Role of sulfatide in vaccinia virus infection

Biology of the Cell

Volumn 103, Issue 7, 2011, Pages 319-331

  Perino, Julien ^a   Foo, Chwan Hong ^b   Spehner, Daniele ^b,c,d,e,f   Cohen, Gary H ^b   Eisenberg, Roselyn J ^b   Crance, Jean Marc ^a   Favier, Anne Laure ^a  

^a CENTRE DE RECHERCHES   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d CNRS   (France)

^e INSERM   (France)

^f UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Ceramide; Intranasal infection; Orthopoxvirus; Sulfatide; Vaccinia virus

Indexed keywords

A27 PROTEIN; CERAMIDE; GALACTOSYLCERAMIDE; GLYCOSPHINGOLIPID; L5 PROTEIN; SULFATE; SULFATIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL STRAIN BHK; ELECTRON MICROSCOPY; FEMALE; HUMAN; HUMAN CELL; LIPID RAFT; MOUSE; NONHUMAN; POXVIRUS INFECTION; PRIORITY JOURNAL; VACCINIA VIRUS; VACCINIA VIRUS INFECTION; VERO CELL; VIRUS PARTICLE; VIRUS REPLICATION;

ANIMALS; CELL LINE, TUMOR; CERAMIDES; CRICETINAE; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; GALACTOSYLCERAMIDES; HUMANS; LIGANDS; MEMBRANE PROTEINS; MICE; STRUCTURE-ACTIVITY RELATIONSHIP; SULFOGLYCOSPHINGOLIPIDS; VACCINIA; VACCINIA VIRUS; VARIOLA VIRUS; VIRAL PROTEINS;

ORTHOPOXVIRUS; VACCINIA VIRUS; VARIOLA VIRUS;

EID: 79959341001     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1042/BC20110012     Document Type: Article

References (83)

