Monkeypox virus and insights into its immunomodulatory proteins

Immunological Reviews

Volumn 225, Issue 1, 2008, Pages 96-113

  Weaver, Jessica R ^a   Isaacs, Stuart N ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Immune evasion; Immune modulatory; Monkeypox virus

Indexed keywords

ANION TRANSPORT PROTEIN; BR 203 PROTEIN; BR 209 PROTEIN; COP B12R PROTEIN; COP B7R PROTEIN; COP C10L PROTEIN; COP C3L PROTEIN; COP E3L PROTEIN; COP E7R PROTEIN; COP K3L PROTEIN; COP K4L PROTEIN; CYTOKINE RECEPTOR; GUANYLATE KINASE; HYDROXYSTERIOD DEHYDROGENASE; INTERLEUKIN 1; INTERLEUKIN 1BETA BINDING PROTEIN; INTERLEUKIN 2; MONKEYPOX INHIBITOR OF COMPLEMENT ENZYME; PHOSPHOLIPASE D; PHOSPHOTRANSFERASE; PROTEIN SERINE THREONINE KINASE; SEMAPHORIN; SMALLPOX INHIBITOR OF COMPLEMENT ENZYME; SMALLPOX VACCINE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VACCINIA VACCINE; VACCINIA VIRUS COMPLEMENT CONTROL PROTEIN; VIRULENCE FACTOR; VIRUS ANTIBODY; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANTIBODY TITER; CARBOXY TERMINAL SEQUENCE; CLINICAL FEATURE; CONSENSUS SEQUENCE; ENDOPLASMIC RETICULUM; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDEMIC; GENE FUNCTION; GENETIC VARIABILITY; HOST PATHOGEN INTERACTION; HUMAN; INCUBATION TIME; LABORATORY DIAGNOSIS; MONKEYPOX; MONKEYPOX VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; ORTHOPOXVIRUS; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN MOTIF; REVIEW; SEROPREVALENCE; SMALLPOX; SMALLPOX VIRUS; UNITED STATES; VACCINATION; VACCINIA VIRUS; VIRUS DIAGNOSIS; VIRUS GENE; VIRUS GENOME; VIRUS IMMUNITY; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; HUMANS; MONKEYPOX; MONKEYPOX VIRUS; PHYLOGENY; VACCINIA VIRUS; VARIOLA VIRUS; VIRAL PROTEINS;

EID: 52049087784     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2008.00691.x     Document Type: Review

References (97)

1. Fenner F, Henderson DA, Arita I, Jezek Z, Ladnyi ID. Smallpox and Its Eradication, 1st edn. Geneva : World Health Organization, 1988.
2. Breman JG, Henderson DA. Poxvirus dilemmas - monkeypox, smallpox. N Engl J Med 1998 339 : 556 559.
3. Reed KD, et al. The detection of monkeypox in humans in the Western Hemisphere. N Engl J Med 2004 350 : 342 350.
4. Amanna IJ, Slifka MK, Crotty S. Immunity and immunological memory following smallpox vaccination. Immunol Rev 2006 211 : 320 337.
5. Ladnyj ID, Ziegler P, Kima E. A human infection caused by monkeypox virus in Basankusu Territory, Democratic Republic of the Congo. Bull World Health Organ 1972 46 : 593 597.
6. Marennikova SS, Seluhina EM, Mal'ceva NN, Cimiskjan KL, Macevic GR. Isolation and properties of the causal agent of a new variola-like disease (monkeypox) in man. Bull World Health Organ 1972 46 : 599 611.
7. Khodakevich L, et al. The role of squirrels in sustaining monkeypox virus transmission. Trop Geogr Med 1987 39 : 115 122.
8. Khodakevich L, et al. Monkeypox virus in relation to the ecological features surrounding human settlements in Bumba zone, Zaire. Trop Geogr Med 1987 39 : 56 63.
9. Hutin YJ, et al. Outbreak of human monkeypox, Democratic Republic of Congo, 1996 to 1997. Emerg Infect Dis 2001 7 : 434 438.
10. Hutson CL, et al. Monkeypox zoonotic associations: insights from laboratory evaluation of animals associated with the multi-state US outbreak. Am J Trop Med Hyg 2007 76 : 757 768.
