1887

Abstract

As viruses are extremely abundant in oceans, marine organisms may have evolved novel metabolites to protect themselves from viral infection. This research examined a well-known commercial gastropod, abalone (Haliotidae), which in Australia have recently experienced disease due to a neurotropic infection, abalone viral ganglioneuritis, caused by an abalone herpesvirus (AbHV). Due to the lack of molluscan cell lines for culturing AbHV, the antiviral activity of the abalone was assessed against another neurotropic herpesvirus, herpes simplex virus type 1 (HSV-1), using a plaque assay. The concentration range at which abalone extract was used for antiviral testing caused minimal (<10 %) mortality in Vero cells. Haemolymph (20 %, v/v) and lipophilic extract of the digestive gland (3000 μg ml) both substantially decreased the number and size of plaques. By adding haemolymph or lipophilic extract at different times during the plaque assay, it was shown that haemolymph inhibited viral infection at an early stage. In contrast, the antiviral effect of the lipophilic extract was greatest when added 1 h after infection, suggesting that it may act at an intracellular stage of infection. These results suggest that abalone have at least two antiviral compounds with different modes of action against viral infection, and provide a novel lead for marine antiviral drug discovery.

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2011-03-01
2024-12-07
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References

  1. Albiol Matanic, V. C. & Castilla, V.(2004). Antiviral activity of antimicrobial cationic peptides against Junin virus and herpes simplex virus. Int J Antimicrob Agents 23, 382–389.[CrossRef] [Google Scholar]
  2. Andersen, J. H., Jenssen, H. & Gutteberg, T. J.(2002). Lactoferricin inhibits the entry of HSV-1. In 27th International Herpesvirus Workshop, Cairns, Australia.
  3. Andersen, J. H., Jenssen, H. & Gutteberg, T. J.(2003). Lactoferrin and lactoferricin inhibit Herpes simplex 1 and 2 infection and exhibit synergy when combined with acyclovir. Antiviral Res 58, 209–215.[CrossRef] [Google Scholar]
  4. Andersen, J. H., Jenssen, H., Sandvik, K. & Gutteberg, T. J.(2004). Anti-HSV activity of lactoferrin and lactoferricin is dependent on the presence of heparan sulphate at the cell surface. J Med Virol 74, 262–271.[CrossRef] [Google Scholar]
  5. Banfield, B. W., Leduc, Y., Esford, L., Visalli, R. J., Brandt, C. R. & Tufaro, F.(1995). Evidence for an interaction of herpes simplex virus with chondroitin sulfate proteoglycans during infection. Virology 208, 531–539.[CrossRef] [Google Scholar]
  6. Benkendorff, K.(2010). Molluscan biological and chemical diversity: secondary metabolites and medicinal resources produced by marine molluscs. Biol Rev Camb Philos Soc 85, 757–775. [Google Scholar]
  7. Bergefall, K., Trybala, E., Johansson, M., Uyama, T., Naito, S., Yamada, S., Kitagawa, H., Sugahara, K. & Bergström, T.(2005). Chondroitin sulfate characterized by the E-disaccharide unit is a potent inhibitor of herpes simplex virus infectivity and provides the virus binding sites on gro2C cells. J Biol Chem 280, 32193–32199.[CrossRef] [Google Scholar]
  8. Bergh, O., Børsheim, K. Y., Bratbak, G. & Heldal, M.(1989). High abundance of viruses found in aquatic environments. Nature 340, 467–468.[CrossRef] [Google Scholar]
