Autophagy is used as a survival program in unfertilized sea urchin eggs that are destined to die by apoptosis after inactivation of MAPK1/3 (ERK2/1)

Autophagy

Volumn 9, Issue 10, 2013, Pages 1527-1539

  Houel Renault, Ludivine ^a   Philippe, Laetitia ^a   Piquemal, Marion ^a   Ciapa, Brigitte ^a  

^a CNRS   (France)

Author keywords

Apoptosis; Autophagy; Bafilomycin A1; Calcium; Cell cycle; Egg; Leupeptin; MAP kinase; MAPK1 3; Mitosis; Oocyte; PtdIns 3 kinase; Sea urchin

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BAFILOMYCIN A1; CALCIUM; CASPASE 3; CYCLIN DEPENDENT KINASE; LEUPEPTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 13; MITOGEN ACTIVATED PROTEIN KINASE 3; PEPSTATIN; PHOSPHATIDYLINOSITOL 3 KINASE; ROSCOVITINE; WORTMANNIN;

APOPTOSIS; ARTICLE; AUTOPHAGY; CALCIUM TRANSPORT; CELL CYCLE; CELL CYCLE ARREST; CELL ORGANELLE; CONTROLLED STUDY; DOWN REGULATION; ELECTRON MICROSCOPY; ENZYME INACTIVATION; ENZYME INHIBITION; FERTILIZATION; IMMUNOFLUORESCENCE; IMMUNOGOLD STAINING; MITOSIS; NONHUMAN; OOCYTE MATURATION; SEA URCHIN; SURVIVAL; WESTERN BLOTTING; ANIMAL; ENZYME ACTIVATION; METABOLISM; OOCYTE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ECHINOIDEA;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL CYCLE; CYCLIN-DEPENDENT KINASES; ENZYME ACTIVATION; FERTILIZATION; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOSIS; OVUM; PHOSPHATIDYLINOSITOL 3-KINASES; SEA URCHINS;

EID: 84885629177     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.25712     Document Type: Article

References (58)

