Immunomodulation by viruses: The myxoma virus story

Immunological Reviews

Volumn 168, Issue , 1999, Pages 103-120

  Nash, Piers ^a,b   Barrett, John ^a   Jing Xin, Cao ^a   Hota Mitchell, Sheela ^a   Lalani, Alshad S ^a,b   Everett, Helen ^b   Xiao Ming, Xu ^a   Robichaud, Janine ^a   Hnatiuk, Shawna ^a   Ainslie, Cheryl ^a   Seet, Bruce T ^a   McFadden, Grant ^a  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; CYTOKINE; VIRUS PROTEIN;

APOPTOSIS; CELLULAR IMMUNITY; IMMUNE RESPONSE; IMMUNOMODULATION; NONHUMAN; POXVIRUS; PRIORITY JOURNAL; RABBIT; REVIEW; VIRUS CELL INTERACTION;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CYTOKINES; HUMANS; MOLECULAR SEQUENCE DATA; MYXOMA VIRUS; MYXOMATOSIS, INFECTIOUS; RABBITS; VIRAL PROTEINS;

EID: 0033037558     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-065X.1999.tb01286.x     Document Type: Review

References (118)

1. 1. Ploegh HL. Viral strategies of immune evasion. Science 1998;280:248-253.
2. 2. Barry M, McFadden G. Virus encoded cytokines and cytokine receptors. Parasitology 1998;115:S89-S100.
3. 3. Gooding LR. Virus proteins that counteract the immune system. Cell 1992;71:5-7.
4. 4. Smith GL. Virus strategies for evasion of the host response to infection. Trends Microbiol 1994;2:81-88.
5. 5. Spriggs MK. One step ahead of the game: viral immunomodulatory molecules. Annu Rev Immunol 1996;14:101-131.
6. 6. Moss B. Replication of poxviruses. In: Fields BN, Knipe DM, Howley PM, eds. Virology. 3rd ed. New York: Lippincott Raven Press; 1996. p. 2637-2671.
7. 7. Fenner F, Wittek R, Dumbell KR. The orthopoxviruses. London: Academic Press; 1989.
8. 8. Turner PC, Moyer RW. The molecular pathogenesis of poxviruses. Curr Top Microbiol Immunol 1990;163:125-151.
9. 9. Buller RLM, Palumbo GJ. Poxvirus pathogenesis. Microbiol Rev 1991;55:80-122.
10. 10. Smith GL. Vaccinia virus glycoproteins and immune evasion. J Gen Virol 1993;74:1725-1740.
11. 11. McFadden G. Viroceptors, virokines and related immune modulators encoded by DNA viruses. Austin (TX): R. G. Landes Company; 1995.
12. 12. Barinaga M. Viruses launch their own "Star Wars". Science 1992;258:1730-1731.
13. 13. Fenner F, Ratcliffe FN. Myxomarosis. Cambridge, UK: Cambridge University Press; 1965.
14. 14. Fenner F, Myers K. Myxoma virus and myxomatosis in retrospect: the first quarter century of a new disease. In: Kurstok E, Maramorosch K, eds. Viruses and environment New York: Academic Press; 1978. p. 539-570.
15. 15. Strayer D. Poxviruses. In: Specter S, Bendinelli M, Friedman H, eds. Virus-induced immunosuppression. New York: Plenum Press; 1989. p. 173-192.
16. 16. DiGiacomo RF, Mare CJ. Viral diseases. In: Manning PJ, Ringler DH, Newcomer CE, eds. The biology of the laboratory rabbit. 2nd ed. New York, London: Academic Press; 1994. p. 171-204.
17. 17. Kerr PJ, Best SM. Myxoma virus in rabbits. Rev Sci Tech 1998;17:256-268.
18. 18. Pickup DJ. Poxviral modifiers of cytokine responses to infection. Infect Agents Dis 1994;3:116-127.
19. 19. Alcami A, Smith GL. Cytokine receptors encoded by poxviruses: a lesson in cytokine biology. Immunol Today 1995;16:474-478.
20. 20. McFadden G, et al. Interruption of cytokine networks by poxviruses: lessons from myxoma virus. J Leuk Biol 1995;57:731-738.
21. 21. Upton C, Macen JL, Schreiber M, McFadden G. Myxoma virus expresses a secreted protein with homology to the tumor necrosis factor receptor gene family that contributes to viral virulence. Virology 1991;184:370-382.
22. 22. Upton C, DeLange AM, McFadden G. Tumorigenic poxviruses: genomic organization and DNA sequence of the telomeric region of the Shope fibroma virus genome. Virology 1987;160:20-30.
