MyD88 expression by CNS-resident cells is pivotal for eliciting protective immunity in brain abscesses

ASN Neuro

Volumn 1, Issue 2, 2009, Pages 77-90

  Garg, Sarita ^a   Nichols, Jessica R ^b   Esen, Nilufer ^c   Liu, Shuliang ^d   Phulwani, Nirmal K ^d   Syed, Mohsin Md ^d   Wood, William H ^e   Zhang, Yongqing ^e   Becker, Kevin G ^e   Aldrich, Amy ^f   Kielian, Tammy ^f  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b ARKANSAS CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^e NATIONAL INSTITUTE ON AGING   (United States)

^f UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Bone marrow chimaera mice; Brain abscess; Central nervous system; MyD88; Staphylococcus aureus; Toll like receptor

Indexed keywords

MYELOID DIFFERENTIATION FACTOR 88;

APOPTOSIS; ARTICLE; BODY BURDEN; BONE MARROW CELL; BRAIN ABSCESS; BRAIN CELL; BRAIN INFECTION; BRAIN PROTECTION; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM; CHIMERA; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; MACROPHAGE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NUCLEOTIDE SEQUENCE; STAPHYLOCOCCUS INFECTION; WILD TYPE;

EID: 70449519526     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1042/AN20090004     Document Type: Article

References (77)

1. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9:143-150.
2. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10:1538-1543.
3. Akira S (2006) TLR signaling. Curr Top Microbiol Immunol 311:1-16.
4. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783-801.
5. Arlt A, Vorndamm J, Breitenbroich M, Folsch UR, Kalthoff H, Schmidt WE, Schafer H (2001) Inhibition of NF-κB sensitizes human pancreatic carcinoma cells to apoptosis induced by etoposide (VP16) or doxorubicin. Oncogene 20:859-868.
6. Arlt A, Rosenstiel P, Kruse ML, Grohmann F, Minkenberg J, Perkins ND, Folsch UR, Schreiber S, Schafer H (2008) IEX-1 directly interferes with RelA/p65 dependent transactivation and regulation of apoptosis. Biochim Biophys Acta 1783:941-952.
7. Baldwin AC, Kielian T (2004) Persistent immune activation associated with a mouse model of Staphylococcus aureus-induced experimental brain abscess. J Neuroimmunol 151:24-32.
8. Becher B, Durell BG, Miga AV, Hickey WF, Noelle RJ (2001) The clinical course of experimental autoimmune encephalomyelitis and inflammation is controlled by the expression of CD40 within the central nervous system. J Exp Med 193:967-974.
9. Bechmann I, Kwidzinski E, Kovac AD, Simburger E, Horvath T, Gimsa U, Dirnagl U, Priller J, Nitsch R (2001) Turnover of rat brain perivascular cells. Exp Neurol 168:242-249.
10. Belka C, Budach W, Kortmann RD, Bamberg M (2001) Radiation induced CNS toxicity: molecular and cellular mechanisms. Br J Cancer 85:1233-1239.
11. Burns K, Martinon F, Esslinger C, Pahl H, Schneider P, Bodmer JL, Di Marco F, French L, Tschopp J (1998) MyD88, an adapter protein involved in interleukin-1 signaling. J Biol Chem 273:12203-12209.
12. Byram SC, Carson MJ, DeBoy CA, Serpe CJ, Sanders VM, Jones KJ (2004) CD4-positive T cell-mediated neuroprotection requires dual compartment antigen presentation. J Neurosci 24:4333-4339.
13. Carpenter J, Stapleton S, Holliman R (2007) Retrospective analysis of 49 cases of brain abscess and review of the literature. Eur J Clin Microbiol Infect Dis 26:1-11.
14. Chakravarty S, Herkenham M (2005) Toll-like receptor 4 on nonhematopoietic cells sustains CNS inflammation during endotoxemia, independent of systemic cytokines. J Neurosci 25:1788-1796.
15. Cheadle C, Vawter MP, Freed WJ, Becker KG (2003) Analysis of microarray data using Z score transformation. J Mol Diagn 5:73-81.
16. Cirl C, Wieser A, Yadav M, Duerr S, Schubert S, Fischer H, Stappert D, Wantia N, Rodriguez N, Wagner H, Svanborg C, Miethke T (2008) Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/ interleukin-1 receptor domain-containing proteins. Nat Med 14:399-406.
17. Davoust N, Vuaillat C, Androdias G, Nataf S (2008) From bone marrow to microglia: barriers and avenues. Trends Immunol 29:227-234.
18. Densen P, Weiler JM, Griffiss JM, Hoffmann LG (1987) Familial properdin deficiency and fatal meningococcemia. Correction of the bactericidal defect by vaccination. N Engl J Med 316:922-926.
19. Devireddy LR, Teodoro JG, Richard FA, Green MR (2001) Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by IL-3 deprivation. Science 293:829-834.
20. Dimitriou ID, Clemenza L, Scotter AJ, Chen G, Guerra FM, Rottapel R (2008) Putting out the fire: coordinated suppression of the innate and adaptive immune systems by SOCS1 and SOCS3 proteins. Immunol Rev 224:265-283.
21. Diserbo M, Agin A, Lamproglou I, Mauris J, Staali F, Multon E, Amourette C (2002) Blood-brain barrier permeability after gamma whole-body irradiation: an in vivo microdialysis study. Can J Physiol Pharmacol 80:670-678.
22. Domachowske JB, Bonville CA, Mortelliti AJ, Colella CB, Kim U, Rosenberg HF (2000) Respiratory syncytial virus infection induces expression of the anti-apoptosis gene IEX-1L in human respiratory epithelial cells. J Infect Dis 181:824-830.
23. Draper DW, Bethea HN, He YW (2006) Toll-like receptor 2-dependent and -independent activation of macrophages by group B streptococci. Immunol Lett 102:202-214.
24. Ehlting C, Lai WS, Schaper F, Brenndorfer ED, Matthes RJ, Heinrich PC, Ludwig S, Blackshear PJ, Gaestel M, Haussinger D, Bode JG (2007) Regulation of suppressor of cytokine signaling 3 (SOCS3) mRNA stability by TNF-α involves activation of the MKK6/p38MAPK/MK2 cascade. J Immunol 178:2813-2826.
25. Emonts M, Hazelzet JA, de Groot R, Hermans PW (2003) Host genetic determinants of Neisseria meningitidis infections. Lancet Infect Dis 3:565-577.
