1887

Abstract

Many viruses have evolved strategies to deregulate the host immune system. These strategies include mechanisms to subvert or recruit the host cytokine network. IL-10 is a pleiotropic cytokine that has both immunostimulatory and immunosuppressive properties. However, its key features relate mainly to its capacity to exert potent immunosuppressive effects. Several viruses have been shown to upregulate the expression of cellular IL-10 (cIL-10) with, in some cases, enhancement of infection by suppression of immune functions. Other viruses encode functional orthologues of cIL-10, called viral IL-10s (vIL-10s). The present review is devoted to these virokines. To date, vIL-10 orthologues have been reported for 12 members of the family , two members of the family and seven members of the family . Study of vIL-10s demonstrated several interesting aspects on the origin and the evolution of these viral genes, e.g. the existence of multiple (potentially up to nine) independent gene acquisition events at different times during evolution, viral gene acquisition resulting from recombination with cellular genomic DNA or cDNA derived from cellular mRNA and the evolution of cellular sequence in the viral genome to restrict the biological activities of the viral orthologues to those beneficial for the virus life cycle. Here, various aspects of the vIL-10s described to date are reviewed, including their genetic organization, protein structure, origin, evolution, biological properties and potential in applied research.

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2014-02-01
2024-04-16
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References

  1. Allavena P., Piemonti L., Longoni D., Bernasconi S., Stoppacciaro A., Ruco L., Mantovani A. 1998; IL-10 prevents the differentiation of monocytes to dendritic cells but promotes their maturation to macrophages. Eur J Immunol 28:359–369 [View Article][PubMed]
    [Google Scholar]
  2. Aoki T., Hirono I., Kurokawa K., Fukuda H., Nahary R., Eldar A., Davison A. J., Waltzek T. B., Bercovier H., Hedrick R. P. 2007; Genome sequences of three koi herpesvirus isolates representing the expanding distribution of an emerging disease threatening koi and common carp worldwide. J Virol 81:5058–5065 [View Article][PubMed]
    [Google Scholar]
  3. Arrand J. R., Rymo L., Walsh J. E., Björck E., Lindahl T., Griffin B. E. 1981; Molecular cloning of the complete Epstein-Barr virus genome as a set of overlapping restriction endonuclease fragments. Nucleic Acids Res 9:2999–3014 [View Article][PubMed]
    [Google Scholar]
  4. Avdic S., Cao J. Z., Cheung A. K., Abendroth A., Slobedman B. 2011; Viral interleukin-10 expressed by human cytomegalovirus during the latent phase of infection modulates latently infected myeloid cell differentiation. J Virol 85:7465–7471 [View Article][PubMed]
    [Google Scholar]
  5. Avdic S., Cao J. Z., McSharry B. P., Clancy L. E., Brown R., Steain M., Gottlieb D. J., Abendroth A., Slobedman B. 2013; Human cytomegalovirus interleukin-10 polarizes monocytes toward a deactivated M2c phenotype to repress host immune responses. J Virol 87:10273–10282 [View Article][PubMed]
    [Google Scholar]
  6. Banchereau J., Pascual V., O’Garra A. 2012; From IL-2 to IL-37: the expanding spectrum of anti-inflammatory cytokines. Nat Immunol 13:925–931 [View Article][PubMed]
    [Google Scholar]
  7. Bartlett N. W., Dumoutier L., Renauld J. C., Kotenko S. V., McVey C. E., Lee H. J., Smith G. L. 2004; A new member of the interleukin 10-related cytokine family encoded by a poxvirus. J Gen Virol 85:1401–1412 [View Article][PubMed]
    [Google Scholar]
  8. Brady M. T., MacDonald A. J., Rowan A. G., Mills K. H. G. 2003; Hepatitis C virus non-structural protein 4 suppresses Th1 responses by stimulating IL-10 production from monocytes. Eur J Immunol 33:3448–3457 [View Article][PubMed]
    [Google Scholar]
  9. Bratke K. A., McLysaght A. 2008; Identification of multiple independent horizontal gene transfers into poxviruses using a comparative genomics approach. BMC Evol Biol 8:67 [View Article][PubMed]
    [Google Scholar]
  10. Brockman M. A., Kwon D. S., Tighe D. P., Pavlik D. F., Rosato P. C., Sela J., Porichis F., Le Gall S., Waring M. T. other authors 2009; IL-10 is up-regulated in multiple cell types during viremic HIV infection and reversibly inhibits virus-specific T cells. Blood 114:346–356 [View Article][PubMed]
    [Google Scholar]
  11. Brodeur N. D., Spencer J. V. 2010; Antibodies to human IL-10 neutralize ebvIL-10-mediated cytokine suppression but have no effect on cmvIL-10 activity. Virus Res 153:265–268 [View Article][PubMed]
    [Google Scholar]
