Contributions of functional genomics and proteomics to the study of immune responses in the Pacific white leg shrimp Litopenaeus vannamei

Veterinary Immunology and Immunopathology

Volumn 128, Issue 1-3, 2009, Pages 110-118

  Robalino, Javier ^a   Carnegie, Ryan B ^b   O'Leary, Nuala ^a   Ouvry Patat, Severine A ^c   de la Vega, Enrique ^a   Prior, Sarah ^d   Gross, Paul S ^a,c   Browdy, Craig L ^d   Chapman, Robert W ^d   Schey, Kevin L ^c   Warr, Gregory ^a,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d SOUTH CAROLINA DEPARTMENT OF NATURAL RESOURCES   (United States)

Author keywords

Functional genomics; Proteomics; Shrimp

Indexed keywords

DOUBLE STRANDED RNA;

ANIMAL GENETICS; ANTIBACTERIAL ACTIVITY; ANTIVIRAL ACTIVITY; ARTICLE; EXPRESSED SEQUENCE TAG; FUNCTIONAL GENOMICS; FUNCTIONAL PROTEOMICS; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; IMMUNE RESPONSE; LITOPENAEUS VANNAMEI; MASS SPECTROMETRY; MEDICAL RESEARCH; MICROARRAY ANALYSIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; RNA INTERFERENCE; SHRIMP; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; TRANSCRIPTOMICS; VIRUS IMMUNITY;

ANIMALS; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENOMICS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PENAEIDAE; PROTEOMICS; RNA INTERFERENCE; RNA, DOUBLE-STRANDED;

CRUSTACEA; DECAPODA (CRUSTACEA); LITOPENAEUS VANNAMEI;

EID: 60549110465     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2008.10.329     Document Type: Article

References (65)