1. Baron, G.S., Wehrly, K., Dorward, D.W., Chesebro, B. and Caughey, B. (2002) Conversion of raft associated prion protein to the protease-resistant state requires insertion of PrP-res [PrP(Sc)] into contiguous membranes. EMBO J. 21, 1031-1040
2. Bavari, S., Bosio, C.M., Wiegand, E., Ruthel, G., Will, A.B., Geisbert, T.W., Hevey, M., Schmaljohn, C., Schmaljohn, A. and Aman, M.J. (2002) Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J. Exp. Med. 195, 593-602
3. Bender, F.C., Whitbeck, J.C., Ponce de Leon, M., Lou, H., Eisenberg, R.J. and Cohen, G.H. (2003) Specific association of glycoprotein B with lipid rafts during herpes simplex virus entry. J. Virol. 77, 9542-9552
4. Brown, D.A. and London, E. (1997) Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes? Biochem. Biophys. Res. ommun. 240, 1-7
5. Brown, D.A. and London, E. (1998) Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111-136
6. Brown, E., Senkevich, T.G. and Moss, B. (2006) Vaccinia virus F9 virion membrane protein is required for entry but not virus assembly, in contrast to the related L1 protein. J. irol. 80, 9455-9464
7. Brugger, B., Glass, B., Haberkant, P., Leibrecht, I., Wieland, F.T. and Krausslich, H.G. (2006) The HIV lipidome: a raft with an unusual composition. Proc. Natl. Acad. Sci. .S.A. 103, 2641-2646
8. Carter, G.C., Law, M., Hollinshead, M. and Smith, G.L. (2005) Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans. J. Gen. Virol. 6, 1279-1290
9. Chahroudi, A., Chavan, R., Kozyr, N., Waller, E.K., Silvestri, G. and Feinberg, M.B. (2005) Vaccinia virus tropism for primary hematolymphoid cells is determined by restricted expression of a unique virus receptor. J. Virol. 79, 10397-10407
10. Chazal, N. and Gerlier, D. (2003) Virus entry, assembly, budding, and membrane rafts. Microbiol. Mol. Biol. Rev. 67, 226-237
11. Chiu, W.L., Lin, C.L., Yang, M.H., Tzou, D.L. and Chang, W. (2007) Vaccinia virus 4c (A26L) protein on intracellular mature virus binds to the extracellular cellular matrix laminin. J. Virol. 81, 2149-2157
12. Chung, C.S., Hsiao, J.C., Chang, Y.S. and Chang, W. (1998) A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. J. Virol. 72, 1577-1585
13. Chung, C.S., Huang, C.Y. and Chang, W. (2005) Vaccinia virus penetration requires cholesterol and results in specific viral envelope proteins associated with lipid rafts. J. Virol. 9, 1623-1634
14. Danthi, P. and Chow, M. (2004) Cholesterol removal by methyl-beta-cyclodextrin inhibits poliovirus entry. J. Virol. 78, 33-41
15. DeBruin, L.S., Haines, J.D., Wellhauser, L.A., Radeva, G., Schonmann, V., Bienzle, D. and Harauz, G. (2005) Developmental partitioning of myelin basic protein into membrane microdomains. J. Neurosci. Res. 80, 211-225
16. Eckhardt, M. (2008) The role and metabolism of sulfatide in the nervous system. Mol. Neurobiol. 37, 93-103
17. Fantini, J., Hammache, D., Delezay, O., Pieroni, G., Tamalet, C. and Yahi, N. (1998) Sulfatide inhibits HIV-1 entry into CD4-/CXCR4+ cells. Virology 246, 211-220
18. Fantini, J., Hammache, D., Delezay, O., Yahi, N., Andre-Barres, C., Rico-Lattes, I. and Lattes, A. (1997) Synthetic soluble analogs of galactosylceramide (GalCer) bind to the V3 domain of HIV-1 gp120 and inhibit HIV-1-induced fusion and entry. J. Biol. Chem. 272, 7245-7252
19. Farooqui, A.A. and Horrocks, L.A. (1985) On the role of sulfolipids in mammalian metabolism. Mol. Cell. Biochem. 66, 87-95
20. Favier, A.L., Burmeister, W.P. and Chroboczek, J. (2004) Unique physicochemical properties of human enteric Ad41 responsible for its survival and replication in the gastrointestinal tract. Virology 322, 93-104
21. Fenner, F. (1958) The biological characters of several strains of vaccinia, cowpox and rabbitpox viruses. Virology 5, 502-529
