1887

Abstract

Interference with dendritic cell (DC) maturation and function is considered to be central to measles virus (MV)-induced immunosuppression. Temporally ordered production of chemokines and switches in chemokine receptor expression are essential for pathogen-driven DC maturation as they are prerequisites for chemotaxis and T cell recruitment. We found that MV infection of immature monocyte-derived DCs induced transcripts specific for CCL-1, -2, -3, -5, -17 and -22, CXCL-10 and CXCL-11, yet did not induce CXCL-8 (interleukin-8) and CCL-20 at the mRNA and protein level. Within 24 h post-infection, T cell attraction was not detectably impaired by these cells. MV infection failed to promote the switch from CCR5 to CCR7 expression and this correlated with chemotactic responses of MV-matured DC cultures to CCL-3 rather than to CCL-19. Moreover, the chemotaxis of MV-infected DCs to either chemokine was compromised, indicating that MV also interferes with this property independently of chemokine receptor modulation.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.008581-0
2009-04-01
2020-09-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/4/909.html?itemId=/content/journal/jgv/10.1099/vir.0.008581-0&mimeType=html&fmt=ahah

References

  1. Ardeshna K. M., Pizzey A. R., Walker S. J., Devereux S., Khwaja A. 2002; The upregulation of CC chemokine receptor 7 and the increased migration of maturing dendritic cells to macrophage inflammatory protein 3 β and secondary lymphoid chemokine is mediated by the p38 stress-activated protein kinase pathway. Br J Haematol 119:826–829 [CrossRef]
    [Google Scholar]
  2. Bieback K., Lien E., Klagge I. M., Avota E., Schneider-Schaulies J., Duprex W. P., Wagner H., Kirschning C. J., ter Meulen V., Schneider-Schaulies S. 2002; Hemagglutinin protein of wild-type measles virus activates toll-like receptor 2 signaling. J Virol 76:8729–8736 [CrossRef]
    [Google Scholar]
  3. Brown D. D., Rima B. K., Allen I. V., Baron M. D., Banyard A. C., Barrett T., Duprex W. P. 2005; Rational attenuation of a morbillivirus by modulating the activity of the RNA-dependent RNA polymerase. J Virol 79:14330–14338 [CrossRef]
    [Google Scholar]
  4. Caparrós, E., Munoz, P., Sierra-Filardi, E., Serrano-Gómez, D., Puig-Kröger, A., Rodríguez-Fernández, J. L., Mellado, M., Sancho, J., Zubiaur, M. & Corbí, A. L. 2006; DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 107:3950–3958 [CrossRef]
    [Google Scholar]
  5. Caux C., Vanbervliet B., Massacrier C., Ait-Yahia S., Vaure C., Chemin K., Dieu-Nosjean And M. C., Vicari A. 2002; Regulation of dendritic cell recruitment by chemokines. Transplantation 73:S7–S11 [CrossRef]
    [Google Scholar]
  6. Condack C., Grivel J. C., Devaux P., Margolis L., Cattaneo R. 2007; Measles virus vaccine attenuation: suboptimal infection of lymphatic tissue and tropism alteration. J Infect Dis 196:541–549 [CrossRef]
    [Google Scholar]
  7. D'Amico G., Frascaroli G., Bianchi G., Transidico P., Doni A., Vecchi A., Sozzani S., Allavena P., Mantovani A. 2000; Uncoupling of inflammatory chemokine receptors by IL-10: generation of functional decoys. Nat Immunol 1:387–391 [CrossRef]
    [Google Scholar]
  8. de Swart R. L., Ludlow M., de Witte L., Yanagi, Y., van Amerongen G., McQuaid S., Yüksel S., Geijtenbeek T. B., Duprex W. P., Osterhaus A. D. 2007; Predominant infection of CD150(+) lymphocytes and dendritic cells during measles virus infection of Macaques. PLoS Pathog 3:e178 [CrossRef]
    [Google Scholar]
  9. de Witte, Abt M., Schneider-Schaulies S., van Kooyk Y., Geijtenbeek T. B. 2006; Measles virus targets DC-SIGN to enhance dendritic cell infection. J Virol 80:3477–3486 [CrossRef]
    [Google Scholar]