  12. Brunovskis P., Kung H. J. 1995; Retrotransposition and herpesvirus evolution. Virus Genes 11:259–270 [View Article][PubMed]
    [Google Scholar]
  13. Cai G., Kastelein R. A., Hunter C. A. 1999; IL-10 enhances NK cell proliferation, cytotoxicity and production of IFN-gamma when combined with IL-18. Eur J Immunol 29:2658–2665 [View Article][PubMed]
    [Google Scholar]
  14. Carson W. E., Lindemann M. J., Baiocchi R., Linett M., Tan J. C., Chou C.-C., Narula S., Caligiuri M. A. 1995; The functional characterization of interleukin-10 receptor expression on human natural killer cells. Blood 85:3577–3585[PubMed]
    [Google Scholar]
  15. Cassatella M. A., Meda L., Bonora S., Ceska M., Constantin G. 1993; Interleukin 10 (IL-10) inhibits the release of proinflammatory cytokines from human polymorphonuclear leukocytes. Evidence for an autocrine role of tumor necrosis factor and IL-1 beta in mediating the production of IL-8 triggered by lipopolysaccharide. J Exp Med 178:2207–2211 [View Article][PubMed]
    [Google Scholar]
  16. Chan A., Baird M., Mercer A. A., Fleming S. B. 2006; Maturation and function of human dendritic cells are inhibited by orf virus-encoded interleukin-10. J Gen Virol 87:3177–3181 [View Article][PubMed]
    [Google Scholar]
  17. Chang W. L., Barry P. A. 2010; Attenuation of innate immunity by cytomegalovirus IL-10 establishes a long-term deficit of adaptive antiviral immunity. Proc Natl Acad Sci U S A 107:22647–22652 [View Article][PubMed]
    [Google Scholar]
  18. Chang W. L. W., Baumgarth N., Yu D., Barry P. A. 2004; Human cytomegalovirus-encoded interleukin-10 homolog inhibits maturation of dendritic cells and alters their functionality. J Virol 78:8720–8731 [View Article][PubMed]
    [Google Scholar]
  19. Chang W. L., Barry P. A., Szubin R., Wang D., Baumgarth N. 2009; Human cytomegalovirus suppresses type I interferon secretion by plasmacytoid dendritic cells through its interleukin 10 homolog. Virology 390:330–337 [View Article][PubMed]
    [Google Scholar]
  20. Cheeran M. C. J., Hu S., Sheng W. S., Peterson P. K., Lokensgard J. R. 2003; CXCL10 production from cytomegalovirus-stimulated microglia is regulated by both human and viral interleukin-10. J Virol 77:4502–4515 [View Article][PubMed]
    [Google Scholar]
  21. Cheung A. K., Gottlieb D. J., Plachter B., Pepperl-Klindworth S., Avdic S., Cunningham A. L., Abendroth A., Slobedman B. 2009; The role of the human cytomegalovirus UL111A gene in down-regulating CD4+ T-cell recognition of latently infected cells: implications for virus elimination during latency. Blood 114:4128–4137 [View Article][PubMed]
    [Google Scholar]
  22. Couper K. N., Blount D. G., Riley E. M. 2008; IL-10: the master regulator of immunity to infection. J Immunol 180:5771–5777[PubMed] [CrossRef]
    [Google Scholar]
  23. D’Andrea A., Aste-Amezaga M., Valiante N. M., Ma X., Kubin M., Trinchieri G. 1993; Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 178:1041–1048 [View Article][PubMed]
    [Google Scholar]
  24. Davison A., Holton M., Dolan A., Dargan D., Gatherer D., Hayward G. 2013; Comparative genomics of primate cytomegaloviruses. In Cytomegaloviruses: From Molecular Pathogenesis to Intervention pp. 1–22 Edited by Reddehase J. M. Norwich: Caister Academic Press/Horizon Scientific Press;
    [Google Scholar]
  25. de Lemos Rieper C., Galle P., Pedersen B. K., Hansen M. B. 2011; Characterization of specific antibodies against cytomegalovirus (CMV)-encoded interleukin 10 produced by 28% of CMV-seropositive blood donors. J Gen Virol 92:1508–1518 [View Article][PubMed]
    [Google Scholar]
  26. de Waal Malefyt R., Abrams J., Bennett B., Figdor C. G., de Vries J. E. 1991a; Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 174:1209–1220 [View Article][PubMed]
    [Google Scholar]
  27. de Waal Malefyt R., Haanen J., Spits H., Roncarolo M. G., te Velde A., Figdor C., Johnson K., Kastelein R., Yssel H., de Vries J. E. 1991b; Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med 174:915–924 [View Article][PubMed]
    [Google Scholar]
  28. Defrance T., Vanbervliet B., Brière F., Durand I., Rousset F., Banchereau J. 1992; Interleukin 10 and transforming growth factor beta cooperate to induce anti-CD40-activated naive human B cells to secrete immunoglobulin A. J Exp Med 175:671–682 [View Article][PubMed]
    [Google Scholar]
  29. Del Prete G., De Carli M., Almerigogna F., Giudizi M. G., Biagiotti R., Romagnani S. 1993; Human IL-10 is produced by both type 1 helper (Th1) and type 2 helper (Th2) T cell clones and inhibits their antigen-specific proliferation and cytokine production. J Immunol 150:353–360[PubMed]
    [Google Scholar]
