Autophagy is a cell survival program for female germ cells in the murine ovary

Reproduction

Volumn 141, Issue 6, 2011, Pages 759-765

  Gawriluk, Thomas R ^c   Hale, Amber N ^c   Flaws, Jodi A ^a   Dillon, Christopher P ^b   Green, Douglas R ^b   Rucker III, Edmund B ^c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATG7 PROTEIN; BECLIN 1; CELL MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; FEMALE FERTILITY; GENE TARGETING; GERM CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; OVARY; OVARY FOLLICLE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL COUNT; CELL SURVIVAL; FEMALE; FERTILITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; OVARY; OVUM; RNA, MESSENGER;

MURINAE;

EID: 79957628020     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-10-0489     Document Type: Article

References (49)

1. Adhikari D, Flohr G, Gorre N, Shen Y, Yang H, Lundin E, Lan Z, Gambello MJ & Liu K 2009 Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Molecular Human Reproduction 15 765-770. (doi:10.1093/molehr/gap092)
2. Adhikari D, Zheng W, Shen Y, Gorre N, Hamalainen T, Cooney AJ, Huhtaniemi I, Lan ZJ & Liu K 2010 Tsc/mTORC1 signaling in oocytes governs the quiescence and activation of primordial follicles. Human Molecular Genetics 19 397-410. (doi:10.1093/hmg/ddp483)
3. Akar U, Chaves-Reyez A, Barria M, Tari A, Sanguino A, Kondo Y, Kondo S, Arun B, Lopez-Berestein G & Ozpolat B 2008 Silencing of Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells. Autophagy 4 669-679.
4. Anasti JN 1998 Premature ovarian failure: an update. Fertility and Sterility 70 1-15. (doi:10.1016/S0015-0282(98)00099-5)
5. Bedell MA, Brannan CI, Evans EP, Copeland NG, Jenkins NA & Donovan PJ 1995 DNA rearrangements located over 100 kb 5′ of the Steel (Sl)-coding region in Steel-panda and Steel-contrasted mice deregulate Sl expression and cause female sterility by disrupting ovarian follicle development. Genes and Development 9 455-470. (doi:10.1101/gad.9.4.455)
6. Bergeron L, Perez GI, Macdonald G, Shi L, Sun Y, Jurisicova A, Varmuza S, Latham KE, Flaws JA, Salter JC et al. 1998 Defects in regulation of apoptosis in caspase-2-deficient mice. Genes and Development 12 1304-1314. (doi:10.1101/gad.12.9.1304)
7. Borgeest C, Symonds D, Mayer LP, Hoyer PB & Flaws JA 2002 Methoxychlor may cause ovarian follicular atresia and proliferation of the ovarian epithelium in the mouse. Toxicological Sciences 68 473-478. (doi:10.1093/toxsci/68.2.473)
8. Byskov AGS 1978 Follicular atresia. In The Vertebrate Ovary, pp 533-562. Ed. RE Jones. New York: Plenum Press.
9. Ciechomska IA, Goemans GC, Skepper JN & Tolkovsky AM 2009 Bcl-2 complexed with Beclin-1 maintains full anti-apoptotic function. Oncogene 28 2128-2141. (doi:10.1038/onc.2009.60)
10. Codogno P & Meijer AJ 2005 Autophagy and signaling: their role in cell survival and cell death. Cell Death and Differentiation 2 1509-1518. (doi:10.1038/sj.cdd.4401751)
11. Dou Z, Pan JA, Lin RZ & ZongWX 2011 The beta identity of class I PtdIns3K: a positive role of p110b in autophagy revealed. Autophagy 7 246-247. (doi:10.4161/auto.7.2.14346)
12. Edson MA, Nagaraja AK & Matzuk MM 2009 The mammalian ovary from genesis to revelation. Endocrine Reviews 30 624-712. (doi:10.1210/er.2009-0012)
13. Escobar ML, Echeverria OM, Ortiz R & Vazquez-Nin GH 2008a Combined apoptosis and autophagy, the process that eliminates the oocytes of atretic follicles in immature rats. Apoptosis 13 1253-1266. (doi:10.1007/s10495-008- 0248-z)
14. Escobar ML, Echeverría OM, Sánchez-Sánchez L, Méndez C, Pedernera E & Vázquez-Nin GH 2008b Analysis of different cell death processes of prepubertal rat oocytes in vitro. Apoptosis 15 511-526. (doi:10.1007/s10495-009-0448-1)
