Marine Biotechnology

, Volume 20, Issue 1, pp 87–97 | Cite as

The Voltage-Dependent Anion Channel (VDAC) of Pacific Oysters Crassostrea gigas Is Upaccumulated During Infection by the Ostreid Herpesvirus-1 (OsHV-1): an Indicator of the Warburg Effect

  • Lizenn Delisle
  • Marine Fuhrmann
  • Claudie Quéré
  • Marianna Pauletto
  • Vianney Pichereau
  • Fabrice Pernet
  • Charlotte Corporeau
Original Article

Abstract

Voltage-dependent anion channel (VDAC) is a key mitochondrial protein. VDAC drives cellular energy metabolism by controlling the influx and efflux of metabolites and ions through the mitochondrial membrane, playing a role in its permeabilization. This protein exerts a pivotal role during the white spot syndrome virus (WSSV) infection in shrimp, through its involvement in a particular metabolism that plays in favor of the virus, the Warburg effect. The Warburg effect corresponds to an atypical metabolic shift toward an aerobic glycolysis that provides energy for rapid cell division and resistance to apoptosis. In the Pacific oyster Crassostrea gigas, the Warburg effect occurs during infection by Ostreid herpesvirus (OsHV-1). At present, the role of VDAC in the Warburg effect, OsHV-1 infection and apoptosis is unknown. Here, we developed a specific antibody directed against C. gigas VDAC. This tool allowed us to quantify the tissue-specific expression of VDAC, to detect VDAC oligomers, and to follow the amount of VDAC in oysters deployed in the field. We showed that oysters sensitive to a mortality event in the field presented an accumulation of VDAC. Finally, we propose to use VDAC quantification as a tool to measure the oyster susceptibility to OsHV-1 depending on its environment.

Keywords

Voltage-dependent anion channel Warburg effect Crassostrea gigas Ostreid herpes virus 

