Proteomic signatures of the oyster metabolic response to herpesvirus OsHV-1 μVar infection

Journal of Proteomics

Volumn 109, Issue , 2014, Pages 176-187

  Corporeau, Charlotte ^a   Tamayo, David ^a,b   Pernet, Fabrice ^a   Quéré, Claudie ^a   Madec, Stéphanie ^c  

^a Universite de Bretagne Occidentale   (France)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c UNIVERSITÉ DE BREST   (France)

Author keywords

Crassostrea gigas; Herpesvirus; Marine bivalves; Metabolism; Warburg

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CRASSOSTREA GIGAS; CYTOSKELETON; DISEASE RESISTANCE; HERPES VIRUS; HERPES VIRUS INFECTION; METABOLISM; NONHUMAN; OYSTER; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEOMICS; SHRIMP; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL ELECTROPHORESIS; ANIMAL; CRASSOSTREA; HERPESVIRIDAE; VIROLOGY;

PROTEOME;

ANIMALS; CRASSOSTREA; HERPESVIRIDAE; HERPESVIRIDAE INFECTIONS; PROTEOME; PROTEOMICS;

EID: 84904656861     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.06.030     Document Type: Article

References (91)

1. EFSA Scientific opinion of the Panel on Animal Health and Welfare on a request from the European Commission on the increased mortality events in Pacific oysters Crassostrea gigas 2010, 8:1894-1953. EFSA.
2. Pernet F., Barret J., Gall P.L., Corporeau C., Dégremont L., Lagarde F., et al. Mass mortalities of Pacific oysters Crassostrea gigas reflect infectious diseases and vary with farming practises in the Thau lagoon. Aquacult Environ Interact 2012, 2:215-237.
3. Pernet F., Lagarde F., Jeannée N., Daigle G., Barret J., Le Gall P., et al. Spatial and temporal dynamics of mass mortalities in oysters is influenced by energetic reserves and food quality. PLoS One 2014, 9:e88469.
4. Petton B., Pernet F., Robert R., Boudry P. Temperature influence on pathogen transmission and subsequent mortalities in juvenile Pacific oysters Crassostrea gigas. Aquacult Environ Interact 2013, 3:257-273.
5. Jolivel A. Analyse statistique des données de mortalité d'huîtres acquises par l'Observatoire National Conchylicole (RESCO): Rennes 2 Agrocampus Ouest 2012.
6. Oden E., Martenot C., Berthaux M., Travaillé E., Malas J.P., Houssin M. Quantification of ostreid herpesvirus 1 (OsHV-1) in Crassostrea gigas by real-time PCR: determination of a viral load threshold to prevent summer mortalities. Aquaculture 2011, 317:27-31.
7. Dégremont L., Guyader T., Tourbiez D., Pépin J.-F. Is horizontal transmission of the Ostreid herpesvirus OsHV-1 in Crassostrea gigas affected by unselected or selected survival status in adults to juveniles?. Aquaculture 2013, 408-409:51-57.
8. Peeler E.J., Reese R.A., Cheslett D.L., Geoghegan F., Power A., Thrush M.A. Investigation of mortality in Pacific oysters associated with Ostreid herpesvirus-1 μVar in the Republic of Ireland in 2009. Prev Vet Med 2012, 105:136-143.
9. Paul-Pont I., Dhand N.K., Whittington R.J. Influence of husbandry practices on OsHV-1 associated mortality of Pacific oysters Crassostrea gigas. Aquaculture 2013, 412-413:202-214.
10. Jenkins C., Hick P., Gabor M., Spiers Z., Fell S.A., Gu X., et al. Identification and characterisation of an ostreid herpesvirus-1 microvariant (OsHV-1 mu-var) in Crassostrea gigas (Pacific oysters) in Australia. Dis Aquat Organ 2013, 105:109-126.
11. Bingham P., Brangenberg N., Williams R., van Andel M. Investigation into the first diagnosis of ostreid herpesvirus type 1 in Pacific oysters. Surveillance 2013, 40:20-24.
12. Clegg T.A., Morrissey T., Geoghegan F., Martin S.W., Lyons K., Ashe S., et al. Risk factors associated with increased mortality of farmed Pacific oysters in Ireland during 2011. Prev Vet Med 2014, 113:257-267.