  30. Delhon G., Tulman E. R., Afonso C. L., Lu Z., de la Concha-Bermejillo A., Lehmkuhl H. D., Piccone M. E., Kutish G. F., Rock D. L. 2004; Genomes of the parapoxviruses orf virus and bovine papular stomatitis virus. J Virol 78:168–177 [View Article][PubMed]
    [Google Scholar]
  31. Demangel C., Bertolino P., Britton W. J. 2002; Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. Eur J Immunol 32:994–1002 [View Article][PubMed]
    [Google Scholar]
  32. Díaz-San Segundo F., Rodríguez-Calvo T., de Avila A., Sevilla N. 2009; Immunosuppression during acute infection with foot-and-mouth disease virus in swine is mediated by IL-10. PLoS ONE 4:e5659 [View Article][PubMed]
    [Google Scholar]
  33. Ding Y., Qin L., Kotenko S. V., Pestka S., Bromberg J. S. 2000; A single amino acid determines the immunostimulatory activity of interleukin 10. J Exp Med 191:213–224 [View Article][PubMed]
    [Google Scholar]
  34. Ding Y., Qin L., Zamarin D., Kotenko S. V., Pestka S., Moore K. W., Bromberg J. S. 2001; Differential IL-10R1 expression plays a critical role in IL-10-mediated immune regulation. J Immunol 167:6884–6892[PubMed] [CrossRef]
    [Google Scholar]
  35. Dunn W., Chou C., Li H., Hai R., Patterson D., Stolc V., Zhu H., Liu F. 2003; Functional profiling of a human cytomegalovirus genome. Proc Natl Acad Sci U S A 100:14223–14228 [View Article][PubMed]
    [Google Scholar]
  36. Eberhardt M. K., Chang W. L., Logsdon N. J., Yue Y., Walter M. R., Barry P. A. 2012; Host immune responses to a viral immune modulating protein: immunogenicity of viral interleukin-10 in rhesus cytomegalovirus-infected rhesus macaques. PLoS ONE 7:e37931 [View Article][PubMed]
    [Google Scholar]
  37. Eberhardt M. K., Deshpande A., Chang W. L., Barthold S. W., Walter M. R., Barry P. A. 2013; Vaccination against a virus-encoded cytokine significantly restricts viral challenge. J Virol 87:11323–11331 [View Article][PubMed]
    [Google Scholar]
  38. Fiorentino D. F., Bond M. W., Mosmann T. R. 1989; Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 170:2081–2095 [View Article][PubMed]
    [Google Scholar]
  39. Fiorentino D. F., Zlotnik A., Mosmann T. R., Howard M., O’Garra A. 1991; IL-10 inhibits cytokine production by activated macrophages. J Immunol 147:3815–3822[PubMed]
    [Google Scholar]
  40. Fleming S. B., McCaughan C. A., Andrews A. E., Nash A. D., Mercer A. A. 1997; A homolog of interleukin-10 is encoded by the poxvirus orf virus. J Virol 71:4857–4861[PubMed]
    [Google Scholar]
  41. Fleming S. B., Haig D. M., Nettleton P., Reid H. W., McCaughan C. A., Wise L. M., Mercer A. 2000; Sequence and functional analysis of a homolog of interleukin-10 encoded by the parapoxvirus orf virus. Virus Genes 21:85–95 [View Article][PubMed]
    [Google Scholar]
  42. Fleming S. B., Anderson I. E., Thomson J., Deane D. L., McInnes C. J., McCaughan C. A., Mercer A. A., Haig D. M. 2007; Infection with recombinant orf viruses demonstrates that the viral interleukin-10 is a virulence factor. J Gen Virol 88:1922–1927 [View Article][PubMed]
    [Google Scholar]
  43. Franken M., Devergne O., Rosenzweig M., Annis B., Kieff E., Wang F. 1996; Comparative analysis identifies conserved tumor necrosis factor receptor-associated factor 3 binding sites in the human and simian Epstein-Barr virus oncogene LMP1. J Virol 70:7819–7826[PubMed]
    [Google Scholar]
  44. Gad H. H., Dellgren C., Hamming O. J., Vends S., Paludan S. R., Hartmann R. 2009; Interferon-λ is functionally an interferon but structurally related to the interleukin-10 family. J Biol Chem 284:20869–20875 [View Article][PubMed]
    [Google Scholar]
  45. Go N. F., Castle B. E., Barrett R., Kastelein R., Dang W., Mosmann T. R., Moore K. W., Howard M. 1990; Interleukin 10, a novel B cell stimulatory factor: unresponsiveness of X chromosome-linked immunodeficiency B cells. J Exp Med 172:1625–1631 [View Article][PubMed]
    [Google Scholar]
  46. Haig D. M., Thomson J., McInnes C., McCaughan C., Imlach W., Mercer A., Fleming S. 2002a; Orf virus immuno-modulation and the host immune response. Vet Immunol Immunopathol 87:395–399 [View Article][PubMed]
    [Google Scholar]
  47. Haig D. M., Thomson J., McInnes C. J., Deane D. L., Anderson I. E., McCaughan C. A., Imlach W., Mercer A. A., Howard C. J., Fleming S. B. 2002b; A comparison of the anti-inflammatory and immuno-stimulatory activities of orf virus and ovine interleukin-10. Virus Res 90:303–316 [View Article][PubMed]
    [Google Scholar]
  48. Halary F., Amara A., Lortat-Jacob H., Messerle M., Delaunay T., Houlès C., Fieschi F., Arenzana-Seisdedos F., Moreau J. F., Déchanet-Merville J. 2002; Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans-infection. Immunity 17:653–664 [View Article][PubMed]
