Shrimp arginine kinase being a binding protein of WSSV envelope protein VP31 -- Journal of Oceanology and Limnology,2016,34(6):1287-1296

	Cite this paper:
	MA Cuiyan, GAO Qiang, LIANG Yan, LI Chen, LIU Chao, HUANG Jie. Shrimp arginine kinase being a binding protein of WSSV envelope protein VP31[J]. Journal of Oceanology and Limnology, 2016, 34(6): 1287-1296

Shrimp arginine kinase being a binding protein of WSSV envelope protein VP31

MA Cuiyan^1,2, GAO Qiang^1,2, LIANG Yan^1,2, LI Chen^1,2, LIU Chao^1,2, HUANG Jie^1,2

1 Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China;
2 National Laboratory for Marine Science and Technology, Qingdao 266071, China

Abstract:

Viral entry into the host is the earliest stage of infection in the viral life cycle in which attachment proteins play a key role. VP31 (WSV340/WSSV396), an envelope protein of white spot syndrome virus (WSSV), contains an Arg-Gly-Asp (RGD) peptide domain known as a cellular attachment site. At present, the process of VP31 interacting with shrimp host cells has not been explored. Therefore, the VP31 gene was cloned into pET30a (+), expressed in Escherichia coli strain BL21 and purified with immobilized metal ion affinity chromatography. Four gill cellular proteins of shrimp (Fenneropenaeus chinensis) were pulled down by an affinity column coupled with recombinant VP31 (rVP31), and the amino acid sequences were identified with MALDI-TOF/TOF mass spectrometry. Hemocyanin, beta-actin, arginine kinase (AK), and an unknown protein were suggested as the putative VP31 receptor proteins. SDS-PAGE showed that AK is the predominant binding protein of VP31. An in vitro binding activity experiment indicated that recombinant AK's (rAK) binding activity with rVP31 is comparable to that with the same amount of WSSV. These results suggested that AK, as a member of the phosphagen kinase family, plays a role in WSSV infection. This is the first evidence showing that AK is a binding protein of VP31. Further studies on this topic will elucidate WSSV infection mechanism in the future.

Key words: white spot syndrome virus (WSSV)|VP31|arginine kinase|shrimp|binding protein

