Estradiol exerts antiapoptotic effects in skeletal myoblasts via mitochondrial PTP and MnSOD

Journal of Endocrinology

Volumn 216, Issue 3, 2013, Pages 331-341

  La Colla, Anabela ^a   Vasconsuelo, Andrea ^a   Boland, Ricardo ^a  

^a UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

Author keywords

17 estradiol; Antiapoptotic effect; C2C12 skeletal myoblasts; MnSOD; MPTP

Indexed keywords

ESTRADIOL; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE;

ANIMAL CELL; ANTIAPOPTOTIC EFFECT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; APOPTOSIS; CELL LINE; ESTRADIOL; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MYOBLASTS, SKELETAL; SUBCELLULAR FRACTIONS; SUPEROXIDE DISMUTASE;

EID: 84875061844     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-12-0486     Document Type: Article

References (49)

1. Antignani A & Youle RJ 2006 How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Current Opinion in Cell Biology 18 685-689. (doi:10.1016/j.ceb.2006.10.004)
2. Armstrong JS 2006 The role of themitochondrial permeability transition in cell death. Mitochondrion 6 225-234. (doi:10.1016/j.mito.2006.07.006)
3. Beato M, Chavez S & Truss M 1996 Transcriptional regulation by steroid hormones. Steroids 61 240-251. (doi:10.1016/0039-128X(96)00030-X)
4. Bhuyan KC & Bhuyan DK 1978 Superoxide dismutase of the eye: relative functions of superoxide dismutase and catalase in protecting the ocular lens from oxidative damage. Biochimica et Biophysica Acta 542 28-38. (doi:10.1016/0304-4165(78)90229-5)
5. BjornstromL & SjobergM 2005 Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Molecular Endocrinology 19 833-842. (doi:10.1210/me.2004-0486)
6. Bradford M 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 248-254. (doi:10.1016/0003-2697(76)90527-3)
7. Burattini S, Ferri P, Battistelli M, Curci R, Luchetti F & Falcieri E 2004 C2C12 murine myoblasts as a model of skeletal muscle development: morphofunctional characterization. European Journal of Histochemistry 48 223-233.
8. Crompton M 1999 The mitochondrial permeability transition pore and its role in cell death. Biochemical Journal 341 233-249. (doi:10.1042/0264-6021:3410233)
9. De Feo P 1996 Hormonal regulation of human protein metabolism. European Journal of Endocrinology 135 7-18. (doi:10.1530/eje.0.1350007)
10. Desagher S & Martinou JC 2000 Mitochondria as the central control point of apoptosis. Trends in Cell Biology 1 369-377. (doi:10.1016/S0962-8924(00)01803-1)
11. Ernster L & Schatz G 1981 Mitochondria: a historical review. Journal of Cell Biology 91 227-255. (doi:10.1083/jcb.91.3.227s)
12. Evans RM 1988 The steroid and thyroid hormone receptor superfamily. Science 240 889-895. (doi:10.1126/science.3283939)
13. Fujimura M, Morita-Fujimura Y, Narasimhan P, Copin JC, Kawase M & Chan PH 1999 Copper-zinc superoxide dismutase prevents the early decrease of apurinic/apyrimidinic endonuclease and subsequent DNA fragmentation after transient focal cerebral ischemia in mice. Stroke 30 2408-2415. (doi:10.1161/01.STR.30.11.2408)
14. Gogvadze V, Orrenius S & Zhivotovsky B 2006 Multiple pathways of cytochrome c release from mitochondria in apoptosis. Biochimica et Biophysica Acta 1757 639-647. (doi:10.1016/j.bbabio.2006.03.016)
15. Gottipati S & Cammarata PR 2008 Mitochondrial superoxide dismutase activation with 17b-estradiol-treated human lens epithelial cells. Molecular Vision 14 898-905.
16. Green DR & Kroemer G 2004 The pathophysiology of mitochondrial cell death. Science 5684 626-629. (doi:10.1126/science.1099320)
17. Halestrap AP, McStay GP & Clarke SJ 2002 The permeability transition pore complex: another view. Biochimie 84 153-166. (doi:10.1016/S0300-9084(02)01375-5)
18. Hall JM, Couse JF & Korach KS 2001 The multifaceted mechanisms of estradiol and estrogen receptor signaling. Journal of Biological Chemistry 276 36869-36872. (doi:10.1074/jbc.R100029200)
19. Hewitt SC & Korach KS 2002 Estrogen receptors: structure, mechanisms and function. Reviews in Endocrine & Metabolic Disorders 3 193-200. (doi:10.1023/A:1020068224909)
20. Jejurikar SS & Kuzon M Jr 2003 Satellite cell depletion in degenerative skeletal muscle. Apoptosis 8 573-578. (doi:10.1023/A:1026127307457)
21. Jejurikar SS, Henkelman EA, Cederna PS, Marcelo CL, Urbanchek MG & Kuzon WMJr 2006 Aging increases the susceptibility of skeletal muscle derived satellite cells to apoptosis. Experimental Gerontology 41 828-836. (doi:10.1016/j.exger.2006.06.053)
22. Jiang X & Wang X 2004 Cytochrome c-mediated apoptosis. Annual Review of Biochemistry 73 87-106. (doi:10.1146/annurev.biochem.73.011303. 073706)
23. Jiang B, Xiao W, Shi Y, Liu M & Xiao X 2005 Role of Smac/DIABLO in hydrogen peroxide-induced apoptosis in C2C12 myogenic cells. Free Radical Biology & Medicine 39 658-667. (doi:10.1016/j.freeradbiomed. 2005.04.018)
