga, L.A.; Penick, K.J.; Welter, J.F. Chondrogenic Differentiation of Bone Marrow-Derived Mesenchymal Stem Cells: Tips and Tricks. Methods Mol. Biol. 2011, 698, 253–278. [Google Scholar]
- Ejtehadifar, M.; Shamsasenjan, K.; Movassaghpour, A.; Akbarzadehlaleh, P.; Dehdilani, N.; Abbasi, P.; Molaeipour, Z.; Saleh, M. The Effect of Hypoxia on Mesenchymal Stem Cell Biology. Adv. Pharm. Bull. 2015, 5, 141–149. Available online: https://europepmc.org/articles/pmc4517092?pdf=render (accessed on 17 November 2022). [CrossRef] [Green Version]
- Antebi, B.; Ii, L.A.R.; Walker, K.P.; Asher, A.M.; Kamucheka, R.M.; Alvarado, L.; Mohammadipoor, A.; Cancio, L.C. Short-term physiological hypoxia potentiates the therapeutic function of mesenchymal stem cells. Stem Cell Res. Ther. 2018, 9, 265. Available online: https://stemcellres.biomedcentral.com/counter/pdf/10.1186/s13287-018-1007-x (accessed on 17 November 2022). [CrossRef] [Green Version]
- Adesida, A.B.; Mulet-Sierra, A.; Jomha, N.M. Hypoxia mediated isolation and expansion enhances the chondrogenic capacity of bone marrow mesenchymal stromal cells. Stem Cell Res. Ther. 2012, 3, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baumgartner, L.; Arnhold, S.; Brixius, K.; Addicks, K.; Bloch, W. Human mesenchymal stem cells: Influence of oxygen pressure on proliferation and chondrogenic differentiation in fibrin glue in vitro. J. Biomed. Mater. Res. A 2010, 93, 930–940. [Google Scholar] [CrossRef] [PubMed]
- Boyette, L.B.; Creasey, O.A.; Guzik, L.; Lozito, T.; Tuan, R.S. Human Bone Marrow-Derived Mesenchymal Stem Cells Display Enhanced Clonogenicity but Impaired Differentiation With Hypoxic Preconditioning. Stem Cells Transl. Med. 2014, 3, 241–254. [Google Scholar] [CrossRef] [PubMed]
- Cicione, C.; Muiños-López, E.; Hermida-Gómez, T.; Fuentes-Boquete, I.; Díaz-Prado, S.; Blanco, F.J. Effects of Severe Hypoxia on Bone Marrow Mesenchymal Stem Cells Differentiation Potential. Stem Cells Int. 2013, 2013, 232896. [Google Scholar] [CrossRef] [Green Version]
- Duval, E.; Baugé, C.; Andriamanalijaona, R.; Bénateau, H.; Leclercq, S.; Dutoit, S.; Poulain, L.; Galéra, P.; Boumédiene, K. Molecular mechanism of hypoxia-induced chondrogenesis and its application in in vivo cartilage tissue engineering. Biomaterials 2012, 33, 6042–6051. [Google Scholar] [CrossRef]
- Wang, J.; Liao, Y.; Wu, S.; Huang, H.; Chou, P.; Chiang, E. Adipose Derived Mesenchymal Stem Cells from a Hypoxic Culture Reduce Cartilage Damage. Stem Cell Rev. Rep. 2021, 17, 1796–1809. Available online: https://link.springer.com/article/10.1007/s12015-021-10169-z (accessed on 17 November 2022). [CrossRef]
- Lim, K.-T.; Patel, D.K.; Seonwoo, H.; Kim, J.; Chung, J.H. A fully automated bioreactor system for precise control of stem cell proliferation and differentiation. Biochem. Eng. J. 2019, 150, 107258. Available online: https://www.sciencedirect.com/science/article/pii/S1369703X19301858 (accessed on 17 November 2022). [CrossRef]