    [Google Scholar]
  49. Hart P. H., Hunt E. K., Bonder C. S., Watson C. J., Finlay-Jones J. J. 1996; Regulation of surface and soluble TNF receptor expression on human monocytes and synovial fluid macrophages by IL-4 and IL-10. J Immunol 157:3672–3680[PubMed]
    [Google Scholar]
  50. Hautaniemi M., Ueda N., Tuimala J., Mercer A. A., Lahdenperä J., McInnes C. J. 2010; The genome of pseudocowpoxvirus: comparison of a reindeer isolate and a reference strain. J Gen Virol 91:1560–1576 [View Article][PubMed]
    [Google Scholar]
  51. Hsu D. H., de Waal Malefyt R., Fiorentino D. F., Dang M. N., Vieira P., de Vries J., Spits H., Mosmann T. R., Moore K. W. 1990; Expression of interleukin-10 activity by Epstein-Barr virus protein BCRF1. Science 250:830–832 [View Article][PubMed]
    [Google Scholar]
  52. Hudson G. S., Bankier A. T., Satchwell S. C., Barrell B. G. 1985; The short unique region of the B95-8 Epstein-Barr virus genome. Virology 147:81–98 [View Article][PubMed]
    [Google Scholar]
  53. Hwu P., Du M. X., Lapointe R., Do M., Taylor M. W., Young H. A. 2000; Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J Immunol 164:3596–3599[PubMed] [CrossRef]
    [Google Scholar]
  54. Ilouze M., Dishon A., Kotler M. 2012; Coordinated and sequential transcription of the cyprinid herpesvirus-3 annotated genes. Virus Res 169:98–106 [View Article][PubMed]
    [Google Scholar]
  55. Imlach W., McCaughan C. A., Mercer A. A., Haig D., Fleming S. B. 2002; Orf virus-encoded interleukin-10 stimulates the proliferation of murine mast cells and inhibits cytokine synthesis in murine peritoneal macrophages. J Gen Virol 83:1049–1058[PubMed]
    [Google Scholar]
  56. Isfort R., Jones D., Kost R., Witter R., Kung H. J. 1992; Retrovirus insertion into herpesvirus in vitro and in vivo. Proc Natl Acad Sci U S A 89:991–995 [View Article][PubMed]
    [Google Scholar]
  57. Jaworowski A., Cheng W. J., Westhorpe C. L., Abendroth A., Crowe S. M., Slobedman B. 2009; Enhanced monocyte Fc phagocytosis by a homologue of interleukin-10 encoded by human cytomegalovirus. Virology 391:20–24 [View Article][PubMed]
    [Google Scholar]
  58. Jayawardane G., Russell G. C., Thomson J., Deane D., Cox H., Gatherer D., Ackermann M., Haig D. M., Stewart J. P. 2008; A captured viral interleukin 10 gene with cellular exon structure. J Gen Virol 89:2447–2455 [View Article][PubMed]
    [Google Scholar]
  59. Jenkins C., Abendroth A., Slobedman B. 2004; A novel viral transcript with homology to human interleukin-10 is expressed during latent human cytomegalovirus infection. J Virol 78:1440–1447 [View Article][PubMed]
    [Google Scholar]
  60. Jenkins C., Garcia W., Abendroth A., Slobedman B. 2008a; Expression of a human cytomegalovirus latency-associated homolog of interleukin-10 during the productive phase of infection. Virology 370:285–294 [View Article][PubMed]
    [Google Scholar]
  61. Jenkins C., Garcia W., Godwin M. J., Spencer J. V., Stern J. L., Abendroth A., Slobedman B. 2008b; Immunomodulatory properties of a viral homolog of human interleukin-10 expressed by human cytomegalovirus during the latent phase of infection. J Virol 82:3736–3750 [View Article][PubMed]
    [Google Scholar]
  62. Jenkins J. K., Malyak M., Arend W. P. 1994; The effects of interleukin-10 on interleukin-1 receptor antagonist and interleukin-1 beta production in human monocytes and neutrophils. Lymphokine Cytokine Res 13:47–54[PubMed]
    [Google Scholar]
  63. Jochum S., Moosmann A., Lang S., Hammerschmidt W., Zeidler R. 2012; The EBV immunoevasins vIL-10 and BNLF2a protect newly infected B cells from immune recognition and elimination. PLoS Pathog 8:e1002704 [View Article][PubMed]
    [Google Scholar]
  64. Jones B. C., Logsdon N. J., Josephson K., Cook J., Barry P. A., Walter M. R. 2002; Crystal structure of human cytomegalovirus IL-10 bound to soluble human IL-10R1. Proc Natl Acad Sci U S A 99:9404–9409 [View Article][PubMed]
    [Google Scholar]
  65. Josephson K., Logsdon N. J., Walter M. R. 2001; Crystal structure of the IL-10/IL-10R1 complex reveals a shared receptor binding site. Immunity 15:35–46 [View Article][PubMed]
    [Google Scholar]
  66. Keravala A., Lechman E. R., Nash J., Mi Z., Robbins P. D. 2006; Human, viral or mutant human IL-10 expressed after local adenovirus-mediated gene transfer are equally effective in ameliorating disease pathology in a rabbit knee model of antigen-induced arthritis. Arthritis Res Ther 8:R91 [View Article][PubMed]
    [Google Scholar]