  9. Bergmann, W. & Feeney, R. J.(1951). Contributions to the study of marine products. XXXII. The nucleosides of sponges. J Org Chem 16, 981–987.[CrossRef] [Google Scholar]
  10. Bevelander, G.(1988).Abalone: Gross and Fine Structure. Pacific Grove, CA. : Boxwood Press. [Google Scholar]
  11. Bouchet, P.(2006). The magnitude of marine biodiversity. In The Exploration of Marine Biodiversity, pp. 33–64. Edited by Duarte, C. M.. Fundacion BBVA. [Google Scholar]
  12. Bradford, M. M.(1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254.[CrossRef] [Google Scholar]
  13. Browne, H. M.(2009). The role of glycoprotein H in herpesvirus membrane fusion. Protein Pept Lett 16, 760–765.[CrossRef] [Google Scholar]
  14. Chang, P. H., Kuo, S. T., Lai, S. H., Yang, H. S., Ting, Y. Y., Hsu, C. L. & Chen, H. C.(2005). Herpes-like virus infection causing mortality of cultured abalone Haliotis diversicolor supertexta in Taiwan. Dis Aquat Organ 65, 23–27.[CrossRef] [Google Scholar]
  15. Chen, H.(1996). Hemolymph collection in abalone (Haliotis diversicolor). Acta Zool 7, 61–71. [Google Scholar]
  16. Cook, P.(1998). The current status of abalone farming in South America. J Shellfish Res 17, 601–602. [Google Scholar]
  17. Davison, A. J.(2002). Evolution of the herpesviruses. Vet Microbiol 86, 69–88.[CrossRef] [Google Scholar]
  18. De Clercq, E.(2002). New anti-HIV agents and targets. Med Res Rev 22, 531–565.[CrossRef] [Google Scholar]
  19. Defer, D., Bourgougnon, N. & Fleury, Y.(2009). Detection and partial characterisation of an antimicrobial peptide (littorein) from the marine gastropod Littorina littorea. Int J Antimicrob Agents 34, 188–190.[CrossRef] [Google Scholar]
  20. Donia, M. & Hamann, M. T.(2003). Marine natural products and their potential applications as anti-infective agents. Lancet Infect Dis 3, 338–348.[CrossRef] [Google Scholar]
  21. Dunlap, W. C., Battershill, C. N., Liptrot, C. H., Cobb, R. E., Bourne, D. G., Jaspars, M., Long, P. F. & Newman, D. J.(2007). Biomedicinals from the phytosymbionts of marine invertebrates: a molecular approach. Methods 42, 358–376.[CrossRef] [Google Scholar]
  22. Egal, M., Conrad, M., MacDonald, D. L., Maloy, W. L., Motley, M. & Genco, C. A.(1999). Antiviral effects of synthetic membrane-active peptides on herpes simplex virus, type 1. Int J Antimicrob Agents 13, 57–60.[CrossRef] [Google Scholar]
  23. Einbond, L. S., Reynertson, K. A., Luo, X.-D., Basile, M. J. & Kennelly, E. J.(2004). Anthocyanin antioxidants from edible fruits. Food Chem 84, 23–28.[CrossRef] [Google Scholar]
  24. Farley, C. A., Banfield, W. G., Kasnic, G., Jr & Foster, W. S.(1972). Oyster herpes-type virus. Science 178, 759–760.[CrossRef] [Google Scholar]
  25. Faulkner, D. J.(1984). Marine natural products: metabolites of marine algae and herbivorous marine molluscs. Nat Prod Rep 1, 251–280.[CrossRef] [Google Scholar]
  26. Faulkner, D. J.(1992). Chemical defences of marine products. In Ecological Roles of Marine Natural Products, pp. 119–163. Edited by Paul, V. J.. Ithaca. : Comstock. [Google Scholar]
  27. Fegan, M., Kvalheim, N., Wong, F., Mohammad, I., Savin, K., Lancaster, M., Crane, M. S. J. & Warner, M. S.(2009). Development of an in situ hybridisation assay for the detection and identification of the abalone herpes-like virus. In 4th FRDC Aquatic Animal Health Subprogram Scientific Conference, Cairns, Australia.