Notes

Acknowledgments

We are grateful to Ifremer and the French ministry of agriculture for partly supporting this study. We acknowledge E. Harney for his help in editing English. The authors are grateful to Bruno Petton and the Ifremer staff involved in oyster and algae production Argenton for their help and delivery of animals used in the study. We thank the shellfish network Resco II (http://wwz.ifremer.fr/observatoire_conchylicole).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Barbosa Solomieu V, Renault T, Travers M-A (2015) Mass mortality in bivalves and the intricate case of the Pacific oyster, Crassostrea gigas. J Invertebr Pathol 131:2–10CrossRefPubMedGoogle Scholar
  2. Brahimi-Horn MC, Lacas-Gervais S, Adaixo R, Ilc K, Rouleau M, Notte A, Dieu M, Michiels C, Voeltzel T, Maguer-Satta V, Pelletier J, Ilie M, Hofman P, Manoury B, Schmidt A, Hiller S, Pouysségur J, Mazure NM (2015) Local mitochondrial-endolysosomal microfusion cleaves voltage-dependent anion channel 1 to promote survival in hypoxia. Mol Cell Biol 35(9):1491–1505CrossRefPubMedPubMedCentralGoogle Scholar
  3. Chen I-T, Aoki T, Huang Y-T, Hirono I, Chen TC, Huang JY, Chang GD, Lo CF, Wang HC (2011) White spot syndrome virus induces metabolic changes resembling the Warburg effect in shrimp hemocytes in the early stage of infection. J Virol 85(24):12919–12928CrossRefPubMedPubMedCentralGoogle Scholar
  4. Corporeau C, Tamayo D, Pernet F, Quéré C, Madec S (2014) Proteomic signatures of the oyster metabolic response to herpesvirus OsHV-1 μVar infection. J Proteome 109:176–187CrossRefGoogle Scholar
  5. Davison AJ (2005) A novel class of herpesvirus with bivalve hosts. J Gen Virol 86(1):41–53CrossRefPubMedGoogle Scholar
  6. Dégremont L (2013) Size and genotype affect resistance to mortality caused by OsHV-1 in Crassostrea gigas. Aquaculture 416–417:129–134CrossRefGoogle Scholar
  7. Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, Lagunoff M (2010) Induction of the Warburg effect by Kaposi’s sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. Proc Natl Acad Sci 107(23):10696–10701CrossRefPubMedPubMedCentralGoogle Scholar
  8. Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA, Proll SC, McDermott JE, Gritsenko MA, Zhang Q, Zhao R, Metz TO, Camp DG, Waters KM, Smith RD, Rice CM, Katze MG (2010) Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog 6(1):e1000719CrossRefPubMedPubMedCentralGoogle Scholar
  9. EFSA Panel on Animal Health and Welfare (AHAW) (2010) Scientific opinion on the increased mortality events in Pacific oysters, (Crassostrea gigas). EFSA J 8(11):1894Google Scholar
  10. EFSA (2015) Oyster mortality: oyster mortality. EFSA J 13(6):4122CrossRefGoogle Scholar
  11. Fabioux C, Corporeau C, Quillien V, Favrel P, Huvet A (2009) In vivo RNA interference in oyster—vasa silencing inhibits germ cell development. FEBS J 276(9):2566–2573CrossRefPubMedGoogle Scholar
  12. Guévélou E, Huvet A, Sussarellu R, Milan M, Guo X, Li L, Zhang G, Quillien V, Daniel JY, Quéré C, Boudry P, Corporeau C (2013) Regulation of a truncated isoform of AMP-activated protein kinase α (AMPKα) in response to hypoxia in the muscle of Pacific oyster Crassostrea gigas. J Comp Physiol B 183(5):597–611CrossRefPubMedGoogle Scholar
  13. Guo Y, Meng X, Ma J, Zheng Y, Wang Q, Wang Y, Shang H (2014) Human papillomavirus 16 E6 contributes HIF-1α induced Warburg effect by attenuating the VHL-HIF-1α interaction. Int J Mol Sci 15(5):7974–7986CrossRefPubMedPubMedCentralGoogle Scholar
  14. Holmborn T, Dahlgren K, Holeton C, Hogfors H, Gorokhova E (2009) Biochemical proxies for growth and metabolism in Acartia bifilosa (Copepoda, Calanoida). Limnol Oceanogr Methods 7(11):785–794CrossRefGoogle Scholar
