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Starvation Induced Alterations in Hepatic Lysine Metabolism in Different Families of Rainbow Trout (Oncorhynchus  mykiss)

Abstract

Lysine is the second limiting amino acid in fish meal based diets, second only to methionine. However, little is known about lysine metabolism in rainbow trout (RBT). Therefore, lysine catabolism by the lysine α-ketoglutarate reductase (LKR) pathway was studied. Additionally, since genetically improved strains could influence fish production, these studies were performed in 4 distinct families of RBT. Two full-sibling families, differing in feed efficiency, were selected from each of 2 strains (A and B) of RBT. Eight fish from each of the 4 families were allotted to individual tanks. Fish were fed until satiation for 5 weeks when four fish within each family were randomly selected for 2 weeks of starvation. After the starvation period, all fish were harvested. Hepatic in-vitro LKR activity and lysine oxidation were measured as was LKR mRNA. No effect of family within strain on LKR activity or lysine oxidation was detected. Strain A exhibited a 55% reduction (p < 0.01) in LKR transcripts compared to strain B pooled across both feeding levels. Within each family, LKR mRNA was decreased (p < 0.01) in starved vs. fed fish. On average, there was a 68% decrease in LKR transcripts for starved fish. LKR activity averaged 104 ± 33 and 150 ± 31 nmol/min*gm liver (p > 0.1) in fed and starved fish, respectively. Lysine oxidation averaged 1.2 ± 0.5 and 2.2 ± 0.4 nmol/min*gm liver (p > 0.1) in fed and starved fish, respectively. LKR transcripts were positively correlated to weight gain (p < 0.01). These data are consistent with multiple modes of LKR regulation in fish.

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Abbreviations

FCR:

Feed Conversion Ratio

LKR:

Lysine α-ketoglutarate reductase

LOX:

Lysine Oxidation

RBT:

Rainbow Trout

SACDH:

Saccharopine Dehydrogenase

References

  • K.P. Blemings T.D. Crenshaw N.J. Benevenga (1994) ArticleTitleLysine α-ketoglutarate reductase and saccharopine dehydrogenase are located only in the mitochondrial matrix in rat liver J. Nutr. 124 332–336

    Google Scholar 

  • K.P. Blemings T.D. Crenshaw N.J. Benevenga (1998) ArticleTitleMitochondrial lysine uptake limits lysine oxidation in rats fed diets containing 5, 20 or 60% casein J. Nutr. 128 2427–2434 Occurrence Handle1:CAS:528:DyaK1cXotVOru7o%3D Occurrence Handle9868191

    CAS  PubMed  Google Scholar 

  • H. Broquist (1991) ArticleTitleLysine-pipecolic acid metabolic relationships in microbes and mammals Annu. Rev. Nutr. 11 435–448 Occurrence Handle10.1146/annurev.nu.11.070191.002251 Occurrence Handle1:CAS:528:DyaK3MXlsFOlsbY%3D Occurrence Handle1909881

    Article  CAS  PubMed  Google Scholar 

  • Z.J. Cheng R.W. Hardy J.L. Ursy (2003a) ArticleTitleEffects of lysine supplementation in plant protein-based diets on the performance of rainbow trout (Oncorhynchus  mykiss) and apparent digestibility coefficients of nutrients Aquaculture 215 255–265 Occurrence Handle10.1016/S0044-8486(02)00166-7 Occurrence Handle1:CAS:528:DC%2BD38XosFCgtb0%3D

    Article  CAS  Google Scholar 

  • Z.J. Cheng R.W. Hardy J.L. Ursy (2003b) ArticleTitlePlant protein ingredients with lysine supplementation reduce dietary protein level in rainbow trout (Oncorhynchus  mykiss) diets, and reduce ammonia nitrogen and soluble phosphorus excretion Aquaculture 218 553–565 Occurrence Handle1:CAS:528:DC%2BD3sXht1Ggsr8%3D

    CAS  Google Scholar 

  • C.Y. Cho S.J. Kauchik (1990) ArticleTitleNutritional energetics in fish: energy and protein utilization in rainbow trout (Salmo  gairdneri) World Rev. Nutr. Diet. 61 132–172 Occurrence Handle1:STN:280:By%2BC2sjjtlw%3D Occurrence Handle2408253

    CAS  PubMed  Google Scholar 

  • S.W. Chu D.M. Hegsted (1976) ArticleTitleAdaptive response of lysine and threonine degrading enzymes in adult rats J. Nutr. 106 1089–1096 Occurrence Handle1:CAS:528:DyaE28Xlt1SksLw%3D Occurrence Handle939989

