Skip to main content

Advertisement

Log in

Changes in Liver Proteome Expression of Senegalese Sole (Solea senegalensis) in Response to Repeated Handling Stress

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The Senegalese sole, a high-value flatfish, is a good candidate for aquaculture production. Nevertheless, there are still issues regarding this species’ sensitivity to stress in captivity. We aimed to characterize the hepatic proteome expression for this species in response to repeated handling and identify potential molecular markers that indicate a physiological response to chronic stress. Two groups of fish were reared in duplicate for 28 days, one of them weekly exposed to handling stress (including hypoxia) for 3 min, and the other left undisturbed. Two-dimensional electrophoresis enabled the detection of 287 spots significantly affected by repeated handling stress (Wilcoxon–Mann–Whitney U test, p < 0.05), 33 of which could be reliably identified by peptide mass spectrometry. Chronic exposure to stress seems to have affected protein synthesis, folding and turnover (40S ribosomal protein S12, cathepsin B, disulfide-isomerase A3 precursor, cell-division cycle 48, and five distinct heat shock proteins), amino acid metabolism, urea cycle and methylation/folate pathways (methionine adenosyltransferase I α, phenylalanine hydroxylase, mitochondrial agmatinase, serine hydroxymethyltransferase, 3-hydroxyanthranilate 3,4-dioxygenase, and betaine homocysteine methyltransferase), cytoskeletal (40S ribosomal protein SA, α-actin, β-actin, α-tubulin, and cytokeratin K18), aldehyde detoxification (aldehyde dehydrogenase 4A1 family and aldehyde dehydrogenase 7A1 family), carbohydrate metabolism and energy homeostasis (fatty acid-binding protein, enolase 3, enolase 1, phosphoglycerate kinase, glyceraldehyde-3-phosphate dehydrogenase, aconitase 1, mitochondrial ATP synthase α-subunit, and electron-transfer flavoprotein α polypeptide), iron and selenium homeostasis (transferrin and selenium binding protein 1), steroid hormone metabolism (3-oxo-5-β-steroid 4-dehydrogenase), and purine salvage (hypoxanthine phosphoribosyltransferase). Further characterization is required to fully assess the potential of these markers for the monitoring of fish stress response to chronic stressors of aquaculture environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Acerete L, Balasch JC, Espinosa E, Josa A, Tort L (2004) Physiological responses in Eurasian perch (Perca fluviatilis, L.) subjected to stress by transport and handling. Aquaculture 237:167–178

    Article  CAS  Google Scholar 

  • Ali KS, Dorgai L, Abraham M, Hermesz E (2003) Tissue- and stressor-specific differential expression of two hsc70 genes in carp. Biochem Bioph Res Co 307:503–509

    Article  CAS  Google Scholar 

  • Allani PK, Sum T, Bhansali SG, Mukherjee SK, Sonee M (2004) A comparative study of the effect of oxidative stress on the cytoskeleton in human cortical neurons. Toxicol Appl Pharm 196:29–36

    Article  CAS  Google Scholar 

  • Alves RN, Cordeiro O, Silva TS, Richard N, De Vareilles M, Marino G, Di Marco P, Rodrigues PM, Conceicao LEC (2010) Metabolic molecular indicators of chronic stress in gilthead seabream (Sparus aurata) using comparative proteomics. Aquaculture 299:57–66

    Article  CAS  Google Scholar 

  • Aragao C, Corte-Real J, Costas B, Dinis MT, Conceicao LE (2008) Stress response and changes in amino acid requirements in Senegalese sole (Solea senegalensis Kaup 1858). Amino Acids 34:143–148

    Article  PubMed  CAS  Google Scholar 

  • Ardini E, Pesole G, Tagliabue E, Magnifico A, Castronovo V, Sobel ME, Colnaghi MI, Menard S (1998) The 67-kDa laminin receptor originated from a ribosomal protein that acquired a dual function during evolution. Mol Biol Evol 15:1017–1025

    Article  PubMed  CAS  Google Scholar 

  • Arends RJ, Mancera JM, Munoz JL, Bonga SEW, Flik G (1999) The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J Endocrinol 163:149–157

