Protective effect of 17β-estradiol on serum deprivation-induced apoptosis and oxidative stress in bone marrow-derived mesenchymal stem cells

Human and Experimental Toxicology

Volumn 35, Issue 3, 2016, Pages 312-322

  Mirzamohammadi, S ^a   Mehrabani, M ^a   Tekiyehmaroof, N ^a   Sharifi, A M ^a,b  

^a IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

17 estradiol; Apoptosis; bone marrow derived mesenchymal stem cells; ROS; serum deprivation

Indexed keywords

5' NUCLEOTIDASE; CASPASE 3; CD44V ANTIGEN; ENDOGLIN; ESTRADIOL; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; THY 1 ANTIGEN; VASCULAR CELL ADHESION MOLECULE 1; BAX PROTEIN, RAT;

ADHERENT CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN ANTIBODY COMPLEX; APOPTOSIS; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL PROLIFERATION; CELL VIABILITY; COLORIMETRY; CONTROLLED STUDY; IMMUNOPRECIPITATION; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION; ANIMAL; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM; SERUM; WISTAR RAT;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL PROLIFERATION; ESTRADIOL; MALE; MESENCHYMAL STROMAL CELLS; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SERUM;

EID: 84957617288     PISSN: 09603271     EISSN: 14770903     Source Type: Journal    
DOI: 10.1177/0960327115586208     Document Type: Article

References (54)

