17β-Estradiol Protects Skeletal Myoblasts From Apoptosis Through p53, Bcl-2, and FoxO Families

Journal of Cellular Biochemistry

Volumn 118, Issue 1, 2017, Pages 104-115

  La Colla, Anabela ^a   Vasconsuelo, Andrea ^a   Milanesi, Lorena ^a   Pronsato, Lucía ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

17 ESTRADIOL; Bcl 2; C2C12 MUSCLE CELLS; FoxOs; p53

Indexed keywords

BIM PROTEIN; ESTRADIOL; HYDROGEN PEROXIDE; PROTEIN BCL 2; PROTEIN MDM2; PROTEIN NOXA; PROTEIN P53; PUMA PROTEIN; TRANSCRIPTION FACTOR FOXO; BCL2 PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GENE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTO ONCOGENE; SKELETAL MYOBLAST; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; METABOLISM;

ANIMALS; APOPTOSIS; CELL LINE; ESTRADIOL; FORKHEAD TRANSCRIPTION FACTORS; HYDROGEN PEROXIDE; MICE; MYOBLASTS, SKELETAL; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-BCL-2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84977090557     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25616     Document Type: Article

References (52)

1. Appella E, Anderson CW. 2001. Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 268:2764–2772.
2. Attardi LD, Reczek EE, Cosmas C, Demicco EG, McCurrach ME, Lowe SW, Jacks T. 2000. PERP, an apoptosis-associated target of p53, is a novel member of the PMP-22/gas3 family. Genes Dev 14:704–718.
3. Bradford M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254.
4. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857–868.
5. Burattini S, Ferri P, Battistelli M, Curci R, Luchetti F, Falcieri E. 2004. C2C12 murine myoblasts as a model of skeletal muscle development: Morpho-functional characterization. Eur J Histochem 48:223–233.
6. Caelles C, Helmberg A, Karin M. 1994. P53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 370:220–223.
7. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG, Colman PM, Day CL, Adams JM, Huang DC. 2005. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17:393–403.
8. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR. 2004. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303:1010–1014.
9. Essers MA, Weijzen S, de Vries-Smits AM, Saarloos I, de Ruiter ND, Bos JL, Burgering BMT. 2004. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 23:4802–4812.
10. Guo J, Gertsberg Z, Ozgen N, Steinberg SF. 2009. P66Shc links alpha1-adrenergic receptors to a reactive oxygen species-dependent AKTFOXO3A phosphorylation pathway in cardiomyocytes. Circ Res 104:660–669.
11. Haldar S, Negrini M, Monne M, Sabbioni S, Croce CM. 1994. Down-regulation of bcl-2 by p53 in breast cancer cells. Cancer Res 15:2095–2097.
12. Harris SL, Levine AJ. 2005. The p53 pathway: Positive and negative feedback loops. Oncogene 24:2899–2908.
13. Hemann MT, Zilfou JT, Zhao Z, Burgess DJ, Hannon GJ, Lowe SW. 2004. Suppression of tumorigenesis by the p53 target PUMA. Proc Natl Acad Sci USA 101:9333–9338.
14. Hyder SM, Nawaz Z, Chiappetta C, Yokoyama K, Stancel GM. 1995. The protooncogene c-jun contains an unusual estrogen-inducible enhancer within the coding sequence. J Biol Chem 270:8506–8513.
15. Jejurikar SS, Henkelman EA, Cederna PS, Marcelo CL, Urbanchek MG, Kuzon WM. 2006. Aging increases the susceptibility of skeletal muscle derived satellite cells to apoptosis. Exp Gerontol 41:828–836.
16. Korsmeyer SJ. 1999. BCL-2 gene family and the regulation of programmed cell death. Cancer Res 59:1693–1700.
17. Kubbutat MH, Jones SN, Vousden KH. 1997. Regulation of p53 stability by Mdm2. Nature 387:299–303.
18. La Colla A, Boland R, Vasconsuelo A. 2015. 17β-Estradiol abrogates apoptosis inhibiting PKCδ, JNK, and p66Shc activation in C2C12 cells. J Cell Biochem 116:1454–1465.
19. La Colla A, Vasconsuelo A, Boland R. 2013. Estradiol exerts antiapoptotic effects in skeletal myoblasts via mitochondrial PTP and MnSOD. J Endocrinol 216:331–341.
20. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685.
21. Liu H, Pedram A, Kim JK. 2011. Oestrogen prevents cardiomyocyte apoptosis by suppressing p38α-mediated activation of p53 and by down-regulating p53 inhibition on p38β. Card Res 89:119–128.
22. Maltzman W, Czyzyk L. 1984. UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol Cell Biol 4:1689–1694.
23. Mayo LD, Seo YR, Jackson MW, Smith ML, Rivera Guzman J, Korgaonkar CK, Donner DB. 2005. Phosphorylation of human p53 at serine 46 determines promoter selection and whether apoptosis is attenuated or amplified. J Biol Chem 280:25953–25959.
