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Gene Expression Profile of Hemocytes of Kuruma Shrimp, Marsupenaeus japonicus Following Peptidoglycan Stimulation

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Abstract

Shrimps are believed to lack an adaptive immune system and therefore rely heavily on their innate immune mechanisms to ward off pathogens. Moreover, their innate defense reactions are triggered by bacterial and fungal cell wall components such as lipopolysaccharides, peptidoglycan and β-glucans. In this study, we used microarray to examine the gene expression profile of kuruma shrimp, Marsupenaeus japonicus, after stimulation with peptidoglycan. Subsequent results show that the number of upregulated genes and percentage of differential expression (21%) was highest at day 1 poststimulation. Differentially expressed genes in day 7 and day 14, on the other hand, were 3.25% and 11.21%, respectively. Sixty-one (61) genes of unknown function were found to have responded outright to peptidoglycan (PG) stimulation. Administration of PG also caused increases in the expressions of crustin, lysozyme, and a few antibacterial peptides, all of which are known to be involved in crustacean immune response. Taken together, our results suggest that innate response in shrimp is triggered instantaneously upon exposure to a bacterial component.

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References

  • Amparyup P, Kondo H, Hirono I, Aoki T, Tassanakajon A (2008) Molecular cloning, genomic organization and recombinant expression of a crustin-like antimicrobial peptide from black tiger shrimp Penaeus monodon. Mol Immunol 45:1085–1093

    Article  PubMed  CAS  Google Scholar 

  • Auslander M, Yudkovski Y, Chalifa-Caspi V, Herut B, Ophir R, Reinhardt R, Neumann PM, Tom M (2008) Pollution-affected fish hepatic transcriptome and its expression patterns on exposure to cadmium. Mar Biotechnol 10(3):250–261

    Article  PubMed  CAS  Google Scholar 

  • Azad I, Panigrahi A, Gopal C, Paulpandi S, Mahima C, Ravichandran P (2005) Routes of Immunostimulation vis-à-vis survival and growth of Penaeus monodon postlarvae. Aquaculture 248:227–234

    Article  Google Scholar 

  • Bachere E, Gueguen Y, Gonzalez M, De Lorgeril J, Garnier J, Romestand B (2004) Insights into the anti-microbial defense of marine invertebrates: the penaeid shrimps and the oyster Crassostrea gigas. Immunol Rev 198:149–168

    Article  PubMed  CAS  Google Scholar 

  • Chang CF, Chen HY, Su MS, Liao IC (2000) Immunomodulation by dietary beta-1, 3-glucan in the brooders of the black tiger shrimp Penaeus monodon. Fish Shellfish Immunol 10:505–514

    Article  PubMed  CAS  Google Scholar 

  • Chang CF, Su MS, Chen HY, Liao IC (2003) Dietary beta-1,3-glucan effectively improves immunity and survival of Penaeus monodon challenged with white spot syndrome virus. Fish Shellfish Immunol 15:297–310

    Article  PubMed  CAS  Google Scholar 

  • Citarasu T, Sivaram V, Immanuel G, Rout N, Murugan V (2006) Influence of selected Indian immunostimulant herbs against white spot syndrome virus (WSSV) infection in black tiger shrimp, Penaeus monodon with reference to haematological, biochemical and immunological changes. Fish Shellfish Immunol 21:372–384

    Article  PubMed  Google Scholar 

  • Darias MJ, Zambonino-Infante JL, Hugot K, Cahu CL, Mazurais D (2008) Gene expression patterns during the larval development of European sea bass (Dicentrarchus labrax) by microarray analysis. Mar Biotechnol (NY) 10:416-428

    Article  CAS  Google Scholar 

  • Decook R, Nettleton D, Foster C, Es W (2006) Identifying differentially expressed genes in unreplicated multi-treatment microarray timecourse experiments. Comput Stat Data Anal 50:518–532

    Article  Google Scholar 

  • De Hoon M, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453–1454

    Article  PubMed  CAS  Google Scholar 

  • Dhar A, Dettori A, Roux M, Klimpel K, Read B (2003) Identification of differentially expressed genes in shrimp (Penaeus stylirostis) infected with White Spot Syndrome Virus by cDNA microarrays. Arch Virol 148:2381–2396