23. 23. Smith CA, et al. A receptor for tumor necrosis factor defines an unusual family of cellular and viral proteins. Science 1990;248:1019-1023.
24. 24. Wong GHW, Kamb A, Goeddel DV. Antiviral properties of TNF. In: Buetler B, ed. Tumor necrosis factors: the molecules and their emerging role in medicine. New York: Raven Press, Ltd; 1992. p. 371-381.
25. 25. Howard ST, Chan YC, Smith GL. Vaccinia virus homologues of the Shope fibroma virus inverted terminal repeat proteins and a discontinuous ORF related to the tumour necrosis factor receptor family. Virology 1991;180:633-647.
26. 26. Hu F-Q, 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.
27. 27. Shchelkunov SN, Blinov VM, Sandakhchiev LS. Genes of variola and vaccinia viruses necessary to overcome the host protective mechanism. FEBS Lett 1993;319:80-83.
28. 28. Schreiber M, McFadden G. The myxoma virus TNF receptor homologue inhibits TNFα in a species specific fashion. Virology 1994;204:692-705.
29. 29. Schreiber M, Rajarathnam K, McFadden G. Mxyoma virus T2 protein, a tumor necrosis factor (TNF) receptor homolog, is secreted as a monomer and dimer that each bind rabbit TNFα, but the dimer is a more potent TNF inhibitor. J Biol Chem 1996;271:13333-13341.
30. 30. Schreiber M, McFadden G. Murational analysis of the ligand binding domain of M-T2 protein, the tumor necrosis factor receptor homologue of myxoma virus. J Immunol 1996;157:4486-4495.
31. 31. Schreiber M, Sedger L, McFadden G. Distinct domains of M-T2, the myxoma virus TNF receptor homolog, mediate extracellular TNF binding and intracellular apoptosis inhibition. J Virol 1997;71:2171-2181.
32. 32. Baggiolini M. Chemokines and leukocyte traffic. Nature 1998;392:565-568.
33. 33. Luster AD. Chemokines: chemotactic cytokines that mediate inflammation. N Engl J Med 1998;338:436-445.
34. 34. Graham KA, et al. The T1/35kDa family of poxvirus secreted proteins bind chemokines and modulate leukocyte influx into virus infected tissues. Virology 1997;229:12-24.
35. 35. Lalani AS, et al. Functional comparisons among members of the poxvirus T1/35kDa family of soluble CC-chemokine inhibitor glycoproteins. Virology 1998;250:173-184.
36. 36. Lalani AS, et al. The purified myxoma virus IFN-γ receptor homolog, M-T7, interacts with the heparin binding domains of chemokines. J Virol 1997;71:4356-4363.
37. 37. Alcami A, Symons JA, Collins PD, Williams TJ, Smith GL. Blockade of chemokine activity by a soluble chemokine binding protein from vaccinia virus. J Immunol 1998;160:624-633.
38. 38. Smith CA, et al. Poxvirus genomes encode a secreted soluble protein that preferentially inhibits β chemokine activity yet lacks sequence homology to known chemokine receptors. Virology 1997;236:316-327.
39. 39. Martinez-Pornares L, Thompson JP, Moyer RW. Mapping and investigation of the role in pathogenesis of the major unique secreted 35-kDa protein of rabbitpox virus. Virology 1995;206:591-600.
40. 40. Patel AH, Gaffney DF, Subak-Sharpe JH, Stow ND. DNA sequence of the gene encoding a major secreted protein of vaccinia virus, strain Lister. J Gen Virol 1990;71:2013-2021.
41. 41. Lalani AS, Masters JM, Graham KA, Liu L-Y, Lucas A, McFadden G. The role of the myxoma virus soluble CC-chemokine inhibitor glycoprotein, M-T1, during myxoma virus pathogenesis. Virology (In press).
42. 42. Boehm U, Klamp T, Groot M, Howard JC. Cellular responses to interferon-γ Annu Rev Immunol 1997;15:749-795.
43. 43. Upton C, Mossman K, McFadden G. Encoding of a homolog of the interferon-γ receptor by myxoma virus. Science 1992;258:1369-1372.
44. 44. Mossman K, Upton C, McFadden G. The myxoma virus-soluble interferon-γ receptor homolog, M-T7, inhibits interferon-γ in a species-specific manner. J Biol Chem 1995;270:3031-3038.
45. 45. Massung RF, et al. Analysis of the complete genome of smallpox variola major virus strain Bangladesh-1975. Virology 1994;201:215-240.
46. 46. Mossman K, Upton C, Buller RM, McFadden G. Species specificity of ectromelia virus and vaccinia virus interferon-γ binding proteins. Virology 1995;208:762-769.
