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Two HSP90 genes in mandarin fish Siniperca chuatsi: identification, characterization and their specific expression profiles during embryogenesis and under stresses

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Abstract

HSP90 plays important roles in multiple cellular stress responses. Here, two cytoplasmic HSP90 isoforms, ScHSP90α and ScHSP90β, were identified from Siniperca chuatsi. Their cDNA and gDNA structures, amino acid sequence features, and sequence identities and phylogenetic analysis with other species were described. Their expression profiles during embryonic development in different tissues and under stressful conditions were analyzed using real-time quantitative PCR. During embryogenesis, transcripts of both genes were detected at low levels during the early developmental stages and were up-regulated from appearance of myomere for ScHSP90a and closure of blastopore for ScHSP90β. ScHSP90α showed a tissue-specific variation with high expression in ovary and brain under non-stressed conditions, while ScHSP90β was ubiquitously highly expressed in different tissues. Acute heat shock resulted in a strong up-regulation of ScHSP90α in heart, liver, and head kidney, while it only weakly induced ScHSP90β in these tissues. ScHSP90α was also markedly induced in liver in a time-dependent manner under hypoxia, while the expression of ScHSP90β was not affected by hypoxia. Additionally, Aeromonas hydrophila infection markedly augmented ScHSP90α in head kidney and spleen and mildly up-regulated ScHSP90β in spleen, while suppressing ScHSP90β in head kidney. These results suggest that ScHSP90α and ScHSP90β are differently involved in embryogenesis and under different environmental conditions including high temperature, hypoxia, and bacterial infection. This study will benefit to further clarify the roles of fish HSP90 isoforms in embryogenesis and under stressful conditions and contribute to further study on enhancing stress tolerance and disease resistance of mandarin fish.

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References

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  PubMed  Google Scholar 

  • Chen CF, Li J (1996) Studies on virulence and isolation of pathogenic bacteria causing bacterial septicemia in mandarin fish (Siniperca chuatsi basilewsky). J Huazhong Agric Univ 15:370–373

    Google Scholar 

  • Chen B, Piel WH, Gui LM, Bruford E, Monteiro A (2005) The HSP90 family of genes in the human genome: insights into their divergence and evolution. Genomics 86:627–637

    Article  CAS  PubMed  Google Scholar 

  • Chen B, Zhong DB, Monteiro A (2006) Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genom 7:156

    Article  Google Scholar 

  • Chen YM, Kuo CE, Wang TY, Shie PS, Wang WC, Huang SL, Tsai TJ, Chen PP, Chen JC, Chen TY (2010) Cloning of an orange-spotted grouper Epinephelus coioides heat shock protein 90AB (HSP90AB) and characterization of its expression in response to nodavirus. Fish Shellfish Immunol 28:895–904

    Article  PubMed  Google Scholar 

  • Chen WX, Liang XF, Fu Y, Ye W (2012) The plankton composition in mandarinfish Siniperca chuatsi ponds and bait fish ponds in hot season. Chin J Fish 25:25–29

    CAS  Google Scholar 

  • Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G (1998) The 90-kda molecular chaperone family: structure, function, and clinical applications: a comprehensive review. Pharmacol Ther 79:129–168

    Article  CAS  PubMed  Google Scholar 

  • Du SJ, Li HQ, Bian YH, Zhong YW (2008) Heat-shock protein 90alpha1 is required for organized myofibril assembly in skeletal muscles of zebrafish embryos. Proc Natl Acad Sci USA 105:554–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Etard C, Behra M, Fischer N, Hutcheson D, Geisler R, Strahle U (2007) The UCS factor STEIF/UNC-45b interacts with the heat shock protein HSP90a during myofibrillogenesis. Dev Biol 308:133–143

    Article  CAS  PubMed  Google Scholar 

  • Etard C, Roostalu U, Strahle U (2008) Shuttling of the chaperones UNC45b and HSP90a between the A band and the Z line of the myofibril. J Cell Biol 180:1163–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gornati R, Papis E, Rimoldi S, Chini V, Terova G, Prati M, Saroglia M, Bernardini G (2005) Molecular markers for animal biotechnology: sea bass (Dicentrarchus labrax, L.) Hmg-coa reductase mRNA. Gene 344:299–305