1. Wei X, Yang X, Han Z-P, et al.Mesenchymal stem cells: a new trend for cell therapy. Acta Pharmacol Sin 2013; 34: 747-654.
2. Rastegar F, Shenaq D, Huang J, et al.Mesenchymal stem cells: molecular characteristics and clinical applications. World J Stem Cells 2010; 2: 67-80.
3. Karp JM, Leng Teo GS,. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 2009; 4: 206-216.
4. Abdi R, Fiorina P, Adra CN, et al.Immunomodulation by mesenchymal stem cells a potential therapeutic strategy for type 1 diabetes. Diabetes 2008; 57: 1759-1767.
5. Geng YJ,. Molecular mechanisms for cardiovascular stem cell apoptosis and growth in the hearts with atherosclerotic coronary disease and ischemic heart failure. Ann N Y Acad Sci 2003; 1010: 687-697.
6. Toma C, Pittenger MF, Cahill KS, et al.Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002; 105: 93-98.
7. Zhang M, Methot D, Poppa V, et al.Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J Mol Cell Cardiol 2001; 33: 907-921.
8. Zhu W, Chen J, Cong X, et al.Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells. Stem Cells 2006; 24: 416-425.
9. Bialik S, Cryns VL, Drincic A, et al.The mitochondrial apoptotic pathway is activated by serum and glucose deprivation in cardiac myocytes. Circ Res 1999; 85: 403-414.
10. Tsubokawa T, Yagi K, Nakanishi C, et al.Impact of anti-apoptotic and anti-oxidative effects of bone marrow mesenchymal stem cells with transient overexpression of heme oxygenase-1 on myocardial ischemia. Am J Physiol-Heart Circ Physiol 2010; 298: H1320-H1329.
11. Chauvier D, Lecoeur H, Langonne A, et al.Upstream control of apoptosis by caspase-2 in serum-deprived primary neurons. Apoptosis 2005; 10: 1243-1259.
12. Valko M, Leibfritz D, Moncol J, et al.Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39: 44-84.
13. Lee SB, Kim HJ, Shin J, et al.Bcl-XL prevents serum deprivation-induced oxidative stress mediated by Romo1. Oncol Rep 2011; 25: 1337-1342.
14. Liu S-Y, Chen C-L, Yang T-T, et al.Albumin prevents reactive oxygen species-induced mitochondrial damage, autophagy, and apoptosis during serum starvation. Apoptosis 2012; 17: 1156-1169.
15. Lee MY, Jung SC, Lee JH, et al.Estradiol-17β protects against hypoxia-induced hepatocyte injury through ER-mediated upregulation of Bcl-2 as well as ER-independent antioxidant effects. Cell Res 2008; 18: 491-499.
16. Ruiz-Larrea MB, Martín C, Martínez R, et al.Antioxidant activities of estrogens against aqueous and lipophilic radicals: differences between phenol and catechol estrogens. Chem Phys Lipids 2000; 105: 179-188.
17. Han HJ, Park SH, Park HJ, et al.Effect of various oestrogens on cell injury and alteration of apical transporters induced by tert-butyl hydroperoxide in renal proximal tubule cells. Clin Exp Pharmacol Physiol 2002; 29: 60-67.
18. Hong L, Zhang G, Sultana H, et al.The effects of 17-β estradiol on enhancing proliferation of human bone marrow mesenchymal stromal cells in vitro. Stem Cells Dev 2010; 20: 925-931.
19. Zhou S, Zilberman Y, Wassermann K, et al.Estrogen modulates estrogen receptor α and β expression, osteogenic activity, and apoptosis in mesenchymal stem cells (MSCs) of osteoporotic mice. J Cell Biochem 2001; 81: 144-155.
20. Kanda N, Watanabe S,. 17β-estradiol inhibits oxidative stress-induced apoptosis in keratinocytes by promoting Bcl-2 expression. J Invest Dermatol 2003; 121: 1500-1509.
21. Vegeto E, Pollio G, Pellicciari C, et al.Estrogen and progesterone induction of survival of monoblastoid cells undergoing TNF-α-induced apoptosis. FASEB J 1999; 13: 793-803.
22. Chen H-Y, Zhang X, Chen S-F, et al.The protective effect of 17β-estradiol against hydrogen peroxide-induced apoptosis on mesenchymal stem cell. Biomed Pharmacother 2012; 66: 57-63.
23. Zhou J, Lu P, Ren H, et al.17β-estradiol protects human eyelid-derived adipose stem cells against cytotoxicity and increases transplanted cell survival in spinal cord injury. J Cell Mol Med 2014; 18: 326-343.
24. Garbern JC, Lee RT,. Cardiac stem cell therapy and the promise of heart regeneration. Cell Stem Cell 2013; 12: 689-698.
25. Mochizuki H, Choong C-J, Yasuda T,. The promises of stem cells: stem cell therapy for movement disorders. Parkinsonism Relat Disord 2014; 20: S128-S131.
26. Steller H,. Mechanisms and genes of cellular suicide. Science 1995; 267: 1445-1449.
