Toll-like receptor (TLR) and inflammasome actions in the central nervous system

Trends in Immunology

Volumn 33, Issue 7, 2012, Pages 333-342

  Hanamsagar, Richa ^a   Hanke, Mark L ^b   Kielian, Tammy ^b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Bacterial meningitis; Brain abscess; IL 1 ; IL 18; Inflammasome; Microglia; Neurodegeneration; Toll like receptor

Indexed keywords

INFLAMMASOME; INTERLEUKIN 1; INTERLEUKIN 18; TOLL LIKE RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; ALZHEIMER DISEASE; AUTOIMMUNE DISEASE; BACTERIAL MENINGITIS; BRAIN ABSCESS; HUMAN; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; REVIEW; SPINAL CORD INJURY; STROKE; TRAUMATIC BRAIN INJURY;

ANIMALS; AUTOIMMUNITY; CENTRAL NERVOUS SYSTEM; HUMANS; INFLAMMASOMES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84862649049     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2012.03.001     Document Type: Review

References (106)

1. Greenwood J., et al. Review: leucocyte-endothelial cell crosstalk at the blood-brain barrier: a prerequisite for successful immune cell entry to the brain. Neuropathol. Appl. Neurobiol. 2011, 37:24-39.
2. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
3. Schroder K., Tschopp J. The inflammasomes. Cell 2010, 140:821-832.
4. Petrilli V., et al. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 2007, 14:1583-1589.
5. Dostert C., et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008, 320:674-677.
6. Craven R.R., et al. Staphylococcus aureus alpha-hemolysin activates the NLRP3-inflammasome in human and mouse monocytic cells. PLoS ONE 2009, 4:e7446.
7. Hornung V., et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 2008, 9:847-856.
8. Schroder K., et al. The NLRP3 inflammasome: a sensor for metabolic danger?. Science 2010, 327:296-300.
9. Martinon F., et al. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 2009, 27:229-265.
10. Kielian T. Toll-like receptors in central nervous system glial inflammation and homeostasis. J. Neurosci. Res. 2006, 83:711-730.
11. Lehnardt S. Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia 2010, 58:253-263.
12. Farina C., et al. Astrocytes are active players in cerebral innate immunity. Trends Immunol. 2007, 28:138-145.
13. Jha S., et al. The inflammasome sensor, NLRP3, regulates CNS inflammation and demyelination via caspase-1 and interleukin-18. J. Neurosci. 2010, 30:15811-15820.
14. Griffin W.S., Mrak R.E. Interleukin-1 in the genesis and progression of and risk for development of neuronal degeneration in Alzheimer's disease. J. Leukoc. Biol. 2002, 72:233-238.
15. Zwijnenburg P.J., et al. IL-1 receptor type 1 gene-deficient mice demonstrate an impaired host defense against pneumococcal meningitis. J. Immunol. 2003, 170:4724-4730.
16. Sutton C., et al. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J. Exp. Med. 2006, 203:1685-1691.
17. Gris D., et al. NLRP3 plays a critical role in the development of experimental autoimmune encephalomyelitis by mediating Th1 and Th17 responses. J. Immunol. 2010, 185:974-981.
18. Echchannaoui H., et al. Toll-like receptor 2-deficient mice are highly susceptible to Streptococcus pneumoniae meningitis because of reduced bacterial clearing and enhanced inflammation. J. Infect. Dis. 2002, 186:798-806.
19. Hoegen T., et al. The NLRP3 inflammasome contributes to brain injury in pneumococcal meningitis and is activated through ATP-dependent lysosomal cathepsin B release. J. Immunol. 2011, 187:5440-5451.
20. Koedel U., et al. Toll-like receptor 2 participates in mediation of immune response in experimental pneumococcal meningitis. J. Immunol. 2003, 170:438-444.
21. Klein M., et al. Innate immunity to pneumococcal infection of the central nervous system depends on toll-like receptor (TLR) 2 and TLR4. J. Infect. Dis. 2008, 198:1028-1036.
22. Koedel U., et al. MyD88 is required for mounting a robust host immune response to Streptococcus pneumoniae in the CNS. Brain 2004, 127:1437-1445.
23. Koedel U., et al. New understandings on the pathophysiology of bacterial meningitis. Curr. Opin. Infect. Dis. 2010, 23:217-223.