    Article  PubMed  CAS  Google Scholar 

  • Arjona FJ, Vargas-Chacoff L, Ruiz-Jarabo I, Goncalves O, Pascoa I, Del Rio MPM, Mancera JM (2009) Tertiary stress responses in Senegalese sole (Solea senegalensis Kaup, 1858) to osmotic challenge: implications for osmoregulation, energy metabolism and growth. Aquaculture 287:419–426

    Article  Google Scholar 

  • Ashley PJ (2007) Fish welfare: current issues in aquaculture. Appl Anim Behav Sci 104:199–235

    Article  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525

    Article  PubMed  CAS  Google Scholar 

  • Barton BA, Ribas L, Acerete L, Tort L (2005) Effects of chronic confinement on physiological responses of juvenile gilthead sea bream, Sparus aurata L., to acute handling. Aquac Res 36:172–179

    Article  Google Scholar 

  • Baskin-Bey ES, Canbay A, Bronk SF, Werneburg N, Guicciardi ME, Nyberg SL, Gores GJ (2005) Cathepsin B inactivation attenuates hepatocyte apoptosis and liver damage in steatotic livers after cold ischemia-warm reperfusion injury. Am J Physiol Gastrointest Liver Physiol 288:G396–G402

    Article  PubMed  CAS  Google Scholar 

  • Baumeister P, Luo SZ, Skarnes WC, Sui GC, Seto E, Shi Y, Lee AS (2005) Endoplasmic reticulum stress induction of the Grp78/BiP promoter: activating mechanisms mediated by YY1 and its interactive chromatin modifiers. Mol Cell Biol 25:4529–4540

    Article  PubMed  CAS  Google Scholar 

  • Becker B, Vogt T, Landthaler M, Stolz W (2001) Detection of differentially regulated genes in keratinocytes by cDNA array hybridization: Hsp27 and other novel players in response to artificial ultraviolet radiation. J Invest Dermatol 116:983–988

    Article  PubMed  CAS  Google Scholar 

  • Biswas AK, Seoka M, Takii K, Maita M, Kumai H (2006) Stress response of red sea bream Pagrus major to acute handling and chronic photoperiod manipulation. Aquaculture 252:566–572

    Article  CAS  Google Scholar 

  • Bomford AB, Munro HN (1985) Transferrin and its receptor—their roles in cell-function. Hepatology 5:870–875

    Article  PubMed  CAS  Google Scholar 

  • Bosutti A, Toigo G, Ciocchi B, Situlin R, Guarnieri G, Biolo G (2002) Regulation of muscle cathepsin B proteolytic activity in protein-depleted patients with chronic diseases. Clin Nutr 21:373–378

    Article  PubMed  CAS  Google Scholar 

  • Broker LE, Huisman C, Span SW, Rodriguez JA, Kruyt FAE, Giaccone G (2004) Cathepsin B mediates caspase-independent cell death induced by microtubule stabilizing agents in non-small cell lung cancer cells. Cancer Res 64:27–30

    Article  PubMed  Google Scholar 

  • Broom DM (1998) Welfare, stress, and the evolution of feelings. Adv Stud Behav 27:371–403

    Article  Google Scholar 

  • Campenhout AV, Van Campenhout CM, Lagrou AR, Keenoy BMY (2003) Transferrin modifications and lipid peroxidation: implications in diabetes mellitus. Free Radical Res 37:1069–1077

    Article  CAS  Google Scholar 

  • Cao K, Nakajima R, Meyer HH, Zheng YX (2003) The AAA-ATPase Cdc48/p97 regulates spindle disassembly at the end of mitosis. Cell 115:355–367

    Article  PubMed  CAS  Google Scholar 

  • Chi NC, Karliner JS (2004) Molecular determinants of responses to myocardial ischemia/reperfusion injury: focus on hypoxia-inducible and heat shock factors. Cardiovasc Res 61:437–447

    Article  PubMed  CAS  Google Scholar 

  • Christensen KE, Mackenzie RE (2006) Mitochondrial one-carbon metabolism is adapted to the specific needs of yeast, plants and mammals. Bioessays 28:595–605

    Article  PubMed  CAS  Google Scholar 

  • Conceicao LEC, Ribeiro L, Engrola S, Aragao C, Morais S, Lacuisse M, Soares F, Dinis MT (2007) Nutritional physiology during development of Senegalese sole (Solea senegalensis). Aquaculture 268:64–81

