Acute injury in the peripheral nervous system triggers an alternative macrophage response

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Ydens, Elke ^a   Cauwels, Anje ^b,c   Asselbergh, Bob ^a   Goethals, Sofie ^a   Peeraer, Lieve ^a   Lornet, Guillaume ^b,c   Almeida Souza, Leonardo ^a   Van Ginderachter, Jo A ^c,d   Timmerman, Vincent ^a   Janssens, Sophie ^b,c  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

Innate immune system; M2; Negative regulation; Neuroprotection; RT qPCR; Wallerian degeneration

Indexed keywords

ARGINASE 1; BIOLOGICAL MARKER; CYTOKINE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12P40; PROTEIN TREM2; PROTEIN YM1; UNCLASSIFIED DRUG;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INNATE IMMUNITY; MACROPHAGE ACTIVATION; MOUSE; NERVE DEGENERATION; NERVE FIBER TRANSECTION; NEUROPROTECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PHENOTYPE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCIATIC NERVE INJURY; SIGNAL TRANSDUCTION; TH2 CELL; TISSUE REPAIR; UPREGULATION; WESTERN BLOTTING;

EID: 84865178023     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-176     Document Type: Article

References (90)

1. Waller A. Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Phil Transact Royal Soc London 1850, 140:423-429.
2. Saxena S, Caroni P. Mechanisms of axon degeneration: from development to disease. Prog Neurobiol 2007, 83:174-191. 10.1016/j.pneurobio.2007.07.007, 17822833.
3. Shamash S, Reichert F, Rotshenker S. The cytokine network of Wallerian degeneration: tumor necrosis factor-alpha, interleukin-1alpha, and interleukin-1beta. J Neurosci 2002, 22:3052-3060.
4. Perrin FE, Lacroix S, Aviles-Trigueros M, David S. Involvement of monocyte chemoattractant protein-1, macrophage inflammatory protein-1alpha and interleukin-1beta in Wallerian degeneration. Brain 2005, 128:854-866. 10.1093/brain/awh407, 15689362.
5. Taskinen HS, Olsson T, Bucht A, Khademi M, Svelander L, Roytta M. Peripheral nerve injury induces endoneurial expression of IFN-gamma, IL-10 and TNF-alpha mRNA. J Neuroimmunol 2000, 102:17-25. 10.1016/S0165-5728(99)00154-X, 10626662.
6. Subang MC, Richardson PM. Influence of injury and cytokines on synthesis of monocyte chemoattractant protein-1 mRNA in peripheral nervous tissue. Eur J Neurosci 2001, 13:521-528. 10.1046/j.1460-9568.2001.01425.x, 11168559.
7. Taskinen HS, Roytta M. Increased expression of chemokines (MCP-1, MIP-1alpha, RANTES) after peripheral nerve transection. J Peripher Nerv Syst 2000, 5:75-81. 10.1046/j.1529-8027.2000.00009.x, 10905466.
8. Toews AD, Barrett C, Morell P. Monocyte chemoattractant protein 1 is responsible for macrophage recruitment following injury to sciatic nerve. J Neurosci Res 1998, 53:260-267. 10.1002/(SICI)1097-4547(19980715)53:2<260::AID-JNR15>3.0.CO;2-A, 9671983.
9. Zuo Y, Perkins NM, Tracey DJ, Geczy CL. Inflammation and hyperalgesia induced by nerve injury in the rat: a key role of mast cells. Pain 2003, 105:467-479. 10.1016/S0304-3959(03)00261-6, 14527707.
10. Moalem G, Tracey DJ. Immune and inflammatory mechanisms in neuropathic pain. Brain Res Rev 2006, 51:240-264. 10.1016/j.brainresrev.2005.11.004, 16388853.
11. Bendszus M, Stoll G. Caught in the act: in vivo mapping of macrophage infiltration in nerve injury by magnetic resonance imaging. J Neurosci 2003, 23:10892-10896.
12. Mueller M, Leonhard C, Wacker K, Ringelstein EB, Okabe M, Hickey WF, Kiefer R. Macrophage response to peripheral nerve injury: the quantitative contribution of resident and hematogenous macrophages. Lab Invest 2003, 83:175-185.
