Altered natural killer cells' response to herpes virus infection in multiple sclerosis involves KIR2DL2 expression

Journal of Neuroimmunology

Volumn 251, Issue 1-2, 2012, Pages 55-64

  Rizzo, Roberta ^a   Gentili, Valentina ^a   Casetta, Ilaria ^a   Caselli, Elisabetta ^a   De Gennaro, Riccardo ^a   Granieri, Enrico ^a   Cassai, Enzo ^a   Di Luca, Dario ^a   Rotola, Antonella ^a  

^a UNIVERSITY OF FERRARA   (Italy)

Author keywords

Herpes virus; KIR; Multiple sclerosis; NK cell

Indexed keywords

KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL2; TOLL LIKE RECEPTOR 9;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DEGRANULATION; FEMALE; HERPES VIRUS INFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFECTION SENSITIVITY; LYMPHOCYTE ACTIVATION; MALE; MULTIPLE SCLEROSIS; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VIRUS PATHOGENESIS;

ADULT; CELLS, CULTURED; CPG ISLANDS; CYTOKINES; FEMALE; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; KILLER CELLS, NATURAL; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; RECEPTORS, KIR2DL2; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 9; VIRAL LOAD; YOUNG ADULT;

EID: 84865642330     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2012.07.004     Document Type: Article

References (65)