    Article  CAS  PubMed  Google Scholar 

  • Gupta RS (1995) Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol Biol Evol 12:1063–1073

    CAS  PubMed  Google Scholar 

  • Hall BG (2013) Building phylogenetic trees from molecular data with mega. Mol Biol Evol 30:1229–1235

    Article  CAS  PubMed  Google Scholar 

  • Hermesz E, Abraham M, Nemcsok J (2001) Identification of two HSP90 genes in carp. Comp Biochem Physiol C Toxicol Pharmacol 129:397–407

    Article  CAS  PubMed  Google Scholar 

  • Jackson SE (2013) HSP90: structure and function. Top Curr Chem 328:155–240

    Article  CAS  PubMed  Google Scholar 

  • Krone PH, Sass JB (1994) HSP90alpha and HSP90beta genes are present in the zebrafish and are differentially regulated in developing embryos. Biochem Biophys Res Commun 204:746–752

    Article  CAS  PubMed  Google Scholar 

  • Langer T, Rosmus S, Fasold H (2003) Intracellular localization of the 90 kDa heat shock protein (HSP90alpha) determined by expression of a EGFP-HSP90alpha-fusion protein in unstressed and heat stressed 3T3 cells. Cell Biol Int 27:47–52

    Article  CAS  PubMed  Google Scholar 

  • Lao HH, Sun YN, Yin ZX, Wang J, Chen C, Weng SP, He W, Guo CJ, Huang XD, Yu XQ, He JG (2008) Molecular cloning of two c1q-like cDNAs in mandarin fish Siniperca chuatsi. Vet Immunol Immunopathol 125:37–46

    Article  CAS  PubMed  Google Scholar 

  • Lele Z, Hartson SD, Martin CC, Whitesell L, Matts RL, Krone PH (1999) Disruption of zebrafish somite development by pharmacologic inhibition of HSP90. Dev Biol 210:56–70

    Article  CAS  PubMed  Google Scholar 

  • Li FH, Luan W, Zhang CS, Zhang JQ, Wang B, Xie YS, Li SH, Xiang JH (2009) Cloning of cytoplasmic heat shock protein 90 (FcHSP90) from Fenneropenaeus chinensis and its expression response to heat shock and hypoxia. Cell Stress Chaperones 14:161–172

    Article  CAS  PubMed  Google Scholar 

  • Lin TS, Xue LY, Sun AF, Zhu YF (2012) Effect of temperature and pathogen on HSP90 expression in Larimichthys crocea. Chi J Cell Biol 34:555–564

    CAS  Google Scholar 

  • Montero D, Terova G, Rimoldi S, Tort L, Negrin D, Zamorano MJ, Izquierdo M (2015) Modulation of adrenocorticotrophin hormone (ACTH)-induced expression of stress-related genes by PUFA in inter-renal cells from european sea bass (Dicentrarchus labrax). J Nutr Sci. doi:10.1017/jns.2015.6

    PubMed  PubMed Central  Google Scholar 

  • Ni M, Wen HS, Li JF , Chi ML, Ren YY, Song ZF , Ding HM (2014) Two HSPs gene from juvenile Amur sturgeon (Acipenser schrenckii): cloning, characterization and expression pattern to crowding and hypoxia stress. Fish Physiol Biochem 40:1801–1816

    Article  CAS  PubMed  Google Scholar 

  • Pan F, Zarate JM, Tremblay GC, Bradley TM (2000) Cloning and characterization of salmon HSP90 cDNA: upregulation by thermal and hyperosmotic stress. J Exp Zool 287:199–212

    Article  CAS  PubMed  Google Scholar 

  • Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33:789–801

    Article  CAS  PubMed  Google Scholar 

  • Rupik W, Jasik K, Bembenek J, Widlak W (2011) The expression patterns of heat shock genes and proteins and their role during vertebrate’s development. Comp Biochem Physiol A Mol Integr Physiol 159:349–366

    Article  PubMed  Google Scholar 

  • Sarkar S, Singh MD, Yadav R, Arunkumar KP, Pittman GW (2011) Heat shock proteins: molecules with assorted functions. Front Biol 6:312–327

    CAS  Google Scholar 

  • Sass JB, Weinberg ES, Krone PH (1996) Specific localization of zebrafish HSP90alpha mRNA to myoD–expressing cells suggests a role for HSP90alpha during normal muscle development. Mech Dev 54:195–204

