Cytotoxic mechanisms may play a role in the local immune response in the central nervous system in neuroborreliosis

Journal of Neuroimmunology

Volumn 232, Issue 1-2, 2011, Pages 186-193

  Nordberg, Marika ^a,b   Forsberg, Pia ^a   Johansson, Anna ^a   Nyman, Dag ^b   Jansson, Christian ^b   Ernerudh, Jan ^a   Ekerfelt, Christina ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

^b Aland Central Hospital   (Finland)

Author keywords

Cytotoxic mechanisms; IL 17; Lyme borreliosis; Neuroborreliosis; Persisting symptoms

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GRANZYME B; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 7; PERFORIN;

ADOLESCENT; ADULT; ANTIBODY PRODUCTION; ARTICLE; CELL DENSITY; CEREBROSPINAL FLUID; CHILD; CONTROLLED STUDY; CYTOTOXICITY TEST; FEMALE; HUMAN; IMMUNE RESPONSE; LYME DISEASE; LYMPHOCYTE; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SCHOOL CHILD; SECRETORY CELL; TARGET CELL;

EID: 79952241552     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2010.09.028     Document Type: Article

References (72)

1. Abbas, A.K., Lichtman, A. H., 2005. Cellular and Molecular Immunology, Elsevier Saunders, Philadelphia, pp. 113, 243-274, 298-317.
2. Acosta-Rodriguez E.V., Rivino L., Geginat J., Jarrossay D., Gattorno M., Lanzavecchia A., Sallusto F., Napolitani G. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol 2007, 8:639-646.
3. Asch E.S., Bujak D.I., Weiss M., Peterson M.G., Weinstein A. Lyme disease: an infectious and postinfectious syndrome. J Rheumatol 1994, 21:454-461.
4. Babbe H., Roers A., Waisman A., Lassmann H., Goebels N., hohlfeld R., Friese M., Schröder R., Deckert M., Schmidt S., Ravid R., Rajewsky K. Clonal expansion of CD8+ T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction. J Exp Med 2000, 192:393-404.
5. Baig S., Olsson T., Höjeberg B., Link H. Cells secreting antibodies to myelin basic protein in cerebrospinal fluid of patients with Lyme neuroborreliosis. Neurology 1986, 41:581-587.
6. Beermann C., Wunderli-Allenspach H., Groscurth P., Filgueira L. Lipoproteins from Borrelia burgdorferi applied in liposomes and presented by dendritic cells induce CD8(+) T-lymphocytes in vitro. Cell Immunol 2000, 201:124-131.
7. Berard M., Brandt K., Bulfone-Paus S., Tough D.F. IL-15 promotes the survival of naive and memory phenotype CD8+ T cells. J Immunol 2003, 170:5018-5026.
8. Borish L. IL-10: evolving concepts. J Allergy Clin Immunol 1998, 101:293-297.
9. Boyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1g. Scand J Clin Lab Invest Suppl 1968, 97:77-89.
10. Burchill M.A., Nardelli D.T., England D.M., DeCoster D.J., Cristopherson J.A., Callister S.M., Shell R.F. Inhibition of interleukin-17 prevents the development of arthritis in vaccinated mice challenged with Borrelia burgdorferi. Infect Immun 2003, 71:3437-3442.
11. Codolo G., Amedei A., Steere A.C., Papinutto E., Cappon A., Polenghi A., Benagiano M., Paccani S.R., Sambri V., Del Prete G., Baldari C.T., Zanotti G., Montecucco C., D'Elios M.M., de Bernard M. Borrelia burgdorferi NapA-driven Th17 cell inflammation in lyme arthritis. Arthritis Rheum 2008, 58:3609-3617.
12. Curtsinger J.M., Lins D.C., Johnson C.M., Mescher M.F. Signal 3 tolerant CD8 T cells degranulate in response to antigen but lack granzyme B to mediate cytolysis. J Immunol 2005, 175:4392-4399.
13. Ekerfelt C., Ernerudh J., Bunikis J., Vrethem M., Aagesen J., Roberg M., Bergstrom S., Forsberg P. Compartmentalization of antigen specific cytokine responses to the central nervous system in CNS borreliosis: secretion of IFN-gamma predominates over IL-4 secretion in response to outer surface proteins of Lyme disease Borrelia spirochetes. J Neuroimmunol 1997, 79:155-162.
