Involvement of the up-regulated FoxO1 expression in follicular granulosa cell apoptosis induced by oxidative stress

Journal of Biological Chemistry

Volumn 287, Issue 31, 2012, Pages 25727-25740

  Shen, Ming ^a   Lin, Fei ^a   Zhang, Jiaqing ^a   Tang, Yiting ^a   Chen, Wei Kang ^b   Liu, Honglin ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b Building C   (China)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC; GRANULOSA CELLS; IN-VITRO; IN-VIVO; INSULIN TREATMENT; NUCLEAR TRANSLOCATIONS; OVER-EXPRESSION; PRO-APOPTOTIC GENES; STAGE OF GROWTH; STRESS-INDUCED; TARGET GENES; UNDERLYING MECHANISM; UP-REGULATION;

CELL DEATH; MAMMALS; OXIDATIVE STRESS; TRANSCRIPTION FACTORS;

GENE EXPRESSION REGULATION;

INSULIN; TRANSCRIPTION FACTOR FKHR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDATIVE GENE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION REGULATION; GRANULOSA CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROAPOPTOTIC GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; UPREGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL NUCLEUS; CELLS, CULTURED; FEMALE; FOLLICULAR ATRESIA; FORKHEAD TRANSCRIPTION FACTORS; GENE KNOCKDOWN TECHNIQUES; GRANULOSA CELLS; INSULIN; MICE; MICE, INBRED ICR; NITRO COMPOUNDS; OXIDANTS; OXIDATIVE STRESS; PRIMARY CELL CULTURE; PROPIONIC ACIDS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; TRANSCRIPTION, GENETIC; UP-REGULATION;

MAMMALIA; MUS;

EID: 84864389133     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.349902     Document Type: Article

References (83)