  28. Fleming, A. E. & Hone, P. W.(1996). Abalone aquaculture. Aquaculture 140, 1–4.[CrossRef] [Google Scholar]
  29. Folch, J., Lees, M. & Stanley, G. H. S.(1957). A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226, 497–509. [Google Scholar]
  30. Fuhrman, J. A.(1999). Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548.[CrossRef] [Google Scholar]
  31. George, V. G., Hierholzer, J. C. & Ades, E. W.(1996). Cell culture. In Virology Methods Manual, pp. 3–23. Edited by Brian, W. J. M. & Hillar, O. K.. London. : Academic Press. [Google Scholar]
  32. Godoy, C. & Jerez, G.(1998). The introduction of abalone in Chile: ten years later. J Shellfish Res 17, 603–605. [Google Scholar]
  33. Gordon, H. R. & Cook, P. A.(2001). World abalone supply, markets and pricing: historical, current and future. J Shellfish Res 20, 567–570. [Google Scholar]
  34. Gordon, H. R. & Cook, P. A.(2004). World abalone fisheries and aquaculture update: supply and market dynamics. J Shellfish Res 23, 935–939. [Google Scholar]
  35. Hayashi, K., Hamada, J. & Hayashi, T.(1996a). A screening strategy for selection of anti-HSV-1 and anti-HIV-1 extracts from algae. Phytother Res 10, 233–237.[CrossRef] [Google Scholar]
  36. Hayashi, K., Hayashi, T. & Kojima, I.(1996b). A natural sulfated polysaccharide, calcium spirulan, isolated from Spirulina platensis: in vitro and ex vivo evaluation of anti-herpes simplex virus and anti-human immunodeficiency virus activities. AIDS Res Hum Retroviruses 12, 1463–1471.[CrossRef] [Google Scholar]
  37. Hooper, C., Hardy-Smith, P. & Handlinger, J.(2007a). Ganglioneuritis causing high mortalities in farmed Australian abalone (Haliotis laevigata and Haliotis rubra). Aust Vet J 85, 188–193.[CrossRef] [Google Scholar]
  38. Hooper, C., Day, R., Slocombe, R., Handlinger, J. & Benkendorff, K.(2007b). Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish Shellfish Immunol 22, 363–379.[CrossRef] [Google Scholar]
  39. Ivanova, V., Rouseva, R., Kolarova, M., Serkedjieva, J., Rachev, R. & Manolova, N.(1994). Isolation of a polysaccharide with antiviral effect from Ulva lactuca. Prep Biochem 24, 83–97. [Google Scholar]
  40. Jenssen, H.(2005). Anti herpes simplex virus activity of lactoferrin/lactoferricin – an example of antiviral activity of antimicrobial protein/peptide. Cell Mol Life Sci 62, 3002–3013.[CrossRef] [Google Scholar]
  41. Jenssen, H., Andersen, J. H., Mantzilas, D. & Gutteberg, T. J.(2004a). A wide range of medium-sized, highly cationic, α-helical peptides show antiviral activity against herpes simplex virus. Antiviral Res 64, 119–126.[CrossRef] [Google Scholar]
  42. Jenssen, H., Andersen, J. H., Uhlin-Hansen, L., Gutteberg, T. J. & Rekdal, Ø.(2004b). Anti-HSV activity of lactoferricin analogues is only partly related to their affinity for heparan sulfate. Antiviral Res 61, 101–109.[CrossRef] [Google Scholar]
  43. Jenssen, H., Sandvik, K., Andersen, J. H., Hancock, R. E. W. & Gutteberg, T. J.(2008). Inhibition of HSV cell-to-cell spread by lactoferrin and lactoferricin. Antiviral Res 79, 192–198.[CrossRef] [Google Scholar]
  44. Kay, E. A., Wells, F. E. & Ponder, W. F.(1998). Class Gastropoda. In Mollusca: the Southern Synthesis Fauna of Australia, pp. 565–604. Edited by Beesley, P. L., Ross, G. J. B. & Wells, A.. Melbourne, Australia. : CSIRO Publishing. [Google Scholar]
  45. Koyama, A. H. & Uchida, T.(1987). The mode of entry of herpes simplex virus type 1 into Vero cells. Microbiol Immunol 31, 123–130.[CrossRef] [Google Scholar]
  46. Li, C. P.(1960). Antimicrobial effect of abalone juice. Proc Soc Exp Biol Med 103, 522–524.[CrossRef] [Google Scholar]
  47. Li, C. P., Prescott, B. & Jahnes, W. G.(1962a). Antiviral activity of abalone juice. Proc Soc Exp Biol Med 109, 534–538.[CrossRef] [Google Scholar]
  48. Li, C. P., Prescott, B., Jahnes, W. G. & Martino, E. C.(1962b). Antimicrobial agents from mollusks. Trans N Y Acad Sci 24, 504–509.[CrossRef] [Google Scholar]