  67. Kim K. N., Watanabe S., Ma Y., Thornton S., Giannini E. H., Hirsch R. 2000; Viral IL-10 and soluble TNF receptor act synergistically to inhibit collagen-induced arthritis following adenovirus-mediated gene transfer. J Immunol 164:1576–1581[PubMed] [CrossRef]
    [Google Scholar]
  68. Kotenko S. V., Pestka S. 2001). Viral IL-10 variants. In Cytokine Reference: A Compendium of Cytokines and Other Mediators of Host Defense pp. 1–13 Edited by Openheimer J. J., Feldmann M. New York: Academic Press;
    [Google Scholar]
  69. Kotenko S. V., Krause C. D., Izotova L. S., Pollack B. P., Wu W., Pestka S. 1997; Identification and functional characterization of a second chain of the interleukin-10 receptor complex. EMBO J 16:5894–5903 [View Article][PubMed]
    [Google Scholar]
  70. Kotenko S. V., Saccani S., Izotova L. S., Mirochnitchenko O. V., Pestka S. 2000; Human cytomegalovirus harbors its own unique IL-10 homolog (cmvIL-10). Proc Natl Acad Sci U S A 97:1695–1700 [View Article][PubMed]
    [Google Scholar]
  71. Lateef Z., Fleming S., Halliday G., Faulkner L., Mercer A., Baird M. 2003; Orf virus-encoded interleukin-10 inhibits maturation, antigen presentation and migration of murine dendritic cells. J Gen Virol 84:1101–1109 [View Article][PubMed]
    [Google Scholar]
  72. Lechman E. R., Jaffurs D., Ghivizzani S. C., Gambotto A., Kovesdi I., Mi Z., Evans C. H., Robbins P. D. 1999; Direct adenoviral gene transfer of viral IL-10 to rabbit knees with experimental arthritis ameliorates disease in both injected and contralateral control knees. J Immunol 163:2202–2208[PubMed]
    [Google Scholar]
  73. Lee H. J., Essani K., Smith G. L. 2001; The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 281:170–192 [View Article][PubMed]
    [Google Scholar]
  74. Lin Y. L., Chang P. C., Wang Y., Li M. 2008; Identification of novel viral interleukin-10 isoforms of human cytomegalovirus AD169. Virus Res 131:213–223 [View Article][PubMed]
    [Google Scholar]
  75. Liu Y., Wei S. H., Ho A. S., de Waal Malefyt R., Moore K. W. 1994; Expression cloning and characterization of a human IL-10 receptor. J Immunol 152:1821–1829[PubMed]
    [Google Scholar]
  76. Liu Y., de Waal Malefyt R., Briere F., Parham C., Bridon J. M., Banchereau J., Moore K. W., Xu J. 1997; The EBV IL-10 homologue is a selective agonist with impaired binding to the IL-10 receptor. J Immunol 158:604–613[PubMed]
    [Google Scholar]
  77. Lockridge K. M., Zhou S. S., Kravitz R. H., Johnson J. L., Sawai E. T., Blewett E. L., Barry P. A. 2000; Primate cytomegaloviruses encode and express an IL-10-like protein. Virology 268:272–280 [View Article][PubMed]
    [Google Scholar]
  78. Logsdon N. J., Eberhardt M. K., Allen C. E., Barry P. A., Walter M. R. 2011; Design and analysis of rhesus cytomegalovirus IL-10 mutants as a model for novel vaccines against human cytomegalovirus. PLoS ONE 6:e28127 [View Article][PubMed]
    [Google Scholar]
  79. Ma Y., Thornton S., Duwel L. E., Boivin G. P., Giannini E. H., Leiden J. M., Bluestone J. A., Hirsch R. 1998; Inhibition of collagen-induced arthritis in mice by viral IL-10 gene transfer. J Immunol 161:1516–1524[PubMed]
    [Google Scholar]
  80. Matsuda M., Salazar F., Petersson M., Masucci G., Hansson J., Pisa P., Zhang Q. J., Masucci M. G., Kiessling R. 1994; Interleukin 10 pretreatment protects target cells from tumor- and allo-specific cytotoxic T cells and downregulates HLA class I expression. J Exp Med 180:2371–2376 [View Article][PubMed]
    [Google Scholar]
  81. Meier-Trummer C. S., Tobler K., Hilbe M., Stewart J. P., Hart J., Campbell I., Haig D. M., Glauser D. L., Ehrensperger F., Ackermann M. 2009; Ovine herpesvirus 2 structural proteins in epithelial cells and M-cells of the appendix in rabbits with malignant catarrhal fever. Vet Microbiol 137:235–242 [View Article][PubMed]
    [Google Scholar]
  82. Miyazaki I., Cheung R. K., Dosch H. M. 1993; Viral interleukin 10 is critical for the induction of B cell growth transformation by Epstein-Barr virus. J Exp Med 178:439–447 [View Article][PubMed]
    [Google Scholar]
  83. Moore K. W., Vieira P., Fiorentino D. F., Trounstine M. L., Khan T. A., Mosmann T. R. 1990; Homology of cytokine synthesis inhibitory factor (IL-10) to the Epstein-Barr virus gene BCRFI. Science 248:1230–1234 [View Article][PubMed]
    [Google Scholar]
  84. Moore K. W., O’Garra A., de Waal Malefyt R., Vieira P., Mosmann T. R. 1993; Interleukin-10. Annu Rev Immunol 11:165–190 [View Article][PubMed]
    [Google Scholar]
  85. Moore K. W., de Waal Malefyt R., Coffman R. L., O’Garra A. 2001; Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683–765 [View Article][PubMed]
    [Google Scholar]
  86. Mosser D. M., Zhang X. 2008; Interleukin-10: new perspectives on an old cytokine. Immunol Rev 226:205–218 [View Article][PubMed]