47. 47. Alcami A, Smith GL. Vaccinia, cowpox and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. J Virol 1995;69:4633-4639.
48. 48. McFadden G, Lalani A, Everett H, Nash P, Xu X. Virus encoded-receptors for cytokines and chemokines. Semin Cell Dev Biol 1998;9:359-368.
49. 49. Mossman K, Nation P, Macen J, Garbutt M, Lucas A, McFadden G. Myxoma virus M-T7, a secreted homolog of the interferon-γ receptor, is a critical virulence factor for the development of myxomatosis in European rabbits. Virology 1996;215:17-30.
50. 50. Schluger NW, Rom WN. Early responses to infection: chemokines as mediators of inflammation. Curr Opin Immunol 1997;9:504-508.
51. 51. Guido D. Integral membrane heparan sulfate proteoglycans. FASEB J 1993;7:1023-1030.
52. 52. Taub DD. Chemokine-leukocyte interactions: the voodoo that they do so well. Cytokine Growth Factor Rev 1996;7:355-376.
53. 53. Kotwal GJ, Moss B. Vaccinia virus encodes a secretory polypeptide structurally related to complement control proteins. Nature 1988;335:176-178.
54. 54. Upton C, Macen JL, Wishart DS, McFadden G. Myxoma virus and malignant rabbit fibroma virus encode a serpin like protein important for virus virulence. Virology 1990;179:618-631.
55. 55. Nash P, Lucas A, McFadden G. SERP-1, a poxvirus-encoded serpin, is expressed as a secreted glycoprotein that inhibits the inflammatory response to myxoma virus infection. In: Church FC, Cunningham DD, Ginsburg D, Huffman M, Stone SR, Tollefsen DM. eds. Chemistry and biology of serpins. New York: Oxford University Press; 1997. p. 195-205.
56. 56. Chang W, Upton C, Hu SL, Purchio AF, McFadden G. The genome of Shope fibroma virus, a tumorigenic poxvirus, contains a growth factor gene with sequence similarity to those encoding epidermal growth factor and transforming growth factor α Mol Cell Biol 1987;7:535-540.
57. 57. Upton C, Macen JL, McFadden G. Mapping and sequencing of a gene from myxoma virus that is related to those encoding epidermal growth factor and transforming growth factor α. J Virol 1987;61:1271-1275.
58. 58. McFadden G, Graham K, Opgenorth A. Poxvirus growth factors. In: McFadden G, ed. Viroceptors, virokines and related immune modulators encoded by DNA viruses. Austin (TX): R. G. Landes Company; 1995. p. 1-15.
59. 59. Chang W, Macaulay C, Hu SL, Tarn JP, McFadden G. Tumorigenic poxviruses: characterization of the expression of an epidermal growth factor related gene in Shope fibroma virus. Virology 1990;179:926-930.
60. 60. Stroobant P, Rice AP, Gullick WJ, Cheng DJ, Kerr IM, Watefield MD. Purification and characterization of vaccinia virus growth factor. Cell 1985;42:383-393.
61. 61. Chang W, Lim JG, Hellström I, Gentry LE. Characterization of vaccinia virus growth factor biosynthetic pathway with an antipeptide antiserum. J Virol 1988;62:1080-1083.
62. 62. Lin Y-Z, Le X-H, Tam JP. Synthesis and structure-activity study of myxoma virus growth factor. Biochemistry 1991;30:3310-3314.
63. 63. Lin Y-Z, Caporaso G, Chang P-Y, Ke X-H, Tam JP. Synthesis of a biological active tumor growth factor from the predicted DNA sequence of Shope fibroma virus. Biochemistry 1988;27:5640-5645.
64. 64. Opgenorth A, Nation N, Graham K, McFadden G. Transforming growth factor α, Shope fibroma growth factor, and vaccinia growth factor can replace myxoma growth factor in the induction of myxomatosis in rabbits. Virology 1993;192:701-709.
65. 65. Opgenorth A, Graham K, Nation N, Strayer D, McFadden G. Deletion analysis of two tandemly arranged virulence genes in myxoma virus, MI IL and myxoma growth factor. J Virol 1992;66:4720-4731.
66. 66. Strayer DS, Yang S, Schwantz MS. Epidermal growth factor-like growth factors. I. Breast malignancies and other epithelial proliferations in transgenic mice. Lab Invest 1993;69:660-673.
67. 67. Tzahar E, et al. Pathogenic poxviruses reveal viral strategies to exploit the ErbB signaling network. EMBO J 1998;17:5948-5963.