24. Kroemer G, Dallaporta B & Resche-Rigon M 1998 The mitochondrial death/life regulator in apoptosis and necrosis. Annual Review of Physiology 60 619-642. (doi:10.1146/annurev.physiol.60.1.619)
25. Kumarswamy R & Chandna S 2009 Putative partners in Bax mediated cytochrome-c release: ANT, CypD, VDAC or none of them? Mitochondrion 9 1-8. (doi:10.1016/j.mito.2008.10.003)
26. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680-685. (doi:10.1038/ 227680a0)
27. Lazarow A & Cooperstein SJ 1953 Studies on the enzymatic basis for the Janus Green B staining reaction. Journal of Histochemistry and Cytochemistry 1 234-241. (doi:10.1177/1.4.234)
28. Liu X, Kim CN, Yang J, Jemmerson R & Wang X 1996 Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86 147-157. (doi:10.1016/S0092-8674(00)80085-9)
29. Manna SK, Zhang HJ, Yan T, Oberley LW & Aggarwal BB 1998 Overexpression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappaB and activated protein-1. Journal of Biological Chemistry 273 13245-13254. (doi:10.1074/jbc.273.21.13245)
30. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC et al. 1998 Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281 2027-2031. (doi:10.1126/science.281.5385. 2027)
31. Narita M, Shimizu S, Ito T, Chittenden T, Lutz RJ, Matsuda H & Tsujimoto Y 1998 Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. PNAS 95 14681-14686. (doi:10.1073/pnas.95.25.14681)
32. Petronilli V, Costantini P, Scorrano L, Colonna R, Passamonti S & Bernardi P 1994 The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. Journal of Biological Chemistry 269 16638-16642.
33. Petronilli V, Miotto G, Canton M, Brini M, Colonna R & Bernardi P 1999 Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophysical Journal 76 725-734. (doi:10.1016/S0006-3495(99)77239-5)
34. Pettersson K, Delaunay F & Gustafsson JA 2000 Estrogen receptor b acts as a dominant regulator of estrogen signaling. Oncogene 19 4970-4978. (doi:10.1038/sj.onc.1203828)
35. 2 in C2C12 skeletal muscle cells through the apoptotic intrinsic pathway. Journal of Endocrinology 212 371-381. (doi:10.1530/JOE-11-0234)
36. Reed JC 1997 Cytochrome c: can't live with it - can't live without it. Cell 91 559-562. (doi:10.1016/S0092-8674(00)80442-0)
37. Reed JC & Kroemer G 1998 The permeability transition pore complex: a target for apoptosis regulation by caspases and Bcl-2-related proteins. Journal of Experimental Medicine 187 1261-1271. (doi:10.1084/jem.187. 8.1261)
38. Ronda A, Vasconsuelo A & Boland R 2010 Extracellular-regulated kinase and p38 mitogen-activated protein kinases are involved in the antiapoptotic action of 17b-estradiol in skeletal muscle cells. Journal of Endocrinology 2 235-246. (doi:10.1677/JOE-09-0429)
39. Sharpe JC, Arnoult D & Youle RJ 2004 Control of mitochondrial permeability by Bcl-2 family members. Biochimica et Biophysica Acta 1644 107-113. (doi:10.1016/j.bbamcr.2003.10.016)
40. 2-mediated oxidative stress in differentiated C2C12 myotubes. Life Sciences 84 468-481. (doi:10.1016/j.lfs.2009.01.014)
41. Stirone C, Duckles SP, Krause DN & Procaccio V 2005 Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Molecular Pharmacology 4 959-965. (doi:10.1124/mol.105. 014662)
42. Tsai MJ & O'Malley BW 1994 Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annual Review of Biochemistry 63 451-486. (doi:10.1146/annurev.bi.63.070194. 002315)
43. Tsujimoto Y 2003 Cell death regulation by the Bcl-2 protein family in the mitochondria. Journal of Cellular Physiology 195 158-167. (doi:10.1002/ jcp.10254)
44. Tukey JW 1953 Some selected quick and easy methods of statistical analysis. Transactions of the New York Academy of Sciences 16 88-97. (doi:10.1111/j.2164-0947.1953.tb01326.x)
45. Van Remmen H, Williams MD, Guo Z, Estlack L, Yang H, Carlson EJ, Epstein CJ, Huang TT & Richardson A 2001 Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. American Journal of Physiology-Heart and Circulatory Physiology 281 1422-1432.
46. Vasconsuelo A, Milanesi LM & Boland RL 2008 17β-Estradiol abrogates apoptosis in murine skeletal muscle cells through estrogen receptors: role of the phosphatidylinositol 3-kinase/Akt pathway. Journal of Endocrinology 196 385-389. (doi:10.1677/JOE-07-0250)
47. Vasconsuelo A, Milanesi L & Boland RL 2010 Participation of HSP27 in the antiapoptotic action of 17β-estradiol in skeletal muscle cells. Cell Stress Chaperones 15 183-192. (doi:10.1007/s12192-009-0132-y)
48. Vasconsuelo A, Pronsato L, Ronda AC, Boland RL & Milanesi L 2011 Role of 17β-estradiol and testosterone in apoptosis. Steroids 76 1223-1231. (doi:10.1016/j.steroids.2011.08.001)
49. Yoshida N, Yoshida S, Koishi K, Masuda K & Nabeshima Y 1998 Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates 'reserve cells'. Journal of Cell Science 111 769-779.