    Article  CAS  Google Scholar 

  • Conte FS (2004) Stress and the welfare of cultured fish. Appl Anim Behav Sci 86:205–223

    Article  Google Scholar 

  • Costa PM, Chicano-Galvez E, Lopez Barea J, Delvalls TA, Costa MH (2010) Alterations to proteome and tissue recovery responses in fish liver caused by a short-term combination treatment with cadmium and benzo[a]pyrene. Environ Pollut 158:3338–3346

    Article  PubMed  CAS  Google Scholar 

  • Costas B (2012) Stress mitigation in sole (Solea senegalensis) through improved nitrogen nutrition: disease resistance, amino acid utilization and immune status (in press)

  • Costas B, Aragao C, Mancera JM, Dinis MT, Conceicao LEC (2008) High stocking density induces crowding stress and affects amino acid metabolism in Senegalese sole Solea senegalensis (Kaup 1858) juveniles. Aquac Res 39:1–9

    Article  CAS  Google Scholar 

  • Cowan ML, Vera J (2008) Proteomics: advances in biomarker discovery. Expert Rev Proteomics 5:21–23

    Article  PubMed  CAS  Google Scholar 

  • Da Conceicao LEC, Aragao C, Richard N, Engrola S, Gavaia P, Mira S, Dias J (2009) Recent advances in nutrition of fish larval. Revista Brasileira De Zootecnia-Brazilian J Anim Sci 38:26–35

    Article  Google Scholar 

  • Demianova M, Formosa TG, Ellis SR (1996) Yeast proteins related to the p40/laminin receptor precursor are essential components of the 40 S ribosomal subunit. J Biol Chem 271:11383–11391

    Article  PubMed  CAS  Google Scholar 

  • Deocaris CC, Kaul SC, Wadhwa R (2006) On the brotherhood of the mitochondrial chaperones mortalin and heat shock protein 60. Cell Stress Chaperon 11:116–128

    Article  CAS  Google Scholar 

  • Dinis MT, Ribeiro L, Soares F, Sarasquete C (1999) A review on the cultivation potential of Solea senegalensis in Spain and in Portugal. Aquaculture 176:27–38

    Article  Google Scholar 

  • Drew RE, Rodnick KJ, Settles M, Wacyk J, Churchill E, Powell MS, Hardy RW, Murdoch GK, Hill RA, Robison BD (2008) Effect of starvation on transcriptomes of brain and liver in adult female zebrafish (Danio rerio). Physiol Genomics 35:283–295

    Article  PubMed  CAS  Google Scholar 

  • Eigler N, Sacca L, Sherwin RS (1979) Synergistic interactions of physiologic increments of glucagon, epinephrine, and cortisol in the dog—model for stress-induced hyperglycemia. J Clin Invest 63:114–123

    Article  PubMed  CAS  Google Scholar 

  • Engrola S, Conceicao LEC, Dias L, Pereira R, Ribeiro L, Dinis MT (2007) Improving weaning strategies for Senegalese sole: effects of body weight and digestive capacity. Aquacult Res 38:696–707

    Article  Google Scholar 

  • Falsone SF, Gesslbauer B, Tirk F, Piccinini AM, Kungl AJ (2005) A proteomic snapshot of the human heat shock protein 90 interactome. FEBS Lett 579:6350–6354

    Article  PubMed  CAS  Google Scholar 

  • Firth JD, Ebert BL, Pugh CW, Ratcliffe PJ (1994) Oxygen-regulated control elements in the phosphoglycerate kinase-1 and lactate-dehydrogenase-a genes—similarities with the erythropoietin 3′ enhancer. P Natl Acad Sci USA 91:6496–6500

    Article  CAS  Google Scholar 

  • Fong WP, Cheng CHK, Tang WK (2006) Antiquitin, a relatively unexplored member in the superfamily of aldehyde dehydrogenases with diversified physiological functions. Cell Mol Life Sci 63:2881–2885

    Article  PubMed  CAS  Google Scholar 

  • Fujimura Y, Umeda D, Kiyohara Y, Sunada Y, Yamada K, Tachibana H (2006) The involvement of the 67 kDa laminin receptor-mediated modulation of cytoskeleton in the degranulation inhibition induced by epigallocatechin-3-O-gallate. Biochem Biophys Res Commun 348:524–531

