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Cell and Tissue Research

, Volume 368, Issue 3, pp 425–439 | Cite as

Apoptosis in fish: environmental factors and programmed cell death

  • Hossein AnvariFarEmail author
  • Abdolsamad Keramat Amirkolaie
  • Hamed Kolangi Miandare
  • Hossein Ouraji
  • M. Ali Jalali
  • Sema İşisağ Üçüncü
Review

Abstract

Apoptosis, a form of programmed cell death, is a critical component in maintaining homeostasis and growth in all tissues and plays a significant role in immunity and cytotoxicity. In contrast to necrosis or traumatic cell death, apoptosis is a well-controlled and vital process characterized mainly by cytoplasmic shrinkage, chromatin condensation, DNA fragmentation, membrane blebbing and apoptotic bodies. Our understanding of apoptosis is partly based on observations in invertebrates but mainly in mammals. Despite the great advantages of fish models in studying vertebrate development and diseases and the tremendous interest observed in recent years, reports on apoptosis in fish are still limited. Although apoptotic machinery is well conserved between aquatic and terrestrial organisms throughout the history of evolution, some differences exist in key components of apoptotic pathways. Core parts of apoptotic machinery in fish are virtually expressed as equivalent to the mammalian models. Some differences are, however, evident, such as the extrinsic and intrinsic pathways of apoptosis including lack of a C-terminal region in the Fas-associated protein with a death domain in fish. Aquatic species inhabit a complex and highly fluctuating environment, making these species good examples to reveal features of apoptosis that may not be easily investigated in mammals. Therefore, in order to gain a wider view on programmed cell death in fish, interactions between the main environmental factors, chemicals and apoptosis are discussed in this review. It is indicated that apoptosis can be induced in fish by exposure to environmental stressors during different stages of the fish life cycle.

Keywords

Apoptosis Cell death Environmental stressors Fish Mammals 

Notes

Acknowledgements

We would like to express a special thanks to Dr. Willem B. Van Muiswinkel for editing and critical comments on the manuscript. This research was funded by a student grant from the Sari and Gorgan Universities of Agricultural Sciences and Natural Resources.

References

  1. Alford PB, Tomasso JR, Bodine AB, Kendall C (1994) Apoptotic death of peripheral leukocytes in channel catfish: effect of confinement-induced stress. J Aquat Anim Health 6:64–69CrossRefGoogle Scholar
  2. Almeida JA, Diniz YS, Marques SG, Faine LA, Ribas BO, Burneiko RC, Novelli EB (2002) The use of the oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environ Int 27:673–679PubMedCrossRefGoogle Scholar
  3. Anders F, Schartl M, Barnekow A, Anders A (1984) Xiphophorus as an in vivo model for studies on normal and defective control of oncogenes. Adv Cancer Res 42:191–275PubMedCrossRefGoogle Scholar
  4. 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 118:221–230PubMedCrossRefGoogle Scholar
  5. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A, Gherardi RK, Chazaud B (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204:1057–1069PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bakke-McKellep A, Penn MH, Salas PM, Refstie S, Sperstad S, Landsverk T, Ringø E, Krogdahl A (2007) Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Brit J Nut 97:699–713CrossRefGoogle Scholar