Received: 2015-07-20 Revised: 2015-09-06

Tools

PDF (1065 KB) Free

Print this page

Add to favorites

Email this article to others

Authors

Articles by MA Cuiyan

Articles by GAO Qiang

Articles by LIANG Yan

Articles by LI Chen

Articles by LIU Chao

Articles by HUANG Jie

References:
Cerenius L, Jiravanichpaisal P, Liu H P, Soderhall I. 2010.Crustacean immunity. In:Söderhäll K ed. Invertebrate Immunity:Advances in Experimental Medicine and Biology. Springer, US. 708:239-259.
Chai C Y, Yoon J, Lee Y S, Kim Y B, Choi T J. 2013. Analysis of the complete nucleotide sequence of a white spot syndrome virus isolated from Pacific white shrimp. J.Microbiol., 51(5):695-699.
Chen L L, Leu J H, Huang C J, Chou C M, Chen S M, Wang C H, Lo C F, Kou G H. 2002. Identification of a nucleocapsid protein (VP35) gene of shrimp white spot syndrome virus and characterization of the motif important for targeting VP35 to the nuclei of transfected insect cells. Virology, 293(1):44-53.
Decker H, Jaenicke E. 2004. Recent findings on phenoloxidase activity and antimicrobial activity of hemocyanins. Dev.Comp. Immunol., 28(7-8):673-687.
Dumas C, Camonis J. 1993. Cloning and sequence analysis of the cDNA for arginine kinase of lobster muscle. J. Biol.Chem., 268(29):21 599-21 605.
France R M, Sellers D S, Grossman S H. 1997. Purification, characterization, and hydrodynamic properties of arginine kinase from Gulf shrimp (Penaeus aztecus). Arch.Biochem. Biophys., 345(1):73-78.
Furukohri T, Okamoto S, Suzuki T. 1994. Evolution of phosphagen kinase (III). Amino acid sequence of arginine kinase from the shrimp Penaeus japonicus. Zoolog. Sci., 11(2):229-234.
Huang J, Song X L, Yu J, Yang C H. 1995. Baculoviral hypodermal and hematopoietic necrosis-study on the pathogen and pathology of the explosive epidemic disease of shrimp. Marine Fisheries Research, 16(1):1-10 (in Chinese with English abstract)
Kinsey S T, Lee B C. 2003. The effects of rapid salinity change on in vivo arginine kinase flux in the juvenile blue crab, Callinectes sapidus. Comp. Biochem. Physiol. B Biochem.Mol. Biol., 135(3):521-531.
Kotlyar S, Weihrauch D, Paulsen R S, Towle D W. 2000.Expression of arginine kinase enzymatic activity and mRNA in gills of the euryhaline crabs Carcinus maenas and Callinectes sapidus. J. Exp. Biol., 203(Pt 16):2 395-2 404.
Lanier L M, Volkman L E. 1998. Actin binding and nucleation by Autographa california M nucleopolyhedrovirus.Virology, 243(1):167-177.
Li L, Lin Z Y, Xu L X, Yang F. 2011. The RGD motif in VP31 of white spot syndrome virus is involved in cell adhesion.Arch. Virol., 156(8):1 317-1 321.
Li L, Xie X X, Yang F. 2005. Identification and characterization of a prawn white spot syndrome virus gene that encodes an envelope protein VP31. Virology, 340:125-132.
Li Q, Yang F, Zhang J H, Chen Y J. 2003. Proteomic analysis of proteins that binds specifically to the homologous repeat regions of white spot syndrome virus. Biol. Pharm.Bull., 26(11):1 517-1 522.
Li W, Tang X Q, Xing J, Sheng X Z, Zhan W B. 2014.Proteomic analysis of differentially expressed proteins in Fenneropenaeus chinensis hemocytes upon white spot syndrome virus infection. PLoS One, 9(2):e89962.
Liang Y, Cheng J J, Yang B, Huang J. 2010. The role of F1 ATP synthase beta subunit in WSSV infection in the shrimp, Litopenaeus vannamei. Virol. J., 7(1):144.
Liang Y, Huang J, Song X L, Zhang P J, Xu H S. 2005. Four viral proteins of white spot syndrome virus (WSSV) that attach to shrimp cell membranes. Dis. Aquat. Organ., 66:81-85.
Liang Y, Song X L, Huang J, Zhang P J. 2003. DIG labeled WSSV and observation of binding phenomenon between WSSV and it's host cell. Oceanologia et Limnologia Sinica, (S):1-9. (in Chinese with English abstract)
Lightner D V. 1996. A Handbook of Shrimp Pathology and Diagnostic Procedures for Diseases of Cultured Penaeid Shrimp. World Aquaculture Society, Tucson, Arizona, U.S.A.
Liu B D, Dai R K, Tian C J, Dawson L, Gorelick R, Yu X F. 1999. Interaction of the human immunodeficiency virus type 1 nucleocapsid with actin. J. Virol., 73(4):2 901-2 908.
Liu C, Zhao P, Liang Y, Gao Q, Liu S P, Huang J, 2014.Preliminary study on the conjunction between arginine kinase of Fenneropenaeus chinensis and the structure proteins of white spot syndrome virus (WSSV). Marine Sciences, 38(3):104-110 (in Chinese with English abstract)
