Laboratory breeding of the short-lived annual killifish Nothobranchius furzeri

Nature Protocols

Volumn 11, Issue 8, 2016, Pages 1396-1413

  Polačik, Matej ^a   Blažek, Radim ^a   Reichard, Martin ^a  

^a INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BREEDING; EMBRYO; EMBRYO DEVELOPMENT; FEEDING BEHAVIOR; FEMALE; FLAGELLATE INFECTION; GROWTH RATE; HATCHING; JUVENILE ANIMAL; KILLIFISH; LABORATORY TEST; LIFE CYCLE; LIFESPAN; MALE; NONHUMAN; NOTHOBRANCHIUS FURZERI; NOTHOBRANCHIUS GUENTHERI; NOTHOBRANCHIUS KORTHAUSAE; OODINOSIS; PARASITOSIS; PRIORITY JOURNAL; SPAWNING; WATER QUALITY; ANIMAL; CYPRINODONTIFORMES; FISH DISEASES; GENETICS; LABORATORY; LONGEVITY; PHYSIOLOGY; PROCEDURES;

ANIMALS; BREEDING; CYPRINODONTIFORMES; FISH DISEASES; LABORATORIES; LONGEVITY;

EID: 84979891814     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2016.080     Document Type: Article

References (69)

1. Gerhard, G.S. Small laboratory fish as models for aging research. Ageing Res. Rev. 6, 64-72 (2007
2. Schartl, M. Beyond the zebrafish: diverse fish species for modelling human disease. Dis. Model. Mech. 7, 181-192 (2014
3. Maan, M.E., & Seehausen, O. Ecology, sexual selection and speciation. Ecol. Lett. 14, 591-602 (2011
4. Sloman, K.A., & McNeil, P.L. Using physiology and behaviour to understand the responses of fish early life stages to toxicants. J. Fish Biol. 81, 2175-2198 (2012
5. Comfort, A. Age and reproduction in female Lebistes. Gerontologia 5, 146-149 (1961
6. Egami, N., & Etoh, H. Life span data for the small fish, Oryzias latipes. Exp. Gerontol. 4, 127-129 (1969
7. Di Cicco, E., Tozzini, E.T., Rossi, G., & Cellerino, A. The short-lived annual fish Nothobranchius furzeri shows a typical teleost aging process reinforced by high incidence of age-dependent neoplasias. Exper. Gerontol. 46, 249-256 (2011
8. Wildekamp R.H. Apintu World of Killies: Atlas of the Oviparous Cyprinodontiform Fishes of the World Vol. 4. (American Killifish Association, 2004
9. Valdesalici, S., & Cellerino, A. Extremely short lifespan in the annual fish Nothobranchius furzeri. Proc. Biol. Sci. 270 (suppl. 2), S189-S191 (2003
10. Wang, A.M., Promislow, D.E., & Kaeberlein, M. Fertile waters for aging research. Cell 160, 814-815 (2015
11. Terzibasi E., et al. Large differences in aging phenotype between strains of the short-lived annual fish Nothobranchius furzeri. PLoS ONE 3, e3866 (2008
12. Tozzini E.T., et al. Parallel evolution of senescence in annual fishes in response to extrinsic mortality. BMC Evol. Biol. 13, 77 (2013
13. Wit, J., Loeschcke, V., & Kellermann, V. Life span variation in 13 Drosophila species: a comparative study on life span, environmental variables and stress resistance. J. Evol. Biol. 28, 1892-1900 (2015
14. Wendler, S., Hartmann, N., Hoppe, B., & Englert, C. Age-dependent decline in fin regenerative capacity in the short-lived fish Nothobranchius furzeri. Aging Cell 14, 857-866 (2015
15. Reichard, M., Polačik, M., & Sedláček, O. Distribution, colour polymorphism and habitat use of the African killifish, Nothobranchius furzeri, the vertebrate with the shortest lifespan. J. Fish Biol. 74, 198-212 (2009
16. Wourms, J.P. The developmental biology of annual fishes. III. Pre-embryonic and embryonic diapause of variable duration in the eggs of annual fishes. J. Exp. Zool. 182, 389-414 (1972
17. Furness, A.I., Lee, K., & Reznick, D.N. Adaptation in a variable environment: phenotypic plasticity and bet-hedging during egg diapause and hatching in an annual killifish. Evolution 69, 1461-1475 (2015
18. Blažek, R., Polačik, M., & Reichard, M. Rapid growth, early maturation and short generation time in African annual fishes. EvoDevo 4, 24 (2013
19. Cellerino, A., Valenzano, D.R., & Reichard, M. From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biol. Rev. 91, 511-533 (2016
20. D?Angelo, L. Brain atlas of an emerging teleostean model: Nothobranchius furzeri. Anat. Rec. 296, 681-691 (2013
21. Valenzano, D.R., Sharp, S., & Brunet, A. Transposon-mediated transgenesis in the short-lived African killifish Nothobranchius furzeri, a vertebrate model for aging. G3 (Bethseda) 1, 531-538 (2011
