Comparative analysis of differentially expressed genes in normal and white spot syndrome virus infected Penaeus monodon

Springer Science and Business Media LLC - Tập 8 Số 1 - 2007
Jiann Horng Leu1, Cheng Chang2, Jinliang Wu3,1, Chun Wei Hsu2, Ikuo Hirono4, Takashi Aoki4, Hsueh‐Fen Juan5, Chu Fang Lo1, Guang Hsiung Kou1, Hsuan‐Cheng Huang2
1Institute of Zoology, National Taiwan University, Taipei 106, Taiwan
2Institute of Bioinformatics, National Yang-Ming University, Taipei 112, Taiwan
3Department of Biological Sciences, National University of Singapore, Singapore
4Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, Minato, Tokyo, Japan
5Department of Life Science, Institute of Molecular and Cellular Biology, National Taiwan University, Taipei 106, Taiwan

Tóm tắt

Abstract Background White spot syndrome (WSS) is a viral disease that affects most of the commercially important shrimps and causes serious economic losses to the shrimp farming industry worldwide. However, little information is available in terms of the molecular mechanisms of the host-virus interaction. In this study, we used an expressed sequence tag (EST) approach to observe global gene expression changes in white spot syndrome virus (WSSV)-infected postlarvae of Penaeus monodon. Results Sequencing of the complementary DNA clones of two libraries constructed from normal and WSSV-infected postlarvae produced a total of 15,981 high-quality ESTs. Of these ESTs, 46% were successfully matched against annotated genes in National Center of Biotechnology Information (NCBI) non-redundant (nr) database and 44% were functionally classified using the Gene Ontology (GO) scheme. Comparative EST analyses suggested that, in postlarval shrimp, WSSV infection strongly modulates the gene expression patterns in several organs or tissues, including the hepatopancreas, muscle, eyestalk and cuticle. Our data suggest that several basic cellular metabolic processes are likely to be affected, including oxidative phosphorylation, protein synthesis, the glycolytic pathway, and calcium ion balance. A group of immune-related chitin-binding protein genes is also likely to be strongly up regulated after WSSV infection. A database containing all the sequence data and analysis results is accessible at http://xbio.lifescience.ntu.edu.tw/pm/. Conclusion This study suggests that WSSV infection modulates expression of various kinds of genes. The predicted gene expression pattern changes not only reflect the possible responses of shrimp to the virus infection but also suggest how WSSV subverts cellular functions for virus multiplication. In addition, the ESTs reported in this study provide a rich source for identification of novel genes in shrimp.

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Tài liệu tham khảo

Lo CF, Ho CH, Peng SE, Chen CH, Hsu HC, Chiu YL, Chang CF, Liu KF, Su MS, Wang CH, Kou GH: White spot syndrome baculovirus (WSBV) detected in cultured and captured shrimp, crabs and other arthropods. Dis Aquat Org. 1996, 27: 215-226.

Lo CF, Leu JH, Ho CH, Chen CH, Peng SE, Chen YT, Chou CM, Yeh PY, Huang CJ, Chou HY, Wang CH, Kou GH: Detection of baculovirus associated with white spot syndrome (WSBV) in penaeid shrimps using polymerase chain reaction. Dis Aquat Org. 1996, 5: 133-141.

van Hulten MC, Witteveldt J, Peters S, Kloosterboer N, Tarchini R, Fiers M, Sandbrink H, Lankhorst RK, Vlak JM: The white spot syndrome virus DNA genome sequence. Virology. 2001, 286: 7-22. 10.1006/viro.2001.1002.

Yang F, He J, Lin X, Li Q, Pan D, Zhang X, Xu X: Complete genome sequence of the shrimp white spot bacilliform virus. J Virol. 2001, 75: 11811-11820. 10.1128/JVI.75.23.11811-11820.2001.

Huang C, Zhang X, Lin Q, Xu X, Hu Z, Hew CL: Proteomic analysis of shrimp white spot syndrome viral proteins and characterization of a novel envelope protein VP466. Mol Cell Proteomics. 2002, 1: 223-231. 10.1074/mcp.M100035-MCP200.

Astrofsky KM, Roux MM, Klimple KR, Fox JG, Dhar AK: Isolation of differentially expressed genes from white spot syndrome virus (WSV) infected Pacific blue shrimp (Penaeus stylirostris). Arch Virol. 2002, 147: 1799-1812. 10.1007/s00705-002-0845-z.