15. Gaytan M, Morales C, Sanchez-Criado JE & Gaytan F 2008 Immunolocalization of beclin 1, a bcl-2-binding, autophagy-related protein, in the human ovary: possible relation to life span of corpus luteum. Cell and Tissue Research 331 509-517. (doi:10.1007/s00441-007-0531-2)
16. Greenfeld CR, Pepling ME, Babus JK, Furth PA & Flaws JA 2007 BAX regulates follicular endowment in mice. Reproduction 133 865-876. (doi:10.1530/REP-06-0270)
17. Huang EJ, Manova K, Packer AI, Sanchez S, Bachvarova RF & Besmer P 1993 The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Developmental Biology 157 100-109. (doi:10.1006/dbio.1993.1115)
18. Hull MG, Glazener CM, Kelly NJ, Conway DI, Foster PA, Hinton RA, Coulson C, Lambert PA, Watt EM & Desai KM 1985 Population study of causes, treatment, and outcome of infertility. BMJ 291 1693-1697. (doi:10.1136/bmj.291. 6510.1693)
19. Jia S, Liu Z, Zhang S, Liu P, Zhang L, Lee SH, Zhang J, Signoretti S, Loda M, Roberts TM et al. 2008 Essential roles of PI(3)K-p110beta in cell growth, metabolism and tumorigenesis. Nature 454 776-779. (doi:10.1038/ nature07091)
20. Kang JS, Lee CJ, Lee JM, Rha JY, Song KW & Park MH 2003 Follicular expression of c-Kit/SCF and inhibin-a in mouse ovary during development. Journal of Histochemistry & Cytochemistry 51 1447-1458. (doi:10.1177/ 002215540305101105)
21. Kim YG, Kim JY, Mohan C & Lee GM 2009 Effect of Bcl-x(L) overexpression on apoptosis and autophagy in recombinant Chinese hamster ovary cells under nutrient-deprived condition. Biotechnology and Bioengineering 103 757-766. (doi:10.1002/bit.22298)
22. Klionsky DJ & Emr SD 2000 Autophagy as a regulated pathway of cellular degradation. Science 290 1717-1721. (doi:10.1126/science.290.5497.1717)
23. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y et al. 2005 Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. Journal of Cell Biology 169 425-434. (doi:10.1083/jcb.200412022)
24. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T & Mizushima N 2004 The role of autophagy during the early neonatal starvation period. Nature 432 1032-1036. (doi:10.1038/nature03029)
25. Levine B & Kroemer G 2008 Autophagy in the pathogenesis of disease. Cell 132 27-42. (doi:10.1016/j.cell.2007.12.018)
26. Liang C, Feng P, Ku B, Dotan I, Canaani D, Oh BH & Jung JU 2006 Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nature Cell Biology 8 688-699. (doi:10.1038/ncb1426)
27. Lobascio AM, Klinger FG, Scaldaferri ML, Farini D & De Felici M 2007 Analysis of programmed cell death in mouse fetal oocytes. Reproduction 134 241-252. (doi:10.1530/REP-07-0141)
28. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N et al. 2007 Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO Journal 26 2527-2539. (doi:10.1038/sj.emboj.7601689)
29. Maiuri MC, Criollo A & Kroemer G 2010 Crosstalk between apoptosis and autophagy within the Beclin 1 interactome. EMBO Journal 29 515-516. (doi:10.1038/emboj.2009.377)
30. Matzuk MM & Lamb DJ 2002 Genetic dissection of mammalian fertility pathways. Nature Cell Biology 4 41-49. (doi:10.1038/ncb-nm-fertilityS41)
31. Matzuk MM & Lamb DJ 2008 The biology of infertility: research advances and clinical challenges. Nature Medicine 14 1197-1213. (doi:10.1038/nm.f.1895)
32. Oberstein A, Jeffrey PD & Shi Y 2007 Crystal structure of the Bcl-XL - Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. Journal of Biological Chemistry 282 13123-13132. (doi:10.1074/jbc.M700492200)
33. Packer AI, Hsu YC, Besmer P & Bachvarova RF 1994 The ligand of the c-kit receptor promotes oocyte growth. Developmental Biology 161 194-205. (doi:10.1006/dbio.1994.1020)