13. Taskinen HS, Roytta M. The dynamics of macrophage recruitment after nerve transection. Acta Neuropathol 1997, 93:252-259. 10.1007/s004010050611, 9083556.
14. Perry VH, Brown MC, Gordon S. The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. J Exp Med 1987, 165:1218-1223. 10.1084/jem.165.4.1218, 2188570, 3559478.
15. Mueller M, Wacker K, Ringelstein EB, Hickey WF, Imai Y, Kiefer R. Rapid response of identified resident endoneurial macrophages to nerve injury. Am J Pathol 2001, 159:2187-2197. 10.1016/S0002-9440(10)63070-2, 1850587, 11733369.
16. Hirata K, Kawabuchi M. Myelin phagocytosis by macrophages and nonmacrophages during Wallerian degeneration. Microsc Res Tech 2002, 57:541-547. 10.1002/jemt.10108, 12112437.
17. Omura T, Omura K, Sano M, Sawada T, Hasegawa T, Nagano A. Spatiotemporal quantification of recruit and resident macrophages after crush nerve injury utilizing immunohistochemistry. Brain Res 2005, 1057:29-36. 10.1016/j.brainres.2005.07.008, 16112089.
18. Sawada T, Sano M, Omura T, Omura K, Hasegawa T, Funahashi S, Nagano A. Spatiotemporal quantification of tumor necrosis factor-alpha and interleukin-10 after crush injury in rat sciatic nerve utilizing immunohistochemistry. Neurosci Lett 2007, 417:55-60. 10.1016/j.neulet.2007.02.028, 17336456.
19. Liefner M, Siebert H, Sachse T, Michel U, Kollias G, Bruck W. The role of TNF-alpha during Wallerian degeneration. J Neuroimmunol 2000, 108:147-152. 10.1016/S0165-5728(00)00262-9, 10900348.
20. Gillen C, Jander S, Stoll G. Sequential expression of mRNA for proinflammatory cytokines and interleukin-10 in the rat peripheral nervous system: comparison between immune-mediated demyelination and Wallerian degeneration. J Neurosci Res 1998, 51:489-496. 10.1002/(SICI)1097-4547(19980215)51:4<489::AID-JNR8>3.0.CO;2-8, 9514202.
21. de la Hoz CL, Oliveira AL, Queiroz Lde S, Langone F. Wallerian degeneration in C57BL/6J and A/J mice: differences in time course of neurofilament and myelin breakdown, macrophage recruitment and iNOS expression. J Anat 2003, 203:567-578. 10.1046/j.1469-7580.2003.00248.x, 1571200, 14686692.
22. Goethals S, Ydens E, Timmerman V, Janssens S. Toll-like receptor expression in the peripheral nerve. Glia 2010, 58:1701-1709. 10.1002/glia.21041, 20578041.
23. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3:RESEARCH0034. 126239, 12184808.
24. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 2007, 8:R19. 10.1186/gb-2007-8-2-r19, 1852402, 17291332.
25. Ghassabeh GH, De Baetselier P, Brys L, Noel W, Van Ginderachter JA, Meerschaut S, Beschin A, Brombacher F, Raes G. Identification of a common gene signature for type II cytokine-associated myeloid cells elicited in vivo in different pathologic conditions. Blood 2006, 108:575-583. 10.1182/blood-2005-04-1485, 16556895.
26. Janssens S, Burns K, Tschopp J, Beyaert R. Regulation of interleukin-1- and lipopolysaccharide-induced NF-kappaB activation by alternative splicing of MyD88. Curr Biol 2002, 12:467-471. 10.1016/S0960-9822(02)00712-1, 11909531.
27. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, Charo IF. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 2007, 117:902-909. 10.1172/JCI29919, 1810572, 17364026.
28. Morita I. Distinct functions of COX-1 and COX-2. Prostaglandins Other Lipid Mediat 2002, 68-69:165-175. 2844927, 19545642.
29. Ma W, Quirion R. Does COX2-dependent PGE2 play a role in neuropathic pain?. Neurosci Lett 2008, 437:165-169. 10.1016/j.neulet.2008.02.072, 18434017.
30. Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 2009, 27:519-550. 10.1146/annurev.immunol.021908.132612, 19302047.
