Hydrogen peroxide inhibits proliferation and endothelial differentiation of bone marrow stem cells partially via reactive oxygen species generation

Life Sciences

Volumn 112, Issue 1-2, 2014, Pages 33-40

  Xiao, Yuan ^a,b   Li, Xin ^b   Cui, Yuqi ^b   Zhang, Jia ^b   Liu, Lingjuan ^b   Xie, Xiaoyun ^b   Hao, Hong ^b   He, Guanglong ^b   Kander, Melissa C ^b   Chen, Minjie ^b   Liu, Zehao ^a   Verfaillie, Catherine M ^c   Zhu, Hua ^b   Lei, Minxiang ^a   Liu, Zhenguo ^b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Bone marrow stem cell; Endothelial differentiation; Hydrogen peroxide; Oct 4; Oxidative stress; ROS

Indexed keywords

ACETYLCYSTEINE; CD31 ANTIGEN; HYDROGEN PEROXIDE; OCTAMER TRANSCRIPTION FACTOR 4; REACTIVE OXYGEN METABOLITE; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DRUG EXPOSURE; ELECTRON SPIN RESONANCE; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPE; FLUORESCENCE MICROSCOPY; GROWTH INHIBITION; HEMATOPOIETIC STEM CELL; IMMUNOBLOTTING; IN VITRO STUDY; INTRACELLULAR MEMBRANE; MULTIPOTENT ADULT PROGENITOR CELL; MULTIPOTENT STEM CELL; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE MARROW CELL; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; RAT;

ACETYLCYSTEINE; ANIMALS; ANTIGENS, CD31; APOPTOSIS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; GENE EXPRESSION; HYDROGEN PEROXIDE; MULTIPOTENT STEM CELLS; OCTAMER TRANSCRIPTION FACTOR-3; RATS; REACTIVE OXYGEN SPECIES; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84908648489     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2014.07.016     Document Type: Article

References (52)