  7. Beattie MS, Hermann GE, Rogers RC, Bresnahan JC (2002) Cell death in models of spinal cord injury. Prog Brain Res 137:37–47PubMedCrossRefGoogle Scholar
  8. Becker CG, Becker T (2008) Adult zebrafish as a model for successful central nervous system regeneration. Restor Neurol Neurosci 26:71–80PubMedGoogle Scholar
  9. Beere HM (2004) ‘The stress of dying’: the role of heat shock proteins in the regulation of apoptosis. J Cell Sci 117:2641–2651PubMedCrossRefGoogle Scholar
  10. Berntssen MHG, Aspholm OO, Hylland K, Wendelaar Bonga SE, Lundebye AK (2001) Tissue metallothionein, apoptosis and cell proliferation responses in Atlantic salmon (Salmo salar L.) parr fed elevated dietary cadmium. Comp Biochem Physiol C 128:299–310CrossRefGoogle Scholar
  11. Berthelet J, Dubrez L (2013) Regulation of apoptosis by inhibitors of apoptosis (IAPs). Cells 2(1):163–187PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bortner CD, Cidlowski JA (2014) Ion channels and apoptosis in cancer. Philos Trans R Soc Lond B 369:20130104CrossRefGoogle Scholar
  13. Bullock AM (1982) The pathological effects of ultraviolet radiation on the epidermis of teleost fish with reference to the solar radiation effect in higher animals. Proc R Soc Edin B 8:199–210Google Scholar
  14. Bury NR, Jie L, Flik G, Lock RAC, Bonga SEW (1998) Cortisol protects against copper induced necrosis and promotes apoptosis in fish gill chloride cells in vitro. Aquat Toxicol 40:193–202CrossRefGoogle Scholar
  15. Celi M, Vazzana M, Sanfratello MA, Parrinello N (2012) Elevated cortisol modulates Hsp70 and Hsp90 gene expression and protein in sea bass head kidney and isolated leukocytes. Gen Comp Endocrinol 175:424–431Google Scholar
  16. Chan CY, Lam WP, Wai MSM, Wang M, Foster EL, Yew DTW (2007) Perinatal hypoxia induces anterior chamber changes in the eyes of offspring fish. J Reprod Dev 53:1159–1167PubMedCrossRefGoogle Scholar
  17. Chen C-F, Chu C-Y, Chen T-H, Lee S-J, Shen C-N, Hsiao C-D (2011) Establishment of a transgenic zebrafish line for superficial skin ablation and functional validation of apoptosis modulators in vivo. PLoS ONE 6(5), e20654PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cole LK, Ross LS (2001) Apoptosis in the developing zebrafish embryo. Dev Biol 240:123–142PubMedCrossRefGoogle Scholar
  19. Dallinger R, Prosi F, Scgner H, Back H (1987) Contaminated food and uptake of heavy metals by fish: a review and a proposal for further research. Oecologia 73:91–98PubMedCrossRefGoogle Scholar
  20. Derakhshan M (2007) Apoptosis at a glance: death or life? Pak J Med Sci 23(6):979–982Google Scholar
  21. Donaldson MR, Cooke SJ, Patterson DA, Macdonald JS (2008) Cold shock and fish. J Fish Biol 73:1491–1530CrossRefGoogle Scholar
  22. Dos Santos NM, do Vale A, Reis MI, Silva MT (2008) Fish and apoptosis: molecules and pathways. Curr Pharm Des 14(2):148–69PubMedCrossRefGoogle Scholar
  23. Eguchi Y, Shimizu S, Tsujimoto Y (1997) Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 57(10):1835–1840PubMedGoogle Scholar
  24. Eguchi Y, Srinivasan A, Tomaselli KJ, Shimizu S, Tsujimoto Y (1999) ATP-dependent steps in apoptotic signal transduction. Cancer Res 59(9):2174–2181PubMedGoogle Scholar
  25. 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 13:1619–1630PubMedCrossRefGoogle Scholar
  26. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516PubMedPubMedCentralCrossRefGoogle Scholar
  27. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Plant Physiol Plant Mol Biol 61:243–282Google Scholar
