title: Expression of heat shock protein (Hsp90) paralogues is regulated by amino acids in skeletal muscle of Atlantic salmon.
abstract: Heat shock proteins 90 (Hsp90) have an essential role in sarcomere formation and differentiation in skeletal muscle and also act as molecular chaperones during protein folding impacting a wide range of physiological processes. We characterised and provided a phylogenetically consistent nomenclature for the complete repertoire of six Hsp90 paralogues present in duplicated salmonid fish genomes (Hsp90α1a, Hsp90α1b, Hsp90α2a, Hsp90α2b, Hsp90ß1a and Hsp90ß1b). The expression of paralogues in fast skeletal muscle was investigated using in vivo fasting-feeding experiments and primary myogenic cultures. Fasted juvenile Atlantic salmon (Salmo salar) showed a transient 2 to 8-fold increase in the expression of all 4 Hsp90α paralogues within 24h of satiation feeding. Hsp90α1a and hsp90α1b also showed a pronounced secondary increase in expression after 10 days, concomitant with muscle differentiation and the expression of myogenin and sarcomeric proteins (mlc2, myhc). Hsp90ß1b was constitutively expressed whereas Hsp90ß1a expression was downregulated 10-fold between fasted and fed individuals. Hsp90α1a and Hsp90α1b were upregulated 10 to 15-fold concomitant with myotube formation and muscle differentiation in vitro whereas other Hsp90 paralogues showed no change in expression. In cells starved of amino acid (AA) and serum for 72h the addition of AA, but not insulin-like growth factor 1, increased phosphorylation of mTor and expression of all 4 hsp90α paralogues and associated co-chaperones including hsp30, tbcb, pdia4, pdia6, stga and fk504bp1, indicating a general activation of the protein folding response. In contrast, Hsp90ß1a expression in vitro was unresponsive to AA treatment indicating that some other as yet uncharacterised signal(s) regulate its expression in response to altered nutritional state.
authors.affiliation: Scottish Oceans Institute, School of Biology, University of St Andrews, Fife, Scotland, United Kingdom.
authors.forename: Daniel
authors.initials: D
authors.lastname: Garcia de la Serrana
authors.forename: Ian A
authors.initials: IA
authors.lastname: Johnston
mesh_terms: D000596:Amino Acids / Q000378:metabolism* / Q000494:pharmacology; D000818:Animals; D004435:Eating; D005215:Fasting; D018507:Gene Expression Regulation, Developmental; D018841:HSP90 Heat-Shock Proteins / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D006801:Humans; D007334:Insulin-Like Growth Factor I / Q000235:genetics / Q000378:metabolism; D009024:Morphogenesis / Q000235:genetics; D018485:Muscle Fibers, Skeletal / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D018482:Muscle, Skeletal / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D010766:Phosphorylation; D010802:Phylogeny; D020033:Protein Isoforms / Q000145:classification / Q000235:genetics / Q000378:metabolism; D020317:Salmo salar / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D015398:Signal Transduction; D058570:TOR Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism
chemical_list: D000596:Amino Acids; D018841:HSP90 Heat-Shock Proteins; D020033:Protein Isoforms; D007334:Insulin-Like Growth Factor I; D058570:TOR Serine-Threonine Kinases
references.citation: Annu Rev Biochem. 2006;75:271-94
references.pmid: 16756493
references.citation: Mol Biol Evol. 2010 Aug;27(8):1759-67
references.pmid: 20207713
references.citation: Gene. 2002 Aug 7;295(2):173-83
references.pmid: 12354651
references.citation: Am J Physiol Regul Integr Comp Physiol. 2010 Jun;298(6):R1615-26
references.pmid: 20375265
references.citation: Biochim Biophys Acta. 2012 Mar;1823(3):624-35
references.pmid: 21951723
references.citation: Exp Cell Res. 2005 Jul 1;307(1):212-23
references.pmid: 15922741
references.citation: BMC Genomics. 2006 Jun 17;7:156
references.pmid: 16780600
references.citation: Cancer Res. 2008 Jan 15;68(2):589-96
references.pmid: 18199556
references.citation: J Eukaryot Microbiol. 2004 May-Jun;51(3):364-73
references.pmid: 15218707
references.citation: Biochem Biophys Res Commun. 1994 Oct 28;204(2):746-52
references.pmid: 7980538
references.citation: Clin Chem. 2009 Apr;55(4):611-22
references.pmid: 19246619
references.citation: Genome Biol. 2002 Jun 18;3(7):RESEARCH0034
references.pmid: 12184808
references.citation: J Biol Chem. 2008 May 9;283(19):13185-93
references.pmid: 18326487
references.citation: Proc Natl Acad Sci U S A. 2008 Jan 15;105(2):554-9
references.pmid: 18182494
references.citation: J Proteomics. 2012 Jun 6;75(10):2790-802
references.pmid: 22236519
references.citation: Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W385-8
references.pmid: 16845033
references.citation: Nat Cell Biol. 2001 Nov;3(11):1009-13
references.pmid: 11715022
references.citation: Dev Biol. 1999 Jun 1;210(1):56-70
references.pmid: 10364427
references.citation: PLoS One. 2012;7(6):e39679
references.pmid: 22768106
references.citation: BMC Genomics. 2007 Nov 28;8:438
references.pmid: 18045468
references.citation: Mol Biol Evol. 2011 Oct;28(10):2731-9
references.pmid: 21546353
references.citation: PLoS One. 2010 Jun 14;5(6):e11100
references.pmid: 20559434
references.citation: Mol Nutr Food Res. 2008 Apr;52(4):393-9
references.pmid: 18306429
references.citation: EMBO J. 2004 Feb 11;23(3):511-9
references.pmid: 14739935
references.citation: Biochim Biophys Acta. 2012 Mar;1823(3):607-13
references.pmid: 22008467
references.citation: Genome Res. 2009 Aug;19(8):1497-505
references.pmid: 19465509
references.citation: Development. 2008 Mar;135(6):1147-56
references.pmid: 18256191
references.citation: FEBS J. 2007 Sep;274(17):4453-63
references.pmid: 17681020
references.citation: Fish Shellfish Immunol. 2012 Jul;33(1):42-7
references.pmid: 22510210
references.citation: J Biol Chem. 1997 Aug 22;272(34):21213-20
references.pmid: 9261129
references.citation: PLoS One. 2012;7(12):e51884
references.pmid: 23284803
references.citation: J Exp Biol. 2011 Jul 1;214(Pt 13):2125-39
references.pmid: 21653807
references.citation: Cell Signal. 2005 Dec;17(12):1477-85
references.pmid: 15935620
references.citation: Physiol Genomics. 2010 Oct;42A(2):114-30
references.pmid: 20663983
references.citation: Dev Biol. 2007 Mar 15;303(2):483-92
references.pmid: 17189627
references.citation: Proc Natl Acad Sci U S A. 2008 Jan 22;105(3):950-4
references.pmid: 18199840
references.citation: J Mol Biol. 2012 Jan 6;415(1):3-15
references.pmid: 22063096
references.citation: J Biol Chem. 2009 Feb 6;284(6):3885-96
references.pmid: 19073599
references.citation: Gene. 2008 Jun 15;416(1-2):77-84
references.pmid: 18442885
references.citation: Br J Nutr. 2012 Dec 28;108(12):2148-57
references.pmid: 22464448