1. Ascherio A., Munger K.L. Environmental risk factor for multiple sclerosis. Part I: role of infection. Ann. Neurol. 2007, 61:288-299.
2. Ashkar A.A., Bauer S., Mitchell W.J., Vieira J., Rosenthal K.L. Local delivery of CpG oligodeoxynucleotides induces rapid changes in the genital mucosa and inhibits replication, but not entry, of herpes simplex virus type 2. J. Virol. 2003, 77:8948-8956.
3. Bauer M., Heeg K., Wagner H., Lipford G.B. DNA activates human immune cells through a CpG sequence-dependent manner. Immunology 1999, 97:699-705.
4. Beutler B. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 2004, 430:257-263.
5. Bergström T., Andersen O., Vahlne A. Isolation of herpes simplex virus type 1 during first attack of multiple sclerosis. Ann. Neurol. 1989, 26:283-285.
6. Biron C.A., Nguyen K.B., Pien G.C., Cousens L.P., Salazar-Mather T.P. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 1999, 17:189-220.
7. Buljevac D., Flach H.Z., Ho W.C., Hijdra D., Laman J.D., Savelkoul H.F.J., van der Meché F.G.A., van Doorn P.A., Hintzen R.Q. Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain 2002, 125:952-960.
8. Burgoon M.P., Cohrs R.J., Bennett J.L., Anderson S.W., Ritchie A.M., Cepok S., Hemmer B., Gilden D., Owens G.P. Varicella zoster virus is not a disease-relevant antigen in multiple sclerosis. Ann. Neurol. 2009, 65:474-479.
9. Cantin E., Tanamachi B., Openshaw H. Role for gamma interferon in control of herpes simplex virus type 1 reactivation. J. Virol. 1999, 73:3418-3423.
10. Carrol M.C., Prodeus A.P. Linkages of innate and adaptive immunity. Curr. Opin. Immunol. 1998, 10:36-40.
11. Casetta I., Granieri E. Clinical infections and multiple sclerosis: contribution from analytical epidemiology. J. Neurovirol. 2000, 6:S147-S151.
12. Correale J., Fiol M., Gilmore W. The risk of relapses in multiple sclerosis during systemic infections. Neurology 2006, 67:652-659.
13. Costantino C.M., Baecher-Allan C., Hafler D.A. Multiple sclerosis and regulatory T cells. J. Clin. Immunol. 2008, 28:697-706.
14. Du Z., Gjertson D.W., Reed E.F., Rajalingam R. Receptor-ligand analyses define minimal killer cell Ig-like receptor (KIR) in humans. Immunogenetics 2007, 59:1-15.
15. Estefanía E., Gómez-Lozano N., Portero F., de Pablo R., Solís R., Sepúlveda S., Vaquero M., González M.A., Suárez E., Roustán G., Vilches C. Influence of KIR gene diversity on the course of HSV-1 infection: resistance to the disease is associated with the absence of KIR2DL2 and KIR2DS2. Tissue Antigens 2007, 70:34-41.
16. Fehniger T.A., Carson W.E., Caligiuri M.A. Costimulation of human natural killer cells is required for interferon gamma production. Transplant. Proc. 1999, 31:1476-1478.
17. Ferrante P., Mancuso R., Pagani E., Guerini F.R., Calvo M.G., Saresella M., Speciale L., Caputo D. Molecular evidences for a role of HSV-1 in multiple sclerosis clinical acute attack. J. Neurovirol. 2000, 6:S109-S114.
18. Ferrò, M.T., Franciotta, D., Prelle, A., Bestetti, A., Cinque, P., in press. Active intrathecal herpes simplex virus type 1 (HSV-1) and human herpes virus-6 (HHV-6) infection at onset of multiple sclerosis. J. Neurovirol.
19. Fotheringham J., Jacobson S. Human herpes virus 6 and multiple sclerosis: potential mechanisms for virus-induced disease. Herpes 2005, 12:4-9.
20. Geiger K.D., Gurushanthaiah D., Howes E.L., Lewandowski G.A., Reed J.C., Bloom F.E., Sarvetnick N.E. Cytokine-mediated survival from lethal herpes simplex virus infection: role of programmed neuronal death. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:3411-3415.
21. Gilden D.H. Infectious causes of multiple sclerosis. Lancet Neurol. 2005, 4:195-202.
22. Guillerey C., Mouriès J., Polo G., Doyen N., Law H.K., Chan S., Kastner P., Leclerc C., Dadaglio G. Pivotal role of plasmacytoid dendritic cells in inflammation and NK cell responses following TLR9 triggering in mice. Blood 2012, 120:90-99.
23. Hawkes C.H., Giovannoni G., Keir G., Cunnington M., Thompson E.J. Seroprevalence of herpes simplex virus type 2 in multiple sclerosis. Acta Neurol. Scand. 2006, 114:363-367.
24. Henel G., Singh K., Cui D., Pryshchep S., Lee W.W., Weyand M.C., Goronzy J.J. Uncoupling of T-cell effector functions by inhibitory killer immunoglobulin-like receptors. Blood 2006, 107:4449-4457.