26. Esen N, Kielian T (2006) Central role for MyD88 in the responses of microglia to pathogen-associated molecular patterns. J Immunol 176:6802-6811.
27. Esen N, Tanga FY, DeLeo JA, Kielian T (2004) Toll-like receptor 2 (TLR2) mediates astrocyte activation in response to the Gram-positive bacterium Staphylococcus aureus. J Neurochem 88:746-758.
28. Flaris NA, Hickey WF (1992) Development and characterization of an experimental model of brain abscess in the rat. Am J Pathol 141:1299-1307.
29. Fremond CM, Yeremeev V, Nicolle DM, Jacobs M, Quesniaux VF, Ryffel B (2004) Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J Clin Invest 114:1790-1799.
30. Fremond CM, Togbe D, Doz E, Rose S, Vasseur V, Maillet I, Jacobs M, Ryffel B, Quesniaux VF (2007) IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J Immunol 179:1178-1189.
31. Garcia J, Ye Y, Arranz V, Letourneux C, Pezeron G, Porteu F (2002) IEX-1: a new ERK substrate involved in both ERK survival activity and ERK activation. EMBO J 21:5151-5163.
32. Hassan-Zahraee M, Tran EH, Bourbonniere L, Owens T (2000) Elevated interferon-γ in CNS inflammatory disease: a potential complication for bone marrow reconstitution in MS. J Neuroimmunol 108:40-44.
33. Hickey WF, Kimura H (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239:290-292.
34. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S (1999) Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11:115-122.
35. Kemper C, Hourcade DE (2008) Properdin: new roles in pattern recognition and target clearance. Mol Immunol 45:4048-4056.
36. Kielian T (2004) Immunopathogenesis of brain abscess. J Neuroinflammation 1:16.
37. Kielian T, Barry B, Hickey WF (2001) CXC chemokine receptor-2 ligands are required for neutrophil-mediated host defense in experimental brain abscesses. J Immunol 166:4634-4643.
38. Kielian T, Bearden ED, Baldwin AC, Esen N. 2004a. IL-1 and TNF-α play a pivotal role in the host immune response in a mouse model of Staphylococcus aureus-induced experimental brain abscess. J Neuropathol Exp Neurol 63:381-396.
39. Kielian T, McMahon M, Bearden ED, Baldwin AC, Drew PD, Esen N. 2004b. S. aureus-dependent microglial activation is selectively attenuated by the cyclopentenone prostaglandin 15-deoxy-Delta12,14- prostaglandin J2 (15d-PGJ2). J Neurochem 90:1163-1172.
40. Kielian T, Haney A, Mayes PM, Garg S, Esen N (2005) Toll-like receptor 2 modulates the proinflammatory milieu in Staphylococcus aureus-induced brain abscess. Infect Immun 73:7428-7435.
41. Kielian T, Phulwani NK, Esen N, Syed MM, Haney AC, McCastlain K, Johnson J (2007) MyD88-dependent signals are essential for the host immune response in experimental brain abscess. J Immunol 178:4528-4537.
42. Kielian T, Syed MMd, Liu S, Phillips N, Wagoner G, Drew PD, Esen N. (2008) The synthetic PPAR-c agonist ciglitazone attenuates neuroinflammation and accelerates encapsulation in bacterial brain abscesses. J Immunol 180:5004-5016.
43. Kjeldsen L, Johnsen AH, Sengelov H, Borregaard N (1993) Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 268:10425-10432.
44. Koedel U, Rupprecht T, Angele B, Heesemann J, Wagner H, Pfister HW, Kirschning CJ (2004) MyD88 is required for mounting a robust host immune response to Streptococcus pneumoniae in the CNS. Brain 127:1437-1445.
45. Lee S, Lee J, Kim S, Park JY, Lee WH, Mori K, Kim SH, Kim IK, Suk K (2007) A dual role of lipocalin 2 in the apoptosis and deramification of activated microglia. J Immunol 179:3231-3241.
46. Li ZW, Chu W, Hu Y, Delhase M, Deerinck T, Ellisman M, Johnson R, Karin M (1999) The IKKβ subunit of IκB kinase (IKK) is essential for nuclear factor βB activation and prevention of apoptosis. J Exp Med 189:1839-1845.
47. Li YQ, Chen P, Jain V, Reilly RM, Wong CS (2004) Early radiation-induced endothelial cell loss and blood-spinal cord barrier breakdown in the rat spinal cord. Radiat Res 161:143-152.
48. Linard C, Marquette C, Mathieu J, Pennequin A, Clarencon D, Mathe D (2004) Acute induction of inflammatory cytokine expression after gammairradiation in the rat: effect of an NF-βB inhibitor. Int J Radiat Oncol Biol Phys 58:427-434.
49. Liu Y, Stewart KN, Bishop E, Marek CJ, Kluth DC, Rees AJ, Wilson HM (2008) Unique expression of suppressor of cytokine signaling 3 is essential for classical macrophage activation in rodents in vitro and in vivo. J Immunol 180:6270-6278.
50. Mathisen GE, Johnson JP (1997) Brain abscess. Clin Infect Dis 25:763-779; quiz 780-761.