Pan D, He N, Yang Z, Liu H, Xu X: Differential gene expression profile in hepatopancreas of WSSV-resistant shrimp (Penaeus japonicus) by suppression subtractive hybridization. Dev Comp Immunol. 2005, 29: 103-112. 10.1016/j.dci.2004.07.001.

He N, Qin Q, Xu X: Differential profile of genes expressed in hemocytes of White Spot Syndrome Virus-resistant shrimp (Penaeus japonicus) by combining suppression subtractive hybridization and differential hybridization. Antivir Res. 2005, 66: 39-45. 10.1016/j.antiviral.2004.12.010.

Dhar AK, Dettroi A, Roux MM, Klimpel KR, Read B: Identification of differential expressed genes in shrimp (Penaeus stylirostris) infected with white spot syndrome virus by cDNA microarrays. Arch Virol. 2003, 148: 2381-2396. 10.1007/s00705-003-0172-z.

Wang B, Li F, Dong B, Zhang X, Zhang C, Xiang J: Discovery of the genes in response to white spot syndrome virus (WSSV) infection in Fenneropenaeus chinensis through cDNA microarray. Mar Biotechnol (NY). 2006, 8: 491-500. 10.1007/s10126-005-6136-4.

Rojtinnakorn J, Hirono I, Itami T, Takahashi Y, Aoki T: Gene expression in heamocytes of kuruma prawn, Penaeus japonicus, in response to infection with WSSV by EST approach. Fish Shell Immunol. 2002, 13: 69-83. 10.1006/fsim.2001.0382.

Lehnert SA, Wilson KJ, Byrne K, Moore SS: Tissue-specific expressed sequence tags from the black tiger shrimp Penaeus monodon. Mar Biotechnol. 1999, 1: 465-76. 10.1007/PL00011803.

Gross PS, Bartlett TC, Browdy CL, Chapman RW, Warr GW: Immune gene discovery by expressed sequence tag analysis of hemocytes and hepatopancreas in the pacific white shrimp, Litopenaeus vannamei, and the Atlantic white shrimp, L setiferus. Dev Comp Immunol. 2001, 25: 565-77. 10.1016/S0145-305X(01)00018-0.

Supungul P, Klinbunga S, Pichyangkura R, Jitrapakdee S, Hirono I, Aoki T, Tassanakajon A: Identification of immune-related genes in hemocytes of black tiger shrimp (Penaeus monodon). Mar Biotechnol. 2002, 4: 487-94. 10.1007/s10126-002-0043-8.

Yamano K, Unuma T: Expressed sequence tags from eyestalk of kuruma prawn, Marsupenaeus japonicus. Comp Biochem Physiol A Mol Integr Physiol. 2006, 143: 155-61. 10.1016/j.cbpa.2005.11.005.

O'Leary NA, Trent HF, Robalino J, Peck MET, Mckillen DJ, Gross PS: Analysis of multiple tissue-specific cDNA libraries from the Pacific whiteleg shrimp, Litopenaeus vannamei. Integrative and Comparative Biology. 2006, 46: 931-939. 10.1093/icb/icl006.

Tassanakajon A, Klinbunga S, Paunglarp N, Rimphanitchayakit V, Udomkit A, Jitrapakdee S, Sritunyalucksana K, Phongdara A, Pongsomboon S, Supungul P, Tang S, Kuphanumart K, Pichyangkura R, Lursinsap C: Penaeus monodon gene discovery project: The generation of an EST collection and establishment of a database. Gene. 2006, 384: 104-12. 10.1016/j.gene.2006.07.012.

Penaeus monodon Functional Genomics Database. [http://xbio.lifescience.ntu.edu.tw/pm/]

Anderson SO, Hojrup P, Roepstoref P: Insect cuticular proteins. Insect Biochem Molec Biol. 1995, 25: 153-176. 10.1016/0965-1748(94)00052-J.

Chang PS, Lo CF, Wang YC, Kou GH: Identification of white spot syndrome associated baculovirus (WSBV) target organs in shrimp, Penaeus monodon, by in situ hybridization. Dis Aquat Org. 1996, 27: 131-139.

Wang CS, Tang KFJ, Kou GH, Chen SN: Light and electron microscopic evidence of white spot disease in the giant tiger shrimp, Penaeus monodon (Fabricius), and the kuruma shrimp, Penaeus japonicus (Bate), cultured in Taiwan. Journal of fish Diseases. 1997, 20: 323-331. 10.1046/j.1365-2761.1997.00301.x.

