Borrelia burgdorferi induces TLR1 and TLR2 in human microglia and peripheral blood monocytes but differentially regulates HLA-class II expression

Journal of Neuropathology and Experimental Neurology

Volumn 65, Issue 6, 2006, Pages 540-548

  Cassiani Ingoni, Riccardo ^a,e,f   Cabral, Erik S ^a   Lünemann, Jan D ^a   Garza, Zoila ^b   Magnus, Tim ^c   Gelderblom, Harald ^a   Munson, Peter J ^b   Marques, Adriana ^d   Martin, Roland ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c NATIONAL INSTITUTE ON AGING   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f Bldg10 ^*  (United States)

Author keywords

Glia; HLA class II; Lyme disease; Microglia; Monocyte; Outer surface protein A; Toll like receptor

Indexed keywords

CELL MARKER; GLYCOPROTEIN P 15095; HLA ANTIGEN CLASS 2; HLA DQ ANTIGEN; HLA DR ANTIGEN; RNA; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; CYTOKINE; MESSENGER RNA;

ANIMAL CELL; ARTICLE; ASTROCYTE; BORRELIA BURGDORFERI; BORRELIA INFECTION; BRAIN CELL; CELL LYSATE; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; GENE EXPRESSION; GLIA CELL; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; INFECTION SENSITIVITY; INNATE IMMUNITY; LYME DISEASE; MICROGLIA; MONOCYTE; NERVE CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; STEM CELL; BRAIN; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; DNA MICROARRAY; FETUS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; MICROBIOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BORRELIA BURGDORFERI; BRAIN; CELLS, CULTURED; CYTOKINES; FETUS; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; MICROGLIA; MONOCYTES; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 2;

EID: 33746778936     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-200606000-00002     Document Type: Article

References (58)

