Interplay of reactive oxygen species (ROS) and tissue engineering: a review on clinical aspects of ROS-responsive biomaterials
Source abstract
Abstract
Reactive oxygen species (ROS) refers to the reactive molecules and free radicals of oxygen generated as the by-products of aerobic respiration. Historically, ROS are known as stress markers that are linked to the response of immune cell against microbial invasion, but recent discoveries suggest their role as secondary messengers in signal transduction and cell cycle. Tissue engineering (TE) techniques have the capabilities to harness such properties of ROS for the effective regeneration of damaged tissues. TE employs stem cells and biomaterial matrix, to heal and regenerate injured tissue and organ. During regeneration, one of the constraints is the unavailability of oxygen as proper vasculature is absent at the injured site. This creates hypoxic conditions at the site of regeneration. Hence, effective response against the stresses like hypoxia spurs the regeneration process. Contrary, hyperoxic condition may increase the risk of ROS stress at the site. TE tries to overcome these limitations with the new class of biomaterials that can sense such stresses and respond accordingly. This review endeavors to explain the role of ROS in stem cell proliferation and differentiation, which is a key component in regeneration. This compilation also highlights the new class of biomaterials that can overcome the hypoxic conditions during tissue regeneration along with emphasis on the ROS-responsive biomaterials and their clinical applications. Incorporating these biomaterials in scaffolds development holds huge potential in tissue or organ regeneration and even in drug delivery.
Source: openaire · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Electrospun Nanofibers in Biomedical Applications · Tissue Engineering and Regenerative Medicine · Bone Tissue Engineering Materials
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (100+)
Show source-provided references
1. Clarke G, Harley P, Hubber EL et al (2018) Bench to bedside: current advances in regenerative medicine. CurrOpin Cell Biol 55:59–66. https://doi.org/10.1016/j.ceb.2018.05.00610.1016/j.ceb.2018.05.006 ↗
2. Katari R, Peloso A, Orlando G (2015) Tissue engineering and regenerative medicine: semantic considerations for an evolving paradigm. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2014.0005710.3389/fbioe.2014.00057 ↗
3. Tonelli FMP, de Cássia Oliveira Paiva N, de Medeiros RVB, Pinto MCX, Tonelli FCP, Resende RR (2017) Tissue engineering: the use of stem cells in regenerative medicine. Elsevier, Amsterdam. doi:https://doi.org/10.1016/B978-0-444-63660-7.00012-710.1016/B978-0-444-63660-7.00012-7 ↗
4. Zakrzewski W, Dobrzyński M, Szymonowicz M et al (2019) Stem cells: past, present, and future. Stem Cell Res Ther 10:68. https://doi.org/10.1186/s13287-019-1165-510.1186/s13287-019-1165-5 ↗
5. Dutta RC, Dutta AK (2009) Cell-interactive 3D-scaffold; advances and applications. Biotechnol Adv 27(4):334–339. https://doi.org/10.1016/j.biotechadv.2009.02.00210.1016/j.biotechadv.2009.02.002 ↗
6. Oryan A, Alidadi S, Moshiri A et al (2014) Bone regenerative medicine: classic options, novel strategies, and future directions. J Orthop Surg Res 9:18. https://doi.org/10.1186/1749-799X-9-1810.1186/1749-799X-9-18 ↗
