Abstract
Heat shock proteins (HSPs), such as HSP70 and HSP90, are a suite of highly conserved proteins produced in all cellular organisms when they are exposed to stresses. In aquatic animals, they have been proved to play important roles in response to environmental pollutants and particularly in the non-specific immune responses to pathogen infections. In the present study, the expression profiles of HSP70 and HSP90 genes in hemocytes and hepatopancreas from the ridgetail white prawn Exopalaemon carinicauda infected with WSSV and Vibrio anguillarum were detected using reverse transcription polymerase chain reaction (RT-PCR). After WSSV challenge, the expression level of HSP 70 gene transcripts in the hemocytes and hepatopancreas increased to peak level at 6 h and 48 h, respectively. HSP90 gene transcripts in hemocytes and hepatopancreas were up-regulated significantly at 12 h and 6 h, respectively. During V. anguillarum challenge, the mRNA content of HSP70 gene in hemocytes and hepatopancreas increased significantly at 12 h and 6 h post-infection, respectively. The expression level of HSP90 gene both in hemocytes and hepatopancreas were up-regulated in the first 3 h. The expression patterns of HSP70 and HSP90 genes in hemocytes and hepatopancreas showed temporal and spatial differences after challenged with WSSV and V. anguillarum. The results suggested that HSPs might be involved in immune responses to pathogens challenge in E. carinicauda.
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Bausinger, H., Lipsker, D., and Hanau, D., 2002. Heat-shock proteins as activators of the innate immune system. Trends in Immunology, 23 (7): 342–343.
Cellura, C., Toubiana, M., Parrinello, N., and Roch, P., 2007. Specific expression of antimicrobial peptide and HSP70 genes in response to heat-shock and several bacterial challenges in mussels. Fish and Shellfish Immunology, 22: 340–350.
Chaurasia, M. K., Nizam, F., Ravichandran, G., Arasu, M. V., Al-Dhabic, N. A., Arshad, A., Elumalai, P., and Arockiaraj, J., 2016. Molecular importance of prawn large heat shock proteins 60, 70 and 90. Fish and Shellfish Immunology, 48: 228–238.
Chen, X., Zeng, D., Chen, X., Xie, D., Zhao, Y., Yang, C., Li, Y., Ma, N., Li, M., Yang, Q., Liao, Z., and Wang, H., 2013. Transcriptome analysis of Litopenaeus vannamei in response to white spot syndrome virus infection. PLoS One, 8 (8): e73218.
Chen, Y., Yuan, F., Bi, H., Zhang, Z., Yue, H., Yuan, K., Chen, Y., Wen, S., and He, J., 2016. Transcriptome analysis of the unfolded protein response in hemocytes of Litopenaeus vannamei. Fish and Shellfish Immunology, 54: 153–163.
Cheng, S. H., So, C. H., Chan, P. K., Cheng, C. W., and Wu, R. S. S., 2003. Cloning of the HSP70 gene in barnacle, larvae and its expression under hypoxic conditions. Marine Pollution Bulletin, 46: 665–671.
Chuang, K. H., Ho, S. H., and Song, Y. L., 2007. Cloning and expression analysis of heat shock cognate 70 gene promoter in tiger shrimp (Penaeus monodon). Gene, 405: 10–18.
Cui, Z., Liu, Y., Luan, W., Li, Q., Wu, D., and Wang, S., 2010. Molecular cloning and characterization of a heat shock protein 70 gene in swimming crab (Portunus trituberculatus). Fish and Shellfish Immunology, 28: 56–64.
Dang, W., Lu, H., Gao, Y., Xu, N., Qu, T., and Liu, Y., 2015. Molecular analysis of inducible heat shock protein 70 of Pelodiscus sinensis and its effects during pathogen (Aeromonas hydrophila) infection. Aquaculture, 442: 93–99.
Du, J., Zhu, H., Liu, P., Chen, J., Xiu, Y., Yao, W., Wu, T., Ren, Q., Meng, Q., Gu, W., and Wang, W., 2013. Immune responses and gene expression in hepatopancreas from Macrobrachium rosenbergii challenged by a novel pathogen spiroplasma MR-1008. Fish and Shellfish Immunology, 34: 315–323.
Duan, Y., Li, J., Zhang, Z., Li, J., Ge, Q., and Liu, P., 2015. The role of oncoprotein NM23 gene from Exopalaemon carinicauda is response to pathogens challenge and ammonia-N stress. Fish and Shellfish Immunology, 47: 1067–1074.