1. Asselin, E., Xiao, C. W., Wang, Y. F., and Tsang, B. K. (2000) Mammalian follicular development and atresia. Role of apoptosis. Biol. Signals Recept. 9, 87-95 (Pubitemid 30301433)
2. Jiang, J. Y., Cheung, C. K., Wang, Y., and Tsang, B. K. (2003) Regulation of cell death and cell survival gene expression during ovarian follicular development and atresia. Front. Biosci. 8, d222-d237 (Pubitemid 39069973)
3. Valdez, K. E., Cuneo, S. P., and Turzillo, A. M. (2005) Regulation of apoptosis in the atresia of dominant bovine follicles of the first follicular wave following ovulation. Reproduction 130, 71-81 (Pubitemid 41015234)
4. Inoue, N., Maeda, A., Matsuda-Minehata, F., Fukuta, K., and Manabe, N. (2006) Expression and localization of Fas ligand and Fas during atresia in porcine ovarian follicles. J. Reprod. Dev. 52, 723-730 (Pubitemid 46143739)
5. Essers, M. A., Weijzen, S., de Vries-Smits, A. M., Saarloos, I., de Ruiter, N. D., Bos, J. L., and Burgering, B. M. (2004) FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J. 23, 4802-4812 (Pubitemid 40069710)
6. Storz, P. (2011) Forkhead homeobox type O transcription factors in the responses to oxidative stress. Antioxid. Redox Signal. 14, 593-605
7. Essers, M. A., de Vries-Smits, L. M., Barker, N., Polderman, P. E., Burgering, B. M., and Korswagen, H. C. (2005) Functional interaction between β-catenin and FOXO in oxidative stress signaling. Science 308, 1181-1184 (Pubitemid 40696437)
8. Clopton, D. A., and Saltman, P. (1995) Low-level oxidative stress causes cell-cycle specific arrest in cultured cells. Biochem. Biophys. Res. Commun. 210, 189-196
9. Dröge, W., and Kinscherf, R. (2008) Aberrant insulin receptor signaling and amino acid homeostasis as a major cause of oxidative stress in aging. Antioxid. Redox Signal. 10, 661-678 (Pubitemid 351225905)
10. Finkel, T., and Holbrook, N. J. (2000) Oxidants, oxidative stress and the biology of aging. Nature 408, 239-247
11. Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T. I., Jones, D. P., and Wang, X. (1997) Prevention of apoptosis by Bcl-2. Release of cytochrome c from mitochondria blocked. Science 275, 1129-1132 (Pubitemid 27097312)
12. Franco, R., Sánchez-Olea, R., Reyes-Reyes, E. M., and Panayiotidis, M. I. (2009) Environmental toxicity, oxidative stress, and apoptosis. Menage a trois. Mutat. Res. 674, 3-22
13. Murdoch, W. J. (1998) Inhibition by oestradiol of oxidative stress-induced apoptosis in pig ovarian tissues. J. Reprod. Fertil. 114, 127-130
14. Kumar, M., Pathak, D., Kriplani, A., Ammini, A. C., Talwar, P., and Dada, R. (2010) Nucleotide variations in mitochondrial DNA and supraphysiological ROS levels in cytogenetically normal cases of premature ovarian insufficiency. Arch. Gynecol. Obstet. 282, 695-705
15. Ortega-Camarillo, C., González-González, A., Vergara-Onofre, M., González-Padilla, E., Avalos-Rodríguez, A., Gutiérrez-Rodríguez, M. E., Arriaga-Pizano, L., Cruz, M., Baiza-Gutman, L. A., and Díaz-Flores, M. (2009) Changes in the glucose-6-phosphate dehydrogenase activity in granulosa cells during follicular atresia in ewes. Reproduction. 137, 979-986
16. Tilly, J. L., and Tilly, K. I. (1995) Inhibitors of oxidative stress mimic the ability of follicle-stimulating hormone to suppress apoptosis in cultured rat ovarian follicles. Endocrinology 136, 242-252
17. Melov, S. (2002) Animal models of oxidative stress, aging, and therapeutic antioxidant interventions. Int. J. Biochem. Cell Biol. 34, 1395-1400
18. Gille, J. J., and Joenje, H. (1992) Cell culture models for oxidative stress. Superoxide and hydrogen peroxide versus normobaric hyperoxia. Mutat. Res. 275, 405-414
19. Song, X., Bao, M., Li, D., and Li, Y. M. (1999) Advanced glycation in D-galactose-induced mouse aging model. Mech. Ageing Dev. 108, 239-251 (Pubitemid 29240629)
20. Sener, G., Sehirli, O., Ipçi, Y., Cetinel, S., Cikler, E., Gedik, N., and Alican, I. (2005) Protective effects of taurine against nicotine-induced oxidative damage of rat urinary bladder and kidney. Pharmacology 74, 37-44 (Pubitemid 40591462)
21. Gupta, R. K., Meachum, S., Hernández-Ochoa, I., Peretz, J., Yao, H. H., and Flaws, J. A. (2009) Methoxychlor inhibits growth of antral follicles by altering cell cycle regulators. Toxicol. Appl. Pharmacol. 240, 1-7
