Autophagy in Drosophila ovaries is induced by starvation and is required for oogenesis

Cell Death and Differentiation

Volumn 18, Issue 6, 2011, Pages 915-924

  Barth, J M I ^a   Szabad, J ^b   Hafen, E ^a   Kohler K ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Autophagy; Drosophila; insulin TOR; oogenesis; starvation

Indexed keywords

AUTOPHAGY PROTEIN 5; INSULIN; TARGET OF RAPAMYCIN KINASE;

ARTICLE; AUTOPHAGY; DROSOPHILA; GENE FUNCTION; GERM CELL; MORPHOGENESIS; NONHUMAN; OOCYTE DEVELOPMENT; OVARY; OVARY FOLLICLE CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STARVATION; UPREGULATION;

ANIMALS; AUTOPHAGY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FAT BODY; FEMALE; GERM CELLS; OOGENESIS; OVARIAN FOLLICLE; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

ANIMALIA;

EID: 79955854666     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2010.157     Document Type: Article

References (39)

1. Melendez A, Neufeld TP. The cell biology of autophagy in metazoans: a developing story. Development 2008; 135: 2347-2360.
2. Neufeld TP. TOR-dependent control of autophagy: biting the hand that feeds. Curr Opin Cell Biol 2010; 22: 157-168.
3. Rusten TE, Lindmo K, Juhasz G, Sass M, Seglen PO, Brech A et al. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev Cell 2004; 7: 179-192. (Pubitemid 39145024)
4. Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell 2004; 7: 167-178. (Pubitemid 39145023)
5. Drummond-Barbosa D, Spradling AC. Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev Biol 2001; 231: 265-278. (Pubitemid 32198402)
6. Bohni R, Riesgo-Escovar J, Oldham S, Brogiolo W, Stocker H, Andruss BF et al. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 1999; 97: 865-875. (Pubitemid 29375046)
7. Richard DS, Rybczynski R, Wilson TG, Wang Y, Wayne ML, Zhou Y et al. Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico1 insulin signaling mutation is autonomous to the ovary. J Insect Physiol 2005; 51: 455-464. (Pubitemid 40678868)
8. Stocker H, Radimerski T, Schindelholz B, Wittwer F, Belawat P, Daram P et al. Rheb is an essential regulator of S6K in controlling cell growth in Drosophila. Nat Cell Biol 2003; 5: 559-565. (Pubitemid 36781091)
9. Werz C, Kohler K, Hafen E, Stocker H. The Drosophila SH2B family adaptor Lnk acts in parallel to chico in the insulin signaling pathway. PLoS Genet 2009; 5: e1000596.
10. Peterson JS, Barkett M, McCall K. Stage-specific regulation of caspase activity in drosophila oogenesis. Dev Biol 2003; 260: 113-123. (Pubitemid 36900339)
11. Hou YC, Chittaranjan S, Barbosa SG, McCall K, Gorski SM. Effector caspase Dcp-1 and IAP protein bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis. J Cell Biol 2008; 182: 1127-1139.
12. Nezis IP, Lamark T, Velentzas AD, Rusten TE, Bjorkoy G, Johansen T et al. Cell death during Drosophila melanogaster early oogenesis is mediated through autophagy. Autophagy 2009; 5: 298-302.
13. Juhasz G, Erdi B, Sass M, Neufeld TP. Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila. Genes Dev 2007; 21: 3061-3066. (Pubitemid 350223523)
14. Scott RC, Juhasz G, Neufeld TP. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol 2007; 17: 1-11. (Pubitemid 46027564)
15. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-5728.
16. Gorski SM, Chittaranjan S, Pleasance ED, Freeman JD, Anderson CL, Varhol RJ et al. A SAGE approach to discovery of genes involved in autophagic cell death. Curr Biol 2003; 13: 358-363. (Pubitemid 36230029)
17. Juhasz G, Puskas LG, Komonyi O, Erdi B, Maroy P, Neufeld TP et al. Gene expression profiling identifies FKBP39 as an inhibitor of autophagy in larval Drosophila fat body. Cell Death Differ 2007; 14: 1181-1190. (Pubitemid 46794922)