51. McClelland CJ, Craig BF, Crockard HA (1978) Brain abscesses in Northern Ireland: a 30 year community review. J Neurol Neurosurg Psychiatry 41:1043-1047.
52. Medzhitov R, Janeway Jr CA (2002) Decoding the patterns of self and nonself by the innate immune system. Science 296:298-300.
53. Medzhitov R, Preston-Hurlburt P, Kopp E, Stadlen A, Chen C, Ghosh S, Janeway Jr CA (1998) MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 2:253-258.
54. + monocytes only under defined host conditions. Nat Neurosci 10:1544-1553.
55. Miller LS, O'Connell RM, Gutierrez MA, Pietras EM, Shahangian A, Gross CE, Thirumala A, Cheung AL, Cheng G, Modlin RL (2006) MyD88 mediates neutrophil recruitment initiated by IL-1R but not TLR2 activation in immunity against Staphylococcus aureus. Immunity 24:79-91.
56. Mittal A, Papa S, Franzoso G, Sen R (2006) NF-kappaB-dependent regulation of the timing of activation-induced cell death of T lymphocytes. J Immunol 176:2183-2189.
57. O'Neill LA, Bowie AG (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7:353-364.
58. Osawa Y, Nagaki M, Banno Y, Brenner DA, Nozawa Y, Moriwaki H, Nakashima S (2003) Expression of the NF-κB target gene X-ray-inducible immediate early response factor-1 short enhances TNF-α-induced hepatocyte apoptosis by inhibiting Akt activation. J Immunol 170:4053-4060.
59. Pietzsch A, Buchler C, Aslanidis C, Schmitz G (1997) Identification and characterization of a novel monocyte/macrophage differentiationdependent gene that is responsive to lipopolysaccharide, ceramide, and lysophosphatidylcholine. Biochem Biophys Res Commun 235:4-9.
60. Schilling D, Pittelkow MR, Kumar R (2001) IEX-1, an immediate early gene, increases the rate of apoptosis in keratinocytes. Oncogene 20:7992-7997.
61. Schliamser SE, Backman K, Norrby SR (1988) Intracranial abscesses in adults: an analysis of 54 consecutive cases. Scand J Infect Dis 20:1-9.
62. Schwaeble W, Huemer HP, Most J, Dierich MP, Strobel M, Claus C, Reid KB, Ziegler-Heitbrock HW (1994) Expression of properdin in human monocytes. Eur J Biochem 219:759-764.
63. Shen L, Guo J, Santos-Berrios C, Wu MX (2006) Distinct domains for anti- and pro-apoptotic activities of IEX-1. J Biol Chem 281:15304-15311.
64. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S (2006) Bone marrowderived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49:489-502.
65. Stenzel W, Soltek S, Miletic H, Hermann MM, Korner H, Sedgwick JD, Schluter D, Deckert M (2005) An essential role for tumor necrosis factor in the formation of experimental murine Staphylococcus aureus-induced brain abscess and clearance. J Neuropathol Exp Neurol 64:27-36.
66. Takeuchi O, Hoshino K, Akira S (2000) Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J Immunol 165:5392-5396.
67. Tanga FY, Nutile-McMenemy N, DeLeo JA (2005) The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc Natl Acad Sci USA 102:5856-5861.
68. Tenney JH (1986) Bacterial infections of the central nervous system in neurosurgery. Neurol Clin 4:91-114.
69. Tong Z, Wu X, Ovcharenko D, Zhu J, Chen CS, Kehrer JP (2005) Neutrophil gelatinase-associated lipocalin as a survival factor. Biochem J 391:441-448.
70. Trinchieri G, Sher A (2007) Cooperation of Toll-like receptor signals in innate immune defence. Nat Rev Immunol 7:179-190.
71. Turrin NP, Plante MM, Lessard M, Rivest S (2007) Irradiation does not compromise or exacerbate the innate immune response in the brains of mice that were transplanted with bone marrow stem cells. Stem Cells 25:3165-3172.
72. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121.
73. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM (1996) Suppression of TNF-α-induced apoptosis by NF-κB. Science 274:787-789.
74. Wesche H, Henzel WJ, Shillinglaw W, Li S, Cao Z (1997) MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7:837-847.
75. Wirthmueller U, Dewald B, Thelen M, Schafer MK, Stover C, Whaley K, North J, Eggleton P, Reid KB, Schwaeble WJ (1997) Properdin, a positive regulator of complement activation, is released from secondary granules of stimulated peripheral blood neutrophils. J Immunol 158:4444-4451.
76. Wu MX, Ao Z, Prasad KV, Wu R, Schlossman SF (1998) IEX-1L, an apoptosis inhibitor involved in NF-κB-mediated cell survival. Science 281:998-1001.
77. Zehntner SP, Bourbonniere L, Hassan-Zahraee M, Tran E, Owens T (2004) Bone marrow-derived versus parenchymal sources of inducible nitric oxide synthase in experimental autoimmune encephalomyelitis. J Neuroimmunol 150:70-79.