22. Hartmann, N., & Englert, C. Apintu microinjection protocol for the generation of transgenic killifish (species: Nothobranchius furzeri). Dev. Dyn. 241, 1133-1141 (2012
23. Allard, J.B., Kamei, H., & Duan, C. Inducible transgenic expression in the short-lived fish Nothobranchius furzeri. J. Fish Biol. 82, 1733-1738 (2013
24. Petzold A., et al. The transcript catalogue of the short-lived fish Nothobranchius furzeri provides insights into age-dependent changes of mRNA levels. BMC Genomics 14, 185 (2013
25. Baumgart M., et al. Age-dependent regulation of tumor-related microRNAs in the brain of the annual fish Nothobranchius furzeri. Mech. Age. Dev. 133, 226-233 (2012
26. Valenzano D.R., et al. The African turquoise killifish genome provides insights into evolution and genetic architecture of lifespan. Cell 163, 1539-1554 (2015
27. Reichwald K., et al. Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell 163, 1527-1538 (2015
28. Harel I., et al. Apintu platform for rapid exploration of aging and diseases in a naturally short-lived vertebrate. Cell 160, 1013-1026 (2015
29. Polačik, M., & Reichard, M. Diet overlap among three sympatric African annual killifish species (Nothobranchius spp.) from Mozambique. J. Fish Biol. 77, 754-768 (2010
30. Polačik, M., Donner, M.T., & Reichard, M. Age structure of annual Nothobranchius fishes in Mozambique: is there a hatching synchrony? J. Fish Biol. 78, 796-809 (2011
31. Reichard, M., Polačik, M., Blažek, R., & Vrtílek, M. Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors. Evol. Ecol. 28, 1105-1120 (2014
32. Bartáková, V., et al. Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique. BMC Evol. Biol. 13, 196 (2013
33. Bartáková, V., Reichard, M., Blažek, R., Polačik, M., & Bryja, J. Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna. J. Biogeogr. 42, 1832-1844 (2015
34. Polačik M., et al. Alternative intrapopulation life-history strategies and their trade-offs in an African annual fish. J. Evol. Biol. 27, 854-865 (2014
35. Podrabsky, J.E., & Culpepper, K.M. Cell cycle regulation during development and dormancy in embryos of the annual killifish Austrofundulus limnaeus. Cell Cycle 11, 1697-1704 (2012
36. Graf, M., Cellerino, A., & Englert, C. Gender separation increases somatic growth in females but does not affect lifespan in Nothobranchius furzeri. PLoS ONE 5, e11958 (2010
37. Noga, E.J Fish Disease: Diagnosis and Treatment 367 (Blackwell Publishing 2000
38. Lom, J., Noga, E.J., & Dyková, I. Occurrence of a microsporean with characteristics of Glugea anomala in ornamental fish of the family Cyprinodontidae. Dis. Aquat. Org. 21, 239-242 (1995
39. Lesseps, R.J., van Kessel, A.H., & Denuce, J.M. Cell patterns and cell movements during early development of an annual fish, Nothobranchius neumanni. J. Exp. Zool. 193, 137-146 (1975
40. Haarlem, R.V. Contact inhibition of overlapping: one of the factors involved in deep cell epiboly of Nothobranchius korthausae. Dev. Biol. 70, 171-179 (1979
41. Van Haarlem, R., Van Wijk, R., & Fikkert, A.H. Analysis of the variability in cleavage times and demonstration of a mitotic gradient during the cleavage stages of Nothobranchius guentheri. Cell Tissue Kinet. 14, 285-300 (1981
42. Markofsky, J., & Matias, J.R. The effects of temperature and season of collection on the onset and duration of diapause in embryos of the annual fish Nothobranchius guentheri. J. Exp. Zool. 202, 49-56 (1977
43. Inglima, K., Perlmutter, A., & Markofsky, J. Reversible stage-specific embryonic inhibition mediated by the presence of adults in the annual fish Nothobranchius guentheri. J. Exp. Zool. 215, 23-33 (1981
44. Levels, P.J., Gubbels, R.E., & Denuce, J.M. Oxygen consumption during embryonic development of the annual fish Nothobranchius korthausae with special reference to diapause. Comp. Biochem. Physiol. Apintu 84, 767-770 (1986
45. Markofsky, J., & Milstoc, M. Histopathological observations of the kidney during aging of the male annual fish Nothobranchius guentheri. Exp. Gerontol. 14, 149-155 (1979
46. Cooper, E.L., Zapata, A., Garcia Barrutia, M., & Ramirez, J.A. Aging changes in lymphopoietic and myelopoietic organs of the annual cyprinodont fish, Nothobranchius guentheri. Exp. Gerontol. 18, 29-38 (1983