    Article  PubMed  CAS  Google Scholar 

  • Duojiao N, Song L, Wu L, Chang Y, Yu Y, Qui L, Wang L (2007) Molecular cloning and mRNA expression of peptidoglycan recognition protein (PGRP) gene in bay scallop (Argopecten irradians, Lamarck 1819). Dev Comp Immunol 31:548–558

    Article  CAS  Google Scholar 

  • Guan R, Mariuzza RA (2007) Peptidoglycan recognition proteins of the innate immune system. Trends Microbiol 15:127–134

    Article  PubMed  CAS  Google Scholar 

  • Hou WY, Chen JC (2005) The immunostimulatory effect of hot-water extract of Gracilaria tenuistipitata on the white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Fish Shellfish Immunol 19:127–138

    PubMed  Google Scholar 

  • Itami T, Kondo M, Uozu M, Suganuma A, Abe T, Nakagawa A, Suzuki N, Takahashi Y (1996) Enhancement of disease resistance against Enterococcus seriolicida infection in yellowtail Seriola quinqueradiata Temminck and Schlegel by oral administration of peptidoglycan derived from Bifidobacterium thermophilum. J Fish Dis 19:185–187

    Article  CAS  Google Scholar 

  • Itami T, Asano M, Tokushige K, Kubono K, Nakagawa A, Takeno N, Nishimura H, Maeda M, Kondo M, Takahashi Y (1998) Enhancement of disease resistance of kuruma shrimp, Panaeus japonicus, after oral administration of peptidoglycan derived from Bifobacterium thermophilium. Aquaculture 164:277–288

    Article  CAS  Google Scholar 

  • Jenny MJ, Chapman RW, Mancia A, Chen YA, Mckillen DJ, Trent H, Lang P, Escoubas JM, Bachere E, Boulo V, Liu ZJ, Gross PS, Cunningham C, Cupit PM, Tanguy A, Guo X, Moraga D, Boutet I, Huvet A, De Guise S, Almeida JS, Warr GW (2007) A cDNA microarray for Crassostrea virginica and C. gigas. Mar Biotechnol 9:577–591

    Article  PubMed  CAS  Google Scholar 

  • Khadijah S, Neo S, Hossain M, Miller L, Mathavan S, Kwang J (2003) Identification of White Spot Syndrome Virus latency-related genes in specific-pathogen-free shrimps by use of a microarray. J Virol 77:10162–10167

    Article  PubMed  CAS  Google Scholar 

  • Klannukarn SS, Wongprasert K (2004) Vibrio bacterin and carboxymenthyl b-1,-3-glucans protect Penaeus monodon from Vibrio harveyi infection. J Aquat Anim Health 16:238–245

    Article  Google Scholar 

  • Kochzius M, Nolte M, Weber H, Silkenbeumer N, Hjorleifsdottir S, Hreggvidsson GO, Marteinsson V, Kappel K, Planes S, Tinti F, Magoulas A, Garcia Vazquez E, Turan C, Hervet C, Campo Falgueras D, Antoniou A, Landi M, Blohm D (2008) DNA microarrays for identifying fishes. Mar Biotechnol (NY) 10:207–217

    Article  CAS  Google Scholar 

  • Kong HJ, Cho HK, Park E-M, Hong G-E, Kim Y-O, Nam B-H, Kim W-J, Lee S-J, Han HS, Jang I-K, Lee CH, Cheong JH, Choi T-J (2008). Molecular cloning of Kazal-type proteinase inhibitor of the shrimp Fenneropenaeus chinensis. Fish Shellfish Immunol DOI 10.1016/j.fsi.2008.03.023

  • Kurobe T, Yasuike M, Kimura T, Hirono I, Aoki T (2005) Expression profiling of immune-related genes from Japanese flounder Paralichthys olivaceus kidney cells using cDNA microarrays. Dev Comp Immunol 29:515–523

    Article  PubMed  CAS  Google Scholar 

  • Lan Y, Xu X, Yang F, Zhang X (2006) Transcriptional profile of shrimp white spot syndrome virus (WSSV) genes with DNA microarray. Arch Virol 151:1723–1733

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Söderhäll K (2002) Early events in crustacean innate immunity. Fish Shellfish Immunol 12:421–437