Duan, Y., Liu, P., Li, J., Li, J., and Chen, P., 2013a. Expression profiles of selenium dependent glutathione peroxidase and glutathione S-transferase from Exopalaemon carinicauda in response to Vibrio anguillarum and WSSV challenge. Fish and Shellfish Immunology, 35: 661–670.
Duan, Y., Liu, P., Li, J., Li, J., and Chen, P., 2013b. Immune gene discovery by expressed sequence tag (EST) analysis of hemocytes in the ridgetail white prawn Exopalaemon carinicauda. Fish and Shellfish Immunology, 34: 173–182.
Duan, Y., Liu, P., Li, J., Li, J., and Chen, P., 2014a. A farnesoic acid O-methyltransferase (FAMeT) from Exopalaemon carinicauda is responsive to Vibrio anguillarum and WSSV challenge. Cell Stress and Chaperones, 19: 367–377.
Duan, Y., Liu, P., Li, J., Li, J., and Chen, P., 2014b. Molecular responses of calreticulin gene to Vibrio anguillarum and WSSV challenge in the ridgetail white prawn Exopalaemon carinicauda. Fish and Shellfish Immunology, 36: 164–171.
Durand, S. V., and Lightner, D. V., 2002. Quantitative real time PCR for the measurement of white spot syndrome virus in shrimp. Journal of Fish Diseases, 25: 381–389.
Erbse, A., Mayer, M. P., and Bukau, B., 2004. Mechanism of substrate recognition by Hsp70 chaperones. Biochemical Society Transactions, 32: 617–621.
Fu, D., Chen, J., Zhang, Y., and Yu, Z., 2011. Cloning and expression of a heat shock protein (HSP) 90 gene in the haemocytes of Crassostrea hongkongensis under osmotic stress and bacterial challenge. Fish and Shellfish Immunology, 31 (1): 118–125.
Fu, W., Zhang, F., Liao, M., Liu, M., Zheng, B., Yang, H., and Zhong, M., 2013. Molecular cloning and expression analysis of a cytosolic heat shock protein 70 gene from mud crab Scylla serrate. Fish and Shellfish Immunology, 34: 1306–1314.
Gao, Q., Song, L., Ni, D., Wu, L., and Chang, Y., 2007. cDNA cloning and mRNA expression of heat shock protein 90 gene in the haemocytes of Zhikong scallop Chlamys farreri. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 147: 704–715.
Gao, Q., Zhao, J., Song, L., Qiu, L., Yu, Y., Zhang, H., and Ni, D., 2008. Molecular cloning, characterization and expression of heat shock protein 90 gene in the haemocytes of bay scallop Argopecten irradians. Fish and Shellfish Immunology, 24: 379–385.
Georgopoulos, C., and Welch, W. J., 1993. Role of the major heat shock proteins as molecular chaperones. Annual Review of Cell Biology, 9: 601–634.
González-Rodríguez, G., Colubi, A., and Gil, M. A., 2012. Fuzzy data treated as functional data: A one-way ANOVA test approach. Computational Statistics & Data Analysis, 56: 943–955.
Han, J., Li, J., Li, J., Chang, Z., Chen, P., and Li, H., 2011. Cloning and expression of Heat Shock Protein 70 (HSP70) of Exopalaemon carinicauda. Journal of Fisheries of China, 35 (8): 1130–1138 (in Chinese).
Iwanaga, S., and Lee, B. L., 2005. Recent advances in the innate immunity of invertebrate animals. Journal of Biochemistry and Molecular Biology, 38: 128–150.
Jiao, C., Wang, Z., Li, F., Zhang, C., and Xiang, J., 2004. Cloning, sequencing and expression analysis of cDNA encoding a constitutive heat shock protein 70 (HSC70) in Fenneropenaeus chinensis. Chinese Science Bulletin, 49: 2385–2393.
Joly, A. L., Wettstein, G., Mignot, G., Ghiringhelli, F., and Garrido, C., 2010. Dual role of heat shock proteins as regulators of apoptosis and innate immunity. Journal of Innate Immunity, 2 (3): 238–247.
Leignel, V., Cibois, M., Moreau, B., and Chénais, B., 2007. Identification of new subgroup of HSP70 in Bythograeidae (hydrothermal crabs) and Xanthidae. Gene, 396 (1): 84–92.
Lemaitre, B., and Hoffmann, J., 2007. The host defense of Drosophila melanogaster. Annual Review of Immunology, 25: 697–743.