25. Hohlfeld R., Wekerle H. Autoimmune concepts of multiple sclerosis as a basis for selective immunotherapy: from pipe dreams to (therapeutic) pipelines. Proc. Natl. Acad. Sci. U. S. A. 2004, 2:14599-14606.
26. Javed A., Reder A.T. Therapeutic role of beta-interferons in multiple sclerosis. Pharmacol. Ther. 2006, 110:35-56.
27. Jelcic I., Hsu K.C., Kakalacheva K., Breiden P., Dupont B., Uhrberg M., Martin R., Münz C., Lünemann J.D. Killer immunoglobulin-like receptor locus polymorphisms in multiple sclerosis. Mult. Scler. 2012, 18:951-958. 10.1177/1352458511431726.
28. Judy B.M., Taylor K., Deeraksa A., Johnston R.K., Endsley J.J., Vijayakumar S., Aronson J.F., Estes D.M., Torres A.G. Prophylactic application of CpG oligonucleotides augments the early host response and confers protection in acute melioidosis. PLoS One 2012, 7:e34176.
29. Kastrukoff L.F., Morgan N.G., Zecchini D., White R., Petkau A.J., Satoh J., Paty D.W. Natural killer cells in relapsing-remitting MS: effect of treatment with interferon beta-1B. Neurology 1999, 52:351-359.
30. Kawai T., Akira S. Innate immune recognition of viral infection. Nat. Immunol. 2006, 7:131-137.
31. La D., Czarnecki C., El-Gabalawy H., Kumar A., Meyers A.F., Bastien N., Simonsen J.N., Plummer F.A., Luo M. Enrichment of variations in KIR3DL1/S1 and KIR2DL2/L3 among H1N1/09 ICU patients: an exploratory study. PLoS One 2011, 6:e29200.
32. Klaschik S., Gursel I., Klinman D.M. CpG-mediated changes in gene expression in murine spleen cells identified by microarray analysis. Mol. Immunol. 2007, 44:1095-1104.
33. Kurtzke J.F. Rating, neurological impairment in multiple sclerosis: an expanded disability scale (EDSS). Neurology 1983, 33:1444-1452.
34. Lorentzen A.R., Karlsen T.H., Olsson M., Smestad C., Mero I.L., Woldseth B., Sun J.Y., Senitzer D., Celius E.G., Thorsby E., Spurkland A., Lie B.A., Harbo H.F. Killer immunoglobulin-like receptor ligand HLA-Bw4 protects against multiple sclerosis. Ann. Neurol. 2009, 65:658-666.
35. Lublin D.F., Reingold S.C. Defining the clinical course of multiple sclerosis: results of an international survey. Neurology 1996, 46:907-911.
36. Lünemann A., Tackenberg B., DeAngelis T., da Silva R.B., Messmer B., Vanoaica L.D., Miller A., Apatoff B., Lublin F.D., Lünemann J.D., Münz C. Impaired IFN-γ production and proliferation of NK cells in multiple sclerosis. Int. Immunol. 2011, 23:139-148.
37. Mancuso R., Delbue S., Borghi E., Pagani E., Calvo M.G., Caputo D., Granieri E., Ferrante P. Increased prevalence of varicella zoster virus DNA in cerebrospinal fluid from patients with multiple sclerosis. J. Med. Virol. 2007, 79:192-199.
38. Marrie R.A. Environmental risk factors in multiple sclerosis aetiology. Lancet Neurol. 2004, 3:709-718.
39. McDonald W.I., Compston A., Edan G., Goodkin D., Hartung H.P., Lublin F.D., McFarland H.F., Paty D.W., Polman C.H., Reingold S.C., Sandberg-Wollheim M., Sibley W., Thompson A., van den Noort S., Weinshenker B.Y., Wolinsky J.S. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the Diagnosis of Multiple Sclerosis. Ann. Neurol. 2001, 50:121-127.
40. McFarland H.F., Martin R. Multiple sclerosis: a complicated picture of autoimmunity. Nat. Immunol. 2007, 8:913-919.
41. Mikloska Z., Cunningham A.L. Alpha and gamma interferons inhibit herpes simplex virus type 1 infection and spread in epidermal cells after axonal transmission. J. Virol. 2001, 75:11821-11826.
42. Mirandola P., Stefan A., Brambilla E., Campadelli-Fiume G., Grimaldi L.M. Absence of human herpes virus 6 and 7 from spinal fluid and serum of multiple sclerosis patients. Neurology 1999, 53:1367-1368.
43. Moraru M., Cisneros E., Gómez-Lozano N., de Pablo R., Portero F., Cañizares M., Vaquero M., Roustán G., Millán I., López-Botet M., Vilches C. Host genetic factors in susceptibility to herpes simplex type 1 virus infection: contribution of polymorphic genes at the interface of innate and adaptive immunity. J. Immunol. 2012, 188:4412-4420.
44. Moretta L., Bottino C., Pende D., Vitale M., Mingari M.C., Moretta A. Different checkpoints in human NK-cell activation. Trends Immunol. 2004, 25:670-676.