    Article  CAS  PubMed  Google Scholar 

  • Sreedhar AS, Csermely P (2004) Heat shock proteins in the regulation of apoptosis—new strategies in tumor therapy: a comprehensive review. Pharmacol Ther 101:227–257

    Article  CAS  PubMed  Google Scholar 

  • Stenslokken KO, Ellefsen S, Larsen HK, Vaage J, Nilsson GE (2010) Expression of heat shock proteins in anoxic crucian carp (Carassius carassius): support for cold as a preparatory cue for anoxia. Am J Physiol Regul Integr Comp Physiol 298:R1499–R1508

    Article  PubMed  Google Scholar 

  • Tokyol C, Karaorman G, Bastug M (2005) Effects of acute and adaptive hypoxia on heat shock protein expression in hepatic tissue. High Alt Med Biol 6:247–255

    Article  CAS  PubMed  Google Scholar 

  • Wang TT, Chen SL, Meng L, Liu Y (2010) Molecular cloning and expression of heat shock protein 90 gene cDNA from turbot Psetta maxima. Prog Fish Sci 31:51–59

    Google Scholar 

  • Wang PF, Zeng S, Xu P, Zhou L, Zeng L, Lu X, Wang HF, Li GF (2014) Identification and expression analysis of two HSP70 isoforms in mandarin fish Siniperca chuatsi. Fish Sci 80:803–817

    Article  CAS  Google Scholar 

  • Wang PF, Xu P, Zeng S, Zhou L, Zeng L, Li GF (2015) Comparative analysis of sequence feature and expression of two heat shock cognate 70 genes in mandarin fish Siniperca chuatsi. Gene 560:226–236

    Article  CAS  PubMed  Google Scholar 

  • Yamashita M, Yabu T, Ojima N (2010) Stress protein HSP70 in fish. Aquat BioSci Monogr 3:111–141

    Article  Google Scholar 

  • Young JC, Obermann WM, Hartl FU (1998) Specific binding of tetratricopeptide repeat proteins to the c-terminal 12-kDa domain of HSP90. J Biol Chem 273:18007–18010

    Article  CAS  PubMed  Google Scholar 

  • Zhou CP, Lin HZ, Huang Z, Wang J, Wang Y, Yu W (2015) Effects of dietary soybean isoflavones on non-specific immune responses and hepatic antioxidant abilities and mRNA expression of two heat shock proteins (HSPs) in juvenile golden pompano Trachinotus ovatus under pH stress. Fish Shellfish Immunol 47:1043–1053

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by Foshan Innovative and Entepreneurial Research Team Program (No. 2014IT100122), The Science and Technology Projects of Guangdong Oceanic and Fisheries (No. A201401A02), The Science and Technology Planning Projects of Guangdong Province (Nos. 2014A020208022, 2015A030310253), the Special Scientific Research Funds for Central Non-profit Institutes, Chinese Academy of Fishery Sciences (No. 2014TS26) and Special Fund for Agro-scientific Research in the Public Interest, China (No. 201303048).

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Authors and Affiliations

  1. Institute of Aquatic Economic Animals, School of Life Sciences, Sun Yatsen University, Guangzhou, 510006, China

    Peng-Fei Wang, Shuang Zeng, Peng Xu, Lei Zhou & Gui-Feng Li

  2. Key Laboratory of South China Sea Fishery Resources Exploitation and Utilization, Ministry of Agriculture, The South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, 510300, China

    Peng-Fei Wang

  3. South China Sea Bio-Resource Exploitation and Utilization Collaborative Innovation Center, Guangzhou, 510275, China

    Peng-Fei Wang, Shuang Zeng, Peng Xu, Lei Zhou & Gui-Feng Li

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  1. Peng-Fei Wang
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  5. Gui-Feng Li
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Correspondence to Gui-Feng Li.

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Wang, PF., Zeng, S., Xu, P. et al. Two HSP90 genes in mandarin fish Siniperca chuatsi: identification, characterization and their specific expression profiles during embryogenesis and under stresses. Fish Physiol Biochem 42, 1123–1136 (2016). https://doi.org/10.1007/s10695-016-0202-x

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