11. Hammarlund E, et al. Multiple diagnostic techniques identify previously vaccinated individuals with protective immunity against monkeypox. Nat Med 2005 11 : 1005 1011.
12. Di Giulio DB, Eckburg PB. Human monkeypox: an emerging zoonosis. Lancet Infect Dis 2004 4 : 15 25.
13. Nalca A, Rimoin AW, Bavari S, Whitehouse CA. Reemergence of monkeypox: prevalence, diagnostics, and countermeasures. Clin Infect Dis 2005 41 : 1765 1771.
14. Li Y, Olson VA, Laue T, Laker MT, Damon IK. Detection of monkeypox virus with real-time PCR assays. J Clin Virol 2006 36 : 194 203.
15. Karem KL, et al. characterization of acute-phase humoral immunity to monkeypox: use of immunoglobulin M enzyme-linked immunosorbent assay for detection of monkeypox infection during the 2003 North American outbreak. Clin Diagn Lab Immunol 2005 12 : 867 872.
16. Shchelkunov SN, et al. Analysis of the monkeypox virus genome. Virology 2002 297 : 172 194.
17. Breman JG, Kalisa R, Steniowski MV, Zanotto E, Gromyko AI, Arita I. Human monkeypox, 1970-79. Bull World Health Organ 1980 58 : 165 182.
18. Jezek Z, Fenner F. Human monkeypox. Monogr Virol 1988 17 : 1 140.
19. Chen N, et al. Virulence differences between monkeypox virus isolates from West Africa and the Congo basin. Virology 2005 340 : 46 63.
20. Likos AM, et al. A tale of two clades: monkeypox viruses. J Gen Virol 2005 86 : 2661 2672.
21. Goebel SJ, Johnson GP, Perkus ME, Davis SW, Winslow JP, Paoletti E. The complete DNA sequence of vaccinia virus. Virology 1990 179 : 247 266 517-563.
22. Johnson GP, Goebel SJ, Paoletti E. An update on the vaccinia virus genome. Virology 1993 196 : 381 401.
23. Barry M, Hnatiuk S, Mossman K, Lee SF, Boshkov L, McFadden G. The myxoma virus M-T4 gene encodes a novel RDEL-containing protein that is retained within the endoplasmic reticulum and is important for the productive infection of lymphocytes. Virology 1997 239 : 360 377.
24. Hnatiuk S, et al. Role of the C-terminal RDEL motif of the myxoma virus M-T4 protein in terms of apoptosis regulation and viral pathogenesis. Virology 1999 263 : 290 306.
25. Alcami A, Smith GL. A soluble receptor for interleukin-1b encoded by vaccinia virus - a novel mechanism of virus modulation of the host response to infection. Cell 1992 71 : 153 167.
26. Spriggs MK, et al. Vaccinia and cowpox viruses encode a novel secreted interleukin-1-binding protein. Cell 1992 71 : 145 152.
27. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 1996 87 : 2095 2147.
28. Smith GL, Symons JA, Khanna A, Vanderplasschen A, Alcami A. Vaccinia virus immune evasion. Immunol Rev 1997 159 : 137 154.
29. Alcami A, Smith GL. A mechanism for the inhibition of fever by a virus. Proc Natl Acad Sci USA 1996 93 : 11029 11034.
30. Kotwal GJ, Moss B. Vaccinia virus encodes a secretory polypeptide structurally related to complement control proteins. Nature 1988 335 : 176 178.
31. Kotwal GJ, Isaacs SN, McKenzie R, Frank MM, Moss B. Inhibition of the complement cascade by the major secretory protein of vaccinia virus. Science 1990 250 : 827 830.
32. Isaacs SN, Kotwal GJ, Moss B. Vaccinia virus complement-control protein prevents antibody-dependent complement-enhanced neutralization of infectivity and contributes to virulence. Proc Natl Acad Sci USA 1992 89 : 628 632.
33. Liszewski MK, et al. Structure and regulatory profile of the monkeypox inhibitor of complement: comparison to homologs in vaccinia and variola and evidence for dimer formation. J Immunol 2006 176 : 3725 3734.