1. Astrofsky K.M., Roux M.M., Klimpel K.R., Fox J.G., and Dhar A.K. Isolation of differentially expressed genes from white spot virus (WSV) infected Pacific blue shrimp (Penaeus stylirostris). Arch. Virol. 147 (2002) 1799-1812
2. Bachère E., Gueguen Y., Gonzalez M., de Lorgeril J., Garnier J., and Romestand B. Insights into the anti-microbial defense of marine invertebrates: the penaeid shrimps and the oyster Crassostrea gigas. Immunol. Rev. 198 (2004) 149-168
3. Bangrak P., Graidist P., Chotigeat W., Supamattaya K., and Phongdara A. A syntenin-like protein with postsynaptic density protein (PDZ) domains produced by black tiger shrimp Penaeus monodon in response to white spot syndrome virus infection. Dis. Aquat. Organ. 49 (2002) 19-25
4. Birkemo G.A., Luders T., Andersen O., Nes I.F., and Nissen-Meyer. J. Hipposin, a histone-derived antimicrobial peptide in Atlantic halibut (Hippoglossus hippoglossus L.). Biochim. Biophys. Acta 1646 (2003) 207-215
5. Cerenius L., and Soderhall K. The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198 (2004) 116-126
6. Chinabut S., and Puttinaowarat S. The choice of disease control strategies to secure international market access for aquaculture products. Dev. Biol. (Basel) 121 (2005) 255-261
7. Cho J.H., Park I.Y., Kim H.S., Lee W.T., Kim M.S., and Kim S.C. Cathepsin D produces antimicrobial peptide parasin I from histone H2A in the skin mucosa of fish. FASEB J. 16 (2002) 429-431
8. Clavero-Salas A., Sotelo-Mundo R.R., Gollas-Galvan T., Hernandez-Lopez J., Peregrino-Uriarte A.B., Muhlia-Almazan A., and Yepiz-Plascencia G. Transcriptome analysis of gills from the white shrimp Litopenaeus vannamei infected with White spot syndrome virus. Fish Shellfish Immunol. 23 (2007) 459-472
9. Cuthbertson B.J., Shepard E.F., Chapman R.W., and Gross P.S. Diversity of the penaeidin antimicrobial peptides in two shrimp species. Immunogenetics 54 (2002) 442-445
10. Cuthbertson B.J., Yang Y., Bachère E., Bullesbach E.E., Gross P.S., and Aumelas A. Solution structure of synthetic penaeidin-4 with structural and functional comparisons with penaeidin-3. J. Biol. Chem. 280 (2005) 16009-16018
11. de la Vega E., Degnan B.M., Hall M.R., and Wilson K.J. Differential expression of immune-related genes and transposable elements in black tiger shrimp (Penaeus monodon) exposed to a range of environmental stressors. Fish Shellfish Immunol. 23 (2007) 1072-1088
12. de la Vega E., Hall M.R., Wilson K.J., Reverter A., Woods R.G., and Degnan B.M. Stress-induced gene expression profiling in the black tiger shrimp Penaeus monodon. Physiol. Genomics 31 (2007) 126-138
13. de la Vega E., O'Leary N.A., Shockey J.E., Robalino J., Payne C., Browdy C.L., Warr G.W., and Gross P.S. Anti-lipopolysaccharide factor in Litopenaeus vannamei (LvALF): a broad spectrum antimicrobial peptide essential for shrimp immunity against bacterial and fungal infection. Mol. Immunol. 45 (2008) 1916-1925
14. de Lorgeril J., Saulnier D., Janech M.G., Gueguen Y., and Bachère E. Identification of genes that are differentially expressed in hemocytes of the Pacific blue shrimp (Litopenaeus stylirostris) surviving an infection with Vibrio penaeicida. Physiol. Genomics 21 (2005) 174-183
15. Destoumieux D., Bulet P., Loew D., Van Dorsselaer A., Rodriguez J., and Bachère E. Penaeidins, a new family of antimicrobial peptides isolated from the shrimp Penaeus vannamei (Decapoda). J. Biol. Chem. 272 (1997) 28398-28406
16. Destoumieux D., Bulet P., Strub J.M., Van Dorsselaer A., and Bachère E. Recombinant expression and range of activity of penaeidins, antimicrobial peptides from penaeid shrimp. Eur. J. Biochem. 266 (1999) 335-346
17. Destoumieux D., Munoz M., Cosseau C., Rodriguez J., Bulet P., Comps M., and Bachère E. Penaeidins, antimicrobial peptides with chitin-binding activity, are produced and stored in shrimp granulocytes and released after microbial challenge. J. Cell Sci. 113 Pt 3 (2000) 461-469
18. Destoumieux-Garzon D., Saulnier D., Garnier J., Jouffrey C., Bulet P., and Bachère E. Crustacean immunity. Antifungal peptides are generated from the C terminus of shrimp hemocyanin in response to microbial challenge. J. Biol. Chem. 276 (2001) 47070-47077
19. Dhar A.K., Dettori A., Roux M.M., Klimpel K.R., and Read B. Identification of differentially expressed genes in shrimp (Penaeus stylirostris) infected with White spot syndrome virus by cDNA microarrays. Arch. Virol. 148 (2003) 2381-2396
20. Diatchenko L., Lau Y.F., Campbell A.P., Chenchik A., Moqadam F., Huang B., Lukyanov S., Lukyanov K., Gurskaya N., Sverdlov E.D., and Siebert P.D. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 6025-6030
21. Fernandes J.M., Kemp G.D., Molle M.G., and Smith V.J. Anti-microbial properties of histone H2A from skin secretions of rainbow trout. Oncorhynchus mykiss. Biochem. J. 368 (2002) 611-620