Inoue H, Ozaki N, Nagasawa H: Purification and Structural Determination of a Phosphorylated Peptide with Anti-calcification and Chitin-binding Activities in the Exoskeleton of the Crayfish, Procambarus clarkii. Biosci Biotechnol Biochem. 2001, 65: 1840-1848. 10.1271/bbb.65.1840.

Inoue H, Ohira T, Ozaki N, Nagasawa H: Cloning and expression of a cDNA encoding a matrix peptide associated with calcification in the exoskeleton of the crayfish. Comp Biochem Physiol B Biochem Mol Biol. 2003, 136: 755-765. 10.1016/S1096-4959(03)00210-0.

Okazaki Y, Shizuri Y: Structures of six cDNAs expressed specifically at cypris larvae of barnacles, Balanus amphitrite. Gene. 2000, 250: 127-135. 10.1016/S0378-1119(00)00184-0.

Lehnert SA, Johnson SE: Expression of hemocyanin and digestive enzyme messenger RNAs in the hepatopancreas of the Black Tiger Shrimp Penaeus monodon. Comp Biochem Physiol B Biochem Mol Biol. 2002, 133: 163-171. 10.1016/S1096-4959(02)00123-9.

Elvin CM, Vuocolo T, Pearson RD, East IJ, Riding GA, Eisemann CH, Tellam RL: Characterization of a major peritrophic membrane protein, peritrophin-44, from the larvae of Lucilia cuprina. cDNA and deduced amino acid sequences. J Biol Chem. 1996, 271: 8925-8935. 10.1074/jbc.271.15.8925.

Shen Z, Jacobs-Lorena M: A type I peritrophic matrix protein from the malaria vector Anopheles gambiae binds to chitin. Cloning, expression, and characterization. J Biol Chem. 1998, 273: 17665-17670. 10.1074/jbc.273.28.17665.

Lehane MJ: Peritrophic matrix structure and function. Annu Rev Entomol. 1997, 42: 525-505. 10.1146/annurev.ento.42.1.525.

Gaines PJ, Walmsley SJ, Wisnewski N: Cloning and characterization of five cDNAs encoding peritrophin A domains from the cat flea, Ctenocephalides felis. Insect Biochem Mol Biol. 2003, 33: 1061-1073. 10.1016/S0965-1748(03)00096-1.

Khayat M, Babin PJ, Funkenstein B, Sammar M, Nagasawa H, Tietz A, Lubzens E: Molecular characterization and high expression during oocyte development of a shrimp ovarian cortical rod protein homologous to insect intestinal peritrophins. Biol Reprod. 2001, 64: 1090-9. 10.1095/biolreprod64.4.1090.

Kim YK, Kawazoe I, Tsutsui N, Jasmani S, Wilder MN, Aida K: Isolation and cDNA cloning of ovarian cortical rod protein in kuruma prawn Marsupenaeus japonicus (Crustacea: Decapoda: Penaeidae). Zoolog Sci. 2004, 21: 1109-19. 10.2108/zsj.21.1109.

Du XJ, Wang JX, Liu N, Zhao XF, Li FH, Xiang JH: Identification and molecular characterization of a peritrophin-like protein from fleshy prawn (Fenneropenaeus chinensis). Mol Immunol. 2006, 43: 1633-44. 10.1016/j.molimm.2005.09.018.

Weis WI, Taylor ME, Drickamer K: The C-type lectin superfamily in the immune system. Immunol Rev. 1998, 163: 19-34. 10.1111/j.1600-065X.1998.tb01185.x.

Yu XQ, Gan H, Kanost MR: Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenol oxidase. Insect Biochem Mol Biol. 1999, 29: 585-597. 10.1016/S0965-1748(99)00036-3.

Suzuki T, Takagi T, Furukohri T, Kawamura K, Nakauchi M: A calcium-dependent galactose-binding lectin from the tunicate Polyandrocarpa misakiensis. Isolation, characterization, and amino acid sequence. J Biol Chem. 1990, 265: 1274-1281.

Luo T, Yang H, Li F, Zhang X, Xu X: Purification, characterization and cDNA cloning of a novel lipopolysaccharide-binding lectin from the shrimp Penaeus monodon. Dev Comp Immunol. 2006, 30: 607-17. 10.1016/j.dci.2005.10.004.

