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Fish as model systems for the study of vertebrate apoptosis

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Abstract

Apoptosis is a process of pivotal importance for multi-cellular organisms and due to its implication in the development of cancer and degenerative disease it is intensively studied in humans and mammalian model systems. Invertebrate models of apoptosis have been well-studied, especially in C. elegans and D. melanogaster, but as these are evolutionarily distant from mammals the relevance of findings for human research is sometimes limited. Presently, a non-mammalian vertebrate model for studying apoptosis is missing. However, in the past few years an increasing number of studies on cell death in fish have been published and thus new model systems may emerge. This review aims at highlighting the most important of these findings, showing similarities and dissimilarities between fish and mammals, and will suggest topics for future research. In addition, the outstanding usefulness of fish as research models will be pointed out, hoping to spark future research on this exciting, often underrated group of vertebrates.

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References

  1. Taylor RC, Cullen SP, Martin SJ (2008) Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 9:231–241. doi:10.1038/nrm2312

    PubMed  CAS  Google Scholar 

  2. Horvitz HR (2003) Worms, life, and death (Nobel lecture). ChemBioChem 4:697–711. doi:10.1002/cbic.200300614

    PubMed  CAS  Google Scholar 

  3. Ribeiro PS, Kuranaga E, Tenev T, Leulier F, Miura M, Meier P (2007) DIAP2 functions as a mechanism-based regulator of drICE that contributes to the caspase activity threshold in living cells. J Cell Biol 179:1467–1480. doi:10.1083/jcb.200706027

    PubMed  CAS  Google Scholar 

  4. Hay BA, Guo M (2006) Caspase-dependent cell death in Drosophila. Annu Rev Cell Dev Biol 22:623–650. doi:10.1146/annurev.cellbio.21.012804.093845

    PubMed  CAS  Google Scholar 

  5. Lettre G, Hengartner MO (2006) Developmental apoptosis in C. elegans: a complex CEDnario. Nat Rev Mol Cell Biol 7:97–108. doi:10.1038/nrm1836

    PubMed  CAS  Google Scholar 

  6. Brancolini C, Lazarevic D, Rodriguez J, Schneider C (1997) Dismantling cell-cell contacts during apoptosis is coupled to a caspase-dependent proteolytic cleavage of beta-catenin. J Cell Biol 139:759–771. doi:10.1083/jcb.139.3.759

    PubMed  CAS  Google Scholar 

  7. Gu Y, Sarnecki C, Aldape RA, Livingston DJ, Su MS (1995) Cleavage of poly (ADP-ribose) polymerase by interleukin-1 beta converting enzyme and its homologs TX and Nedd-2. J Biol Chem 270:18715–18718. doi:10.1074/jbc.270.19.11238

    PubMed  CAS  Google Scholar 

  8. Liu X, Zou H, Slaughter C, Wang X (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89:175–184. doi:10.1016/S0092-8674(00)80197-X

    PubMed  CAS  Google Scholar 

  9. Letai AG (2008) Diagnosing and exploiting cancer’s addiction to blocks in apoptosis. Nat Rev Cancer 8:121–132. doi:10.1038/nrc2297

    PubMed  CAS  Google Scholar 

  10. Uren RT, Dewson G, Chen L, Coyne SC, Huang DC, Adams JM, Kluck RM (2007) Mitochondrial permeabilization relies on BH3 ligands engaging multiple prosurvival Bcl-2 relatives, not Bak. J Cell Biol 177:277–287. doi:10.1083/jcb.200606065

    PubMed  CAS  Google Scholar 

  11. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, Hsieh JJ, Cheng EH (2006) Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 8:1348–1358. doi:10.1038/ncb1499

    PubMed  CAS  Google Scholar 

  12. Bernardi P, Krauskopf A, Basso E, Petronilli V, Blachly-Dyson E, Di Lisa F, Forte MA (2006) The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J 273:2077–2099. doi:10.1111/j.1742-4658.2006.05213.x

    PubMed  CAS  Google Scholar 

  13. Leung AW, Halestrap AP (2008) Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore. Biochim Biophys Acta 1777:946–952. doi:10.1016/j.bbabio.2008.03.009

    PubMed  CAS  Google Scholar 

  14. Kim JS, He L, Lemasters JJ (2003) Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 304:463–470. doi:10.1016/S0006-291X(03)00618-1

    PubMed  CAS  Google Scholar 

  15. Barnhart BC, Alappat EC, Peter ME (2003) The CD95 type I/type II model. Semin Immunol 15:185–193. doi:10.1016/S1044-5323(03)00031-9

    PubMed  CAS  Google Scholar 

  16. Eimon PM, Kratz E, Varfolomeev E, Hymowitz SG, Stern H, Zha J, Ashkenazi A (2006) Delineation of the cell-extrinsic apoptosis pathway in the zebrafish. Cell Death Differ 13:1619–1630. doi:10.1038/sj.cdd.4402015

    PubMed  CAS  Google Scholar 

  17. Inohara N, Nunez G (2000) Genes with homology to mammalian apoptosis regulators identified in zebrafish. Cell Death Differ 7:509–510. doi:10.1038/sj.cdd.4400679

    PubMed  CAS  Google Scholar 

  18. 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. doi:10.1038/sj.cdd.4402016

    PubMed  CAS  Google Scholar 

  19. Bobe J, Goetz FW (2001) Molecular cloning and expression of a TNF receptor and two TNF ligands in the fish ovary. Comp Biochem Physiol B Biochem Mol Biol 129:475–481. doi:10.1016/S1096-4959(01)00353-0

    PubMed  CAS  Google Scholar 

  20. Long Q, Huang H, Shafizadeh E, Liu N, Lin S (2000) Stimulation of erythropoiesis by inhibiting a new hematopoietic death receptor in transgenic zebrafish. Nat Cell Biol 2:549–552. doi:10.1038/35019592

    PubMed  CAS  Google Scholar 

  21. Laing KJ, Wang T, Zou J, Holland J, Hong S, Bols N, Hirono I, Aoki T, Secombes CJ (2001) Cloning and expression analysis of rainbow trout Oncorhynchus mykiss tumour necrosis factor-alpha. Eur J Biochem 268:1315–1322. doi:10.1046/j.1432-1327.2001.01996.x

    PubMed  CAS  Google Scholar 

  22. Nascimento DS, Pereira PJ, Reis MI, do VA, Zou J, Silva MT, Secombes CJ, dos Santos NM (2007) Molecular cloning and expression analysis of sea bass (Dicentrarchus labrax L.) tumor necrosis factor-alpha (TNF-alpha). Fish Shellfish Immunol 23:701–710. doi:10.1016/j.fsi.2007.02.003