1. Abdanipour A, Tiraihi T, Noori-Zadeh A, Majdi A, Gosaili R. Evaluation of lovastatin effects on expression of anti-apoptotic Nrf2 and PGC-1α genes in neural stem cells treated with hydrogen peroxide. Mol Neurobiol 2014;49:1364-72.
2. Aicher A, Rentsch M, Sasaki K, Ellwart JW, Fändrich F, Siebert R, et al. Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circ Res 2007;100:581-9.
3. Ben-Shushan E, Thompson JR, Gudas LJ, Bergman Y. Rex-1, a gene encoding a transcription factor expressed in the early embryo, is regulated via Oct-3/4 and Oct-6 binding to an octamer site and a novel protein, Rox-1, binding to an adjacent site. Mol Cell Biol 1998;18:1866-78.
4. Breton-Romero R, Lamas S. Hydrogen peroxide signaling in vascular endothelial cells. Redox Biol. 2014;2:529-34.
5. Breyer A, Estharabadi N, Oki M, Ulloa F, Nelson-Holte M, Lien L, et al. Multipotent adult progenitor cell isolation and culture procedures. Exp Hematol 2006;34:1596-601.
6. Chu L, Jiang JH, Hao H, Xia Y, Xu J, Liu ZH, et al. Nitric oxide enhances Oct-4 expression in bone marrow stem cells and promotes endothelial differentiation. Eur J Pharmacol 2008;591:59-65.
7. Chu L, Hao H, Luo M, Huang Y, Chen Z, Lu TW, et al. Ox-LDL modifies the behavior of bone marrow stem cells and impairs their endothelial differentiation via inhibition of Akt phosphorylation. J Cell Mol Med 2011;15:423-32.
8. D'Autreaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007;8:813-24.
9. Devasagayam TP, Tilak JC, Boloor KK, Sane KS, Ghaskadbi SS, Lele RD. Free radicals and antioxidants in human health: current status and future prospects. J Assoc Physicians India 2004;52:794-804.
10. Dimmeler S, Zeiher AM. Vascular repair by circulating endothelial progenitor cells: the missing link in atherosclerosis? J Mol Med 2004;82:671-7.
11. Donahue M, Quintavalle C, Chiariello GA, Condorelli G, Briguori C. Endothelial progenitor cells in coronary artery disease. Biol Chem 2013;394:1241-52.
12. Haidara MA, Yassin HZ, Rateb M, Ammar H, Zorkani MA. Role of oxidative stress in development of cardiovascular complications in diabetes mellitus. Curr Vasc Pharmacol 2006;4:215-27.
13. Ho PJ, Yen ML, Tang BC, Chen CT, Yen BL. H2O2 accumulation mediates differentiation capacity alteration, but not proliferative decline, in senescent human fetal mesenchymal stem cells. Antioxid Redox Signal 2013;18:1895-905.
14. Ivanova N, Dobrin R, Lu R, Kotenko I, Levorse J, DeCoste C, et al. Dissecting self-renewal in stem cells with RNA interference. Nature 2006;442:533-8.
15. Janssen-Heininger YM, Mossman BT, Heintz NH, Forman HJ, Kalyanaraman B, Finkel T, et al. Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic Biol Med 2008;45:1-17.
16. Kang J, Gemberling M, Nakamura M, Whitby FG, Handa H, Fairbrother WG, et al. A general mechanism for transcription regulation by Oct1 and Oct4 in response to genotoxic and oxidative stress. Genes Dev 2009;23:208-22.
17. Kellner S, Kikyo N. Transcriptional regulation of the Oct4 gene, a master gene for pluripotency. Histol Histopathol 2010;25:405-12.
18. Kim J, Wong PK. Loss of ATM impairs proliferation of neural stem cells through oxidative stress-mediated p38 MAPK signaling. Stem Cells 2009;27:1987-98.
19. Li S, Deng Y, Feng J, Ye W. Oxidative preconditioning promotes bone marrow mesenchymal stem cells migration and prevents apoptosis. Cell Biol Int 2009;33:411-8.
20. Li D, Xu Y, Gao CY, Zhai YP. Adaptive protection against damage of preconditioning human umbilical cord-derived mesenchymal stem cells with hydrogen peroxide. Genet Mol Res 2014. [Feb 21;13(AOP), Epub ahead of print].
21. Lin CP, Lin FY, Huang PH, Chen YL, Chen WC, Chen HY, et al. Endothelial progenitor cell dysfunction in cardiovascular diseases: role of reactive oxygen species and inflammation. Biomed Res Int 2013;2013:845037. http://dx.doi.org/10.1155/2013/845037.
22. Lisanti MP, Martinez-Outschoorn UE, Lin Z, Pavlides S, Whitaker-Menezes D, Pestell RG, et al. Hydrogen peroxide fuels aging, inflammation, cancer metabolism and metastasis: the seed and soil also needs "fertilizer". Cell Cycle 2011;10:2440-9.
23. Liu H, Bian W, Liu S, Huang K. Selenium protects bone marrow stromal cells against hydrogen peroxide-induced inhibition of osteoblastic differentiation by suppressing oxidative stress and ERK signaling pathway. Biol Trace Elem Res 2012;150:441-50.
24. Liu J, Wang Y, Du W, Liu W, Liu F, Zhang L, et al. Wnt1 inhibits hydrogen peroxide-induced apoptosis in mouse cardiac stem cells. PLoS One 2013;8:e58883. http://dx.doi.org/10.1371/journal.pone.0058883.
25. Lu T, Parthasarathy S, Hao H, Luo M, Ahmed S, Zhu J, et al. Reactive oxygen species mediate oxidized low-density lipoprotein-induced inhibition of oct-4 expression and endothelial differentiation of bone marrow stem cells. Antioxid Redox Signal 2010;13:1845-56.