- Khan, W.S.; Adesida, A.B.; Hardingham, T.E. Hypoxic conditions increase hypoxia-inducible transcription factor 2α and enhance chondrogenesis in stem cells from the infrapatellar fat pad of osteoarthritis patients. Arthritis Res. Ther. 2007, 9, R55. [Google Scholar] [CrossRef] [Green Version]
- Khan, W.S.; Adesida, A.B.; Tew, S.R.; Lowe, E.T.; Hardingham, T.E. Bone marrow-derived mesenchymal stem cells express the pericyte marker 3G5 in culture and show enhanced chondrogenesis in hypoxic conditions. J. Orthop. Res. 2010, 28, 834–840. [Google Scholar] [CrossRef]
- Lee, J.-S.; Kim, S.K.; Jung, B.-J.; Choi, S.-B.; Choi, E.-Y.; Kim, C.-S. Enhancing proliferation and optimizing the culture condition for human bone marrow stromal cells using hypoxia and fibroblast growth factor-2. Stem Cell Res. 2018, 28, 87–95. Available online: http://ovidsp.ovid.com/ovidweb.cgi?T=JS&PAGE=reference&D=med15&NEWS=N&AN=29448134 (accessed on 17 November 2022). [CrossRef]
- Lee, J.-S.; Park, J.-C.; Kim, T.-W.; Jung, B.-J.; Lee, Y.; Shim, E.-K.; Park, S.; Choi, E.-Y.; Cho, K.-S.; Kim, C.-S. Human bone marrow stem cells cultured under hypoxic conditions present altered characteristics and enhanced in vivo tissue regeneration. Bone 2015, 78, 34–45. [Google Scholar] [CrossRef] [PubMed]
- Legendre, F.; Ollitrault, D.; Gomez-Leduc, T.; Bouyoucef, M.; Hervieu, M.; Gruchy, N.; Mallein-Gerin, F.; Leclercq, S.; Demoor, M.; Galéra, P. Enhanced chondrogenesis of bone marrow-derived stem cells by using a combinatory cell therapy strategy with BMP-2/TGF-beta1, hypoxia, and COL1A1/HtrA1 siRNAs. Sci. Rep. 2017, 7, 3406. Available online: http://ovidsp.ovid.com/ovidweb.cgi?T=JS&PAGE=reference&D=med14&NEWS=N&AN=28611369 (accessed on 17 November 2022). [CrossRef] [PubMed]
- Markway, B.; Tan, G.-K.; Brooke, G.; Hudson, J.E.; Cooper-White, J.J.; Doran, M.R. Enhanced Chondrogenic Differentiation of Human Bone Marrow-Derived Mesenchymal Stem Cells in Low Oxygen Environment Micropellet Cultures. Cell Transplant. 2010, 19, 29–42. Available online: http://ovidsp.ovid.com/ovidweb.cgi?T=JS&PAGE=reference&D=med8&NEWS=N&AN=19878627 (accessed on 17 November 2022). [CrossRef] [PubMed]
- Merceron, C.; Vinatier, C.; Portron, S.; Masson, M.; Amiaud, J.; Guigand, L.; Chérel, Y.; Weiss, P.; Guicheux, J. Differential effects of hypoxia on osteochondrogenic potential of human adipose-derived stem cells. Am. J. Physiol. Physiol. 2010, 298, C355–C364. [Google Scholar] [CrossRef] [PubMed]
- Munir, S.; Foldager, C.B.; Lind, M.; Zachar, V.; Søballe, K.; Koch, T.G. Hypoxia enhances chondrogenic differentiation of human adipose tissue-derived stromal cells in scaffold-free and scaffold systems. Cell Tissue Res. 2013, 355, 89–102. [Google Scholar] [CrossRef] [PubMed]
- Neybecker, P.; Henrionnet, C.; Pape, E.; Mainard, D.; Galois, L.; Loeuille, D.; Gillet, P.; Pinzano, A. In vitro and in vivo potentialities for cartilage repair from human advanced knee osteoarthritis synovial fluid-derived mesenchymal stem cells. Stem Cell Res. Ther. 2018, 9, 329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ohara, T.; Muneta, T.; Nakagawa, Y.; Matsukura, Y.; Ichinose, S.; Koga, H.; Tsuji, K.; Sekiya, I. Hypoxia enhances proliferation through increase of colony formation rate with chondrogenic potential in primary synovial mesenchymal stem cells. J. Med. Dent. Sci. 2016, 63, 61–70. [Google Scholar] [PubMed]
