Viral exploitation and subversion of the immune system through chemokine mimicry

Nature Immunology

Volumn 2, Issue 2, 2001, Pages 116-122

  Murphy, Philip M ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; TRANSACTIVATOR PROTEIN;

ANIMAL; CYTOMEGALOVIRUS; HUMAN; HUMAN HERPESVIRUS 6; HUMAN HERPESVIRUS 8; IMMUNOLOGY; MOLECULAR MIMICRY; PATHOGENICITY; REVIEW; VIRUS;

ANIMALS; CHEMOKINES; CYTOMEGALOVIRUS; GENE PRODUCTS, TAT; HERPESVIRUS 6, HUMAN; HERPESVIRUS 8, HUMAN; HUMANS; MOLECULAR MIMICRY; VIRUSES;

EID: 0035259780     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/84214     Document Type: Review

References (107)

1. Zlotnik, A. & Yoshie, O. Chemokines: a new classification system and their role in immunity. Immunity 12, 121-127 (2000).
2. Murphy, P. M. et al. International Union of Pharmacology nomenclature for chemokine receptors. Phamacol. Rev. 52, 145-176 (2000).
3. Tulman, E. R. et al. The genome of a very virulent Marek's disease virus. J. Virol. 74, 7980-7988 (2000).
4. Boshoff, C et al. Angiogenic and HIV-inhibitory functions of KSHV-encoded chemokines. Science 278, 290-294 (1997).
5. Spriggs, M. K. One step ahead of the game: viral immunomodulatory molecules. Annu. Rev. Immunol. 14, 101-130 (1996).
6. McFadden, G. & Murphy, P. M. Host-related immunomodulators encoded by DNA viruses. Curr. Opin. Microbiol 3, 371-378 (2000).
7. Berger, E.A., Murphy, P. M. & Farber, J. M. Chemokine receptors as HIV-1 coreceptors: Roles in viral entry, tropism and disease. Ann Rev. Immunol. 17, 657-700 (1999).
8. Littman, D. R. Chemokine receptors: keys to AIDS pathogenesis? Cell 93, 677-680 (1998).
9. Baba, M. A small-molecule, non-peptide CCRS antagonist with highly potent and selective anti-HIV-1 activity. Proc. Natl Acad Sci USA 96, 5698-5703 (1999).
10. LaCasse, R. A. et al Fusion-competent vaccines: broad neutralization of primary isolates of HIV Science 283, 357-362 (1999).
11. Weissman, D. et al. Macrophage-tropic HIV and SIV envelope proteins induce a signal through the CCR5 chemokine receptor.Nature 389, 981-985 (1997).
12. Davis, C. B. et al Signal transduction due to HIV-1 envelope interactions with chemokine receptors CXCR4 or CCR5. J. Exp. Med 186, 1793-1798 (1997).
13. Iyengar, S., Schwartz, D. H. & Hildreth, J. E. T cell-tropic HIV gp 120 mediates CD4 and CD8 cell chemotaxis through CXCR4 independent of CC4; implications for HIV pathogenesis. J. Immunol. 162, 6263-6267 (1999).
14. Hesselgesser,J. et al. Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1 α is mediated by the chemokine receptor CXCR4. Curr. Biol. 8, 595-598 (1998).
15. Herbein, G. et al. Apoptosis of CD8(+) T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature 395, 189-194 (1998).
16. Wyatt, R. & Sodroski, J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280, 1834-1888 (1998).
17. Berger, E.A. et al. A new classification for HIV-1. Nature 391, 240 (1998).
18. Liu, R. et al. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply exposed individuals to HIV-1 infection. Cell 86, 367-377 (1996).
19. Samson, M. et al. Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382, 722-725 (1996).
20. Dean, M. et al. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKRS structural gene. Science 273, 1856-1862 (1996).
21. Lu, Z et al. Evolution of HIV-1 coreceptor usage through interactions with distinct CCRS and CXCR4 domains. Proc. Natl Acad. Sci. USA 94, 6426-6431 (1997).
22. Michael, N. L. et al. Exclusive and persistent use of the entry coreceptor CXCR4 by human immunodeficiency virus type I from a subject homozygous for CCRS Δ32. J. Virol. 72, 6040-6047 (1998).
23. Zhang, Y. J. et al. Use of coreceptors other than CCR5 by non-syncytium-inducing adult and pediatric isolates of human immunodeficiency virus type 1 is rare in vitro. J. Virol. 72, 9337-9344 (1998).