18. Zinke I, Schutz CS, Katzenberger JD, Bauer M, Pankratz MJ. Nutrient control of gene expression in Drosophila: microarray analysis of starvation and sugar-dependent response. EMBO J 2002; 21: 6162-6173. (Pubitemid 35415333)
19. Berry DL, Baehrecke EH. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 2007; 131: 1137-1148. (Pubitemid 350235023)
20. Saucedo LJ, Gao X, Chiarelli DA, Li L, Pan D, Edgar BA. Rheb promotes cell growth as a component of the insulin/TOR signalling network. Nat Cell Biol 2003; 5: 566-571. (Pubitemid 36781092)
21. Illmensee K, Mahowald AP. Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc Natl Acad Sci USA 1974; 71: 1016-1020.
22. Chang YY, Neufeld TP. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol Biol Cell 2009; 20: 2004-2014.
23. Bass BP, Tanner EA, Mateos San Martin D, Blute T, Kinser RD, Dolph PJ et al. Cell-autonomous requirement for DNaseII in nonapoptotic cell death. Cell Death Differ 2009; 16: 1362-1371.
24. Erdelyi M, Szabad J. Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. I. Mutations on the third chromosome. Genetics 1989; 122: 111-127.
25. Beadle GW, Ephrussi B. Ovary transplants in Drosophila melanogaster: meiosis and crossing-over in superfemales. Proc Natl Acad Sci USA 1937; 23: 356-360.
26. Wieschaus E, Marsh JL, Gehring W. fs(1)K10, a germline-dependent female sterile mutation causing abnormal chorion morphology in Drosophila melanogaster. Wilhelm Roux's Arch Dev Biol 1978; 184: 75-82. (Pubitemid 8270998)
27. Poulton JS, Deng WM. Cell-cell communication and axis specification in the Drosophila oocyte. Dev Biol 2007; 311: 1-10. (Pubitemid 47588234)
28. Cavaliere V, Donati A, Hsouna A, Hsu T, Gargiulo G. dAkt kinase controls follicle cell size during Drosophila oogenesis. Dev Dyn 2005; 232: 845-854. (Pubitemid 40315302)
29. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, Hafen E et al. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 2001; 292: 104-106. (Pubitemid 32289136)
30. Flatt T, Min KJ, D'Alterio C, Villa-Cuesta E, Cumbers J, Lehmann R et al. Drosophila germ-line modulation of insulin signaling and lifespan. Proc Natl Acad Sci USA 2008; 105: 6368-6373. (Pubitemid 351758352)
31. Dunaif A, Thomas A. Current concepts in the polycystic ovary syndrome. Annu Rev Med 2001; 52: 401-419. (Pubitemid 32195332)
32. Avellaira C, Villavicencio A, Bacallao K, Gabler F, Wells P, Romero C et al. Expression of molecules associated with tissue homeostasis in secretory endometria from untreated women with polycystic ovary syndrome. Hum Reprod 2006; 21: 3116-3121. (Pubitemid 44811612)
33. Buszczak M, Cooley L. Eggs to die for: cell death during Drosophila oogenesis. Cell Death Differ 2000; 7: 1071-1074.
34. Terashima J, Bownes M. Translating available food into the number of eggs laid by Drosophila melanogaster. Genetics 2004; 167: 1711-1719. (Pubitemid 39265908)
35. Berg CA. The Drosophila shell game: patterning genes and morphological change. Trends Genet 2005; 21: 346-355. (Pubitemid 40726392)
36. Nezis IP, Stravopodis DJ, Margaritis LH, Papassideri IS. Programmed cell death of follicular epithelium during the late developmental stages of oogenesis in the fruit flies Bactrocera oleae and Ceratitis capitata (Diptera, Tephritidae) is mediated by autophagy. Dev Growth Differ 2006; 48: 189-198.
37. Thumm M, Kadowaki T. The loss of Drosophila APG4/AUT2 function modifies the phenotypes of cut and Notch signaling pathway mutants. Mol Genet Genomics 2001; 266: 657-663. (Pubitemid 33145129)
38. Erdelyi M, Michon AM, Guichet A, Glotzer JB, Ephrussi A. Requirement for Drosophila cytoplasmic tropomyosin in oskar mRNA localization. Nature 1995; 377: 524-527.
39. Galanopoulos VK, Orr W, Szabad J, Kafatos FC. Genetic analysis of chorion formation in Drosophila melanogaster: I. The effects of one somatic-specific and seven germ-line-specific mutations. Dev Genet 1989; 10: 87-97.