1. Gordo AC, Rodrigues P, Kurokawa M, Jellerette T, Exley GE, Warner C, Fissore R. Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol Reprod 2002; 66:1828-37; PMID:12021069; http://dx.doi.org/10.1095/biolreprod66.6.1828
2. Fissore RA, Kurokawa M, Knott J, Zhang M, Smyth J. Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 2002; 124:745-54; PMID:12530912; http://dx.doi.org/10.1530/rep.0.1240745
3. Greenwood J, Gautier J. From oogenesis through gastrulation: developmental regulation of apoptosis. Semin Cell Dev Biol 2005; 16:215-24; PMID:15797832; http://dx.doi.org/10.1016/j.semcdb.2004.12.002
4. Lera S, Pellegrini D. Evaluation of the fertilization capability of Paracentrotus lividus sea urchin storaged gametes by the exposure to different aqueous matrices. Environ Monit Assess 2006; 119:1-13; PMID:16767501; http://dx.doi.org/10.1007/s10661-005-9000-0
5. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, Baehrecke EH, Bazan NG, Blagosklonny MV, Blomgren K, Borner C, et al. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 2009; 16:1093-107; PMID:19373242; http://dx.doi.org/10.1038/ cdd.2009.44
6. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, et al.; Nomenclature Committee on Cell Death 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009; 16:3-11; PMID:18846107; http://dx.doi.org/10.1038/cdd.2008.150
7. De Felici M, Lobascio AM, Klinger FG. Cell death in fetal oocytes: many players for multiple pathways. Autophagy 2008; 4:240-2; PMID:18094606
8. Oita E, Harada K, Chiba K. Degradation of polyubiquitinated cyclin B is blocked by the MAPK pathway at the metaphase I arrest in starfish oocytes. J Biol Chem 2004; 279:18633-40; PMID:14985367; http://dx.doi.org/10.1074/jbc. M311122200
9. Sasaki K, Chiba K. Fertilization blocks apoptosis of starfish eggs by inactivation of the MAP kinase pathway. Dev Biol 2001; 237:18-28; PMID:11518502; http://dx.doi.org/10.1006/dbio.2001.0337
10. Voronina E, Wessel GM. Apoptosis in sea urchin oocytes, eggs, and early embryos. Mol Reprod Dev 2001; 60:553-61; PMID:11746966; http://dx.doi.org/10. 1002/mrd.1120
11. Nezis IP, Papassideri I. Monitoring autophagy in insect eggs. Methods Enzymol 2008; 451:669-83; PMID:19185745; http://dx.doi.org/10.1016/S0076- 6879(08)03237-0
12. Chiarelli R, Agnello M, Roccheri MC. Sea urchin embryos as a model system for studying autophagy induced by cadmium stress. Autophagy 2011; 7:1028-34; PMID:21628995; http://dx.doi.org/10.4161/auto.7.9.16450
13. Shaul YD, Seger R. The MEK/ERK cascade: from signaling specificity to diverse functions. Biochim Biophys Acta 2007; 1773:1213-26; PMID:17112607; http://dx.doi.org/10.1016/j.bbamcr.2006.10.005
14. Kishimoto T. Cell-cycle control during meiotic maturation. Curr Opin Cell Biol 2003; 15:654-63; PMID:14644189; http://dx.doi.org/10.1016/j.ceb.2003.10. 010
15. Hara M, Mori M, Wada T, Tachibana K, Kishimoto T. Start of the embryonic cell cycle is dually locked in unfertilized starfish eggs. Development 2009; 136:1687-96; PMID:19369392; http://dx.doi.org/10.1242/dev.035261
16. Kondoh E, Tachibana K, Deguchi R. Intracellular Ca2+ increase induces post-fertilization events via MAP kinase dephosphorylation in eggs of the hydrozoan jellyfish Cladonema pacificum. Dev Biol 2006; 293:228-41; PMID:16530749; http://dx.doi.org/10.1016/j.ydbio.2006.02.005
17. Amiel A, Leclère L, Robert L, Chevalier S, Houliston E. Conserved functions for Mos in eumetazoan oocyte maturation revealed by studies in a cnidarian. Curr Biol 2009; 19:305-11; PMID:19230670; http://dx.doi.org/10.1016/ j.cub.2008.12.054
18. Dumollard R, Levasseur M, Hebras C, Huitorel P, Carroll M, Chambon JP, McDougall A. Mos limits the number of meiotic divisions in urochordate eggs. Development 2011; 138:885-95; PMID:21303846; http://dx.doi.org/10.1242/dev. 057133
19. Wu JQ, Kornbluth S. Across the meiotic divide -CSF activity in the post-Emi2/XErp1 era. J Cell Sci 2008; 121:3509-14; PMID:18946022; http://dx.doi.org/10.1242/jcs.036855
