Salmon spawning migration: Metabolic shifts and environmental triggers

Comparative Biochemistry and Physiology - Part D: Genomics and Proteomics

Volumn 4, Issue 2, 2009, Pages 75-89

  Miller, Kristina M ^a   Schulze, Angela D ^a   Ginther, Norma ^a   Li, Shaorong ^a   Patterson, David A ^b   Farrell, Anthony P ^c   Hinch, Scott G ^c  

^a PACIFIC BIOLOGICAL STATION   (Canada)

^b FISHERIES AND OCEANS CANADA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Atrophy; Genomics; Microarray; Migration; Muscle; Sockeye

Indexed keywords

ACTIN; GLYCOLYTIC ENZYME; HEAT SHOCK PROTEIN; HELICASE; MUSCLE PROTEIN; NITRIC OXIDE; PROTEASOME;

ANAEROBIC GLYCOLYSIS; ARTICLE; CONTROLLED STUDY; DEATH; ENZYME ACTIVITY; ESTUARY; FAST MUSCLE; FEEDING; FRESHWATER ENVIRONMENT; FUNCTIONAL GENOMICS; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; LYSOSOME; MUSCLE METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; POPULATION MIGRATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; RIVER; SALMON; SPAWNING; STARVATION; UPREGULATION; WATER TEMPERATURE;

ONCORHYNCHUS NERKA;

ANIMAL MIGRATION; ANIMALS; BRITISH COLUMBIA; ENERGY METABOLISM; GENE EXPRESSION REGULATION; MUSCLE FIBERS, FAST-TWITCH; OCEANS AND SEAS; RIVERS; SALMON;

EID: 64849088285     PISSN: 1744117X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbd.2008.11.002     Document Type: Article

References (72)

