Home LiteratureArticle Details
PMID: 17151286 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Toll-like receptor 2 signaling in response to brain injury: an innate bridge to neuroinflammation.

Babcock AA, Wirenfeldt M, Holm T, Nielsen HH, Dissing-Olesen L, Toft-Hansen H, Millward JM, Landmann R, Rivest S, Finsen B, Owens T

Abstract

Reactive gliosis is a prominent feature of neurodegenerative and neuroinflammatory disease in the CNS, yet the stimuli that drive this response are not known. There is growing appreciation that signaling through Toll-like receptors (TLRs), which is key to generating innate responses to infection, may have pathogen-independent roles. We show that TLR2 was selectively upregulated by microglia in the denervated zones of the hippocampus in response to stereotactic transection of axons in the entorhinal cortex. In mice lacking TLR2, there were transient, selective reductions in lesion-induced expression of cytokines and chemokines. Recruitment of T cells, but not macrophages, was delayed in TLR2-deficient mice, as well as in mice lacking TNFR1 (tumor necrosis factor receptor 1). TLR2 deficiency also affected microglial proliferative expansion, whereas all of these events were unaffected in TLR4-mutant mice. Consistent with the fact that responses in knock-out mice had all returned to wild-type levels by 8 d, there was no evidence for effects on neuronal plasticity at 20 d. These results identify a role for TLR2 signaling in the early glial response to brain injury, acting as an innate bridge to neuroinflammation.

MeSH Terms
Animals Axons/pathology Brain Injuries/genetics,metabolism,pathology Inflammation/genetics,metabolism,pathology Mice Mice, Inbred C3H Mice, Inbred C57BL Mice, Knockout Microglia/metabolism,pathology Neurons/metabolism,pathology Signal Transduction/genetics,physiology Toll-Like Receptor 2/biosynthesis,deficiency,genetics,physiology
Chemicals
Toll-Like Receptor 2
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Babcock Alicia A
Medical Biotechnology Center, University of Southern Denmark, 5000 Odense C, Denmark.
Wirenfeldt Martin
Holm Thomas
Nielsen Helle H
Dissing-Olesen Lasse
Toft-Hansen Henrik
Millward Jason M
Landmann Regine
Rivest Serge
Finsen Bente
Owens Trevor
References (79)
79 references, click to expand
  1. Severity of symptoms and demyelination in MOG-induced EAE depends on TNFR1.
    Eur J Immunol. 1999 Feb;29(2):626-32 PMID: 10064079
  2. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma.
    J Neurosci. 1999 Oct 1;19(19):8182-98 PMID: 10493720
  3. Proliferation of microglia and astrocytes in the dentate gyrus following entorhinal cortex lesion: a quantitative bromodeoxyuridine-labelling study.
    Eur J Neurosci. 1999 Sep;11(9):3359-64 PMID: 10510203
  4. IFNgamma enhances microglial reactions to hippocampal axonal degeneration.
    J Neurosci. 2000 May 15;20(10):3612-21 PMID: 10804203
  5. Lens injury stimulates axon regeneration in the mature rat optic nerve.
    J Neurosci. 2000 Jun 15;20(12):4615-26 PMID: 10844031
  6. Involvement of non-neuronal cells in entorhinal-hippocampal reorganization following lesions.
    Ann N Y Acad Sci. 2000 Jun;911:192-206 PMID: 10911875
  7. In situ tolerance within the central nervous system as a mechanism for preventing autoimmunity.
    J Exp Med. 2000 Sep 18;192(6):871-80 PMID: 10993917
  8. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13766-71 PMID: 11095740
  9. Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism.
    Nat Immunol. 2001 Apr;2(4):346-52 PMID: 11276206
  10. Presence of B7--2 (CD86) and lack of B7--1 (CD(80) on myelin phagocytosing MHC-II-positive rat microglia is associated with nondestructive immunity in vivo.
    FASEB J. 2001 Apr;15(6):1086-8 PMID: 11292676
  11. An essential role of the NF-kappa B/Toll-like receptor pathway in induction of inflammatory and tissue-repair gene expression by necrotic cells.