22. Alston, T. A., Mela, L., and Bright, H. J. (1977) 3-Nitropropionate, the toxic substance of Indigofera, is a suicide inactivator of succinate dehydrogenase. Proc. Natl. Acad. Sci. U.S.A. 74, 3767-3771 (Pubitemid 8189964)
23. Beal, M. F., Brouillet, E., Jenkins, B., Henshaw, R., Rosen, B., and Hyman, B. T. (1993) Age-dependent striatal excitotoxic lesions produced by the endogenous mitochondrial inhibitor malonate. J. Neurochem. 61, 1147-1150 (Pubitemid 23241258)
24. Brouillet, E., Hantraye, P., Ferrante, R. J., Dolan, R., Leroy-Willig, A., Kowall, N. W., and Beal, M. F. (1995) Chronic mitochondrial energy impairment produces selective striatal degeneration and abnormal choreiform movements in primates. Proc. Natl. Acad. Sci. U.S.A. 92, 7105-7109
25. Montilla, P., Túnez, I., Muñoz, M. C., Salcedo, M., Feijóo, M., Muñoz- Castañeda, J. R., and Bujalance, I. (2004) Effect of glucocorticoids on 3-nitropropionic acid-induced oxidative stress in synaptosomes. Eur. J. Pharmacol. 488, 19-25 (Pubitemid 38388519)
26. Alexi, T., Hughes, P. E., Faull, R. L., and Williams, C. E. (1998) 3-Nitropropionic acid's lethal triplet. Cooperative pathways of neurodegeneration. Neuroreport 9, R57-R64 (Pubitemid 28387125)
27. Schulz, J. B., Henshaw, D. R., MacGarvey, U., and Beal, M. F. (1996) Involvement of oxidative stress in 3-nitropropionic acid neurotoxicity. Neurochem. Int. 29, 167-171 (Pubitemid 26232004)
28. Fontaine, M. A., Geddes, J. W., Banks, A., and Butterfield, D. A. (2000) Effect of exogenous and endogenous antioxidants on 3-nitropionic acid-induced in vivo oxidative stress and striatal lesions. Insights into Huntington's disease. J. Neurochem. 75, 1709-1715
29. Kim, G. W., Copin, J. C., Kawase, M., Chen, S. F., Sato, S., Gobbel, G. T., and Chan, P. H. (2000) Excitotoxicity is required for induction of oxidative stress and apoptosis in mouse striatum by the mitochondrial toxin, 3-nitropropionic acid. J. Cereb. Blood Flow Metab. 20, 119-129 (Pubitemid 30019837)
30. Kumar, P., Kalonia, H., and Kumar, A. (2011) Novel protective mechanisms of antidepressants against 3-nitropropionic acid induced Huntington's- like symptoms. A comparative study. J. Psychopharmacol. 25, 1399-1411
31. 2 availability to ARPE-19 cultures in models of oxidative stress. Free Radic. Biol. Med. 48, 1064-1070
32. Henzler, T., and Steudle, E. (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina. Model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J. Exp. Bot. 51, 2053-2066 (Pubitemid 32100632)
33. Floyd, R. A., and Carney, J. M. (1992) Free radical damage to protein and DNA. Mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann. Neurol. 32, S22-S27
34. Farombi, E. O., Møller, P., and Dragsted, L. O. (2004) Ex vivo and in vitro protective effects of kolaviron against oxygen-derived radical-induced DNA damage and oxidative stress in human lymphocytes and rat liver cells. Cell Biol. Toxicol. 20, 71-82 (Pubitemid 38988054)
35. Barthel, A., Schmoll, D., and Unterman, T. G. (2005) FoxO proteins in insulin action and metabolism. Trends Endocrinol. Metab. 16, 183-189 (Pubitemid 40603098)
36. Accili, D., and Arden, K. C. (2004) FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117, 421-426 (Pubitemid 38610228)
37. Greer, E. L., and Brunet, A. (2005) FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24, 7410-7425 (Pubitemid 41637981)
38. Giannakou, M. E., and Partridge, L. (2004) The interaction between FOXO and SIRT1. Tipping the balance towards survival. Trends Cell Biol. 14, 408-412 (Pubitemid 39092697)
39. Huang, H., and Tindall, D. J. (2007) Dynamic FoxO transcription factors. J. Cell Sci. 120, 2479-2487 (Pubitemid 47323857)
40. Hughes, K. J., Meares, G. P., Hansen, P. A., and Corbett, J. A. (2011) FoxO1 and SIRT1 regulate α-cell responses to nitric oxide. J. Biol. Chem. 286, 8338-8348
41. Brunet, A., Kanai, F., Stehn, J., Xu, J., Sarbassova, D., Frangioni, J. V., Dalal, S. N., DeCaprio, J. A., Greenberg, M. E., and Yaffe, M. B. (2002) 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J. Cell Biol. 156, 817-828 (Pubitemid 34839865)
42. Nakamura, N., Ramaswamy, S., Vazquez, F., Signoretti, S., Loda, M., and Sellers, W. R. (2000) Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol. Cell. Biol. 20, 8969-8982 (Pubitemid 32245927)
