Age-associated changes in the subcellular localization of phosphorylated p38 MAPK in human granulosa cells

Molecular Human Reproduction

Volumn 16, Issue 12, 2010, Pages 928-937

  Ito, Megumu ^a   Miyado, Kenji ^a   Nakagawa, Koji ^a,e   Muraki, Miho ^a,f   Imai, Misa ^a,g   Yamakawa, Naomi ^b   Qin, Junwen ^c   Hosoi, Yoshihiko ^d   Saito, Hidekazu ^a   Takahashi, Yuji ^a  

^a NATIONAL CENTER FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^c JINAN UNIVERSITY   (China)

^d KINKI UNIVERSITY   (Japan)

^e Sugiyama Clinic   (Japan)

^f UNIVERSITY OF TOKYO   (Japan)

^g TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Granulosa cell; Localization; p38 MAPK

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACETYLCYSTEINE; FOLLITROPIN; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR ALPHA;

AGING; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE ACTIVATION; GRANULOSA CELL; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ADULT; AGE FACTORS; CELL LINE; ENZYME ACTIVATION; FEMALE; FOLLICLE STIMULATING HORMONE; GRANULOSA CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78649482868     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gaq076     Document Type: Article

References (58)

1. Abidi P, Leers-Sucheta S, Cortez Y, Han J, Azhar S. Evidence that age-related changes in p38 MAP kinase contribute to the decreased steroid production by the adrenocortical cells from old rats. Aging Cell 2008;7:168-178.
2. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005;3:28.
3. Aplin AE, Hogan BP, Tomeu J, Juliano RL. Cell adhesion differentially regulates the nucleocytoplasmic distribution of active MAP kinases. J Cell Sci 2002;115:2781-2790.
4. Ben-Levy R, Hooper S, Wilson R, Paterson HF, Marshall CJ. Nuclear export of the stress-activated protein kinase p38 mediated by its substrate MAPKAP kinase-2. Curr Biol 1998;8:1049-1057.
5. Caballero M, Liton PB, Challa P, Epstein DL, Gonzalez P. Effects of donor age on proteasome activity and senescence in trabecular meshwork cells. Biochem Biophys Res Commun 2004;323:1048-1054.
6. Chandel NS, Schumacker PT, Arch RH. Reactive oxygen species are downstream products of TRAF-mediated signal transduction. J Biol Chem 2001;276:42728-42736.
7. Chao HT, Lee SY, Lee HM, Liao TL, Wei YH, Kao SH. Repeated ovarian stimulations induce oxidative damage and mitochondrial DNA mutations in mouse ovaries. Ann N Y Acad Sci 2005;1042: 148-156.
8. Chen RH, Sarnecki C, Blenis J. Nuclear localization and regulation of erk- and rsk-encoded protein kinases. Mol Cell Biol 1992;12:915-927.
9. Davis T, Wyllie FS, Rokicki MJ, Bagley MC, Kipling D. The role of cellular senescence in Werner syndrome: toward therapeutic intervention in human premature aging. Ann N Y Acad Sci 2007;1100:455-469.
10. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2002;82:47-95.
11. Engel K, Kotlyarov A, Gaestel M. Leptomycin B-sensitive nuclear export of MAPKAP kinase 2 is regulated by phosphorylation. EMBO J 1998;17:3363-3371.
12. Ge B, Gram H, Di Padova F, Huang B, New L, Ulevitch RJ, Luo Y, Han J. MAPKK-independent activation of p38alpha mediated by TAB1-dependent autophosphorylation of p38alpha. Science 2002;295:1291-1294.
13. Han J, Lee JD, Tobias PS, Ulevitch RJ. Endotoxin induces rapid protein tyrosine phosphorylation in 70Z/3 cells expressing CD14. J Biol Chem 1993;268:25009-25014.
14. Haq R, Brenton JD, Takahashi M, Finan D, Finkielsztein A, Damaraju S, Rottapel R, Zanke B. Constitutive p38HOG mitogen-activated protein kinase activation induces permanent cell cycle arrest and senescence. Cancer Res 2002;62:5076-5082.
15. Hensley K, Floyd RA, Zheng NY, Nael R, Robinson KA, Nguyen X, Pye QN, Stewart CA, Geddes J, Markesbery WR et al. p38 kinase is activated in the Alzheimer's disease brain. J Neurochem 1999;72:2053-2058.
16. Higashimoto T, Panopoulos A, Hsieh CL, Zandi E. TNFalpha induces chromosomal abnormalities independent of ROS through IKK, JNK, p38 and caspase pathways. Cytokine 2006;34:39-50.