  15. Hoogenboom BW, Suda K, Engel A, Fotiadis D (2007) The supramolecular assemblies of voltage-dependent anion channels in the native membrane. J Mol Biol 370(2):246–255CrossRefPubMedGoogle Scholar
  16. Jouaux A, Lafont M, Blin J-L, Houssin M, Mathieu M, Lelong C (2013) Physiological change under OsHV-1 contamination in Pacific oyster Crassostrea gigas through massive mortality events on fields. BMC Genomics 14(1):590CrossRefPubMedPubMedCentralGoogle Scholar
  17. Krause J, Hay R, Kowollik CH, Brdiczka D (1986) Cross-linking analysis of yeast mitochondrial outer membrane. Biochim Biophys Acta Biomembr 860(3):690–698CrossRefGoogle Scholar
  18. Lemasters JJ, Holmuhamedov E (2006) Voltage-dependent anion channel (VDAC) as mitochondrial governator—thinking outside the box. Biochim Biophys Acta (BBA) - Mol Basis Dis 1762(2):181–190CrossRefGoogle Scholar
  19. Leu J-H, Lin S-J, Huang J-Y, Chen TC, Lo CF (2013) A model for apoptotic interaction between white spot syndrome virus and shrimp. Fish Shellfish Immunol 34(4):1011–1017CrossRefPubMedGoogle Scholar
  20. Li Y, Zhang L, Qu T, Li L, Zhang G (2016) Characterization of oyster voltage-dependent anion channel 2 (VDAC2) suggests its involvement in apoptosis and host defense. PLoS One 11(1):e0146049CrossRefPubMedPubMedCentralGoogle Scholar
  21. Lindén M, Gellerfors P (1983) Hydrodynamic properties of porin isolated from outer membranes of rat liver mitochondria. Biochim Biophys Acta Biomembr 736(1):125–129CrossRefGoogle Scholar
  22. Lü A-J, Dong C-W, Du C-S, Zhang Q-Y (2007) Characterization and expression analysis of Paralichthys olivaceus voltage-dependent anion channel (VDAC) gene in response to virus infection. Fish Shellfish Immunol 23(3):601–613CrossRefPubMedGoogle Scholar
  23. Martel C, Wang Z, Brenner C (2014) VDAC phosphorylation, a lipid sensor influencing the cell fate. Mitochondrion 19:69–77CrossRefPubMedGoogle Scholar
  24. Mazure NM (2017) VDAC in cancer. Biochim Biophys Acta BBA Bioenerg 1858(8):665–673CrossRefGoogle Scholar
  25. Mesri EA, Feitelson MA, Munger K (2014) Human viral oncogenesis: a cancer hallmarks analysis. Cell Host Microbe 15(3):266–282CrossRefPubMedPubMedCentralGoogle Scholar
  26. Miossec L, Le Deuff R-M, Goulletquer P (2009) Alien species alert: Crassostrea gigas (Pacific oyster). ICES Coop Res Rep 299:1–41Google Scholar
  27. Moran A, Manahan D (2004) Physiological recovery from prolonged “starvation” in larvae of the Pacific oyster Crassostrea gigas. J Exp Mar Biol Ecol 306(1):17–36CrossRefGoogle Scholar
  28. Munger J, Bajad SU, Coller HA, Shenk T, Rabinowitz JD (2006) Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathog 2(12):e132CrossRefPubMedPubMedCentralGoogle Scholar
  29. Naghdi S, Hajnóczky G (2016) VDAC2-specific cellular functions and the underlying structure. Biochim Biophys Acta 1863(10):2503–2514CrossRefPubMedPubMedCentralGoogle Scholar
  30. Pedersen PL (2007) Warburg, me and hexokinase 2: multiple discoveries of key molecular events underlying one of cancers’ most common phenotypes, the “Warburg Effect”, i.e., elevated glycolysis in the presence of oxygen. J Bioenerg Biomembr 39(3):211–222CrossRefPubMedGoogle Scholar
  31. Pernet F, Barret J, Le Gall P, Corporeau C, Dégremont L, Lagarde F, Pépin JF, Keck N (2012) Mass mortalities of Pacific oysters Crassostrea gigas reflect infectious diseases and vary with farming practices in the Mediterranean Thau lagoon, France. Aquac Environ Interact 2(3):215–237CrossRefGoogle Scholar
  32. Pernet F, Lupo C, Bacher C, Whittington RJ (2016) Infectious diseases in oyster aquaculture require a new integrated approach. Philos Trans R Soc Lond B Biol Sci 371(1689):20150213CrossRefPubMedPubMedCentralGoogle Scholar
  33. Petton B, Pernet F, Robert R, Boudry P (2013) Temperature influence on pathogen transmission and subsequent mortalities in juvenile Pacific oysters Crassostrea gigas. Aquac Environ Interact 3(3):257–273CrossRefGoogle Scholar