14. Ekerfelt C., Ernerudh J., Forsberg P., Bergstrom S. Augmented intrathecal secretion of interferon-gamma in response to Borrelia garinii in neuroborreliosis. J Neuroimmunol 1998, 89:177-181.
15. Ekerfelt C., Masreliez C., Svenvik M., Ernerudh J., Roberg M., Forsberg P. Antibodies and T-cell reactivity to Borrelia burgdorferi in an asymptomatic population: a study of healthy blood donors in an inland town district in the south-east of Sweden. Scand J Infect Dis 2001, 33:806-808.
16. Ekerfelt C., Jarefors S., Tynngard N., Hedlund M., Sander B., Bergstrom S., Forsberg P., Ernerudh J. Phenotypes indicating cytolytic properties of Borrelia-specific interferon-gamma secreting cells in chronic Lyme neuroborreliosis. J Neuroimmunol 2003, 145:115-126.
17. Fahrer H., Sauvain M.J., Zhioua E., Van Hoecke C., Gern L.E. Longterm survey (7years) in a population at risk for Lyme borreliosis: what happens to the seropositive individuals?. Eur J Epidemiol 1998, 14:117-123.
18. Forsberg P., Ernerudh J., Ekerfelt C., Roberg M., Vrethem M., Bergstrom S. The outer surface proteins of Lyme disease borrelia spirochetes stimulate T cells to secrete interferon-gamma (IFN-gamma): diagnostic and pathogenic implications. Clin Exp Immunol 1995, 101:453-460.
19. Frey M., Jaulhac B., Piemont Y., Marcellin L., Boohs P.M., Vautravers P., Jesel M., Kuntz J.L., Monteil H., Sibilia J. Detection of Borrelia burgdorferi DNA in muscle of patients with chronic myalgia related to Lyme disease. Am J Med 1998, 104:591-594.
20. Frietzsche M. Chronic Lyme borreliosis at the root of multiple sclerosis-is a cure with antibiotics attainable?. Med Hypothesis 2005, 64:438-448.
21. Garcia-Monco J.C., Benach J.L. Lyme neuroborreliosis. Ann Neurol 1995, 37:691-702.
22. Gross D.M., Steere A.C., Huber B.T. T helper 1 response is dominant and localized to the synovial fluid in patients with Lyme arthritis. J Immunol 1998, 160:1022-1028.
23. Groux H., Bigler M., de Vries J.E., Roncarolo M.G. Inhibitory and stimulatory effects of IL-10 on human CD8+ T cells. J Immunol 1998, 160:3188-3193.
24. Grusell M., Widhe M., Ekerfelt C. Increased expression of the Th1-inducing cytokines interleukin-12 and interleukin-18 in cerebrospinal fluid but not in sera from patients with Lyme neuroborreliosis. J Neuroimmunol 2002, 131:173-178.
25. Halperin J.J. Neuroborreliosis: central nervous system involvement. Semin Neurol 1997, 17:19-24.
26. Harrington L.E., Hatton R.D., Mangan P.R., Turner H., Murphy T.L., Murphy K.M., Weaver C.T. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005, 6:1123-1132.
27. Hemmer B., Gran B., Zhao Y., Marques A., Pascal J., Tzou A., Kondo T., Cortese I., Bielekova B., Straus S.E., McFarland H.F., Houghten R., Simon R., Pinilla C., Martin R. Identification of candidate T-cell epitopes and molecular mimics in chronic Lyme disease. Nat Med 1999, 5:1375-1382.
28. Iliopoulou B.P., Alroy J., Huber B.T. Persistent arthritis in Borrelia burgdorferi-infected HLA-DR4-positive CD28-negative mice post-antibiotic treatment. Arthritis Rheum 2008, 58:3892-3901.
29. Infante-Duarte C., Horton H.F., Byrne M.C., Kamradt T. Microbial lipopeptides induce the production of IL-17 in Th cells. J Immunol 2000, 165:6107-6115.
30. Jacobsen M., Cepok S., Quak E., Happel M., Gaber R., Ziegler A., Schock S., Oertel W.H., Sommer N., Hemmer B. Oligoclonal expansion of memory CD8+ T cells in cerebrospinal fluid from multiple sclerosis patients. Brain 2002, 125:538-550.
31. Jacobsen M., Zhou D., Cepok S., Nessler S., Happel M., Stei S., Wilske B., Sommer N., Hemmer B. Clonal accumulation of activated CD8+ T cells in the central nervous system during the early phase of neuroborreliosis. J Infect Dis 2003, 187:963-973.