7. Inamdar N, Borenstein J (2011) Microfluidic cell culture models for tissue engineering. Curr Opin Biotechnol 22(5):681–689. https://doi.org/10.1016/j.copbio.2011.05.51210.1016/j.copbio.2011.05.512 ↗
8. Sthijns M, van Blitterswijk C, LaPointe V (2018) Redox regulation in regenerative medicine and tissue engineering: the paradox of oxygen. J Tissue Eng Regen Med. https://doi.org/10.1002/term.273010.1002/term.2730 ↗
9. Eunok C, David MB (2005) Chemistry and reactions of reactive oxygen species in foods. J Food Sci 70:9
10. Lushchak VI, Bagnyukova TV (2006) Effects of different environmental oxygen levels on free radical processes in fish. Comp BiochemPhysiol B BiochemMol Biol 144(3):283–289. https://doi.org/10.1016/j.cbpb.2006.02.01410.1016/j.cbpb.2006.02.014 ↗
11. Zorov DB, Juhaszova M, Sollott SJ (2014) Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 94(3):909–950. https://doi.org/10.1152/physrev.00026.201310.1152/physrev.00026.2013 ↗
12. Brieger K, Schiavone S, Miller FJ, Krause KH (2012) Reactive oxygen species: from health to disease. Swiss Med Wkly. https://doi.org/10.4414/smw.2012.1365910.4414/smw.2012.13659 ↗
13. Imlay J, Chin S, Linn S (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science (1979) 240(4852):640–642. https://doi.org/10.1126/science.283482110.1126/science.2834821 ↗
14. Poljsak B, Šuput D, Milisav I (2013) Achieving the balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxid Med Cell Longev. https://doi.org/10.1155/2013/95679210.1155/2013/956792 ↗
15. Bernstein HS, Srivastava D (2012) Stem cell therapy for cardiac disease. Pediatr Res 71(4 Pt 2):491–499. https://doi.org/10.1038/pr.2011.6110.1038/pr.2011.61 ↗
16. Mashayekhan S, Hajiabbas M, Fallah A (2013) Stem cells in tissue engineering. Pluripotent Stem Cells. https://doi.org/10.5772/5437110.5772/54371 ↗
17. Nugud A, Sandeep D, El-Serafi AT (2018) Two faces of the coin: minireview for dissecting the role of reactive oxygen species in stem cell potency and lineage commitment, vol 14. Cairo University, Egypt. doi:https://doi.org/10.1016/j.jare.2018.05.01210.1016/j.jare.2018.05.012 ↗
18. Vats A, Tolley NS, Bishop AE, Polak JM (2005) Embryonic stem cells and tissue engineering: delivering stem cells to the clinic. J R Soc Med 98(8):346–350. https://doi.org/10.1258/jrsm.98.8.34610.1258/jrsm.98.8.346 ↗
19. Elçin Y (2004) Stem cells and tissue engineering. Adv Exp Med Biol. https://doi.org/10.1007/978-0-306-48584-8_2310.1007/978-0-306-48584-8_23 ↗
20. Wang A, Tang Z, Park IH et al (2011) Induced pluripotent stem cells for neural tissue engineering. Biomaterials 32(22):5023–5032. https://doi.org/10.1016/j.biomaterials.2011.03.07010.1016/j.biomaterials.2011.03.070 ↗
21. Gadue P, Huber TL, Nostro MC, Kattman S, Keller GM (2005) Germ layer induction from embryonic stem cells. Exp Hematol 33(9):955–964. https://doi.org/10.1016/j.exphem.2005.06.00910.1016/j.exphem.2005.06.009 ↗
22. Månsson R, Hultquist A, Luc S et al (2007) Molecular evidence for hierarchical transcriptional lineage priming in fetal and adult stem cells and multipotent progenitors. Immunity 26(4):407–419. https://doi.org/10.1016/j.immuni.2007.02.01310.1016/j.immuni.2007.02.013 ↗
23. Tsuji W, Rubin JP, Marra KG (2014) Adipose-derived stem cells: implications in tissue regeneration. World J Stem Cells 6(3):312–321. https://doi.org/10.4252/wjsc.v6.i3.31210.4252/wjsc.v6.i3.312 ↗