22. Fenner, F., Henderson, D.A., Arita, I., Jezek, Z. and Ladnyi, I.D. (1988) Smallpox and its Eradication, World Health Organization, Geneva
23. Fogg, C., Lustig, S., Whitbeck, J.C., Eisenberg, R.J., Cohen, G.H. and Moss, B. (2004) Protective immunity to vaccinia virus induced by vaccination with multiple recombinant outer membrane proteins of intracellular and extracellular virions. J. Virol. 78, 10230-10237
24. Foo, C.H., Lou, H., Whitbeck, J.C., Ponce-de-Leon, M., Atanasiu, D., Eisenberg, R.J. and Cohen, G.H. (2009) Vaccinia virus L1 binds to cell surfaces and blocks virus entry independently of glycosaminoglycans. Virology 385, 368-382
25. Gandhi, N.S. and Mancera, R.L. (2008) The structure of glycosaminoglycans and their interactions with proteins. Chem. Biol. Drug. Des. 72, 455-482
26. Gatfield, J. and Pieters, J. (2000) Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288, 1647-1650
27. Grassme, H., Jendrossek, V., Riehle, A., von Kurthy, G., Berger, J., Schwarz, H., Weller, M., Kolesnick, R. and Gulbins, E. (2003) Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med. 9, 322-330
28. Grassme, H., Riehle, A., Wilker, B. and Gulbins, E. (2005) Rhinoviruses infect human epithelial cells via ceramide-enriched membrane platforms. J. Biol. Chem. 280, 26256-6262
29. Hayasaka, D., Ennis, F.A. and Terajima, M. (2007) Pathogeneses of respiratory infections with virulent and attenuated vaccinia viruses. J. Virol. 4, 22
30. Hileman, R.E., Fromm, J.R., Weiler, J.M. and Linhardt, R.J. (1998) Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. BioEssays 20, 156-167
31. Hsiao, J.C., Chung, C.S. and Chang, W. (1999) Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J. Virol. 73, 8750-8761
32. Ichihashi, Y., Takahashi, T. and Oie, M. (1994) Identification of a vaccinia virus penetration protein. Virology 202, 834-843
33. Ikonen, E. (2001) Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13, 470-477
34. Ishizuka, I. (1997) Chemistry and functional distribution of sulfoglycolipids. Prog. Lipid Res. 36, 245-319
35. Izmailyan, R.A., Huang, C.Y., Mohammad, S., Isaacs, S.N. and Chang, W. (2006) The envelope G3L protein is essential for entry of vaccinia virus into host cells. J. Virol. 80, 402-8410
36. Jesus, D.M., Santos, E.S., Schnellrath, L.C. and Damaso, C.R. (2009) Development of a 1-step cell-based assay for cost-effective screening of antiviral drugs for vaccinia virus. Diagn. Microbiol. Infect Dis. 64, 350-353
37. Karlsson, K.A. (1995) Microbial recognition of target-cell glycoconjugates. Curr. Opin. Struct. Biol. 5, 622-635
38. Kensinger, R.D., Catalone, B.J., Krebs, F.C., Wigdahl, B. and Schengrund, C.L. (2004) Novel polysulfated galactose-derivatized dendrimers as binding antagonists of human immunodeficiency virus type 1 infection. Antimicrob. Agents Chemother. 48, 1614-1623
39. Kochan, G., Escors, D., Gonzalez, J.M., Casasnovas, J.M. and Esteban, M. (2008) Membrane cell fusion activity of the vaccinia virus A17-A27 protein complex. Cell Microbiol. 10, 149-164
40. Krivan, H.C., Olson, L.D., Barile, M.F., Ginsburg, V. and Roberts, D.D. (1989) Adhesion of Mycoplasma pneumoniae to sulfated glycolipids and inhibition by dextran sulfate. J. Biol. Chem. 264, 9283-9288
41. Kumar, R.B., Maher, D.M., Herzberg, M.C. and Southern, P.J. (2006) Expression of HIV receptors, alternate receptors and co-receptors on tonsillar epithelium: implications for HIV binding and primary oral infection. J. Virol. 3, 25
42. Lai, C.F., Gong, S.C. and Esteban, M. (1990) Structural and functional properties of the 14-kDa envelope protein of vaccinia virus synthesized in Escherichia coli. J. Biol. Chem. 65, 22174-22180