  28. Fink SL, Brad T, Cookson BT (2005) Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73(4):1907–1916PubMedPubMedCentralCrossRefGoogle Scholar
  29. Frankfurt O, Rosen ST (2004) Mechanisms of glucocorticoid-induced apoptosis in hematologic malignancies: updates. Curr Opin Oncol 16:553–563PubMedCrossRefGoogle Scholar
  30. Gamboa VM (2015) The effect of environmental changes of food on apoptosis in zebrafish ovarian tissue. AAAS Annual Meeting, 12–16 February 2015, San Jose, CAGoogle Scholar
  31. Gonzalez P, Baudrimont M, Boudou A, Bourdineaud JP (2006) Comparative effects of direct cadmium contamination on gene expression in gills, liver, skeletal muscles and brain of the zebrafish (Danio rerio). Biometals 19:225–235PubMedCrossRefGoogle Scholar
  32. Handy RD (1992) The assessment of episodic metal pollution. II. The effects of cadmium and copper enriched diets on tissue contamination analysis in rainbow trout (Oncorhynchus mykiss). Arch Environ Contam Toxicol 22:82–87PubMedCrossRefGoogle Scholar
  33. Harris J, Bird DJ (2000) Mini review: modulation of the fish immune system by hormones. Vet Immunol Immunopathol 77:163–176PubMedCrossRefGoogle Scholar
  34. Hashimoto H, Matsuo Y, Yokoyama Y, Toyohara H, Sakaguchi M (1998) Induction of apoptosis in fish cells by hypertonic stress. Fish Sci 64:820–825Google Scholar
  35. Hirano T (1986) The spectrum of prolactin action in teleosts. Prog Clin Biol Res 205:53–74PubMedGoogle Scholar
  36. Hirano T (1991) Endocrine control of osmoregulation in migratory fishes. In: Mauchline J, Nemoto T (eds) Marine Biology. Hakusen-sha, Tokyo, pp 3–14Google Scholar
  37. Hoffmann EK, Simonsen LO (1989) Membrane mechanismsin volume and pH regulation in vertebrate cells. Physiol Rev 69:315–382Google Scholar
  38. Hogan RJ, Taylor WR, Cuchens MA, Naftel JP, Clem LW, Miller NW, Chinchar VG (1999) Induction of target cell apoptosis by channel catfish cytotoxic cells. Cell Immunol 195(2):110–118PubMedCrossRefGoogle Scholar
  39. Hongmei Z (2012) Extrinsic and intrinsic apoptosis signal pathway review. Intech  10.5772/50129
  40. Huang NF, Zac-Varghese S, Luke S (2003) Apoptosis in skin wound healing. Wounds:15(6). http://www.woundsresearch.com/article/1746
  41. Iger Y, Wendelaar Bonga SE (1994) Cellular responses of the skin of carp (Cyprinus carpio) exposed to acidified water. Cell Tissue Res 275:481–492CrossRefGoogle Scholar
  42. Iger Y, Abraham M, Wendelaar Bonga SE (1994a) Response of club cells in the skin of the carp Cyprinus carpio to exogenous stressors. Cell Tissue Res 277:485–491CrossRefGoogle Scholar
  43. Iger Y, Balm PHM, Wendelaar Bonga SE (1994b) Cellular responses of the skin and changes in plasma cortisol levels of trout (Oncorhynchus mykiss) exposed to acidified water. Cell Tissue Res 278:535–542CrossRefGoogle Scholar
  44. Israels LG, Israels ED (1999) Apoptosis. Oncologist 4:332–339PubMedGoogle Scholar
  45. Ito LS, Yamashita M, Takahashi C, Strussman CA (2003) Gonadal degeneration in sub-adult male pejerrey (Odontesthes bonariensis) during exposure to warm water. Fish Physiol Biochem 28:421–423CrossRefGoogle Scholar
  46. Janz DM, Van Der Kraak G (1997) Suppression of apoptosis by gonadotropin, 17b-estradiol and epidermal growth factor in rainbow trout preovulatory ovarian follicles. Gen Comp Endocrinol 105:186–193PubMedCrossRefGoogle Scholar
  47. Janz DM, McMaster ME, Munkittrick KR, Van Der Kraak G (1997) Elevated ovarian follicular apoptosis and heat shock protein 70 expression in white sucker exposed to bleached kraft pulp mill effluent. Toxicol Appl Pharmacol 147:391–398PubMedCrossRefGoogle Scholar