34. Rosengard AM, Liu Y, Nie Z, Jimenez R. Variola virus immune evasion design: expression of a highly efficient inhibitor of human complement. Proc Natl Acad Sci USA 2002 99 : 8808 8813.
35. Blue CE, Spiller OB, Blackbourn DJ. The relevance of complement to virus biology. Virology 2004 319 : 176 184.
36. Liszewski MK, Farries TC, Lublin DM, Rooney IA, Atkinson JP. Control of the complement system. Adv Immunol 1996 61 : 201 283.
37. McKenzie R, Kotwal GJ, Moss B, Hammer CH, Frank MM. Regulation of complement activity by vaccinia virus complement-control protein. J Infect Dis 1992 166 : 1245 1250.
38. Sahu A, Isaacs SN, Soulika AM, Lambris JD. Interaction of vaccinia virus complement control protein with human complement proteins: factor I-mediated degradation of C3b to iC3b1 inactivates the alternative complement pathway. J Immunol 1998 160 : 5596 5604.
39. Rosengard AM, et al. Functional characterization of soluble and membrane-bound forms of vaccinia virus complement control protein (VCP). Mol Immunol 1999 36 : 685 697.
40. Smith SA, et al. Mapping of regions within the vaccinia virus complement control protein involved in dose-dependent binding to key complement components and heparin using surface plasmon resonance. Biochim Biophys Acta 2003 1650 : 30 39.
41. Bernet J, Mullick J, Panse Y, Parab PB, Sahu A. Kinetic analysis of the interactions between vaccinia virus complement control protein and human complement proteins C3b and C4b. J Virol 2004 78 : 9446 9457.
42. Sfyroera G, Katragadda M, Morikis D, Isaacs SN, Lambris JD. Electrostatic modeling predicts the activities of orthopoxvirus complement control proteins. J Immunol 2005 174 : 2143 2151.
43. Yadav VN, Pyaram K, Mullick J, Sahu A. Identification of hot spots in the variola virus complement inhibitor (SPICE) for human complement regulation. J Virol 2008 82 : 3283 3294.
44. Smith SA, et al. Conserved surface-exposed K/R-X-K/R motifs and net positive charge on poxvirus complement control proteins serve as putative heparin-binding sites and contribute to inhibition of molecular interactions with human endothelial cells: a novel mechanism for evasion of host defense. J Virol 2000 74 : 5659 5666.
45. Uvarova EA, Shchelkunov SN. Species-specific differences in the structure of orthopoxvirus complement-binding protein. Virus Res 2001 81 : 39 45.
46. Girgis NM, Dehaven BC, Fan X, Viner KM, Shamim M, Isaacs SN. Cell surface expression of the vaccinia virus complement control protein is mediated by interaction with the viral a56 protein and protects infected cells from complement attack. J Virol 2008 82 : 4205 4214.
47. Carroll MC. The complement system in regulation of adaptive immunity. Nat Immunol 2004 5 : 981 986.
48. Kemper C, Atkinson JP. T-cell regulation: with complements from innate immunity. Nat Rev Immunol 2007 7 : 9 18.
49. Shchelkunov SN, et al. Human monkeypox and smallpox viruses: genomic comparison. FEBS Lett 2001 509 : 66 70.
50. Massung RF, et al. Analysis of the complete genome of smallpox variola major virus strain Bangladesh-1975. Virology 1994 201 : 215 240.
51. Shchelkunov SN, Massung RF, Esposito JJ. Comparison of the genome DNA sequences of Bangladesh-1975 and India-1967 variola viruses. Virus Res 1995 36 : 107 118.
52. Moore JB, Smith GL. Steroid hormone synthesis by a vaccinia enzyme - a new type of virus virulence factor. EMBO J 1992 11 : 1973 1980.
53. Reading PC, Moore JB, Smith GL. Steroid hormone synthesis by vaccinia virus suppresses the inflammatory response to infection. J Exp Med 2003 197 : 1269 1278.
54. Price N, Tscharke DC, Hollinshead M, Smith GL. Vaccinia virus gene B7R encodes an 18-kDa protein that is resident in the endoplasmic reticulum and affects virus virulence. Virology 2000 267 : 65 79.