- Pattappa, G.; Schewior, R.; Hofmeister, I.; Seja, J.; Zellner, J.; Johnstone, B.; Docheva, D.; Angele, P. Physioxia Has a Beneficial Effect on Cartilage Matrix Production in Interleukin-1 Beta-Inhibited Mesenchymal Stem Cell Chondrogenesis. Cells 2019, 8, 936. Available online: http://ovidsp.ovid.com/ovidweb.cgi?T=JS&PAGE=reference&D=med16&NEWS=N&AN=31434236 (accessed on 17 November 2022). [CrossRef] [Green Version]
- Pattappa, G.; Thorpe, S.D.; Jegard, N.C.; Heywood, H.K.; de Bruijn, J.D.; Lee, D.A. Continuous and Uninterrupted Oxygen Tension Influences the Colony Formation and Oxidative Metabolism of Human Mesenchymal Stem Cells. Tissue Eng. Part C Methods 2013, 19, 68–79. [Google Scholar] [CrossRef] [Green Version]
- Tian, H.-T.; Zhang, B.; Tian, Q.; Liu, Y.; Yang, S.-H.; Shao, Z.-W. Construction of self-assembled cartilage tissue from bone marrow mesenchymal stem cells induced by hypoxia combined with GDF-5. J. Huazhong Univ. Sci. Technol. 2013, 33, 700–706. [Google Scholar] [CrossRef]
- van de Walle, A.; Faissal, W.; Wilhelm, C.; Luciani, N. Role of growth factors and oxygen to limit hypertrophy and impact of high magnetic nanoparticles dose during stem cell chondrogenesis. Comput. Struct. Biotechnol. J. 2018, 16, 532–542. Available online: http://ovidsp.ovid.com/ovidweb.cgi?T=JS&PAGE=reference&D=pmnm4&NEWS=N&AN=30524668 (accessed on 17 November 2022). [CrossRef] [PubMed]
- Wan Safwani, W.K.Z.; Wong, C.W.; Yong, K.W.; Choi, J.R.; Mat Adenan, N.A.; Omar, S.Z.; Abas, W.A.B.W.; Pingguan-Murphy, B. The effects of hypoxia and serum-free conditions on the stemness properties of human adipose-derived stem cells. Cytotechnology 2016, 68, 1859–1872. [Google Scholar] [CrossRef] [PubMed]
- Weijers, E.M.; Van Den Broek, L.J.; Waaijman, T.; Van Hinsbergh, V.W.M.; Gibbs, S.; Koolwijk, P. The Influence of Hypoxia and Fibrinogen Variants on the Expansion and Differentiation of Adipose Tissue-Derived Mesenchymal Stem Cells. Tissue Eng. Part A 2011, 17, 2675–2685. Available online: http://ovidsp.ovid.com/ovidweb.cgi?T=JS&PAGE=reference&D=med8&NEWS=N&AN=21830936 (accessed on 17 November 2022). [CrossRef] [PubMed]
- Zhao, A.G.; Shah, K.; Freitag, J.; Cromer, B.; Sumer, H. Differentiation Potential of Early- and Late-Passage Adipose-Derived Mesenchymal Stem Cells Cultured under Hypoxia and Normoxia. Stem Cells Int. 2020, 2020, 8898221. [Google Scholar] [CrossRef] [PubMed]
- Dominici, M.; Le Blanc, K.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F.C.; Krause, D.S.; Deans, R.J.; Keating, A.; Prockop, D.J.; Horwitz, E.M. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8, 315–317. Available online: http://www.ncbi.nlm.nih.gov/pubmed/16923606 (accessed on 17 November 2022). [CrossRef] [PubMed]