    PubMed  CAS  Google Scholar 

  23. Long S, Wilson M, Bengten E, Clem LW, Miller NW, Chinchar VG (2004) Identification and characterization of a FasL-like protein and cDNAs encoding the channel catfish death-inducing signaling complex. Immunogenetics 56:518–530. doi:10.1007/s00251-004-0701-2

    PubMed  CAS  Google Scholar 

  24. Kurobe T, Hirono I, Kondo H, Saito-Taki T, Aoki T (2007) Molecular cloning, characterization, expression and functional analysis of Japanese flounder Paralichthys olivaceus Fas ligand. Dev Comp Immunol 31:687–695. doi:10.1016/j.dci.2006.08.006

    PubMed  CAS  Google Scholar 

  25. Sakamaki K, Nozaki M, Kominami K, Satou Y (2007) The evolutionary conservation of the core components necessary for the extrinsic apoptotic signaling pathway, in Medaka fish. BMC Genomics 8:141. doi:10.1186/1471-2164-8-141

    PubMed  Google Scholar 

  26. Glenney GW, Wiens GD (2007) Early diversification of the TNF superfamily in teleosts: genomic characterization and expression analysis. J Immunol 178:7955–7973

    PubMed  CAS  Google Scholar 

  27. Jette CA, Flanagan AM, Ryan J, Pyati UJ, Carbonneau S, Stewart RA, Langenau DM, Look AT, Letai A (2008) BIM and other BCL-2 family proteins exhibit cross-species conservation of function between zebrafish and mammals. Cell Death Differ 15:1063–1072. doi:10.1038/cdd.2008.42

    PubMed  CAS  Google Scholar 

  28. Robinson-Rechavi M, Marchand O, Escriva H, Bardet PL, Zelus D, Hughes S, Laudet V (2001) Euteleost fish genomes are characterized by expansion of gene families. Genome Res 11:781–788. doi:10.1101/gr.165601

    PubMed  CAS  Google Scholar 

  29. Chen MC, Gong HY, Cheng CY, Wang JP, Hong JR, Wu JL (2000) Cloning and characterization of a novel nuclear Bcl-2 family protein, zfMcl-1a, in zebrafish embryo. Biochem Biophys Res Commun 279:725–731. doi:10.1006/bbrc.2000.3977

    PubMed  CAS  Google Scholar 

  30. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9:47–59. doi:10.1038/nrm2308

    PubMed  CAS  Google Scholar 

  31. Valentijn AJ, Upton JP, Bates N, Gilmore AP (2008) Bax targeting to mitochondria occurs via both tail anchor-dependent and -independent mechanisms. Cell Death Differ 15:1243–1254. doi:10.1038/cdd.2008.39

    PubMed  CAS  Google Scholar 

  32. Coultas L, Huang DC, Adams JM, Strasser A (2002) Pro-apoptotic BH3-only Bcl-2 family members in vertebrate model organisms suitable for genetic experimentation. Cell Death Differ 9:1163–1166. doi:10.1038/sj.cdd.4401096

    PubMed  CAS  Google Scholar 

  33. Puthalakath H, Villunger A, O’Reilly LA, Beaumont JG, Coultas L, Cheney RE, Huang DC, Strasser A (2001) Bmf: a proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science 293:1829–1832. doi:10.1126/science.1062257

    PubMed  CAS  Google Scholar 

  34. Mok CL, Gil-Gomez G, Williams O, Coles M, Taga S, Tolaini M, Norton T, Kioussis D, Brady HJ (1999) Bad can act as a key regulator of T cell apoptosis and T cell development. J Exp Med 189:575–586. doi:10.1084/jem.189.3.575

    PubMed  CAS  Google Scholar 

  35. Hsieh YC, Chang MS, Chen JY, Yen JJ, Lu IC, Chou CM, Huang CJ (2003) Cloning of zebrafish BAD, a BH3-only proapoptotic protein, whose overexpression leads to apoptosis in COS-1 cells and zebrafish embryos. Biochem Biophys Res Commun 304:667–675. doi:10.1016/S0006-291X(03)00646-6

    PubMed  CAS  Google Scholar 

  36. Her GM, Cheng CH, Hong JR, Sundaram GS, Wu JL (2006) Imbalance in liver homeostasis leading to hyperplasia by overexpressing either one of the Bcl-2-related genes, zfBLP1 and zfMcl-1a. Dev Dyn 235:515–523. doi:10.1002/dvdy.20624

    PubMed  CAS  Google Scholar 

  37. Langenau DM, Jette C, Berghmans S, Palomero T, Kanki JP, Kutok JL, Look AT (2005) Suppression of apoptosis by bcl-2 overexpression in lymphoid cells of transgenic zebrafish. Blood 105:3278–3285. doi:10.1182/blood-2004-08-3073

    PubMed  CAS  Google Scholar 

  38. Chen J, Jette C, Kanki JP, Aster JC, Look AT, Griffin JD (2007) NOTCH1-induced T-cell leukemia in transgenic zebrafish. Leukemia 21:462–471. doi:10.1038/sj.leu.2404546

    PubMed  Google Scholar 

  39. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481–490. doi:10.1016/S0092-8674(00)81589-5

    PubMed  CAS  Google Scholar 

  40. Werner AB, Tait SW, de Vries E, Eldering E, Borst J (2004) Requirement for aspartate-cleaved bid in apoptosis signaling by DNA-damaging anti-cancer regimens. J Biol Chem 279:28771–28780. doi:10.1074/jbc.M400268200

    PubMed  CAS  Google Scholar 

  41. Kim SH, Ricci MS, El Deiry WS (2008) Mcl-1: a gateway to TRAIL sensitization. Cancer Res 68:2062–2064. doi:10.1158/0008-5472.CAN-07-6278

    PubMed  CAS  Google Scholar 

  42. Kroemer G, Martin SJ (2005) Caspase-independent cell death. Nat Med 11:725–730. doi:10.1038/nm1263

    PubMed  Google Scholar 

  43. Takle H, Andersen O (2007) Caspases and apoptosis in fish. J Fish Biol 71:326–349. doi:10.1111/j.1095-8649.2007.01665.x