24. Woodbury D, Reynolds K, Black IB (2002) Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. J Neurosci Res 69(6):908–917. https://doi.org/10.1002/jnr.1036510.1002/jnr.10365 ↗
25. Seita J, Weissman IL (2010) Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip Rev Syst Biol Med 2(6):640–653. https://doi.org/10.1002/wsbm.8610.1002/wsbm.86 ↗
26. Kondo M (2010) Lymphoid and myeloid lineage commitment in multipotent hematopoietic progenitors. Immunol Rev 238(1):37–46. https://doi.org/10.1111/j.1600-065X.2010.00963.x10.1111/j.1600-065X.2010.00963.x ↗
27. Iwasaki H, Akashi K (2007) Myeloid lineage commitment from the hematopoietic stem cell. Immunity 26(6):726–740. https://doi.org/10.1016/j.immuni.2007.06.00410.1016/j.immuni.2007.06.004 ↗
28. Kawamoto H, Katsura Y (2009) A new paradigm for hematopoietic cell lineages: revision of the classical concept of the myeloid-lymphoid dichotomy. Trends Immunol 30(5):193–200. https://doi.org/10.1016/j.it.2009.03.00110.1016/j.it.2009.03.001 ↗
29. Ullah I, Subbarao RB, Rho GJ (2015) Human mesenchymal stem cells: current trends and future prospective. Biosci Rep. https://doi.org/10.1042/BSR2015002510.1042/BSR20150025 ↗
30. Solchaga LA, Penick KJ, Welter JF (2011) Chondrogenic differentiation of bone marrow-derived mesenchymal stem cells: tips and tricks. Methods Mol Biol 698:253–278. https://doi.org/10.1007/978-1-60761-999-4_2010.1007/978-1-60761-999-4_20 ↗
31. Heino T, Hentunen T (2008) Differentiation of osteoblasts and osteocytes from mesenchymal stem cells. Curr Stem Cell Res Ther 3(2):131–145. https://doi.org/10.2174/15748880878422303210.2174/157488808784223032 ↗
32. Munir H, Ward LSC, Sheriff L et al (2017) Adipogenic differentiation of mesenchymal stem cells alters their immunomodulatory properties in a tissue-specific manner. Stem Cells 35(6):1636–1646. https://doi.org/10.1002/stem.262210.1002/stem.2622 ↗
33. Jeon B, Jang S, Park J et al (2015) Differentiation potential of mesenchymal stem cells isolated from human dental tissues into non-mesodermal lineage. Anim Cells Syst (Seoul) 19(5):321–331. https://doi.org/10.1080/19768354.2015.108743010.1080/19768354.2015.1087430 ↗
34. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676. https://doi.org/10.1016/j.cell.2006.07.02410.1016/j.cell.2006.07.024 ↗
35. Mao SH, Chen CH, Chen CT (2019) Osteogenic potential of induced pluripotent stem cells from human adipose-derived stem cells. Stem Cell Res Ther 10:303. https://doi.org/10.1186/s13287-019-1402-y10.1186/s13287-019-1402-y ↗
36. Isogai S, Yamamoto N, Hiramatsu N et al (2018) Preparation of induced pluripotent stem cells using human peripheral blood monocytes. Cell Reprogram 20(6):347–355. https://doi.org/10.1089/cell.2018.002410.1089/cell.2018.0024 ↗
37. Chatterjee I, Li F, Kohler EE, Rehman J, Malik AB, Wary KK (2016) Induced pluripotent stem (iPS) cell culture methods and induction of differentiation into endothelial cells. Methods Mol Biol 1357:311–327. https://doi.org/10.1007/7651_2015_20310.1007/7651_2015_203 ↗
38. Moradi S, Mahdizadeh H, Šarić T et al (2019) Research and therapy with induced pluripotent stem cells (iPSCs): social, legal, and ethical considerations. Stem Cell Res Ther 10:341. https://doi.org/10.1186/s13287-019-1455-y10.1186/s13287-019-1455-y ↗
39. Halevy T, Urbach A (2014) Comparing ESC and iPSC-based models for human genetic disorders. J Clin Med 3(4):1146–1162. https://doi.org/10.3390/jcm304114610.3390/jcm3041146 ↗