31. Kishimoto T. IL-6: from its discovery to clinical applications. Int Immunol 2010, 22:347-352. 10.1093/intimm/dxq030, 20410258.
32. Boone DL, Turer EE, Lee EG, Ahmad RC, Wheeler MT, Tsui C, Hurley P, Chien M, Chai S, Hitotsumatsu O, McNally E, Pickart C, Ma A. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 2004, 5:1052-1060. 10.1038/ni1110, 15334086.
33. Jacobs MD, Harrison SC. Structure of an IkappaBalpha/NF-kappaB complex. Cell 1998, 95:749-758. 10.1016/S0092-8674(00)81698-0, 9865693.
34. Wald D, Qin J, Zhao Z, Qian Y, Naramura M, Tian L, Towne J, Sims JE, Stark GR, Li X. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 2003, 4:920-927. 10.1038/ni968, 12925853.
35. Yasukawa H, Misawa H, Sakamoto H, Masuhara M, Sasaki A, Wakioka T, Ohtsuka S, Imaizumi T, Matsuda T, Ihle JN, Yoshimura A. The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J 1999, 18:1309-1320. 10.1093/emboj/18.5.1309, 1171221, 10064597.
36. Van Ginderachter JA, Movahedi K. Hassanzadeh Ghassabeh G, Meerschaut S, Beschin A, Raes G, De Baetselier P: Classical and alternative activation of mononuclear phagocytes: picking the best of both worlds for tumor promotion. Immunobiology 2006, 211:487-501. 10.1016/j.imbio.2006.06.002, 16920488.
37. Raes G, Van den Bergh R, De Baetselier P, Ghassabeh GH, Scotton C, Locati M, Mantovani A, Sozzani S. Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells. J Immunol 2005, 174:6561. Author reply 6561-6562.
38. Kohler C. Allograft inflammatory factor-1/Ionized calcium-binding adapter molecule 1 is specifically expressed by most subpopulations of macrophages and spermatids in testis. Cell Tissue Res 2007, 330:291-302. 10.1007/s00441-007-0474-7, 17874251.
39. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011, 11:723-737. 10.1038/nri3073, 21997792.
40. Mege JL, Mehraj V, Capo C. Macrophage polarization and bacterial infections. Curr Opin Infect Dis 2011, 24:230-234. 10.1097/QCO.0b013e328344b73e, 21311324.
41. Hsieh CS, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science 1993, 260:547-549. 10.1126/science.8097338, 8097338.
42. Gately MK, Renzetti LM, Magram J, Stern AS, Adorini L, Gubler U, Presky DH. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol 1998, 16:495-521. 10.1146/annurev.immunol.16.1.495, 9597139.
43. Mattner F, Ozmen L, Podlaski FJ, Wilkinson VL, Presky DH, Gately MK, Alber G. Treatment with homodimeric interleukin-12 (IL-12) p40 protects mice from IL-12-dependent shock but not from tumor necrosis factor alpha-dependent shock. Infect Immun 1997, 65:4734-4737. 175679, 9353058.
44. MacMicking J, Xie QW, Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol 1997, 15:323-350. 10.1146/annurev.immunol.15.1.323, 9143691.
45. Cai D, Deng K, Mellado W, Lee J, Ratan RR, Filbin MT. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 2002, 35:711-719. 10.1016/S0896-6273(02)00826-7, 12194870.
46. Wheelock MJ, Jensen PJ. Regulation of keratinocyte intercellular junction organization and epidermal morphogenesis by E-cadherin. J Cell Biol 1992, 117:415-425. 10.1083/jcb.117.2.415, 2289421, 1373144.
47. Suffia I, Reckling SK, Salay G, Belkaid Y. A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection. J Immunol 2005, 174:5444-5455.
48. Brown GD, Taylor PR, Reid DM, Willment JA, Williams DL, Martinez-Pomares L, Wong SY, Gordon S. Dectin-1 is a major beta-glucan receptor on macrophages. J Exp Med 2002, 196:407-412. 10.1084/jem.20020470, 2193936, 12163569.