24. Kielian T., et al. 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. 2004, 63:381-396.
25. Kielian T., et al. MyD88-dependent signals are essential for the host immune response in experimental brain abscess. J. Immunol. 2007, 178:4528-4537.
26. Garg S., et al. MyD88 expression by CNS-resident cells is pivotal for eliciting protective immunity in brain abscesses. ASN Neuro 2009, 1:e0007. 10.1042/AN20090004.
27. Vidlak D., et al. Roles of Toll-like receptor 2 (TLR2) and superantigens on adaptive immune responses during CNS staphylococcal infection. Brain Behav. Immun. 2011, 25:905-914.
28. Kielian T., et al. Toll-like receptor 2 modulates the proinflammatory milieu in Staphylococcus aureus-induced brain abscess. Infect. Immun. 2005, 73:7428-7435.
29. Stenzel W., et al. Both TLR2 and TLR4 are required for the effective immune response in Staphylococcus aureus-induced experimental murine brain abscess. Am. J. Pathol. 2008, 172:132-145.
30. Koedel U., et al. Role of caspase-1 in experimental pneumococcal meningitis: evidence from pharmacologic caspase inhibition and caspase-1-deficient mice. Ann. Neurol. 2002, 51:319-329.
31. Kayagaki N., et al. Non-canonical inflammasome activation targets caspase-11. Nature 2011, 479:117-121.
32. Holley M.M., et al. Toll-like receptor 2 (TLR2)-TLR9 crosstalk dictates IL-12 family cytokine production in microglia. Glia 2012, 60:29-42.
33. Butchi N.B., et al. Interactions between TLR7 and TLR9 agonists and receptors regulate innate immune responses by astrocytes and microglia. Glia 2010, 58:650-664.
34. Hanamsagar R., et al. Inflammasome activation and IL-1β/IL-18 processing are influenced by distinct pathways in microglia. J. Neurochem. 2011, 119:736-748.
35. Gorina R., et al. Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling, MAPK, and Jak1/Stat1 pathways. Glia 2011, 59:242-255.
36. Bsibsi M., et al. Broad expression of Toll-like receptors in the human central nervous system. J. Neuropathol. Exp. Neurol. 2002, 61:1013-1021.
37. Saura J. Microglial cells in astroglial cultures: a cautionary note. J. Neuroinflamm. 2007, 4:26.
38. Holm T.H., et al. Microglia are required for astroglial Toll-like receptor 4 response and for optimal TLR2 and TLR3 response. Glia 2012, 60:630-638.
39. Liu S., Kielian T. MyD88 is pivotal for immune recognition of Citrobacter koseri and astrocyte activation during CNS infection. J. Neuroinflamm. 2011, 8:35.
40. Alboni S., et al. Interleukin 18 in the CNS. J. Neuroinflamm. 2010, 7:9.
41. Liu S., et al. TLR2 is a primary receptor for Alzheimer's amyloid β peptide to trigger neuroinflammatory activation. J. Immunol. 2012, 188:1098-1107.
42. Hao W., et al. Myeloid differentiation factor 88-deficient bone marrow cells improve Alzheimer's disease-related symptoms and pathology. Brain 2011, 134:278-292.
43. Ajami B., et al. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat. Neurosci. 2007, 10:1538-1543.
44. Ajami B., et al. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat. Neurosci. 2011, 14:1142-1149.
45. Lim J.E., et al. MyD88 deficiency ameliorates beta-amyloidosis in an animal model of Alzheimer's disease. Am. J. Pathol. 2011, 179:1095-1103.
46. Richard K.L., et al. Toll-like receptor 2 acts as a natural innate immune receptor to clear amyloid β 1-42 and delay the cognitive decline in a mouse model of Alzheimer's disease. J. Neurosci. 2008, 28:5784-5793.
47. Reed-Geaghan E.G., et al. CD14 and Toll-like receptors 2 and 4 are required for fibrillar A β-stimulated microglial activation. J. Neurosci. 2009, 29:11982-11992.
48. Van Der Putten C., et al. Statins amplify TLR-induced responses in microglia via inhibition of cholesterol biosynthesis. Glia 2012, 60:43-52.
49. Miranda-Hernandez S., et al. Role for MyD88, TLR2 and TLR9 but not TLR1, TLR4 or TLR6 in experimental autoimmune encephalomyelitis. J. Immunol. 2011, 187:791-804.
50. Prinz M., et al. Innate immunity mediated by TLR9 modulates pathogenicity in an animal model of multiple sclerosis. J. Clin. Invest. 2006, 116:456-464.