43. Lai, C.F., Gong, S.C. and Esteban, M. (1991) The 32-kilodalton envelope protein of vaccinia virus synthesized in Escherichia coli binds with specificity to cell surfaces. J. Virol. 5, 499-504
44. Lee, H.J., Essani, K. and Smith, G.L. (2001) The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 281, 170-192
45. Lee, M.S., Roos, J.M., McGuigan, L.C., Smith, K.A., Cormier, N., Cohen, L.K., Roberts, B.E. and Payne, L.G. (1992) Molecular attenuation of vaccinia virus: mutant generation and animal characterization. J. Virol. 66, 2617-2630
46. Lin, C.L., Chung, C.S., Heine, H.G. and Chang, W. (2000) Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infection in vitro and in vivo. J. Virol. 74, 3353-3365
47. Long, D., Berson, J.F., Cook, D.G. and Doms, R.W. (1994) Characterization of human immunodeficiency virus type 1 gp120 binding to liposomes containing galactosylceramide. J. Virol. 68, 5890-5898
48. Mackett, M., Smith, G. and Moss, B. (1985) The construction and characterization of vaccinia virus recombinants expressing foreign genes. In DNA cloning: A Practical Approach, volume 2 (Glover, D.M., ed.), pp. 191-211, IRL Press, Oxford
49. Moss, B. (2006) Poxvirus entry and membrane fusion. Virology 344, 48-54
50. Nayak, D.P. and Barman, S. (2002) Role of lipid rafts in virus assembly and budding. Adv. Virus Res. 58, 1-28
51. Nayak, D.P. and Hui, E.K. (2004) The role of lipid microdomains in virus biology. Subcell. Biochem. 37, 443-491
52. Nichols, R.J., Stanitsa, E., Unger, B. and Traktman, P. (2008) The vaccinia virus gene I2L encodes a membrane protein with an essential role in virion entry. J. Virol. 82, 10247-0261
53. Ohta, K., Sato, C., Matsuda, T., Toriyama, M., Lennarz, W.J. and Kitajima, K. (1999) Isolation and characterization of low density detergent-insoluble membrane (LD-DIM) fraction from sea urchin sperm. Biochem. Biophys. Res. Commun. 258, 616-623
54. Ojeda, S., Domi, A. and Moss, B. (2006a) Vaccinia virus G9 protein is an essential component of the poxvirus entry-fusion complex. J. Virol. 80, 9822-9830
55. Ojeda, S., Senkevich, T.G. and Moss, B. (2006b) Entry of vaccinia virus and cell-cell fusion require a highly conserved cysteine-rich membrane protein encoded by the A16L gene. J. Virol. 80, 51-61
56. Ono, A. and Freed, E.O. (2001) Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. U.S.A. 98, 13925-13930
57. Orynbayeva, Z., Kolusheva, S., Groysman, N., Gavrielov, N., Lobel, L. and Jelinek, R. (2007) Vaccinia virus interactions with the cell membrane studied by new chromatic vesicle and cell sensor assays. J. Virol. 81, 1140-1147
58. Perino, J., Crouzier, D., Spehner, D., Debouzy, J.C., Garin, D., Crance, J.M. and Favier, A.L. (2011) Lung surfactant DPPG phospholipid inhibits vaccinia virus infection. ntiviral Res. 89, 89-97
59. Pike, L.J. (2006) Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 47, 1597-1598
60. Ricketts, C.R. (1952) Dextran sulphate-a synthetic analogue of heparin. Biochem. J. 51, 129-133
61. Riethmuller, J., Riehle, A., Grassme, H. and Gulbins, E. (2006) Membrane rafts in host-pathogen interactions. Biochim. Biophys. Acta 1758, 2139-2147
62. Samuel, B.U.,Mohandas, N., Harrison, T., McManus, H., Rosse, W., Reid, M. and Haldar, K. (2001) The role of cholesterol and glycosylphosphatidylinositol-anchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J. Biol. Chem. 276, 29319-29329
63. Sandhoff, R., Grieshaber, H., Djafarzadeh, R., Sijmonsma, T.P., Proudfoot, A.E., Handel, T.M., Wiegandt, H., Nelson, P.J. and Grone, H.J. (2005) Chemokines bind to sulfatides as revealed by surface plasmon resonance. Biochim. Biophys. Acta 1687, 52-63
64. Scheiffele, P., Roth, M.G. and Simons, K. (1997) Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16, 5501-5508
