Hypoxia turns genotypic female medaka fish into phenotypic males

Ecotoxicology

Volumn 23, Issue 7, 2014, Pages 1260-1269

  Cheung, Catis Hin Ying ^a   Chiu, Jill Man Ying ^b   Wu, Rudolf Shiu Sun ^c  

^a CITY UNIVERSITY OF HONG KONG   (Hong Kong)

^b HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

DMY; Hypoxia; Male biased F1 generation; Sex determination; vasa

Indexed keywords

OXYGEN;

FISH; GENOTYPE; HYPOXIA; METABOLISM; PHENOTYPE; SEX DETERMINATION; SEX HORMONE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DMY GENE; DOWN REGULATION; EMBRYO; ENVIRONMENTAL EXPOSURE; FEMALE; GENE; GENE EXPRESSION; GENOTYPE; HATCHING; HYPOXIA; MALE; NONHUMAN; ORYZIAS LATIPES; OVARY; PHENOTYPE; PRIORITY JOURNAL; SEX DETERMINATION; SEX DIFFERENTIATION; TESTIS; UPREGULATION; VASA GENE; ANIMAL; ANOXIA; EUTROPHICATION; GENE EXPRESSION REGULATION; GONAD; ORYZIAS; PHYSIOLOGY; SEX DETERMINATION PROCESS; SEX RATIO;

ORYZIAS LATIPES; ORYZIINAE; VERTEBRATA;

ANIMALS; ANOXIA; EUTROPHICATION; FEMALE; GENE EXPRESSION REGULATION; GENOTYPE; GONADS; MALE; ORYZIAS; PHENOTYPE; SEX DETERMINATION PROCESSES; SEX DIFFERENTIATION; SEX RATIO;

EID: 84906315450     PISSN: 09639292     EISSN: 15733017     Source Type: Journal    
DOI: 10.1007/s10646-014-1269-8     Document Type: Article

References (54)