24. Milanesi L, Russo de Boland A, Boland R. 2008. Expression and localization of estrogen receptor alpha in C2C12 murine muscle cell line. J Cell Biochem 104:1254–1273.
25. Miyashita T, Harigai M, Hanada M, Reed JC. 1994. Identification of a p53-dependent negative response element in the bcl-2 gene. Cancer Res 54:3131–3135.
26. Morley JE, Malmstrom TK. 2013. Frailty, sarcopenia, and hormones. Endocrinol Metab Clin North Am 42:391–405.
27. Nakano K, Vousden KH. 2001. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7:683–694.
28. O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, Cory S, Huang DC. 1998. Bim: A novel member of the Bcl-2 family that promotes apoptosis. EMBO J 17:384–395.
29. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, Tokino T, Taniguchi T, Tanaka N. 2000. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288:1053–1058.
30. Oh SW, Mukhopadhyay A, Svrzikapa N, Jiang F, Davis RJ, Tissenbaum HA. 2005. JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16. Proc Natl Acad Sci USA 102:4494–4499.
31. Perillo B, Sasso A, Abbondanza C, Palumbo G. 2000. 17β-Estradiol inhibits apoptosis in MCF-7 cells, inducing bcl-2 expression via two estrogen-responsive elements present in the coding sequence. Mol Cell Biol 20:2890–2901.
32. Piette J, Neel H, Marechal V. 1997. Mdm2: Keeping p53 under control. Oncogene 15:1001–1010.
33. Plas DR, Thompson CB. 2003. Akt activation promotes degradation of tuberin and FOXO3a via the proteasome. J Biol Chem 278:12361–12366.
34. Prives C, Hall PA. 1999. The p53 pathway. J Pathol 187:112–126.
35. Pronsato L, Boland R, Milanesi L. 2012. Testosterone exerts antiapoptotic effects against H2O2 in C2C12 skeletal muscle cells through the apoptotic intrinsic pathway. J Endocrinol 212:371–381.
36. Renault VM, Thekkat PU, Hoang KL, White JL, Brady CA, Broz DK, Venturelli OS, Johnson TM, Oskoui PR, Xuan Z, Santo EE, Zhang MQ, Vogel H, Attardi LD, Brunet A. 2011. The pro-longevity gene FoxO3 is a direct target of the p53 tumor suppressor. Oncogene 30:3207–3221.
37. Ries S, Biederer C, Woods D, Shifman O, Shirasawa S, Sasazuki T, McMahon M, Oren M, McCormick F. 2000. Opposing effects of Ras on p53: Transcriptional activation of mdm2 and induction of p19ARF. Cell 103:321–330.
38. Ryan KM, Phillips AC, Vousden KH. 2001. Regulation and function of the p53 tumor suppressor protein. Curr Opin Cell Biol 13:332–337.
39. Samejima K, Earnshaw WC. 2005. Trashing the genome: The role of nucleases during apoptosis. Nat Rev Mol Cell Biol 6:677–688.
40. Salih DA, Brunet A. 2008. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol 20:126–136.
41. Sax JK, Fei P, Murphy ME, Bernhard E, Korsmeyer SJ, El-Deiry WS. 2002. BID regulation by p53 contributes to chemosensitivity. Nat Cell Biol 4:842–849.
42. Seto M, Jaeger U, Hockett RD, Graninger W, Bennett S, Goldman P, Korsmeyer SJ. 1988. Alternative promoters and exons, somatic mutation and deregulation of the bcl-2-Ig fusion gene in lymphoma. EMBO J 7:123–131.
43. Storz P. 2011. Forkhead homeobox type O transcription factors in the responses to oxidative stress. Antioxid Redox Signal 14:593–605.
44. Strasser A, O'Connor L, Dixit VM. 2000. Apoptosis signaling. Ann Rev Biochem 69:217–245.
45. Tukey JW. 1953. Some selected quick and easy methods of statistical analysis. Trans NY Acad Sci 16:88–97.
46. Vasconsuelo A, Milanesi L, Boland R. 2008. 17β-Estradiol abrogates apoptosis in murine skeletal muscle cells through estrogen receptors: Role of the phosphatidylinositol 3-kinase/Akt pathway. J Endocrinol 196:385–397.
47. Vasconsuelo A, Milanesi L, Boland RL. 2010. Participation of HSP27 in the antiapoptotic action of 17b-estradiol in skeletal muscle cells. Cell Stress Chaperones 15:183–192.
48. Vousden KH, Lu X. 2002. Live or let die: The cell's response to p53. Nat Rev Cancer 2:594–604.
49. Wang M, Tsai BM, Reiger KM, Brown JW, Meldrum DR. 2006. 17-beta-Estradiol decreases p38 MAPK-mediated myocardial inflammation and dysfunction following acute ischemia. J Mol Cell Card 40:205–212.
50. Yamamoto H, Ozaki T, Nakanishi M, Kikuchi H, Yoshida K, Horie H, Kuwano H, Nakagawara A. 2007. Oxidative stress induces p53-dependent apoptosis in hepatoblastoma cell through its nuclear translocation. Genes Cells 12:461–471.
51. Yang JY, Zong CS, Xia W, Yamaguchi H, Ding Q, Xie X, Lang JY, Lai CC, Chang CJ, Huang WC, Huang H, Kuo HP, Lee DF, Li LY, Lien HC, Cheng X, Chang KJ, Hsiao CD, Tsai FJ, Tsai CH, Sahin AA, Muller WJ, Mills GB, Yu D, Hortobagyi GN, Hung MC. 2008. ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 10:138–148.
52. Yu J, Zhang L. 2008. PUMA, a potent killer with or without p53. Oncogene 27:S71–S83.