68. 68. Rubin H. Serine protease inhibitors (SERPINS): where mechanism meets medicine. Nat Med 1996;2:632-633.
69. 69. Church FC, Cunningham DD, Ginsburg D, Hoffman M, Stone SR, Tollefson DM, eds. Chemistry and biology of serpins. New York: Oxford University Press; 1997.
70. 70. Stein PE, Carrell RW. What do dysfunctional serpms tell us about molecular mobility and disease? Nat Struct Biol 1995;2:96-113.
71. 71. Yenbutr P, Scott AI.. Molecular cloning of a serine proteinase inhibitor from Brugia malayi. Infect Immun 1995;63:1745-1753.
72. 72. Ghendler Y, Arnon R, Fishelson Z. Schistosoma mansoni: isolation and characterization of Smpi56, a novel serine protease inhibitor. Exp Parisitol 1994;78:121-131.
73. 73. Blanton RE, Licate LS, Aman RA. Characterization of a native and recombinant Schistosoma haematobium serine protease inhibitor gene product. Mol Biochem Parasitol 1994;63:1-11.
74. 74. Turner PC, Musy PW, Moyer RW. Poxvirus serpins. In: McFadden G, ed. Viroceptors, virokines and related immune modulators encoded by DNA viruses. Austin (TX): R. G. Landes Company; 1995. p. 67-88.
75. 75. Macen JL, Upton C, Nation N, McFadden G. SERP-1, a serine proteinase inhibitor encoded by myxoma virus, is a secreted glycoprotein that interferes with inflammation. Virology 1993;195:348-363.
76. 76. Lomas DA, Evans DL, Upton C, McFadden C, Carrell RW. Inhibition of plasmin, urokinase, tissue plasminogen activator, and C1S by a myxoma virus serine proteinase inhibitor. J Biol Chem 1993;268:516-521.
77. 77. Nash P, Whitty A, Handwerker J, Macen J, McFadden G. Inhibitory specificity of the anti inflammatory myxoma virus serpin, Serp-1. J Biol Chem 1998;273:20982-20991.
78. 78. Lucas A, et al. Virus-encoded serine proteinase inhibitor SERP-1 inhibits atherosclerotic plaque development after balloon angioplasty. Circulation 1996;94:2890-2900.
79. 79. Maksymowych WP, et al. Amelioration of antigen-induced arthritis in rabbits treated with a secreted viral serine proteinase inhibitor. J Rheum 1996;23:878-882.
80. 80. McFadden G, Barry M. How poxviruses oppose apoptosis. Semin Virol 1998;8:429-442.
81. 81. O'Brien V. Viruses and apoptosis. J Gen Virol 1998;79:1833-1845.
82. 82. Nicholson DW, Thornberry NA. Caspases: killer proteases. Trends Biochem Sci 1997;22:299-306.
83. 83. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science 1998;281:1312-1316.
84. 84. Petit F, Bertagnoli S, Gelfi J, Fassy F, Boucraut-Baralon C, Milon A. Characterization of a myxoma virus encoded serpin-like protein with activity against interleukin-1β converting enzyme. J Virol 1996;70:5860-5866.
85. 85. Pickup DJ, Ink BS, Hu W, Ray CA, Joklik WK. Hemorrhage in lesions caused by cowpox virus is induced by a viral protein that is related to plasma protein inhibitors of serine protease. Proc Natl Acad Sci USA 1986;83:7698-7702.
86. 86. Smith GL, Howard ST, Chan YS. Vaccinia virus encodes a family of genes with homology to serine proteinase inhibitors. J Gen Virol 1989;70:2333-2343.
87. 87. Ray CA, et al. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin 1β converting enzyme. Cell 1992;69:597-604.
88. 88. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Litwack G, Alnemri ES. Molecular ordering of the Fas-apoptotic pathway: the Fas/APO-1 protease Mch5 is a CrmA-inhibitable protease that activates multiple Ced-3/ICE-like cysteine proteases. Proc Natl Acad Sci USA 1996;93:14486-14491.
89. 89. Quan LT, Caputo A, Bleackley RC, Pickup DJ, Salvesen GS. Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A. J Biol Chem 1995;270:10377-10379.
90. 90. Miura M, Zhu H, Rotello R, Hatweig EA, Yuan J. Induction of apoptosis in fibroblasts by IL-1β-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 1993;75:653-660.
91. 91. Enari M, Hug H, Nagata S. Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature 1995;375:78-81.
92. 92. Tewari M, Dixit VM. Fas-and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product. J Biol Chem 1995;270:3255-3260.
