Opposing effects of Toll-like receptors 2 and 4 on synaptic stability in the spinal cord after peripheral nerve injury

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Freria, Camila Marques ^a   Velloso, Licio Augusto ^a   Oliveira, Alexandre L R ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL ACTIVITY; CELL CULTURE; CELL LOSS; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; GLIA CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LUMBAR SPINAL CORD; MALE; MOTONEURON; MOUSE; NERVE CELL PLASTICITY; NERVE ENDING; NERVE FIBER TRANSECTION; NERVE POTENTIAL; NEWBORN; NONHUMAN; PERIPHERAL NERVE INJURY; PRESERVATION; PROTEIN FUNCTION; SCIATIC NERVE; SPINAL CORD; SPINAL CORD FUNCTION; UPREGULATION;

EID: 84867685114     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-240     Document Type: Article

References (44)

1. Huh GS, Boulanger LM, Du H, Riquelme PA, Brotz TM, Shatz CJ. Functional requirement for class I MHC in CNS development and plasticity. Science 2000, 290(5499):2155-2159. 10.1126/science.290.5499.2155, 2175035, 11118151.
2. Oliveira AL, Thams S, Lidman O, Piehl F, Hökfelt T, Kärre K, Lindå H, Culheim S. A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc Natl Acad Sci 2004, 101:17843-17848. 10.1073/pnas.0408154101, 539738, 15591351.
3. Berg A, Zelano J, Stephan A, Thams S, Barres BA, Pekny M, Pekna M, Cullheim S. Reduced removal of synaptic terminals from axotomized spinal motoneurons in the absence of complement C3. Exp Neurol 2012, 237(1):8-17. 10.1016/j.expneurol.2012.06.008, 22721768.
4. Fourgeaud L, Boulanger LM. Synapse remodeling, compliments of the complement system. Cell 2007, 131(6):1034-1036. 10.1016/j.cell.2007.11.031, 18083091.
5. Aldskogius H, Liu L, Svensson M. Glial responses to synaptic damage and plasticity. J Neurosci Res 1999, 58(1):33-41. 10.1002/(SICI)1097-4547(19991001)58:1<33::AID-JNR5>3.0.CO;2-M, 10491570.
6. Emirandetti A, Zanon RG, Sabha JR, Oliveira ALR. Astrocyte reactivity influences the number of presynaptic terminals apposed to spinal motoneurons after axotomy. Brain Res 2006, 1095:35-42. 10.1016/j.brainres.2006.04.021, 16714003.
7. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, Jensen FE, Rosenberg PA, Volpe JJ, Vartanian T. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 2002, 22(7):2478-2486.
8. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T. 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, 100(14):8514-8519. 10.1073/pnas.1432609100, 166260, 12824464.
9. Lehnardt S. Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia 2010, 58(3):253-263.
10. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, McCrea E, Shapiro A, Antel JP. TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 2005, 22:4320-4330.
11. Henn A, Kirner S, Leist M. TLR2 hypersensitivity of astrocytes as functional consequence of previous inflammatory episodes. J Immunol 2011, 186(5):3237-3247. 10.4049/jimmunol.1002787, 21282508.
12. Goethals S, Ydens E, Timmerman V, Janssens S. Toll-like receptor expression in the peripheral nerve. Glia 2010, 58(14):1701-1709. 10.1002/glia.21041, 20578041.
13. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, Jo DG, Lathia JD, Siler DA, Chigurupati S, Ouyang X, Magnus T, Camandola S, Mattson MP. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci USA 2007, 104(34):13798-13803. 10.1073/pnas.0702553104, 1959462, 17693552.
14. Bowman CC, Rasley A, Tranguch SL, Marriott I. Cultured astrocytes express toll-like receptors for bacterial products. Glia 2003, 43(3):281-291. 10.1002/glia.10256, 12898707.
15. Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 2004, 173(6):3916-3924.