    Article  PubMed  CAS  Google Scholar 

  • Gnaiger E (ed) (2007) Mitochondrial pathways and respiratory control. OROBOROS MiPNet Publications, Innsbruck

    Google Scholar 

  • Gobom J, Nordhoff E, Mirgorodskaya E, Ekman R, Roepstorff P (1999) Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J Mass Spectrom 34:105–116

    Article  PubMed  CAS  Google Scholar 

  • Gomme PT, Mccann KB (2005) Transferrin: structure, function and potential therapeutic actions. Drug Discov Today 10:267–273

    Article  PubMed  CAS  Google Scholar 

  • Guicciardi ME, Deussing J, Miyoshi H, Bronk SF, Svingen PA, Peters C, Kaufmann SH, Gores GJ (2000) Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J Clin Invest 106:1127–1137

    Article  PubMed  CAS  Google Scholar 

  • Guicciardi ME, Miyoshi H, Bronk SF, Gores GJ (2001) Cathepsin B knockout mice are resistant to tumor necrosis factor-alpha-mediated hepatocyte apoptosis and liver injury: implications for therapeutic applications. Am J Pathol 159:2045–2054

    Article  PubMed  CAS  Google Scholar 

  • Gutteridge JMC, Quinlan GJ (1993) Antioxidant protection against organic and inorganic oxygen radicals by normal human plasma—the important primary role for iron-binding and iron-oxidizing proteins. Biochim Biophys Acta 1156:144–150

    Article  PubMed  CAS  Google Scholar 

  • Hartl FU, Martin J, Neupert W (1992) Protein folding in the cell—the role of molecular chaperones Hsp70 and Hsp60. Annu Rev Bioph Biom 21:293–322

    Article  CAS  Google Scholar 

  • Hatahet F, Ruddock LW (2007) Substrate recognition by the protein disulfide isomerases. FEBS J 274:5223–5234

    Article  PubMed  CAS  Google Scholar 

  • Imsland AK, Foss A, Conceicao LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P (2003) A review of the culture potential of Solea solea and S-senegalensis. Rev Fish Biol Fisher 13:379–407

    Article  Google Scholar 

  • Inada H, Izawa I, Nishizawa M, Fujita E, Kiyono T, Takahashi T, Momoi T, Inagaki M (2001) Keratin attenuates tumor necrosis factor-induced cytotoxicity through association with TRADD. J Cell Biol 155:415–425

    Article  PubMed  CAS  Google Scholar 

  • Iwama GK, Vijayan MM, Forsyth RB, Ackerman PA (1999) Heat shock proteins and physiological stress in fish. Am Zool 39:901–909

    CAS  Google Scholar 

  • Iwama GK, Afonso LOB, Todgham A, Ackerman P, Nakano K (2004) Are HSPs suitable for indicating stressed states in fish? J Exp Biol 207:15–19

    Article  PubMed  CAS  Google Scholar 

  • Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperon 14:105–111

    Article  CAS  Google Scholar 

  • Kelly KJ (2005) Heat shock (stress response) proteins and renal ischemia/reperfusion injury. Contrib Nephrol 148:86–106

    Article  PubMed  CAS  Google Scholar 

  • Kondo KH, Kai MH, Setoguchi Y, Eggertsen G, Sjoblom P, Setoguchi T, Okuda KI, Bjorkhem I (1994) Cloning and expression of cDNA of human delta 4-3-oxosteroid 5 beta-reductase and substrate specificity of the expressed enzyme. Eur J Biochem 219:357–363

    Article  PubMed  CAS  Google Scholar 

  • Kozutsumi Y, Segal M, Normington K, Gething MJ, Sambrook J (1988) The presence of malfolded proteins in the endoplasmic-reticulum signals the induction of glucose-regulated proteins. Nature 332:462–464

    Article  PubMed  CAS  Google Scholar 

  • Langer T, Neupert W (1991) Heat-shock proteins Hsp60 and Hsp70—their roles in folding, assembly and membrane translocation of proteins. Curr Top Microbiol 167:3–30

