Autophagy and apoptosis interplay during follicular atresia in fish ovary: A morphological and immunocytochemical study

Cell and Tissue Research

Volumn 347, Issue 2, 2012, Pages 467-478

  Morais, R D V S ^a   Thome R G ^a   Lemos, F S ^a   Bazzoli, N ^b   Rizzo, E ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b PONTIFICAL CATHOLIC UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Bax; Bcl 2; Beclin 1; Caspase 3; Cathepsin D; Fish; Follicular atresia

Indexed keywords

ACTIN; BECLIN 1; CASPASE 3; CATHEPSIN D; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; FRESHWATER FISH; HUMAN; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOLOCALIZATION; NICK END LABELING; NONHUMAN; OVARY FOLLICLE ATRESIA; OVARY FUNCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STRUCTURE ANALYSIS;

ANIMALS; APOPTOSIS; AUTOPHAGY; DISEASE MODELS, ANIMAL; FEMALE; FISH PROTEINS; FISHES; FOLLICULAR ATRESIA; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; OVARIAN FOLLICLE; OVARY;

RADIATA;

EID: 84859436160     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-012-1327-6     Document Type: Article

References (50)

1. Adams JM, Cory S (2001) Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci 26:61-66 (Pubitemid 32124712)
2. Andreu-Vieyra CV, Habibi HR (2000) Factors controlling ovarian apoptosis. Can J Physiol Pharmacol 78:1003-1012 (Pubitemid 32109431)
3. Apel A, Zentgraf H, Buchler MW, Herr I (2009) Autophagy - a double-edged sword in oncology. Int J Cancer 125:991-995
4. Arantes FP, Santos HB, Rizzo E, Sato Y, Bazzoli N (2011) Influence of water temperature on induced reproduction by hypophysation, sex steroids concentrations and final oocyte maturation of the "curimatapacu" Prochilodus argenteus (Pisces: Prochilodontidae). Gen Comp Endocrinol 172:400-408
5. Assunção Guimarães C, Linden R (2004) Programmed cell deaths. Apoptosis and alternative deathstyles. Eur J Biochem 271:1638-1650
6. a ed. PUC Minas, Belo Horizonte, pp 291-306
7. Borner C (2003) The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol 39:615-647
8. Burton TR, Gibson SB (2009) The role of Bcl-2 family member BNIP3 in cell death and disease: NIPping at the heels of cell death. Cell Death Differ 16:515-523
9. Cao Y, Klionsky DJ (2007) Physiological functions of Atg6/Beclin-1: a unique autophagy-related protein. Cell Res 17:839-849 (Pubitemid 47585112)
10. Carmona-Gutierrez D, Bauer MA, Ring J, Knauer H, Eisenberg T, Buttner S, Ruckenstuhl C, Reisenbichler A, Magnes C, Rechberger GN, Birner-Gruenberger R, Jungwirth H, Frohlich KU, Sinner F, Kroemer G, Madeo F (2011) The propeptide of yeast cathepsin-D inhibits programmed necrosis. Cell Death Dis 2:e161
11. Cho DH, Jo YK, Hwang JJ, Lee YM, Roh SA, Kim JC (2009) Caspase-mediated cleavage of ATG6/Beclin-1 links apoptosis to autophagy in HeLa cells. Cancer Lett 274:95-100
12. Ciechomska IA, Goemans GC, Skepper JN, Tolkovsky AM(2009a) Bcl-2 complexed with Beclin-1 maintains full anti-apoptotic function. Oncogene 28:2128-2141
13. Ciechomska IA, Goemans CG, Tolkovsky AM (2009b) Why doesn't Beclin-1, a BH3-only protein, suppress the anti-apoptotic function of Bcl-2? Autophagy 5:880-881
14. Degterev A, Yuan J (2008) Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 9:378-390 (Pubitemid 351574200)
15. Djavaheri-Mergny M, Maiuri MC, Kroemer G (2010) Cross talk between apoptosis and autophagy by caspase-mediated cleavage of Beclin-1. Oncogene 29:1717-1719
16. Fimia GM, Piacentini M (2010) Regulation of autophagy in mammals and its interplay with apoptosis. Cell Mol Life Sci 67:1581-1588
17. 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 Tissue Res 331:509-517
18. Hasui K, Wang J, Jia X, Tanaka M, Nagai T, Matsuyama T, Eizuru Y (2011) Enhanced autophagy and reduced expression of cathepsin-D are related to autophagic cell death in Epstein-Barr virus-associated nasal natural killer/T-cell lymphomas: an immunohistochemical analysis of beclin-1, LC3, mitochondria (AE-1), and cathepsin-D in nasopharyngeal lymphomas. Acta Histochem Cytochem 44:119-131
19. Hussein MR (2005) Apoptosis in the ovary: molecular mechanisms. Hum Reprod Update 11:162-177
20. Jahreiss L, Menzies FM, Rubinsztein DC (2008) The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic 9:574-587 (Pubitemid 351351616)
21. Kang R, Zeh HJ, Lotze MT, Tang D (2011) The Beclin-1 network regulates autophagy and apoptosis. Cell Death Differ 18:571-580
22. Kratz E, Eimon PM, Mukhyala K, Stern H, Zha J, Strasser A, Hart R, Ashkenazi A (2006) Functional characterization of the Bcl-2 gene family in the zebrafish. Cell Death Differ 13:1631-1640 (Pubitemid 44390851)
23. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nunez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16:3-11
24. Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, Vergne I, Deretic V, Feng P, Akazawa C, Jung JU (2008) Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 10:776-787 (Pubitemid 351927707)
25. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8:741-752 (Pubitemid 47312826)
26. Maiuri MC, Criollo A, Kroemer G (2010) Crosstalk between apoptosis and autophagy within the Beclin 1 interactome. EMBO J 29:515-516
27. Miranda AC, Bazzoli N, Rizzo E, Sato Y (1999) Ovarian follicular atresia in two teleost species: a histological and ultrastructural study. Tissue Cell 31:480-488 (Pubitemid 29531290)
28. Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451:1069-1075 (Pubitemid 351317450)
29. Moreau K, Luo S, Rubinsztein DC (2010) Cytoprotective roles for autophagy. Curr Opin Cell Biol 22:206-211
30. Mpakou VE, Velentzas AD, Velentzas PD, Margaritis LH, Stravopodis DJ, Papassideri IS (2011) Programmed cell death of the ovarian nurse cells during oogenesis of the ladybird beetle Adalia bipunctata (Coleoptera: Coccinellidae). Dev Growth Differ 53:804-815
31. Nahum R, Beyth Y, Chun SY, Hsueh AJ, Tsafriri A (1996) Early onset of deoxyribonucleic acid fragmentation during atresia of preovulatory ovarian follicles in rats. Biol Reprod 55:1075-1080 (Pubitemid 26346543)
32. Ndozangue-Touriguine O, Hamelin J, Breard J (2008) Cytoskeleton and apoptosis. Biochem Pharmacol 76:11-18
33. Nezis IP, Stravopodis DJ, Margaritis LH, Papassideri IS (2006) Autophagy is required for the degeneration of the ovarian follicular epithelium in higher Diptera. Autophagy 2:297-298 (Pubitemid 44342373)
34. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B (2005) Bcl-2 antiapoptotic proteins inhibit Beclin-1-dependent autophagy. Cell 122:927-939 (Pubitemid 41345209)
35. Reggiori F, Monastyrska I, Shintani T, Klionsky DJ (2005) The actin cytoskeleton is required for selective types of autophagy, but not nonspecific autophagy, in the yeast Saccharomyces cerevisiae. Mol Biol Cell 16:5843-5856 (Pubitemid 41752231)
36. Rizzo E, Bazzoli N (1995) Follicular atresia in curimatá-pioa Prochilodus affinis Reinhardt 1874 (Pisces, Characiformes). Rev Bras Bio 55:697-703
37. Saidapur SK (1978) Follicular atresia in the ovaries of nonmammalian vertebrates. Int Rev Cytol 54:225-244
38. Santos HB, Rizzo E, Bazzoli N, Sato Y, Moro L (2005) Ovarian regression and apoptosis in the South American teleost Leporinus taeniatus Lütken (Characiformes, Anostomidae) from the São Francisco Basin. J Fish Biol 67:1446-1459 (Pubitemid 44922283)
39. Santos HB, Thome 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
40. Sasson R, Amsterdam A (2002) Stimulation of apoptosis in human granulosa cells from in vitro fertilization patients and its prevention by dexamethasone: involvement of cell contact and bcl-2 expression. J Clin Endocrinol Metab 87:3441-3451 (Pubitemid 34816402)
41. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB, Tsujimoto Y (2004) Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6:1221-1228 (Pubitemid 39625121)
42. Thomé RG, Santos HB, Arantes FP, Domingos FF, Bazzoli N, Rizzo E (2009) Dual roles for autophagy during follicular atresia in fish ovary. Autophagy 5:117-119
43. Thomé R, Santos HB, Sato Y, Rizzo E, Bazzoli N (2010) Distribution of laminin β2, collagen type IV, fibronectin and MMP-9 in ovaries of the teleost fish. J Mol Histol 41:215-224
44. Uchiyama Y (2001) Autophagic cell death and its execution by lysosomal cathepsins. Arch Histol Cytol 64:233-246
45. Velentzas AD, Nezis IP, Stravopodis DJ, Papassideri IS, Margaritis LH (2007a) Apoptosis and autophagy function cooperatively for the efficacious execution of programmed nurse cell death during Drosophila virilis oogenesis. Autophagy 3:130-132 (Pubitemid 46449102)
46. Velentzas AD, Nezis IP, Stravopodis DJ, Papassideri IS, Margaritis LH (2007b) Mechanisms of programmed cell death during oogenesis in Drosophila virilis. Cell Tissue Res 327:399-414 (Pubitemid 46011249)
47. Wirawan E, Vande Walle L, Kersse K, Cornelis S, Claerhout S, Vanoverberghe I, Roelandt R, De Rycke R, Verspurten J, Declercq W, Agostinis P, Vanden Berghe T, Lippens S, Vandenabeele P (2010) Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis 1:e18
48. Zaidi N, Maurer A, Nieke S, Kalbacher H (2008) Cathepsin-D: a cellular roadmap. Biochem Biophys Res Commun 376:5-9
49. Zhang T, Rawson DM, Tosti L, Carnevali O (2008) Cathepsin activities and membrane integrity of zebrafish (Danio rerio) oocytes after freezing to -196 degrees C using controlled slow cooling. Cryobiology 56:138-143
50. Zhou F, Yang Y, Xing D (2010) Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J 278:403-441