24. Lee, B. et al. Influence of the CCR2-V641 polymorphism on human immunodeficiency virus type 1 coreceptor activity and on chemokine receptor function of CCR2b, CCR3, CCR5, and CXCR4.J.Virol. 72, 7450-7458 (1998).
25. He, J. et al. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 385, 645-649 (1997).
26. Lee, S. et al. CCR8 on human thymocytes functions as a Human Immunodeficiency Virus type 1 coreceptor. J. Virol. 74, 6946-6952 (2000).
27. Faure, S. et al. Rapid progression to AIDS in HIV: individuals with a structural variant of the chemokine receptor CX3CRI. Science 287, 2274-2277 (2000).
28. McDermott D. A. et al. Technical Comment Genetic polymorphism in the HIV coreceptor CX3CRI and risk of HIV disease. Science 290, 5499 (2000).
29. Rizzuto, C. D. et al. A conserved HIV gp 120 glycoprotein structure involved in chemokine receptor binding. Science 280, 1949-1953 (1998).
30. Farzan, M. et al. Tyrosine sulfation of the amino terminus of CCRS facilitates HIV-1 entry. Cell 96, 667-676 (1999).
31. Berson, J.F. & Doms, R. W. Structure-function studies of the HIV-1 coreceptors. Semin. Immunol. 10, 237-248 (1998).
32. Speck, R. F. et al. Selective employment of chemokine receptors as human immunodeficiency virus type I coreceptors determined by individual amino acids within the envelope V3 loop.J.Virol. 71, 7136-7139 (1997).
33. Salzwedel, K., Smith, E. D., Dey, B. & Berger, E.A. Sequential CD4-coreceptor interactions in human immunodeficiency virus type 1 Env function: soluble CD4 activates Env for coreceptor-dependent fusion and reveals blocking activities of antibodies against cryptic conserved epitopes on gp120. J. Virol. 74, 326-333 (2000).
34. Xiao, H. et al. Constitutive cell surface association between CD4 and CCR5. Proc. Natl Acad. Sci. USA 96, 7496-7501 (1999).
35. Lapham, C. K., Zaitseva, M. B., Lee, S., Romanstseva, T. & Golding, H. Fusion of monocytes and macrophages with HIV-1 correlates with biochemical properties of CXCR4 and CCR5. Nature Med. 5, 303-308 (1999).
36. Vila-Coro, A.J. et al. HIV-1 infection through the CCRS receptor is blocked by receptor dimerization. Proc. Natl Acad. Sci. USA 97, 3383-3393 (2000).
37. Rodriguez-Frade, J. M. et al. The chemokine monocyte chemoattractant protein-1 induces functional responses through dimerization of its receptor CCR2. Proc. Natl Acad. Sci. USA 96, 3628-3633 (1999).
38. Grivel, J. C. & Margolis, L. B. CCRS- and CXCR4-tropic HIV-1 are equally cytopathic for their T-cell targets in human lymphoid tissue. Nature Med. 5, 344-346 (1999).
39. Malkevitch, N. et al. Coreceptor choice and T cell depletion by R5,X4 and R5X4 HIV-1 variants in CCR5-deficient (CCR5Δ32) and normal human lymphoid tissue. Virology (in the press, 2001).
40. Lee, S. et al. Coreceptor competition for association with CD4 may change the susceptibility of human cells to infection with T-tropic and macrophagetropic isolates of human immunodeficiency virus type I. J. Virol. 74, 5016-5023 (2000).
41. Arthos, J. et al. CCR5 signal transduction in macrophages by human immunodeficiency virus and simian immunodeficiency virus envelopes. J. Virol. 74, 6418-6424 (2000).
42. Connor, R. I., Sheridan, K. E., Ceradini, D., Choe, S. & Landau. N. R. Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J. Exp. Med. 185, 621-628 (1997).
43. Zhang, L. Q., He, T., Talal,A.,Wang, G., Frankel, S. S. & Ho, D. D. In vivo distribution of the human immunodeficiency virus simian immunodeficiency virus coreceptors: CXCR4, CCR3, and CCR5. J. Virol 72, 5035-5045 (1998).
44. Ghezzi, S. et al. Inhibition of CXCR4-dependent HIV-1 infection by extracellular HIV-1 Tat. Biochem. Biophys. Res. Commun. 270, 992-996 (2000).
45. Xiao, H. et al. Selective CXCR4-antagonism by Tat Implications for in vivo expansion of co-receptor use by HIV-1. Proc. Natl. Acad. Sci. USA 97, 11466-11471 (2000).