32. Jarefors S., Karlsson M., Forsberg P., Eliasson I., Ernerudh J., Ekerfelt C. Reduced number of interleukin-12 secreting cells in patients with Lyme borreliosis previously exposed to Anaplasma phagocytophilum. Clin Exp Immunol 2006, 143:322-328.
33. Jarefors S., Janefjord C.K., Forsberg P., Jenmalm M.C., Ekerfelt C. Decreased up-regulation of the interleukin-12Rbeta2-chain and interferon-gamma secretion and increased number of forkhead box P3-expressing cells in patients with a history of chronic Lyme borreliosis compared with asymptomatic Borrelia-exposed individuals. Clin Exp Immunol 2007, 147:18-27.
34. Kaiser R. Variable CSF findings in early and late Lyme neuroborreliosis: a follow-up study in 47 patients. J Neurol 1994, 242:26-36.
35. Kang I., Barthold S.W., Persing D.H., Bockenstedt L.K. T-helper-cell cytokines in the early evolution of murine Lyme arthritis. Infect Immun 1997, 65:3107-3111.
36. Kebir H., Ifergan I., Alvarez J.I., Bernard M., Poirier J., Arbour N., Duquette P., Prat A. Preferential recruitment of interferon-gamma-expressing TH 17 cells in multiple sclerosis. Ann Neurol 2009, 66:390-402.
37. Klonowski K.D., Williams K.J., Marzo A.L., Blair D.A., Lingenheld E.G., Lefrancois L. Dynamics of blood-borne CD8 memory T cell migration in vivo. Immunity 2004, 20:551-562.
38. Kolls J.K., Linden A. Interleukin-17 family members and inflammation. Immunity 2004, 21:467-476.
39. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 Cells. Annu Rev Immunol 2009, 27:485-517.
40. Levings M.K., Bacchetta R., Schulz U., Roncarolo M.G. The role of IL-10 and TGF-beta in the differentiation and effector function of T regulatory cells. Int Arch Allergy Immunol 2002, 129:263-276.
41. Lock C., Hermans G., Pedotti R., Brendolan A., Schadt E., Garren H., Langer-Gould A., Strober S., Cannella B., Allard J., Klonowski P., Austin A., Lad N., Kaminski N., Galli S.J., Oksenberg J.R., Raine C.S., Heller R., Steinman L. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 2002, 8:500-508.
42. Ma A., Koka R., Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 2006, 24:657-679.
43. Matusevicius D., Kivisakk P., He B., Kostulas N., Ozenci V., Fredrikson S., Link H. Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis. Mult Scler 1999, 5:101-104.
44. Nakae S., Saijo S., Horai R., Sudo K., Mori S., Iwakura Y. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci USA 2003, 100:5986-5990.
45. Nocton J.J., Steere A.C. Lyme disease. Adv Intern Med 1995, 40:69-117.
46. Oksi J., Kalimo H., Marttila R.J., Marjamaki M., Sonninen P., Nikoskelainen J., Viljanen M.K. Inflammatory brain changes in Lyme borreliosis. A report on three patients and review of literature. Brain 1996, 119(Pt 6):2143-2154.
47. Oksi J., Savolainen J., Pene J., Bousquet J., Laippala P., Viljanen M.K. Decreased interleukin-4 and increased gamma interferon production by peripheral blood mononuclear cells of patients with Lyme borreliosis. Infect Immun 1996, 64:3620-3623.
48. Oksi J., Marjamaki M., Nikoskelainen J., Viljanen M.K. Borrelia burgdorferi detected by culture and PCR in clinical relapse of disseminated Lyme borreliosis. Ann Med 1999, 31:225-232.
49. Oschmann P., Dorndorf W., Hornig C., Schafer C., Wellensiek H.J., Pflughaupt K.W. Stages and syndromes of neuroborreliosis. J Neurol 1998, 245:262-272.
50. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., Wang Y., Hood L., Zhu Z., Tian Q., Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005, 6:1133-1141.
51. Pfister H.W., Rupprecht T.A. Clinical aspects of neuroborreliosis and post-Lyme disease syndrome in adult patients. Int J Med Microbiol 2006, 296(Suppl 40):11-16.