  48. Janz DM, McMaster ME, Weber LP, Munkittrick KR, Van Der Kraak GM (2001) Recovery of ovary size, follicle cell apoptosis, and HSP70 expression in fish exposed to bleached pulp mill effluent. Can J Fish Aquat Sci 58(3):620–625Google Scholar
  49. Jeffery WR (2005) Adaptive evolution of eye degeneration in the Mexican blind cavefish. J Hered 96:185–196Google Scholar
  50. Jeong S, Kim J, Lee W, Hans-Uwe Dahms HU, Han KN (2014) Salinity changes in the anadromous river pufferfish, Takifugu obscurus, mediate gene regulation. Fish Physiol Biochem 40:205–219PubMedCrossRefGoogle Scholar
  51. Jhapmann C, Noonan FP, Merlino G (2003) Ultraviolet radiation and cutaneous malignant melanoma. Oncogene 22:3099–3112CrossRefGoogle Scholar
  52. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239–257PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kerr JF, Winterford CM, Harmon BV (1994) Apoptosis. Its significance in cancer and cancer therapy. Cancer 73(8):2013–2026PubMedCrossRefGoogle Scholar
  54. King KL, Cidlowski JA (1995) Cell cycle and apoptosis: common pathways to life and death. J Cell Biochem 58:175–180PubMedCrossRefGoogle Scholar
  55. Kroehne V, Freudenreich D, Hans S, Kaslin J, Brand M (2011) Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors. Development 138:4831–4841PubMedCrossRefGoogle Scholar
  56. Krumschnabel G, Podrabsky JE (2009) Fish as model systems for the study of vertebrate apoptosis. Apoptosis 14:1–21PubMedCrossRefGoogle Scholar
  57. Kulms D, Schwarz T (2000) Molecular mechanisms of UV-induced apoptosis. Photodermatol Photoimmunol Photomed 16:195–201PubMedCrossRefGoogle Scholar
  58. 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 25:303–312PubMedCrossRefGoogle Scholar
  59. Leist M, Single B, Naumann H (1999) Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Exp Cell Res 249(2):396–403PubMedCrossRefGoogle Scholar
  60. 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 204:157–164PubMedGoogle Scholar
  61. Li L, Yan B, Shi YQ, Zhang WQ, Wen ZL (2012) Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration. J Biol Chem 287:25353–25360PubMedPubMedCentralCrossRefGoogle Scholar
  62. 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 5:20PubMedPubMedCentralCrossRefGoogle Scholar
  63. Lindquist S, Craig E (1988) The heat-shock proteins. Annu Rev Genet 22:631–677PubMedCrossRefGoogle Scholar
  64. 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 68:258–263PubMedCrossRefGoogle Scholar
  65. Lü LH, Li JC, Wai MSM, Lam WP, Forster EL, Fang MR, Yew DT (2007) Perinatal hypoxia induces subsequent retinal degeneration in the offspring of ovoviviparous fish, Xiphophorus maculatus. Vet Ophthalmol 10:289–294PubMedCrossRefGoogle Scholar
  66. Lundebye AK, Berntssen MHG, Wendelaar Bongaà SE, Maage A (1999) Biochemical and physiological responses in atlantic salmon (Salmo salar) following dietary exposure to copper and cadmium. Mar Pollut Bull 39(1–12):137–144CrossRefGoogle Scholar
  67. Luzio A, Monteiro SM, Fontaı’nhas-Fernandes AA, Pinto-Carnide O, Matos M, Coimbra AM (2013) Copper induced upregulation of apoptosis related genes in zebrafish (Danio rerio) gill. Aquatic Toxicol 128–129:183–189Google Scholar
  68. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci U S A 17:9487–9492CrossRefGoogle Scholar
  69. Manzon LA (2002) The role of prolactin in fish osmoregulation: a review. Gen Comp Endocrinol 125:291–310PubMedCrossRefGoogle Scholar