40. Lee E, Kasper F, Mikos A (2013) Biomaterials for tissue engineering. Ann Biomed Eng 13:565–576
41. Chan BP, Leong KW (2008) Scaffolding in tissue engineering: general approaches and tissue-specific considerations. Eur Spine J 17(Suppl 4):467–479. https://doi.org/10.1007/s00586-008-0745-310.1007/s00586-008-0745-3 ↗
42. Keane T, Badylak S (2014) Biomaterials for tissue engineering applications. Seminars Pediat Surg. https://doi.org/10.1053/j.sempedsurg.2014.06.01010.1053/j.sempedsurg.2014.06.010 ↗
43. Loh QL, Choong C (2013) Three-dimensional scaffolds for tissue engineering applications: role of porosity and pore size. Tissue Eng B Rev 19(6):485–502. https://doi.org/10.1089/ten.TEB.2012.043710.1089/ten.TEB.2012.0437 ↗
44. Place E, Evans N, Stevens M (2009) Complexity in biomaterials for tissue engineering. Nat Mater. https://doi.org/10.1038/nmat244110.1038/nmat2441 ↗
45. Wade R, Burdick J (2012) Engineering ECM signals into biomaterials. Mater Today 15(10):454–459. https://doi.org/10.1016/s1369-7021(12)70197-910.1016/s1369-7021(12)70197-9 ↗
46. Santos E, Orive G, Luis J (2011) Cell-biomaterial interaction: strategies to mimic the extracellular matrix. On Biomimetics. https://doi.org/10.5772/2163410.5772/21634 ↗
47. Stratton S, Shelke N, Hoshino K, Rudraiah S, Kumbar S (2016) Bioactive polymeric scaffolds for tissue engineering. Bioact Mater 1(2):93–108. https://doi.org/10.1016/j.bioactmat.2016.11.00110.1016/j.bioactmat.2016.11.001 ↗
48. Ivanov AN, Saveleva MS, Kozadaev MN et al (2019) New approaches to scaffold biocompatibility assessment. BioNanoSci 9:395–405. https://doi.org/10.1007/s12668-019-00613-310.1007/s12668-019-00613-3 ↗
49. O’Brien F (2011) Biomaterials and scaffolds for tissue engineering. Mater Today 14(3):88–95. https://doi.org/10.1016/s1369-7021(11)70058-x10.1016/s1369-7021(11)70058-x ↗
50. Liu C, Czernuszka J (2007) Development of biodegradable scaffolds for tissue engineering: a perspective on emerging technology. Mater Sci Technol 23(4):379–391. https://doi.org/10.1179/174328407x17702710.1179/174328407x177027 ↗
51. Anderson J (2012) Biocompatibility. Polym Sci A Compreh Ref. https://doi.org/10.1016/b978-0-444-53349-4.00229-610.1016/b978-0-444-53349-4.00229-6 ↗
52. Chen FM, Liu X (2016) Advancing biomaterials of human origin for tissue engineering. Prog Polym Sci 53:86–168. https://doi.org/10.1016/j.progpolymsci.2015.02.00410.1016/j.progpolymsci.2015.02.004 ↗
53. Dolcimascolo A, Calabrese G, Conoci S, Parenti R (2019) Innovative biomaterials for tissue engineering. Biomater Supp Tissue Reconst Regen. https://doi.org/10.5772/intechopen.8383910.5772/intechopen.83839 ↗
54. Hickey R, Pelling A (2019) Cellulose biomaterials for tissue engineering. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2019.0004510.3389/fbioe.2019.00045 ↗
55. Brovold M, Almeida J, Pla-Palacín I, Sainz-Arnal P, Sánchez-Romero N, Rivas J, Almeida H, Dachary P, Serrano-Aulló T, Soker S, Baptista P (2018) Naturally-derived biomaterials for tissue engineering applications. Adv Exp Med Biol. https://doi.org/10.1007/978-981-13-0947-2_2310.1007/978-981-13-0947-2_23 ↗
56. Tang X, Thankappan S, Lee P, Fard S, Harmon M, Tran K, Yu X (2014) Polymeric biomaterials in tissue engineering and regenerative medicine. Nat Synth Biomed Polym. https://doi.org/10.1016/B978-0-12-396983-5.00022-310.1016/B978-0-12-396983-5.00022-3 ↗