- Olmedo-Moreno, L.; Aguilera, Y.; Baliña-Sánchez, C.; Martín-Montalvo, A.; Capilla-González, V. Heterogeneity of In Vitro Expanded Mesenchymal Stromal Cells and Strategies to Improve Their Therapeutic Actions. Pharmaceutics 2022, 14, 1112. Available online: https://www.mdpi.com/1999-4923/14/5/1112/pdf?version=1653371370 (accessed on 17 November 2022). [CrossRef] [PubMed]
- Stroncek, D.F.; Jin, P.; McKenna, D.H.; Takanashi, M.; Fontaine, M.J.; Pati, S.; Schäfer, R.; Peterson, E.; Benedetti, E.; Reems, J.-A. Human Mesenchymal Stromal Cell (MSC) Characteristics Vary Among Laboratories When Manufactured From the Same Source Material: A Report by the Cellular Therapy Team of the Biomedical Excellence for Safer Transfusion (BEST) Collaborative. Front. Cell Dev. Biol. 2020, 8, 458. [Google Scholar] [CrossRef]
- Murphy, J.M.; Dixon, K.; Beck, S.; Fabian, D.; Feldman, A.; Barry, F. Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthritis Rheum. 2002, 46, 704–713. Available online: http://www.ncbi.nlm.nih.gov/pubmed/11920406 (accessed on 17 November 2022). [CrossRef]
- Sotiropoulou, P.A.; Perez, S.A.; Salagianni, M.; Baxevanis, C.N.; Papamichail, M. Characterization of the Optimal Culture Conditions for Clinical Scale Production of Human Mesenchymal Stem Cells. Stem Cells 2005, 24, 462–471. Available online: https://stemcellsjournals.onlinelibrary.wiley.com/doi/pdfdirect/10.1634/stemcells.2004-0331 (accessed on 17 November 2022). [CrossRef] [Green Version]
- Rojewski, M.T.; Weber, B.M.; Schrezenmeier, H. Phenotypic Characterization of Mesenchymal Stem Cells from Various Tissues. Transfus. Med. Hemotherapy 2008, 35, 168–184. Available online: https://www.karger.com/Article/Pdf/129013 (accessed on 17 November 2022). [CrossRef] [Green Version]
- Wilson, A.J.; Rand, E.; Webster, A.J.; Genever, P.G. Characterisation of mesenchymal stromal cells in clinical trial reports: Analysis of published descriptors. Stem Cell Res. Ther. 2021, 12, 360. [Google Scholar] [CrossRef] [PubMed]
- Horwitz, E.M.; Le Blanc, K.; Dominici, M.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F.C.; Deans, R.J.; Krause, D.S.; Keating, A.; International Society for Cellular, T. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005, 7, 393–395. Available online: http://www.ncbi.nlm.nih.gov/pubmed/16236628 (accessed on 17 November 2022). [CrossRef] [PubMed]
- Lafont, J.E. Lack of oxygen in articular cartilage: Consequences for chondrocyte biology. Int. J. Exp. Pathol. 2010, 91, 99–106. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2965894/pdf/iep0091-0099.pdf (accessed on 17 November 2022). [CrossRef] [PubMed]
- Ishikawa, Y.; Ito, T. Kinetics of hemopoietic stem cells in a hypoxic culture. Eur. J. Haematol. 1988, 40, 126–129. Available online: http://www.ncbi.nlm.nih.gov/pubmed/3278928 (accessed on 17 November 2022). [CrossRef]
- Koh, M.Y.; Powis, G. Passing the baton: The HIF switch. Trends Biochem. Sci. 2012, 37, 364–372. [Google Scholar] [CrossRef] [Green Version]
- Zhou, G.; Garofalo, S.; Mukhopadhyay, K.; Lefebvre, V.; Smith, C.; Eberspaecher, H.; de Crombrugghe, B. A 182 bp fragment of the mouse pro alpha 1 (II) collagen gene is sufficient to direct chondrocyte expression in transgenic mice. J. Cell Sci. 1995, 108 Pt 12, 3677–3684. Available online: http://www.ncbi.nlm.nih.gov/pubmed/8719874 (accessed on 17 November 2022). [CrossRef]