  70. Martin P, Leibovich SJ (2005) Inflammatory cells during wound repair. The good, the bad, and the ugly. Trends Cell Biol 15:599–607PubMedCrossRefGoogle Scholar
  71. Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684PubMedPubMedCentralCrossRefGoogle Scholar
  72. McGeer JC, Szebedinszky C, McDonald DG, Wood CM (2000) Effects of chronic sublethal exposure to waterborne Cu, Cd or Zn in rainbow trout. 1: Iono-regulatory disturbance and metabolic costs. Aquat Toxicol 50:231–243PubMedCrossRefGoogle Scholar
  73. Metzstein MM, Stanfield GM, Horvitz HR (1998) Genetics of programmed cell death in C. elegans: past, present and future. Trends Genet 14:410–416PubMedCrossRefGoogle Scholar
  74. Miranda ACL, Bazzoli N, Rizzo E, Sato Y (1999) Ovarian follicular atresia in two teleost species: a histological and ultrastructural study. Tissue Cell 31:480–488PubMedCrossRefGoogle Scholar
  75. Mohapatra S, Chakraborty T, Prusty AK, PaniPrasad K, Mohanta KN (2014) Beneficial effects of dietary probiotics mixture on hemato-immunology and cell apoptosis of Labeo rohita fingerlings reared at higher water temperatures. PLoS ONE 9(6), e100929PubMedPubMedCentralCrossRefGoogle Scholar
  76. Nilsson GE (2007) Gill remodeling in fish—a new fashion or an ancient secret? J Exp Biol 210:2403–2409PubMedCrossRefGoogle Scholar
  77. 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 72:111–119PubMedCrossRefGoogle Scholar
  78. Okada Y, Maeno E (2001) Apoptosis, cell volume regulation and volume-regulatory chloride channels. Comp Biochem Physiol A 130(3):377–83CrossRefGoogle Scholar
  79. 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 72:2170–2186CrossRefGoogle Scholar
  80. Pathak N, Mitra S, Khandelwal S (2013) Cadmium induces thymocyte apoptosis via caspase-dependent and caspase-independent pathways. J Biochem Mol Toxicol 27(3):193–203PubMedCrossRefGoogle Scholar
  81. Piechotta G, Lacorn M, Lang T, Kammann U, Simat T, Jenke HS, Steinhart H (1999) Apoptosis in dab (Limanda limanda) as possible new biomarker for anthropogenic stress. Ecotoxicol Environ Saf 42:50–56PubMedCrossRefGoogle Scholar
  82. 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 210:2253–2266PubMedCrossRefGoogle Scholar
  83. 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 23:6023–6029PubMedGoogle Scholar
  84. Pouzand C, Tyrrell RM (1999) Apoptosis, the role of oxidative stress and the example of solar radiation. Photochem Photobiol 70:380–390CrossRefGoogle Scholar
  85. Profyris C, Cheema SS, Zang D, Azari MF, Boyle K, Petratos S (2004) Degenerative and regenerative mechanisms governing spinal cord injury. Neurobiol Dis 15:415–436PubMedCrossRefGoogle Scholar
  86. Provencher C, Bertolo A, Magnan P, Maria-Grazia Martinoli M-G (2014) Modulation of specific apoptotic DNA fragmentation after short term exposure to natural UVR in fish larvae. Open J Apop 39–51Google Scholar
  87. Pushchina EV, Varaksin AA, Obukhov DK (2016) Reparative neurogenesis in the brain and changes in the optic nerve of adult trout Oncorhynchus mykiss after mechanical damage of the eye. Russ J Dev Biol 47(1):11–32CrossRefGoogle Scholar
  88. Rajendran RS, Wellbrock UM, Zupanc GKH (2008) Apoptotic cell death, long-term persistence, and neuronal differentiation of aneuploid cells generated in the adult brain of teleost fish. Dev Neuropsychol 68:1257–1268Google Scholar
  89. Read AP, Strachan T (1999) Human molecular genetics 2. New York: Wiley; ISBN 0-471-33061-2. Chapter 18: Cancer GeneticsGoogle Scholar