22. Fernandes J.M., Molle G., Kemp G.D., and Smith V.J. Isolation and characterisation of oncorhyncin II, a histone H1-derived antimicrobial peptide from skin secretions of rainbow trout. Oncorhynchus mykiss. Dev. Comp. Immunol. 28 (2004) 127-138
23. Griffitt R.J., Chandler G.T., Greig T.W., and Quattro J.M. Cathepsin B and glutathione peroxidase show differing transcriptional responses in the grass shrimp. Palaemonetes pugio following exposure to three xenobiotics. Environ. Sci. Technol. 40 (2006) 3640-3645
24. Gross P.S., Bartlett T.C., Browdy C.L., Chapman R.W., and Warr G.W. 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. 25 (2001) 565-577
25. He N., Liu H., and Xu X. Identification of genes involved in the response of haemocytes of Penaeus japonicus by suppression subtractive hybridization (SSH) following microbial challenge. Fish Shellfish Immunol. 17 (2004) 121-128
26. He N., Qin Q., and 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. Antiviral. Res. 66 (2005) 39-45
27. Huang X., and Madan A. CAP3: a DNA sequence assembly program. Genome Res. 9 (1999) 868-877
28. Kawasaki H., Isaacson T., Iwamuro S., and Conlon J.M. A protein with antimicrobial activity in the skin of Schlegel's green tree frog Rhacophorus schlegelii (Rhacophoridae) identified as histone H2B. Biochem. Biophys. Res. Commun. 312 (2003) 1082-1086
29. Kim H.S., Cho J.H., Park H.W., Yoon H., Kim M.S., and Kim S.C. Endotoxin-neutralizing antimicrobial proteins of the human placenta. J. Immunol. 168 (2002) 2356-2364
30. Lehnert S.A., Wilson K.J., Byrne K., and Moore S.S. Tissue-specific expressed sequence tags from the Black Tiger Shrimp Penaeus monodon. Mar. Biotechnol. (NY) 1 (1999) 465-0476
31. Leu J.H., Chang C.C., Wu J.L., Hsu C.W., Hirono I., Aoki T., Juan H.F., Lo C.F., Kou G.H., and Huang H.C. Comparative analysis of differentially expressed genes in normal and white spot syndrome virus infected Penaeus monodon. BMC Genomics 8 (2007) p120
32. Loker E.S., Adema C.M., Zhang S.M., and Kepler T.B. Invertebrate immune systems-not homogeneous, not simple, not well understood. Immunol. Rev. 198 (2004) 10-24
33. Maneeruttanarungroj C., Pongsomboon S., Wuthisuthimethavee S., Klinbunga S., Wilson K.J., Swan J., Li Y., Whan V., Chu K.H., Li C.P., Tong J., Glenn K., Rothschild M., Jerry D., and Tassanakajon A. Development of polymorphic expressed sequence tag-derived microsatellites for the extension of the genetic linkage map of the black tiger shrimp (Penaeus monodon). Anim. Genet. 37 (2006) 363-368
34. McKillen D.J., Chen Y.A., Chen C., Jenny M.J., Trent III H.F., Robalino J., McLean Jr. D.C., Gross P.S., Chapman R.W., Warr G.W., and Almeida J.S. Marine genomics: a clearing-house for genomic and transcriptomic data of marine organisms. BMC Genomics 6 (2005) p34
35. Nair S.V., Del Valle H., Gross P.S., Terwilliger D.P., and Smith L.C. Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol. Genomics 22 (2005) 33-47
36. Noga E.J., Fan Z., and Silphaduang U. Histone-like proteins from fish are lethal to the parasitic dinoflagellate Amyloodinium ocellatum. Parasitology 123 (2001) 57-65
37. O'Leary N.A., and Gross P.S. Genomic structure and transcriptional regulation of the penaeidin gene family from Litopenaeus vannamei. Gene 371 (2006) 75-83
38. O'Leary N.A., Trent III H.F., Robalino J., Peck M.E.T., McKillen D.J., and Gross P.S. Analysis of multiple tissue-specific cDNA libraries from the Pacific white leg shrimp. Litopenaeus vannamei. Int. Comp. Biol. 46 (2006) 931-939
39. Pan D., He N., Yang Z., Liu H., and Xu X. Differential gene expression profile in hepatopancreas of WSSV-resistant shrimp (Penaeus japonicus) by suppression subtractive hybridization. Dev. Comp. Immunol. 29 (2005) 103-112
40. Park C.B., Kim M.S., and Kim S.C. A novel antimicrobial peptide from Bufo bufo gargarizans. Biochem. Biophys. Res. Commun. 218 (1996) 408-413
41. Park I.Y., Park C.B., Kim M.S., and Kim S.C. Parasin I, an antimicrobial peptide derived from histone H2A in the catfish, Parasilurus asotus. FEBS Lett. 437 (1998) 258-262
42. Patat S.A., Carnegie R.B., Kingsbury C., Gross P.S., Chapman R., and Schey K.L. Antimicrobial activity of histones from hemocytes of the Pacific white shrimp. Eur. J. Biochem. 271 (2004) 4825-4833
43. Perez F., Ortiz J., Zhinaula M., Gonzabay C., Calderon J., and Volckaert F.A. Development of EST-SSR markers by data mining in three species of shrimp: Litopenaeus vannamei, Litopenaeus stylirostris, and Trachypenaeus birdy. Mar. Biotechnol. (NY) 7 (2005) 554-569
44. Preechaphol R., Leelatanawit R., Sittikankeaw K., Klinbunga S., Khamnamtong B., Puanglarp N., and Menasveta P. Expressed sequence tag analysis for identification and characterization of sex-related genes in the giant tiger shrimp Penaeus monodon. J. Biochem. Mol. Biol. 40 (2007) 501-510
45. Rattanarojpong T., Wang H.C., Lo C.F., and Flegel T.W. Analysis of differently expressed proteins and transcripts in gills of Penaeus vannamei after yellow head virus infection. Proteomics 7 (2007) 3809-3814