Li, J. T., Li, J., Chen, P., Liu, P., and He, Y., 2015. Transcriptome analysis of eyestalk and hemocytes in the ridgetail white prawn Exopalaemon carinicauda: Assembly, annotation and marker discovery. Molecular Biology Reports, 42 (1): 135–147.
Li, F., and Xiang, J., 2013. Recent advances in researches on the innate immunity of shrimp in China. Developmental and Comparative Immunology, 39: 11–26.
Li, F., Luan, W., Zhang, C., Zhang, J., Wang, B., Xie, Y., Li, S., and Xiang, J., 2009. Cloning of cytoplasmic heat shock protein 90 (FcHSP90) from Fenneropenaeus chinensis and its expression response to heat shock and hypoxia. Cell Stress and Chaperones, 14: 161–172.
Li, J., Han, J., Chen, P., Liu, P., and Li, J., 2012. Cloning of a heat shock protein 90 (HSP90) gene and expression analysis in the ridgetail white prawn Exopalaemon carinicauda. Fish and Shellfish Immunology, 32 (6): 1191–1197.
Lightner, D. V., 2011. Virus diseases of farmed shrimp in the Western Hemisphere (the Americas): A review. Journal of Invertebrate Pathology, 106: 110–130.
Lindquist, S., and Craig, E. A., 1988. The heat-shock proteins. Annual Review of Genetics, 22: 631–677.
Liu, J., Yang, W., Zhu, X., Karouna-Renier, N. K., and Rao, R. K., 2004. Molecular cloning and expression of two HSP70 genes in the prawn, Macrobrachium rosenbergii. Cell Stress and Chaperones, 9 (3): 313–323.
Livak, K. J., and Schmittgen, T. D., 2001. Analysis of relative gene expression data using realtime quantitative PCR and the 2 (delta delta C(T)) method. Methods, 25: 402–408.
Lo, W., Liu, K., Liao, I., and Song, Y., 2004. Cloning and molecular characterization of heat shock cognate 70 from tiger shrimp (Penaeus monodon). Cell Stress and Chaperones, 9 (4): 332–343.
Luan, W., Li, F., and Zhang, J., 2010. Identification of a novel inducible cytosolic Hsp70 gene in Chinese shrimp Fenneropenaeus chinensis and comparison of its expression with the cognate Hsc70 under different stresses. Cell Stress and Chaperones, 15 (1): 83–93.
Ming, J., Xie, J., Xu, P., Liu, W., Ge, X., Liu, B., He, Y., Cheng, Y., Zhou, Q., and Pan, L., 2010. Molecular cloning and expression of two HSP70 genes in the Wuchang bream (Megalobrama amblycephala Yih). Fish and Shellfish Immunology, 28 (3): 407–418.
Mjahed, H., Girodon, F., Fontenay, M., and Garrido, C., 2012. Heat shock proteins in hematopoietic malignancies. Experimental Cell Research, 318 (15): 1946–1958.
Moseley, P. L., 1997. Heat shock proteins and heat adaptation of the whole organism. Journal of Applied Physiology, 83: 1413–1417.
Multhoff, G., 2007. Heat shock protein 70 (Hsp70): Membrane location, export and immunological relevance. Methods, 43: 229–237.
Pan, F., Zarate, J. M., Tremblay, G. C., and Bradley, T. M., 2000. Cloning and characterization of salmon hsp90 cDNA: Upregulation by thermal and hyperosmotic stress. Journal of Experimental Zoology, 287 (3): 199–212.
Pearl, L. H., and Prodromou, C., 2006. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annual Review of Biochemistry, 75: 271–294.
Pockley, A. G., 2003. Heat shock proteins as regulators of the immune response. The Lancet, 362: 469–476.
Pratt, W. B., and Toft, D. O., 2003. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Experimental Biology and Medicine, 228: 111–133.
Qin, C., Zhao, D., Gong, Q., Qi, Z., Zou, Y., Yue, X., and Xie, B., 2013. Effects of pathogenic bacterial challenge after acute sublethal ammonia-N exposure on heat shock protein 70 expression in Botia reevesae. Fish and Shellfish Immunology, 35 (3): 1044–1047.
Ravaux, J., Toullec, J. Y., Leger, N., Lopez, P., Gaill, F., and Shillito, B., 2007. First hsp70 from two hydrothermal vent shrimps, Mirocaris fortunata and Rimicaris exoculata: Characterization and sequence analysis. Gene, 386 (1-2): 162–172.