    J Immunol. 2001 Jun 15;166(12):7128-35 PMID: 11390458
  12. Bacterial peptidoglycan and immune reactivity in the central nervous system in multiple sclerosis.
    Brain. 2001 Aug;124(Pt 8):1544-54 PMID: 11459746
  13. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells.
    J Biol Chem. 2001 Oct 5;276(40):37692-9 PMID: 11477091
  14. Neuroinflammation-induced acceleration of amyloid deposition in the APPV717F transgenic mouse.
    Eur J Neurosci. 2001 Aug;14(3):474-82 PMID: 11553297
  15. Circulating cell wall components derived from gram-negative, not gram-positive, bacteria cause a profound induction of the gene-encoding Toll-like receptor 2 in the CNS.
    J Neurochem. 2001 Nov;79(3):648-57 PMID: 11701768
  16. Induction of proinflammatory molecules in mice with amyotrophic lateral sclerosis: no requirement for proapoptotic interleukin-1beta in neurodegeneration.
    Ann Neurol. 2001 Nov;50(5):630-9 PMID: 11706969
  17. Intrahippocampal LPS injections reduce Abeta load in APP+PS1 transgenic mice.
    Neurobiol Aging. 2001 Nov-Dec;22(6):1007-12 PMID: 11755009
  18. Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4.
    J Biol Chem. 2002 Apr 26;277(17):15028-34 PMID: 11836257
  19. Innate immune recognition.
    Annu Rev Immunol. 2002;20:197-216 PMID: 11861602
  20. IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking.
    J Immunol. 2002 Apr 1;168(7):3195-204 PMID: 11907072
  21. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS.
    J Neurosci. 2002 Apr 1;22(7):2478-86 PMID: 11923412
  22. The danger model: a renewed sense of self.
    Science. 2002 Apr 12;296(5566):301-5 PMID: 11951032
  23. Perforant path lesioning induces sprouting of CA3-associated fibre systems in mouse hippocampal formation.
    Exp Brain Res. 2002 May;144(1):79-87 PMID: 11976761
  24. Innate immunity: the missing link in neuroprotection and neurodegeneration?
    Nat Rev Neurosci. 2002 Mar;3(3):216-27 PMID: 11994753
  25. The neuropathological and behavioral consequences of intraspinal microglial/macrophage activation.
    J Neuropathol Exp Neurol. 2002 Jul;61(7):623-33 PMID: 12125741
  26. Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis.
    Glia. 2002 Nov;40(2):218-31 PMID: 12379909
  27. Broad expression of Toll-like receptors in the human central nervous system.
    J Neuropathol Exp Neurol. 2002 Nov;61(11):1013-21 PMID: 12430718
  28. Interactions between hemopoietically derived TNF and central nervous system-resident glial chemokines underlie initiation of autoimmune inflammation in the brain.
    J Immunol. 2002 Dec 15;169(12):7054-62 PMID: 12471141
  29. Pattern recognition receptors: doubling up for the innate immune response.
    Cell. 2002 Dec 27;111(7):927-30 PMID: 12507420
  30. Chemokines in experimental autoimmune encephalomyelitis and multiple sclerosis.
    Adv Exp Med Biol. 2003;520:120-32 PMID: 12613576
  31. Molecular approaches to spinal cord repair.
    Annu Rev Neurosci. 2003;26:411-40 PMID: 12626698
  32. Macrophages and microglia in central nervous system injury: are they helpful or harmful?
    J Cereb Blood Flow Metab. 2003 Apr;23(4):385-94 PMID: 12679714
  33. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8514-9 PMID: 12824464
  34. Signals that induce sprouting in the central nervous system: sprouting is delayed in a strain of mouse exhibiting delayed axonal degeneration.
    Exp Neurol. 1992 Dec;118(3):340-51 PMID: 1284863
  35. Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS.