    Article  PubMed  CAS  Google Scholar 

  • Lewin B (2004) Genes VIII. Pearson Education, Inc, Pearson Prentice Hall

    Google Scholar 

  • Liu WJ, Chang YS, Wang CH, Kou GH, Lo CF (2005) Microarray and RT-PCR screening for white spot syndrome virus immediate-early genes in cycloheximide-treated shrimp. Virology 334:327–341

    Article  PubMed  CAS  Google Scholar 

  • Maningas MB, Kondo H, Hirono I, Saito-Taki T, Aoki T (2008) Essential function of transglutaminase and clotting protein in shrimp immunity. Mol Immunol 45:1269–1275

    Article  PubMed  CAS  Google Scholar 

  • Marks H, Vorst O, Van Houwelingen AM, Van Hulten MC, Vlak JM (2005) Gene-expression profiling of White spot syndrome virus in vivo. J Gen Virol 86:2081–2100

    Article  PubMed  CAS  Google Scholar 

  • Matsuo K, Miyazano I (1993) The influence of long-term administration of peptidoglucan on disease resistance and growth of juvenile rainbow trout. Nippon Suisan Gakkaishi 59:1377–1379

    Google Scholar 

  • McDonald C, Inohara N, Nunez G (2005) Peptidoglycan signaling in innate immunity and inflammatory disease. J Biol Chem 280:20177–20180

    Article  PubMed  CAS  Google Scholar 

  • Misra CK, Das BK, Pradhan J, Pattnaik P, Sethi S, Mukherjee SC (2004) Changes in lysosomal enzyme activity and protection against Vibrio infection in Macrobrachium rosenbergii (De Man) post larvae after bath immunostimulation with beta-glucan. Fish Shellfish Immunol 17:389–395

    Article  PubMed  CAS  Google Scholar 

  • Moriya S, Sato S, Azumaya T, Suzuki O, Urawa S, Urano A, Abe S (2007) Genetic stock identification of chum salmon in the Bering Sea and North Pacific Ocean using mitochondrial DNA microarray. Mar Biotechnol (NY) 9:179–191

    Article  CAS  Google Scholar 

  • Okumura T (2007) Effects of lipopolysaccharides on gene expression of antibacterial peptides (penaeidins and crustin), serine proteinase and prophenoloxidase in haemocytes of the Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 22:68–76

    Article  PubMed  CAS  Google Scholar 

  • Peng X, Wood CL, Blalock EM, Chen KC, Landfield PW, Stromberg AJ (2003) Statistical implications of pooling RNA samples for microarray experiments. BMC Bioinformatics 4:26–35

    Article  PubMed  Google Scholar 

  • Rattanachai A, Hirono I, Ohira T, Takahashi Y, Aoki T (2004) Cloning of kuruma prawn Marsupenaeus japonicus crustin-like peptide cDNA and analysis of its expression. Fish Sci 70:765–771

    Article  CAS  Google Scholar 

  • Rattanachai A, Hirono I, Ohira T, Takahashi Y, Aoki T (2005) Peptidoglycan inducible expression of a serine proteinase homologue from kuruma shrimp (Marsupenaeus japonicus). Fish Shellfish Immunol 18:39–48

    Article  PubMed  CAS  Google Scholar 

  • Rojtinnakorn J, Hirono I, Itami T, Takahashi Y, Aoki T (2002) Gene expression in haemocytes of kuruma prawn, Penaeus japonicus, in response to infection with WSSV by EST approach. Fish Shellfish Immunol 13:69–83

    Article  PubMed  CAS  Google Scholar 

  • Sakai M (1999) Current research status of fish immunostimulants. Aquaculture 172:63–92

    Article  CAS  Google Scholar 

  • Saldanha AJ (2004) Java Treeview—extensible visualization of microarray data. Bioinformatics 20:3246–3248

    Article  PubMed  CAS  Google Scholar 

  • Smith VJ, Brown JH, Hauton C (2003) Immunostimulation in crustaceans: does it really protect against infection? Fish Shellfish Immunol 15:71–90

    Article  PubMed  Google Scholar 

  • Song YL, Liu JJ, Chan LC, Sung HH (1997) Glucan-induced disease resistance in tiger shrimp (Penaeus monodon). Dev Biol Stand 90:413–421