17. Hsieh CC, Papaconstantinou J. The effect of aging on p38 signaling pathway activity in the mouse liver and in response to ROS generated by 3-nitropropionic acid. Mech Ageing Dev 2002;123:1423-1435.
18. Hsieh CC, Papaconstantinou J. Akt/PKB and p38 MAPK signaling, translational initiation and longevity in Snell dwarf mouse livers. Mech Ageing Dev 2004;125:785-798.
19. Hsieh CC, Rosenblatt JI, Papaconstantinou J. Age-associated changes in SAPK/JNK and p38 MAPK signaling in response to the generation of ROS by 3-nitropropionic acid. Mech Ageing Dev 2003;124: 733-746.
20. Huang C, Ma WY, Maxiner A, Sun Y, Dong Z. p38 kinase mediates UV-induced phosphorylation of p53 protein at serine 389. J Biol Chem 1999;274:12229-12235.
21. Hunzicker-Dunn M, Maizels ET. FSH signaling pathways in immature granulosa cells that regulate target gene expression: branching out from protein kinase A. Cell Signal 2006;18:1351-1359.
22. Imai M, Muraki M, Takamatsu K, Saito H, Seiki M, Takahashi Y. Spontaneous transformation of human granulosa cell tumours into an aggressive phenotype: a metastasis model cell line. BMC Cancer 2008;8:319.
23. Ito M, Muraki M, Takahashi Y, Imai M, Tsukui T, Yamakawa N, Nakagawa K, Ohgi S, Horikawa T, Iwasaki W et al. Glutathione S-transferase theta 1 expressed in granulosa cells as a biomarker for oocyte quality in age-related infertility. Fertil Steril 2008;90:1026-1035.
24. Janknecht R, Hunter T. Convergence of MAP kinase pathways on the ternary complex factor Sap-1a. EMBO J 1997;16:1620-1627.
25. Jones DP. Radical-free biology of oxidative stress. Am J Physiol 2008;295:C849-C868.
26. Klein NA, Battaglia DE, Fujimoto VY, Davis GS, Bremner WJ, Soules MR. Reproductive aging: accelerated ovarian follicular development associated with a monotropic follicle-stimulating hormone rise in normal older women. J Clin Endocrinol Metab 1996;81:1038-1045.
27. Kotlyarov A, Yannoni Y, Fritz S, Laass K, Telliez JB, Pitman D, Lin LL, Gaestel M. Distinct cellular functions of MK2. Mol Cell Biol 2002;22:4827-4835.
28. Kwong J, Hong L, Liao R, Deng Q, Han J, Sun P. p38alpha and p38gamma mediate oncogenic ras-induced senescence through differential mechanisms. J Biol Chem 2009;284:11237-11246.
29. Lee HC, Wei YH. Oxidative stress, mitochondrial DNA mutation, and apoptosis in aging. Exp Biol Med 2007;232:592-606.
30. Li J, Holbrook NJ. Common mechanisms for declines in oxidative stress tolerance and proliferation with aging. Free Radic Biol Med 2003;35:292-299.
31. Lu G, Kang YJ, Han J, Herschman HR, Stefani E, Wang Y. TAB-1 modulates intracellular localization of p38 MAP kinase and downstream signaling. J Biol Chem 2006;281:6087-6095.
32. Maezawa I, Nivison M, Montine KS, Maeda N, Montine TJ. Neurotoxicity from innate immune response is greatest with targeted replacement of E4 allele of apolipoprotein E gene and is mediated by microglial p38MAPK. Faseb J 2006;20:797-799.
33. Maizels ET, Cottom J, Jones JC, Hunzicker-Dunn M. Follicle stimulating hormone (FSH) activates the p38 mitogen-activated protein kinase pathway, inducing small heat shock protein phosphorylation and cell rounding in immature rat ovarian granulosa cells. Endocrinology 1998;139:3353-3356.
34. McTavish KJ, Jimenez M, Walters KA, Spaliviero J, Groome NP, Themmen AP, Visser JA, Handelsman DJ, Allan CM. Rising follicle-stimulating hormone levels with age accelerate female reproductive failure. Endocrinology 2007;148:4432-4439.
35. Nakagawa K, Ohgi S, Horikawa T, Kojima R, Ito M, Saito H. Laparoscopy should be strongly considered for women with unexplained infertility. J Obstet Gynaecol Res 2007;33:665-670.
36. Natale DR, Paliga AJ, Beier F, D'Souza SJ, Watson AJ. p38 MAPK signaling during murine preimplantation development. Dev Biol 2004;268:76-88.
37. New L, Jiang Y, Han J. Regulation of PRAK subcellular location by p38 MAP kinases. Mol Biol Cell 2003;14:2603-2616.