    J Neurosci. 2003 Aug 27;23(21):7922-30 PMID: 12944523
  36. Importance of extra- and intracellular domains of TLR1 and TLR2 in NFkappa B signaling.
    J Cell Biol. 2003 Sep 15;162(6):1099-110 PMID: 12975352
  37. TNF-alpha microinjection upregulates chemokines and chemokine receptors in the central nervous system without inducing leukocyte infiltration.
    J Interferon Cytokine Res. 2003 Aug;23(8):457-66 PMID: 13678434
  38. The LPS receptor (CD14) links innate immunity with Alzheimer's disease.
    FASEB J. 2004 Jan;18(1):203-5 PMID: 14597556
  39. Toll-like receptor-2 modulates ventricular remodeling after myocardial infarction.
    Circulation. 2003 Dec 9;108(23):2905-10 PMID: 14656915
  40. Neuronal injury mediated via stimulation of microglial toll-like receptor-9 (TLR9).
    FASEB J. 2004 Feb;18(2):412-4 PMID: 14688201
  41. IFN-inducible protein 10/CXC chemokine ligand 10-independent induction of experimental autoimmune encephalomyelitis.
    J Immunol. 2004 Jan 1;172(1):550-9 PMID: 14688366
  42. Saturated fatty acid activates but polyunsaturated fatty acid inhibits Toll-like receptor 2 dimerized with Toll-like receptor 6 or 1.
    J Biol Chem. 2004 Apr 23;279(17):16971-9 PMID: 14966134
  43. Drosophila: the genetics of innate immune recognition and response.
    Annu Rev Immunol. 2004;22:457-83 PMID: 15032585
  44. Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain.
    Neurochem Int. 2004 Jul-Aug;45(2-3):397-407 PMID: 15145554
  45. Efficient T-cell surveillance of the CNS requires expression of the CXC chemokine receptor 3.
    J Neurosci. 2004 May 19;24(20):4849-58 PMID: 15152045
  46. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses.
    Nat Rev Immunol. 2004 Jun;4(6):469-78 PMID: 15173835
  47. Endogenous ligands of Toll-like receptors.
    J Leukoc Biol. 2004 Sep;76(3):514-9 PMID: 15178705
  48. Innate immune reaction in response to seizures: implications for the neuropathology associated with epilepsy.
    Neurobiol Dis. 2004 Jul;16(2):321-34 PMID: 15193289
  49. Microglia and Alzheimer's disease pathogenesis.
    J Neurosci Res. 2004 Jul 1;77(1):1-8 PMID: 15197750
  50. Toll-like receptor signalling.
    Nat Rev Immunol. 2004 Jul;4(7):499-511 PMID: 15229469
  51. Microglia and neuroinflammation: a pathological perspective.
    J Neuroinflammation. 2004 Jul 30;1(1):14 PMID: 15285801
  52. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs.
    J Immunol. 2004 Sep 15;173(6):3916-24 PMID: 15356140
  53. CXCR3-dependent microglial recruitment is essential for dendrite loss after brain lesion.
    J Neurosci. 2004 Sep 29;24(39):8500-9 PMID: 15456824
  54. Key metalloproteinases are expressed by specific cell types in experimental autoimmune encephalomyelitis.
    J Immunol. 2004 Oct 15;173(8):5209-18 PMID: 15470066
  55. Differential activation of astrocytes by innate and adaptive immune stimuli.
    Glia. 2005 Feb;49(3):360-74 PMID: 15538753
  56. Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3-dependent MyD88-independent pathway.
    J Immunol. 2004 Dec 15;173(12):7115-9 PMID: 15585830
  57. Bone-marrow-derived cells contribute to the recruitment of microglial cells in response to beta-amyloid deposition in APP/PS1 double transgenic Alzheimer mice.
    Neurobiol Dis. 2005 Feb;18(1):134-42 PMID: 15649704
  58. Proliferating resident microglia express the stem cell antigen CD34 in response to acute neural injury.
    Glia. 2005 Apr 15;50(2):121-31 PMID: 15657941
  59. Circulating monocytic cells infiltrate layers of anterograde axonal degeneration where they transform into microglia.