13. Segarra A., Pepin J.F., Arzul I., Morga B., Faury N., Renault T. Detection and description of a particular Ostreid herpesvirus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Res 2010, 153:92-99.
14. Renault T., Moreau P., Faury N., Pepin J.F., Segarra A., Webb S. Analysis of clinical ostreid herpesvirus 1 (Malacoherpesviridae) specimens by sequencing amplified fragments from three virus genome areas. J Virol 2012, 86:5942-5947.
15. Schikorski D., Renault T., Saulnier D., Faury N., Moreau P., Pepin J.F. Experimental infection of Pacific oyster Crassostrea gigas spat by ostreid herpesvirus 1: demonstration of oyster spat susceptibility. Vet Res 2011, 42.
16. Schikorski D., Faury N., Pepin J.F., Saulnier D., Tourbiez D., Renault T. Experimental ostreid herpesvirus 1 infection of the Pacific oyster Crassostrea gigas: kinetics of virus DNA detection by q-PCR in seawater and in oyster samples. Virus Res 2011, 155:28-34.
17. Wang H.-C., Wang H.-C., Leu J.-H., Kou G.-H., Wang A.H.J., Lo C.-F. Protein expression profiling of the shrimp cellular response to white spot syndrome virus infection. Dev Comp Immunol 2007, 31:672-686.
18. Huvet A., Herpin A., Degremont L., Labreuche Y., Samain J.F., Cunningham C. The identification of genes from the oyster Crassostrea gigas that are differentially expressed in progeny exhibiting opposed susceptibility to summer mortality. Gene 2004, 343:211-220.
19. Fleury E., Huvet A. Microarray analysis highlights immune response of Pacific oysters as a determinant of resistance to summer mortality. Mar Biotechnol 2012, 14:203-217.
20. Fleury E., Huvet A., Lelong C., de Lorgeril J., Boulo V., Gueguen Y., et al. Generation and analysis of a 29,745 unique Expressed Sequence Tags from the Pacific oyster (Crassostrea gigas) assembled into a publicly accessible database: the GigasDatabase. BMC Genomics 2009, 10.
21. Fleury E., Moal J., Boulo V., Daniel J.-Y., Mazurais D., Hénaut A., et al. Microarray-based identification of gonad transcripts differentially expressed between lines of Pacific oyster selected to be resistant or susceptible to summer mortality. Mar Biotechnol 2010, 12:326-339.
22. Normand J., Li R., Quillien V., Nicolas J.-L., Boudry P., Pernet F., et al. Contrasted survival under field or controlled conditions displays associations between mRNA levels of candidate genes and response to OsHV-1 infection in the Pacific oyster Crassostrea gigas. Mar Genomics 2014, 15:95-102.
23. Renault T., Faury N., Barbosa-Solomieu V., Moreau K. Suppression substractive hybridisation (SSH) and real time PCR reveal differential gene expression in the Pacific cupped oyster, Crassostrea gigas, challenged with Ostreid herpesvirus 1. Dev Comp Immunol 2011, 35:725-735.
24. Schmitt P., Santini A., Vergnes A., Degremont L., de Lorgeril J. Sequence polymorphism and expression variability of Crassostrea gigas immune related genes discriminate two oyster lines contrasted in term of resistance to summer mortalities. PLoS One 2013, 8:e75900.
25. Jouaux A., Lafont M., Blin J.-L., Houssin M., Mathieu M., Lelong C. Physiological change under OsHV-1 contamination in Pacific oyster Crassostrea gigas through massive mortality events on fields. BMC Genomics 2013, 14.
26. Suquet M., de Kermoysan G., Araya R.G., Queau I., Lebrun L., Le Souchu P., et al. Anesthesia in Pacific oyster, Crassostrea gigas. Aquat Living Resour 2009, 22:29-34.
27. Pepin J.-F., Riou A., Renault T. Rapid and sensitive detection of ostreid herpesvirus 1 in oyster samples by real-time PCR. J Virol Methods 2008, 149:269-276.