55. Kluczyk A, Siemion IZ, Szewczuk Z, Wieczorek Z. The immunosuppressive activity of peptide fragments of vaccinia virus C10L protein and a hypothesis on the role of this protein in the viral invasion. Peptides 2002 23 : 823 834.
56. McCraith S, Holtzman T, Moss B, Fields S. Genome-wide analysis of vaccinia virus protein-protein interactions. Proc Natl Acad Sci USA 2000 97 : 4879 4884.
57. Chang HW, Jacobs BL. Identification of a conserved motif that is necessary for binding of the vaccinia virus E3L gene products to double-stranded RNA. Virology 1993 194 : 537 547.
58. Brandt TA, Jacobs BL. Both carboxy- and amino-terminal domains of the vaccinia virus interferon resistance gene, E3L, are required for pathogenesis in a mouse model. J Virol 2001 75 : 850 856.
59. Chang HW, Watson JC, Jacobs BL. The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. Proc Natl Acad Sci USA 1992 89 : 4825 4829.
60. Beattie E, Paoletti E, Tartaglia J. Distinct patterns of IFN sensitivity observed in cells infected with vaccinia K3L- and E3L-mutant viruses. Virology 1995 210 : 254 263.
61. Alcami A, Smith GL. Receptors for gamma-interferon encoded by poxviruses: implications for the unknown origin of vaccinia virus. Trends Microbiol 1996 4 : 321 326.
62. Rivas C, Gil J, Melkova Z, Esteban M, Diaz-Guerra M. Vaccinia virus E3L protein is an inhibitor of the interferon (i.f.n.)-induced 2-5A synthetase enzyme. Virology 1998 243 : 406 414.
63. Yuwen H, Cox JH, Yewdell JW, Bennink JR, Moss B. Nuclear localization of a double-stranded RNA-binding protein encoded by the vaccinia virus E3L gene. Virology 1993 195 : 732 744.
64. Kwon JA, Rich A. Biological function of the vaccinia virus Z-DNA-binding protein E3L: gene transactivation and antiapoptotic activity in HeLa cells. Proc Natl Acad Sci USA 2005 102 : 12759 12764.
65. Langland JO, Kash JC, Carter V, Thomas MJ, Katze MG, Jacobs BL. Suppression of proinflammatory signal transduction and gene expression by the dual nucleic acid binding domains of the vaccinia virus E3L proteins. J Virol 2006 80 : 10083 10095.
66. Davies MV, Elroy-Stein O, Jagus R, Moss B, Kaufman RJ. The vaccinia virus K3L gene product potentiates translation by inhibiting double-stranded-RNA- activated protein kinase and phosphorylation of the alpha subunit of eukaryotic initiation factor 2. J Virol 1992 66 : 1943 1950.
67. Beattie E, Tartaglia J, Paoletti E. Vaccinia virus encoded eIF-2a homolog abrogates the antiviral effect of interferon. Virology 1991 183 : 419 422.
68. Martin KH, Grosenbach DW, Franke CA, Hruby DE. Identification and analysis of three myristylated vaccinia virus late proteins. J Virol 1997 71 : 5218 5226.
69. Eckert D, Williams O, Meseda CA, Merchlinsky M. Vaccinia virus nicking-joining enzyme is encoded by K4L (VACWR035). J Virol 2005 79 : 15084 15090.
70. Banham AH, Smith GL. Characterization of vaccinia virus gene B12R. J Gen Virol 1993 74 : 2807 2812.
71. Sedgwick SG, Smerdon SJ. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 1999 24 : 311 316.
72. Oguiura N, Spehner D, Drilien R. Detection of a protein encoded by the vaccinia virus C7L open reading frame and study of its effect on virus multiplication in different cell lines. J Gen Virol 1993 74 : 1409 1413.
73. Meng X, Chao J, Xiang Y. Identification from diverse mammalian poxviruses of host-range regulatory genes functioning equivalently to vaccinia virus C7L. Virology 2008 372 : 372 383.
74. Spehner D, Gillard S, Drillien R, Kirn A. A cowpox virus gene required for multiplication in Chinese hamster ovary cells. J Virol 1988 62 : 1297 1304.