Liu YC, Li FH, Dong B, Wang B, Luan W, Zhang XJ, Zhang LS, Xiang JH: Molecular cloning, characterization and expression analysis of a putative C-type lectin (Fclectin) gene in Chinese shrimp Fenneropenaeus chinensis. Mol Immunol. 2007, 44: 598-607. 10.1016/j.molimm.2006.01.015.

Luo T, Zhang XB, Shao ZZ, Xu X: PmAV, a novel gene involved in virus resistance of shrimp Penaeus monodon. FEBS Lett. 2003, 551: 53-57. 10.1016/S0014-5793(03)00891-3.

Wnuk W, Jauegai-Adell J: Polymorphism in high affinity calcium binding proteins from crustacean sarcoplasm. Eur J Biochem. 1983, 131: 177-182. 10.1111/j.1432-1033.1983.tb07246.x.

Takagi T, Konishi K: Amino acid sequence of alpha chain of sarcoplasmic calcium binding protein obtained from shrimp tail muscle. J Biochem. 1984, 95: 1603-1615.

Takagi T, Konishi K: Amino acid sequence of beta chain of sarcoplasmic calcium binding protein (SCP) obtained from shrimp tail muscle. J Biochem. 1984, 96: 59-67.

Gao Y, Gilen CM, Wheatly MG: Molecular characterization of the sarcoplasmic calcium-binding protein (SCP) from crayfish Procambarus clarkii. Comp Biochem Physiol B Biochem Mol Biol. 2006, 144: 478-87. 10.1016/j.cbpb.2006.04.007.

Sirover MA: Emerging new functions of the glycolytic protein, glyceraldehydes-3-phosphate dehydrogenase, in mammalian cells. Life Sci. 1996, 58: 2271-2272. 10.1016/0024-3205(96)00123-3.

Sirover MA: New insights into an old protein: the functional diversity of mammalian glyceraldehydes-3-phosphate dehydrogenase. Biochim Biophys Acta. 1999, 1432: 159-184.

Kim JW, Dang CV: Multifaceted roles of glycolytic enzymes. Trends Biochem Sci. 2005, 30: 142-150. 10.1016/j.tibs.2005.01.005.

Miles LA, Dahlberg CM, Plescia J, Felez J, Kato K, Plow EF: Role of cell-surface lysines in plasminogen binding to cells: identification of alpha-enolase as a candidate plasminogen receptor. Biochemistry. 1991, 30: 1682-1691. 10.1021/bi00220a034.

Redlitz A, Flowler BJ, Plow EF, Miles LA: The role of an enolase-related molecule in plasminogen binding to cells. Eur J Biochem. 1995, 227: 407-415. 10.1111/j.1432-1033.1995.tb20403.x.

Ogino T, Yamadera T, Nonaka T, Imajoh-Ohmi S, Mizumoto K: Enolase, a cellular glycolytic enzyme, is required for efficient transcription of Sendai virus genome. Biochem Biophys Res Commun. 2001, 285: 447-455. 10.1006/bbrc.2001.5160.

Aaronson RM, Graven KK, Tucci M, McDonald RJ, Farber HW: Non-neuronal enolase is an endothelial hypoxic stress protein. J Biol Chem. 1995, 270: 27752-27757. 10.1074/jbc.270.46.27752.

Radovanovic J, Todorovic V, Boricic I, Jankovic-Hladni M, Korac A: Comparative ultrastructural studies on mitochondrial pathology in the liver of AIDS patients: clusters of mitochondria, protuberances, "minimitochondria," vacuoles, and virus-like particles. Ultrastruct Pathol. 1999, 23: 19-24. 10.1080/019131299281798.

D'Agostino DM, Ranzato L, Arrigoni G, Cavallari I, Belleudi F, Torrisi MR, Silic-Benussi M, Ferro T, Petronilli V, Marin O, Chieco-Bianchi L, Bernardi P, Ciminale V: Mitochondrial alterations induced by the p13II protein of human T-cell leukemia virus type I. Critical role of arginine residues. J Biol Chem. 2002, 277: 34424-34433. 10.1074/jbc.M203023200.

Lee JY, Marshall JA, Bowden DS: Localization of rubella virus core particles in Vero cells. Virology. 1999, 265: 110-119. 10.1006/viro.1999.0016.