- Sekiya, I.; Tsuji, K.; Koopman, P.; Watanabe, H.; Yamada, Y.; Shinomiya, K.; Nifuji, A.; Noda, M. SOX9 Enhances Aggrecan Gene Promoter/Enhancer Activity and Is Up-regulated by Retinoic Acid in a Cartilage-derived Cell Line, TC6. J. Biol. Chem. 2000, 275, 10738–10744. Available online: https://www.jbc.org/content/275/15/10738.full.pdf (accessed on 17 November 2022). [CrossRef] [Green Version]
- D’Ippolito, G.; Diabira, S.; Howard, G.A.; Roos, B.A.; Schiller, P.C. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 2006, 39, 513–522. Available online: http://www.ncbi.nlm.nih.gov/pubmed/16616713 (accessed on 17 November 2022). [CrossRef]
- Taheem, D.K.; Jell, G.; Gentleman, E. Hypoxia Inducible Factor-1α in Osteochondral Tissue Engineering. Tissue Eng. Part B Rev. 2020, 26, 105–115. [Google Scholar] [CrossRef] [Green Version]
- Buravkova, L.B.; Andreeva, E.R.; Gogvadze, V.; Zhivotovsky, B. Mesenchymal stem cells and hypoxia: Where are we? Mitochondrion 2014, 19 Pt A, 105–112. Available online: http://www.ncbi.nlm.nih.gov/pubmed/25034305 (accessed on 17 November 2022).
- Pfander, D.; Swoboda, B.; Cramer, T. The role of HIF-1alpha in maintaining cartilage homeostasis and during the pathogenesis of osteoarthritis. Arthritis Res. Ther. 2006, 8, 104. [Google Scholar] [CrossRef] [Green Version]
- Thoms, B.L.; Dudek, K.A.; Lafont, J.E.; Murphy, C.L. Hypoxia Promotes the Production and Inhibits the Destruction of Human Articular Cartilage. Arthritis Care Res. 2013, 65, 1302–1312. [Google Scholar] [CrossRef] [PubMed]
- Yang, S.; Kim, J.; Ryu, J.-H.; Oh, H.; Chun, C.-H.; Kim, B.J.; Min, B.H.; Chun, J.-S. Hypoxia-inducible factor-2α is a catabolic regulator of osteoarthritic cartilage destruction. Nat. Med. 2010, 16, 687–693. [Google Scholar] [CrossRef] [PubMed]
- Hirao, M.; Tamai, N.; Tsumaki, N.; Yoshikawa, H.; Myoui, A. Oxygen Tension Regulates Chondrocyte Differentiation and Function during Endochondral Ossification. J. Biol. Chem. 2006, 281, 31079–31092. Available online: https://pubmed.ncbi.nlm.nih.gov/16905540/ (accessed on 17 November 2022). [CrossRef] [PubMed] [Green Version]
- Shukunami, C.; Ohta, Y.; Sakuda, M.; Hiraki, Y. Sequential Progression of the Differentiation Program by Bone Morphogenetic Protein-2 in Chondrogenic Cell Line ATDC5. Exp. Cell Res. 1998, 241, 1–11. Available online: https://pubmed.ncbi.nlm.nih.gov/9633508/ (accessed on 17 November 2022). [CrossRef] [PubMed]
- White, R.; Gibson, J.S. The effect of oxygen tension on calcium homeostasis in bovine articular chondrocytes. J. Orthop. Surg. Res. 2010, 5, 27. [Google Scholar] [CrossRef] [Green Version]
- Ge, Y.; Li, Y.; Wang, Z.; Li, L.; Teng, H.; Jiang, Q. Effects of Mechanical Compression on Chondrogenesis of Human Synovium-Derived Mesenchymal Stem Cells in Agarose Hydrogel. Front. Bioeng. Biotechnol. 2021, 9, 697281. Available online: https://www.frontiersin.org/articles/10.3389/fbioe.2021.697281/pdf (accessed on 17 November 2022). [CrossRef]