75. Ink BS, Gilbert CS, Evan GI. Delay of vaccinia virus-induced apoptosis in nonpermissive Chinese hamster ovary cells by the cowpox virus CHOhr and adenovirus E1B 19 K genes. J Virol 1995 69 : 661 668.
76. Schwarz DA, Katayama CD, Hedrick SM. Schlafen, a new family of growth regulatory genes that affect thymocyte development. Immunity 1998 9 : 657 668.
77. Jezek Z, Szczeniowski M, Paluku KM, Mutombo M. Human monkeypox: clinical features of 282 patients. J Infect Dis 1987 156 : 293 298.
78. Fine PE, Jezek Z, Grab B, Dixon H. The transmission potential of monkeypox virus in human populations. Int J Epidemiol 1988 17 : 643 650.
79. Karem KL, Reynolds M, Olson V, Li Y, Damon IK. Monkeypox outbreak diagnostics and implications for vaccine protective effect. Nat Med 2006 12 : 495 496 author reply 496-497.
80. Manes NP, et al. Comparative proteomics of human monkeypox and vaccinia intracellular mature and extracellular enveloped virions. J Proteome Res 2008 7 : 960 968.
81. Monath TP, et al. ACAM2000 clonal Vero cell culture vaccinia virus (New York City Board of Health Strain) - a second-generation smallpox vaccine for biological defense. Int J Infect Dis 2004 8 (Suppl.) : 31 44.
82. CDC. Notice to readers: newly licensed smallpox vaccine to replace old smallpox vaccine. Morb Mortal Wkly Rep 2008 57 : 207 208.
83. Pelletier J, Sonenberg N. Insertion mutagenesis to increase secondary structure within the 5′ noncoding region of a eukaryotic mRNA reduces translational efficiency. Cell 1985 40 : 515 526.
84. Colamonici OR, Domanski P, Sweitzer SM, Larner A, Buller RM. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling. J Biol Chem 1995 270 : 15974 15978.
85. Alcami A, Symons JA, Smith GL. The vaccinia virus soluble alpha/beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J Virol 2000 74 : 11230 11239.
86. Xu RH, et al. The orthopoxvirus type I IFN binding protein is essential for virulence and an effective target for vaccination. J Exp Med 2008 205 : 981 992.
87. Hu FQ, Smith CA, Pickup DJ. Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. Virology 1994 204 : 343 356.
88. Alcami A, Khanna A, Paul NL, Smith GL. Vaccinia virus strains Lister, USSR and Evans express soluble and cell-surface tumour necrosis factor receptors. J Gen Virol 1999 80 : 949 959.
89. Jezek Z, Arita I, Mutombo M, Dunn C, Nakano JH, Szczeniowski M. Four generations of probable person-to-person transmission of human monkeypox. Am J Epidemiol 1986 123 : 1004 1012.
90. Jezek Z, Grab B, Szczeniowski MV, Paluku KM, Mutombo M. Human monkeypox: secondary attack rates. Bull World Health Organ 1988 66 : 465 470.
91. CDC. Human monkeypox - Kasai Oriental, Democratic Republic of Congo. Morb Mortal Wkly Rep 1997 46 : 1168 1171.
92. CDC. Human monkeypox - Kasai Oriental, Democratic Republic of Congo, February 1996-October 1997. Morb Mortal Wkly Rep 1997 46 : 1168 1171.
93. Heymann DL, Szczeniowski M, Esteves K. Re-emergence of monkeypox in Africa: a review of the past six years. Br Med Bull 1998 54 : 693 702.
94. Learned LA, et al. Extended interhuman transmission of monkeypox in a hospital community in the Republic of the Congo, 2003. Am J Trop Med Hyg 2005 73 : 428 434.
95. Antia R, Regoes RR, Koella JC, Bergstrom CT. The role of evolution in the emergence of infectious diseases. Nature 2003 426 : 658 661.
96. Lederman ER, et al. Prevalence of antibodies against orthopoxviruses among residents of Likouala region, Republic of Congo: evidence for monkeypox virus exposure. Am J Trop Med Hyg 2007 77 : 1150 1156.
97. Jezek Z, Nakano JH, Arita I, Mutombo M, Szczeniowski M, Dunn C. Serological survey for human monkeypox infections in a selected population in Zaire. J Trop Med Hyg 1987 90 : 31 38.