Murata T, Goshima F, Daikoku T, Inagaki-Ohara K, Takakuwa H, Kato K, Nishiyama Y: Mitochondrial distribution and function in herpes simplex virus-infected cells. J Gen Virol. 2000, 81: 401-406.

Takada S, Shirakata Y, Kaneniwa N, Koike K: Association of hepatitis B virus X protein with mitochondria casuses mitochondrial aggregation at the nuclear periphery, leading to cell death. Oncogene. 1999, 18: 6965-6973. 10.1038/sj.onc.1203188.

Norkin LC: Cell killing by simian virus 40: impairment of membrane formation and function. J Virol. 1977, 21: 872-879.

Koundouris A, Kass GE, Johnson CR, Boxall A, Sanders PG, Carter MJ: Poliovirus induces an early impairment of mitochondrial function by inhibiting succinate dehydrogenase activity. Biochem Biophys Res Commun. 2000, 271: 610-4. 10.1006/bbrc.2000.2675.

Derakhshan M, Willcocks MM, Salako MA, Kass GEN, Carter MJ: Human herpesvirus 1 proteins Us3 induces an inhibition of mitochondrial electron transport. J Gen Vriol. 2006, 87: 2155-2159. 10.1099/vir.0.81949-0.

Pollard TD: Actin. Curr Opin Cell Biol. 1990, 2: 33-40. 10.1016/S0955-0674(05)80028-6.

Durica DS, Schloss JA, Crain WR: Organization of actin gene sequences in the sea urchin: molecular cloning of an intron containing DNA sequence coding for a cytoplasmic actin. Proc Natl Acad Sci USA. 1980, 77: 5683-5687. 10.1073/pnas.77.10.5683.

Radtke K, Dohner K, Sodeik B: Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Microbiol. 2006, 8: 387-400. 10.1111/j.1462-5822.2005.00679.x.

Rice AP, Roberts BE: Vaccinia virus induces cellular mRNA degradation. J Virol. 1983, 47: 529-39.

Strom T, Frenkel N: Effects of herpes simplex virus on mRNA stability. J Virol. 1987, 61: 2198-207.

Xie X, Yang F: Interaction of white spot syndrome virus VP26 protein with actin. Virology. 2005, 336: 93-9. 10.1016/j.virol.2005.03.011.

Hooper SL, Thuma JB: Invertebrate muscles: muscle-specific genes and proteins. Physiol Rev. 2005, 85: 1001-1060. 10.1152/physrev.00019.2004.

Fyrberg EA, Bond BJ, Hershey ND, Mixter KS, Davidson N: The actin genes of Drosophila: protein coding regions are highly conserved but intron positions are not. Cell. 1981, 24: 107-16. 10.1016/0092-8674(81)90506-7.

Vandekerckhove J, Weber K: Chordate muscle actins differ distinctly from invertebrate muscle actins. The evolution of the different vertebrate muscle actins. J Mol Biol. 1984, 179: 391-413. 10.1016/0022-2836(84)90072-X.

Wang CH, Lo CF, Leu JH, Chou CM, Yeh PY, Chou HY, Tung MC, Chang CF, Su MS, Kou GH: Purification and genomic analysis of baculovirus associated with white spot syndrome (WSBV) of Panaeus monodon. Dis Aquat Org. 1995, 23: 239-242.

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol. 1990, 215: 403-10.

Hwang DM, Dempsey AA, Lee CY, Liew CC: Identification of differentially expressed genes in cardiac hypertrophy by analysis of expressed sequence tags. Genomics. 2000, 66: 1-14. 10.1006/geno.2000.6171.

Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O'Donovan C, Redaschi N, Yeh LS: UniProt: the Universal Protein knowledgebase. Nucleic Acids Res. 2004, 32: D115-11971. 10.1093/nar/gkh131.

Fisher RA: Statistical Methods and Scientific Inference. 1973, New York: Macmillan Hafner, 3

Schmitt AO, Specht T, Beckmann G, Dahl E, Pilarsky CP, Hinzmann B, Rosenthal A: Exhaustive mining of EST libraries for genes differentially expressed in normal and tumour tissues. Nucleic Acids Res. 1999, 27: 4251-4260. 10.1093/nar/27.21.4251.

Chen Z, Wang W, Ling XB, Liu JJ, Chen L: GO-Diff: mining functional differentiation between EST-based transcriptomes. BMC bioinformatics. 2006, 7: 72-10.1186/1471-2105-7-72.

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