51. Salvetti M., et al. Epstein-Barr virus and multiple sclerosis. Curr. Opin. Neurol. 2009, 22:201-206.
52. Visser L., et al. Phagocytes containing a disease-promoting Toll-like receptor/Nod ligand are present in the brain during demyelinating disease in primates. Am. J. Pathol. 2006, 169:1671-1685.
53. Schrijver I.A., et al. Bacterial peptidoglycan and immune reactivity in the central nervous system in multiple sclerosis. Brain 2001, 124:1544-1554.
54. Marta M., et al. Unexpected regulatory roles of TLR4 and TLR9 in experimental autoimmune encephalomyelitis. Eur. J. Immunol. 2008, 38:565-575.
55. Li Q., et al. Endothelial IL-1R1 is a critical mediator of EAE pathogenesis. Brain Behav. Immun. 2011, 25:160-167.
56. Pineau I., et al. Astrocytes initiate inflammation in the injured mouse spinal cord by promoting the entry of neutrophils and inflammatory monocytes in an IL-1 receptor/MyD88-dependent fashion. Brain Behav. Immun. 2010, 24:540-553.
57. Kigerl K.A., et al. Toll-like receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J. Neurochem. 2007, 102:37-50.
58. Babcock A.A., et al. Signaling through MyD88 regulates leukocyte recruitment after brain injury. J. Immunol. 2008, 181:6481-6490.
59. Babcock A.A., et al. Toll-like receptor 2 signaling in response to brain injury: an innate bridge to neuroinflammation. J. Neurosci. 2006, 26:12826-12837.
60. Marsh B.J., et al. Toll-like receptor signaling in endogenous neuroprotection and stroke. Neuroscience 2009, 158:1007-1020.
61. Tang S.C., et al. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:13798-13803.
62. Halle A., et al. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat. Immunol. 2008, 9:857-865.
63. Shaftel S.S., et al. The role of interleukin-1 in neuroinflammation and Alzheimer disease: an evolving perspective. J. Neuroinflamm. 2008, 5:7.
64. Mawhinney L.J., et al. Heightened inflammasome activation is linked to age-related cognitive impairment in Fischer 344 rats. BMC Neurosci. 2011, 12:123.
65. Pontillo A., et al. NALP1/NLRP1 genetic variants are associated with Alzheimer disease. Alzheimer Dis. Assoc. Disord. 2012, in press.
66. Shaw P.J., et al. Critical role for PYCARD/ASC in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2010, 184:4610-4614.
67. de Jong B.A., et al. Production of IL-1β and IL-1Ra as risk factors for susceptibility and progression of relapse-onset multiple sclerosis. J. Neuroimmunol. 2002, 126:172-179.
68. Chung Y., et al. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 2009, 30:576-587.
69. Matsuki T., et al. Abnormal T cell activation caused by the imbalance of the IL-1/IL-1R antagonist system is responsible for the development of experimental autoimmune encephalomyelitis. Int. Immunol. 2006, 18:399-407.
70. Lalor S.J., et al. Caspase-1-processed cytokines IL-1beta and IL-18 promote IL-17 production by gamma delta and CD4 T cells that mediate autoimmunity. J. Immunol. 2011, 186:5738-5748.
71. Mason J.L., et al. Interleukin-1beta promotes repair of the CNS. J. Neurosci. 2001, 21:7046-7052.
72. de Rivero Vaccari J.P., et al. A molecular platform in neurons regulates inflammation after spinal cord injury. J. Neurosci. 2008, 28:3404-3414.
73. Faustin B., et al. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol. Cell 2007, 25:713-724.
74. Abulafia D.P., et al. Inhibition of the inflammasome complex reduces the inflammatory response after thromboembolic stroke in mice. J. Cereb. Blood Flow Metab. 2009, 29:534-544.
75. de Rivero Vaccari J.P., et al. Therapeutic neutralization of the NLRP1 inflammasome reduces the innate immune response and improves histopathology after traumatic brain injury. J. Cereb. Blood Flow Metab. 2009, 29:1251-1261.
76. Levine B., et al. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
77. Shi C.S., et al. Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 2012, 13:255-263.
78. Shimada K., et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 2012, 36:401-414.
79. Nakahira K., et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 2011, 12:222-230.