  49. Li, C. P., Prescott, B., Eddy, B., Caldes, G., Green, W. R., Martino, E. C. & Young, A. M.(1965). Antiviral activity of paolins from clams. Ann N Y Acad Sci 130, 374–382. [Google Scholar]
  50. Lindahl, U., Lidholt, K., Spillmann, D. & Kjellen, L.(1994). More to ‘heparin’ than anticoagulation. Thromb Res 75, 1–32.[CrossRef] [Google Scholar]
  51. MacLean, C. A.(1998). HSV entry and spread. In Herpes Simplex Virus Protocols, pp. 9–18. Edited by Brown, S. M. & MacLean, A. R.. Totowa, NJ. : Humana Press. [Google Scholar]
  52. Marchetti, M., Longhi, C., Conte, M. P., Pisani, S., Valenti, P. & Seganti, L.(1996). Lactoferrin inhibits herpes simplex virus type 1 adsorption to Vero cells. Antiviral Res 29, 221–231.[CrossRef] [Google Scholar]
  53. Mårdberg, K., Trybala, E., Tufaro, F. & Bergström, T.(2002). Herpes simplex virus type 1 glycoprotein C is necessary for efficient infection of chondroitin sulfate-expressing gro2C cells. J Gen Virol 83, 291–300. [Google Scholar]
  54. Marderosian, A. D.(1969). Marine pharmaceuticals. J Pharm Sci 58, 1–33.[CrossRef] [Google Scholar]
  55. Marr, A. K., Jenssen, H., Moniri, M. R., Hancock, R. E. W. & Panté, N.(2009). Bovine lactoferrin and lactoferricin interfere with intracellular trafficking of herpes simplex virus-1. Biochimie 91, 160–164.[CrossRef] [Google Scholar]
  56. Matutte, B., Storey, K. B., Knoop, F. C. & Conlon, J. M.(2000). Induction of synthesis of an antimicrobial peptide in the skin of the freeze-tolerant frog, Rana sylvatica, in response to environmental stimuli. FEBS Lett 483, 135–138.[CrossRef] [Google Scholar]
  57. Montgomery, R. I., Warner, M. S., Lum, B. J. & Spear, P. G.(1996). Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87, 427–436.[CrossRef] [Google Scholar]
  58. Nybakken, J. W. & Bertness, M. D.(2005).Marine Biology: an Ecological Approach. San Francisco. : Pearson Education/Benjamin Cummings. [Google Scholar]
  59. Ohta, S., Ono, F., Shiomi, Y., Nakao, T., Aozasa, O., Nagate, T., Kitamura, K., Yamaguchi, S., Nishi, M. & Miyata, H.(1998). Anti-herpes simplex virus substances produced by the marine green alga, Dunaliella primolecta. J Appl Phycol 10, 349–356.[CrossRef] [Google Scholar]
  60. Olicard, C., Didier, Y., Marty, C., Bourgougnon, N. & Renault, T.(2005a).In vitro research of anti-HSV-1 activity in different extracts from Pacific oysters Crassostrea gigas. Dis Aquat Organ 67, 141–147.[CrossRef] [Google Scholar]
  61. Olicard, C., Renault, T., Torhy, C., Benmansour, A. & Bourgougnon, N.(2005b). Putative antiviral activity in hemolymph from adult Pacific oysters, Crassostrea gigas. Antiviral Res 66, 147–152.[CrossRef] [Google Scholar]
  62. Pan, J., Kurosky, A., Xu, B., Chopra, A. K., Coppenhaver, D. H., Singh, I. P. & Baron, S.(2000). Broad antiviral activity in tissues of crustaceans. Antiviral Res 48, 39–47.[CrossRef] [Google Scholar]
  63. Park, H.-J., Kurokawa, M., Shiraki, K., Nakamura, N., Choi, J.-S. & Hattori, M.(2005). Antiviral activity of the marine alga Symphyocladia latiuscula against herpes simplex virus (HSV-1) in vitro and its therapeutic efficacy against HSV-1 infection in mice. Biol Pharm Bull 28, 2258–2262.[CrossRef] [Google Scholar]
  64. Pechenik, J. A.(2000).Biology of the Inverterbrates, 4th edn. New York. : McGraw Hill. [Google Scholar]
  65. Prescott, B., Li, C. P., Martino, E. C. & Caldes, G.(1964). Isolation and characterization of antiviral substances from marine animals. Fed Proc 23, 508. [Google Scholar]
  66. Qie, L., Marcellino, D. & Herold, B. C.(1999). Herpes simplex virus entry is associated with tyrosine phosphorylation of cellular proteins. Virology 256, 220–227.[CrossRef] [Google Scholar]
  67. Reed, L. J. & Muench, H.(1938). A simple method of estimating fifty per cent endpoints. Am J Hyg 27, 493–497. [Google Scholar]
  68. Renault, T.(2008). Herpes virus infecting marine molluscs. http://www.scitopics.com/Herpes_virus_infecting_marine_molluscs.html. SciTopics.