57. Samavedi S, Poindexter L, Van Dyke M, Goldstein A (2014) Synthetic biomaterials for regenerative medicine applications. Regen Med Appl Org Transp. https://doi.org/10.1016/b978-0-12-398523-1.00007-010.1016/b978-0-12-398523-1.00007-0 ↗
58. Ren X, Zhao M, Lash B, Martino M, Julier Z (2020) Growth factor engineering strategies for regenerative medicine applications. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2019.0046910.3389/fbioe.2019.00469 ↗
59. Lee K, Silva E, Mooney D (2010) Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. J R Soc Interf. https://doi.org/10.1098/rsif.2010.022310.1098/rsif.2010.0223 ↗
60. Rouwkema J, Khademhosseini A (2016) Vascularization and angiogenesis in tissue engineering: beyond creating static networks. Trends Biotechnol. https://doi.org/10.1016/j.tibtech.2016.03.00210.1016/j.tibtech.2016.03.002 ↗
61. Maddaluno L, Urwyler C, Werner S (2017) Fibroblast growth factors: key players in regeneration and tissue repair. Development. https://doi.org/10.1242/dev.15258710.1242/dev.152587 ↗
62. Yun Y, Won J, Jeon E, Lee S, Kang W, Jo H, Jang J, Shin U, Kim H (2010) Fibroblast growth factors: biology, function, and application for tissue regeneration. J Tissue Eng. https://doi.org/10.4061/2010/21814210.4061/2010/218142 ↗
63. Bessa P, Casal M, Reis R (2008) Bone morphogenetic proteins in tissue engineering: the road from the laboratory to the clinic, part I (basic concepts). J Tissue Eng Regen Med. https://doi.org/10.1002/term.6310.1002/term.63 ↗
64. Kowalczewski C, Saul J (2018) Biomaterials for the delivery of growth factors and other therapeutic agents in tissue engineering approaches to bone regeneration. Front Pharmacol. https://doi.org/10.3389/fphar.2018.0051310.3389/fphar.2018.00513 ↗
65. Wong R, Guillaud L (2004) The role of epidermal growth factor and its receptors in mammalian CNS. Cytokine Growth Factor Rev. https://doi.org/10.1016/j.cytogfr.2004.01.00410.1016/j.cytogfr.2004.01.004 ↗
66. Bodnar R (2013) Epidermal growth factor and epidermal growth factor receptor: the Yin and Yang in the treatment of cutaneous wounds and cancer. Adv Wound Care 2(1):24–2910.1089/wound.2011.0326 ↗
67. Shu D, Hutcheon A, Zieske J, Guo X (2019) Epidermal growth factor stimulates transforming growth factor-beta receptor Type II expression in corneal epithelial cells. Sci Rep. https://doi.org/10.1038/s41598-019-42969-210.1038/s41598-019-42969-2 ↗
68. Avendaño C, Menéndez J (2015) Drugs that inhibit signaling pathways for tumor cell growth and proliferation. Med Chem Anticancer Drugs. https://doi.org/10.1016/j.jconrel.2019.05.02810.1016/j.jconrel.2019.05.028 ↗
69. Youssef A, Aboalola D, Han V (2017) The roles of insulin-like growth factors in mesenchymal stem cell niche. Stem Cells Int. https://doi.org/10.1155/2017/945310810.1155/2017/9453108 ↗
70. Liu C, Wang C, Zhao Q, Li X, Xu F, Yao X, Wang M (2018) Incorporation and release of dual growth factors for nerve tissue engineering using nanofibrousbicomponent scaffolds. Biomed Mater 13(4):044107. https://doi.org/10.1088/1748-605X/aab69310.1088/1748-605X/aab693 ↗
71. Gu X, Ding F, Yang Y, Liu J (2015) Tissue engineering in peripheral nerve regeneration. Neural Regen. https://doi.org/10.1016/B978-0-12-801732-6.00005-710.1016/B978-0-12-801732-6.00005-7 ↗