- Ravalli, S.; Szychlinska, M.A.; Lauretta, G.; Musumeci, G. New Insights on Mechanical Stimulation of Mesenchymal Stem Cells for Cartilage Regeneration. Appl. Sci. 2020, 10, 2927. Available online: https://www.mdpi.com/2076-3417/10/8/2927 (accessed on 17 November 2022). [CrossRef]
Study | Source of MSC | MSC Markers Assessed | Pellet Culture vs. SCAFFOLD vs. Monolayer | Oxygen Tension Used and Stage Exposed |
---|---|---|---|---|
Adesida et al. [21] | Human bone marrow | CD13, CD29, CD34, CD44, CD73, CD90, CD105, CD151 | Pellet | 4 groups:
|
Baumgartner et al. [22] | Human bone marrow | CD14, CD34, CD45, CD105, CD106 | Scaffold | 3% O2 (hypoxia) vs. 21% O2 (normoxia) during differentiation |
Boyette et al. [23] | Human bone marrow | CD34, CD45, CD73, CD90, CD105, CD146, Stro-1 | Pellet | 4 groups:
|
Cicione et al. [24] | Human bone marrow | CD29, CD34, CD44, CD45, CD73, CD90, CD105, CD106, CD66, SSEA-4, Stro-1 | Pellet and then scaffold during chondrogenic differentiation | 1% O2 (severe hypoxia) vs. 21% O2 (normoxia) during differentiation |
Duval et al. [25] | Human bone marrow | CD34, CD45 | Scaffold | 5% O2 (hypoxia) vs. 21% O2 (normoxia) during differentiation |
Wang et al. [26] |
| CD19, CD34, CD45, CD79a, HLA-DR, CD29, CD44, CD73, CD90, CD105 | Pellet | 1% O2 (hypoxia) vs. 20% O2 (normoxia) during the expansion of MSCs data only shown for the human adipose tissue group. |
Lim et al. [27] | Human bone marrow | CD13, CD34, CD90, CD146 | Bioreactor | 8% O2 (hypoxia) vs. 20% O2 (normoxia) during differentiation |
Khan et al., 2007 [28] | Human adipose tissue | CD13, CD29, CD34, CD44, CD90, LNGFR, Stro-1, CD56, | Pellet | 5% O2 (hypoxia) vs. 20% O2 (normoxia) during differentiation |
Khan et al., 2010 [29] | Human bone marrow | CD13, CD34, CD44, CD56, CD90, CD105, LNGFR, Stro1, | Pellet | 5% O2 (hypoxia) vs. 20% O2 (normoxia) during differentiation |
Lee et al., 2018 [30] | Human bone marrow | CD14, CD29, CD34, CD44, CD45, CD73, CD105, HLA-DR | Pellet | 1% O2 (hypoxia) vs. 21% O2 (normoxia) during expansion |
Lee et al., 2015 [31] | Human bone marrow | CD14, CD29, CD34, CD44, CD45, CD73, CD90, CD105, Stro-1. | Pellet | 1% O2 (hypoxia) vs. 21% O2 (normoxia) during expansion |
Legendre et al. [32] | Human bone marrow | CD14, CD29, CD34, CD44, CD45, CD64, CD73, CD90, CD105 CD146, HLA-DR | Scaffold | 3% O2 (hypoxia) vs. 21% O2 (normoxia) during differentiation |
Markway et al. [33] | Human bone marrow | CD45, CD73, CD90, CD105 | Pellet or micropellet | 2% O2 (hypoxia) for both groups during expansion and then 2% O2 (Hypoxia) vs. 20% O2 (Normoxia) during differentiation |
Merceron et al. [34] | Human adipose tissue | CD29, CD34, CD44, CD45, CD90, CD105 | Pellets | 20% O2 (Normoxia) vs. 5% O2 (hypoxia) during differentiation |
Munir et al. [35] | Human adipose tissue | CD34, CD45, CD74, CD90 and CD105, HLA-DR | Pellet/micromass+ scaffold | 5% O2 (hypoxia) vs. 21% O2 (normoxia) during differentiation |