34. Pan H, O'Brien MJ,Wigglesworth K, Eppig JJ & Schultz RM 2005 Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Developmental Biology 286 493-506. (doi:10.1016/j.ydbio.2005.08.023)
35. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y et al. 2003 Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. Journal of Clinical Investigation 112 1809-1820. (doi:10.1172/JCI20039)
36. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hamalainen T & Peng SL 2008 Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319 611-613. (doi:10.1126/science.1152257)
37. Reddy P, Adhikari D, Zheng W, Liang S, Hamalainen T, Tohonen V, Ogawa W, Noda T, Volarevic S & Huhtaniemi I 2009 PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Human Molecular Genetics 18 2813-2824. (doi:10.1093/hmg/ddp217)
38. Riedlinger G, Okagaki R, Wagner KU, Rucker EB III, Oka T, Miyoshi K, Flaws JA & Hennighausen L 2002 Bcl-x is not required for maintenance of follicles and corpus luteum in the postnatal mouse ovary. Biology of Reproduction 66 438-444. (doi:10.1095/biolreprod66.2.438)
39. Rodrigues P, Limback D, McGinnis LK, Plancha CE & Albertini DF 2009 Multiple mechanisms of germ cell loss in the perinatal mouse ovary. Reproduction 137 709-720. (doi:10.1530/REP-08-0203)
40. Rosales-Torres AM, Avalos-Rodríguez A, Vergara-Onofre M, Hernández-Pérez O, Ballesteros LM, García-Macedo R, Ortíz-Navarrete V & Rosado A 2000 Multiparametric study of atresia in ewe antral follicles: histology, flow cytometry, internucleosomal DNA fragmentation, and lysosomal enzyme activities in granulosa cells and follicular fluid. Molecular Reproduction and Development 55 270-281. (doi:10.1002/(SICI) 1098-2795(200003)55:3〉270::AID-MRD5〉3.0.CO;2-H)
41. Rucker EB III, Dierisseau P, Wagner KU, Garrett L, Wynshaw-Boris A, Flaws JA & Hennighausen L 2000 Bcl-x and Bax regulate mouse primordial germ cell survival and apoptosis during embryogenesis. Molecular Endocrinology 14 1038-1052. (doi:10.1210/me.14.7.1038)
42. Santos HB, Thomé RG, Arantes FP, Sato Y, Bazzoli N & Rizzo E 2008 Ovarian follicular atresia is mediated by heterophagy, autophagy, and apoptosis in Prochilodus argenteus and Leporinus taeniatus (Teleostei: Characiformes). Theriogenology 70 1449-1460. (doi:10.1016/j.theriogenology.2008. 06.091)
43. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB & Tsujimoto Y 2004 Role of Bcl-2 family proteins in a nonapoptotic programmed cell death dependent on autophagy genes. Nature Cell Biology 6 1221-1228. (doi:10.1038/ncb1192)
44. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y, Liang C, Jung JU, Cheng JQ, Mulé JJ et al. 2007 Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nature Cell Biology 9 1142-1151. (doi:10.1038/ncb1634)
45. Tingen CM, Bristol-Gould SK, Kiesewetter SE, Wellington JT, Shea L & Woodruff TK 2009 Prepubertal primordial follicle loss in mice is not due to classical apoptotic pathways. Biology of Reproduction 81 16-25. (doi:10.1095/biolreprod.108.074898)
46. Velentzas AD, Nezis IP, Stravopodis DJ, Papassideri IS & Margaritis LH 2007 Mechanisms of programmed cell death during oogenesis in Drosophila virilis. Cell and Tissue Research 327 399-414. (doi:10.1007/s00441-006-0298-x)
47. Wagner KU, Wall RJ, St-Onge L, Gruss P, Garrett L, Wynshaw-Boris A, Li M, Furth PA & Hennighausen L 1997 Cre mediated gene deletion in the mammary gland. Nucleic Acids Research 25 4323-4330. (doi:10.1093/nar/25.21.4323)
48. Yue Z, Jin S, Yang C, Levine AJ & Heintz N 2003 Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. PNAS 100 15077-15082. (doi:10.1073/pnas.2436255100)
49. Zarnescu O 2004 Ultrastructural observations of previtellogenic ovarian follicles of dove. Zygote 12 285-292. (doi:10.1017/S0967199404002837)