    [Google Scholar]
  87. Nachtwey J., Spencer J. V. 2008; HCMV IL-10 suppresses cytokine expression in monocytes through inhibition of nuclear factor-kappaB. Viral Immunol 21:477–482 [View Article][PubMed]
    [Google Scholar]
  88. Nast C. C., Moudgil A., Zuo X. J., Toyoda M., Jordan S. C. 1997; Long-term allograft acceptance in a patient with posttransplant lymphoproliferative disorder: correlation with intragraft viral interleukin-10. Transplantation 64:1578–1582 [View Article][PubMed]
    [Google Scholar]
  89. Niiro H., Otsuka T., Abe M., Satoh H., Ogo T., Nakano T., Furukawa Y., Niho Y. 1992; Epstein-Barr virus BCRF1 gene product (viral interleukin 10) inhibits superoxide anion production by human monocytes. Lymphokine Cytokine Res 11:209–214[PubMed]
    [Google Scholar]
  90. Niiro H., Otsuka T., Kuga S., Nemoto Y., Abe M., Hara N., Nakano T., Ogo T., Niho Y. 1994; IL-10 inhibits prostaglandin E2 production by lipopolysaccharide-stimulated monocytes. Int Immunol 6:661–664 [View Article][PubMed]
    [Google Scholar]
  91. Odom M. R., Hendrickson R. C., Lefkowitz E. J. 2009; Poxvirus protein evolution: family wide assessment of possible horizontal gene transfer events. Virus Res 144:233–249 [View Article][PubMed]
    [Google Scholar]
  92. Ouyang W., Rutz S., Crellin N. K., Valdez P. A., Hymowitz S. G. 2011; Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 29:71–109 [View Article][PubMed]
    [Google Scholar]
  93. Ouyang P., Rakus K., Boutier M., Reschner A., Leroy B., Ronsmans M., Fournier G., Scohy S., Costes B. other authors 2013; The IL-10 homologue encoded by cyprinid herpesvirus 3 is essential neither for viral replication in vitro nor for virulence in vivo. Vet Res 44:53 [View Article][PubMed]
    [Google Scholar]
  94. Pepperl-Klindworth S., Besold K., Frankenberg N., Farkas M., Kuball J., Theobald M., Plachter B. 2006; Cytomegalovirus interleukin-10 expression in infected cells does not impair MHC class I restricted peptide presentation on bystanding antigen-presenting cells. Viral Immunol 19:92–101 [View Article][PubMed]
    [Google Scholar]
  95. Pestka S., Krause C. D., Sarkar D., Walter M. R., Shi Y., Fisher P. B. 2004; Interleukin-10 and related cytokines and receptors. Annu Rev Immunol 22:929–979 [View Article][PubMed]
    [Google Scholar]
  96. Pinto R. D., Nascimento D. S., Reis M. I., do Vale A., Dos Santos N. M. 2007; Molecular characterization, 3D modelling and expression analysis of sea bass (Dicentrarchus labrax L.) interleukin-10. Mol Immunol 44:2056–2065 [View Article][PubMed]
    [Google Scholar]
  97. Qin L., Chavin K. D., Ding Y., Tahara H., Favaro J. P., Woodward J. E., Suzuki T., Robbins P. D., Lotze M. T., Bromberg J. S. 1996; Retrovirus-mediated transfer of viral IL-10 gene prolongs murine cardiac allograft survival. J Immunol 156:2316–2323[PubMed]
    [Google Scholar]
  98. Raftery M. J., Wieland D., Gronewald S., Kraus A. A., Giese T., Schönrich G. 2004; Shaping phenotype, function, and survival of dendritic cells by cytomegalovirus-encoded IL-10. J Immunol 173:3383–3391[PubMed] [CrossRef]
    [Google Scholar]
  99. Raftery M. J., Hitzler M., Winau F., Giese T., Plachter B., Kaufmann S. H. E., Schönrich G. 2008; Inhibition of CD1 antigen presentation by human cytomegalovirus. J Virol 82:4308–4319 [View Article][PubMed]
    [Google Scholar]
  100. Rouas-Freiss N., Gonçalves R. M. B., Menier C., Dausset J., Carosella E. D. 1997; Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci U S A 94:11520–11525 [View Article][PubMed]
    [Google Scholar]
  101. Rousset F., Garcia E., Defrance T., Péronne C., Vezzio N., Hsu D. H., Kastelein R., Moore K. W., Banchereau J. 1992; Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci U S A 89:1890–1893 [View Article][PubMed]
    [Google Scholar]
  102. Rowbottom A. W., Lepper M. W., Garland R. J., Cox C. V., Corley E. G., Oakhill A., Steward C. G. 1999; Interleukin-10-induced CD8 cell proliferation. Immunology 98:80–89 [View Article][PubMed]
    [Google Scholar]
  103. Sabat R. 2010; IL-10 family of cytokines. Cytokine Growth Factor Rev 21:315–324 [View Article][PubMed]
    [Google Scholar]
  104. Sabat R., Grütz G., Warszawska K., Kirsch S., Witte E., Wolk K., Geginat J. 2010; Biology of interleukin-10. Cytokine Growth Factor Rev 21:331–344 [View Article][PubMed]
    [Google Scholar]
  105. Salek-Ardakani S., Arrand J. R., Mackett M. 2002a; Epstein-Barr virus encoded interleukin-10 inhibits HLA-class I, ICAM-1, and B7 expression on human monocytes: implications for immune evasion by EBV. Virology 304:342–351 [View Article][PubMed]
    [Google Scholar]