1. Steere AC, Coburn J, Glickstein L. The emergence of Lyme disease. J Clin Invest 2004;113:1093-101
2. Pachner AR, Dail D, Narayan K, et al. Increased expression of B-lymphocyte chemoattractant, but not pro-inflammatory cytokines, in muscle tissue in rhesus chronic Lyme borreliosis. Cytokine 2002;19:297-307
3. Isogai E, Isogai H, Kimura K, et al. Cytokines in the serum and brain in mice infected with distinct species of Lyme disease Borrelia. Microb Pathog 1996;21:413-19
4. Aloisi F. Immune function of microglia. Glia 2001;36:165-79
5. Benveniste EN. Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. J Mol Med 1997;75:165-73
6. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004;5:987-95
7. Lien E, Sellati TJ, Yoshimura A, et al. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J Biol Chem 1999;274:33419-25
8. Alexopoulou L, Thomas V, Schnare M, et al. Hyporesponsiveness to vaccination with Borrelia burgdorferi OspA in humans and in TLR1- and TLR2-deficient mice. Nat Med 2002;8:878-84
9. Takeuchi O, Sato S, Horiuchi T, et al. Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J Immunol 2002;169:10-14
10. Rasley A, Anguita J, Marriott I. Borrelia burgdorferi induces inflammatory mediator production by murine microglia. J Neuroimmunol 2002;130:22-31
11. Maric D, Maric I, Barker JL. Flow cytometric strategies to study CNS development. In: Boulton AA, Baker GB, eds. Neuromethods. Totowa, NJ: Humana, 1999:287-318
12. Maric D, Maric I, Barker JL. Developmental changes in cell calcium homeostasis during neurogenesis of the embryonic rat cerebral cortex. Cereb Cortex 2000;10:561-73
13. Wu YY, Mujtaba T, Han SS, et al. Isolation of a glial-restricted tripotential cell line from embryonic spinal cord cultures. Glia 2002;38:65-79
14. Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 2004;173:3916-24
15. Carpentier PA, Begolka WS, Olson JK, et al. Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 2005;49:360-74
16. Haupl T, Landgraf S, Netusil P, et al. Activation of monocytes by three OspA vaccine candidates: Lipoprotein OspA is a potent stimulator of monokines. FEMS Immunol Med Microbiol 1997;19:15-23
17. Donnelly RP, Dickensheets H, Finbloom DS. The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J Interferon Cytokine Res 1999;19:563-73
18. Perrier P, Martinez FO, Locati M, et al. Distinct transcriptional programs activated by interleukin-10 with or without lipopolysaccharide in dendritic cells: Induction of the B cell-activating chemokine, CXC chemokine ligand 13. J Immunol 2004;172:7031-42
19. Yee CS, Yao Y, Xu Q, et al. Enhanced production of IL-10 by dendritic cells deficient in CIITA. J Immunol 2005;174:1222-29
20. Greter M, Heppner FL, Lemos MP, et al. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat Med 2005;11:328-34
21. Suter T, Malipiero U, Otten L, et al. Dendritic cells and differential usage of the MHC class II transactivator promoters in the central nervous system in experimental autoimmune encephalitis. Eur J Immunol 2000;30:794-802
22. McMahon EJ, Bailey SL, Castenada CV, et al. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat Med 2005;11:335-39
23. Akira S, Hemmi H. Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 2003;85:85-95
24. Morr M, Takeuchi O, Akira S, et al. Differential recognition of structural details of bacterial lipopeptides by toll-like receptors. Eur J Immunol 2002;32:3337-47
25. Bsibsi M, Ravid R, Gveric D, et al. Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 2002;61:1013-21
26. Ebert S, Gerber J, Bader S, et al. Dose-dependent activation of microglial cells by Toll-like receptor agonists alone and in combination. J Neuroimmunol 2005;159:87-96
27. Hirschfeld M, Kirschning CJ, Schwandner R, et al. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol 1999;163:2382-86
28. Thomas V, Fikrig E. The Lyme disease vaccine takes its toll. Vector Borne Zoonotic Dis 2002;2:217-22
29. Wang G, Ma Y, Buyuk A, et al. Impaired host defense to infection and Toll-like receptor 2-independent killing of Borrelia burgdorferi clinical isolates in TLR2-deficient C3H/HeJ mice. FEMS Microbiol Lett 2004;231:219-25
30. Chen ZJ, Negra M, Levine A, et al. Oligodendrocyte precursor cells: reactive cells that inhibit axon growth and regeneration. J Neurocytol 2002;31:481-95
31. Seong SY, Matzinger P. Hydrophobicity: An ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 2004;4:469-78
32. Matzinger P. The danger model: A renewed sense of self. Science 2002;296:301-305
33. Chiao JW, Pavia C, Riley M, et al. Antigens of Lyme disease of spirochaete Borrelia burgdorferi inhibits antigen or mitogen-induced lymphocyte proliferation. FEMS Immunol Med Microbiol 1994;8:151-55
34. Diterich I, Rauter C, Kirschning CJ, et al. Borrelia burgdorferi-induced tolerance as a model of persistence via immunosuppression. Infect Immun 2003;71:3979-87
35. Noss EH, Harding CV, Boom WH. Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell Immunol 2000;201:63-74
36. Fortune SM, Solache A, Jaeger A, et al. Mycobacterium tuberculosis inhibits macrophage responses to IFN-gamma through myeloid differentiation factor 88-dependent and -independent mechanisms. J Immunol 2004;172:6272-80
37. Noss EH, Pai RK, Sellati TJ, et al. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol 2001;167:910-18
38. Gehring AJ, Rojas RE, Canaday DH, et al. The Mycobacterium tuberculosis 19-kilodalton lipoprotein inhibits gamma interferon-regulated HLA-DR and Fc gamma R1 on human macrophages through Toll-like receptor 2. Infect Immun 2003;71:4487-97
39. Montgomery RR, Nathanson MH, Malawista SE. The fate of Borrelia burgdorferi, the agent for Lyme disease, in mouse macrophages. Destruction, survival, recovery. J Immunol 1993;150:909-15
40. Girschick HJ, Huppertz HI, Russmann H, et al. Intracellular persistence of Borrelia burgdorferi in human synovial cells. Rheumatol Int 1996;16:125-32
41. Klempner MS, Noring R, Rogers RA. Invasion of human skin fibroblasts by the Lyme disease spirochete, Borrelia burgdorferi. J Infect Dis 1993;167:1074-81
42. Liang FT, Jacobs MB, Bowers LC, et al. An immune evasion mechanism for spirochetal persistence in Lyme borreliosis. J Exp Med 2002;195:415-22
43. Bubeck-Martinez S. Immune evasion of the Lyme disease spirochetes. Front Biosci 2005;10:873-78
44. Kraiczy P, Skerka C, Kirschfink M, et al. Immune evasion of Borrelia burgdorferi: insufficient killing of the pathogens by complement and antibody. Int J Med Microbiol 2002;291(suppl 33):141-46
45. Wolk K, Kunz S, Crompton NE, et al. Multiple mechanisms of reduced major histocompatibility complex class II expression in endotoxin tolerance. J Biol Chem 2003;278:18030-36
46. Jasinski M, Wieckiewicz J, Ruggiero I, et al. Isotype-specific regulation of MHC class II gene expression in human monocytes by exogenous and endogenous tumor necrosis factor. J Clin Immunol 1995;15:185-93
47. Kowalczyk D, Mytar B, Jasinski M, et al. Modulation of monocyte antigen-presenting capacity by tumour necrosis factor-alpha (TNF): Opposing effects of exogenous TNF before and after an antigen pulse and the role of TNF gene activation in monocytes. Immunol Lett 1995;44:51-57
48. Pashenkov M, Teleshova N, Kouwenhoven M, et al. Recruitment of dendritic cells to the cerebrospinal fluid in bacterial neuroinfections. J Neuroimmunol 2002;122:106-16
49. Imitola J, Raddassi K, Park KI, et al. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A 2004;101:18117-22
50. Dziembowska M, Tham TN, Lau P, et al. A role for CXCR4 signaling in survival and migration of neural and oligodendrocyte precursors. Glia 2005;50:258-69
51. Segal BM, Logigian EL. Sublime diagnosis of Lyme neuroborreliosis. Neurology 2005;65:351-52
52. Rupprecht TA, Pfister HW, Angele B, et al. The chemokine CXCL13 (BLC): A putative diagnostic marker for neuroborreliosis. Neurology 2005;65:448-50
53. Pachner AR, Amemiya K, Delaney E, et al. Interleukin-6 is expressed at high levels in the CNS in Lyme neuroborreliosis. Neurology 1997;49:147-52
54. Fischer HG, Bonifas U, Reichmann G. Phenotype and functions of brain dendritic cells emerging during chronic infection of mice with Toxoplasma gondii. J Immunol 2000;164:4826-34
55. Fischer HG, Reichmann G. Brain dendritic cells and macrophages/microglia in central nervous system inflammation. J Immunol 2001;166:2717-26
56. O'Doherty U, Ignatius R, Bhardwaj N, et al. Generation of monocyte-derived dendritic cells from precursors in rhesus macaque blood. J Immunol Methods 1997;207:185-94
57. Kokkinopoulos I, Jordan WJ, Ritter MA. Toll-like receptor mRNA expression patterns in human dendritic cells and monocytes. Mol Immunol 2005;42:957-68
58. Suhonen J, Komi J, Soukka J, et al. Interaction between Borrelia burgdorferi and immature human dendritic cells. Scand J Immunol 2003;58:67-75