52. Preac-Mursic V., Weber K., Pfister H.W., Wilske B., Gross B., Baumann A., Prokop J. Survival of Borrelia burgdorferi in antibiotically treated patients with Lyme borreliosis. Infection 1989, 17:355-359.
53. Roessner K., Trivedi H., Gaur L., Howard D., Aversa J., Cooper S.M., Sigal L.H., Budd R.C. Biased T-cell antigen receptor repertoire in Lyme arthritis. Infect Immun 1998, 66:1092-1099.
54. Rosenberg S.A., Yannelli J.R., Yang J.C., Topalian S.L., Schwartzentruber D.J., Weber J.S., Parkinson D.R., Seipp C.A., Einhorn J.H., White D.E. Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2. J Natl Cancer Inst 1994, 86:1159-1166.
55. Rowbottom A.W., Lepper M.A., Garland R.J., Cox C.V., Corley E.G. Interleukin-10-induced CD8 cell proliferation. Immunology 1999, 98:80-89.
56. Schluns K.S., Kieper W.C., Jameson S.C., Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 2000, 1:426-432.
57. Shi Y., Liu C.H., Roberts A.I., Das J., Xu G., Ren G., Zhang Y., Zhang L., Yuan Z.R., Tan H.S., Das G., Devadas S. Granulocyte-macrophage colony-stimulating factor (GM-CSF) and T-cell responses: what we do and don't know. Cell Res 2006, 16:126-133.
58. Sigal L.H. Immunologic mechanisms in Lyme neuroborreliosis: the potential role of autoimmunity and molecular mimicry. Semin Neurol 1997, 17:63-68.
59. Singh S.K., Girschick H.J. Lyme borreliosis: from infection to autoimmunity. Clin Microbiol Infect 2004, 10:598-614.
60. Sjowall J., Carlsson A., Vaarala O., Bergstrom S., Ernerudh J., Forsberg P., Ekerfelt C. Innate immune responses in Lyme borreliosis: enhanced tumour necrosis factor-alpha and interleukin-12 in asymptomatic individuals in response to live spirochetes. Clin Exp Immunol 2005, 141:89-98.
61. Steere A.C. Lyme disease. N Engl J Med 2001, 345:115-125.
62. Steere A.C., Sikand V.K., Schoen R.T., Nowakowski J. Asymptomatic infection with Borrelia burgdorferi. Clin Infect Dis 2003, 37:528-532.
63. Steere A.C., Klitz W., Drouin E.E., Falk B.A., Kwok W.W., Nepom G.T., Baxter-Lowe L.A. Antibiotic-refractory Lyme arthritis is associated with HLA-DR molecules that bind a Borrelia burgdorferi peptide. J Exp Med 2006, 203:961-971.
64. Tesmer L.A., Lundy S.K., Sarkar S., Fox D.A. Th17 cells in human disease. Immunol Rev 2008, 223:87-113.
65. Thompson L.J., Kolumam G.A., Thomas S., Murali-Krishna K. Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J Immunol 2006, 177:1746-1754.
66. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003, 3:133-146.
67. Wada H., Noguchi Y., Marino M.W., Dunn A.R., Old L.J. T cell functions in granulocyte/macrophage colony-stimulating factor deficient mice. Proc Natl Acad Sci USA 1997, 94:12557-12561.
68. Wang W.Z., Fredrikson S., Sun J.B., Link H. Lyme neuroborreliosis: evidence for persistent up-regulation of Borrelia burgdorferi-reactive cells secreting interferon-gamma. Scand J Immunol 1995, 42:694-700.
69. Wang G., Ojaimi C., Wu H., Saksenberg V., Iyer R., Liveris D., McClain S.A., Wormser G.P., Schwartz I. Disease severity in a murine model of lyme borreliosis is associated with the genotype of the infecting Borrelia burgdorferi sensu stricto strain. J Infect Dis 2002, 186:782-791.
70. Weigelt W., Schneider T., Lange R. Sequence homology between spirochaete flagellin and human myelin basic protein. Immunol Today 1992, 13:279-280.
71. Widhe M., Jarefors S., Ekerfelt C., Vrethem M., Bergstrom S., Forsberg P., Ernerudh J. Borrelia-specific interferon-gamma and interleukin-4 secretion in cerebrospinal fluid and blood during Lyme borreliosis in humans: association with clinical outcome. J Infect Dis 2004, 189:1881-1891.
72. Williams M.A., Bevan M.J. Effector and memory CTL differentiation. Annu Rev Immunol 2007, 25:171-192.