Innate immune response gene expression profiles of N9 microglia are pathogen-type specific

Journal of Neuroimmunology

Volumn 175, Issue 1-2, 2006, Pages 128-141

  McKimmie, Clive S ^a   Roy, Douglas ^a   Forster, Thorsten ^a   Fazakerley, John K ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; LECTIN; LIPOPOLYSACCHARIDE; SCAVENGER RECEPTOR; TOLL LIKE RECEPTOR;

ARTICLE; GENE EXPRESSION; INNATE IMMUNITY; MICROARRAY ANALYSIS; MICROGLIA; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ALPHAVIRUS INFECTIONS; ANIMALS; CELLS, CULTURED; EPITOPES; GENE EXPRESSION PROFILING; IMMUNITY, NATURAL; MICE; MICROGLIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, PATTERN RECOGNITION; SEMLIKI FOREST VIRUS;

EID: 33646813652     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2006.03.012     Document Type: Article

References (77)

1. Akira S., and Takeda K. Toll-like receptor signalling. Nat. Rev., Immunol. 4 (2004) 499-511
2. Alarcon R., Fuenzalida C., Santibanez M., and von Bernhardi R. Expression of scavenger receptors in glial cells. Comparing the adhesion of astrocytes and microglia from neonatal rats to surface-bound beta-amyloid. J. Biol. Chem. 280 (2005) 30406-30415
3. Amor S., Scallan M.F., Morris M.M., Dyson H., and Fazakerley J.K. Role of immune responses in protection and pathogenesis during Semliki Forest virus encephalitis. J. Gen. Virol. 77 Pt. 2 (1996) 281-291
4. Ashkenas J., Penman M., Vasile E., Acton S., Freeman M., and Krieger M. Structures and high and low affinity ligand binding properties of murine type I and type II macrophage scavenger receptors. J. Lipid Res. 34 (1993) 983-1000
5. Bakker A.B., Baker E., Sutherland G.R., Phillips J.H., and Lanier L.L. Myeloid DAP12-associating lectin (MDL)-1 is a cell surface receptor involved in the activation of myeloid cells. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 9792-9796
6. Bate C., Veerhuis R., Eikelenboom P., and Williams A. Microglia kill amyloid-beta1-42 damaged neurons by a CD14-dependent process. NeuroReport 15 (2004) 1427-1430
7. Bouchon A., Hernandez-Munain C., Cella M., and Colonna M. A DAP12-mediated pathway regulates expression of CC chemokine receptor 7 and maturation of human dendritic cells. J. Exp. Med. 194 (2001) 1111-1122
8. Brown A.R., Webb J., Rebus S., Walker R., Williams A., and Fazakerley J.K. Inducible cytokine gene expression in the brain in the ME7/CV mouse model of scrapie is highly restricted, is at a strikingly low level relative to the degree of gliosis and occurs only late in disease. J. Gen. Virol. 84 (2003) 2605-2611
9. Buechler C., Ritter M., Quoc C.D., Agildere A., and Schmitz G. Lipopolysaccharide inhibits the expression of the scavenger receptor Cla-1 in human monocytes and macrophages. Biochem. Biophys. Res. Commun. 262 (1999) 251-254
10. Carson M.J. Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis. Glia 40 (2002) 218-231
11. Carson M.J., Reilly C.R., Sutcliffe J.G., and Lo D. Mature microglia resemble immature antigen-presenting cells. Glia 22 (1998) 72-85
12. Chen K., Iribarren P., Hu J., Chen J., Gong W., Cho E.H., Lockett S., Dunlop N.M., and Wang J.M. Activation of Toll-like receptor 2 on microglia promotes cell uptake of Alzheimer disease-associated amyloid beta peptide. J. Biol. Chem. 281 (2006) 3651-3659
13. Coraci I.S., Husemann J., Berman J.W., Hulette C., Dufour J.H., Campanella G.K., Luster A.D., Silverstein S.C., and El Khoury J.B. CD36, a class B scavenger receptor, is expressed on microglia in Alzheimer's disease brains and can mediate production of reactive oxygen species in response to beta-amyloid fibrils. Am. J. Pathol. 160 (2002) 101-112
14. D'Aversa T.G., Weidenheim K.M., and Berman J.W. CD40-CD40L interactions induce chemokine expression by human microglia: implications for human immunodeficiency virus encephalitis and multiple sclerosis. Am. J. Pathol. 160 (2002) 559-567
15. Dziarski R. Peptidoglycan recognition proteins (PGRPs). Mol. Immunol. 40 (2004) 877-886