20. Tachibana K, Tanaka D, Isobe T, Kishimoto T. c-Mos forces the mitotic cell cycle to undergo meiosis II to produce haploid gametes. Proc Natl Acad Sci U S A 2000; 97:14301-6; PMID:11121036; http://dx.doi.org/10.1073/pnas.97.26. 14301
21. Sasaki K, Chiba K. Induction of apoptosis in starfish eggs requires spontaneous inactivation of MAPK (extracellular signal-regulated kinase) followed by activation of p38MAPK. Mol Biol Cell 2004; 15:1387-96; PMID:14699071; http://dx.doi.org/10.1091/mbc.E03-06-0367
22. Chiri S, De Nadai C, Ciapa B. Evidence for MAP kinase activation during mitotic division. J Cell Sci 1998; 111:2519-27; PMID:9701551
23. Zhang WL, Huitorel P, Glass R, Fernandez-Serra M, Arnone MI, Chiri S, Picard A, Ciapa B. A MAPK pathway is involved in the control of mitosis after fertilization of the sea urchin egg. Dev Biol 2005; 282:192-206; PMID:15936340; http://dx.doi.org/10.1016/j.ydbio.2005.03.008
24. Philipova R, Kisielewska J, Lu P, Larman M, Huang JY, Whitaker M. ERK1 activation is required for S-phase onset and cell cycle progression after fertilization in sea urchin embryos. Development 2005; 132:579-89; PMID:15634691; http://dx.doi.org/10.1242/dev.01607
25. Zhang WL, Huitorel P, Geneviere AM, Chiri S, Ciapa B. Inactivation of MAPK in mature oocytes triggers progression into mitosis via a Ca2+ -dependent pathway but without completion of S phase. J Cell Sci 2006; 119:3491-501; PMID:16912079; http://dx.doi.org/10.1242/jcs.03082
26. Whitaker M. Calcium microdomains and cell cycle control. Cell Calcium 2006; 40:585-92; PMID:17045645; http://dx.doi.org/10.1016/j.ceca.2006.08.018
27. Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R. Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene 2008; 27:6407-18; PMID:18955969; http://dx.doi.org/10.1038/onc.2008.308
28. Gavet O, Pines J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev Cell 2010; 18:533-43; PMID:20412769; http://dx.doi.org/10. 1016/j.devcel.2010.02.013
29. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, Inagaki N, Inagaki M, Delcros JG, Moulinoux JP. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 1997; 243:527-36; PMID:9030781; http://dx.doi.org/10.1111/j. 1432-1033.1997.t01-2-00527.x
30. Philipova R, Larman MG, Leckie CP, Harrison PK, Groigno L, Whitaker M. Inhibiting MAP kinase activity prevents calcium transients and mitosis entry in early sea urchin embryos. J Biol Chem 2005; 280:24957-67; PMID:15843380; http://dx.doi.org/10.1074/jbc.M414437200
31. Wilding M, Wright EM, Patel R, Ellis-Davies G, Whitaker M. Local perinuclear calcium signals associated with mitosis-entry in early sea urchin embryos. J Cell Biol 1996; 135:191-9; PMID:8858173; http://dx.doi.org/10.1083/ jcb.135.1.191
32. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-75; PMID:18188003
33. Kimura S, Fujita N, Noda T, Yoshimori T. Monitoring autophagy in mammalian cultured cells through the dynamics of LC3. Methods Enzymol 2009; 452:1-12; PMID:19200872; http://dx.doi.org/10.1016/S0076-6879(08)03601-X
34. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. Role of autophagy in temozolomideinduced cytotoxicity for malignant glioma cells. Cell Death Differ 2004; 11:448-57; PMID:14713959; http://dx.doi.org/10.1038/sj.cdd. 4401359
35. Zakeri Z, Melendez A, Lockshin RA. Detection of autophagy in cell death. Methods Enzymol 2008; 442:289-306; PMID:18662576; http://dx.doi.org/10.1016/ S0076-6879(08)01415-8
36. Ylä-Anttila P, Vihinen H, Jokitalo E, Eskelinen E-L. Monitoring autophagy by electron microscopy in Mammalian cells. Methods Enzymol 2009; 452:143-64; PMID:19200881; http://dx.doi.org/10.1016/S0076-6879(08)03610-0
37. Haspel J, Shaik RS, Ifedigbo E, Nakahira K, Dolinay T, Englert JA, Choi AM. Characterization of macroautophagic flux in vivo using a leupeptin-based assay. Autophagy 2011; 7:629-42; PMID:21460622; http://dx.doi.org/10.4161/auto. 7.6.15100
38. Klionsky DJ, Elazar Z, Seglen PO, Rubinsztein DC. Does bafilomycin A1 block the fusion of autophagosomes with lysosomes? Autophagy 2008; 4:849-950; PMID:18758232
