Abstract
Heat shock proteins (Hsps) are highly conserved proteins whose expression can be induced by high temperature and play an important role in a variety of biological processes. However, systematic identification of the Hsp60/10 and small Hsp (sHsp) gene family in rainbow trout has not yet been reported, and there is little available information about its roles in evolution in rainbow trout, a typical economical cold-water fish. In this study, we performed a comprehensive analysis of the rainbow trout Hsp60/10 and sHsp gene family and to investigate their expression profiles. A total of one Hsp60 gene, one Hsp10 gene, and ten sHsp genes were identified. According to RNA-seq analysis of rainbow trout liver and head kidney under heat stress, a total of six out of ten sHsp genes were significantly upregulated in liver and head kidney. Real-time RT-PCR (RT-qPCR) was used to quantitatively analyze the expression levels of these genes in different tissues of rainbow trout. Results showed that the expression of hspe1 and hspd1 was lowest in liver and gill, respectively, and highest in brain. In sHsp gene family, all genes are highly expressed in the liver and head kidney, but relatively low in the heart, spleen, brain, gills, and muscles. This systematic analysis provided valuable information about the diverse roles of Hsp60/10 and sHsp in the evolution of teleost fish, which will contribute to the functional characterization of Hsp60/10 and sHsp genes in further research.
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References
Bols NC, Mosser DD, Steels GB (1992) Temperature studies and recent advances with fish cells in vitro. Comp Biochem Physiol 103A:1–14. https://doi.org/10.1016/0300-9629(92)90235-I
Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195. https://doi.org/10.1371/journal.pcbi.1002195
Eggert-Kruse W, Batschulat K, Demirakca T, Strowitzki T (2015) Male immunity to the chlamydial 60 kDa heat shock protein (HSP60) associated with semen quality? Andrologia 47:66–76. https://doi.org/10.1111/and.12224
Elicker KS, Hutson LD (2007)Genome-wide analysis and expression profiling of the small heat shock proteins in zebrafish. Gene 403:60–69. https://doi.org/10.1016/j.gene.2007.08.003
Evgen’ev MB, Garbuz DG, Zatsepina OG (2014) Heat shock proteins and whole body adaptation to extreme environments. Springer, Berlin. https://doi.org/10.1007/978-94-017-9235-6
Fang DA, Zhou YF, Zhang MY, Xu DP, Liu K, Duan JR (2017) Developmental expression of HSP60 and HSP10 in the Coilia nasus testis during upstream spawning migration. GENES 8:189–206. https://doi.org/10.3390/genes8070189
Favet N, Duverger O, Loones MT, Poliard A, Kellermann O, Morange M (2001) Overexpression of murine small heat shock protein HSP25 interferes with chondrocyte differentiation and decreases cell adhesion. Cell Death Differ 8:603–613. https://doi.org/10.1038/sj.cdd.4400847
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:29–37. https://doi.org/10.1093/nar/gkr367
Fortna A, Kim Y, MacLaren E, Marshall K, Hahn G, Meltesen L, Brenton M, Hink R, Burgers S, Hernandez-Boussard T, Anis Karimpour-Fard Glueck D, McGavran L, Berry R, Pollack J, Sikela JM (2004)Lineage-specific gene duplication and loss in human and great ape evolution. PLoS Biol 2(7):E207. https://doi.org/10.1371/journal.pbio.0020207
Franck E, Madsen O, van Rheede T, Ricard G, Huynen MA, de Jong WW (2004) Evolutionary diversity of vertebrate small heat shock proteins. J Mol Evol 59:792–805. https://doi.org/10.1007/s00239-323004-0013-z
Fu X (2014) Chaperone function and mechanism of small heat-shock proteins. Acta Biochim Biophys Sin Shanghai 46:347–356. https://doi.org/10.1093/abbs/gmt152
Garrido C, Paul C, Seigneuric R, Kampinga HH (2012) The small heat shock proteins family: the long forgotten chaperones. Int J Biochem Cell Biol 44:1588–1592. https://doi.org/10.1016/j.biocel.2012.02.022
He B, Gu YH, Tao X, Cheng XJ, Wei CH, Fu J (2015) De novo transcriptome sequencing of Oryza officinalis Wall ex Watt to identify disease-resistance genes. Int J Mol Sci 16:29482–29495. https://doi.org/10.3390/ijms161226178