16. Dziarski R., Platt K.A., Gelius E., Steiner H., and Gupta D. Defect in neutrophil killing and increased susceptibility to infection with nonpathogenic gram-positive bacteria in peptidoglycan recognition protein-S (PGRP-S)-deficient mice. Blood 102 (2003) 689-697
17. Ebrahimi B., Dutia B.M., Roberts K.L., Garcia-Ramirez J.J., Dickinson P., Stewart J.P., Ghazal P., Roy D.J., and Nash A.A. Transcriptome profile of murine gammaherpesvirus-68 lytic infection. J. Gen. Virol. 84 (2003) 99-109
18. El Khoury J., Hickman S.E., Thomas C.A., Cao L., Silverstein S.C., and Loike J.D. Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature 382 (1996) 716-719
19. El Khoury J.B., Moore K.J., Means T.K., Leung J., Terada K., Toft M., Freeman M.W., and Luster A.D. CD36 mediates the innate host response to beta-amyloid. J. Exp. Med. 197 (2003) 1657-1666
20. Fazakerley J.K. Pathogenesis of Semliki Forest virus encephalitis. J. Neurovirology 8 Suppl. 2 (2002) 66-74
21. Febbraio M., Hajjar D.P., and Silverstein R.L. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J. Clin. Invest. 108 (2001) 785-791
22. Ferrari D., Villalba M., Chiozzi P., Falzoni S., Ricciardi-Castagnoli P., and Di Virgilio F. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J. Immunol. 156 (1996) 1531-1539
23. Forster T., Roy D., and Ghazal P. Experiments using microarray technology: limitations and standard operating procedures. J. Endocrinol. 178 (2003) 195-204
24. Franc N.C., White K., and Ezekowitz R.A. Phagocytosis and development: back to the future. Curr. Opin. Immunol. 11 (1999) 47-52
25. Gordon S. Pattern recognition receptors: doubling up for the innate immune response. Cell 111 (2002) 927-930
26. Grewal R.P., Yoshida T., Finch C.E., and Morgan T.E. Scavenger receptor mRNAs in rat brain microglia are induced by kainic acid lesioning and by cytokines. NeuroReport 8 (1997) 1077-1081
27. Hampton R.Y., Golenbock D.T., Penman M., Krieger M., and Raetz C.R. Recognition and plasma clearance of endotoxin by scavenger receptors. Nature 352 (1991) 342-344
28. Hanisch U.K. Microglia as a source and target of cytokines. Glia 40 (2002) 140-155
29. Hirano K., Yamashita S., Nakagawa Y., Ohya T., Matsuura F., Tsukamoto K., Okamoto Y., Matsuyama A., Matsumoto K., Miyagawa J., and Matsuzawa Y. Expression of human scavenger receptor class B type I in cultured human monocyte-derived macrophages and atherosclerotic lesions. Circ. Res. 85 (1999) 108-116
30. Ho Y.S., Xiong Y., Ma W., Spector A., and Ho D.S. Mice lacking catalase develop normally but show differential sensitivity to oxidant tissue injury. J. Biol. Chem. 279 (2004) 32804-32812
31. Honda M., Akiyama H., Yamada Y., Kondo H., Kawabe Y., Takeya M., Takahashi K., Suzuki H., Doi T., Sakamoto A., Ookawara S., Mato M., Gough P.J., Greaves D.R., Gordon S., Kodama T., and Matsushita M. Immunohistochemical evidence for a macrophage scavenger receptor in Mato cells and reactive microglia of ischemia and Alzheimer's disease. Biochem. Biophys. Res. Commun. 245 (1998) 734-740
32. Howard L.M., Miga A.J., Vanderlugt C.L., Dal Canto M.C., Laman J.D., Noelle R.J., and Miller S.D. Mechanisms of immunotherapeutic intervention by anti-CD40L (CD154) antibody in an animal model of multiple sclerosis. J. Clin. Invest. 103 (1999) 281-290
33. Huang Q., Liu D., Majewski P., Schulte L.C., Korn J.M., Young R.A., Lander E.S., and Hacohen N. The plasticity of dendritic cell responses to pathogens and their components. Science 294 (2001) 870-875
34. Husemann J., Loike J.D., Kodama T., and Silverstein S.C. Scavenger receptor class B type I (SR-BI) mediates adhesion of neonatal murine microglia to fibrillar beta-amyloid. J. Neuroimmunol. 114 (2001) 142-150
35. Husemann J., Loike J.D., Anankov R., Febbraio M., and Silverstein S.C. Scavenger receptors in neurobiology and neuropathology: their role on microglia and other cells of the nervous system. Glia 40 (2002) 195-205
36. Jana M., Liu X., Koka S., Ghosh S., Petro T.M., and Pahan K. Ligation of CD40 stimulates the induction of nitric-oxide synthase in microglial cells. J. Biol. Chem. 276 (2001) 44527-44533