28. Le Deuff R.-M., Renault T. Purification and partial genome characterization of a herpes-like virus infecting the Japanese oyster, Crassostrea gigas. J Gen Virol 1999, 80:1317-1322.
29. Guévélou E., Huvet A., Galindo-Sanchez C.E., Milan M., Quillien V., Daniel J.-Y., et al. Sex-Specific Regulation of AMP-Activated Protein Kinase (AMPK) in the Pacific Oyster Crassostrea gigas 1. Biol Reprod 2013, 89.
30. Guévélou E., Huvet A., Sussarellu R., Milan M., Guo X., Li L., et al. Regulation of a truncated isoform of AMP-activated protein kinase alpha (AMPKalpha) in response to hypoxia in the muscle of Pacific oyster Crassostrea gigas. J Comp Physiol B 2013, 183:597-611.
31. Corporeau C., Gl Vanderplancke, Boulais M., Suquet M., Quéré C., Boudry P., et al. Proteomic identification of quality factors for oocytes in the Pacific oyster Crassostrea gigas. J Proteomics 2012, 75:5554-5563.
32. Zhang G., Fang X., Guo X., Li L., Luo R., Xu F., et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 2012, 490:49-54.
33. Thiele H., Glandorf J., Hufnagel P., Korting G., Bluggel M. Managing proteomics data: from generation and data warehousing to central data repository. J Proteomics Bioinforma 2008, 1:485-507.
34. Sauvage C., Pépin J.F., Lapègue S., Boudry P., Renault T. Ostreid herpes virus 1 infection in families of the Pacific oyster, Crassostrea gigas, during a summer mortality outbreak: differences in viral DNA detection and quantification using real-time PCR. Virus Res 2009, 142:181-187.
35. Petton B., Alunno-Bruscia M., Boudry P., Pernet F. Investigating risk factors associated with disease mortality of Pacific oysters Crassostrea gigas using standardized seed and controlled temperature elevation. Aquacult Environ Interact 2014, [in preparation].
36. Lan S., Wang H.-C., Jiang H., Maou H., Liu X., Zhang X., et al. Direct interaction between alpha-actinin and hepatitis C virus NS5. FEBS Lett 2003, 554:289-294.
37. Otey C.A., Carpen O. Alpha-actinin revisited: a fresh look at an old player. Cell Motil Cytoskeleton 2004, 58:104-111.
38. Gordon-Alonso M., Rocha-Perugini V., Alvarez S., Ursa A., Izquierdo-Useros N., Martinez-Picado J., et al. Actin-binding protein drebrin regulates HIV-1-triggered actin polymerization and viral infection. J Biol Chem 2013, 288:28382-28397.
39. Radtke K., Dahner K., Sodeik B. Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Microbiol 2006, 8:387-400.
40. Taylor M.P., Koyuncu O.O., Enquist L.W. Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol 2011, 9:427-439.
41. Li L., Liu X., Zhou Y., Wang J. On resistance to virus entry into host cells. Biophys J 2012, 102:2230-2233.
42. Lyman M.G., Enquist L.W. Herpesvirus interactions with the host cytoskeleton. J Virol 2009, 83:2058-2066.
43. Zhang H., Ghai P., Wu H., Wang C., Field J., Zhou G.-L. Mammalian CAP1 (adenylyl Cyclase-Associated Protein 1) Regulates Cofilin Function, the Actin Cytoskeleton and Cell Adhesion. J Biol Chem 2013, 288:20966-20977.
44. Chen H., Bernstein B.W., Bamburg J.R. Regulating actin-filament dynamics in vivo. Trends Biochem Sci 2000, 25:19-23.
45. Paudel N., Sadagopan S., Balasubramanian S., Chandran B. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen and angiogenin interact with common host proteins, including annexin A2, which is essential for survival of latently infected cells. J Virol 2012, 86:1589-1607.
46. Hutagalung A.H., Novick P.J. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011, 91:119-149.
47. Johns H.L., Gonzalez-Lopez C., Sayers C.L., Hollinshead M., Elliott G. Rab6 dependent post-Golgi trafficking of HSV1 envelope proteins to sites of virus envelopment. Traffic 2013, 15:157-178.