Neybecker et al. [36] | Human synovium | CD34, CD45, CD73, CD90, CD105 | Scaffold | 5% O2 (hypoxia) vs. 20% O2 (normoxia) during differentiation |
Ohara et al. [37] | Human synovium | CD45, CD73, CD90, CD105, CD140b | Pellet | 5% O2 (hypoxia) vs. 21% O2 (normoxia) during expansion |
Pattappa et al., 2019 [38] | Human bone marrow | None assessed; referenced previous studies using the same isolation method which assessed CD19, CD34, CD44, CD45, CD73, CD90, CD105, CD166 | Pellet | 2% O2 (hypoxia) vs. 20% O2 (normoxia) during both expansion and differentiation |
Pattappa et al., 2013 [39] | Human bone marrow | CD11b, CD19, CD34, CD44, CD45, CD73, CD90, CD105, HLA-DR. | Pellet | 5% O2 or 2% O2 (hypoxia) vs. 20% O2 (normoxia) during both expansion and differentiation |
Tian et al. [40] | Human bone marrow | CD14, CD29, CD44, CD45, CD105 | Monolayer | 5% O2 (hypoxia) vs. 21% O2 (normoxia) during differentiation |
Van de Walle et al. [41] | Human bone marrow | CD44, CD73, CD90, CD105, CD166 | Pellet | 3% O2 (hypoxia) then 21 % O2 normoxia during differentiation vs. 3% O2 (hypoxia) continuously during differentiation |
Safwani et al [42,43] | Human adipose tissue | CD14, CD19. CD34, CD45, CD73, CD90, CD105 | Pellet | 2% O2 (hypoxia) vs. 21% O2 (normoxia) during both expansion and differentiation (also compared with and without fetal bovine serum in the culture medium) |
Weijers et al. [43] | Human adipose tissue | CD31, CD34, CD54, CD90, CD105, and CD166 | Pellet | 1% O2 (hypoxia) vs. 20% O2 (normoxia) during both expansion and differentiation |
Zhao et al. [44] | Human adipose tissue | CD14, CD19, CD34, CD45, CD73, CD90, CD105 | Monolayer | 2% O2 (hypoxia) vs. 21% O2 (normoxia) during the expansion of MSCs |
Study | Outcome Measures | Effect of Hypoxia on Chondrogenesis |
---|---|---|
Adesida et al. [21] |
| Effect of hypoxia at expansion phase:
Hypoxia-expanded cells showed greater expression of TGFβ-RI but no significant change in TGFβ-RII compared to normoxia-expanded cells when exposed to hypoxia in differentiation. Summary: groups exposed to hypoxia during expansion showed enhanced chondrogenic potential compared to normoxia exposed groups. |
Baumgartner et al. [22] |
| Effect of hypoxia during the differentiation phase:
|
Boyette et al. [23] |
| Effect of hypoxia during the expansion phase compared to normoxia during the expansion phase (with hypoxia differentiation in both groups)
|
Cicione et al. [24] |
| Effect of hypoxia during the differentiation phase:
|
Duval et al. [25] |
| Effect of hypoxia during the differentiation phase: Increased SOX, ACAN, COL2A1 gene expression, procollagen II protein expression, and increased alcain blue staining in hypoxia exposed cells compared to normoxia exposed. Summary: groups exposed to hypoxia during the differentiation phase showed enhanced chondrogenic markers compared to the normoxia exposed group. |
Wang et al. [26] |
| Adipose-derived stem cells: Effect of hypoxia during the expansion phase:
|
Lim et al. [27] |
| Effect of hypoxia during the differentiation phase:
|
Khan et al., 2007 [28] |