    CAS  Google Scholar 

  44. Takle H, McLeod A, Andersen O (2006) Cloning and characterization of the executioner caspases 3, 6, 7 and Hsp70 in hyperthermic Atlantic salmon (Salmo salar) embryos. Comp Biochem Physiol B Biochem Mol Biol 144:188–198. doi:10.1016/j.cbpb.2006.02.006

    PubMed  Google Scholar 

  45. Lamkanfi M, Festjens N, Declercq W, Vanden Berghe T, Vandenabeele P (2007) Caspases in cell survival, proliferation and differentiation. Cell Death Differ 14:44–55. doi:10.1038/sj.cdd.4402047

    PubMed  CAS  Google Scholar 

  46. Sakata S, Yan Y, Satou Y, Momoi A, Ngo-Hazelett P, Nozaki M, Furutani-Seiki M, Postlethwait JH, Yonehara S, Sakamaki K (2007) Conserved function of caspase-8 in apoptosis during bony fish evolution. Gene 396:134–148. doi:10.1016/j.gene.2007.03.010

    PubMed  CAS  Google Scholar 

  47. Yabu T, Kishi S, Okazaki T, Yamashita M (2001) Characterization of zebrafish caspase-3 and induction of apoptosis through ceramide generation in fish fathead minnow tailbud cells and zebrafish embryo. Biochem J 360:39–47. doi:10.1042/0264-6021:3600039

    PubMed  CAS  Google Scholar 

  48. Reis MI, Nascimento DS, do VA, Silva MT, dos Santos NM (2007) Molecular cloning and characterisation of sea bass (Dicentrarchus labrax L.) caspase-3 gene. Mol Immunol 44:774–783. doi:10.1016/j.molimm.2006.04.028

    PubMed  CAS  Google Scholar 

  49. Lee KC, Goh WL, Xu M, Kua N, Lunny D, Wong JS, Coomber D, Vojtesek B, Lane EB, Lane DP (2008) Detection of the p53 response in zebrafish embryos using new monoclonal antibodies. Oncogene 27:629–640. doi:10.1038/sj.onc.1210695

    PubMed  CAS  Google Scholar 

  50. Sidi S, Sanda T, Kennedy RD, Hagen AT, Jette CA, Hoffmans R, Pascual J, Imamura S, Kishi S, Amatruda JF, Kanki JP, Green DR, D’Andrea AA, Look AT (2008) Chk1 suppresses a caspase-2 apoptotic response to DNA damage that bypasses p53, Bcl-2, and caspase-3. Cell 133:864–877. doi:10.1016/j.cell.2008.03.037

    PubMed  CAS  Google Scholar 

  51. Lu G, Mak YT, Wai SM, Kwong WH, Fang M, James A, Randall D, Yew DT (2005) Hypoxia-induced differential apoptosis in the central nervous system of the sturgeon (Acipenser schrenckii). Microsc Res Tech 68:258–263. doi:10.1002/jemt.20243

    PubMed  Google Scholar 

  52. Yamashita M, Mizusawa N, Hojo M, Yabu T (2008) Extensive apoptosis and abnormal morphogenesis in pro-caspase-3 transgenic zebrafish during development. J Exp Biol 211:1874–1881. doi:10.1242/jeb.012690

    PubMed  CAS  Google Scholar 

  53. Valencia CA, Bailey C, Liu R (2007) Novel zebrafish caspase-3 substrates. Biochem Biophys Res Commun 361:311–316. doi:10.1016/j.bbrc.2007.06.173

    PubMed  CAS  Google Scholar 

  54. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, Flavell RA (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384:368–372. doi:10.1038/384368a0

    PubMed  CAS  Google Scholar 

  55. Chauvier D, Ankri S, Charriaut-Marlangue C, Casimir R, Jacotot E (2007) Broad-spectrum caspase inhibitors: from myth to reality? Cell Death Differ 14:387–391. doi:10.1038/sj.cdd.4402044

    PubMed  CAS  Google Scholar 

  56. McStay GP, Salvesen GS, Green DR (2008) Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death Differ 15:322–331. doi:10.1038/sj.cdd.4402260

    PubMed  CAS  Google Scholar 

  57. Laing KJ, Holland J, Bonilla S, Cunningham C, Secombes CJ (2001) Cloning and sequencing of caspase 6 in rainbow trout, Oncorhynchus mykiss, and analysis of its expression under conditions known to induce apoptosis. Dev Comp Immunol 25:303–312. doi:10.1016/S0145-305X(00)00061-6

    PubMed  CAS  Google Scholar 

  58. Santoro MM, Samuel T, Mitchell T, Reed JC, Stainier DY (2007) Birc2 (cIap1) regulates endothelial cell integrity and blood vessel homeostasis. Nat Genet 39:1397–1402. doi:10.1038/ng.2007.8

    PubMed  CAS  Google Scholar 

  59. Varfolomeev EE, Schuchmann M, Luria V, Chiannilkulchai N, Beckmann JS, Mett IL, Rebrikov D, Brodianski VM, Kemper OC, Kollet O, Lapidot T, Soffer D, Sobe T, Avraham KB, Goncharov T, Holtmann H, Lonai P, Wallach D (1998) Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9:267–276. doi:10.1016/S1074-7613(00)80609-3

    PubMed  CAS  Google Scholar 

  60. Reis MI, do VA, Pinto C, Nascimento DS, Costa-Ramos C, Silva DS, Silva MT, dos Santos NM (2007) First molecular cloning and characterisation of caspase-9 gene in fish and its involvement in a gram negative septicaemia. Mol Immunol 44:1754–1764. doi:10.1016/j.molimm.2006.07.293

    PubMed  CAS  Google Scholar 

  61. Ali M, Rahman S, Rehman H, Bhatia K, Ansari RA, Raisuddin S (2007) Pro-apoptotic effect of fly ash leachates in hepatocytes of freshwater fish (Channa punctata Bloch). Toxicol In Vitro 21:63–71. doi:10.1016/j.tiv.2006.08.011

    PubMed  CAS  Google Scholar 

  62. Chen SP, Wu JL, Su YC, Hong JR (2007) Anti-Bcl-2 family members, zfBcl-x(L) and zfMcl-1a, prevent cytochrome c release from cells undergoing betanodavirus-induced secondary necrotic cell death. Apoptosis 12:1043–1060. doi:10.1007/s10495-006-0032-x

    PubMed  CAS  Google Scholar 

  63. Risso-de Faverney C, Orsini N, de Sousa G, Rahmani R (2004) Cadmium-induced apoptosis through the mitochondrial pathway in rainbow trout hepatocytes: involvement of oxidative stress. Aquat Toxicol 69:247–258. doi:10.1016/j.aquatox.2004.05.011