39. Backer JM. The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem J 2008; 410:1-17; PMID:18215151; http://dx.doi.org/10.1042/ BJ20071427
40. Wu YT, Tan HL, Shui G, Bauvy C, Huang Q, Wenk MR, Ong CN, Codogno P, Shen HM. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem 2010; 285:10850-61; PMID:20123989; http://dx.doi.org/10.1074/jbc.M109. 080796
41. Robertson AJ, Croce J, Carbonneau S, Voronina E, Miranda E, McClay DR, Coffman JA. The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus. Dev Biol 2006; 300:321-34; PMID:17010332; http://dx.doi.org/10.1016/ j.ydbio.2006.08.053
42. Rankin S, Kirschner MW. The surface contraction waves of Xenopus eggs reflect the metachronous cell-cycle state of the cytoplasm. Curr Biol 1997; 7:451-4; PMID:9197242; http://dx.doi.org/10.1016/S0960-9822(06)00192-8
43. Beckhelling C, Penny C, Clyde S, Ford C. Timing of calcium and protein synthesis requirements for the first mitotic cell cycle in fertilised Xenopus eggs. J Cell Sci 1999; 112:3975-84; PMID:10547358
44. Mebratu Y, Tesfaigzi Y. How ERK1/2 activation controls cell proliferation and cell death: Is subcellular localization the answer? Cell Cycle 2009; 8:1168-75; PMID:19282669; http://dx.doi.org/10.4161/cc.8.8.8147
45. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ 2008; 15:1153-62; PMID:18404154; http://dx.doi.org/10.1038/cdd.2008.47
46. Giacomello M, Drago I, Pizzo P, Pozzan T. Mitochondrial Ca2+ as a key regulator of cell life and death. Cell Death Differ 2007; 14:1267-74; PMID:17431419; http://dx.doi.org/10.1038/sj.cdd.4402147
47. Chakrabarti L, Eng J, Ivanov N, Garden GA, La Spada AR. Autophagy activation and enhanced mitophagy characterize the Purkinje cells of pcd mice prior to neuronal death. Mol Brain 2009; 2:24; PMID:19640278; http://dx.doi.org/10.1186/1756-6606-2-24
48. Rodríguez-Muela N, Germain F, Mariño G, Fitze PS, Boya P. Autophagy promotes survival of retinal ganglion cells after optic nerve axotomy in mice. Cell Death Differ 2012; 19:162-9; PMID:21701497; http://dx.doi.org/10. 1038/cdd.2011.88
49. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93; PMID:19653858; http://dx.doi.org/10. 1146/annurev-genet-102808-114910
50. Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 2010; 22:124-31; PMID:20034776; http://dx.doi.org/10.1016/j.ceb.2009.11.014
51. Zhdanov AV, Dmitriev RI, Papkovsky DB. Bafilomycin A1 activates respiration of neuronal cells via uncoupling associated with flickering depolarization of mitochondria. Cell Mol Life Sci 2011; 68:903-17; PMID:20820851; http://dx.doi.org/10.1007/s00018-010-0502-8
52. Morgan AJ. Sea urchin eggs in the acid reign. Cell Calcium 2011; 50:147-56; PMID:21251713; http://dx.doi.org/10.1016/j.ceca.2010.12.007
53. Yin XM. Bid, a BH3-only multi-functional molecule, is at the cross road of life and death. Gene 2006; 369:7-19; PMID:16446060; http://dx.doi.org/10. 1016/j.gene.2005.10.038
54. Degterev A, Yuan J. Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 2008; 9:378-90; PMID:18414491; http://dx.doi.org/10.1038/ nrm2393
55. Duronio V. The life of a cell: apoptosis regulation by the PI3K/PKB pathway. Biochem J 2008; 415:333-44; PMID:18842113; http://dx.doi.org/10.1042/ BJ20081056
56. Yang Y, Herrup K. Cell division in the CNS: protective response or lethal event in post-mitotic neurons? Biochim Biophys Acta 2007; 1772:457-66; PMID:17158035; http://dx.doi.org/10.1016/j.bbadis.2006.10.002
57. Dumollard R, Hammar K, Porterfield M, Smith PJ, Cibert C, Rouvière C, Sardet C. Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion. Development 2003; 130:683-92; PMID:12505999; http://dx.doi.org/10.1242/dev.00296
58. Prodon F, Chenevert J, Hébras C, Dumollard R, Faure E, Gonzalez-Garcia J, Nishida H, Sardet C, McDougall A. Dual mechanism controls asymmetric spindle position in ascidian germ cell precursors. Development 2010; 137:2011-21; PMID:20463032; http://dx.doi.org/10.1242/dev.047845