  69. Roch, P., Beschin, A. & Bernard, E.(2004). Antiprotozoan and antiviral activities of non-cytotoxic truncated and variant analogues of mussel defensin. Evid Based Complement Alternat Med 1, 167–174.[CrossRef] [Google Scholar]
  70. Russell, W. C.(1962). A sensitive and precise plaque assay for herpes virus. Nature 195, 1028–1029.[CrossRef] [Google Scholar]
  71. Savin, K. W., Cocks, B. G., Wong, F., Sawbridge, T., Cogan, N., Savage, D. & Warner, S.(2010). A neurotropic herpesvirus infecting the gastropod, abalone, shares ancestry with oyster herpesvirus and a herpesvirus associated with the amphioxus genome. Virol J 7, 308.[CrossRef] [Google Scholar]
  72. Smit, A. J.(2004). Medicinal and pharmaceutical uses of seaweed natural products: a review. J Appl Phycol 16, 245–262.[CrossRef] [Google Scholar]
  73. Spear, P. G.(2004). Herpes simplex virus: receptors and ligands for cell entry. Cell Microbiol 6, 401–410.[CrossRef] [Google Scholar]
  74. Speck, P. G. & Simmons, A.(1991). Divergent molecular pathways of productive and latent infection with a virulent strain of herpes simplex virus type 1. J Virol 65, 4001–4005. [Google Scholar]
  75. Speck, P. G. & Simmons, A.(1992). Synchronous appearance of antigen-positive and latently infected neurons in spinal ganglia of mice infected with a virulent strain of herpes simplex virus. J Gen Virol 73, 1281–1285.[CrossRef] [Google Scholar]
  76. Stringer, S. E. & Gallagher, J. T.(1997). Heparan sulphate. Int J Biochem Cell Biol 29, 709–714.[CrossRef] [Google Scholar]
  77. Suttle, C. A.(2007). Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 5, 801–812.[CrossRef] [Google Scholar]
  78. Tal-Singer, R., Peng, C., Ponce de Leon, M., Abrams, W. R., Banfield, B. W., Tufaro, F., Cohen, G. H. & Eisenberg, R. J.(1995). Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J Virol 69, 4471–4483. [Google Scholar]
  79. Tan, J., Lancaster, M., Hyatt, A., van Driel, R., Wong, F. & Warner, S.(2008). Purification of a herpes-like virus from abalone (Haliotis spp.) with ganglioneuritis and detection by transmission electron microscopy. J Virol Methods 149, 338–341.[CrossRef] [Google Scholar]
  80. WuDunn, D. & Spear, P. G.(1989). Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J Virol 63, 52–58. [Google Scholar]
  81. Yasin, B., Pang, M., Turner, J. S., Cho, Y., Dinh, N. N., Waring, A. J., Lehrer, R. I. & Wagar, E. A.(2000). Evaluation of the inactivation of infectious herpes simplex virus by host-defense peptides. Eur J Clin Microbiol Infect Dis 19, 187–194.[CrossRef] [Google Scholar]
  82. Zhang, X., Huang, C. & Qin, Q.(2004). Antiviral properties of hemocyanin isolated from shrimp Penaeus monodon. Antiviral Res 61, 93–99.[CrossRef] [Google Scholar]
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