    Article  CAS  Google Scholar 

  • Lecavalier L, Bolli G, Gerich J (1990) Glucagon-cortisol interactions on glucose-turnover and lactate gluconeogenesis in normal humans. Am J Physiol 258:E569–E575

    PubMed  CAS  Google Scholar 

  • Lee AS (2005) The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35:373–381

    Article  PubMed  CAS  Google Scholar 

  • Li H, Ko HP, Whitlock JP (1996) Induction of phosphoglycerate kinase 1 gene expression by hypoxia—roles of Arnt and HIF1 alpha. J Biol Chem 271:21262–21267

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Yang Q, Radhakrishnan K, Whitfield DE, Everhart CL, Parsons-Wingerter P, Fisher SA (2009) Role of VEGF and tissue hypoxia in patterning of neural and vascular cells recruited to the embryonic heart. Dev Dyn 238:2760–2769

    Article  PubMed  CAS  Google Scholar 

  • Lopez JL (2007) Two-dimensional electrophoresis in proteome expression analysis. J Chromatogr B 849:190–202

    Article  CAS  Google Scholar 

  • Luders J, Demand J, Hohfeld J (2000) The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J Biol Chem 275:4613–4617

    Article  PubMed  CAS  Google Scholar 

  • Madsen L, Seeger M, Semple CA, Hartmann-Petersen R (2009) New ATPase regulators—p97 goes to the PUB. Int J Biochem Cell Biol 41:2380–2388

    Article  PubMed  CAS  Google Scholar 

  • Martin SAM, Cash P, Blaney S, Houlihan DF (2001) Proteome analysis of rainbow trout (Oncorhynchus mykiss) liver proteins during short term starvation. Fish Physiol Biochem 24:259–270

    Article  CAS  Google Scholar 

  • Mato JM, Lu SC (2007) Role of S-adenosyl-l-methionine in liver health and injury. Hepatology 45:1306–1312

    Article  PubMed  CAS  Google Scholar 

  • Mato JM, Corrales FJ, Lu SC, Avila MA (2002) S-adenosylmethionine: a control switch that regulates liver function. FASEB J 16:15–26

    Article  PubMed  CAS  Google Scholar 

  • Meneghini R (1997) Iron homeostasis, oxidative stress, and DNA damage. Free Radical Bio Med 23:783–792

    Article  CAS  Google Scholar 

  • Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp PCC 6803. Mol Microbiol 46:905–915

    Article  PubMed  CAS  Google Scholar 

  • Miller EK, Raese JD, Morrisonbogorad M (1991) Expression of heat-shock protein-70 and heat-shock cognate-70 messenger-RNAs in rat cortex and cerebellum after heat-shock or amphetamine treatment. J Neurochem 56:2060–2071

    Article  PubMed  CAS  Google Scholar 

  • Mirabelli F, Salis A, Vairetti M, Bellomo G, Thor H, Orrenius S (1989) Cytoskeletal alterations in human-platelets exposed to oxidative stress are mediated by oxidative and Ca2+-dependent mechanisms. Arch Biochem Biophys 270:478–488

    Article  PubMed  CAS  Google Scholar 

  • Miwa S, Brand MD (2003) Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling. Biochem Soc Trans 31:1300–1301

    Article  PubMed  CAS  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fisher 9:211–268

    Article  Google Scholar 

  • Montero D, Izquierdo MS, Tort L, Robaina L, Vergara JM (1999) High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata, juveniles. Fish Physiol Biochem 20:53–60

    Article  CAS  Google Scholar 

  • Morgan MY, Milsom JP, Sherlock S (1978) Plasma ratio of valine, leucine and isoleucine to phenylalanine and tyrosine in liver-disease. Gut 19:1068–1073

    Article  PubMed  CAS  Google Scholar 

  • Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, Clay J, Folke C, Lubchenco J, Mooney H, Troell M (2000) Effect of aquaculture on world fish supplies. Nature 405:1017–1024

    Article  PubMed  CAS  Google Scholar 

  • Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M, Farrell AP, Forster I, Gatlin DM, Goldburg RJ, Hua K, Nichols PD (2009) Feeding aquaculture in an era of finite resources. Proc Natl Acad Sci U S A 106:15103–15110