46. Gallo, R. C.Tat as one key to HIV-induced immune pathogenesis and Tat (correction of Pat) toxoid as an important component of a vaccine. Proc. Natl Acad. Sci USA 96, 8324-6326 (1999).
47. Albini, A. et al. HIV-1 Tat protein mimicry of chemokines. Proc. Natl Acad Sci USA 95, 13153-13158 (1998).
48. Benelli, R. et al. Human Immunodeficiency Virus Transactivator Protein (Tat) stimulates chemotaxis, calcium mobilization, and activation of human polymorphonuclear leukocytes: Implications for Tat-mediated pathogenesis. J. infect. Dis. 182, 1643-1651 (2000).
49. de Paulis,A. et al. Tat protein is an HIV-1-encoded ss-chemokine homolog that promotes migration and up-regulates CCR3 expression on human FcepsilonRI(+) cells. J. Immunol. 165, 7171-7179 (2000).
50. Huang, L, Bosch, I, Hofmann, W., Sodroski, J. & Pardee,A. B.Tat protein induces human immunodeficiency virus type I (HIV-1) coreceptors and promotes infection with both macrophage-tropic and T-lymphotropic HIV-1 strains. J. Virol 72.8952-8960 (1998).
51. Pauza,C. D. et al. Vaccination with tat toxoid attenuates disease in simian/HIV-challenged macaques. Proc. Natl Acad. Sci. USA 97, 3515-3519 (2000).
52. Doranz, B. J. et al. A small-molecule inhibitor directed against the chemokine receptor CXCR4 prevents its use as an HIV-I coreceptor. J. Exp. Med 186, 1395-1400 (1997).
53. Gallo, R. C. The enigmas of Kaposi's sarcoma. Science 282, 1837-1839 (1998).
54. Arvanitakis, L, Geras-Raaka, E., Varma, A., Gershengorn, M. C. & Cesarman, E. Human herpesvirus KSHV encodes a constitutively active G-protein-coupled receptor linked to cell proliferation. Nature 385, 347-350 (1997).
55. Yang, B.T. et al Transgenic expression of the chemokine receptor encoded by human herpesvirus 8 induces an angioproliferative disease resembling Kaposi's Sarcoma. J. Exp. Med. 191, 445-454 (2000).
56. Kirshner, J. R., Staskus, K., Haase,A, Lagunoff, M. & Ganem, D. Expression of the open reading frame 74 (G-protein-coupled receptor) gene of Kaposi's sarcoma (KS)-associated herpesvirus: implications for KS pathogenesis. J. Virol. 73, 6006-6014 (1999).
57. Schwarz, M. & Murphy, P. M. Kaposi's Sarcoma-associated herpesvirus (KSHV) G protein-coupled receptor constitutively activates NF-κB and induces pro-inflammatory cytokine production via a C-terminal signaling determinant. J. Immunol. (Submitted).
58. Moser, B. et al. Expression of transcripts for two interleukin 8 receptors in human phagocytes, lymphocytes and melanoma cells. Biochem. J. 294, 285-292 (1993).
59. Addison, C. L et al. The CXC chemokine receptor Z CXCR2, is the putative receptor for ELR(+) CXC chemokine-induced angiogenic activity. J. Immunol. 165, 5269-5277 (2000).
60. Virgin, H.W.IVth et al. Complete sequence and genomic analysis of murine γherpesvirus 68. J. Virol. 71, 5894-5904 (1997).
61. Ahuja, S. K. & Murphy, P. M. Molecular piracy of mammalian interleukin-8 receptor type B by herpesvirus saimiri. J. Biol. Chem. 268, 20691-20694 (1993).
62. Dittmer, D. & Kedes, D. H. Do viral chemokines modulate Kaposi's sarcoma? Bioessays. 20, 367-370 (1998).
63. Kledal,T. N. et al A broad-spectrum chemokine antagonist encoded by Kaposi's sarcoma-associated herpesvirus. Science 277, 1656-1659 (1997).
64. Stine, J.T. et al KSHV-encoded CC chemokine vMIP-III is a CCR4 agonist, stimulates angiogenesis, and selectively chemoattracts TH2 cells. Blood 95, 1151-1157 (2000).