    PubMed  CAS  Google Scholar 

  • Sritunyalucksana K, Sithisarn P, Withayachumnarnkul B, Flegel T (1999) Activation of prophenoloxidase, agglutinin and antibacterial activity in haemolymph of the black tiger prawn, Penaeus monodon, by immunostimulants. Fish Shellfish Immunol 9:21–30

    Article  Google Scholar 

  • Stears RL, Martinsky T, Schena M (2003) Trends in microarray analysis. Nat Med 9:140–145

    Article  PubMed  CAS  Google Scholar 

  • Steiner H (2004) Peptidoglycan recognition proteins: on and off switches for innate immunity. Immunol Rev 198:83–96

    Article  PubMed  CAS  Google Scholar 

  • Supungul P, Klinbunga S, Pichyangkura R, Jitrapakdee S, Hirono I, Aoki T, Tassanakajon A (2002) Identification of immune-related genes in hemocytes of black tiger shrimp (Penaeus monodon). Mar Biotechnol (NY) 4:487–494

    Article  CAS  Google Scholar 

  • Supungul P, Tang S, Maneeruttanarungroj C, Rimphanitchayakit V, Hirono I, Aoki T, Tassanakajon A (2008) Cloning, expression and antimicrobial activity of crustinPm1, a major isoform of crustin, from the black tiger shrimp Penaeus monodon. Dev Comp Immunol 32:61–70

    Article  PubMed  CAS  Google Scholar 

  • Takahashi Y, Kondo M, Itami T, Honda T, Inagawa H, Nishizawa T, Soma G-I, Yokomizo Y (2000) Enhancement of disease resistance against penaeid acute viraemia and induction of virus-activating activity in haemolymph of kuruma shrimp, Penaeus japonicus, by oral administration of Pantoea agglomerans lipopolysaccharide (LPS). Fish Shellfish Immunol 10:555–558

    Article  PubMed  CAS  Google Scholar 

  • Tincu JA, Taylor SW (2004) Antimicrobial peptides from marine invertebrates. Antimicrob Agents Chemother 48:3645–3654

    Article  PubMed  CAS  Google Scholar 

  • Tsai JM, Wang HC, Leu JH, Hsiao HH, Wang AH, Kou GH, Lo CF (2004) Genomic and proteomic analysis of thirty-nine structural proteins of shrimp white spot syndrome virus. J Virol 78:11360–11370

    Article  PubMed  CAS  Google Scholar 

  • Tyagi A, Khushiramani R, Karunasagar I, Karunasagar I (2007) Antivibrio activity of recombinant lysozyme expressed from black tiger shrimp, Penaeus monodon. Aquaculture 272:246–253

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wongpanya R, Yasuike M, Aoki T, Hirono I, Tassanakjon A (2007) Analysis of gene expression in haemocyte of shrimp Penaeus monodon challenged with white spot syndrome virus by cDNA microarray. Sci Asia 33:165–174

    Article  CAS  Google Scholar 

  • Yasuike Y, Kondo H, Hirono I, Aoki T (2006) Difference in Japanese flounder, Paralichthys olivaceus gene expression profile following hirame rhabdovirus (HIRRV) G and N protein DNA vaccination. Fish Shellfish Immunol 23:531–541

    Article  PubMed  CAS  Google Scholar 

  • Yeh ST, Lee CS, Chen JC (2006) Administration of hot-water extract of brown seaweed Sargassum duplicatum via immersion and injection enhances the immune resistance of white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 20:332–345

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported in part by Grants-in-Aid for Scientific Researches from the Ministry of Education, Culture, Sports, Science and Technology of Japan and the grant from the Japan Science and Technology Corporation (JST); Creation and Support Program for Start-ups from Universities. Special thanks to Mr. Mudjekeewis D. Santos for proofreading the manuscript.

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Correspondence to Takashi Aoki.

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Supplementary Table 1

Differentially expressed genes in each sampling period (DOC 292 KB)

Supplementary Table 2

Overview of clustered genes with their corresponding deduced functions (DOC 215 KB)

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Fagutao, F.F., Yasuike, M., Caipang, C.M. et al. Gene Expression Profile of Hemocytes of Kuruma Shrimp, Marsupenaeus japonicus Following Peptidoglycan Stimulation. Mar Biotechnol 10, 731–740 (2008). https://doi.org/10.1007/s10126-008-9110-0

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  • DOI: https://doi.org/10.1007/s10126-008-9110-0

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