    Article  PubMed  CAS  Google Scholar 

  • Nijhout HF, Reed MC, Lam SL, Shane B, Gregory JF 3rd, Ulrich CM (2006) In silico experimentation with a model of hepatic mitochondrial folate metabolism. Theor Biol Med Model 3:40

    Article  PubMed  CAS  Google Scholar 

  • Nishizawa J, Nakai A, Higashi T, Tanabe M, Nomoto S, Matsuda K, Ban T, Nagata K (1996) Reperfusion causes significant activation of heat shock transcription factor 1 in ischemic rat heart. Circulation 94:2185–2192

    Article  PubMed  CAS  Google Scholar 

  • Ochi A, Hori H (2007) Hydroxyl radical probing of tRNA (Gm18) methyltransferase [TrmH]-AdoMet-artificial tRNA ternary complex. Nucleic Acids Symp Ser (Oxf) 373374

  • Paquet C, Sane AT, Beauchemin M, Bertrand R (2005) Caspase- and mitochondrial dysfunction-dependent mechanisms of lysosomal leakage and cathepsin B activation in DNA damage-induced apoptosis. Leukemia 19:784–791

    Article  PubMed  CAS  Google Scholar 

  • Perez LM, Milkiewicz P, Ahmed-Choudhury J, Elias E, Ochoa JE, Pozzi EJS, Coleman R, Roma MG (2006) Oxidative stress induces actin-cyto skeletal and tight-junctional alterations in hepatocytes by a Ca2+-dependent, PKC-mediated mechanism: protective effect of PKA. Free Radical Bio Med 40:2005–2017

    Article  CAS  Google Scholar 

  • Peri S, Steen H, Pandey A (2001) GPMAW—a software tool for analyzing proteins and peptides. Trends Biochem Sci 26:687–689

    Article  PubMed  CAS  Google Scholar 

  • Prentice HM, Milton SL, Scheurle D, Lutz PL (2004) The upregulation of cognate and inducible heat shock proteins in the anoxic turtle brain. J Cerebr Blood F Met 24:826–828

    Article  CAS  Google Scholar 

  • Rivera RE, Christensen VL, Edens FW, Wineland MJ (2005) Influence of selenium on heat shock protein 70 expression in heat stressed turkey embryos (Meleagris gallopavo). Comp Biochem Physiol A Mol Integr Physiol 142:427–432

    Article  PubMed  CAS  Google Scholar 

  • Rockett JC, Mapp FL, Garges JB, Luft JC, Mori C, Dix DJ (2001) Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice. Biol Reprod 65:229–239

    Article  PubMed  CAS  Google Scholar 

  • Rotllant J, Balm PHM, Perez-Sanchez J, Wendelaar-Bonga SE, Tort L (2001) Pituitary and interrenal function in gilthead sea bream (Sparus aurata L., Teleostei) after handling and confinement stress. Gen Comp Endocr 121:333–342

    Article  PubMed  CAS  Google Scholar 

  • Satriano J, Matsufuji S, Murakami Y, Lortie MJ, Schwartz D, Kelly CJ, Hayashi S, Blantz RC (1998) Agmatine suppresses proliferation by frameshift induction of antizyme and attenuation of cellular polyamine levels. J Biol Chem 273:15313–15316

    Article  PubMed  CAS  Google Scholar 

  • Schuberth C, Buchberger A (2008) UBX domain proteins: major regulators of the AAA ATPase Cdc48/p97. Cell Mol Life Sci 65:2360–2371

    Article  PubMed  CAS  Google Scholar 

  • Semenza GL, Agani F, Booth G, Forsythe J, Iyer N, Jiang BH, Leung S, Roe R, Wiener C, Yu A (1997) Structural and functional analysis of hypoxia-inducible factor 1. Kidney Int 51:553–555

    Article  PubMed  CAS  Google Scholar 

  • Smith AR, Rossifanelli F, Ziparo V, James JH, Perelle BA, Fischer JE (1978) Alterations in plasma and CSF amino acids, amines and metabolites in hepatic-coma. Ann Surg 187:343–350

    Article  PubMed  CAS  Google Scholar 

  • Sorensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Article  Google Scholar 

  • Southgate P, Wall T (2001) Welfare of farmed fish at slaughter. In Practice 23:277–284