  10. Dittmar S., Harms H., Runkler N., Maisner A., Kim K. S., Schneider-Schaulies J. 2008; Measles virus-induced block of transendothelial migration of T lymphocytes and infection-mediated virus spread across endothelial cell barriers. J Virol 82:11273–11282 [CrossRef]
    [Google Scholar]
  11. Dubois B., Lamy P. J., Chemin K., Lachaux A., Kaiserlian D. 2001; Measles virus exploits dendritic cells to suppress CD4+ T-cell proliferation via expression of surface viral glycoproteins independently of T-cell trans-infection. Cell Immunol 214:173–183 [CrossRef]
    [Google Scholar]
  12. Fugier-Vivier I., Servet-Delprat C., Rivailler P., Rissoan M., Liu Y. J., Rabourdin-Combe C. 1997; Measles virus suppresses cell-mediated immunity by interfering with the survival and functions of dendritic and T cells. J Exp Med 186:813–823 [CrossRef]
    [Google Scholar]
  13. Geissmann F., Dieu-Nosjean M. C., Dezutter C., Valladeau J., Kayal S., Leborgne M., Brousse N., Saeland S., Davoust J. 2002; Accumulation of immature Langerhans cells in human lymph nodes draining chronically inflamed skin. J Exp Med 196:417–430 [CrossRef]
    [Google Scholar]
  14. Griffin D. E., Ward B. J., Esolen L. M. 1994; Pathogenesis of measles virus infection: an hypothesis for altered immune responses. J Infect Dis 170:S24–S31 [CrossRef]
    [Google Scholar]
  15. Gringhuis S. I., den Dunnen J., Litjens M., van Het Hof B., van Kooyk Y., Geijtenbeek T. B. 2007; C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF- κ B. Immunity 26:605–616 [CrossRef]
    [Google Scholar]
  16. Grosjean I., Caux C., Bella C., Berger I., Wild F., Banchereau J., Kaiserlian D. 1997; Measles virus infects human dendritic cells and blocks their allostimulatory properties for CD4+ T cells. J Exp Med 186:801–812 [CrossRef]
    [Google Scholar]
  17. Hegde S., Pahne J., Smola-Hess S. 2004; Novel immunosuppressive properties of interleukin-6 in dendritic cells: inhibition of NF- κ B binding activity and CCR7 expression. FASEB J 18:1439–1441
    [Google Scholar]
  18. Hodges A., Sharrocks K., Edelmann M., Baban D., Moris A., Schwartz O., Drakesmith H., Davies K., Kessler B. other authors 2007; Activation of the lectin DC-SIGN induces an immature dendritic cell phenotype triggering Rho-GTPase activity required for HIV-1 replication. Nat Immunol 8:569–577 [CrossRef]
    [Google Scholar]
  19. Hopken U. E., Foss H. D., Meyer D., Hinz M., Leder K., Stein H., Lipp M. 2002; Up-regulation of the chemokine receptor CCR7 in classical but not in lymphocyte-predominant Hodgkin disease correlates with distinct dissemination of neoplastic cells in lymphoid organs. Blood 99:1109–1116 [CrossRef]
    [Google Scholar]
  20. Humrich J. Y., Thumann P., Greiner S., Humrich J. H., Averbeck M., Schwank C., Kämpgen E., Schuler G., Jenne L. 2007; Vaccinia virus impairs directional migration and chemokine receptor switch of human dendritic cells. Eur J Immunol 37:954–965 [CrossRef]
    [Google Scholar]
  21. Kaiserlian D., Grosjean I., Caux C. 1997; Infection of human dendritic cells by measles virus induces immune suppression. Adv Exp Med Biol 417:421–423
    [Google Scholar]
  22. Kerdiles Y. M., Sellin C. I., Druelle J., Horvat B. 2006; Immunosuppression caused by measles virus: role of viral proteins. Rev Med Virol 16:49–63 [CrossRef]
    [Google Scholar]
  23. Klagge I. M., ter Meulen V., Schneider-Schaulies S. 2000; Measles virus-induced promotion of dendritic cell maturation by soluble mediators does not overcome the immunosuppressive activity of viral glycoproteins on the cell surface. Eur J Immunol 30:2741–2750 [CrossRef]
    [Google Scholar]
  24. Klagge I. M., Abt M., Fries B., Schneider-Schaulies S. 2004; Impact of measles virus dendritic-cell infection on Th-cell polarization in vitro . J Gen Virol 85:3239–3247 [CrossRef]
    [Google Scholar]
  25. Lammermann T., Bader B. L., Monkley S. J., Worbs T., Wedlich-Soldner R., Hirsch K., Keller M., Forster R., Critchley D. R. other authors 2008; Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453:51–55 [CrossRef]