    FASEB J. 2005 Apr;19(6):647-9 PMID: 15671154
  60. Toll-like receptors, endogenous ligands, and systemic autoimmune disease.
    Immunol Rev. 2005 Apr;204:27-42 PMID: 15790348
  61. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy.
    Proc Natl Acad Sci U S A. 2005 Apr 19;102(16):5856-61 PMID: 15809417
  62. Cytokine and chemokine inter-regulation in the inflamed or injured CNS.
    Brain Res Brain Res Rev. 2005 Apr;48(2):178-84 PMID: 15850656
  63. Microglial cell population dynamics in the injured adult central nervous system.
    Brain Res Brain Res Rev. 2005 Apr;48(2):196-206 PMID: 15850658
  64. Innate (inherent) control of brain infection, brain inflammation and brain repair: the role of microglia, astrocytes, "protective" glial stem cells and stromal ependymal cells.
    Brain Res Brain Res Rev. 2005 Apr;48(2):220-33 PMID: 15850661
  65. Inflammatory-mediated injury and repair in the traumatically injured spinal cord.
    Curr Pharm Des. 2005;11(10):1223-36 PMID: 15853679
  66. LPS receptor (CD14): a receptor for phagocytosis of Alzheimer's amyloid peptide.
    Brain. 2005 Aug;128(Pt 8):1778-89 PMID: 15857927
  67. TLR signaling tailors innate immune responses in human microglia and astrocytes.
    J Immunol. 2005 Oct 1;175(7):4320-30 PMID: 16177072
  68. Systemic injections of lipopolysaccharide accelerates myelin phagocytosis during Wallerian degeneration in the injured mouse spinal cord.
    Glia. 2006 Jan 1;53(1):103-13 PMID: 16206158
  69. Reactive microgliosis engages distinct responses by microglial subpopulations after minor central nervous system injury.
    J Neurosci Res. 2005 Nov 15;82(4):507-14 PMID: 16237722
  70. Responses of microglia in vitro to the gram-positive bacterial component, lipoteichoic acid.
    J Neurosci Res. 2005 Nov 15;82(4):515-24 PMID: 16237723
  71. Toll-like receptors in central nervous system glial inflammation and homeostasis.
    J Neurosci Res. 2006 Apr;83(5):711-30 PMID: 16541438
  72. Tumor necrosis factor and its p55 and p75 receptors are not required for axonal lesion-induced microgliosis in mouse fascia dentata.
    Glia. 2006 Nov 1;54(6):591-605 PMID: 16927297
  73. Microglial and astroglial reactions to anterograde axonal degeneration: a histochemical and immunocytochemical study of the adult rat fascia dentata after entorhinal perforant path lesions.
    Exp Brain Res. 1994;98(2):245-60 PMID: 8050511
  74. Mechanisms of sprouting in the adult central nervous system: cellular responses in areas of terminal degeneration and reinnervation in the rat hippocampus.
    Neuroscience. 1994 Feb;58(4):705-25 PMID: 8190252
  75. Effects of chronic intrahippocampal infusion of lipopolysaccharide in the rat.
    Neuroscience. 1996 Jan;70(1):57-65 PMID: 8848136
  76. Morphological and immunophenotypic microglial changes in the denervated fascia dentata of adult rats: correlation with blood-brain barrier damage and astroglial reactions.
    Exp Neurol. 1997 Jan;143(1):103-16 PMID: 9000449
  77. Central nervous system microglial cell activation and proliferation follows direct interaction with tissue-infiltrating T cell blasts.
    J Immunol. 1998 Jun 1;160(11):5320-30 PMID: 9605131
  78. Immune surveillance in the injured nervous system: T-lymphocytes invade the axotomized mouse facial motor nucleus and aggregate around sites of neuronal degeneration.
    J Neurosci. 1998 Aug 1;18(15):5804-16 PMID: 9671668
  79. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene.
    Science. 1998 Dec 11;282(5396):2085-8 PMID: 9851930
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2006-12-06
Pages
12826-37
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6674840
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]