72. Heldin C, Westermark B (1999) Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev. https://doi.org/10.1152/physrev.1999.79.4.128310.1152/physrev.1999.79.4.1283 ↗
73. Chew S, Hinojosa V, Arriaga M (2017) Bioresorbable polymer microparticles in the medical and pharmaceutical fields. Biores Polym Biomed Appl. https://doi.org/10.1016/B978-0-08-100262-9.00011-210.1016/B978-0-08-100262-9.00011-2 ↗
74. Madry H, Rey-Rico A, Venkatesan J, Johnstone B, Cucchiarini M (2014) Transforming growth factor beta-releasing scaffolds for cartilage tissue engineering. Tissue Eng B Rev. https://doi.org/10.1089/ten.TEB.2013.027110.1089/ten.TEB.2013.0271 ↗
75. Poniatowski Ł, Wojdasiewicz P, Gasik R, Szukiewicz D (2015) Transforming growth factor beta family: insight into the role of growth factors in regulation of fracture healing biology and potential clinical applications. Med Inflam. https://doi.org/10.1155/2015/13782310.1155/2015/137823 ↗
76. Khan S, Villalobos M, Choron R, Chang S, Brown S, Carpenter J, Tulenko T, Zhang P (2017) Fibroblast growth factor and vascular endothelial growth factor play a critical role in endotheliogenesis from human adipose-derived stem cells. J Vasc Surg 65(5):1483–1492. https://doi.org/10.1016/j.jvs.2016.04.03410.1016/j.jvs.2016.04.034 ↗
77. Lifirsu E, Ramalingam M, Haidar Z (2012) Vascular endothelial growth factors in tissue engineering: challenges and prospects for therapeutic angiogenesis. Integ Biomater Tissue Eng. https://doi.org/10.1002/9781118371183.ch1110.1002/9781118371183.ch11 ↗
78. Wang Z, Li Y, Sarkar F (2010) Signaling mechanism(s) of reactive oxygen species in epithelial-mesenchymal transition reminiscent of cancer stem cells in tumor progression. Curr Stem Cell Res Ther 5(1):74–80. https://doi.org/10.2174/15748881079044281310.2174/157488810790442813 ↗
79. Abdollahi H, Harris LJ, Zhang P et al (2011) The role of hypoxia in stem cell differentiation and therapeutics. J Surg Res 165(1):112–117. https://doi.org/10.1016/j.jss.2009.09.05710.1016/j.jss.2009.09.057 ↗
80. Vieira HLA, Alves PM, Vercelli A (2011) Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species. Prog Neurobiol 93(3):444–455. https://doi.org/10.1016/j.pneurobio.2011.01.00710.1016/j.pneurobio.2011.01.007 ↗
81. Rodrigues M, Turner O, Stolz D, Griffith LG, Wells A (2012) Production of reactive oxygen species by multipotent stromal cells/mesenchymal stem cells upon exposure to fas ligand. Cell Transplant 21(10):2171–2187. https://doi.org/10.3727/096368912X63903510.3727/096368912X639035 ↗
82. Kim SH, Kim KY, Park SG et al (2017) Mitochondrial ROS activates ERK/autophagy pathway as a protected mechanism against deoxypodophyllotoxin-induced apoptosis. Oncotarget 8(67):111581–111596. https://doi.org/10.18632/oncotarget.2287510.18632/oncotarget.22875 ↗
83. Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U (2011) Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells 29(3):486–495. https://doi.org/10.1002/stem.59010.1002/stem.590 ↗
84. Facucho-Oliveira JM, St John JC (2009) The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev Rep 5:140–158. https://doi.org/10.1007/s12015-009-9058-010.1007/s12015-009-9058-0 ↗
85. Nishimura K, Fukuda A, Hisatake K (2019) Mechanisms of the metabolic shift during somatic cell reprogramming. Int J Mol Sci. https://doi.org/10.3390/ijms2009225410.3390/ijms20092254 ↗