  90. Rojo C, Gonzalez E (1999) Ontogeny and apoptosis of chloride cells in the gill epithelium of newly hatched rainbow trout. Acta Zool 80:11–23CrossRefGoogle Scholar
  91. Rojo MC, Blanquez MJ, Gonzalez ME (1997) Ultrastructural evidence for apoptosis of pavement cells, chloride cells and hatching gland cells in the developing branchial area of the trout Salmo trutta. J Zool 243:637–651CrossRefGoogle Scholar
  92. Romano N, Ceccarelli G, Caprera C, Caccia E, Baldassini MR, Marino G (2013) Apoptosis in thymus of teleost fish. Fish Shellfish Immunol 35(2):589–94PubMedCrossRefGoogle Scholar
  93. Rose WL, Nisbet RM, Green PG, Norris S, Fan T, Smith EH, Cherr GN, Anderson SL (2006) Using an integrated approach to link biomarker responses and physiological stress to growth impairment of cadmium-exposed larval topsmelt. Aquat Toxicol 80:298–308PubMedCrossRefGoogle Scholar
  94. Ryoo DH, Bergmann A (2012) The role of apoptosis-induced proliferation for regeneration and cancer. Cold Spring Harb Perspect Biol 4:a008797PubMedPubMedCentralCrossRefGoogle Scholar
  95. Sakamoto T, Oda A, Narita K, Takahashi H, Oda T, Fujiwara J, Godo W (2005a) Prolactin: fishy tales of its primary regulator and function. Ann NY Acad Sci 1040:184–188PubMedCrossRefGoogle Scholar
  96. Sakamoto T, Amano M, Hyodo S, Moriyama S, Takahashi A, Kawauchi H, Ando M (2005b) Expression of prolactin-releasing peptide and prolactin in the euryhaline mudskippers (Periophthalmus modestus): prolactin-releasing peptide as a primary regulator of prolactin. J Mol Endocrinol 34:825–834PubMedCrossRefGoogle Scholar
  97. Sakata S, Yan Y, Satou Y, Momoi A, Ngo-Hazelett P, Nozaki M, Furutani-Seiki M, Postlethwait J, Yonehara S, Sakamaki K (2007) Conserved function of caspase-8 in apoptosis during bony fish evolution. Gene 396:134–148PubMedPubMedCentralCrossRefGoogle Scholar
  98. Salinas I, Meseguer J, Esteban MA (2007a) Antiproliferative effects and apoptosis induction by probiotic cytoplasmic extracts in fish cell lines. Vet Microbiol 126(1–3):287–294PubMedGoogle Scholar
  99. Salinas I, Rodriguez A, Meseguer J, Esteban MA (2007b) Adenosine arrests apoptosis in lymphocytes but not in phagocytes from primary leucocyte cultures of the teleost fish, Sparus aurata L. Develop. Compr Immunol 31:1233–1241CrossRefGoogle Scholar
  100. 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 70:1449–1460PubMedCrossRefGoogle Scholar
  101. Schimdt R, Strähle U, Scholp S (2013) Neurogenesis in zebrafish – from embryo to adult. Neural Dev 8:3CrossRefGoogle Scholar
  102. Schulte PM (2014) What is environmental stress? insights from fish living in a variable environment. J Exp Biol 217:23–34PubMedCrossRefGoogle Scholar
  103. Shaw TJ, Martin P (2009) Wound repair at a glance. J Cell Sci 122:3209–3213PubMedPubMedCentralCrossRefGoogle Scholar
  104. Sîrbulescu RF, Zupanc GKH (2009) Dynamics of caspase-3-mediated apoptosis during spinal cord regeneration in the teleost fish, Apteronotus leptorhynchus. Brain Res 1304:14–25PubMedCrossRefGoogle Scholar
  105. Sîrbulescu RF, Ilieş I, Zupanc GKH (2009) Structural and functional regeneration after spinal cord injury in the weakly electric teleost fish, Apteronotus leptorhynchus. J Comp Physiol A 195:699–714CrossRefGoogle Scholar
  106. Solé M, Manzanera M, Bartolomé A, Tort L, Caixach J (2013) Persistent organic pollutants (POPs) in sediments from fishing grounds in the NW Mediterranean: ecotoxicological implications for the benthic fish Solea sp. Mar Pollut Bull 67:158–165PubMedCrossRefGoogle Scholar
