The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus

Journal of Experimental Biology

Volumn 202, Issue 19, 1999, Pages 2567-2580

  Podrabsky, Jason E ^a,b   Hand, Steven C ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Austrofundulus limnaeus; Calorimetry; Diapause; Energetics; Killifish; Metabolic depression; Respirometry

Indexed keywords

BIOENERGY; DIAPAUSE; EMBRYO DEVELOPMENT;

AUSTROFUNDULUS LIMNAEUS;

EID: 0032711374     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. Bergmeyer, H.-U. (1974). Methods of Enzymatic Analysis. 3rd edition. New York: Academic Press.
2. Boulekbache, H. (1981). Energy metabolism in fish development. Am. Zool. 21, 377-389.
3. Burton, K. (1956). A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem. J. 62, 315-323.
4. Carling, D. and Hardie, D. G. (1989). The substrate and sequence specificity of the AMP-activated protein kinase. Phosphorylation of glycogen synthase and phosphorylase kinase. Biochim. Biophys. Acta 1012, 81-86.
5. Carpenter, J. F. and Hand, S. C. (1986). Arrestment of carbohydrate metabolism during anaerobic dormancy and aerobic acidosis in Artemia embryos: determination of pH-sensitive control points. J. Comp. Physiol. B 156, 451-459.
6. Clegg, J. S., Drinkwater, L. E. and Sorgeloos, P. (1996). The metabolic status of diapause embryos of Artemia franciscana (SFB). Physiol. Zool. 69, 49-66.
7. Corton, J. M., Gillespie, J. G., Hawley, S. A. and Hardie, D. G. (1995). 5-Aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur. J. Biochem. 229, 558-565.
8. Darken, R. S., Martin, K. L. M. and Fisher, M. C. (1998). Metabolism during delayed hatching in terrestrial eggs of a marine fish, the Grunion Leuresthes tenuis. Physiol. Zool. 71, 400-406.
9. DiMichele, L. and Powers, D. A. (1984). The relationship between oxygen consumption rate and hatching in Fundulus heteroclitus. Physiol. Zool. 57, 46-51.
10. DiMichele, L. and Taylor, M. H. (1980). The environmental control of hatching in Fundulus heteroclitus. J. Exp. Zool. 214, 181-187.
11. Drinkwater, L. E. and Clegg, J. S. (1991). Experimental biology of cyst diapause. In Artemia Biology (ed. R. A. Browne, P. Sorgeloos and C. N. A. Trotman), pp. 93-117. Boca Raton, FL: CRC Press.
12. Drinkwater, L. E. and Crowe, J. H. (1987). Regulation of embryonic diapause in Artemia: environmental and physiological signals. J. Exp. Zool. 241, 297-307.
13. Ferrer, A., Caelles, C., Massot, N. and Hegardt, F. G. (1987). Affinity labeling of the catalytic and AMP allosteric sites of 3-hydroxy-3-methylglutaryl-coenzyme A reductase kinase by 5′-p-fluorosulfonylbenzoyladenosine. J. Biol. Chem. 262, 13507-13512.
14. Finn, R. N., Widdows, J. and Fyhn, H. J. (1995). Calorespirometry of developing embryos and yolk-sac larvae of turbot (Scophthalmus maximus). Mar. Biol. 122, 157-163.
15. Giles, K. W. and Myers, A. (1965). An improved diphenylamine method for the estimation of deoxyribonucleic acid. Nature 206, 93.
16. Gnaiger, E. (1983). Heat dissipation and energetic efficiency in animal anoxibiosis: Economy contra power. J. Exp. Zool. 228, 471-490.
17. Gnaiger, E. and Kemp, R. B. (1990). Anaerobic metabolism in aerobic mammalian cells: information from the ratio of calorimetric heat flux and respirometric oxygen flux. Biochim. Biophys. Acta 1016, 328-332.
18. Gnaiger, E., Lackner, R., Ortner, M., Putzer, V. and Kaufmann, R. (1981). Physiological and biochemical parameters in anoxic and aerobic energy metabolism of embryonic salmonids, Salvelinus alpinus. Eur. J. Physiol. (Suppl.) 131, R57.
19. Hand, S. C. (1991). Metabolic dormancy in aquatic invertebrates. Adv. Comp. Env. Physiol. 8, 1-50.