    PubMed  CAS  Google Scholar 

  64. Guo Y, Cheong N, Zhang Z, De Rose R, Deng Y, Farber SA, Fernandes-Alnemri T, Alnemri ES (2004) Tim50, a component of the mitochondrial translocator, regulates mitochondrial integrity and cell death. J Biol Chem 279:24813–24825. doi:10.1074/jbc.M402049200

    PubMed  CAS  Google Scholar 

  65. Jiang X, Wang X (2000) Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to Apaf-1. J Biol Chem 275:31199–31203. doi:10.1074/jbc.C000405200

    PubMed  CAS  Google Scholar 

  66. Hand SC, Menze MA (2008) Mitochondria in energy-limited states: mechanisms that blunt the signaling of cell death. J Exp Biol 211:1829–1840. doi:10.1242/jeb.000299

    PubMed  CAS  Google Scholar 

  67. Krumschnabel G, Sohm B, Bock F, Manzl C, Villunger A (2008) The enigma of caspase-2—the laymen’s view. Cell Death Differ. doi:10.1038/cdd.2008.170

  68. Zhivotovsky B, Orrenius S (2005) Caspase-2 function in response to DNA damage. Biochem Biophys Res Commun 331:859–867. doi:10.1016/j.bbrc.2005.03.191

    PubMed  CAS  Google Scholar 

  69. Gyrd-Hansen M, Darding M, Miasari M, Santoro MM, Zender L, Xue W, Tenev T, da Fonseca PC, Zvelebil M, Bujnicki JM, Lowe S, Silke J, Meier P (2008) IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-kappaB as well as cell survival and oncogenesis. Nat Cell Biol 10:1309–1317. doi:10.1038/ncb1789

    PubMed  CAS  Google Scholar 

  70. Eckhart L, Fischer H, Tschachler E (2007) Phylogenomics of caspase-activated DNA fragmentation factor. Biochem Biophys Res Commun 356:293–299. doi:10.1016/j.bbrc.2007.02.122

    PubMed  CAS  Google Scholar 

  71. Hentschel DM, Park KM, Cilenti L, Zervos AS, Drummond I, Bonventre JV (2005) Acute renal failure in zebrafish: a novel system to study a complex disease. Am J Physiol Ren Physiol 288:F923–F929. doi:10.1152/ajprenal.00386.2004

    CAS  Google Scholar 

  72. Ma AC, Lin R, Chan PK, Leung JC, Chan LY, Meng A, Verfaillie CM, Liang R, Leung AY (2007) The role of survivin in angiogenesis during zebrafish embryonic development. BMC Dev Biol 7:50. doi:10.1186/1471-213X-7-50

    PubMed  Google Scholar 

  73. Murakawa M, Jung SK, Iijima K, Yonehara S (2001) Apoptosis-inducing protein, AIP, from parasite-infected fish induces apoptosis in mammalian cells by two different molecular mechanisms. Cell Death Differ 8:298–307. doi:10.1038/sj.cdd.4400811

    PubMed  CAS  Google Scholar 

  74. Mason JM, Naidu MD, Barcia M, Porti D, Chavan SS, Chu CC (2004) IL-4-induced gene-1 is a leukocyte L-amino acid oxidase with an unusual acidic pH preference and lysosomal localization. J Immunol 173:4561–4567

    PubMed  CAS  Google Scholar 

  75. Demarchi F, Schneider C (2007) The calpain system as a modulator of stress/damage response. Cell Cycle 6:136–138

    PubMed  CAS  Google Scholar 

  76. Salem M, Nath J, Rexroad CE, Killefer J, Yao J (2005) Identification and molecular characterization of the rainbow trout calpains (Capn1 and Capn2): their expression in muscle wasting during starvation. Comp Biochem Physiol B Biochem Mol Biol 140:63–71. doi:10.1016/j.cbpc.2004.09.007

    PubMed  Google Scholar 

  77. Salem M, Silverstein J, Rexroad CEIII, Yao J (2007) Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics 8:328. doi:10.1186/1471-2164-8-328

    PubMed  Google Scholar 

  78. Lepage SE, Bruce AE (2008) Characterization and comparative expression of zebrafish calpain system genes during early development. Dev Dyn 237:819–829. doi:10.1002/dvdy.21459

    PubMed  CAS  Google Scholar 

  79. Wulff T, Jessen F, Roepstorff P, Hoffmann EK (2008) Long term anoxia in rainbow trout investigated by 2-DE and MS/MS. Proteomics 8:1009–1018. doi:10.1002/pmic.200700460

    PubMed  CAS  Google Scholar 

  80. Ji L, Chen Y, Liu T, Wang Z (2008) Involvement of Bcl-xL degradation and mitochondrial-mediated apoptotic pathway in pyrrolizidine alkaloids-induced apoptosis in hepatocytes. Toxicol Appl Pharmacol 231:393–400. doi:10.1016/j.taap.2008.05.015

    PubMed  CAS  Google Scholar 

  81. Vousden KH, Lane DP (2007) p53 in health and disease. Nat Rev Mol Cell Biol 8:275–283. doi:10.1038/nrm2147

    PubMed  CAS  Google Scholar 

  82. de Caron F, Pakdel F, Chapus A, Baney C, May P, Soussi T (1992) Rainbow trout p53: cDNA cloning and biochemical characterization. Gene 112:241–245

    Google Scholar 

  83. Krause MK, Rhodes LD, Van Beneden RJ (1997) Cloning of the p53 tumor suppressor gene from the Japanese medaka (Oryzias latipes) and evaluation of mutational hotspots in MNNG-exposed fish. Gene 189:101–106. doi:10.1016/S0378-1119(96)00841-4

    PubMed  CAS  Google Scholar 

  84. Cheng R, Ford BL, O’Neal PE, Mathews CZ, Bradford CS, Thongtan T, Barnes DW, Hendricks JD, Bailey GS (1997) Zebrafish (Danio rerio) p53 tumor suppressor gene: cDNA sequence and expression during embryogenesis. Mol Mar Biol Biotechnol 6:88–97

    PubMed  CAS  Google Scholar 

  85. Le Bras M, Bensaad K, Soussi T (2003) Data mining the p53 pathway in the Fugu genome: evidence for strong conservation of the apoptotic pathway. Oncogene 22:5082–5090. doi:10.1038/sj.onc.1206424