48. Porat A., Sagiv Y., Elazar Z. A 56-kDa selenium-binding protein participates in intra-Golgi protein transport. J Biol Chem 2000, 275:14457-14465.
49. Browne H., Bell S., Minson T., Wilson D.W. An endoplasmic reticulum-retained herpes simplex virus glycoprotein H is absent from secreted virions: evidence for reenvelopment during egress. J Virol 1996, 70:4311-4316.
50. Whiteley A., Bruun B., Minson T., Browne H. Effects of targeting herpes simplex virus type 1 gD to the endoplasmic reticulum and trans-Golgi network. J Virol 1999, 73:9515-9520.
51. Henaff D., Radtke K., Lippe R. Herpesviruses exploit several host compartments for envelopment. Traffic 2012, 13:1443-1449.
52. Mettenleiter T.C. Herpesvirus assembly and egress. J Virol 2002, 76:1537-1547.
53. Beck R., Ravet M., Wieland F.T., Cassel D. The COPI system: molecular mechanisms and function. FEBS Lett 2009, 583:2701-2709.
54. Hershko A., Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998, 67:425-479.
55. Boutell C., Sadis S., Everett R.D. Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases in vitro. J Virol 2002, 76:841-850.
56. 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. Antiviral Res 2005, 66:39-45.
57. Barik S. Immunophilins: for the love of proteins. Cell Mol Life Sci 2006, 63:2889-2900.
58. Watashi K., Ishii N., Hijikata M., Inoue D., Murata T., Miyanari Y., et al. Cyclophilin B is a functional regulator of hepatitis C virus RNA polymerase. Mol Cell 2005, 19:111-122.
59. Negrutskii B., El'skaya A. Eukaryotic translation elongation-factor 1-alpha, structure, expression, functions and possible role in aminoacyl-tRNA channeling. Prog Nucleic Acid Res Mol Biol 1998, 60:47-78.
60. Gourlay C.W., Carpp L.N., Timpson P., Winder S.J., Ayscough K.R. A role for the actin cytoskeleton in cell death and aging in yeast. J Cell Biol 2004, 164:803-809.
61. Lee C.-K., Han J.S., Won K.-J., Jung S.-H., Park H.-J., Lee H.M., et al. Diminished expression of dihydropteridine reductase is a potent biomarker for hypertensive vessels. Proteomics 2009, 9:4851-4858.
62. Vasiliou V., Pappa A., Petersen D.R. Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem Biol Interact 2000, 129:1-19.
63. Lin Y.P., Cheng T.J. Why can't Chinese Han drink alcohol? Hepatitis B virus infection and the evolution of acetaldehyde dehydrogenase deficiency. Med Hypotheses 2002, 59:204-207.
64. Lin Y.-R., Hung H.-C., Leu J.-H., Wang H.-C., Kou G.-H., Lo C.-F. The role of aldehyde dehydrogenase and HSP70 in suppression of white spot syndrome virus replication at high temperature. J Virol 2011, 85:3517-3525.
65. Kapoor A., He R., Venkatadri R., Forman M., Arav-Boger R. Wnt modulating agents inhibit human cytomegalovirus replication. Antimicrob Agents Chemother 2013, 57:2761-2767.
66. Cox J.A. Calcium vector protein and sarcoplasmic calcium binding proteins from invertebrate muscle. Stimulus response coupling: the role of intracellular calcium-binding proteins 1990, 83-107. J.R. Dedman, V.L. Smith (Eds.).
67. Cheshenko N., Del Rosario B., Woda C., Marcellino D., Satlin L.M., Herold B.C. Herpes simplex virus triggers activation of calcium-signaling pathways. J Cell Biol 2003, 163:283-293.
68. Mattson M.P., Chan S.L. Calcium orchestrates apoptosis. Nat Cell Biol 2003, 5:1041-1043.
69. Leu J.-H., Lin S.-J., Huang J.-Y., Chen T.-C., Lo C.-F. A model for apoptotic interaction between white spot syndrome virus and shrimp. Fish Shellfish Immunol 2013, 34:1011-1017.
70. Biradar V., Narwade S., Paingankar M., Deobagkar D. White spot syndrome virus infection in Penaeus monodon is facilitated by housekeeping molecules. J Biosci 2013, 38:917-924.