20. i and arrest of biosynthesis in brine shrimp embryos. Acta Physiol. Scand. 161, 543-551.
21. Hand, S. C. (1999). Calorimetric approaches to animal physiology and bioenergetics. In Handbook of Thermal Analysis and Calorimetry, vol. 4 (ed. R. B. Kemp). Amsterdam: Elsevier Science (in press).
22. Hardie, D. G. and Carling, D. (1997). The AMP-activated kinase. Fuel gauge of the mammalian cell? Eur. J. Biochem. 246, 259-271.
23. Hardie, D. G., Carling, D. and Carlson, M. (1998). The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu. Rev. Biochem. 67, 821-855.
24. Hishida, T.-O. and Nakano, E. (1954). Respiratory metabolism during fish development. Embryologia 2, 67-79.
25. Hutber, C. A., Hardie, D. G. and Winder, W. W. (1997). Electrical stimulation inactivates muscle acetyl-CoA carboxylase and increases AMP-activated protein kinase. Am. J. Physiol. 272, E262-E266.
26. Jermyn, M. A. (1975). Increasing the sensitivity of the anthrone method for carbohydrates. Analyt. Biochem. 68, 332-335.
27. Johansson, D., Nilsson, G. E. and Törnblom, E. (1995). Effects of anoxia on energy metabolism in crucian carp brain slices studied with microcalorimetry. J. Exp. Biol. 198, 853-859.
28. Kwast, K. E. and Hand, S. C. (1996). Oxygen and pH regulation of protein synthesis in mitochondria from Artemia franciscana embryos. Biochem. J. 313, 207-213.
29. Kwast, K. E., Shapiro, J. I., Rees, B. B. and Hand, S. C. (1995). Oxidative phosphorylation and realkalinization of intracellular pH during recovery from anoxia in Anemia franciscana embryos. Biochim. Biophys. Acta. 1232, 5-12.
30. Levels, P. J. and Denucé, J. M. (1988). Intrinsic variability in the frequency of embryonic diapauses of the annual fish Nothobranchius korthausae, regulated by light:dark cycle and temperature. Env. Biol. Fishes 22, 211-223.
31. Levels, P. J., Gubbels, R. E. M. B. and Denuce, J. M. (1986). Oxygen consumption during embryonic development of the annual fish Nothobranchius korthausae with special reference to diapause. Comp. Biochem. Physiol. 84A, 767-770.
32. Lilyestrom, C. and Taphorn, D. (1982). El control biologico de mosquitos mediante peces en la cuenca del Lago de Maracaibo, Venezuela. Informe Tecnico del Vice - Rectorado de Produccion Agricola 6, 1-38.
33. Loomis, S. H., Hand, S. C. and Fell, P. E. (1996a). Metabolism of gemmules from the freshwater sponge Eunapius fragilis during diapause and post-diapause states. Biol. Bull. 191, 385-392.
34. Loomis, S. H., Ungemach, L. F., Branchini, B. R., Hand, S. C. and Fell, P. E. (1996b). Carbohydrate mobilization during germination of post-diapausing gemmules of the freshwater sponge Eunapius fragilis. Biol. Bull. 191, 393-401.
35. Lowry, O. H. and Passoneau, J. V. (1972). A Flexible System of Enzymatic Analysis. London: Academic Press.
36. Mandoli, D. F., Ford, G. A., Waldron, L. J., Nemson, J. A. and Briggs, W. R. (1990). Some spectral properties of several soil types: implications for photomorphogenesis. Plant Cell Env. 13, 287-294.
37. Markofsky, J. and Matias, J. R. (1977). 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.
38. Markofsky, J., Matias, J. R., Inglima, K., Vogelman, J. H. and Orentreich, N. (1979). The variable effects of ambient and artificial light:dark cycles on embryonic diapause in a laboratory population of the annual fish Nothobranchius guentheri. J. Exp. Biol. 83, 203-215.
39. Milman, L. S. and Yurowitzki, Yu. G. (1967). The control of glycolysis in early embryogenesis. Biochim. Biophys. Acta 148, 362-371.
40. Milman, L. S. and Yurowitzki, Yu. G. (1973). Regulation of glycolysis in the early development of fish embryos. In Monographs in Developmental Biology, vol. 6 (ed. A. Wolsky). New York: S. Karger. 106pp.