1. Batt J., Bain J., Goncalves J., Michalski B., Plant P., Fahnestock M., and Woodgett J. Differential gene expression profiling of short and long term denervated muscle. FASEB J. 20 (2006) 115-117
2. Bax N.J. Early marine mortality of marked juvenile chum salmon released into Hood Canal, Puget Sound, Washington in 1980. Can. J. Fish. Aquat. Sci. 40 (1983) 426-435
3. Beacham T.D., Candy J.R., McIntosh B., MacConnachie C., Tabata A., Kaukinen K., Deng L., Miller K.M., Withler R.E., and Varnavskaya N.V. Estimation of stock composition and individual identification of sockeye salmon on a Pacific Rim basis using microsatellite and major histocompatibility complex variation. Trans. Am. Fish. Soc. 134 (2005) 1124-1146
4. Beamish R.J., and Mahnken C. A critical size and period hypothesis to explain natural regulation of salmon abundance and the linkage to climate and climate change. Prog. Oceanogr. 49 (2001) 423-437
5. Belcastro A.N., Albisser T.A., and Littlejohn B. Role of calcium-activated neutral protease (calpain) with diet and exercise. Can. J. Appl. Biol. 21 (1996) 328-346
6. Brett J.R. The swimming energetics of salmon. Sci. Am. 213 (1965) 80-85
7. Burgner R.L. Life history of sockeye salmon (Oncorhynchus nerka). In: Groot C., and Margolis L. (Eds). Pacific Salmon Life Histories (1991), University of British Columbia Press, Vancouver, B.C. 3-117
8. Cooke S.J., Hinch S.G., Farrell A.P., Lapointe M., Healey M.C., Patterson D., Macdonald S., Jones S.R.M., and Van Der Kraak G. Early-migration and abnormal mortality of late-run sockeye salmon in the Fraser River, British Columbia. Fisheries 29 (2004) 22-33
9. Cooke S.J., Hinch S.G., Crossin G.T., Patterson D.A., English K.K., Healey M.C., Macdonald J.S., Shrimpton J.M., Young J.L., Lister A., Van Der Kraak G., and Farrell A.P. Physiological correlates of coastal arrival and river entry timing in Late Summer Fraser River sockeye salmon (Oncorhynchus nerka). Behav. Ecol. 19 (2008) 747-758
10. Crossin G.T., Hinch S.G., Cooke S.J., Welch D.W., Lotto A.G., Patterson D.A., Jones S.R.M., Leggatt R.A., Mathes M.T., Shrimpton J.M., Van Der Kraak G., and Farrell A.P. Exposure to high temperature influences the behaviour, physiology, and survival of sockeye salmon during spawning migration. Can. J. Zool. 86 (2008) 127-140
11. Cuervo A.M., and Dice J.F. Lysosomes, a meeting point of proteins, chaperones, and proteases. J. Mol. Med. 76 (1998) 6-12
12. Cuervo A.M., Palmer A., Rivett A.J., and Knecht E. Degradation of proteosomes by lysosomes in rat liver. Eur. J. Biochem. 227 (1995) 792-800
13. Donaldson E.M., Smith J., Barnes D., Clarke W.C., Gordon R., and Martens D. Physiological and endocrine changes during the anadromous migration of early Stuart sockeye salmon (Oncorhynchus nerka) in 1997. In: Macdonald (Ed). Canadian Technical Report of Fisheries and Aquatic Sciences vol. 2315 (2000) 67-73
14. English K.K., Koski W.R., Sliwinski C., Blakley A., Cass A., and Woodey J.C. Migration timing and river survival of late-run Fraser River sockeye salmon estimated using radiotelemetry techniques. Trans. Am. Fish Soc. 134 (2005) 1342-1365
15. Finkel T., and Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 408 (2000) 239-247
16. French C.J., Hochachka P.W., and Mommsen T.P. Metabolic organization of liver during spawning migrations of sockeye salmon. Am. J. Physiol. 245 (1983) R827-R830
17. Gilhousen P. Energy sources and expenditures in Fraser River sockeye salmon during their spawning migration. Int. Pac.Salmon Fish. Comm. Bull. (1980) No. 22
18. Goll D.E., Thompson V.F., Taylor R.G., and Christiansen J.A. Role of the calpain system in muscle growth. Biochimie 74 (1992) 225-237
19. Groot C., and Margolis L. Pacific Salmon Life Histories (1991), University of British Columbia Press, Vancouver British Columbia
20. Haschemeyer A.E.V. A comparative study of protein synthesis in Nototheniids and icefish at Palmer station, Antarctica. Comp. Biochem. Physiol. 76B (1983) 541-543
21. Hershko A., Ciechanover A., and Varshavsky A. The ubiquitin system. Nat. Med. 6 (2000) 1073-1081
22. Hinch S.G., Cooke S.J., Healey M.C., and Farrell A.P. Behaviour and physiology of fish. In: Sloman K., Balshine S., and Wilson R. (Eds). Fish Physiology vol. 24 (2006), Elsevier 239-295
23. Huang J., and Forsberg N.E. Role of the calpain in skeletal-muscle protein degradation. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 12100-12105
24. Huang D.W., Sherman B.T., Tan Q., Collins J.R., Alvord W.G., Roayaei J., Stephens R., Baseler M.W., Lane H.C., and Lempicki R.A. The DAVID gene functional classification tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol. 8 (2007) R183