Liu Q H, Zhang X L, Ma C Y, Liang Y, Huang J. 2009. VP37of white spot syndrome virus interact with shrimp cells.Lett. Appl. Microbiol., 48(1):44-50.
Ma F F, Liu Q H, Guan G K, Li C, Huang J. 2014. Arginine kinase of Litopenaeus vannamei involved in white spot syndrome virus infection. Gene, 539(1):99-106.
Mandl C W, Guirakhoo F, Holzmann H, Heinz F X, Kunz C. 1989. Antigenic structure of the flavivirus envelope protein E at the molecular level, using tick-borne encephalitis virus as a model. J. Virol., 63(2):564-571.
OIE. 2012. Manual of Diagnostic Tests for Aquatic Animals.Chapter 2.2.6 White Spot Disease. World Organisation of Aquatic Animal Health.
Pierschbacher M D, Ruoslahti E. 1984. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature, 309(5963):30-33.
Pineda Jr A, Ellington W R. 1998. Immunogold transmission electron microscopic localization of arginine kinase in Arthropod mitochondria. J. Exp. Zool., 281(2):73-79.
Sánchez-Paz A. 2010. White spot syndrome virus:an overview on an emergent concern. Vet. Res., 41(6):43.
Smith A E, Helenius A. 2004. How viruses enter animal cells.Science, 304(5668):237-242.
Song C W, Cui Z X, Liu Y, Li Q Q, Wang S Y. 2012. Cloning and expression of arginine kinase from a swimming crab, Portunus trituberculatus. Mol. Biol. Rep., 39(4):4 879-4 888.
Sritunyalucksana K, Wannapapho W, Lo C F, Flegel T W. 2006. PmRab7 is a VP28-binding protein involved in white spot syndrome virus infection in shrimp. J. Virol., 80(21):10 734-10 742.
Strong S J, Ellington W R. 1995. Isolation and sequence analysis of the gene for arginine kinase from the chelicerate arthropod, Limulus polyphemus:insights into catalytically important residues. Biochim. Biophys. Acta, 1246(2):197-200.
Terwilliger N B. 1998. Functional adaptations of oxygentransport proteins. J. Exp. Biol., 201(Pt 8):1 085-1 098.
Tsai J M, Wang H C, Leu J H, Hsiao H H, Wang A H J, Kou G H, Lo C F. 2004. Genomic and proteomic analysis of thirty-nine structural proteins of shrimp white spot syndrome virus. J. Virol., 78(20):11 360-11 370.
Valentim-Neto P A, Fraga A P M, Marques M R F. 2014.Differential expression of proteins in the gills of Litopenaeus vannamei infected with white spot syndrome virus. Aquacult. Int., 22(5):1 605-1 620.
van Hulten M C W, Witteveldt J, Peters S, Kloosterboer N, Tarchini R, Fiers M, Sandbrink H, Lankhorst R K, Vlak J M. 2001. The white spot syndrome virus DNA genome sequence. Virology, 286(1):7-22.
Verdaguer N, Mateu M G, Andreu D, Giralt E, Domingo E, Fita I. 1995. Structure of the major antigenic loop of footand-mouth disease virus complexed with a neutralizing antibody:direct involvement of the Arg-Gly-Asp motif in the interaction. EMBO J., 14(8):1 690-1 696.
Wang B, Li F H, Luan W, Xie Y S, Zhang C S, Luo Z, Gui L, Yan H, Xiang J X. 2008. Comparison of gene expression profiles of Fenneropenaeus chinensis challenged with WSSV and Vibrio. Mar. Biotechnol., 10(6):664-675.
Wu J J, Li F, Huang J J, Xu L M, Yang F. 2015. Crayfish hematopoietic tissue cells but not hemocytes are permissive for white spot syndrome virus replication.Fish Shellfish Immunol., 43(1):67-74.
Xie X X, Yang F. 2005. Interaction of white spot syndrome virus VP26 protein with actin. Virology, 336(1):93-99.
Xu H, Yan F, Deng X B, Wang J C, Zou T T, Ma X, Zhang X, Qi Y P. 2009. The interaction of white spot syndrome virus envelope protein VP28 with shrimp Hsc70 is specific and ATP-dependent. Fish Shellfish Immunol., 26(3):414-421.
Yang F, He J, Lin X H, Li Q, Pan D, Zhang X B, Xu X. 2001.Complete genome sequence of the shrimp white spot bacilliform virus. J. Virol., 75(23):11 811-11 820.
Yao C L, Ji P F, Kong P, Wang Z Y, Xiang J H. 2009. Arginine kinase from Litopenaeus vannamei:cloning, expression and catalytic properties. Fish Shellfish Immunol., 26(3):553-558.
Yao C L, Wu C G, Xiang J H, Dong B. 2005. Molecular cloning and response to laminarin stimulation of arginine kinase in haemolymph in Chinese shrimp, Fenneropenaeus chinensis. Fish Shellfish Immunol., 19(4):317-329.
Yu C J, Lin Y F, Chiang B L, Chow L P. 2003. Proteomics and immunological analysis of a novel shrimp allergen, Pen m 2. J Immunol., 170(1):445-453.
Zhang X B, Huang C H, Qin Q W. 2004. Antiviral properties of hemocyanin isolated from shrimp Penaeus monodon.Antiviral Res., 61(2):93-99.