41. Morowitz, H. J. (1968). Energy Flow in Biology. Biological Organization as a Problem in Thermal Physics. New York: Academic Press. 96pp.
42. Morrison, D. K. and Cutler, R. E. (1997). The complexity of Raf-1 regulation. Curr. Opin. Cell Biol. 9, 174-179.
43. Morrison, D. K., Heidecker, G., Rapp, U. R. and Copeland, T. D. (1993). Identification of the major phosphorylation sites of the Raf-1 kinase. J. Biol. Chem. 268, 17309-17316.
44. Myers, G. S. (1952). Annual fishes. Aquarium J. 23, 125-141.
45. Nico, L. G. and Thomerson, J. E. (1989). Ecology, food habits and spatial interactions of Orinoco Basin annual killifish. Acta Biol. Venez. 12, 106-120.
46. Paynter, K. T., DiMichele, L., Hand, S. C. and Powers, D. A. (1991). Metabolic implications of Ldh-B genotype during early development in Fundulus heteroclitus. J. Exp. Zool. 257, 24-33.
47. Peters, N. (1963). Embryonale Anpassungen oviparer Zahnkarpfen aus periodisch austrocknenden Gewassern. Int. Rev. Ges. Hydrobiol. 48, 257-313.
48. Peterson, G. L. (1977). A simplification of the protein assay method of Lowry et al., which is generally more applicable. Analyt. Biochem. 83, 346-356.
49. Podrabsky, J. E. (1999). Husbandry of the annual killifish Austrofundulus limnaeus with special emphasis on collection and rearing of embryos. Env. Biol. Fishes 54, 421-431.
50. Podrabsky, J. E., Hrbek, T. and Hand, S. C. (1998). Physical and chemical characteristics of ephemeral pond habitats in the Maracaibo basin and Llanos region of Venezuela. Hydrobiologia 362, 67-78.
51. Rees, B. B. and Hand, S. C. (1991). Regulation of glycolysis in the land snail Oreohelix during estivation and artificial hypercapnia. J. Comp. Physiol. B 161, 237-246.
52. Sato, R., Goldstein, J. L. and Brown, M. S. (1993). Replacement of serine-871 of hamster 3-hydroxy-3-methylglutaryl-CoA reductase prevents phosphorylation by AMP-activated kinase and blocks inhibition of sterol synthesis induced by ATP depletion. Proc. Natl. Acad. Sci. USA 90, 9261-9265.
53. Simpson, B. R. C. (1979). The phenology of annual killifishes. Symp. Zool. Soc. Lond. 44, 243-261.
54. Tester, M. and Morris, C. (1987). The penetration of light through soil. Plant Cell Env. 10, 281-286.
55. van Waversveld, J., Addink, A. D. F. and van den Thillart, G. (1989). The anaerobic energy metabolism of goldfish determined by simultaneous direct and indirect calorimetry during anoxia and hypoxia. J. Comp. Physiol. B 159, 263-268.
56. Vavvas, D., Apazidis, A., Saha, A. K., Gamble, J., Patel, A., Kemp, B. E., Witters, L. A. and Ruderman, N. B. (1997). Contraction-induced changes in acetyl-CoA carboxylase and 5′-AMP-activated kinase in skeletal muscle. J. Biol. Chem. 272, 13255-13261.
57. Walsh, W. A., Swanson, C., Lee, C.-S., Banno, J. E. and Eda, H. (1989). Oxygen consumption by eggs and larvae of striped mullet, Mugil cephalus, in relation to development, salinity and temperature. J. Fish Biol. 35, 347-358.
58. Widdows, J. (1987). Application of calorimetric methods in ecological studies. In Thermal and Energetic Studies of Cellular Biological Systems (ed. A. M. James), pp. 182-215. Bristol: IOP Publishing.
59. Wourms, J. P. (1972a). Developmental biology of annual fishes. I. Stages in the normal development of Austrofundulus myersi Dahl. J. Exp. Zool. 182, 143-168.
60. Wourms, J. P. (1972b). The developmental biology of annual fishes. II. Naturally occurring dispersion and reaggregation of blastomeres during the development of annual fish eggs. J. Exp. Zool. 182, 169-200.
61. Wourms, J. P. (1972c). 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.