    Article  Google Scholar 

  • Spallholz JE (1997) Free radical generation by selenium compounds and their prooxidant toxicity. Biomed Environ Sci 10:260–270

    PubMed  CAS  Google Scholar 

  • Stover PJ, Chen LH, Suh JR, Stover DM, Keyomarsi K, Shane B (1997) Molecular cloning, characterization, and regulation of the human mitochondrial serine hydroxymethyltransferase gene. J Biol Chem 272:1842–1848

    Article  PubMed  CAS  Google Scholar 

  • Tang WK, Cheng CHK, Fong WP (2002) First purification of the antiquitin protein and demonstration of its enzymatic activity. FEBS Lett 516:183–186

    Article  PubMed  CAS  Google Scholar 

  • Tang WK, Chan CB, Cheng CHK, Fong WP (2005) Seabream antiquitin: molecular cloning, tissue distribution, subcellular localization and functional expression. FEBS Lett 579:3759–3764

    Article  PubMed  CAS  Google Scholar 

  • Tapiero H, Tew KD, Gate L, Machover D (2001) Prevention of pathologies associated with oxidative stress and dietary intake deficiencies: folate deficiency and requirements. Biomed Pharmacother 55:381–390

    Article  PubMed  CAS  Google Scholar 

  • Tirosh O, Levy E, Reifen R (2007) High selenium diet protects against TNBS-induced acute inflammation, mitochondrial dysfunction, and secondary necrosis in, rat colon. Nutrition 23:878–886

    Article  PubMed  CAS  Google Scholar 

  • Valery C, Grob JJ, Verrando P (2001) Identification by cDNA microarray technology of genes modulated by artificial ultraviolet radiation in normal human melanocytes: relation to melanocarcinogenesis. J Invest Dermatol 117:1471–1482

    Article  PubMed  CAS  Google Scholar 

  • Vente JP, Vonmeyenfeldt MF, Vaneijk HMH, Vanberlo CLH, Gouma DJ, Vanderlinden CJ, Soeters PB (1989) Plasma-amino acid profiles in sepsis and stress. Ann Surg 209:57–62

    Article  PubMed  CAS  Google Scholar 

  • Vijayan MM, Raptis S, Sathiyaa R (2003) Cortisol treatment affects glucocorticoid receptor and glucocorticoid-responsive genes in the liver of rainbow trout. Gen Comp Endocr 132:256–263

    Article  PubMed  CAS  Google Scholar 

  • Wandinger SK, Richter K, Buchner J (2008) The Hsp90 chaperone machinery. J Biol Chem 283:18473–18477

    Article  PubMed  CAS  Google Scholar 

  • Wang QY, Li LY, Ye YH (2008) Inhibition of p97-dependent protein degradation by eeyarestatin I. J Biol Chem 283:7445–7454

    Article  PubMed  CAS  Google Scholar 

  • Wegele H, Muller L, Buchner J (2004) Hsp70 and Hsp90—a relay team for protein folding. Rev Physiol Bioch P 151:1–44

    Article  CAS  Google Scholar 

  • Wu G, Davis PK (1998) Compartmentation and kinetics of urea cycle enzymes in pig enterocytes. FASEB J 12:A861–A861

    Google Scholar 

  • Wulff T, Hoffmann EK, Roepstorff P, Jessen F (2008) Comparison of two anoxia models in rainbow trout cells by a 2-DE and MS/MS-based proteome approach. Proteomics 8:2035–2044

    Article  PubMed  CAS  Google Scholar 

  • Yuan X, Kuramitsu Y, Furumoto H, Zhang X, Hayashi E, Fujimoto M, Nakamura K (2007) Nuclear protein profiling of Jurkat cells during heat stress-induced apoptosis by 2-DE and MS/MS. Electrophoresis 28:2018–2026

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pedro M. Rodrigues.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 780 kb)

ESM 2

(DOCX 745 kb)

ESM 3

(XLSX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cordeiro, O.D., Silva, T.S., Alves, R.N. et al. Changes in Liver Proteome Expression of Senegalese Sole (Solea senegalensis) in Response to Repeated Handling Stress. Mar Biotechnol 14, 714–729 (2012). https://doi.org/10.1007/s10126-012-9437-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-012-9437-4

Keywords

Navigation