86. Bigarella CL, Liang R, Ghaffari S (2014) Stem cells and the impact of ROS signaling. Development 141(22):4206–4218. https://doi.org/10.1242/dev.10708610.1242/dev.107086 ↗
87. Ogasawara MA, Zhang H (2009) Redox regulation and its emerging roles in stem cells and stem-like cancer cells. Antioxidants Redox Signal 11(5):1107–1122. https://doi.org/10.1089/ars.2008.230810.1089/ars.2008.2308 ↗
88. Lyublinskaya OG, Borisov YG, Pugovkina NA et al (2015) Reactive oxygen species are required for human mesenchymal stem cells to initiate proliferation after the quiescence exit. Oxid Med Cell Longev. https://doi.org/10.1155/2015/50210510.1155/2015/502105 ↗
89. Atashi F, Modarressi A, Pepper MS (2015) The role of reactive oxygen species in mesenchymal stem cell adipogenic and osteogenic differentiation: a review, vol 24. doi:https://doi.org/10.1089/scd.2014.048410.1089/scd.2014.0484 ↗
90. Chen Q, Shou P, Zheng C et al (2016) Fate decision of mesenchymal stem cells: adipocytes or osteoblasts? Cell Death Differ 23(7):1128–1139. https://doi.org/10.1038/cdd.2015.16810.1038/cdd.2015.168 ↗
91. Korswagen H (2006) Regulation of the Wnt/β-catenin pathway by redox signaling. Dev Cell 10(6):687–688. https://doi.org/10.1016/j.devcel.2006.05.00710.1016/j.devcel.2006.05.007 ↗
92. Eyrich NW, Potts CR, Robinson MH, Maximov V, Kenney AM (2019) Reactive oxygen species signaling promotes hypoxia-inducible factor 1α stabilization in sonic hedgehog-driven cerebellar progenitor cell proliferation. Mol Cell Biol 39(8):e00268-e318. https://doi.org/10.1128/MCB.00268-1810.1128/MCB.00268-18 ↗
93. Kim J, Choi H, Kim T, Leem S, Oh I (2015) Regulation of mesenchymal stromal cells through fine tuning of canonical Wnt signaling. Stem Cell Res 14(3):356–368. https://doi.org/10.1016/j.scr.2015.02.00710.1016/j.scr.2015.02.007 ↗
94. Fan C, Zhang Y, Wang J, Cheng J. Roles of Hedgehog signaling pathway in adipogenic differentiation potential of porcine adipose-derived mesenchymal stem cells.
95. Rharass T, Lemcke H, Lantow M, Kuznetsov SA, Weiss DG, Panáková D (2014) Ca2+-mediated mitochondrial reactive oxygen species metabolism augments Wnt/β-catenin pathway activation to facilitate cell differentiation. J Biol Chem 289(40):27937–27951. https://doi.org/10.1074/jbc.M114.57351910.1074/jbc.M114.573519 ↗
96. Arai M, Shibata Y, Pugdee K, Abiko Y, Ogata Y (2007) Effects of reactive oxygen species (ROS) on antioxidant system and osteoblastic differentiation in MC3T3-E1 cells. IUBMB Life 59(1):27–33. https://doi.org/10.1080/1521654060115618810.1080/15216540601156188 ↗
97. Klotz LO, Sánchez-Ramos C, Prieto-Arroyo I, Urbánek P, Steinbrenner H, Monsalve M (2015) Redox regulation of FoxO transcription factors. Redox Biol 6:51–72. https://doi.org/10.1016/j.redox.2015.06.01910.1016/j.redox.2015.06.019 ↗
98. Ma X, Su P, Yin C et al (2020) The roles of FoxO transcription factors in regulation of bone cells function. Int J Mol Sci 21(3):692. https://doi.org/10.3390/ijms2103069210.3390/ijms21030692 ↗
99. Masschelin PM, Cox AR, Chernis N, Hartig SM (2020) The impact of oxidative stress on adipose tissue energy balance. Front Physiol 10:1638. https://doi.org/10.3389/fphys.2019.0163810.3389/fphys.2019.01638 ↗
100. Nugud A, Sandeep D, El-Serafi A (2018) Two faces of the coin: minireview for dissecting the role of reactive oxygen species in stem cell potency and lineage commitment. J Adv Res 14:73–79. https://doi.org/10.1016/j.jare.2018.05.01210.1016/j.jare.2018.05.012 ↗