Hilton GR, Lioe H, Stengel F, Baldwin AJ, Benesch JL (2013) Small heat-shock proteins: paramedics of the cell. Top Curr Chem 328:69–98. https://doi.org/10.1007/128_2012_324
Huang XN, Li SG, Gao YC, Zhan AB (2018)Genome-wide identification, characterization and expression analyses of heat shock protein-related genes in a highly invasive Ascidian Ciona savignyi. Front Physiol 9:1043. https://doi.org/10.3389/fphys.2018.01043
Jiang L, Zhang S, Dong C, Chen B, Feng J, Peng W, Mahboob S, Al-Ghanim KA, Xu P (2016, Gene) Genome wide identification, phylogeny, and expression of fibroblast growth genes in common carp. 578:225–231. https://doi.org/10.1016/j.gene.2015.12.027
de Jong WW, Leunissen JA, Voorter CE (1993) Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol 10:103–126. https://doi.org/10.1093/oxfordjournals.molbev.a039992
Kaya CM, Calvin M (1978) Thermal resistance of rainbow trout from a permanently heated stream, and of two hatchery strains. Prog Fish-Cult 40:138–142. https://doi.org/10.1577/1548-8659(1978)40[138:TRORTF]2.0.CO;2
Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J (2010) Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 24:3633–3642. https://doi.org/10.1096/fj.10-156992
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Landry J, Chretien P, Lambert H, Hickey E, Weber LA (1989) Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. Cell Biol 109:7–15. 353. https://doi.org/10.1083/jcb.109.1.7
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Le Hir H, Nott A, Moore MJ (2003) How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 28:215–220. https://doi.org/10.1016/S0968-0004(03)00052-5
Martín M, Hernández C, Bodega G, Suárez I, Boyano CM, Fernández B (1998)Heat-shock proteins expression in fish central nervous system and its possible relation with water acidosis resistance. Neurosci Res 31:97–106. https://doi.org/10.1016/S0168-0102(98)00028-5
Matthews KR, Berg NH (1997) Rainbow trout responses to water temperature and dissolved oxygen stress in two southern California stream pools. J Fish Biol 50:50–67. https://doi.org/10.1111/j.1095-8649.1997.tb01339.x
Mosser DD, Heikkila JJ, Bols NC (1986) Temperature ranges over which rainbow trout fibroblasts survive and synthesize heat-shock proteins. J Cell Physiol 128:432–440. https://doi.org/10.1002/jcp.1041280312
Nakamoto H, Vigh L (2007) The small heat shock proteins and their clients. Cell Mol Life Sci 64:294–369. https://doi.org/10.1007/s00018-006-6321-2
Niimura Y, Matsui A, Touhara K (2014) Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res 24:1485–1496. https://doi.org/10.1101/gr.169532.113
Ojima N (2007) Rainbow trout hspb1 (hsp27): Rainbow trout hspb1 (hsp27): identification of two mRNA splice variants that show predominant expression in muscle tissues. Comp Biochem Physiol C 148(375):277–285. https://doi.org/10.1016/j.cbpb.2007.06.005
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612. https://doi.org/10.1002/jcc.2008
Press CM, Evensen Ø (1999) The morphology of the immune system in teleost fishes. Fish Shellfish Immunol 9:309–318. https://doi.org/10.1006/fsim.1998.0181
Quan G, Duan J, Ladd T, Krell PJ (2017) Identification and expression analysis of multiple small heat shock protein genes in spruce budworm, Choristoneura fumiferana (L.). Cell Stress Chaperones:1–14. https://doi.org/10.1007/s38312192-017-0832-7
Ranford JC, Coates AR, Henderson B (2000) Chaperonins are cell-signalling proteins: the unfolding biology of molecular chaperones. Expert Rev Mol Med 2:1–17. https://doi.org/10.1017/S1462399400002015
Salinthone S, Ba M, Hanson L, Martin JL, Halayko AJ, Gerthoffer WT (2007) Overexpression of human Hsp27 inhibits serum-induced proliferation in airway smooth muscle myocytes and confers resistance to hydrogen peroxide cytotoxicity. Am J Physiol Lung Cell Mol Physiol 293:L1194–L1207. https://doi.org/10.1152/ajplung.00453.2006
Shi HN, Liu Z, Zhang JP, Kang YJ, Wang JF, Huang JQ, Wang WM (2015) Effect of heat stress on heat shock protein (Hsp60) mRNA expression in rainbow trout Oncorhynchus mykiss. Genet Mol Biol 14:5280–5286. https://doi.org/10.4238/2015.May.18.20