45. Orr M.T., Murphy W.J., Lanier L.L. 'Unlicensed' natural killer cells dominate the response to cytomegalovirus infection. Nat. Immunol. 2010, 11:321-327.
46. Rabinovich B.A., Li J., Shannon J., Hurren R., Chalupny J., Cosman D., Miller R.G. Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J. Immunol. 2003, 170:3572-3576.
47. Raulet D.H., Vance R.E.N. Self-tolerance of natural killer cells. Rev. Immunol. 2006, 6:520-531.
48. Rodríguez Carnero S., Martínez-Vázquez C., Potel Alvarellos C., Alvarez Fernández M., Prieto González J.M., Noya García M., de la Fuente Aguado J., Sopeña Argüelles B. Lack of human herpes virus type 6 DNA in CSF by nested PCR among patients with multiple sclerosis. Rev. Clin. Esp. 2002, 202:588-591.
49. Rotola A., Merlotti I., Caniatti L., Caselli E., Granieri E., Tola M.R., Di Luca D., Cassai E. Human herpes virus 6 infects the central nervous system of multiple sclerosis patients in the early stages of the disease. Mult. Scler. 2004, 10:348-354.
50. Sargsyan S.A., Shearer A.J., Ritchie A.M., Burgoon M.P., Anderson S., Hemmer B., Stadelmann C., Gattenlöhner S., Owens G.P., Gilden D., Bennett J.L. Absence of Epstein-Barr virus in the brain and CSF of patients with multiple sclerosis. Neurology 2010, 74:1127-1135.
51. Scarisbrick I.A., Rodriguez M. Hit-hit and hit-run: viruses in the playing field of multiple sclerosis. Curr. Neurol. Neurosci. Rep. 2003, 3:265-271.
52. Seich A., Basatena N.K., Macnamara A., Vine A.M., Thio C.L., Astemborski J., Usuku K., Osame M., Kirk G.D., Donfield S.M., Goedert J.J., Bangham C.R., Carrington M., Khakoo S.I., Asquith B. KIR2DL2 enhances protective and detrimental HLA class I-mediated immunity in chronic viral infection. PLoS Pathog. 2011, 7:e1002270.
53. Serafini B., Rosicarelli B., Franciotta D., Magliozzi R., Reynolds R., Cinque P., Andreoni L., Trivedi P., Salvetti M., Faggioni A., Aloisi F. Dysregulated Epstein-Barr virus infection in the multiple sclerosis brain. J. Exp. Med. 2007, 204:2899-2912.
54. Sivori S., Falco M., Della Chiesa M., Carlomagno S., Vitale M., Moretta L., Moretta A. CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10116-10121.
55. Sivori S., Carlomagno S., Moretta L., Moretta A. Comparison of different CpG oligodeoxynucleotide classes for their capability to stimulate human NK cells. Eur. J. Immunol. 2006, 36:961-967.
56. Sivori S., Falco M., Carlomagno S., Romeo E., Soldani C., Bensussan A., Viola A., Moretta L., Moretta A. A novel KIR-associated function: evidence that CpG DNA uptake and shuttling to early endosomes is mediated by KIR3DL2. Blood 2010, 116:1637-1647.
57. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005, 23:683-747.
58. Takahashi K., Aranami T., Endoh M., Miyake S., Yamamura T. The regulatory role of natural killer cells in multiple sclerosis. Brain 2004, 127:1917-1927.
59. Uhrberg M., Valiante N.M., Shum B.P., Shilling H.G., Lienert-Weidenbach K., Corliss B., Tyan D., Lanier L.L., Parham P. Human diversity in killer cell inhibitory receptor genes. Immunity 1997, 7:753-763.
60. Wandinger K., Jabs W., Siekhaus A., Bubel S., Trillenberg P., Wagner H., Wessel K., Kirchner H., Hennig H. Association between clinical disease activity and Epstein-Barr virus reactivation in MS. Neurology 2000, 55:178-184.
61. Winkler-Pickett R., Young H.A., Cherry J.M., Diehl J., Wine J., Back T., Bere W.E., Mason A.T., Ortaldo J.R. In vivo regulation of experimental autoimmune encephalomyelitis by NK cells: alteration of primary adaptive responses. J. Immunol. 2008, 180:4495-4506.
62. Wu G.Q., Zhao Y.M., Huang H., Lai X.Y. Effects of blocking inhibitory KIR receptors on cytotoxic activity of human NK cells in vitro. Zhejiang Da Xue Xue Bao Yi Xue Ban 2011, 40:475-481.
63. Xu W., Fazekas G., Hara H., Tabira T. Mechanism of natural killer (NK) cell regulatory role in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 2005, 163:24-30.
64. Zhang B., Yamamura T., Kondo T., Fujiwara M., Tabira T. Regulation of experimental autoimmune encephalomyelitis by natural killer (NK) cells. J. Exp. Med. 1997, 186:1677-1687.
65. Zhu D., Corral L.G., Fleming Y.W., Stein B. Immunomodulatory drugs Revlimid (lenalidomide) and CC-4047 induce apoptosis of both hematological and solid tumor cells through NK cell activation. Cancer Immunol. Immunother. 2008, 57:1849-1859.