    CAS  PubMed  Google Scholar 

  • O. Emanuelsson H. Nielsen S. Brunak G. Heijne (2002) ArticleTitlePredicting subcellular localization of proteins based on their N-terminal amino acid sequence J. Mol. Biol. 300 1005–1016

    Google Scholar 

  • S. Epelbaum R. McDevitt S.C. Falco (1997) ArticleTitleLysine-ketoglutarate reductase and saccharopine dehydrogenase from Arabidopsis thaliana: nucleotide sequence and characterization Plant Mol. Bio. 35 735–748 Occurrence Handle1:CAS:528:DyaK1cXis1Ggtg%3D%3D

    CAS  Google Scholar 

  • A.R. Foster P.W.D. Scislowski I. Harris M.F. Fuller (1993) ArticleTitleMetabolic response of liver lysine α-ketoglutarate reductase activity in rats fed lysine limiting or lysine excessive diets Nutr. Res. 13 1433–1443 Occurrence Handle1:CAS:528:DyaK2cXisVeitLY%3D

    CAS  Google Scholar 

  • G.D. Foster T.W. Moon (1991) ArticleTitleHypometabolism with fasting in the yellow perch (Perca flavescens): A study of enzymes, hepatocyte metabolism, and tissue size Physiol. Zool. 64 259–275 Occurrence Handle1:CAS:528:DyaK3MXks1yrsb4%3D

    CAS  Google Scholar 

  • Gatlin, D.M. and Hardy, R.W. 2002. Manipulations of diets and feeding to reduce losses of nutrients in intensive aquaculture. In: Aquaculture and the Environment in the United States. pp. 155–165. Edited by J.R. Tomasso. World Aquaculture Society.

  • R.W. Hardy (1999) ArticleTitleAquaculture’s rapid growth requirements for alternate protein sources Feed Management 50 25–28

    Google Scholar 

  • A.E. Harper (1965) ArticleTitleEffect of variation in protein intake on enzymes of amino acid metabolism Can. J. Biochem. 43 1589–1603 Occurrence Handle1:CAS:528:DyaF2MXksFKksrg%3D Occurrence Handle4379380

    CAS  PubMed  Google Scholar 

  • J. Hutzler J. Dancis (1968) ArticleTitleConversion of lysine to saccharopine by human tissues Biochim. Biophys. Acta 158 62–69 Occurrence Handle1:CAS:528:DyaF1cXhtVajs7c%3D Occurrence Handle4385118

    CAS  PubMed  Google Scholar 

  • A.S. Kiess B.M. Stinefelt C.M. Cantrell A.D. Higgins M.E. Wilson H. Klandorf K.P. Blemings (2004) ArticleTitleRegulation of hepatic lysine α-ketoglutarate reductase in mice fed high or adequate protein diets FASEB J. 18 A539

    Google Scholar 

  • K.I. Kim T.W. Grimshaw T.B. Kayes H.A. Clyde (1992) ArticleTitleEffect of fasting or feeding diets containing different levels of protein or amino acids on the activities of the liver amino acid-degrading enzymes and amino acid oxidation in rainbow trout (Oncorhynchus  mykiss) Aquaculture 107 89–105 Occurrence Handle10.1016/0044-8486(92)90052-M Occurrence Handle1:CAS:528:DyaK3sXlvVKjsg%3D%3D

    Article  CAS  Google Scholar 

  • K.I. Kim T.B. Kayes C.H. Amundson (1991) ArticleTitlePurified diet development and re-evaluation of the dietary protein requirement of fingerling rainbow trout (Oncorhynchus  mykiss) Aquaculture 96 57–67 Occurrence Handle10.1016/0044-8486(91)90139-X Occurrence Handle1:CAS:528:DyaK3MXmsFCru7c%3D

    Article  CAS  Google Scholar 

  • D. Miron S. Ben-Yaacov H. Karchi G. Galili (1997) ArticleTitleIn vitro dephosporylation inhibits the activity of soybean lysine-ketoglutarate reductase in a lysine-regulated manner The Plant J. 12 1453–1458 Occurrence Handle1:CAS:528:DyaK1cXlvVWhsQ%3D%3D

    CAS  Google Scholar 

  • C. Noda A. Ichirara (1978) ArticleTitlePurification and properties of l-lysine alpha-ketoglutarate reducatase from rat liver mitochondria Bioch. Biophy. Acta 525 307–313 Occurrence Handle1:CAS:528:DyaE1cXlsVansL4%3D