    [Google Scholar]
  26. Mathas S., Hinz M., Anagnostopoulos I., Krappmann D., Lietz A., Jundt F., Bommert K., Mechta-Grigoriou F., Stein H. other authors 2002; Aberrantly expressed c-Jun and JunB are a hallmark of Hodgkin lymphoma cells, stimulate proliferation and synergize with NF- κ B. EMBO J 21:4104–4113 [CrossRef]
    [Google Scholar]
  27. Minagawa H., Tanaka K., Ono N., Tatsuo H., Yanagi Y. 2001; Induction of the measles virus receptor SLAM (CD150) on monocytes. J Gen Virol 82:2913–2917
    [Google Scholar]
  28. Moutaftsi M., Brennan P., Spector S. A., Tabi Z. 2004; Impaired lymphoid chemokine-mediated migration due to a block on the chemokine receptor switch in human cytomegalovirus-infected dendritic cells. J Virol 78:3046–3054 [CrossRef]
    [Google Scholar]
  29. Muller N., Avota E., Schneider-Schaulies J., Harms H., Krohne G., Schneider-Schaulies S. 2006; Measles virus contact with T cells impedes cytoskeletal remodeling associated with spreading, polarization, and CD3 clustering. Traffic 7:849–858 [CrossRef]
    [Google Scholar]
  30. Ohl L., Mohaupt M., Czeloth N., Hintzen G., Kiafard Z., Zwirner J., Blankenstein T., Henning G., Forster R. 2004; CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21:279–288 [CrossRef]
    [Google Scholar]
  31. Padovan E., Spagnoli G. C., Ferrantini M., Heberer M. 2002; IFN- α 2a induces IP-10/CXCL10 and MIG/CXCL9 production in monocyte-derived dendritic cells and enhances their capacity to attract and stimulate CD8+ effector T cells. J Leukoc Biol 71:669–676
    [Google Scholar]
  32. Piccioli D., Tavarini S., Borgogni E., Steri V., Nuti S., Sammicheli C., Bardelli M., Montagna D., Locatelli F., Wack A. 2007; Functional specialization of human circulating CD16 and CD1c myeloid dendritic-cell subsets. Blood 109:5371–5379 [CrossRef]
    [Google Scholar]
  33. Piqueras B., Connolly J., Freitas H., Palucka A. K., Banchereau J. 2006; Upon viral exposure, myeloid and plasmacytoid dendritic cells produce 3 waves of distinct chemokines to recruit immune effectors. Blood 107:2613–2618 [CrossRef]
    [Google Scholar]
  34. Pollara G., Kwan A., Newton P. J., Handley M. E., Chain B. M., Katz D. R. 2005; Dendritic cells in viral pathogenesis: protective or defective?. Int J Exp Pathol 86:187–204 [CrossRef]
    [Google Scholar]
  35. Prechtel A. T., Turza N. M., Kobelt D. J., Eisemann J. I., Coffin R. S., McGrath Y., Hacker C., Ju X., Zenke M., Steinkasserer A. 2005; Infection of mature dendritic cells with herpes simplex virus type 1 dramatically reduces lymphoid chemokine-mediated migration. J Gen Virol 86:1645–1657 [CrossRef]
    [Google Scholar]
  36. Real E., Kaiser A., Raposo G., Amara A., Nardin A., Trautmann A., Donnadieu E. 2004; Immature dendritic cells (DCs) use chemokines and intercellular adhesion molecule (ICAM)-1, but not DC-specific ICAM-3-grabbing nonintegrin, to stimulate CD4+ T cells in the absence of exogenous antigen. J Immunol 173:50–60 [CrossRef]
    [Google Scholar]
  37. Sabatté J., Maggini J., Nahmod K., Amaral M. M., Martínez D., Salamone G., Ceballos A., Giordano M., Vermeulen M., Geffner J. 2007; Interplay of pathogens, cytokines and other stress signals in the regulation of dendritic cell function. Cytokine Growth Factor Rev 18:5–17 [CrossRef]
    [Google Scholar]
  38. Salentin R., Gemsa D., Sprenger H., Kaufmann A. 2003; Chemokine receptor expression and chemotactic responsiveness of human monocytes after influenza A virus infection. J Leukoc Biol 74:252–259 [CrossRef]
    [Google Scholar]
  39. Sallusto F., Schaerli P., Loetscher P., Schaniel C., Lenig D., Mackay C. R., Qin S., Lanzavecchia A. 1998; Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur J Immunol 28:2760–2769 [CrossRef]
    [Google Scholar]