  107. 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 206:3667–3673PubMedCrossRefGoogle Scholar
  108. Soutschek J, Zupanc GK (1995) Apoptosis as a regulator of cell proliferation in the central posterior/prepacemaker nucleus of adult gymnotiform fish, Apteronotus leptorhynchus. Neurosci Lett 202:133–136PubMedCrossRefGoogle Scholar
  109. Soutschek J, Zupanc GK (1996) Apoptosis in the cerebellum of adult teleost fish, Apteronotus leptorhynchus. Dev Brain Res 97:279–286CrossRefGoogle Scholar
  110. Stukaneva ME, Puschina EV, Varaksin AA, Shukla S (2015) Monitoring of cell migration and apoptosis in cerebellum of juvenile masu salmon Oncorhynchus masou after injury. Am J BioSci, Special Issue: adult and reparative neurogenesis: actual questions 3(2–3):19–27Google Scholar
  111. Sweet LI, Passino-Reader DR, Meier PG, Omann GM (1999) Xenobiotic-induced apoptosis: significance and potential application as a general biomarker of response. Biomarkers 4:237–253CrossRefGoogle Scholar
  112. Takahashi H, Sakamoto T, Narita K (2006a) Cell proliferation and apoptosis in the anterior intestine of an amphibious, euryhaline mudskipper (Periophthalmus modestus). J Comp Physiol B 176(5):463–468PubMedCrossRefGoogle Scholar
  113. Takahashi H, Takahashi A, Sakamoto T (2006b) In vivo effects of thyroid hormone, corticosteroids and prolactin on cell proliferation and apoptosis in the anterior intestine of the euryhaline mudskipper (Periophthalmus modestus). Life Sci 79:1873–1880PubMedCrossRefGoogle Scholar
  114. 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 152:326–331PubMedCrossRefGoogle Scholar
  115. Takahashi H, Susumu H, Tsukasa A, Chiyo T, Grau GE, Sakamoto T (2014) Effects of fasting and refeeding on intestinal cell proliferation and apoptosis in hammerhead shark (Sphyrna lewini). J Coastal Life Med 2(4):253–258Google Scholar
  116. 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 144:188–198PubMedCrossRefGoogle Scholar
  117. Tsujimoto Y (1997) Apoptosis and necrosis: intracellular ATP level as a determinant for cell death modes. Cell Death Different 4:429–434CrossRefGoogle Scholar
  118. 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 205:711–718PubMedGoogle Scholar
  119. 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 137:11–20CrossRefGoogle Scholar
  120. Valencia CA, Bailey C, Liu R (2007) Novel zebrafish caspase-3 substrates. Biochem Biophys Res Commun 361:311–316PubMedCrossRefGoogle Scholar
  121. van Ham TJ, Kokel D, Randall T, Peterson RT (2012) Apoptotic cells are cleared by directional migration and elmo1-dependent macrophage engulfment. Curr Biol 22(9):830–836PubMedPubMedCentralCrossRefGoogle Scholar
  122. Wendelaar Bonga SE, Van der Meij JCA (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 255:235–243CrossRefGoogle Scholar
  123. Wendelaar Bonga SE, Flik G, Balm PHM, Van der Meij JCA (1990) The ultrastructure of chloride cells in the gills of the teleost Oreochromis mossambicus during exposure to acidified water. Cell Tissue Res 259:575–585CrossRefGoogle Scholar
  124. Whitley D, Goldberg SP, Jordan WD (1999) Heat shock proteins: a review of the molecular chaperones. J Vasc Sur 29:748–751Google Scholar
  125. Wilson SE, He YG, Weng J, Li Q, McDowall AW, Vital M, Chwang EL (1996) Epithelial injury induces keratocyte apoptosis: hypothesized role for the interleukin-1 system in the modulation of corneal tissue organization and wound healing. Exp Eye Res 62(4):325–327PubMedCrossRefGoogle Scholar