65. Geras-Raaka, E., Varma, A., Clark-Lewis, I. & Gershengorn, M. C. Kaposi's sarcoma-associated herpesvirus (KSHV) chemokine vMIP-II and human SDF-1α inhibit signaling by KSHV G protein-coupled receptor. Biochem. Biophys. Res. Commun. 253, 725-727 (1993).
66. Endres, M. J., Garlisi, C.G., Xiao, H., Shan, L & Hedrick, J.A.The Kaposi's sarcoma-related herpesvirus (KSHV)-encoded chemokine vMIP-1 is a specific agonist for the CC chemokine receptor (CCR)8. J. Exp. Med 189, 1993-1998 (1999).
67. Luttichau, H. R. et al. A highly selective CC chemokine receptor (CCR)8 antagonist encoded by the poxvirus molluscum contagiosum. J. Exp. Med. 191, 171-180 (2000).
68. Dairaghi, D. J., Fan, R. A., McMaster, B. E., Hanley, M. R. & Schall, T.J. HHV8-encoded vMIP-1 selectively engages chemokine receptor CCR8.Agonist and antagonist profiles of viral chemokines. J. Biol. Chem. 274, 21569-21574 (1999).
69. Chen, S. et al. In vivo inhibition of CC and CX3C chemokine-induced leukocyte infiltration and attenuation of glomerulonephritis in Wistar-Kyoto (WKY) rats by vMIP-II J. Exp. Med 188, 193-198 (1998).
70. Penfold, M. E. et al. Cytomegalovirus encodes a potent alpha chemokine. Proc. Natl Acad. Sci. USA 96, 9839-9844 (1999).
71. Gao, J. L & Murphy, P. M. Human cytomegalovirus open reading frame US28 encodes a functional β chemokine receptor. J. Biol. Chem. 269, 28539-28542 (1994).
72. Kledal, T. N., Rosenkilde, M. M. & Schwartz,T.W. Selective recognition of the membrane-bound CX3C chemokine, fractalkine. by the human cytomegalovirus-encoded broad-spectrum receptor US28. FEBS Lett 441, 209-214 (1998).
73. Bodaghi, B. et al. Chemokine sequestration by viral chemoreceptors as a novel viral escape strategy: withdrawal of chemokines from the environment of cytomegalovirus-infected cells. J. Exp. Med. 108, 855-866 (1998).
74. Billstrom, M. A., Lehman, LA. & Worthen G. S. Depletion of extracellular RANTES during human cytomegalovirus infection of endothelial cells. Am. J. Respir. Cell Mol. Biol. 21, 163-167 (1999).
75. Streblow, D. N. et al. The human cytomegalovirus chemokine receptor US28 mediates vascular smooth muscle cell migration. Cell 99, 511-520 (1999).
76. Pleskoff, O.,Treboute, C. & Alizon, M. The cytomegalovirus-encoded chemokine receptor US28 can enhance cell-cell fusion mediated by different viral proteins. J. Virol. 72, 6389-6397 (1998).
77. Margulies, B. J., Browne, H. & Gibson. W. Identification of the human cytomegalovirus G protein-coupled receptor homologue encoded by UL33 in infected cells and enveloped virus particles. Virology 225, 111-125 (1996).
78. Pleskoff, O. et al. Identification of a chemokine receptor encoded by human cytomegalovirus as a cofactor for HIV-I entry. Science 276, 1874-1878 (1997).
79. Casarosa, P et al. Constitutive signaling of the human cytomegalovirus-encoded chemokine receptor US28. J. Biol. Chem. 276, 1133-1137 (2001).
80. MacDonald, M. R., Burney, M. W., Resnick, S. B. & Virgin, H.W. IV Spliced mRNA encoding the murine cytomegalovirus chemokine homolog predicts a β chemokine of novel structure. J. Virol. 73, 3682-3691 (1999).
81. Fleming, P. et al. The Murine Cytomegalovirus chemokine homolog, m131/129, is a determinant of viral pathogenicity. J. Virol. 73, 6800-6809 (1999).
82. Saederup, N., Lin, Y. C., Dairaghi, D. J., Schall, T. J. & Mocarski, E. S. Cytomegalovirus-encoded β chemokine promotes monocyte-associated viremia in the host. Proc. Natl. Acad. Sci USA 96, 10881-10886 (1999).
83. Salazar-Mather, T. P., Orange, J. S. & Biron, C.A. Early murine cytomegalovirus (MCMV) infection induces liver natural killer (NK) cell inflammation and protection through macrophage inflammatory protein lα (MIP-1α)-dependent pathways. J. Exp. Med. 187, 1-14 (1998).