  34. Petton B, Alunno-Bruscia M, Pernet F (2015) Factors influencing disease-induced mortality of Pacific oysters Crassostrea gigas. Aquac Environ Interact 6(3):205–222Google Scholar
  35. Poliseno L (2012) Pseudogenes: newly discovered players in human cancer. Sci Signal 5:5CrossRefGoogle Scholar
  36. Puyraimond-Zemmour D, Vignot S (2013) Le métabolisme de la cellule tumorale: l’effet Warburg. Oncologie 15(9):435–440CrossRefGoogle Scholar
  37. Ramagli LS (1999) Quantifying protein in 2-D PAGE solubilization buffers. In: Link AJ (eds) 2-D proteome analysis protocols, vol 112. Humana Pres, New YorkGoogle Scholar
  38. Renault T, Faury N, Barbosa-Solomieu V, Moreau K (2011) 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 35(7):725–735CrossRefPubMedGoogle Scholar
  39. Rostovtseva TK, Komarov A, Bezrukov SM, Colombini M (2002) VDAC channels differentiate between natural metabolites and synthetic molecules. J Membr Biol 187(2):147–156CrossRefPubMedGoogle Scholar
  40. Schikorski D, Faury N, Pepin JF, Saulnier D, Tourbiez D, Renault T (2011) 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 155(1):28–34CrossRefPubMedGoogle Scholar
  41. Segarra A, Pépin JF, Arzul I, Morga B, Faury N, Renault T (2010) 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 153(1):92–99CrossRefPubMedGoogle Scholar
  42. Segarra A, Baillon L, Tourbiez D, Benabdelmouna A, Faury N, Bourgougnon N, Renault T (2014) Ostreid herpesvirus type 1 replication and host response in adult Pacific oysters, Crassostrea gigas. Vet Res 45(1):103CrossRefPubMedPubMedCentralGoogle Scholar
  43. Shen X, Wang T, Xu D, Lu L (2014) Proteomic identification, characterization and expression analysis of Ctenopharyngodon idella VDAC1 upregulated by grass carp reovirus infection. Fish Shellfish Immunol 37(1):96–107CrossRefPubMedGoogle Scholar
  44. Su M-A, Huang Y-T, Chen I-T, Lee DY, Hsieh YC, Li CY, Ng TH, Liang SY, Lin SY, Huang SW, Chiang YA, Yu HT, Khoo KH, Chang GD, Lo CF, Wang HC (2014) An invertebrate Warburg effect: a shrimp virus achieves successful replication by altering the host metabolome via the PI3K-Akt-mTOR pathway. PLoS Pathog 10(6):e1004196CrossRefPubMedPubMedCentralGoogle Scholar
  45. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324(5930):1029–1033CrossRefPubMedPubMedCentralGoogle Scholar
  46. Wang H-C, Wang H-C, Leu J-H, Kou GH, Wang AHJ, Lo CF (2007) Protein expression profiling of the shrimp cellular response to white spot syndrome virus infection. Dev Comp Immunol 31(7):672–686CrossRefPubMedGoogle Scholar
  47. Wang H-C, Kondo H, Hirono I, Aoki T (2010) The Marsupenaeus japonicus voltage-dependent anion channel (MjVDAC) protein is involved in white spot syndrome virus (WSSV) pathogenesis. Fish Shellfish Immunol 29(1):94–103CrossRefPubMedGoogle Scholar
  48. Warburg (1956) On the origin of cancer cells. Science 123(3191):309–314CrossRefPubMedGoogle Scholar
  49. Young T, Kesarcodi-Watson A, Alfaro AC, Merien F, Nguyen TV, Mae H, Le DV, Villas-Bôas S (2017) Differential expression of novel metabolic and immunological biomarkers in oysters challenged with a virulent strain of OsHV-1. Dev Comp Immunol 73:229–245CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Ifremer, UMR 6539 CNRS/UBO/IRD/Ifremer, Laboratoire des sciences de l’Environnement Marin (LEMAR)PlouzanéFrance
  2. 2.Ifremer, Laboratoire de physiologie des invertébrés (LPI), Unité de physiologie fonctionnelle des organismes marins (PFOM), Centre Ifremer de BretagnePlouzanéFrance
  3. 3.Department of Comparative Biomedicine and Food ScienceUniversity of PadovaPadovaItaly
  4. 4.Université de Bretagne OccidentaleUMR 6539 CNRS/UBO/IRD/Ifremer, Laboratoire des sciences de l’Environnement Marin (LEMAR)PlouzanéFrance

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