25. Idler D.R., and Clemens W.A. The energy expenditures of Fraser River sockeye salmon during the spawning migration to Chilko and Stuart Lakes. Int. Pacific Salmon Fish. Comm. Prog. Rept. No. 6 (1959) (80 pp.).
26. Ilian, M.A., Forsberg, N.E., 1992. Gene expression of calpains and their specific endogenous inhibitor, calpastatin, in skeletal muscle of fed and fasted rabbits. Biochem. J. 287 (Pt 1), 163-171.
27. Jurss K., and Bastrop R. Amino acid metabolism in fish. In: Hochachka P.W., and Mommsen T.P. (Eds). Biochemistry and Molecular Biology of Fishes vol. 4 (1995), Elsevier, Amsterdam 159-189
28. Kiessling A., Lindahl-Kiessling K., and Kiessling K.H. Energy utilization and metabolism in spawning migrating Early Stuart sockeye salmon (Oncorhynchus nerka): the migratory paradox. Can. J. Fish. Aquat. Sci. 61 (2004) 452-465
29. Kondo H., Harano R., Nakaya M., and Watabe S. Characterization of goldfish heat shock protein-30 induced upon severe heat shock in cultured cells. Cell Stress Chaperones 9 4 (2004) 350-368
30. Kuehl L., and Sumsion E.N. Turnover of several glycolytic enzymes in rat liver. J. Biol. Chem. 245 24 (1970) 6616-6623
31. Lapointe M.F., Cooke S.J., Hinch S.G., Farrell A.P., Jones S., Macdonald S., Patterson D., Healey M.C., and Van Der Kraak G. Late-run sockeye salmon in the Fraser River, British Columbia are experiencing early upstream migration and unusually high rates of mortality: what is going on?. In: Vancouver B.C., Droscher T.W., and Fraser D.A. (Eds). Proceedings of the 2003 Georgia Basin/Puget Sound Research Conference, 31 March - 3 April 2003 (2004), Puget Sound Action Team, Olympia, Wash 1-14
32. Lee C.-K., Klopp R.G., Weindruch R., and Prolla T.A. Gene expression profile of aging and its retardation by caloric restriction. Science 285 (1999) 1390-1393
33. Lee C.G., Farrell A.P., Lotto A., MacNutt M.J., Hinch S.G., and Healey M.C. The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. J. Exp. Biol. 206 (2003) 3239-3251
34. Lecker S.H., Solomon V., Mitch W.E., and Goldberg A.L. Muscle protein breakdown and the critical role of the ubiquitin-proteosome pathway in normal and disease states. J. Nutr. 129 (1999) S227-237
35. Lecker S.H., Jagoe R.T., Gilbert A., Gomes M., Baracos V., Bailey J., Price S.R., Mitch W.E., and Goldberg A.L. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18 (2004) 39-51
36. Loughna P.T., and Goldspink G. The effects of starvation upon protein turnover in red and white myotomal muscle of rainbow trout, Salmo gairdneri. J. Fish. Biol. 25 (1984) 223-230
37. Love R.M. The Chemical Biology of Fishes vol. 2 (1980), Academic Press, New York
38. Lowery M.S., and Somero G.N. Starvation effects on protein synthesis in red and white muscle of the barred sand bass, Paralabrax nebulifer. Physiol. Zool. 63 (1990) 630-648
39. Macdonald J.S. Mortality during the migration of Fraser River sockeye salmon (Oncorhynchus nerka): a study of the effect of ocean and river environmental conditions in 1997. Can. Tech Rep. Fish. Aquat. Sci. 2315 (2000) 39-57
40. Magnoni L.J., Patterson D.A., Farrell A.P., and Weber J.-M. Effects of long-distance migration on the circulating lipids of sockeye salmon (Oncorhynchus nerka). Can. J. Fish. Aquat. Sci. 63 (2006) 1822-1829
41. Martin S.A., Blancy S., Bowman A.S., and Houlihan D.F. Ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncohorhynchus mykiss): effect of food deprivation. Plungers Arch. 445 (2002) 257-266
42. McPhee M.V., and Quinn T.P. Factors affecting the duration of nest defense and reproductive lifespan of female sockeye salmon, Oncorhynchus nerka. Environ. Biol. Fishes 9 (1998) 211-268
43. Mommsen T.P. Salmon spawning migration and muscle protein metabolism: the August Krogh principle at work. Rev. Comp. Biochem. Physiol. B Biochem. Molec. Biol. 39 (2004) 383-400
44. Mommsen T.P., French C.J., and Hochachka P.W. Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Can. J. Zool. (1980) 785-1799
45. Mote P.W., Parson E.A., Hamlet A.F., et al. Preparing for climatic change: the water, salmon, and forests of the Pacific Northwest. Clim. Change 61 (2003) 45-88
46. Nagasaka R., Okamoto N., and Ushio H. Increased leptin may be involved in the short life span of ayu (Plecoglossus altivelis). J. Exp. Zool. 305A (2006) 507-512
47. Navarro I., and Guitierrez J. Fasting and starvation. In: Hochachka P.W., and Mommsen T.P. (Eds). Biochemistry and Molecular Biology of Fishes vol. 4 (1995), Elsevier, Amsterdam 393-434
48. Orr W.C., and Sohal R.S. Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263 (1994) 1128-1130
49. Pankhurst N., Purser G., Van der Kraak G., Thomas P., and Forteath G. Effect of holding temperature on ovulation, egg fertility, plasma levels of reproductive hormones and in vitro ovarian steroidogenesis in the rainbow trout, Oncorhynchus mykiss. Aquaculture 146 (1996) 277-290