  40. Schneider-Schaulies S., Dittmer U. 2006; Silencing T cells or T-cell silencing: concepts in virus-induced immunosuppression. J Gen Virol 87:1423–1438 [CrossRef]
    [Google Scholar]
  41. Schneider-Schaulies S., ter Meulen V. 2002; Modulation of immune functions by measles virus. Springer Semin Immunopathol 24:127–148 [CrossRef]
    [Google Scholar]
  42. Schneider-Schaulies S., Klagge I. M., ter Meulen V. 2003; Dendritic cells and measles virus infection. Curr Top Microbiol Immunol 276:77–101
    [Google Scholar]
  43. Schnorr J. J., Xanthakos S., Keikavoussi P., Kampgen E., ter Meulen V., Schneider-Schaulies S. 1997; Induction of maturation of human blood dendritic cell precursors by measles virus is associated with immunosuppression. Proc Natl Acad Sci U S A 94:5326–5331 [CrossRef]
    [Google Scholar]
  44. Servet-Delprat C., Vidalain P. O., Bausinger H., Manie S., Le Deist F., Azocar O., Hanau D., Fischer A., Rabourdin-Combe C. 2000; Measles virus induces abnormal differentiation of CD40 ligand-activated human dendritic cells. J Immunol 164:1753–1760 [CrossRef]
    [Google Scholar]
  45. Servet-Delprat C., Vidalain P. O., Valentin H., Rabourdin-Combe C. 2003; Measles virus and dendritic cell functions: how specific response cohabits with immunosuppression. Curr Top Microbiol Immunol 276:103–123
    [Google Scholar]
  46. Shi G., Partida-Sánchez S., Misra R. S., Tighe M., Borchers M. T., Lee J. J., Simon M. I., Lund F. E. 2007; Identification of an alternative G α q-dependent chemokine receptor signal transduction pathway in dendritic cells and granulocytes. J Exp Med 204:2705–2718 [CrossRef]
    [Google Scholar]
  47. Shingai M., Ebihara T., Begum N. A., Kato A., Honma T., Matsumoto K., Saito H., Ogura H., Matsumoto M., Seya T. 2007; Differential type I IFN-inducing abilities of wild-type versus vaccine strains of measles virus. J Immunol 179:6123–6133 [CrossRef]
    [Google Scholar]
  48. Shishkova Y., Harms H., Krohne G., Avota E., Schneider-Schaulies S. 2007; Immune synapses formed with measles virus-infected dendritic cells are unstable and fail to sustain T cell activation. Cell Microbiol 9:1974–1986 [CrossRef]
    [Google Scholar]
  49. Sozzani S., Allavena P., D'Amico G., Luini W., Bianchi G., Kataura M., Imai T., Yoshie O., Bonecchi R., Mantovani A. 1998; Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J Immunol 161:1083–1086
    [Google Scholar]
  50. Steinman R. M., Granelli-Piperno A., Pope M., Trumpfheller C., Ignatius R., Arrode G., Racz P., Tenner-Racz K. 2003; The interaction of immunodeficiency viruses with dendritic cells. Curr Top Microbiol Immunol 276:1–30
    [Google Scholar]
  51. van Lieshout A. W., van der Voort R., le Blanc L. M., Roelofs M. F., Schreurs B. W., van Riel P. L., Adema G. J., Radstake T. R. 2006; Novel insights in the regulation of CCL18 secretion by monocytes and dendritic cells via cytokines, toll-like receptors and rheumatoid synovial fluid. BMC Immunol 7:23 [CrossRef]
    [Google Scholar]
  52. Varani S., Frascaroli G., Homman-Loudiyi M., Feld S., Landini M. P., Soderberg-Naucler C. 2005; Human cytomegalovirus inhibits the migration of immature dendritic cells by down-regulating cell-surface CCR1 and CCR5. J Leukoc Biol 77:219–228
    [Google Scholar]
  53. Wesa A., Galy A. 2002; Increased production of pro-inflammatory cytokines and enhanced T cell responses after activation of human dendritic cells with IL-1 and CD40 ligand. BMC Immunol 3:14 [CrossRef]
    [Google Scholar]
  54. Zilliox M. J., Parmigiani G., Griffin D. E. 2006; Gene expression patterns in dendritic cells infected with measles virus compared with other pathogens. Proc Natl Acad Sci U S A 103:3363–3368 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.008581-0
Loading
/content/journal/jgv/10.1099/vir.0.008581-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error