  106. Salek-Ardakani S., Stuart A. D., Arrand J. E., Lyons S., Arrand J. R., Mackett M. 2002b; High level expression and purification of the Epstein-Barr virus encoded cytokine viral interleukin 10: efficient removal of endotoxin. Cytokine 17:1–13 [View Article][PubMed]
    [Google Scholar]
  107. Santin A. D., Hermonat P. L., Ravaggi A., Bellone S., Pecorelli S., Roman J. J., Parham G. P., Cannon M. J. 2000; Interleukin-10 increases Th1 cytokine production and cytotoxic potential in human papillomavirus-specific CD8+ cytotoxic T lymphocytes. J Virol 74:4729–4737 [View Article][PubMed]
    [Google Scholar]
  108. Shackelton L. A., Holmes E. C. 2004; The evolution of large DNA viruses: combining genomic information of viruses and their hosts. Trends Microbiol 12:458–465 [View Article][PubMed]
    [Google Scholar]
  109. Slobedman B., Barry P. A., Spencer J. V., Avdic S., Abendroth A. 2009; Virus-encoded homologs of cellular interleukin-10 and their control of host immune function. J Virol 83:9618–9629 [View Article][PubMed]
    [Google Scholar]
  110. Spencer J. V. 2007; The cytomegalovirus homolog of interleukin-10 requires phosphatidylinositol 3-kinase activity for inhibition of cytokine synthesis in monocytes. J Virol 81:2083–2086 [View Article][PubMed]
    [Google Scholar]
  111. Spencer J. V., Lockridge K. M., Barry P. A., Lin G., Tsang M., Penfold M. E. T., Schall T. J. 2002; Potent immunosuppressive activities of cytomegalovirus-encoded interleukin-10. J Virol 76:1285–1292 [View Article][PubMed]
    [Google Scholar]
  112. Spencer J. V., Cadaoas J., Castillo P. R., Saini V., Slobedman B. 2008; Stimulation of B lymphocytes by cmvIL-10 but not LAcmvIL-10. Virology 374:164–169 [View Article][PubMed]
    [Google Scholar]
  113. Stuart A. D., Stewart J. P., Arrand J. R., Mackett M. 1995; The Epstein-Barr virus encoded cytokine viral interleukin-10 enhances transformation of human B lymphocytes. Oncogene 11:1711–1719[PubMed]
    [Google Scholar]
  114. Sunarto A., Liongue C., McColl K. A., Adams M. M., Bulach D., Crane M. S. J., Schat K. A., Slobedman B., Barnes A. C. other authors 2012; Koi herpesvirus encodes and expresses a functional interleukin-10. J Virol 86:11512–11520 [View Article][PubMed]
    [Google Scholar]
  115. Takanaski S., Nonaka R., Xing Z., O’Byrne P., Dolovich J., Jordana M. 1994; Interleukin 10 inhibits lipopolysaccharide-induced survival and cytokine production by human peripheral blood eosinophils. J Exp Med 180:711–715 [View Article][PubMed]
    [Google Scholar]
  116. Telford E. A. R., Watson M. S., Aird H. C., Perry J., Davison A. J. 1995; The DNA sequence of equine herpesvirus 2. J Mol Biol 249:520–528 [View Article][PubMed]
    [Google Scholar]
  117. Thompson-Snipes L., Dhar V., Bond M. W., Mosmann T. R., Moore K. W., Rennick D. M. 1991; Interleukin 10: a novel stimulatory factor for mast cells and their progenitors. J Exp Med 173:507–510 [View Article][PubMed]
    [Google Scholar]
  118. Touitou R., Cochet C., Joab I. 1996; Transcriptional analysis of the Epstein-Barr virus interleukin-10 homologue during the lytic cycle. J Gen Virol 77:1163–1168 [View Article][PubMed]
    [Google Scholar]
  119. Tulman E. R., Afonso C. L., Lu Z., Zsak L., Kutish G. F., Rock D. L. 2001; Genome of lumpy skin disease virus. J Virol 75:7122–7130 [View Article][PubMed]
    [Google Scholar]
  120. Tulman E. R., Afonso C. L., Lu Z., Zsak L., Sur J. H., Sandybaev N. T., Kerembekova U. Z., Zaitsev V. L., Kutish G. F., Rock D. L. 2002; The genomes of sheeppox and goatpox viruses. J Virol 76:6054–6061 [View Article][PubMed]
    [Google Scholar]
  121. Tulman E. R., Afonso C. L., Lu Z., Zsak L., Kutish G. F., Rock D. L. 2004; The genome of canarypox virus. J Virol 78:353–366 [View Article][PubMed]
    [Google Scholar]
  122. van Beurden S. J., Bossers A., Voorbergen-Laarman M. H., Haenen O. L., Peters S., Abma-Henkens M. H., Peeters B. P., Rottier P. J., Engelsma M. Y. 2010; Complete genome sequence and taxonomic position of anguillid herpesvirus 1. J Gen Virol 91:880–887 [View Article][PubMed]
    [Google Scholar]
  123. van Beurden S. J., Forlenza M., Westphal A. H., Wiegertjes G. F., Haenen O. L., Engelsma M. Y. 2011; The alloherpesviral counterparts of interleukin 10 in European eel and common carp. Fish Shellfish Immunol 31:1211–1217 [View Article][PubMed]
    [Google Scholar]
  124. van Beurden S. J., Peeters B. P. H., Rottier P. J. M., Davison A. J., Engelsma M. Y. 2013; Genome-wide gene expression analysis of anguillid herpesvirus 1. BMC Genomics 14:83 [View Article][PubMed]
    [Google Scholar]
  125. van Putten S. M., Wübben M., Hennink W. E., van Luyn M. J., Harmsen M. C. 2009; The downmodulation of the foreign body reaction by cytomegalovirus encoded interleukin-10. Biomaterials 30:730–735 [View Article][PubMed]