65. Schmitter, T., Agerer, F., Peterson, L., Munzner, P. and Hauck, C.R. (2004) Granulocyte CEACAM3 is a phagocytic receptor of the innate immune system that mediates recognition and elimination of human-specific pathogens. J. Exp. Med. 199, 35-46
66. Senkevich, T.G. and Moss, B. (2005) Vaccinia virus H2 protein is an essential component of a complex involved in virus entry and cell-cell fusion. J. Virol. 79, 4744-4754
67. Senkevich, T.G., Ojeda, S., Townsley, A., Nelson, G.E. and Moss, B. (2005) Poxvirus multiprotein entry-fusion complex. Proc. Natl. Acad. Sci. U.S.A. 102, 18572-18577
68. Senkevich, T.G., Ward, B.M. and Moss, B. (2004) Vaccinia virus entry into cells is dependent on a virion surface protein encoded by the A28L gene. J. Virol. 78, 2357-1266
69. Shin, J.S., Gao, Z. and Abraham, S.N. (2000) Involvement of cellular caveolae in bacterial entry into mast cells. Science 289, 785-788
70. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569-572
71. Sundell, I.B., Halder, R., Zhang, M., Maricic, I., Koka, P.S. and Kumar, V. (2010) Sulfatide administration leads to inhibition of HIV-1 replication and enhanced hematopoeisis. J. Stem Cells 5, 33-42
72. Suzuki, T., Sometani, A., Yamazaki, Y., Horiike, G., Mizutani, Y., Masuda, H., Yamada, M., Tahara, H., Xu, G., Miyamoto, D. et al. (1996) Sulphatide binds to human and animal influenza A viruses, and inhibits the viral infection. Biochem. J. 318, 389-393
73. Takahashi, T., Murakami, K., Nagakura, M., Kishita, H., Watanabe, S., Honke, K., Ogura, K., Tai, T., Kawasaki, K., Miyamoto, D. et al. (2008) Sulfatide is required for efficient replication of influenza A virus. J. Virol. 82, 5940-5950
74. Takahashi, T., Satoh, H., Takaguchi, M., Takafuji, S., Yokoyama, H., Fujii, S. and Suzuki, T. (2010a) Binding of sulfatide to recombinant hemagglutinin of influenza A virus produced by a baculovirus protein expression system. J. Biochem. 147, 459-462
75. Takahashi, T., Satoh, H., Takaguchi, M., Takafuji, S., Yokoyama, H., Fujii, S. and Suzuki, T. (2010b) Binding of sulphatide to recombinant haemagglutinin of influenza A virus produced by a baculovirus protein expression system. J. Biochem. 147, 459-462
76. Townsley, A.C., Senkevich, T.G. and Moss, B. (2005a) The product of the vaccinia virus L5R gene is a fourth membrane protein encoded by all poxviruses that is required for cell entry and cell-cell fusion. J. Virol. 79, 10988-10998
77. Townsley, A.C., Senkevich, T.G. and Moss, B. (2005b) Vaccinia virus A21 virion membrane protein is required for cell entry and fusion. J. Virol. 79, 9458-9469
78. Tsung, K., Yim, J.H., Marti, W., Buller, R.M. and Norton, J.A. (1996) Gene expression and cytopathic effect of vaccinia virus inactivated by psoralen and long-wave UV light. J. Virol. 70, 165-171
79. Vazquez, M.I. and Esteban, M. (1999) Identification of functional domains in the 14-kilodalton envelope protein (A27L) of vaccinia virus. J. Virol. 73, 9098-9109
80. Voisset, C., Lavie, M., Helle, F., Op De Beeck, A., Bilheu, A., Bertrand-Michel, J., Terce, F., Cocquerel, L., Wychowski, C., Vu-Dac, N. and Dubuisson, J. (2008) Ceramide enrichment of the plasma membrane induces CD81 internalization and inhibits hepatitis C virus entry. Cell Microbiol. 10, 606-617
81. Vos, J.P., Lopes-Cardozo, M. and Gadella, B.M. (1994) Metabolic and functional aspects of sulfogalactolipids. Biochim. Biophys. Acta 1211, 125-149
82. Watarai, S., Onuma, M., Yamamoto, S. and Yasuda, T. (1990) Inhibitory effect of liposomes containing sulfatide or cholesterol sulfate on syncytium formation induced by bovine immunodeficiency virus-infected cells. J. Biochem. (Tokyo) 108, 507-509
83. Zhang, Y., Li, X., Becker, K.A. and Gulbins, E. (2009) Ceramide-enriched membrane domains-structure and function. Biochim. Biophys. Acta 1788, 178-183