47. van der Hoeven, J.C., Bruggeman, I.M., Alink, G.M., & Koeman, J.H. The killifish Nothobranchius rachowi, a new animal in genetic toxicology. Mutat. Res. 97, 35-42 (1982
48. Haas, R. Behavioral biology of the annual killifish Nothobranchius guentheri. Copeia 1976, 80-91 (1976
49. Genade T., et al. Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell 4, 223-233 (2005
50. Valenzano D.R., et al. Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Curr. Biol. 16, 296-300 (2006
51. Valenzano, D.R., Terzibasi, E., Cattaneo, A., Domenici, L., & Cellerino, A. Temperature affects longevity and age-related locomotor and cognitive decay in the short-lived fish Nothobranchius furzeri. Aging Cell 5, 275-278 (2006
52. Terzibasi E., et al. Effects of dietary restriction on mortality and age-related phenotypes in the short-lived fish Nothobranchius furzeri. Aging Cell 8, 88-99 (2009
53. Hartmann N., et al. Telomeres shorten while Tert expression increases during ageing of the short-lived fish Nothobranchius furzeri. Mech. Ageing. Dev. 130, 290-296 (2009
54. Hartmann N., et al. Mitochondrial DNA copy number and function decrease with age in the short-lived fish Nothobranchius furzeri. Aging Cell 10, 824-831 (2011
55. Tozzini, E.T., Baumgart, M., Battistoni, G., & Cellerino, A. Adult neurogenesis in the short-lived teleost Nothobranchius furzeri: localization of neurogenic niches, molecular characterization and effects of aging. Aging Cell 11, 241-251 (2012
56. Kirschner J., et al. Mapping of quantitative trait loci controlling lifespan in the short-lived fish Nothobranchius furzeri-A new vertebrate model for age research. Aging Cell 11, 252-261 (2012
57. Hoppe B., et al. MiR-21 is required for efficient kidney regeneration in fish. BMC Dev. Biol. 15, 43 (2015
58. Baumgart, M., Di Cicco, E., Rossi, G., Cellerino, A., & Tozzini, E.T. Comparison of captive lifespan, age-Associated liver neoplasias and age-dependent gene expression between two annual fish species: Nothobranchius furzeri and Nothobranchius korthause. Biogerontology 16, 63-69 (2015
59. Vrtílek, M., & Reichard, M. Highly plastic resource allocation to growth and reproduction in females of an African annual fish. Ecol. Freshw. Fish 24, 616-628 (2014
60. Polačik, M., & Reichard, M. Asymmetric reproductive isolation between two sympatric annual killifish with extremely short lifespans. PLoS ONE 6, e22684 (2011
61. Podrabsky, J.E., Garrett, I.D., & Kohl, Z.F. Alternative developmental pathways associated with diapause regulated by temperature and maternal influences in embryos of the annual killifish Austrofundulus limnaeus. J. Exp. Biol. 213, 3280-3288 (2010
62. Calviño, P.A., Alonso, F., & Sanjuán de Torres, J. Llenado de gas de la vejiga natatoria de post-larvas de peces anuales sudamericanos (Cyprinodontiformes; Rivulidae). Boletín del Killi Club Argentino 13, 19-38 (2007
63. Podrabsky, J.E. Husbandry of the annual killifish Austrofundulus limnaeus with special emphasis on the collection and rearing of embryos. Envir. Biol. Fishes 54, 421-431 (1999
64. Gerhard G.S., et al. Life spans and senescent phenotypes of zebrafish (Danio rerio). Exp. Gerontol. 37, 1055-1068 (2002
65. Reed, B., & Jennings, M Guidance on the housing and care of zebrafish Danio rerio.: Research Animals Department, Science Group, RSPCA, last updated 2011) https://www.scilifelab.se/wp-content/uploads/2013/10/Guidance-zebrafish.pdf
66. Davis, C.R., Okihiro, M.S., & Hinton, D.E. Effects of husbandry practices, gender, and normal physiological variation on growth and reproduction of Japanese medaka, Oryzias latipes. Aquat. Toxicol. 60, 185-201 (2002
67. Denny, J.S., Spehar, R.L., Mead, K.E., & Youssuf, S.C. Guidelines for culturing the Japanese medaka Oryzias latipes. United States Environmental Protection Agency, Office of Research and Development http://nepis.epa.gov/Exe/ZyPDF.cgi/30000OXS.PDF?Dockey=30000OXS.PDF1991
68. Ding, L., Kuhne, W.W., Hinton, D.E., Song, J., & Dynan, W.S. Quantifiable biomarkers of normal aging in the Japanese medaka fish (Oryzias latipes). PLoS ONE 5, e13287 (2010
69. Hirshfield, M.F. An experimental analysis of reproductive effort and cost in the Japanese medaka, Oryzias latipes. Ecology 61, 282-292 (1980