1. Alderdice DF, Wickett WP, Brett JR (1958) Some effects of temporary exposure to low dissolved oxygen levels on pacific salmon eggs. J Fish Res Board Can 15:229-250
2. Ankoma-Sey V, Wang Y, Dai Z (2000) Hypoxic stimulation of vascular endothelial growth factor expression in activated rat hepatic stellate cells. Hepatology 31:141-148 (Pubitemid 30033700)
3. Baroiller JF, D'Cotta H, Saillant E (2009) Environmental effects on fish sex determination and differentiation. Sex Dev 3:118-135
4. Blázquez M, González A, Mylonas CC, Piferrer F (2011) Cloning and sequence analysis of a vasa homolog in the European sea bass (Dicentrarchus labrax): tissue distribution and mRNA expression levels during early development and sex differentiation. Gen Comp Endocrinol 170:322-333
5. Boswell MG, Wells MC, Kirk LM, Ju Z, Zhang Z, Booth RE, Walter RB (2009) Comparison of gene expression responses to hypoxia in viviparous (Xiphophorus) and oviparous (Oryzias) fishes using a medaka microarray. Comp Biochem Physiol C 149:258-265
6. Braat AK, Zandbergen T, Van de Water S, Goos HJT, Zivkovic D (1999) Characterization of zebrafish primordial germ cells: morphology and early distribution of vasa RNA. Dev Dyn 216:153-167 (Pubitemid 29471178)
7. Burggren W (1999) Genetic, environmental and maternal influences on embryonic cardiac rhythms. Comp Biochem Physiol A 124:423-427
8. Czerkies P, Brzuzan P, Kordalski K, Luczynski M (2001) Critical partial pressures of oxygen causing precocious hatching in Coregonus lavaretus and C. albula embryos. Aquaculture 196:151-158 (Pubitemid 32247641)
9. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191-364 (Pubitemid 34641603)
10. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926-929
11. Diaz RJ, Rosenberg R (2011) Introduction to environmental and economic consequences of hypoxia. Int J Water Resour D 27:71-82
12. Geist DR, Abernethy CS, Hand KD, Cullinan VI, Chandler JA, Groves PA (2006) Survival, development, and growth of fall Chinook salmon embryos, alevins, and fry exposed to variable thermal and dissolved oxygen regimes. Trans Am Fish Soc 135:1462-1477 (Pubitemid 46673052)
13. Godwin J, Luckenbach JA, Borski RJ (2003) Ecology meets endocrinology: environmental sex determination in fishes. Evol Dev 5:40-49 (Pubitemid 36174976)
14. Gray JS, Wu RSS, Or YY (2002) Effects of hypoxia and organic enrichment on the coastal marine environment. Mar Ecol Prog Ser 238:249-279 (Pubitemid 34973398)
15. Grim KC, Wolfe M, Hawkins W, Johnson R, Wolf J (2007) Intersex in Japanese medaka (Oryzias latipes) used as negative controls in toxicologic bioassays: a review of 54 cases from 41 studies. Environ Toxicol Chem 26:1636-1643 (Pubitemid 47265505)
16. Iwamatsu T (2004) Stages of normal development in the medaka Oryzias latipes. Mech Dev 121:605-618
17. Jewell UR, Kvietikova I, Scheid A, Bauer C, Wenger RH, Gassmann M (2001) Induction of HIF-1a in response to hypoxia is instantaneous. FASEB J 15:1312-1314
18. Keckeis H, Bauer-Nemeschkal E, Kamler E (1996) Effects of reduced oxygen level on the mortality and hatching rate of Chondrostoma nasus embryos. J Fish Biol 49:430-440
19. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y (2000) Differential expression of vasa homologue gene in the germ cells during oogenesis and spermatogenesis in a teleost fish, tilapia, Oreochromis niloticus. Mech Dev 99:139-142
20. Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N, Nakamoto M, Shibata N, Nagahama Y (2004) Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev Dyn 231:518-526 (Pubitemid 39410886)
21. Kurauchi K, Nakaguchi Y, Tsutsumi M, Hori H, Kurihara R, Hashimoto S, Ohnuma R, Yamamoto Y, Matsuoka S, Kawai S, Hirata T, Kinoshita M (2005) In vivo visual reporter system for detection of estrogen-like substances by transgenic medaka. Environ Sci Technol 39:2762-2768 (Pubitemid 40570302)
22. Landry CA, Steele SL, Manning S, Cheek AO (2007) Long term hypoxia suppresses reproductive capacity in the estuarine fish, Fundulus grandis. Comp Biochem Physiol A 148:317-323 (Pubitemid 47199098)
23. Liu CC, Chiu JMY, Li L, Shin PKS, Cheung SG (2011) Physiological responses of two sublittoral nassariid gastropods to hypoxia. Mar Ecol Prog Ser 429:75-85
24. Lo KH, Hui MNY, Yu RMK, Wu RSS, Cheng SH (2011) Hypoxia impairs primordial germ cell migration in Zebrafish (Danio rerio) embryos. PLoS One 6:e24540
25. Lorke DE, Yew DT (2005) Worldwide decline of sturgeons. Science 310:1427-1429
26. Lu XY, Yu RMK, Murphy MB, Lau K, Wu RSS (2014) Hypoxia disrupts gene modulation along the brain - pituitary - gonad (BPG)-liver axis. Ecotoxicol Environ Saf 102:70-78
27. Martinovic D, Villeneuve DL, Kahl MD, Blake LS, Brodin JD, Ankley GT (2009) Hypoxia alters gene expression in the gonads of zebrafish (Danio rerio). Aquat Toxicol 95:258-272
28. Matsuda M (2005) Sex determination in the teleost medaka, Oryzias latipes. Annu Rev Genet 39:293-307
29. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559-563 (Pubitemid 34595924)
30. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M (2002) A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 99:11778-11783 (Pubitemid 34994475)
31. Oehlers LP, Perez AN, Walter RB (2007) Detection of hypoxia-related proteins in medaka (Oryzias latipes) brain tissue by difference gel electrophoresis and de novo sequencing of 4-sulfophenyl isothiocyanate- derivatized peptides by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Comp Biochem Physiol C 145:120-133 (Pubitemid 46205458)
32. Paul-Prasanth B, Matsuda M, Lau EL, Suzuki A, Sakai F, Kobayashi T, Nagahama Y (2006) Knock-down of DMY initiates female pathway in the genetic male medaka, Oryzias latipes. Biochem Biophys Res Commun 351:815-819 (Pubitemid 44715857)
33. Pincetich CA, Viant MR, Hinton DE, Tjeerdema RS (2005) Metabolic changes in Japanese medaka (Oryzias latipes) during embryogenesis and hypoxia as determined by in vivo 31P NMR. Comp Biochem Physiol C 140:103-113 (Pubitemid 40416711)
34. Roussel JM (2007) Carry-over effects in brown trout (Salmo trutta): hypoxia on embryos impairs predator avoidance by alevins in experimental channels. Can J Fish Aquat Sci 64:786-792
35. Satoh N, Egami N (1972) Sex differentiation of germ cells in the teleost, Oryzias latipes, during normal embryonic development. J Embryol Exp Morphol 28:385-395
36. Shang EHH, Wu RSS (2004) Aquatic hypoxia is a teratogen and affects fish embryonic development. Environ Sci Technol 38:4763-4767 (Pubitemid 39242693)
37. Shang EHH, Yu RMK, Wu RSS (2006) Hypoxia affects sex differentiation and development, leading to a male-dominated population in Zebrafish (Danio rerio). Environ Sci Technol 40:3118-3122 (Pubitemid 43673320)
38. Shima A, Mitani H (2004) Medaka as a research organism: past, present and future. Mech Dev 121:599-604 (Pubitemid 38813121)
39. Shinomiya A, Tanaka M, Kobayashi T, Nagahama Y, Hamaguchi S (2000) The vasa-like gene, olvas, identifies the migration path of primordial germ cells during embryonic body formation stage in the medaka, Oryzias latipes. Dev Growth Differ 42:317-326 (Pubitemid 30662888)
40. Shinomiya A, Otake H, Togashi K, Hamaguchi S, Sakaizumi M (2004) Field survey of sex-reversals in the medaka, Oryzias latipes: genotypic sexing of wild populations. Zool Sci 21:613-619 (Pubitemid 38946925)
41. STAP (2011) Hypoxia and nutrient reduction in the coastal zone: advice for prevention, remediation and research. A STAP Advisory Document. Global Environment Facility, Washington, DC
42. Taglialatela R, Della Corte F (1997) Human and recombinant erythropoietin stimulate erythropoiesis in the goldfish Carassius auratus. Eur J Histochem 41:301-304 (Pubitemid 28059227)
43. Thomas P, Rahman MS (2011) Extensive reproductive disruption, ovarian masculinization and aromatase suppression in Atlantic croaker in the northern Gulf of Mexico hypoxic zone. Proc R Soc B 279:28-38
44. Thomas P, Rahman MS, Kummer JA, Lawson S (2006) Reproductive endocrine dysfunction in Atlantic croaker exposed to hypoxia. Mar Environ Res 62(Suppl. 1):S249-S252 (Pubitemid 43867742)
45. Thomas P, Rahman MS, Khan IA, Kummer JA (2007) Widespread endocrine disruption and reproductive impairment in an estuarine fish population exposed to seasonal hypoxia. Proc R Soc B 274:2693-2702
46. Wiener CM, Booth G, Semenza GL (1996) In vivo expression of mRNAs encoding hypoxia-inducible factor 1. Biochem Biophys Res Commun 225:485-488 (Pubitemid 26355627)
47. Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35-45
48. Wu RSS (2009) Chapter 3 effects of hypoxia on fish reproduction and development. In: Richards JG, Farrell AP, Brauner CJ (eds) Fish physiology, vol 27. Academic Press, Amsterdam, pp 79-141
49. Wu RSS, Zhou BS, Randall DJ, Woo NYS, Lam PKS (2003) Aquatic hypoxia is an endocrine disruptor and impairs fish reproduction. Environ Sci Technol 37:1137-1141 (Pubitemid 36504980)
50. Yu R, Chen E, Kong R, Ng P, Mok H, Au D (2006) Hypoxia induces telomerase reverse transcriptase (TERT) gene expression in non-tumor fish tissues in vivo: the marine medaka (Oryzias melastigma) model. BMC Mol Biol 7:1-12
51. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Englewood Cliffs
52. Zhang Z, Wu RSS, Mok HOL, Wang Y, Poon WWL, Cheng SH, Kong RYC (2003) Isolation, characterization and expression analysis of a hypoxia-responsive glucose transporter gene from the grass carp, Ctenopharyngodon idellus. Eur J Biochem 270:3010-3017 (Pubitemid 36876270)
53. Zhang Z, Ju Z, Wells MC, Walter RB (2009) Genomic approaches in the identification of hypoxia biomarkers in model fish species. J Exp Mar Biol Ecol 381(Suppl.):S180-S187
54. Zhang Z, Wells MC, Boswell MG, Beldorth I, Kirk LM, Wang Y, Wang S, Savage M, Walter RB, Booth RE (2012) Identification of robust hypoxia biomarker candidates from fin of medaka (Oryzias latipes). Comp Biochem Physiol C 155:11-17