50. Parker R.R. Marine mortality schedules of pink salmon of the Bella Coola River, Central British Columbia. J. Fish Res. Board Can. 25 (1968) 757-794
51. Pearse P.H., and Larkin P.A. Managing salmon in the Fraser. Vancouver, B.C., Department of Fisheries and Oceans (1992)
52. Podrabsky J.E., and Somero G.N. Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J. Exp. Biol. 207 (2004) 2237-2254
53. Salem M., Nath J., Rexroad C.E., Killefer J., and Yao J. Identification and molecular characterization of the rainbow trout calpains (Calpn1 and Capn2): their expression in muscle wasting during starvation. Comp. Biochem. Physiol. B 140 (2005) 63-71
54. Salem M., Kenney P.B., Rexroad C.E., and Yao J. Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model. Physiol. Genomics 28 (2006) 33-45
55. Salem M., Kenney P.B., Rexroad C.E., and Yao J. Molecular characterization of muscle atrophy and proteolysis associated with spawning in rainbow trout. Comp. Biochem. Physiol. D 1 (2006) 227-237
56. Salem M., Silverstein J., Rexroad C.E., and Yao J. Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics 8 (2007) 328
57. Salem M., Kenney P.B., Rexroad C.E., and Yao J. Development of a 37 k high-density oligonucleotide microarray: a new tool for functional genome research in rainbow trout. J. Fish Biol. 72 (2008) 2187-2206
58. Sanders J.E., Pilcher K.S., and Fryer J.L. Relation of water temperature to bacterial kidney disease in coho salmon (Oncorhynchus kisutch), sockeye salmon (Oncorhynchus nerka), and steelhead trout (Salmo gairdneri). J. Fish. Res. Board Can. 35 (1978) 8-11
59. Shibanuma M., Mochizuki E., Maniwa R., Mashimo J., Nishiya N., Imai S., Takano T., Oshimura M., and Nose K. Induction of senescence-like phenotypes by forced expression of hic-5, which encodes a novel LIM motif protein, in immortalized human fibroblasts. Mol. Cell. Biol. 17 (1997) 1224-1235
60. Shigenaga M.K., Hagen T.M., and B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci USA 91 (1994) 10771-10778
61. Sonna L.A., Gaffin S.L., Pratt R.E., Cullivan M.L., Angel K.C., and Lilly C.M. Effect of acute heat shock on gene expression by human peripheral blood mononuclear cells. J. Appl. Physiol. 92 (2002) 2208-2220
62. Toyohara H., Ito K., Ando M., Kinoshita M., Shimizu Y., and Sakaguchi M. Effect of maturation on activities of various proteases and protease inhibitors in the muscle of ayu (Plecoglossus altivelis). Comp. Biochem. B 99 (1991) 419-424
63. Van den Thillart G., and van Raaij M. Endogenous fuels: noninvasive versus invasive approaches. In: Hochachka P.W., and Mommsen T.P. (Eds). Biochemistry and Molecular Biology of Fishes vol. 4 (1995), Elsevier, Amsterdam 33-63
64. von Schalburg K.R., Rise M.L., Cooper G.A., Brown G.D., Gibbs R.A., Nelson C.C., Davidson W.S., and Koop B.F. Fish and chips: various methodologies demonstrate utility of a 16,006-gene salmonid microarray. BMC Genomics 6 1 (2005) 126
65. Walton M.J., and Cowey C.B. Aspects of intermediary metabolism in salmonid fish. Comp. Biochem. Physiol. B 73 (1982) 59-79
66. Wagner G.N., Hinch S.G., Kuchel L.J., Lotto A., Jones S.R.M., Patterson D.A., Macdonald J.S., Van Der Kraak G., Shrimpton M., English K.K., Larsson S., Cooke S.J., Healey M.C., and Farrell A.P. Metabolic rates and swimming performance of adult Fraser River sockeye salmon (Oncorhynchus nerka) after a controlled infection with Parvicapsula minibicornis. Can. J. Fish. Aquat. Sci. 62 (2005) 2124-2133
67. Weindruch R., and Walford R.L. The Retardation of Aging and Disease by Dietary Restriction (1988), Thomas, Springfield, IL 1988
68. Welle S., Brooks A.I., Delehanty J.M., Needler N., and Thornton C.A. Gene expression profile of aging in human muscle. Physiol. Genomics 13 (2003) 149-159
69. Wertheimer A.C., and Thrower F.P. Mortality rates of chum salmon during their initial marine residency. In: Grimes C.B., Brodeur R.D., Haldorson L.J., and McKinnell S.M. (Eds). Ecology of Juvenile Salmon in the Northeast Pacific Ocean: Regional Comparisons. Am. Fish. Soc. Symp. vol. 57 (2007), Bethesda, Maryland 233-247
70. Williams B. 2004 Southern salmon fishery post-season review. Part one: Fraser River sockeye report. Report for Canadian Minister of Fisheries and Oceans (2005) 1-91. http://www-comm.pac.dfo-%20mpo.gc.ca/publications/2004psr/williams_e.pdf (http://www-comm.pac.dfo-mpo.gc.ca/publications/2004psr/williams_e.pdf)
71. Yamashita M., and Konagaya S. High activities of cathepsins B, D, H and L in the white muscle of chum salmon in spawning migration. Comp. Biochem. Physiol. B 95 (1990) 149-152
72. Yang Y.H., Dudoit S., Luu P., Lin D.M., Peng V., Ngai J., and Speed T.P. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30 (2002) e15-e15