16. Phulwani NK, Esen N, Syed MM, Kielian T. TLR2 expression in astrocytes is induced by TNF-alpha- and NF-kappa B-dependent pathways. J Immunol 2008, 181(6):3841-3849. 2649826, 18768838.
17. Lindå H, Shupliakov O, Örnung G, Ottersen OP, Storm-Mathisen J, Risling M, Cullheim S. Ultrastructural evidence for a preferential elimination of glutamate-immunoreactive synaptic terminals from spinal motoneurons after intramedullary axotomy. J Comp Neurol 2000, 425:10-23. 10.1002/1096-9861(20000911)425:1<10::AID-CNE2>3.0.CO;2-#, 10940938.
18. Cullheim S, Thams S. The microglial networks of brain and their role in neural network plasticity after lesion. Brain Res Rev 2007, 55:89-96. 10.1016/j.brainresrev.2007.03.012, 17509690.
19. Schiefer J, Kampe K, Dodt HU, Zieglgänsberger W, Kreutzberg GW. Microglial motility in the rat facial nucleus following peripheral axotomy. J Neurocytol 1999, 28(6):439-453. 10.1023/A:1007048903862, 10767097.
20. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282(5396):2085-2088.
21. Conradi S. On motoneuron synaptology in adult cats. Acta Physiol Scand 1969, 332:1-57.
22. McCarthy KD, Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 1980, 85:890-902. 10.1083/jcb.85.3.890, 2111442, 6248568.
23. Boulanger LM, Huh GS, Shatz CJ. Neuronal plasticity and cellular immunity: shared molecular mechanisms. Curr Opin Neurobiol 2001, 11(5):568-578. 10.1016/S0959-4388(00)00251-8, 11595490.
24. Ma Y, Li J, Chiu I, Wang Y, Sloane JA, Lü J, Kosaras B, Sidman RL, Volpe JJ, Vartanian T. Toll-like receptor 8 functions as a negative regulator of neurite outgrowth and inducer of neuronal apoptosis. J Cell Biol 2006, 175(2):209-215. 10.1083/jcb.200606016, 2064562, 17060494.
25. Li Y, Li H, Zhang Y, Sun X, Hanley GA, LeSage G, Zhang Y, Sun S, Peng Y, Yin D. Toll-like receptor 2 is required for opioids-induced neuronal apoptosis. Biochem Biophys Res Commun 2010, 391(1):426-430. 10.1016/j.bbrc.2009.11.074, 2812588, 19914204.
26. Rolls A, Shechter R, London A, Ziv Y, Ronen A, Levy R, Schwartz M. Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol 2007, 9(9):1081-1088. 10.1038/ncb1629, 17704767.
27. Wainwright DA, Xin J, Mesnard NA, Sanders VM, Jones KJ. Toll-like receptor 2 and facial motoneuron survival after facial nerve axotomy. Neurosci Lett 2010, 471(1):10-14. 10.1016/j.neulet.2009.12.076, 2825370, 20056129.
28. Ziegler G, Harhausen D, Schepers C, Hoffmann O, Röhr C, Prinz V, König J, Lehrach H, Nietfeld W, Trendelenburg G. TLR2 has a detrimental role in mouse transient focal cerebral ischemia. Biochem Biophys Res Commun 2007, 359(3):574-579. 10.1016/j.bbrc.2007.05.157, 17548055.
29. Okun E, Griffioen KJ, Mattson MP. Toll-like receptor signaling in neural plasticity and disease. TINS 2011, 34(5):269-281. 3095763, 21419501.
30. Kigerl KA, Lai W, Rivest S, Hart RP, Satoskar AR, Popovich PG. Toll-like receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J Neurochem 2007, 102(1):37-50. 10.1111/j.1471-4159.2007.04524.x, 17403033.
31. Boivin A, Pineau I, Barrette B, Filali M, Vallieres N, Rivest S, Lacroix S. Toll like receptor signaling is critical for wallerian degeneration and functional recovery after peripheral nerve injury. J Neurosci 2007, 27:12565-12576. 10.1523/JNEUROSCI.3027-07.2007, 18003835.