38. Parker CG, Hunt J, Diener K, McGinley M, Soriano B, Keesler GA, Bray J, Yao Z, Wang XS, Kohno T et al. Identification of stathmin as a novel substrate for p38 delta. Biochem Biophys Res Commun 1998;249:791-796.
39. Paul A, Wilson S, Belham CM, Robinson CJ, Scott PH, Gould GW, Plevin R. Stress-activated protein kinases: activation, regulation and function. Cell Signal 1997;9:403-410.
40. Pfundt R, van Vlijmen-Willems I, Bergers M, Wingens M, Cloin W, Schalkwijk J. In situ demonstration of phosphorylated c-jun and p38 MAP kinase in epidermal keratinocytes following ultraviolet B irradiation of human skin. J Pathol 2001;193:248-255.
41. Raman M, Chen W, Cobb MH. Differential regulation and properties of MAPKs. Oncogene 2007;26:3100-3112.
42. Seternes OM, Johansen B, Hegge B, Johannessen M, Keyse SM, Moens U. Both binding and activation of p38 mitogen-activated protein kinase (MAPK) play essential roles in regulation of the nucleocytoplasmic distribution of MAPK-activated protein kinase 5 by cellular stress. Mol Cell Biol 2002;22:6931-6945.
43. Shibuya H, Yamaguchi K, Shirakabe K, Tonegawa A, Gotoh Y, Ueno N, Irie K, Nishida E, Matsumoto K. TAB1: an activator of the TAK1 MAPKKK in TGF-beta signal transduction. Science 1996;272:1179-1182.
44. Shin MH, Rhie GE, Kim YK, Park CH, Cho KH, Kim KH, Eun HC, Chung JH. H2O2 accumulation by catalase reduction changes MAP kinase signaling in aged human skin in vivo. J Invest Dermatol 2005;125:221-229.
45. Suh Y. Age-specific changes in expression, activity, and activation of the c-Jun NH(2)-terminal kinase and p38 mitogen-activated protein kinases by methyl methanesulfonate in rats. Mech Ageing Dev 2001;122:1797-1811.
46. Sumbayev VV, Yasinska IM. Regulation of MAP kinase-dependent apoptotic pathway: implication of reactive oxygen and nitrogen species. Arch Biochem Biophys 2005;436:406-412.
47. Tan Y, Rouse J, Zhang A, Cariati S, Cohen P, Comb MJ. FGF and stress regulate CREB and ATF-1 via a pathway involving p38 MAP kinase and MAPKAP kinase-2. EMBO J 1996;15:4629-4642.
48. Tatone C, Carbone MC, Falone S, Aimola P, Giardinelli A, Caserta D, Marci R, Pandolfi A, Ragnelli AM, Amicarelli F. Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol Hum Reprod 2006;12:655-660.
49. Tatone C, Amicarelli F, Carbone MC, Monteleone P, Caserta D, Marci R, Artini PG, Piomboni P, Focarelli R. Cellular and molecular aspects of ovarian follicle ageing. Hum Reprod Update. 2008;14:131-142.
50. Tsai-Turton M, Luderer U. Opposing effects of glutathione depletion and follicle-stimulating hormone on reactive oxygen species and apoptosis in cultured preovulatory rat follicles. Endocrinology 2006;147:1224-1236.
51. Villa-Diaz LG, Miyano T. Activation of p38 MAPK during porcine oocyte maturation. Biol Reprod 2004;71:691-696.
52. Wang XZ, Ron D. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase. Science 1996;272:1347-1349.
53. Wang W, Chen JX, Liao R, Deng Q, Zhou JJ, Huang S, Sun P. Sequential activation of the MEK-extracellular signal-regulated kinase and MKK3/6-p38 mitogen-activated protein kinase pathways mediates oncogenic ras-induced premature senescence. Mol Cell Biol 2002;22:3389-3403.
54. White A, Pargellis CA, Studts JM, Werneburg BG, Farmer BT 2nd. Molecular basis of MAPK-activated protein kinase 2:p38 assembly. Proc Natl Acad Sci USA 2007;104:6353-6358.
55. Yoon SO, Yun CH, Chung AS. Dose effect of oxidative stress on signal transduction in aging. Mech Ageing Dev 2002;123:1597-1604.
56. Yu FQ, Han CS, Yang W, Jin X, Hu ZY, Liu YX. Activation of the p38 MAPK pathway by follicle-stimulating hormone regulates steroidogenesis in granulosa cells differentially. J Endocrinol 2005;186:85-96.
57. Zarubin T, Han J. Activation and signaling of the p38 MAP kinase pathway. Cell Res 2005;15:11-8.
58. Zhang Y, Herman B. Ageing and apoptosis. Mech Ageing Dev 2002;123:245-260.