71. Davison A., Trus B., Cheng N., Steven A., Watson M., Cunningham C., et al. A novel class of herpesvirus with bivalve hosts. J Gen Virol 2005, 86:41-53.
72. Stocco D.M., Clark B.J. The role of the steroidogenic acute regulatory protein in steroidogenesis. Steroids 1997, 62:29-36.
73. Sanchez E.R. Chaperoning steroidal physiology: lessons from mouse genetic models of Hsp90 and its cochaperones. Biochim Biophys Acta - Mol Cell Res 1823, 2012:722-729.
74. Bahat A., Perlberg S., Melamed-Book N., Lauria I., Langer T., Orly J. StAR enhances transcription of genes encoding the mitochondrial proteases involved in its own degradation. Mol Endocrinol 2014, 28:208-224.
75. Chen I.-T., Aoki T., Huang Y.-T., Hirono I., Chen T.-C., Huang J.-Y., et al. White spot syndrome virus induces metabolic changes resembling the Warburg effect in shrimp hemocytes in the early stage of infection. J Virol 2011, 85:12919-12928.
76. Yu Y., Clippinger A.J., Alwine J.C. Viral effects on metabolism: changes in glucose and glutamine utilization during human cytomegalovirus infection. Trends Microbiol 2011, 19:360-367.
77. Pernet F., Barret J., Marty C., Moal J., Le Gall P., Boudry P. Environmental anomalies, energetic reserves and fatty acid modifications in oysters coincide with an exceptional mortality event. Mar Ecol Prog Ser 2010, 401:129-146.
78. Tamayo D., Corporeau C., Petton B., Quéré C., Pernet F. Physiological changes in Pacific oyster Crassostrea gigas exposed to the herpesvirus OsHV-1 μvar. Aquaculture 2014, 432:304-310.
79. Zimmerman A.W., Veerkamp J.H. New insights into the structure and function of fatty acid-binding proteins. Cell Mol Life Sci 2002, 59:1096-1116.
80. Borchers T., Spener F. Fatty acid binding proteins. Curr Top Membr 1994, 261-294.
81. Lerat H., Kammoun H.L., Hainault I., Mérour E., Higgs M.R., Callens C., et al. Hepatitis C virus proteins induce lipogenesis and defective triglyceride secretion in transgenic mice. J Biol Chem 2009, 284:33466-33474.
82. Diamond D.L., Syder A.J., Jacobs J.M., Sorensen C.M., Walters K.-A., Proll S.C., et al. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog 2010, 6:e1000719.
83. Blachly-Dyson E., Forte M. VDAC channels. IUBMB Life 2001, 52:113-118.
84. Colombini M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 2004, 256-257:107-115.
85. Boya P., Pauleau A.-L., Poncet D., Gonzalez-Polo R.-A., Zamzami N., Kroemer G. Viral proteins targeting mitochondria: controlling cell death. Biochim Biophys Acta Bioenerg 2004, 1659:178-189.
86. Wang H.-C.K.C., Kondo H., Hirono I., Aoki T. The Marsupenaeus japonicus voltage-dependent anion channel (MjVDAC) protein is involved in white spot syndrome virus (WSSV) pathogenesis. Fish Shellfish Immunol 2010, 29:94-103.
87. Maldonado E.N., Lemasters J.J. Warburg revisited: regulation of mitochondrial metabolism by voltage-dependent anion channels in cancer cells. J Pharmacol Exp Ther 2012, 342:637-641.
88. Warburg O., Posener K., Negelein E. The metabolism of cancer cells. Biochem Z 1924, 152:319-344.
89. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
90. Medina-Felix D., Lopez-Elias J.A., Martinez-Cordova L.R., Lopez-Torres M.A., Hernandez-Lopez J., Rivas-Vega M.E., et al. Evaluation of the productive and physiological responses of Litopenaeus vannamei infected with WSSV and fed diets enriched with Dunaliella sp. J Invertebr Pathol 2014, 117:9-12.
91. Vizcaíno J.A., Côté R.G., Csordas A., Dianes J.A., Fabregat A., Foster J.M., et al. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 2013, 41:D1063-D1069.