    PubMed  Google Scholar 

  86. Blas-Machado U, Taylor HW, Means JC (2000) Apoptosis, PCNA, and p53 in Fundulus grandis fish liver after in vivo exposure to N-methyl-N′-nitro-N-nitrosoguanidine and 2-aminofluorene. Toxicol Pathol 28:601–609. doi:10.1177/019262330002800414

    PubMed  CAS  Google Scholar 

  87. Lesser MP, Farrell JH, Walker CW (2001) Oxidative stress, DNA damage and p53 expression in the larvae of atlantic cod (Gadus morhua) exposed to ultraviolet (290–400 nm) radiation. J Exp Biol 204:157–164

    PubMed  CAS  Google Scholar 

  88. Chen S, Hong Y, Scherer SJ, Schartl M (2001) Lack of ultraviolet-light inducibility of the medakafish (Oryzias latipes) tumor suppressor gene p53. Gene 264:197–203. doi:10.1016/S0378-1119(01)00340-7

    PubMed  CAS  Google Scholar 

  89. Rau EM, Billiard SM, Di Giulio RT (2006) Lack of p53 induction in fish cells by model chemotherapeutics. Oncogene 25:2004–2010. doi:10.1038/sj.onc.1209238

    Google Scholar 

  90. Momand J, Wu HH, Dasgupta G (2000) MDM2—master regulator of the p53 tumor suppressor protein. Gene 242:15–29. doi:10.1016/S0378-1119(99)00487-4

    PubMed  CAS  Google Scholar 

  91. Poyurovsky MV, Prives C (2006) Unleashing the power of p53: lessons from mice and men. Genes Dev 20:125–131. doi:10.1101/gad.1397506

    PubMed  CAS  Google Scholar 

  92. Thisse C, Neel H, Thisse B, Daujat S, Piette J (2000) The Mdm2 gene of zebrafish (Danio rerio): preferential expression during development of neural and muscular tissues, and absence of tumor formation after overexpression of its cDNA during early embryogenesis. Differentiation 66:61–70. doi:10.1046/j.1432-0436.2000.660201.x

    PubMed  CAS  Google Scholar 

  93. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr, Butel JS, Bradley A (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215–221. doi:10.1038/356215a0

    PubMed  CAS  Google Scholar 

  94. Jones SN, Hancock AR, Vogel H, Donehower LA, Bradley A (1998) Overexpression of Mdm2 in mice reveals a p53-independent role for Mdm2 in tumorigenesis. Proc Natl Acad Sci USA 95:15608–15612. doi:10.1073/pnas.95.26.15608

    PubMed  CAS  Google Scholar 

  95. Langheinrich U, Hennen E, Stott G, Vacun G (2002) Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling. Curr Biol 12:2023–2028. doi:10.1016/S0960-9822(02)01319-2

    PubMed  CAS  Google Scholar 

  96. Chen LJ, Hsu CC, Hong JR, Jou LK, Tseng HC, Wu JL, Liou YC, Her GM (2008) Liver-specific expression of p53-negative regulator mdm2 leads to growth retardation and fragile liver in zebrafish. Dev Dyn 237:1070–1081. doi:10.1002/dvdy.21477

    PubMed  CAS  Google Scholar 

  97. Berghmans S, Murphey RD, Wienholds E, Neuberg D, Kutok JL, Fletcher CD, Morris JP, Liu TX, Schulte-Merker S, Kanki JP, Plasterk R, Zon LI, Look AT (2005) tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci USA 102:407–412. doi:10.1073/pnas.0406252102

    PubMed  CAS  Google Scholar 

  98. Plaster N, Sonntag C, Busse CE, Hammerschmidt M (2006) p53 deficiency rescues apoptosis and differentiation of multiple cell types in zebrafish flathead mutants deficient for zygotic DNA polymerase delta1. Cell Death Differ 13:223–235. doi:10.1038/sj.cdd.4401747

    PubMed  CAS  Google Scholar 

  99. Tiano L, Fedeli D, Santoni G, Davies I, Falcioni G (2003) Effect of tributyltin on trout blood cells: changes in mitochondrial morphology and functionality. Biochim Biophys Acta 1640:105–112. doi:10.1016/S0167-4889(03)00025-9

    PubMed  CAS  Google Scholar 

  100. Toninello A, Salvi M, Colombo L (2000) The membrane permeability transition in liver mitochondria of the great green goby Zosterisessor ophiocephalus (Pallas). J Exp Biol 203:3425–3434

    PubMed  CAS  Google Scholar 

  101. Krumschnabel G, Manzl C, Berger C, Hofer B (2005) Oxidative stress, mitochondrial permeability transition, and cell death in Cu-exposed trout hepatocytes. Toxicol Appl Pharmacol 209:62–73. doi:10.1016/j.taap.2005.03.016

    PubMed  CAS  Google Scholar 

  102. Krumschnabel G, Maehr T, Nawaz M, Schwarzbaum PJ, Manzl C (2007) Staurosporine-induced cell death in salmonid cells: the role of apoptotic volume decrease, ion fluxes and MAP kinase signaling. Apoptosis 12:1755–1768. doi:10.1007/s10495-007-0103-7

    PubMed  CAS  Google Scholar 

  103. Bortner CD, Cidlowski JA (1998) A necessary role for cell shrinkage in apoptosis. Biochem Pharmacol 56:1549–1559. doi:10.1016/S0006-2952(98)00225-1

    PubMed  CAS  Google Scholar 

  104. Okada Y, Maeno E (2001) Apoptosis, cell volume regulation and volume-regulatory chloride channels. Comp Biochem Physiol A Mol Integr Physiol 130:377–383. doi:10.1016/S1095-6433(01)00424-X

    PubMed  CAS  Google Scholar 

  105. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431–1568

    PubMed  CAS  Google Scholar 

  106. Felderhoff-Mueser U, Bittigau P, Sifringer M, Jarosz B, Korobowicz E, Mahler L, Piening T, Moysich A, Grune T, Thor F, Heumann R, Bührer C, Ikonomidou C (2004) Oxygen causes cell death in the developing brain. Neurobiol Dis 17:273–282. doi:10.1016/j.nbd.2004.07.019

    PubMed  CAS  Google Scholar 

  107. Podrabsky JE, Hrbek T, Hand SC (1998) Physical and chemical characteristics of ephemeral pond habitats in the Maracaibo basin and Llanos region of Venezuela. Hydrobiologia 362:67–78. doi:10.1023/A:1003168704178

    Google Scholar 

  108. Nilsson GE (2007) Gill remodeling in fish—a new fashion or an ancient secret? J Exp Biol 210:2403–2409. doi:10.1242/jeb.000281