    [Google Scholar]
  126. Vieira P., de Waal-Malefyt R., Dang M. N., Johnson K. E., Kastelein R., Fiorentino D. F., deVries J. E., Roncarolo M. G., Mosmann T. R., Moore K. W. 1991; Isolation and expression of human cytokine synthesis inhibitory factor cDNA clones: homology to Epstein-Barr virus open reading frame BCRFI. Proc Natl Acad Sci U S A 88:1172–1176 [View Article][PubMed]
    [Google Scholar]
  127. Walter M. R., Nagabhushan T. L. 1995; Crystal structure of interleukin 10 reveals an interferon gamma-like fold. Biochemistry 34:12118–12125 [View Article][PubMed]
    [Google Scholar]
  128. Whalen J. D., Lechman E. L., Carlos C. A., Weiss K., Kovesdi I., Glorioso J. C., Robbins P. D., Evans C. H. 1999; Adenoviral transfer of the viral IL-10 gene periarticularly to mouse paws suppresses development of collagen-induced arthritis in both injected and uninjected paws. J Immunol 162:3625–3632[PubMed]
    [Google Scholar]
  129. Willems F., Marchant A., Delville J. P., Gérard C., Delvaux A., Velu T., de Boer M., Goldman M. 1994; Interleukin-10 inhibits B7 and intercellular adhesion molecule-1 expression on human monocytes. Eur J Immunol 24:1007–1009 [View Article][PubMed]
    [Google Scholar]
  130. Wise L., McCaughan C., Tan C. K., Mercer A. A., Fleming S. B. 2007; Orf virus interleukin-10 inhibits cytokine synthesis in activated human THP-1 monocytes, but only partially impairs their proliferation. J Gen Virol 88:1677–1682 [View Article][PubMed]
    [Google Scholar]
  131. Wolk K., Witte E., Reineke U., Witte K., Friedrich M., Sterry W., Asadullah K., Volk H. D., Sabat R. 2005; Is there an interaction between interleukin-10 and interleukin-22?. Genes Immun 6:8–18[PubMed] [CrossRef]
    [Google Scholar]
  132. Xu Z. G., Iwatsuki K., Oyama N., Ohtsuka M., Satoh M., Kikuchi S., Akiba H., Kaneko F. 2001; The latency pattern of Epstein-Barr virus infection and viral IL-10 expression in cutaneous natural killer/T-cell lymphomas. Br J Cancer 84:920–925 [View Article][PubMed]
    [Google Scholar]
  133. Yamamoto-Tabata T., McDonagh S., Chang H. T., Fisher S., Pereira L. 2004; Human cytomegalovirus interleukin-10 downregulates metalloproteinase activity and impairs endothelial cell migration and placental cytotrophoblast invasiveness in vitro. J Virol 78:2831–2840 [View Article][PubMed]
    [Google Scholar]
  134. Yoon S. I., Jones B. C., Logsdon N. J., Walter M. R. 2005; Same structure, different function crystal structure of the Epstein-Barr virus IL-10 bound to the soluble IL-10R1 chain. Structure 13:551–564 [View Article][PubMed]
    [Google Scholar]
  135. Yoon S. I., Logsdon N. J., Sheikh F., Donnelly R. P., Walter M. R. 2006; Conformational changes mediate interleukin-10 receptor 2 (IL-10R2) binding to IL-10 and assembly of the signaling complex. J Biol Chem 281:35088–35096 [View Article][PubMed]
    [Google Scholar]
  136. Yu X. L., Cheng Y. M., Shi B. S., Qian F. X., Wang F. B., Liu X. N., Yang H. Y., Xu Q. N., Qi T. K. other authors 2008; Measles virus infection in adults induces production of IL-10 and is associated with increased CD4+ CD25+ regulatory T cells. J Immunol 181:7356–7366[PubMed] [CrossRef]
    [Google Scholar]
  137. Yue Y., Barry P. A. 2008; Rhesus cytomegalovirus: a nonhuman primate model for the study of human cytomegalovirus. Adv Virus Res 72:207–226 [View Article][PubMed]
    [Google Scholar]
  138. Zdanov A. 2004; Structural features of the interleukin-10 family of cytokines. Curr Pharm Des 10:3873–3884 [View Article][PubMed]
    [Google Scholar]
  139. Zdanov A., Schalk-Hihi C., Gustchina A., Tsang M., Weatherbee J., Wlodawer A. 1995; Crystal structure of interleukin-10 reveals the functional dimer with an unexpected topological similarity to interferon gamma. Structure 3:591–601 [View Article][PubMed]
    [Google Scholar]
  140. Zdanov A., Schalk-Hihi C., Wlodawer A. 1996; Crystal structure of human interleukin-10 at 1.6 A resolution and a model of a complex with its soluble receptor. Protein Sci 5:1955–1962 [View Article][PubMed]
    [Google Scholar]
  141. Zdanov A., Schalk-Hihi C., Menon S., Moore K. W., Wlodawer A. 1997; Crystal structure of Epstein-Barr virus protein BCRF1, a homolog of cellular interleukin-10. J Mol Biol 268:460–467 [View Article][PubMed]
    [Google Scholar]
  142. Zhang D. C., Shao Y. Q., Huang Y. Q., Jiang S. G. 2005; Cloning, characterization and expression analysis of interleukin-10 from the zebrafish (Danio rerion). J Biochem Mol Biol 38:571–576 [View Article][PubMed]
    [Google Scholar]
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