84. Chee, M. S., Satchwell, S. C., Preddie, E., Weston, K. M. & Barrell, B. G. Human cytomegalovirus encodes three G protein-coupled receptor homologues. Nature 344, 774-777 (1990).
85. Isegawa, Y., Ping, Z., Nakano, K., Sugimoto, N. & Yamanishi, K. Human herpesvirus 6 open reading frame U12 encodes a functional β-chemokine receptor. J. Virol. 72, 6104-6112 (1998).
86. Davis-Poynter, N. J. et al. Identification and characterization of a G protein-coupled receptor homolog encoded by murine cytomegalovirus. J. Virol. 71, 1521-1529 (1997).
87. Beisser, P. S. et al. The R33 G protein-coupled receptor gene of rat cytomegalovirus plays an essential role in the pathogenesis of viral infection. J. Virol. 72, 2352-2363 (1998).
88. Martin, W.J. Chemokine receptor-related genetic sequences in an african green monkey simian cytomegalovirus-derived stealth virus. Exp. Mol. Pathol. 69, 10-16 (2000).
89. Martin, W. J. Melanoma growth stimulatory activity (MGSA/GRO-α) chemokine genes incorporated into an African green monkey simian cytomegalovirus-derived stealth virus. Exp. Mol. Pathol. 66, 15-18 (1999).
90. Lusso, P. & Gallo, R. C. Human herpesvirus 6 in AIDS. Immunol. Today. 16, 67-71 (1995).
91. Milne, R. S. et al. RANTES binding and down-regulation by a novel human herpesvirus-6β chemokine receptor. J. Immunol. 164, 2396-2404 (2000).
92. Zou, P. et al. Human herpesvirus 6 open reading frame U83 encodes a functional chemokine. J. Virol. 73, 5926-5933 (1999).
93. Liu, L. et al. A viral anti-inflammatory chemokine binding protein, M-T7, reduces intimal hyperplasia after vascular injury. J. Clin. invest 105,1613-1621 (2000).
94. Dabbagh, K. et al. Local blockade of allergic airway hyperreactivity and inflammation by the poxvirus-derived pan-CC-chemokine inhibitor vCCI. J. Immunol. 165, 3418-3422 (2000).
95. Lalani, A. S. & McFadden, G. Evasion and exploitation of chemokines by viruses. Cytok. Growth Factor Rev. 10, 219-233 (1999).
96. Alcami, A. & Koszinowski, U. H. Viral mechanisms of immune evasion. Immunol. Today. 21, 447-455 (2000).
97. Parry, B. C. et al. A broad spectrum secreted chemokine binding protein encoded by a herpesvirus. J. Exp. Med. 191, 573-578 (2000).
98. van Berkel, V. et al. Identification of a γ herpesvirus-selective chemokine binding protein that inhibits chemokine action. J. Virol. 74, 6741-6747 (2000).
99. Lalani, A. S. et al. Role of myxoma virus soluble CC-chemokine inhibitor glycoprotein, M-TI, during myxoma virus pathogenesis. Virology 256, 233-245 (1999).
100. Carfi, A., Smith, C.A., Smolak, P.J., McGrew, J. & Wiley, D. C. Structure of a soluble secreted chemokine inhibitor vCCI (p35) from cowpox virus. Proc. Natl. Acad. Sci. USA 96, 12379-12383 (1999).
101. Yang, D. et al. β-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286, 525-528 (1999).
102. Lalani, A. et al. Use of chemokine receptors by poxviruses. Science 286, 1968-1971 (1999).
103. Bais, C. et al. G-protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator. Nature 391, 86-59 (1998).
104. Camarda, G. et al. The equine herpesvirus 2 E1 open reading frame encodes a functional chemokine receptor. J. Virol. 73, 9843-9848 (1999).
105. Nicholas, J. Determination and analysis of the complete nucleotide sequence of human herpesvirus 7. J. Virol. 70, 5975-5989 (1996).
106. Damon, I., Murphy, P. M. & Moss, B. Broad spectrum chemokine antagonistic activity of a human poxvirus chemokine homolog. Proc. Natl Acad. Sci. USA 95, 6403-6407 (1998).
107. Krathwohl, M. D., Hromas, R., Brown, D. R., Broxmeyer, H. E., & Fife, K. H. Functional characterization of the C-C chemokine-like molecules encoded by molluscum contagiosum virus types 1 and 2. Proc. Natl Acad. Sci. USA 94, 9875-9880 (1997).p