46. Reyes A., Salazar M., and Granja C. Temperature modifies gene expression in subcuticular epithelial cells of white spot syndrome virus-infected Litopenaeus vannamei. Dev. Comp. Immunol. 31 (2007) 23-29
47. Richards R.C., O'Neil D.B., Thibault P., and Ewart K.V. Histone H1: an antimicrobial protein of Atlantic salmon (Salmo salar). Biochem. Biophys. Res. Commun. 284 (2001) 549-555
48. Robalino J., Browdy C.L., Prior S., Metz A., Parnell P., Gross P., and Warr G. Induction of antiviral immunity by double-stranded RNA in a marine invertebrate. J. Virol. 78 (2004) 10442-10448
49. Robalino J., Bartlett T., Shepard E., Prior S., Jaramillo G., Scura E., Chapman R.W., Gross P.S., Browdy C.L., and Warr G.W. Double-stranded RNA induces sequence-specific antiviral silencing in addition to nonspecific immunity in a marine shrimp: convergence of RNA interference and innate immunity in the invertebrate antiviral response?. J. Virol. 79 (2005) 13561-13571
50. Robalino J., Almeida J.S., McKillen D., Colglazier J., Trent III H.F., Chen Y.A., Peck M.E., Browdy C.L., Chapman R.W., Warr G.W., and Gross P.S. Insights into the immune transcriptome of the shrimp Litopenaeus vannamei: tissue-specific expression profiles and transcriptomic responses to immune challenge. Physiol. Genomics 29 (2007) 44-56
51. Rojtinnakorn J., Hirono I., Itami T., Takahashi Y., and Aoki T. Gene expression in haemocytes of kuruma prawn, Penaeus japonicus, in response to infection with WSSV by EST approach. Fish Shellfish Immunol. 13 (2002) 69-83
52. Rose F.R., Bailey K., Keyte J.W., Chan W.C., Greenwood D., and Mahida Y.R. Potential role of epithelial cell-derived histone H1 proteins in innate antimicrobial defense in the human gastrointestinal tract. Infect. Immun. 66 (1998) 3255-3263
53. Somboonwiwat K., Supungul P., Rimphanitchayakit V., Aoki T., Hirono I., and Tassanakajon A. Differentially expressed genes in hemocytes of Vibrio harveyi-challenged shrimp Penaeus monodon. J. Biochem. Mol. Biol. 39 (2006) 26-36
54. Supungul P., Klinbunga S., Pichyangkura R., Jitrapakdee S., Hirono I., Aoki T., and Tassanakajon A. Identification of immune-related genes in hemocytes of black tiger shrimp (Penaeus monodon). Mar. Biotechnol. 4 (2002) 487-494
55. Supungul P., Klinbunga S., Pichyangkura R., Hirono I., Aoki T., and Tassanakajon A. Antimicrobial peptides discovered in the black tiger shrimp Penaeus monodon using the EST approach. Dis. Aquat. Organ. 61 (2004) 123-135
56. van de Braak C.B., Botterblom M.H., Huisman E.A., Rombout J.H., and van der Knaap W.P. Preliminary study on haemocyte response to white spot syndrome virus infection in black tiger shrimp Penaeus monodon. Dis. Aquat. Organ. 51 (2002) 149-155
57. Wang B., Li F., Dong B., Zhang X., Zhang C., and Xiang J. Discovery of the genes in response to white spot syndrome virus (WSSV) infection in Fenneropenaeus chinensis through cDNA microarray. Mar. Biotechnol. (NY) 8 (2006) 491-500
58. Wang H.C., Leu J.H., Kou G.H., Wang A.H., and Lo C.F. Protein expression profiling of the shrimp cellular response to white spot syndrome virus infection. Dev. Comp. Immunol. 31 (2007) 672-686
59. Watson F.L., Puttmann-Holgado R., Thomas F., Lamar D.L., Hughes M., Kondo M., Rebel V.I., and Schmucker D. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309 (2005) 1874-1878
60. Wilson K., Li Y., Whan V., Byrne L.S., Moore K., Pongsomboon S., Tassanakajon S., Rosenberg A., Ballment G., Fayazia E., Swana Z., Kenwaya J., and Benzie M.J. Genetic mapping of the black tiger shrimp Penaeus monodon with amplified fragment length polymorphism. Aquaculture 204 (2002) 185-519
61. Wu J., Lin Q., Lim T.K., Liu T., and Hew C.L. White spot syndrome virus proteins and differentially expressed host proteins identified in shrimp epithelium by shotgun proteomics and cleavable isotope-coded affinity tag. J. Virol. 81 (2007) 11681-11689
62. Zhang S.M., Adema C.M., Kepler T.B., and Loker E.S. Diversification of Ig superfamily genes in an invertebrate. Science 305 (2004) 251-254
63. Zhang Y., Wang S., Xu A., Chen J., Lin B., and Peng X. Affinity proteomic approach for identification of an IgA-like protein in Litopenaeus vannamei and study on its agglutination characterization. J. Proteome Res. 5 (2006) 815-821
64. Zhang L., Yang C., Zhang Y., Li L., Zhang X., Zhang Q., and Xiang J. A genetic linkage map of Pacific white shrimp (Litopenaeus vannamei): sex-linked microsatellite markers and high recombination rates. Genetica 131 (2007) 37-49
65. Zhao Z.Y., Yin Z.X., Weng S.P., Guan H.J., Li S.D., Xing K., Chan S.M., and He J.G. Profiling of differentially expressed genes in hepatopancreas of white spot syndrome virus-resistant shrimp (Litopenaeus vannamei) by suppression subtractive hybridisation. Fish Shellfish Immunol. 22 (2007) 520-534