Rungrassamee, W., Leelatanawit, R., Jiravanichpaisal, P., Klinbunga, S., and Karoonuthaisiri, N., 2010. Expression and distribution of three heat shock protein genes under heat shock stress and under exposure to Vibrio harveyi in Penaeus monodon. Developmental & Comparative Immunology, 34 (10): 1082–1089.
Soderhall, K., and Smith, V. J., 1983. Separation of the haemocyte populations of Carcinus maenas and other marine decapods. Developmental & Comparative Immunology, 7 (2): 229–239.
Song, L., Wu, L., Ni, D., Chang, Y., Xu, W., and Xing, K., 2006. The cDNA cloning and mRNA expression of heat shock protein 70 gene in the haemocytes of bay scallop (Argopecten irradians, Lamarck 1819) responding to bacteria challenge and naphthalin stress. Fish and Shellfish Immunology, 21 (4): 335–345.
Sreedhar, A. S., Kalmar, E., Csermely, P., and Shen, Y., 2004. Hsp90 isoforms: Functions, expression and clinical importance. FEBS Letters, 562 (1-3): 11–15.
Tassanakajon, A., Somboonwiwat, K., Supungul, P., and Tang, S., 2013. Discovery of immune molecules and their crucial functions in shrimp immunity. Fish and Shellfish Immunology, 34 (4): 954–967.
Terasawa, K., Minami, M., and Minami, Y., 2005. Constantly updated knowledge of HSP90. Journal of Biochemistry, 137 (4): 443–447.
Threechada, D., Fernand, F. F., Aiko, S., Hidehiro, K., Takashi, A., Reiko, N., and Ikuo, H., 2011. Molecular characterization and expression analysis of heat shock proteins 40, 70 and 90 from kuruma shrimp Marsupenaeus japonicus. Fisheries Science, 77 (6): 929–937.
Tsan, M. F., and Gao, B., 2004. Cytokine function of heat shock proteins. American Journal of Physiology-Cell Physiology, 286 (4): C739-744.
Wang, B., Li, F., Dong, B., Zhang, X., Zhang, C., and Xiang, J., 2006. Discovery of the genes in response to white spot syndrome virus (WSSV) infection in Fenneropenaeus chinensis through cDNA microarray. Marine Biotechnology, 8 (5): 491–500.
Wang, Z., Wu, Z., Jian, J., and Lu, Y., 2008. Cloning and expression of heat shock protein 70 gene in the hemocytes of pearl oyster (Pinctada fucata, Gould 1850) responding to bacterial challenge. Fish and Shellfish Immunology, 26 (4): 639–645.
Wu, R., Sun, Y., Lei, L., and Xie, S., 2008. Molecular identification and expression of heat shock cognate 70 (HSC70) in the pacific white shrimp Litopenaeus vannamei. Molecular Biology, 42 (2): 265–274.
Xie, Y., Song, L., Weng, Z., Liu, S., and Liu, Z., 2015. Hsp90, Hsp60 and sHsp families of heat shock protein genes in channel catfish and their expression after bacterial infections. Fish and Shellfish Immunology, 44 (2): 642–651.
Xu, H., Yan, F., Deng, X., Wang, J., Zou, T., Ma, X., Zhang, X., and Qi, Y., 2009. The interaction of white spot syndrome virus envelope protein VP28 with shrimp HSC70 is specific and ATP-dependent. Fish and Shellfish Immunology, 26 (3): 414–421.
Xu, W., Xie, J., Shi, H., and Li, C., 2010. Hematodinium infections in cultured ridgetail white prawns, Exopalaemon carinicauda, in eastern China. Aquaculture, 300 (1-4): 25–31.
Acknowledgements
This study was supported by the earmarked fund for Modern Agro-industry Technology Research System (No. CARS-48), the Program of Shandong Leading Talent (No. LNJY2015002), the National Natural Science Foundation of China (No. 31472275), and Qingdao Industrial Development Program (Science and Technology Benefit Special Project, No. 17-3-3-62-nsh).
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Li, J., Li, J., Duan, Y. et al. The Roles of Heat Shock Proteins 70 and 90 in Exopalaemon carinicauda After WSSV and Vibrio anguillarum Challenges. J. Ocean Univ. China 17, 399–406 (2018). https://doi.org/10.1007/s11802-018-3392-2
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DOI: https://doi.org/10.1007/s11802-018-3392-2