    PubMed  Google Scholar 

  109. Sollid J, De Angelis P, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673. doi:10.1242/jeb.00594

    PubMed  Google Scholar 

  110. Podrabsky JE, Lopez JP, Fan TWM, Higashi R, Somero GN (2007) Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus: insights from a metabolomics analysis. J Exp Biol 210:2253–2266. doi:10.1242/jeb.005116

    PubMed  CAS  Google Scholar 

  111. Fergusson-Kolmes L, Podrabsky JE (2007) Differential effects of anoxia on heart activity in anoxia-tolerant and anoxia-sensitive embryos of the annual killifish Austrofundulus limnaeus. J Exp Zool A Ecol Genet Physiol 307A:419–423

    Google Scholar 

  112. Lang KS, Fillon S, Schneider D, Rammensee H-G, Lang F (2002) Stimulation of TNFα expression by hyperosmotic stress. Pflugers Arch Eur J Physiol 443:798–803. doi:10.1007/s00424-001-0768-7

    CAS  Google Scholar 

  113. Lee W-K, Thévenod F (2006) A role for mitochondrial aquaporins in cellular life-and-death decisions? Am J Physiol Cell Physiol 291:C195–C202. doi:10.1152/ajpcell.00641.2005

    PubMed  CAS  Google Scholar 

  114. Bortner CD, Cidlowski JA (2007) Cell shrinkage and monvalent cation fluxes: role in apoptosis. Arch Biochem Biophys 462:176–188. doi:10.1016/j.abb.2007.01.020

    PubMed  CAS  Google Scholar 

  115. Niswander JM, Dokas LA (2007) Hyperosmotic stress-induced caspase-3 activation is mediated by p38 MAPK in the hippocampus. Brain Res 1186:1–11. doi:10.1016/j.brainres.2007.10.008

    PubMed  CAS  Google Scholar 

  116. Takahashi H, Sakamoto T, Narita K (2006) Cell proliferation and apoptosis in the anterior intestine of an amphibious, euryhaline mudskipper (Periophthalmus modestus). J Comp Physiol [B] 176:463–468. doi:10.1007/s00360-006-0067-x

    CAS  Google Scholar 

  117. Takahashi H, Prunet P, Kitahashi T, Kajimura S, Hirano T, Grau EG, Sakamoto T (2007) Prolactin receptor and proliferating/apoptotic cells in the esophagus of the Mozambique tilapia (Oreochromis mossambicus) in fresh water and in seawater. Gen Comp Endocrinol 152:326–331. doi:10.1016/j.ygcen.2007.02.021

    PubMed  CAS  Google Scholar 

  118. Suzuki Y (2004) Fine structural aspects of apoptosis in the olfactory epithelium. J Neurocytol 33:693–702. doi:10.1007/s11068-005-3337-8

    PubMed  Google Scholar 

  119. Taupin P, Gage FH (2002) Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 69:745–749. doi:10.1002/jnr.10378

    PubMed  CAS  Google Scholar 

  120. Zikopoulos B, Kentouri M, Dermon CR (2000) Proliferation zones in the adult brain of a sequential hermaphrodite teleost species (Sparus aurata). Brain Behav Evol 56:310–322. doi:10.1159/000047215

    PubMed  CAS  Google Scholar 

  121. Herrup K, Neve R, Ackerman SL, Copani A (2004) Divide and die: cell cycle events as triggers of nerve cell death. J Neurosci 24:9232–9239. doi:10.1523/JNEUROSCI.3347-04.2004

    PubMed  CAS  Google Scholar 

  122. Soutschek J, Zupanc GKH (1996) Apoptosis in the cerebellum of adult teleost fish, Apteronotus leptorhynchus. Dev Brain Res 97:279–286. doi:10.1016/S0165-3806(96)00145-9

    CAS  Google Scholar 

  123. Zupanc GKH (1999) Neurogenesis, cell death and regeneration in the adult gymnotiform brain. J Exp Biol 202:1435–1446

    PubMed  CAS  Google Scholar 

  124. Miranda ACL, Bazzoli N, Rizzo E, Sato Y (1999) Ovarian follicular atresia in two teleost species: a histological and ultrastructural study. Tissue Cell 31:480–488. doi:10.1054/tice.1999.0045

    PubMed  CAS  Google Scholar 

  125. Santos HB, Thome RG, Arantes FP, Sato Y, Bazzoli N, Rizzo E (2008) Ovarian follicular atresia is medaited by heterophagy, autophagy, and apoptosis in Prochilodus argenteus and Leporinus taeniatus (Teleostei: Characiformes). Theriogenology. doi:10.1016/j.theriogenology.2008.06.091

    Google Scholar 

  126. Uchida D, Yamashita M, Kitano T, Iguchi T (2002) Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J Exp Biol 205:711–718

    PubMed  Google Scholar 

  127. Liarte S, Chaves-Pozo E, Garcia-Alcazar A, Mulero V, Meseguer J, Garcia-Ayala A (2007) Testicular involution prior to sex change in gilthead seabream is characterized by a decrease in DMRT1 gene expression and by massive leukocyte infiltration. Reprod Biol Endocrinol 5:20. doi:10.1186/1477-7827-5-20

    PubMed  Google Scholar 

  128. Morgentaler A, Stahl BC, Yin Y (1999) Testis and temperature: an historical, clinical, and research perspective. J Androl 20:189–195

    PubMed  CAS  Google Scholar 

  129. David JR, Araripe LO, Chakir M, Legout H, Lemos B, Petavy G, Rohmer C, Joly D, Moreteau B (2005) Male sterility at extreme temperatures: a significant but neglected phenomenon for understanding Drosophila climate adaptations. J Evol Biol 18:838–846. doi:10.1111/j.1420-9101.2005.00914.x

    PubMed  CAS  Google Scholar 

  130. Yin Y, Hawkins KL, Dewolf WC, Morgentaler A (1997) Heat stress causes testicular germ cell apoptosis in mice. J Androl 18:159–165

    PubMed  CAS  Google Scholar 

  131. Ito LS, Yamashita M, Takahashi C, Strüssman CA (2003) Gonadal degeneration in sub-adult male pejerrey (Odontesthes bonariensis) during exposure to warm water. Fish Physiol Biochem 28:421–423. doi:10.1023/B:FISH.0000030613.33121.95