  126. Wu YS, Chen SN (2014) Apoptotic cell: linkage of inflammation and wound healing frontiers in pharmacol inflam. Pharmacology 5:1–6Google Scholar
  127. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555–556PubMedCrossRefGoogle Scholar
  128. Wyllie AH (1997) Apoptosis: an overview. Br Med Bull 53(3):451–465PubMedCrossRefGoogle Scholar
  129. Yabu T, Todoriki S, Yamashita M (2001) Stress-induced apoptosis by heat shock, UV and y-ray irradiation in zebrafish embryos detected by increased caspase activity and whole mount TUNEL staining. Fish Sci 67:333–340CrossRefGoogle Scholar
  130. Yabu T, Ishibashi Y, Yamashita M (2003) Stress-induced apoptosis in larval embryos of Japanese flounder. Fish Sci 69:1218–1223CrossRefGoogle Scholar
  131. Yamashita M, Hojo M (2004) Generation of a transgenic zebrafish model overexpressing heat shock protein HSP70. Mar. Biotechnol., 6: S1–S7. In: Yamashita, M., Yabu, T., Ojima, N., 2010. Stress protein HSP70 in fish. Aqua-BioSci Monogr 3:111–141Google Scholar
  132. Yamashita M, Uchino K, Taguchi Y, Imamura S, Uchida D, Yabu T, Hojo M, Ojima N (2003) Stress response and apoptosis in zebrafish embryos. In: Shimizu N, Aoki T, Hirono I, Takashima F (eds) Aquatic genomics: steps toward a great future. Springer, Tokyo, pp 195–206CrossRefGoogle Scholar
  133. 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 211:1874–1881PubMedCrossRefGoogle Scholar
  134. Yamashita M, Yabu T, Ojima N (2010) Stress protein HSP70 in fish. Aqua-Bio Sci Monogr 3:111–141CrossRefGoogle Scholar
  135. Zagarese HE, Williamson CE (2001) The implications of solar UV radiation exposure for fish and fisheries. Fish Fish 2:250–260CrossRefGoogle Scholar
  136. Zeiss CJ (2003) The apoptosis-necrosis continuum: insights from genetically altered mice. Vet Pathol 40:481–95PubMedCrossRefGoogle Scholar
  137. Zhang H, Shao D, Wu Y, Dai B, Cai C, Fang W, Ye B, Zhang Y, Liu J, Jia X (2013) Regulation of nodularin-induced apoptosis by epigallocatechin-3-gallate on fish lymphocytes in vitro. Fish & Shellfish Immunol 34:1085e1Google Scholar
  138. Zupanc GKH (1999) Neurogenesis, cell death and regeneration in the adult gymnotiform brain. J Exp Biol 202:1435–1446PubMedGoogle Scholar
  139. Zupanc GKH (2006) Neurogenesis and neuronal regeneration in the adult fish brain. J Comp Physiol A 192:649–670CrossRefGoogle Scholar
  140. Zupanc GKH, Ott R (1999) Cell proliferation after lesions in the cerebellum of adult teleost fish: time course, origin, and type of new cells produced. Exp Neurol 160:78–87PubMedCrossRefGoogle Scholar
  141. Zupanc GKH, Kompass KS, Horschke I, Ott R, Schwarz H (1998) Apoptosis after injuries in the cerebellum of adult teleost fish. Exp Neurol 152:221–230PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Hossein AnvariFar
    • 1
    • 2
    Email author
  • Abdolsamad Keramat Amirkolaie
    • 1
  • Hamed Kolangi Miandare
    • 3
  • Hossein Ouraji
    • 1
  • M. Ali Jalali
    • 3
    • 4
    • 5
  • Sema İşisağ Üçüncü
    • 6
  1. 1.Faculty of Animal Science and Fisheries, Department of FisheriesUniversity of Agriculture and Natural ResourcesSariIran
  2. 2.University of Applied Science and TechnologyGolestanIran
  3. 3.Faculty of Fisheries and Environmental SciencesGorgan University of Agricultural Sciences and Natural ResourcesGorganIran
  4. 4.Sturgeon Affairs ManagementGorganIran
  5. 5.Center for Integrative Ecology, School of Life and Environmental SciencesDeakin UniversityVictoriaAustralia
  6. 6.Faculty of Science, Department of BiologyEge UniversityBornovaTurkey

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