80. Zhou R., et al. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.
81. Schultz M.L., et al. Clarifying lysosomal storage diseases. Trends Neurosci. 2011, 34:401-410.
82. Kragh C.L., et al. Autophagy in dementias. Brain Pathol. 2012, 22:99-109.
83. Lim J.E., et al. MyD88 deficiency ameliorates beta-amyloidosis in an animal model of Alzheimer's disease. Am. J. Pathol. 2011, 179:1095-1103.
84. Silverman W.R., et al. The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J. Biol. Chem. 2009, 284:18143-18151.
85. Bauer C., et al. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut 2010, 59:1192-1199.
86. Zaki M.H., et al. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 2010, 32:379-391.
87. Nour A.M., et al. Anthrax lethal toxin triggers the formation of a membrane-associated inflammasome complex in murine macrophages. Infect. Immun. 2009, 77:1262-1271.
88. Barker B.R., et al. Cross-regulation between the IL-1β/IL-18 processing inflammasome and other inflammatory cytokines. Curr. Opin. Immunol. 2011, 23:591-597.
89. Duewell P., et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010, 464:1357-1361.
90. Martinon F., et al. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006, 440:237-241.
91. Maelfait J., et al. Stimulation of Toll-like receptor 3 and 4 induces interleukin-1β maturation by caspase-8. J. Exp. Med. 2008, 205:1967-1973.
92. Gringhuis S.I., et al. Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1β via a noncanonical caspase-8 inflammasome. Nat. Immunol. 2012, 13:246-254.
93. Taxman D.J., et al. The NLR adaptor ASC/PYCARD regulates DUSP10, mitogen-activated protein kinase (MAPK), and chemokine induction independent of the inflammasome. J. Biol. Chem. 2011, 286:19605-19616.
94. McElvania Tekippe E., et al. Granuloma formation and host defense in chronic Mycobacterium tuberculosis infection requires PYCARD/ASC but not NLRP3 or caspase-1. PLoS ONE 2010, 5:e12320.
95. Ippagunta S.K., et al. The inflammasome adaptor ASC regulates the function of adaptive immune cells by controlling Dock2-mediated Rac activation and actin polymerization. Nat. Immunol. 2011, 12:1010-1016.
96. Taxman D.J., et al. Cutting edge: ASC mediates the induction of multiple cytokines by Porphyromonas gingivalis via caspase-1-dependent and -independent pathways. J. Immunol. 2006, 177:4252-4256.
97. Ellebedy A.H., et al. Inflammasome-independent role of the apoptosis-associated speck-like protein containing CARD (ASC) in the adjuvant effect of MF59. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:2927-2932.
98. Kolly L., et al. Inflammatory role of ASC in antigen-induced arthritis is independent of caspase-1, NALP-3, and IPAF. J. Immunol. 2009, 183:4003-4012.
99. Ippagunta S.K., et al. Inflammasome-independent role of apoptosis-associated speck-like protein containing a CARD (ASC) in T cell priming is critical for collagen-induced arthritis. J. Biol. Chem. 2010, 285:12454-12462.
100. Esen N., Kielian T. Toll-like receptors in brain abscess. Curr. Top. Microbiol. Immunol. 2009, 336:41-61.
101. Coll R.C., O'Neill L.A. New insights into the regulation of signalling by toll-like receptors and nod-like receptors. J. Innate Immun. 2010, 2:406-421.
102. Matsushita K., et al. A splice variant of ASC regulates IL-1β release and aggregates differently from intact ASC. Mediat. Inflamm. 2009, 2009. 287387.
103. Stehlik C., et al. The PAAD/PYRIN-family protein ASC is a dual regulator of a conserved step in nuclear factor κB activation pathways. J. Exp. Med. 2002, 196:1605-1615.
104. Holley M.M., Kielian T. Th1 and Th17 cells regulate innate immune responses and bacterial clearance during central nervous system infection. J. Immunol. 2012, 188:1360-1370.
105. Covacu R., et al. TLR activation induces TNF-alpha production from adult neural stem/progenitor cells. J. Immunol. 2009, 182:6889-6895.
106. Lathia J.D., et al. Toll-like receptor 3 is a negative regulator of embryonic neural progenitor cell proliferation. J. Neurosci. 2008, 28:13978-13984.