43. Dijkers, P. F., Medema, R. H., Pals, C., Banerji, L., Thomas, N. S., Lam, E. W., Burgering, B. M., Raaijmakers, J. A., Lammers, J. W., Koenderman, L., and Coffer, P. J. (2000) Forkhead transcription factor FKHR-L1 modulates cytokine-dependent transcriptional regulation of p27Kip1. Mol. Cell. Biol. 20, 9138-9148 (Pubitemid 32246103)
44. Gilley, J., Coffer, P. J., and Ham, J. (2003) FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J. Cell Biol. 162, 613-622 (Pubitemid 37022939)
45. Modur, V., Nagarajan, R., Evers, B. M., and Milbrandt, J. (2002) FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer. J. Biol. Chem. 277, 47928-47937 (Pubitemid 36159321)
46. Lee, S. S., Kennedy, S., Tolonen, A. C., and Ruvkun, G. (2003) DAF-16 target genes that control C. elegans life span and metabolism. SCIENCE 300, 644-647 (Pubitemid 36520589)
47. Greer, E. L., and Brunet, A. (2008) FOXO transcription factors in ageing and cancer. Acta Physiol. 192, 19-28 (Pubitemid 350284502)
48. Henderson, S. T., and Johnson, T. E. (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr. Biol. 11, 1975-1980 (Pubitemid 33146425)
49. Brunet, A., Sweeney, L. B., Sturgill, J. F., Chua, K. F., Greer, P. L., Lin, Y., Tran, H., Ross, S. E., Mostoslavsky, R., Cohen, H. Y., Hu, L. S., Cheng, H. L., Jedrychowski, M. P., Gygi, S. P., Sinclair, D. A., Alt, F. W., and Greenberg, M. E. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303, 2011-2015 (Pubitemid 38393275)
50. Martinez, S. C., Tanabe, K., Cras-Méneur, C., Abumrad, N. A., Bernal- Mizrachi, E., and Permutt, M. A. (2008) Inhibition of Foxo1 protects pancreatic islet β-cells against fatty acid and endoplasmic reticulum stress-induced apoptosis. Diabetes 57, 846-859
51. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., Anderson, M. J., Arden, K. C., Blenis, J., and Greenberg, M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868 (Pubitemid 29165088)
52. Cui, M., Huang, Y., Zhao, Y., and Zheng, J. (2009) New insights for FOXO and cell fate decision in HIV infection and HIV-associated neurocognitive disorder. Adv. Exp. Med. Biol. 665, 143-159
53. Kops, G. J., Dansen, T. B., Polderman, P. E., Saarloos, I., Wirtz, K. W., Coffer, P. J., Huang, T. T., Bos, J. L., Medema, R. H., and Burgering, B. M. (2002) Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419, 316-321
54. Marinkovic, D., Zhang, X., Yalcin, S., Luciano, J. P., Brugnara, C., Huber, T., and Ghaffari, S. (2007) Foxo3 is required for the regulation of oxidative stress in erythropoiesis. J. Clin. Invest. 117, 2133-2144 (Pubitemid 47219558)
55. Alcendor, R. R., Gao, S., Zhai, P., Zablocki, D., Holle, E., Yu, X., Tian, B., Wagner, T., Vatner, S. F., and Sadoshima, J. (2007) Sirt1 regulates aging and resistance to oxidative stress in the heart. Circ. Res. 100, 1512-1521 (Pubitemid 46834764)
56. Burgering, B. M., and Kops, G. J. (2002) Cell cycle and death control. Long live Forkheads. Trends Biochem. Sci. 27, 352-360 (Pubitemid 34756518)
57. 2-M checkpoint in response to oxidative stress. J. Biol. Chem. 277, 26729-26732
58. 2 mRNA expression by Forkhead transcription factors. Novel mechanism for cell cycle control by phosphoinositide 3-kinase and Forkhead. Mol. Cell. Biol. 24, 2181-2189
59. Medema, R. H., Kops, G. J., Bos, J. L., and Burgering, B. M. (2000) AFX-like Forkhead transcription factors mediate cell cycle regulation by Ras and PKB through p27Kip1. Nature 404, 782-787 (Pubitemid 30212408)
60. Tran, H., Brunet, A., Grenier, J. M., Datta, S. R., Fornace, A. J., Jr., DiStefano, P. S., Chiang, L. W., and Greenberg, M. E. (2002) DNA repair pathway stimulated by the Forkhead transcription factor FOXO3a through the Gadd45 protein. Science 296, 530-534 (Pubitemid 34408672)
61. Kim, G. W., and Chan, P. H. (2001) Oxidative stress and neuronal DNA fragmentation mediate age-dependent vulnerability to the mitochondrial toxin, 3-nitropropionic acid, in the mouse striatum. Neurobiol. Dis. 8, 114-126 (Pubitemid 32171823)
62. Nicolson, G. L., Yanagimachi, R., and Yanagimachi, H. (1975) Ultrastructural localization of lectin-binding sites on the zonae pellucidae and plasma membranes of mammalian eggs. J. Cell Biol. 66, 263-274
63. Kajihara, T., Uchino, S., Suzuki, M., Itakura, A., Brosens, J. J., and Ishihara, O. (2009) Increased ovarian follicle atresia in obese Zucker rats is associated with enhanced expression of the Forkhead transcription factor FOXO1. Med. Mol. Morphol. 42, 216-221