| Effect of hypoxia during the differentiation phase:
|
Khan et al., 2010 [29] |
| Effect of hypoxia during the differentiation phase:
|
Lee et al. [30] |
| Effect of hypoxia during the expansion phase:
|
Lee et al. [31] |
| Effect of hypoxia during the expansion phase:
|
Legendre et al. [32] |
| Effect of hypoxia during the differentiation phase:
|
Markway et al. [33] |
| Effect of hypoxia during the differentiation phase (with both groups exposed to hypoxia during the expansion phase):
|
Merceron et al. [34] |
| Effect of hypoxia during the differentiation phase:
|
Munir et al. [35] |
| Effect of hypoxia during the differentiation phase:Pellet culture:
Summary: group exposed to hypoxia during the differentiation phase showed increases in some chondrogenic markers compared to the normoxia exposed group. (Some markers however showed no difference) |
Neybecker et al. [36] |
| Effect of hypoxia during the differentiation phase:
|
Ohara et al. [37] |
| Effect of hypoxia during the expansion phase:
|
Pattappa et al., 2019 [38] |
| Effect of continuous hypoxia during expansion and differentiation phases: Donors were found to either be responsive or nonresponsive to hypoxic conditions:
|
Pattappa et al., 2013 [39] |
| Effect of continuous hypoxia during expansion and differentiation phases:
|
Tian et al. [40] |
| Effect of hypoxia during the differentiation phase:
|
Van de Walle et al. [41] |
| Effect of hypoxia during the differentiation phase:
|
Safwani et al. [42] |
| Effect of continuous hypoxia during expansion and differentiation phases:
|
Weijers et al. [43] |
| Effect of continuous hypoxia during expansion and differentiation phases:
|
Zhao et al. [44] |
| Effect of hypoxia during the expansion phase:
|
Stem Cell Marker | Number of Studies Used in |
---|---|
CD11b | 1 |
CD14 | 7 |
CD13 | 4 |
CD19 | 4 |
CD29 | 10 |
CD31 | 1 |
CD34 | 19 |
CD44 | 12 |
CD45 | 17 |
CD54 | 1 |
CD56 | 1 |
CD64 | 1 |
CD66 | 1 |
CD73 | 14 |
CD74 | 1 |
CD79a | 1 |
CD90 | 20 |
CD105 | 20 |
CD106 | 2 |
CD140b | 1 |
CD146 | 3 |
CD151 | 1 |
CD166 | 2 |
Stro1 | 5 |
SSEA-4 | 1 |
HLA-DR | 5 |
LGNFR | 2 |
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Ranmuthu, C.K.I.; Ranmuthu, C.D.S.; Wijewardena, C.K.; Seah, M.K.T.; Khan, W.S. Evaluating the Effect of Hypoxia on Human Adult Mesenchymal Stromal Cell Chondrogenesis In Vitro: A Systematic Review. Int. J. Mol. Sci. 2022, 23, 15210. https://doi.org/10.3390/ijms232315210
Ranmuthu CKI, Ranmuthu CDS, Wijewardena CK, Seah MKT, Khan WS. Evaluating the Effect of Hypoxia on Human Adult Mesenchymal Stromal Cell Chondrogenesis In Vitro: A Systematic Review. International Journal of Molecular Sciences. 2022; 23(23):15210. https://doi.org/10.3390/ijms232315210
Chicago/Turabian StyleRanmuthu, Charindu K. I., Chanuka D. S. Ranmuthu, Chalukya K. Wijewardena, Matthew K. T. Seah, and Wasim S. Khan. 2022. "Evaluating the Effect of Hypoxia on Human Adult Mesenchymal Stromal Cell Chondrogenesis In Vitro: A Systematic Review" International Journal of Molecular Sciences 23, no. 23: 15210. https://doi.org/10.3390/ijms232315210