    CAS  Google Scholar 

  132. McClusky LM (2006) Stage-dependency of apoptosis and the blood-testis barrier in the dogfish shark (Squalus acanthias): cadmium-induced changes as assessed by vital fluorescence techniques. Cell Tissue Res 325:541–553. doi:10.1007/s00441-006-0184-6

    PubMed  CAS  Google Scholar 

  133. McClusky LM (2008) Fetal bovine serum simultaneously stimulates apoptosis and DNA synthesis in premeiotic stages of spermatogenesis in spiny dogfish (Squalus acanthias) in vitro: modulation by androgen and spermatogenic activity status. Apoptosis 13:649–658. doi:10.1007/s10495-008-0205-x

    PubMed  CAS  Google Scholar 

  134. Vize PD, Seufert DW, Carroll TJ, Wallingford JB (1997) Model systems for the study of kidney development: use of the pronephros in the analysis of organ induction and patterning. Dev Biol 188:189–204. doi:10.1006/dbio.1997.8629

    PubMed  CAS  Google Scholar 

  135. Moore MA, Metcalf D (1969) Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol 18:279–296. doi:10.1111/j.1365-2141.1970.tb01443.x

    Google Scholar 

  136. Ogawa M, Nishikawa S, Ikuta K, Yamamura F, Naito M, Takahashi K, Nishikawa S (1988) B cell ontogeny in murine embryo studied by a culture system with the monolayer of a stromal cell clone, ST2: B cell progenitor develops first in the embryonal body rather than in the yolk sac. EMBO J 7:1337–1343

    PubMed  CAS  Google Scholar 

  137. Campinho MA, Silva N, Sweeney GE, Power DM (2007) Molecular, cellular and histological changes in skin from a larval to an adult phenotype during bony fish metamorphosis. Cell Tissue Res 327:267–284. doi:10.1007/s00441-006-0262-9

    PubMed  CAS  Google Scholar 

  138. Soffientino B, Specker JL (2001) Metamorphosis of summer flounder, Paralichthys dentatus: cell proliferation and differentiation of the gastric mucosa and developmental effects of altered thyroidal status. J Exp Zool 290:31–40. doi:10.1002/jez.1033

    PubMed  CAS  Google Scholar 

  139. Kurz T, Terman A, Brunk UT (2007) Autophagy, ageing, and apoptosis: the role of oxidative stress and lysosomal iron. Arch Biochem Biophys 462:220–230. doi:10.1016/j.abb.2007.01.013

    PubMed  CAS  Google Scholar 

  140. Masoro EJ (2000) Caloric restriction and aging: an update. Exp Gerontol 35:299–305. doi:10.1016/S0531-5565(00)00084-X

    PubMed  CAS  Google Scholar 

  141. Bergamini E, Cavallini G, Donati A, Gori Z (2004) The role of macroautophagy in the ageing process, anti-ageing intervention and age-associated diseases. Int J Biochem Cell Biol 36:2392–2404. doi:10.1016/j.biocel.2004.05.007

    PubMed  CAS  Google Scholar 

  142. Rios FS, Kalinin AL, Rantin FT (2002) The effects of long-term food deprivation on respiration and haematology of the neotropical fish Hoplias malabaricus. J Fish Biol 61:85–95. doi:10.1111/j.1095-8649.2002.tb01738.x

    Google Scholar 

  143. Martin SAM, Cash P, Blaney S, Houlihan DF (2001) Proteome analysis of rainbow trout (Oncorhynchus mykiss) liver proteins during short term starvation. Fish Physiol Biochem 24:259–270. doi:10.1023/A:1014015530045

    CAS  Google Scholar 

  144. Herrera M, Jagadeeswaran P (2004) Annual fish as a genetic model for aging. J Gerontol A Biol Sci Med Sci 59:B101–B107

    Google Scholar 

  145. Moyes CD, Sharma ML, Lyons C, Leary SC, Leon M, Petrie A, Lund S, Tufts BL (2002) Origins and consequences of mitochondrial decline in nucleated erythrocytes. Biochim Biophys Acta 1591:11–20. doi:10.1016/S0167-4889(02)00224-0

    PubMed  CAS  Google Scholar 

  146. Caputo V, Candi G, Arneri E, La Mesa M, Cinti C, Provinciali M, Nisi Cerioni P, Gregorini A (2002) Short lifespan and apoptosis in Aphia minuta. J Fish Biol 60:775–779. doi:10.1111/j.1095-8649.2002.tb01703.x

    Google Scholar 

  147. Valenzano DR, Terzibasi E, Genade T, Cattaneo A, Domenici L, Cellerino A (2006) Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Curr Biol 16:296–300

    PubMed  CAS  Google Scholar 

  148. Valdesalici S, Cellerino A (2003) Extremely short lifespan in the annual fish Nothobranchius furzeri. Proc R Soc Lond B Biol Sci 270(Suppl):S189–S191. doi:10.1098/rsbl.2003.0048

    Google Scholar 

  149. Cole LK, Ross LS (2001) Apoptosis in the developing zebrafish embryo. Dev Biol 240:123–142. doi:10.1006/dbio.2001.0432

    PubMed  CAS  Google Scholar 

  150. Jeffery WR (2001) Cavefish as a model system in evolutionary developmental biology. Dev Biol 231:1–12. doi:10.1006/dbio.2000.0121

    PubMed  CAS  Google Scholar 

  151. Strickler AG, Byerly MS, Jeffery WR (2007) Lens gene expression reveals downregulation of the anti-apoptotic chaperone αA-crystallin during cavefish eye degeneration. Dev Genes Evol 217:771–782. doi:10.1007/s00427-007-0190-z

    PubMed  CAS  Google Scholar 

  152. Mader MM, Cameron DA (2004) Photoreceptor differentiation during retinal development, growth, and regeneration in a metamorphic vertebrate. J Neurosci 24:11463–11472. doi:10.1523/JNEUROSCI.3343-04.2004

    PubMed  CAS  Google Scholar 

  153. Iger Y, Abraham M, Wendelaar Bonga SE (1994) Response of club cells in the skin of the carp Cyprinus carpio to exogenous stressors. Cell Tissue Res 277:485–491. doi:10.1007/BF00300221

    Google Scholar 

  154. Evans DL, Leary JHIII, Jaso-Friedmann L (2001) Nonspecific cytotoxic cells and innate immunity: regulation by programmed cell death. Dev Comp Immunol 25:791–805. doi:10.1016/S0145-305X(01)00036-2