    CAS  Google Scholar 

  • F. Papes E.D. Kemper G. Cord-Neto F. Langone P. Arruda (1999) ArticleTitleLysine degradation through the saccharopine pathway in mammals: involvement of both bifunctional and monofunctional lysine degrading enzymes in mouse Biochem. J. 344 555–563 Occurrence Handle10.1042/0264-6021:3440555 Occurrence Handle1:CAS:528:DC%2BD3cXltFyj Occurrence Handle10567240

    Article  CAS  PubMed  Google Scholar 

  • M.W. Pfaffl (2001) ArticleTitleA new mathematical model for relative quantification in real-time RT-PCR Nuc. Acids Res. 29 2002–2007

    Google Scholar 

  • A.L. Pierce J.T. Dickey D.A. Larsen H. Fukada P. Swanson W.W. Dickhoff (2004) ArticleTitleA quantitative real-time RT-PCR assay for salmon IGF-I mRNA, and its application in the study of GH regulation of IGF-I gene expression in primary culture of salmon heptocytes Gen. Comp. Endrocrinol. 135 401–411 Occurrence Handle1:CAS:528:DC%2BD2cXjtVChsg%3D%3D

    CAS  Google Scholar 

  • M. Rodehutscord S. Mandel E. Pfeffer (1994) ArticleTitleReduced protein content and use of wheat gluten in diets for rainbow trout: effects on water loading with N and P J. Appl. Ichthyol. 10 271–273 Occurrence Handle1:CAS:528:DyaK2MXmtFylur4%3D

    CAS  Google Scholar 

  • Y.C. Shang J. Tomasso (1990) Aquaculture Economic Analysis: An Introduction The World Aquaculture Society Baton Rouge

    Google Scholar 

  • J.T. Silverstein (2004) ArticleTitleUsing genetic variation to understand control of feed intake in fish Fish Physiol. Biochem. 27 173–178

    Google Scholar 

  • J.T. Silverstein M. Hostuttler K.P. Blemings (2005) ArticleTitleStrain difference in feed efficiency measured as residual feed intake in individually reared rainbow trout, Oncorhynchus  mykiss (Walbaum) Aquac. Res. 36 704–711 Occurrence Handle10.1111/j.1365-2109.2005.01278.x

    Article  Google Scholar 

  • N. Torres L. Martinez G. Aleman H. Bourges A.R. Tovar (1998) ArticleTitleHistidase expression is regulated by dietary protein at the pretranslational level in rat liver J. Nutr. 128 818–824 Occurrence Handle1:CAS:528:DyaK1cXjtFegsrk%3D Occurrence Handle9566987

    CAS  PubMed  Google Scholar 

  • S. Viola E. Lahav (1991) ArticleTitleEffects of lysine supplementation in practical carp feeds on total protein sparing and reduction in pollution Isr. J. Aquac.-Bamidgen 43 112–118

    Google Scholar 

  • S. Viola E. Lahav H. Angeoni (1992) ArticleTitleReduction of feed protein levels and of nitrogenous N-excretions by lysine supplementation in intensive carp culture Aquat. Living Resour. 5 277–285

    Google Scholar 

  • M.J. Walton C.B. Cowey J.W. Adron (1984) ArticleTitleThe effect of dietary lysine levels on growth and metabolism of rainbow trout (Salmo  gairdneri) Brit. J. Nutr. 52 115–122 Occurrence Handle10.1079/BJN19840077 Occurrence Handle1:CAS:528:DyaL2cXkvV2ntr0%3D Occurrence Handle6430341

    Article  CAS  PubMed  Google Scholar 

  • S.H. Wang L.O. Crosby M.C. Nesheim (1973) ArticleTitleEffect of dietary excesses of lysine and arginine on the degradation of lysine by chicks J. Nutr. 103 384–391 Occurrence Handle1:CAS:528:DyaE3sXht1ejtL8%3D Occurrence Handle4688150

    CAS  PubMed  Google Scholar 

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Correspondence to Kenneth P. Blemings.

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Higgins, A.D., Silverstein, J.T., Engles, J. et al. Starvation Induced Alterations in Hepatic Lysine Metabolism in Different Families of Rainbow Trout (Oncorhynchus  mykiss). Fish Physiol Biochem 31, 33–44 (2005). https://doi.org/10.1007/s10695-005-4587-1

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  • DOI: https://doi.org/10.1007/s10695-005-4587-1

Keywords

  • feed efficiency
  • lysine
  • lysine α-ketoglutarate reductase
  • rainbow trout