Shi J, Fu M, Zhao C, Zhou F, Yang Q, Qiu L (2016) Characterization and function analysis of Hsp60 and Hsp10 under different acute stresses in black tiger shrimp, Penaeus monodon. Cell Stress Chaperones 21:295–312. https://doi.org/10.1007/s12192-015-0660-6
Song L, Li C, Xie YJ, Liu SK, Zhang JR, Yao J, Jiang C, Li Y, Liu ZJ (2016)Genome-wide identification of Hsp70 genes in channel catfish and their regulated expression after bacterial infection. Fish Shellfish Immunol 49:154–162. https://doi.org/10.1016/j.fsi.2015.12.009
Szalay MS, Kovacs IA, Korcsmaros T, Bode C, Csermely P (2007)Stress-induced rearrangements of ellular networks: consequences for protection and drug design. FEBS Lett 581:3675–3680. https://doi.org/10.1016/j.febslet.2007.03.083
Vandepoele K, De Vos W, Taylor JS, Meyer A, Van de Peer Y (2004) Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc Natl Acad Sci U S A 101:1638–1643. https://doi.org/10.1073/pnas.0307968100
Wang J, Wei Y, Li X, Cao H, Xu MQ, Dai JY (2007) The identification of heat shock protein genes in goldfish (Carassius auratus) and their expression in a complex environment in Gaobeidian Lake, Beijing, China. Comp Biochem Physiol 145:350–362. https://doi.org/10.1016/j.cbpc.2007.01.018
Wang PF, Xu P, Zhou L, Zeng S, Li G (2017) Molecular cloning, characterization, and expression analysis of HSP60 in mandarin fish Siniperca chuatsi. Isr J Aquacult-413 Bamidgeh 69:1–13. https://doi.org/10.1016/j.fsi.2011.07.028
Wei T, Sun Y, Shi G, Wang RX, Xu TJ (2012) Characterization and SNP variation analysis of a HSP70 gene from miiuy croaker and its expression as related to bacterial challenge and heat shock. Fish Shellfish Immunol 33:632–640. https://doi.org/10.1016/j.fsi.2012.06.018
Xia BP, Liu Z, Zhou YJ, Wang YJ, Huang JQ, Li YJ, Liu XX (2018) Effects of heat stress on biochemical parameters and heat shock protein family A (Hsp70) member 5 (HSPA5) mRNA expression in rainbow trout (Oncorhynchus mykiss). Mar Freshw Res 69:1674–1680. https://doi.org/10.1071/MF18029
Xie Y, Song L, Weng Z, Liu S, Liu Z (2015) Hsp90, Hsp60 and sHsp families of heat shock protein genes in channel catfish and their expression after bacterial infections. Fish Shellfish Immunol 44:642–651. https://doi.org/10.1016/j.fsi.2015.03.027
Xu D, Sun L, Liu S, Zhang L, Ru X, Zhao Y, Yang H (2014) Molecular cloning of heat shock protein 10 (Hsp10) and 60 (Hsp60) cDNAs and their expression analysis under thermal stress in the sea cucumber Apostichopus japonicus. Comp Biochem Physiol B: Biochem Mol Biol 171:49–57. https://doi.org/10.1016/j.cbpb.2014.03.009
Zhang J, Li J, Liu B, Zhang L, Chen J, Lu M (2013)Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization, and heat stress responses. BMC Genomics 14:532. https://doi.org/10.1186/1471-2164-14-532
Zhou A, Xie S, Wang Z, Chen Y, Zhang Y, Fan L, Zeng F, Zou J (2018) HSP60 expression profile under different extreme temperature stress in albino northern snakehead, Channa argus. Cell Stress Chaperones 23:791–796. https://doi.org/10.1007/s12192-017-0869-7
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This work was supported by the National Natural Science Foundation of China under Grant (No. 31960268).
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FA and LT conceived and designed the study; FA and QN performed experiments; FA, LT, and QN analyzed the data; and FA, LT, and QN edited and revised the manuscript.
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All the methods used in this study were carried out according to the guiding principles of the Chinese Legislation on the Use and Care of Laboratory Animals. Protocol was approved by the Institutional Ethic Committee of Tianshui Normal University (TSAU).
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Ma, F., Luo, L.T. & Wang, Q. Hsp60/10 and sHsp families of heat shock protein genes in rainbow trout (Oncorhynchus mykiss) and their expression under heat stress. Aquacult Int 30, 1–18 (2022). https://doi.org/10.1007/s10499-020-00638-6
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DOI: https://doi.org/10.1007/s10499-020-00638-6