64. Burgering, B. M., and Medema, R. H. (2003) Decisions on life and death. FOXO Forkhead transcription factors are in command when PKB/Akt is off duty. J. Leukoc. Biol. 73, 689-701 (Pubitemid 38040447)
65. Urbich, C., Knau, A., Fichtlscherer, S., Walter, D. H., Brühl, T., Potente, M., Hofmann, W. K., de Vos, S., Zeiher, A. M., and Dimmeler, S. (2005) FOXO-dependent expression of the proapoptotic protein Bim: pivotal role for apoptosis signaling in endothelial progenitor cells. FASEB J. 19, 974-976 (Pubitemid 40827722)
66. Adachi, M., Osawa, Y., Uchinami, H., Kitamura, T., Accili, D., and Brenner, D. A. (2007) The Forkhead transcription factor FoxO1 regulates proliferation and transdifferentiation of hepatic stellate cells. Gastroenterology 132, 1434-1446 (Pubitemid 46627569)
67. Matsuda-Minehata, F., Inoue, N., Goto, Y., and Manabe, N. (2006) The regulation of ovarian granulosa cell death by pro- and antiapoptotic molecules. J. Reprod. Dev. 52, 695-705 (Pubitemid 46150826)
68. Dlamini, Z., Mbita, Z., and Zungu, M. (2004) Genealogy, expression, and molecular mechanisms in apoptosis. Pharmacol. Ther. 101, 1-15 (Pubitemid 38068522)
69. Yuan, H., Zhang, X., Huang, X., Lu, Y., Tang, W., Man, Y., Wang, S., Xi, J., and Li, J. (2010) NADPH oxidase 2-derived reactive oxygen species mediate FFAs-induced dysfunction and apoptosis of β-cells via JNK, p38 MAPK, and p53 pathways. PLoS One 5, e15726
70. Shen, B., Gao, L., Hsu, Y. T., Bledsoe, G., Hagiwara, M., Chao, L., and Chao, J. (2010) Kallistatin attenuates endothelial apoptosis through inhibition of oxidative stress and activation of Akt-eNOS signaling. Am. J. Physiol. Heart Circ. Physiol. 299, H1419-H1427
71. shc-dependent signaling pathway. Science 295, 2450-2452
72. Buczyńska, A., and Szadkowska-Stańczyk, I. (2005) Identification of health hazards to rural population living near pesticide dump sites in Poland. Int. J. Occup. Med. Environ. Health 18, 331-339
73. Hoyer, P. B., and Sipes, I. G. (2007) Development of an animal model for ovotoxicity using 4-vinylcyclohexene. A case study. Birth Defects Res. B Dev. Reprod. Toxicol. 80, 113-125 (Pubitemid 46762320)
74. Hu, X., Roberts, J. R., Apopa, P. L., Kan, Y. W., and Ma, Q. (2006) Accelerated ovarian failure induced by 4-vinyl cyclohexene diepoxide in Nrf2 null mice. Mol. Cell. Biol. 26, 940-954 (Pubitemid 43146488)
75. Grotowski, W., Lecybył, R., Warenik-Szymankiewicz, A., and Trzeciak, W. H. (1997) [The role of apoptosis of granulosa cells in follicular atresia]. Ginekol Pol. 68, 317-326
76. Schiaffonati, L., Rappocciolo, E., Tacchini, L., Cairo, G., and Bernelli- Zazzera, A. (1990) Reprogramming of gene expression in postischemic rat liver. Induction of proto-oncogenes and hsp70 gene family. J. Cell. Physiol. 143, 79-87
77. Salo, D. C., Donovan, C. M., and Davies, K. J. (1991) HSP70 and other possible heat shock or oxidative stress proteins are induced in skeletal muscle, heart, and liver during exercise. Free Radic. Biol. Med. 11, 239-246 (Pubitemid 121003919)
78. Mujahid, A., Akiba, Y., and Toyomizu, M. (2007) Acute heat stress induces oxidative stress and decreases adaptation in young white leghorn cockerels by down-regulation of avian uncoupling protein. Poult. Sci. 86, 364-371 (Pubitemid 47581121)
79. Silva, J. E. (2006) Thermogenic mechanisms and their hormonal regulation. Physiol. Rev. 86, 435-464
80. Venditti, P., Pamplona, R., Ayala, V., De Rosa, R., Caldarone, G., and Di Meo, S. (2006) Differential effects of experimental and cold-induced hyperthyroidism on factors inducing rat liver oxidative damage. J. Exp. Biol. 209, 817-825
81. Morales, A. E., Pérez-Jiménez, A., Hidalgo, M. C., Abellán, E., and Cardenete, G. (2004) Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 139, 153-161 (Pubitemid 39535800)
82. Zafir, A., and Banu, N. (2009) Induction of oxidative stress by restraint stress and corticosterone treatments in rats. Indian J. Biochem. Biophys. 46, 53-58
83. Silva, R. H., Abílio, V. C., Takatsu, A. L., Kameda, S. R., Grassl, C., Chehin, A. B., Medrano, W. A., Calzavara, M. B., Registro, S., Andersen, M. L., Machado, R. B., Carvalho, R. C., Ribeiro Rde, A., Tufik, S., and Frussa- Filho, R. (2004) Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice. Neuropharmacology 46, 895-903 (Pubitemid 38368922)