27. Hockenbery DM, Zutter M, Hickey W, et al. BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc Natl Acad Sci U S A 1991; 88: 6961-6965.
28. Boise LH, González-Garcia M, Postema CE, et al.Bcl-x, bcl-2 -related gene that functions as a dominant regulator of apoptotic cell death. Cell 1993; 74: 597-608.
29. Hockenbery D, Nuñez G, Milliman C, et al.Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 1990; 348: 334-336.
30. Lalier L, Cartron P-F, Juin P, et al.Bax activation and mitochondrial insertion during apoptosis. Apoptosis 2007; 12: 887-896.
31. Charles I, Khalyfa A, Kumar DM, et al.Serum deprivation induces apoptotic cell death of transformed rat retinal ganglion cells via mitochondrial signaling pathways. Invest Ophthalmol Vis Sci 2005; 46: 1330-1338.
32. Vanden Hoek TL, Li C, Shao Z, et al.Significant levels of oxidants are generated by isolated cardiomyocytes during ischemia prior to reperfusion. J Mol Cell Cardiol 1997; 29: 2571-2583.
33. Razmara A, Sunday L, Stirone C, et al.Mitochondrial effects of estrogen are mediated by estrogen receptor α in brain endothelial cells. J Pharmacol Exp Ther 2008; 325: 782-790.
34. Razmara A, Duckles SP, Krause DN, et al.Estrogen suppresses brain mitochondrial oxidative stress in female and male rats. Brain Res 2007; 1176: 71-81.
35. Stirone C, Duckles SP, Krause DN, et al.Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 2005; 68: 959-965.
36. Yin H, Xu L, Porter NA,. Free radical lipid peroxidation: mechanisms and analysis. Chem Rev 2011; 111: 5944-5972.
37. Sharma P, Jha AB, Dubey RS, et al.Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012; 2012: 1-26.
38. El-Shafey AF, Armstrong AE, Terrill JR, et al.Screening for increased protein thiol oxidation in oxidatively stressed muscle tissue. Free Rad Res 2011; 45: 991-999.
39. Ayres S, Tang M, Ravi Subbiah M,. Estradiol-17β as an antioxidant: some distinct features when compared with common fat-soluble antioxidants. J Lab Clin Med 1996; 128: 367-375.
40. Ayres S, Abplanalp W, Liu JH, et al.Mechanisms involved in the protective effect of estradiol-17β on lipid peroxidation and DNA damage. Am J Physiol-Endocrinol Metab 1998; 274: E1002-E1008.
41. Bredesen DE,. Neural apoptosis. Ann Neurol 1995; 38: 839-851.
42. Li H, Télémaque S, Miller RE, et al.High glucose inhibits apoptosis induced by serum deprivation in vascular smooth muscle cells via upregulation of Bcl-2 and Bcl-xl. Diabetes 2005; 54: 540-545.
43. Cadenas E,. Biochemistry of oxygen toxicity. Annu Rev Biochem 1989; 58: 79-110.
44. Chen C-S, Tseng Y-T, Hsu Y-Y, et al.Nrf2-Keap1 antioxidant defense and cell survival signaling are upregulated by 17β-estradiol in homocysteine-treated dopaminergic SH-SY5Y cells. Neuroendocrinology 2012; 97: 232-241.
45. Lee SB, Kim JJ, Kim TW, et al.Serum deprivation-induced reactive oxygen species production is mediated by Romo1. Apoptosis 2010; 15: 204-218.
46. Song J-Y, Kim M-J, Jo H-H, et al.Antioxidant effect of estrogen on bovine aortic endothelial cells. J Steroid Biochem Mol Biol 2009; 117: 74-80.
47. McCubrey JA, LaHair MM, Franklin RA,. Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 2006; 8: 1775-1789.
48. Son Y, Cheong Y-K, Kim N-H, et al.Mitogen-activated protein kinases and reactive oxygen species: how can ROS activate MAPK pathways? J Signal Transduct 2011; 2011: 792639.
49. Xia Z, Dickens M, Raingeaud J, et al.Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995; 270: 1326-1331.
50. Eckhoff DE, Smyth CA, Eckstein C, et al.Suppression of the c-Jun N-terminal kinase pathway by 17β-estradiol can preserve human islet functional mass from proinflammatory cytokine-induced destruction. Surgery 2003; 134: 169-179.
51. Kim JK, Pedram A, Razandi M, et al.Estrogen prevents cardiomyocyte apoptosis through inhibition of reactive oxygen species and differential regulation of p38 kinase isoforms. J Biol Chem 2006; 281: 6760-6767.
52. Fan T-J, Han L-H, Cong R-S, et al.Caspase family proteases and apoptosis. Acta Biochim Biophys Sin 2005; 37: 719-727.
53. Brendel A, Felzen V, Morawe T, et al.Differential regulation of apoptosis-associated genes by estrogen receptor alpha in human neuroblastoma cells. Restor Neurol Neurosci 2013; 31: 199-211.
54. Patten RD, Pourati I, Aronovitz MJ, et al.17β-Estradiol reduces cardiomyocyte apoptosis in vivo and in vitro via activation of phospho-inositide-3 kinase/Akt signaling. Circ Res 2004; 95: 692-699.