37. Jenner R.G., and Young R.A. Insights into host responses against pathogens from transcriptional profiling. Nat. Rev., Microbiol. 3 (2005) 281-294
38. Kadowaki N., Ho S., Antonenko S., Malefyt R.W., Kastelein R.A., Bazan F., and Liu Y.J. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194 (2001) 863-869
39. Kane M.D., Jatkoe T.A., Stumpf C.R., Lu J., Thomas J.D., and Madore S.J. Assessment of the sensitivity and specificity of oligonucleotide (50mer) microarrays. Nucleic Acids Res. 28 (2000) 4552-4557
40. Kielian T. Microglia and chemokines in infectious diseases of the nervous system: views and reviews. Front. Biosci. 9 (2004) 732-750
41. Krieger M. Charting the fate of the "good cholesterol": identification and characterization of the high-density lipoprotein receptor SR-BI. Annu. Rev. Biochem. 68 (1999) 523-558
42. Krieger M., and Stern D.M. Series introduction: multiligand receptors and human disease. J. Clin. Invest. 108 (2001) 645-647
43. Mack C.L., Vanderlugt-Castaneda C.L., Neville K.L., and Miller S.D. Microglia are activated to become competent antigen presenting and effector cells in the inflammatory environment of the Theiler's virus model of multiple sclerosis. J. Neuroimmunol. 144 (2003) 68-79
44. Matsumoto M., Tanaka T., Kaisho T., Sanjo H., Copeland N.G., Gilbert D.J., Jenkins N.A., and Akira S. A novel LPS-inducible C-type lectin is a transcriptional target of NF-IL6 in macrophages. J. Immunol. 163 (1999) 5039-5048
45. McKimmie C.S., and Fazakerley J.K. In response to pathogens, glial cells dynamically and differentially regulate Toll-like receptor gene expression. J. Neuroimmunol. 169 (2005) 116-125
46. McKimmie C.S., Johnson N., Fooks A.R., and Fazakerley J.K. Viruses selectively upregulate Toll-like receptors in the central nervous system. Biochem. Biophys. Res. Commun. 336 (2005) 925-933
47. Meda L., Cassatella M.A., Szendrei G.I., Otvos Jr. L., Baron P., Villalba M., Ferrari D., and Rossi F. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374 (1995) 647-650
48. Moller T., Nolte C., Burger R., Verkhratsky A., and Kettenmann H. Mechanisms of C5a and C3a complement fragment-induced [Ca2+]i signaling in mouse microglia. J. Neurosci. 17 (1997) 615-624
49. Mukhopadhyay S., Peiser L., and Gordon S. Activation of murine macrophages by Neisseria meningitidis and IFN-{gamma} in vitro: distinct roles of class A scavenger and Toll-like pattern recognition receptors in selective modulation of surface phenotype. J. Leukoc. Biol. (2004)
50. Muller U., Steinhoff U., Reis L.F., Hemmi S., Pavlovic J., Zinkernagel R.M., and Aguet M. Functional role of type I and type II interferons in antiviral defense. Science 264 (1994) 1918-1921
51. Nakamura K., Funakoshi H., Miyamoto K., Tokunaga F., and Nakamura T. Molecular cloning and functional characterization of a human scavenger receptor with C-type lectin (SRCL), a novel member of a scavenger receptor family. Biochem. Biophys. Res. Commun. 280 (2001) 1028-1035
52. Napolitani G., Rinaldi A., Bertoni F., Sallusto F., and Lanzavecchia A. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 6 (2005) 769-776
53. Nystrom K., Biller M., Grahn A., Lindh M., Larson G., and Olofsson S. Real time PCR for monitoring regulation of host gene expression in herpes simplex virus type 1-infected human diploid cells. J. Virol. Methods 118 (2004) 83-94
54. Okuno T., Nakatsuji Y., Kumanogoh A., Koguchi K., Moriya M., Fujimura H., Kikutani H., and Sakoda S. Induction of cyclooxygenase-2 in reactive glial cells by the CD40 pathway: relevance to amyotrophic lateral sclerosis. J. Neurochem. 91 (2004) 404-412
55. Olson J.K., and Miller S.D. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J. Immunol. 173 (2004) 3916-3924
56. Olson J.K., Girvin A.M., and Miller S.D. Direct activation of innate and antigen-presenting functions of microglia following infection with Theiler's virus. J. Virol. 75 (2001) 9780-9789