32. Benveniste EN, Sparacio SM, Norris JG, Grenett HE, Fuller GM. Induction and regulation of interleukin-6 gene expression in rat astrocytes. J Neuroimmunol 1990, 30(2-3):201-212.
33. Lee SC, Liu W, Dickson DW, Brosnan CF, Berman JW. Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J Immunol 1993, 150(7):2659-2667.
34. John GR, Lee SC, Song X, Rivieccio M, Brosnan CF. IL-1-regulated responses in astrocytes: relevance to injury and recovery. Glia 2005, 49(2):161-176. 10.1002/glia.20109, 15472994.
35. Herx LM, Rivest S, Yong VW. Central nervous system-initiated inflammation and neurotrophism in trauma: IL-1 beta is required for the production of ciliary neurotrophic factor. J Immunol 2000, 165(4):2232-2239.
36. Pinteaux E, Rothwell NJ, Boutin H. Neuroprotective actions of endogenous interleukin-1 receptor antagonist (IL-1ra) are mediated by glia. Glia 2006, 53(5):551-556. 10.1002/glia.20308, 16374779.
37. Hailer NP, Vogt C, Korf HW, Dehghani F. Interleukin-1beta exacerbates and interleukin-1 receptor antagonist attenuates neuronal injury and microglial activation after excitotoxic damage in organotypic hippocampal slice cultures. Eur J Neurosci 2005, 21(9):2347-2360. 10.1111/j.1460-9568.2005.04067.x, 15932594.
38. Joseph MS, Bilousova T, Zdunowski S, Wu ZP, Middleton B, Boudzinskaia M, Wong B, Ali N, Zhong H, Yong J, Washburn L, Escande-Beillard N, Dang H, Edgerton VR, Tillakaratne NJ, Kaufman DL. Transgenic mice with enhanced neuronal major histocompatibility complex class I expression recover locomotor function better after spinal cord injury. J Neurosci 2011, 89(3):365-372.
39. Kim D, Kim MA, Cho IH, Kim MS, Lee S, Jo EK, Choi SY, Park K, Kim JS, Akira S, Na HS, Oh SB, Lee SJ. A critical role of toll-like receptor 2 in nerve injury-induced spinal cord glial cell activation and pain hypersensitivity. J Biol Chem 2007, 282(20):14975-14983. 10.1074/jbc.M607277200, 17355971.
40. Rao JS, Kellom M, Kim HW, Rapoport SI, Reese EA. Neuroinflammation and synaptic loss. Neurochem Res 2012, 37(5):903-910. 10.1007/s11064-012-0708-2, 3478877, 22311128.
41. Boyd JG, Gordon T. Glial cell line-derived neurotrophic factor and brain-derived neurotrophic factor sustain the axonal regeneration of chronically axotomized motoneurons in vivo. Exp Neurol 2003, 183:610-619. 10.1016/S0014-4886(03)00183-3, 14552902.
42. Black IB. Trophic regulation of synaptic plasticity. J Neurobiol 1999, 41(1):108-118. 10.1002/(SICI)1097-4695(199910)41:1<108::AID-NEU14>3.0.CO;2-U, 10504198.
43. Novikov LN, Novikova LN, Holmberg P, Kellerth J. Exogenous brain-derived neurotrophic factor regulates the synaptic composition of axonally lesioned and normal adult rat motoneurons. Neuroscience 2000, 100(1):171-181. 10.1016/S0306-4522(00)00256-6, 10996467.
44. Naveilhan P, ElShamy WM, Ernfors P. Differential regulation of mRNAs for GDNF and its receptors Ret and GDNFR alpha after sciatic nerve lesion in the mouse. Eur J Neurosci 1997, 9(7):1450-1460. 10.1111/j.1460-9568.1997.tb01499.x, 9240402.