    PubMed  CAS  Google Scholar 

  155. Hu G-B, Cong R-S, Fan T-J, Mei X-G (2004) Induction of apoptosis in a flounder gill cell line by lymphocystis disease virus infection. J Fish Dis 27:657–662. doi:10.1111/j.1365-2761.2004.00588.x

    PubMed  Google Scholar 

  156. Wendelaar Bonga SE, van der Meij CJM (1989) Degeneration and death, by apoptosis and necrosis, of the pavement and chloride cells in the gills of the teleost Oreochromis mossambicus. Cell Tissue Res 255:235–243

    Google Scholar 

  157. Rojo C, González E (1999) Ontogeny and apoptosis of chloride cells in the gill epithelium of newly hatched rainbow trout. Acta Zoologica 80:11–23. doi:10.1046/j.1463-6395.1999.20003.x

    Google Scholar 

  158. Iger Y, Wendelaar Bonga SE (1994) Cellular responses of the skin of carp (Cyprinus carpio) exposed to acidified water. Cell Tissue Res 275:481–492. doi:10.1007/BF00318817

    Google Scholar 

  159. Poli A, Beraudi A, Villani L, Storto M, Battaglia G, Gerevini VDG, Cappuccio I, Caricasole A, D’Onofrio M, Nicoletti F (2003) Group II metabotropic glutamate receptors regulate the vulnerability to hypoxic brain damage. J Neurosci 23:6023–6029

    PubMed  CAS  Google Scholar 

  160. Lutz PL, Nilsson GE (2004) Vertebrate brains at the pilot light. Respir Physiol Neurobiol 141:285–296. doi:10.1016/j.resp.2004.03.013

    PubMed  CAS  Google Scholar 

  161. Stecyk JA, Stensløkken KO, Farrell AP, Nilsson GE (2004) Maintained cardiac pumping in anoxic crucian carp. Science 306:77. doi:10.1126/science.1100763

    PubMed  CAS  Google Scholar 

  162. Olohan LA, Li W, Wulff T, Jarmer H, Gracey AY, Cossins AR (2008) Detection of anoxia-responsive genes in cultured cells of the rainbow trout Oncorhynchus mykiss (Walbaum), using an optimized, genome-wide oligoarray. J Fish Biol 72:2170–2186. doi:10.1111/j.1095-8649.2008.01877.x

    Google Scholar 

  163. Chan CY, Lam WP, Wai MSM, Wang M, Foster EL, Yew DT-W (2007) Perinatal hypoxia induces anterior chamber changes in the eyes of offspring fish. J Reprod Dev 53:1159–1167. doi:10.1262/jrd.19018

    PubMed  Google Scholar 

  164. Lü L-H, Li J-C, Wai MSM, Lam WP, Forster EL, Fang M-R, Yew DT (2007) Perinatal hypoxia induces subsequent retinal degeneration in the offspring of ovoviviparous fish, Xiphophorus maculates. Vet Ophthalmol 10:289–294. doi:10.1111/j.1463-5224.2007.00552.x

    PubMed  Google Scholar 

  165. Arab H, Walker NI, Cheung K, Winterford C, Hickman PE, Potter JM, Roberts MS (1998) Functional and structural characterization of isolated perfused stingray liver including effects of ischaemia/reperfusion. J Comp Pathol 118:221–230. doi:10.1016/S0021-9975(05)80128-8

    PubMed  CAS  Google Scholar 

  166. Yabu T, Todoriki S, Yamashita M (2001) Stress-induced apoptosis by heat shock, UV, and γ-ray irradiation in zebrafish embryos detected by increased caspase activity and whole-mount TUNEL staining. Fish Sci 67:333–340. doi:10.1046/j.1444-2906.2001.00233.x

    CAS  Google Scholar 

  167. O’Reilly JP, Mothersill C (1997) Comparative effects of UV A and UV B on clonogenic survival and delayed cell death in skin cell lines from humans and fish. Int J Radiat Biol 72:111–119. doi:10.1080/095530097143590

    PubMed  CAS  Google Scholar 

  168. Yabu T, Ishibashi Y, Yamashita M (2003) Stress-induced apoptosis in larval embryos of Japanese flounder. Fish Sci 69:1218–1223. doi:10.1111/j.0919-9268.2003.00748.x

    CAS  Google Scholar 

  169. Drummond CD, Bazzoli N, Rizzo E, Sato Y (2000) Postovulatory follicle: a model for experimental studies of programmed cell death or apoptosis in teleosts. J Exp Zool 287:176–182. doi :10.1002/1097-010X(20000701)287:2<176∷AID-JEZ8>3.0.CO;2-2

    PubMed  CAS  Google Scholar 

  170. Chaves-Pozo E, Mulero V, Meseguer J, Ayala AG (2005) An overview of cell renewal in the testis throughout the reproductive cycle of a seasonal breeding teleost, the Gilthead Seabream (Sparus aurata L.). Biol Reprod 72:593–601. doi:10.1095/biolreprod.104.036103

    PubMed  CAS  Google Scholar 

  171. Donaldson MR, Cooke SJ, Patterson DA, Macdonald JS (2008) Cold shock and fish. J Fish Biol 73:1491–1530. doi:10.1111/j.1095-8649.2008.02061.x

    Google Scholar 

  172. Uchida D, Yamashita M, Kitano T, Iguchi T (2004) An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal. Comp Biochem Physiol A 137:11–20

    Google Scholar 

  173. Stokes EA, Lonergan W, Weber LP, Janz DM, Poznanski AA, Balch GC, Metcalfe CD, Grober MS (2004) Decreased apoptosis in the forebrain of adult male medaka (Oryzias latipes) after exposure to ethinylestradiol. Comp Biochem Physiol C 138:163–167. doi:10.1016/j.cbpc.2004.03.006

    Google Scholar 

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Acknowledgments

GK is supported by a grant from the Austrian Science Fund (FWF; Y212-B13 START), JP is funded by the United States National Science Foundation (IOB-0344578). We thank A. Villunger for critical comments on an early version of the manuscript.

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  1. Division of Developmental Immunology, Biocenter, Innsbruck Medical University, 6020, Innsbruck, Austria

    Gerhard Krumschnabel

  2. Department of Biology, Portland State University, P. O. Box 751, Portland, OR, 97207-0751, USA

    Jason E. Podrabsky

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Correspondence to Gerhard Krumschnabel or Jason E. Podrabsky.

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Krumschnabel, G., Podrabsky, J.E. Fish as model systems for the study of vertebrate apoptosis. Apoptosis 14, 1–21 (2009). https://doi.org/10.1007/s10495-008-0281-y

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