93. 93. Tewari M, Telford WG, Miller RA, Dixit VM. Crm A, a poxvirus encoded serpin, inhibits cytotoxic T-lymphocyte-mediated apoptosis. J Biol Chem 1995;270:22705-22708.
94. 94. Gagliardini V, et al. Prevention of vertebrate neuronal death by the crmA gene. Science 1994;263:826-828.
95. 95. Turner PC, Moyer RW. The control of apoptosis by poxviruses. Semin Virol 1998;8:453-469.
96. 96. Messud-Petit F, et al. SERP-2, an inhibitor of the interleukin-1β-converting enzyme, is critical in the pathobiology of myxoma virus. J Virol 1998;72:7830-7839.
97. 97. Macen JL, Graham KA, Lee SF, Schreiber M, Boshkov LK, McFadden G. Expression of the myxoma virus tumor necrosis factor receptor homologue (T2) and MI IL genes is required to prevent virus-induced apoptosis in infected rabbit T lymphocytes. Virology 1996;218:232-237.
98. 98. Graham KA, Opgenorth A, Upton C, McFadden G. Myxoma virus MIII. ORF encodes a protein for which cell surface localization is critical for manifestation of viral virulence. Virology 1992;191:112-124.
99. 99. Lambert S, et al. cDNA sequence for human erythrocyte ankyrin. Proc Natl Acad Sci USA 1990;87:1730-1734.
100. 100. Mossman K, Lee SF, Barry M, Boshkov L, McFadden G. Disruption of M-T5, a novel myxoma virus gene member of the poxvirus host range superfamily, results in dramatic attentuation of myxomatosis in infected European rabbits. J Virol 1996;70:4394-4410.
101. 101. Dedhar S, Hannigan GF. Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr Opin Cell Biol 1996;8:657-659.
102. 102. Baldwin AS Jr. The NF κB and IκB proteins: new discoveries and insights. Annu Rev Immunol 1996;14:641-681.
103. 103. Sachdev S, Hoffman A, Hannink M. Nuclear localization of IκB is mediated by the second ankyrin repeat: the IκBα ankyrin repeats define a novel class of cis-acting nuclear import sequences. Mol Cell Biol 1998;18:2524-2534.
104. 104. Revilla Y, Cebrián A, Baixerás E, Martiacute;nez C, Vinuela E, Salas ML. Inhibition of apoptosis by the African swine fever virus bcl-2 homologue: role of the BH1 domain. Virology 1997;228:400-404.
105. 105. Miskin JE, Abrams CC, Goatley LC, Dixon LK. A viral mechanism for inhibition of the cellular phosphatase calcineurin. Science 1998;281:562-565.
106. 106. Barry M, Hnatiuk S, Mossman K, Lee S-F, 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.
107. 107. Pelham HRB. The retention signal for soluble proteins of the endoplasmic reticulum. Trends Biochem Sci 1990;15:483-486.
108. 108. Pelham HRB. Control of protein exit from the endoplasmic reticulum. Annu Rev Cell Biol 1989;5:1-23.
109. 109. Liu LX, et al. Binding of HIV-1 Nef to a novel thioesterase enzyme correlates with Nef-mediated CD4 downregulation. J Biol Chem 1997;272:13779-13785.
110. 110. Aiken C, Konner J, Lindau NR, Lenburg ME, Trono D. Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 1994;76:853-864.
111. 111. Willey RL, Maldarelli F, Martin MA, Strebel K. Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J Virol 1992;66:7193-7200.
112. 112. Boshkov LK, Macen JL, McFadden G. Virus-induced loss of class I major histocompatibility antigens from the surface of cells infected with myxoma virus and malignant rabbit fibroma virus. J Immunol 1992;148:881-887.
113. 113. Wold WSM, Gooding L. Region E3 of adenovirus: a cassette of genes involved in host immunosurveillance and virus cell interactions. Virology 1991;184:1-8.
114. + T lymphocytes. J Virol 1995;69:5243-5251.
115. 115. Bertin J, et al. Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas-and TNFR1-induced apoptosis. Proc Natl Acad Sci USA 1997;94:1772-1776.
116. 116. Shisler JL, Senkevich TG, Berry MJ, Moss B. Ultraviolet-induced cell death blocked by a selenoprotein from a human dermatotropic poxvirus. Science 1998;279:102-105.
117. 117. Essani K, Chalasani S, Eversole R, Beuving L, Birmingham L. Multiple anti-cytokine activities secreted from tanapox virus-infected cells. Microb Pathog 1994;17:347-353.
118. 118. Perkus ME, Goebel SJ, Davis SW, Johnson GP, Norton EK, Paoletti E. Deletion of 55 open reading frames from the termini of vaccinia virus. Virology 1991;180:406-410