57. Paglinawan R., Malipiero U., Schlapbach R., Frei K., Reith W., and Fontana A. TGFbeta directs gene expression of activated microglia to an anti-inflammatory phenotype strongly focusing on chemokine genes and cell migratory genes. Glia 44 (2003) 219-231
58. Palecanda A., Paulauskis J., Al Mutairi E., Imrich A., Qin G., Suzuki H., Kodama T., Tryggvason K., Koziel H., and Kobzik L. Role of the scavenger receptor MARCO in alveolar macrophage binding of unopsonized environmental particles. J. Exp. Med. 189 (1999) 1497-1506
59. Peress N.S., Fleit H.B., Perillo E., Kuljis R., and Pezzullo C. Identification of Fc gamma RI, II and III on normal human brain ramified microglia and on microglia in senile plaques in Alzheimer's disease. J. Neuroimmunol. 48 (1993) 71-79
60. Qi H., Denning T.L., and Soong L. Differential induction of interleukin-10 and interleukin-12 in dendritic cells by microbial toll-like receptor activators and skewing of T-cell cytokine profiles. Infect. Immun. 71 (2003) 3337-3342
61. Re F., and Strominger J.L. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells. J. Biol. Chem. 276 (2001) 37692-37699
62. Rempel J.D., Quina L.A., Blakely-Gonzales P.K., Buchmeier M.J., and Gruol D.L. Viral induction of central nervous system innate immune responses. J. Virol. 79 (2005) 4369-4381
63. Reverter A., McWilliam S.M., Barris W., and Dalrymple B.P. A rapid method for computationally inferring transcriptome coverage and microarray sensitivity. Bioinformatics 21 (2005) 80-89
64. Righi M., Mori L., De Libero G., Sironi M., Biondi A., Mantovani A., Donini S.D., and Ricciardi-Castagnoli P. Monokine production by microglial cell clones. Eur. J. Immunol. 19 (1989) 1443-1448
65. Savill J., Dransfield I., Gregory C., and Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev., Immunol. 2 (2002) 965-975
66. Scallan M.F., Allsopp T.E., and Fazakerley J.K. bcl-2 acts early to restrict Semliki Forest virus replication and delays virus-induced programmed cell death. J. Virol. 71 (1997) 1583-1590
67. Schmid C.D., Sautkulis L.N., Danielson P.E., Cooper J., Hasel K.W., Hilbush B.S., Sutcliffe J.G., and Carson M.J. Heterogeneous expression of the triggering receptor expressed on myeloid cells-2 on adult murine microglia. J. Neurochem. 83 (2002) 1309-1320
68. Streit W.J. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40 (2002) 133-139
69. Tan J., Town T., Crawford F., Mori T., DelleDonne A., Crescentini R., Obregon D., Flavell R.A., and Mullan M.J. Role of CD40 ligand in amyloidosis in transgenic Alzheimer's mice. Nat. Neurosci. 5 (2002) 1288-1293
70. Tsunawaki S., Kagara S., Yoshikawa K., Yoshida L.S., Kuratsuji T., and Namiki H. Involvement of p40phox in activation of phagocyte NADPH oxidase through association of its carboxyl-terminal, but not its amino-terminal, with p67phox. J. Exp. Med. 184 (1996) 893-902
71. Tunaru S., Kero J., Schaub A., Wufka C., Blaukat A., Pfeffer K., and Offermanns S. PUMA-G and HM74 are receptors for nicotinic acid and mediate its anti-lipolytic effect. Nat. Med. 9 (2003) 352-355
72. van der Laan L.J., Dopp E.A., Haworth R., Pikkarainen T., Kangas M., Elomaa O., Dijkstra C.D., Gordon S., Tryggvason K., and Kraal G. Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J. Immunol. 162 (1999) 939-947
73. Wang T., Town T., Alexopoulou L., Anderson J.F., Fikrig E., and Flavell R.A. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med. 10 (2004) 1366-1373
74. Warrington J.A., Nair A., Mahadevappa M., and Tsyganskaya M. Comparison of human adult and fetal expression and identification of 535 housekeeping/maintenance genes. Physiol. Genomics 2 (2000) 143-147
75. Yamada Y., Doi T., Hamakubo T., and Kodama T. Scavenger receptor family proteins: roles for atherosclerosis, host defence and disorders of the central nervous system. Cell. Mol. Life Sci. 54 (1998) 628-640
76. Zarember K.A., and Godowski P.J. Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J. Immunol. 168 (2002) 554-561
77. Zelko I.N., Mariani T.J., and Folz R.J. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic. Biol. Med. 33 (2002) 337-349