26. Marinho HS, Real C, Cyrne L, Soares H, Antunes F. Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol 2014;2:535-62.
27. Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 2014;20:1126-67.
28. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000;24:372-6.
29. Noble M, Mayer-Proschel M, Proschel C. Redox regulation of precursor cell function: insights and paradoxes. Antioxid Redox Signal 2005;7:1456-67.
30. Pervaiz S, Taneja R, Ghaffari S. Oxidative stress regulation of stem and progenitor cells. Antioxid Redox Signal 2009;11:2777-89.
31. Piccoli C, D'Aprile A, Ripoli M, Scrima R, Lecce L, Boffoli D, et al. Bone-marrow derived hematopoietic stem/progenitor cells express multiple isoforms of NADPH oxidase and produce constitutively reactive oxygen species. Biochem Biophys Res Commun 2007;353:965-72.
32. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, Wang T, Gregg D, Ramaswami P, et al. Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 2003;108:457-63.
33. Singh U, Jialal I. Oxidative stress and atherosclerosis. Pathophysiology 2006;13:129-42.
34. Sirker AA, Astroulakis ZM, Hill JM. Vascular progenitor cells and translational research: the role of endothelial and smooth muscle progenitor cells in endogenous arterial remodelling in the adult. Clin Sci (Lond) 2009;116:283-99.
35. Smith J, Ladi E, Mayer-Proschel M, Noble M. Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell. Proc Natl Acad Sci U S A 2000;97:10032-7.
36. Strehlow K, Werner N, Berweiler J, Link A, Dirnagl U, Priller J, et al. Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation 2003;107:3059-65.
37. Subramanian K, Geraerts M, Pauwelyn KA, Park Y, Owens DJ, Muijtjens M, et al. Isolation procedure and characterization of multipotent adult progenitor cells from rat bone marrow. Methods Mol Biol 2010;636:55-78.
38. Sun B, Feng M, Tian X, Lu X, Zhang Y, Ke X, et al. DL-3-n-butylphthalide protects rat bone marrow stem cells against hydrogen peroxide-induced cell death through antioxidation and activation of PI3K-Akt pathway. Neurosci Lett 2012;516:247-52.
39. Tousoulis D, Andreou I, Antoniades C, Tentolouris C, Stefanadis C. Role of inflammation and oxidative stress in endothelial progenitor cell function and mobilization: therapeutic implications for cardiovascular diseases. Atherosclerosis 2008;201:236-47.
40. Ulloa-Montoya F, Kidder BL, Pauwelyn KA, Chase LG, Luttun A, Crabbe A, et al. Comparative transcriptome analysis of embryonic and adult stem cells with extended and limited differentiation capacity. Genome Biol 2007;8:163-71.
41. Urbich C, Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 2004;95:343-53.
42. Vitetta L, Linnane AW. Endocellular regulation by free radicals and hydrogen peroxide: key determinants of the inflammatory response. Inflammopharmacology 2014;22:69-72.
43. Wang TT, Zeng GC, Li XC, Zeng HP. In vitro studies on the antioxidant and protective effect of 2-substituted -8-hydroxyquinoline derivatives against H(2)O(2)-induced oxidative stress in BMSCs. Chem Biol Drug Des 2010;75:214-22.
44. Wang FW, Wang Z, Zhang YM, Du ZX, Zhang XL, Liu Q, et al. Protective effect of melatonin on bone marrow mesenchymal stem cells against hydrogen peroxide-induced apoptosis in vitro. Cell Biochem 2013;114:2346-55.
45. Wang L, Yuan R, Yao C, Wu Q, Christelle M, Xie W, et al. Effects of resolvin D1 on inflammatory responses and oxidative stress of lipopolysaccharide-induced acute lung injury in mice. Chin Med J (Engl) 2014;127:803-9.
46. Werner N, Junk S, Laufs U, Link A, Walenta K, Bohm M, et al. Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ Res 2003;93:e17-24.
47. Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005;353:999-1007.
48. Widlansky ME, Gokce N, Keaney Jr JF, Vita JA. The clinical implications of endothelial dysfunction. J Am Coll Cardiol 2003;42:1149-60.
49. Xu J, Liu X, Chen J, Zacharek A, Cui X, Savant-Bhonsale S, et al. Simvastatin enhances bone marrow stromal cell differentiation into endothelial cells via notch signaling pathway. AJP Cell Physiol 2009;296:C535-43.
50. Xu J, Liu X, Chen J, Zacharek A, Cui X, Savant-Bhonsale S, et al. Cell-cell interaction promotes rat marrow stromal cell differentiation into endothelial cells via the activation of TACE/TNF-alpha signaling. Cell Transplant 2010;19:43-53.
51. Yang K, Wang XQ, He YS, Lu L, Chen QJ, Liu J, et al. Advanced glycation end products induce chemokine/cytokine production via activation of p38 pathway and inhibit proliferation and migration of bone marrow mesenchymal stem cells. Cardiovasc Diabetol 2010;9:66.
52. Zhu X, Zuo L, Cardounel AJ, Zweier JL, He G. Characterization of in vivo tissue redox status, oxygenation, and formation of reactive oxygen species in postischemic myocardium. Antioxid Redox Signal 2007;9:447-55.