49. Teng X, Li D, Champion HC, Johns RA. FIZZ1/RELMalpha, a novel hypoxia-induced mitogenic factor in lung with vasoconstrictive and angiogenic properties. Circ Res 2003, 92:1065-1067. 10.1161/01.RES.0000073999.07698.33, 12714564.
50. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 2009, 27:451-483. 10.1146/annurev.immunol.021908.132532, 19105661.
51. Swain SL, Weinberg AD, English M, Huston G. IL-4 directs the development of Th2-like helper effectors. J Immunol 1990, 145:3796-3806.
52. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001, 19:683-765. 10.1146/annurev.immunol.19.1.683, 11244051.
53. Wynn TA. IL-13 effector functions. Annu Rev Immunol 2003, 21:425-456. 10.1146/annurev.immunol.21.120601.141142, 12615888.
54. Chieppa M, Bianchi G, Doni A, Del Prete A, Sironi M, Laskarin G, Monti P, Piemonti L, Biondi A, Mantovani A, Introna M, Allavena P. Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program. J Immunol 2003, 171:4552-4560.
55. Sparvero LJ, Asafu-Adjei D, Kang R, Tang D, Amin N, Im J, Rutledge R, Lin B, Amoscato AA, Zeh HJ, Lotze MT. RAGE (Receptor for Advanced Glycation Endproducts), RAGE ligands, and their role in cancer and inflammation. J Transl Med 2009, 7:17. 10.1186/1479-5876-7-17, 2666642, 19292913.
56. Daws MR, Sullam PM, Niemi EC, Chen TT, Tchao NK, Seaman WE. Pattern recognition by TREM-2: binding of anionic ligands. J Immunol 2003, 171:594-599.
57. Turnbull IR, Gilfillan S, Cella M, Aoshi T, Miller M, Piccio L, Hernandez M, Colonna M. Cutting edge: TREM-2 attenuates macrophage activation. J Immunol 2006, 177:3520-3524.
58. Owhashi M, Arita H, Hayai N. Identification of a novel eosinophil chemotactic cytokine (ECF-L) as a chitinase family protein. J Biol Chem 2000, 275:1279-1286. 10.1074/jbc.275.2.1279, 10625674.
59. Arora M, Chen L, Paglia M, Gallagher I, Allen JE, Vyas YM, Ray A, Ray P. Simvastatin promotes Th2-type responses through the induction of the chitinase family member Ym1 in dendritic cells. Proc Natl Acad Sci U S A 2006, 103:7777-7782. 10.1073/pnas.0508492103, 1472521, 16682645.
60. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003, 3:23-35. 10.1038/nri978, 12511873.
61. Piccinini AM, Midwood KS. DAMPening inflammation by modulating TLR signalling. Mediators Inflamm 2010, 2010: . pii: 672395, 3034973, 21318153.
62. Li M, Carpio DF, Zheng Y, Bruzzo P, Singh V, Ouaaz F, Medzhitov RM, Beg AA. 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, 166:7128-7135.
63. Van den Bossche J, Bogaert P, van Hengel J, Guerin CJ, Berx G, Movahedi K, Van den Bergh R, Pereira-Fernandes A, Geuns JM, Pircher H, Dorny P, Grooten J, De Baetselier P, Van Ginderachter JA. Alternatively activated macrophages engage in homotypic and heterotypic interactions through IL-4 and polyamine-induced E-cadherin/catenin complexes. Blood 2009, 114:4664-4674. 10.1182/blood-2009-05-221598, 19726720.
64. Anthony RM, Rutitzky LI, Urban JF, Stadecker MJ, Gause WC. Protective immune mechanisms in helminth infection. Nat Rev Immunol 2007, 7:975-987. 10.1038/nri2199, 2258092, 18007680.
65. Nadeau S, Filali M, Zhang J, Kerr BJ, Rivest S, Soulet D, Iwakura Y, de Rivero Vaccari JP, Keane RW, Lacroix S. Functional recovery after peripheral nerve injury is dependent on the pro-inflammatory cytokines IL-1beta and TNF: implications for neuropathic pain. J Neurosci 2011, 31:12533-12542. 10.1523/JNEUROSCI.2840-11.2011, 21880915.
66. Loke P, Gallagher I, Nair MG, Zang X, Brombacher F, Mohrs M, Allison JP, Allen JE. Alternative activation is an innate response to injury that requires CD4+ T cells to be sustained during chronic infection. J Immunol 2007, 179:3926-3936.
67. Shechter R, London A, Varol C, Raposo C, Cusimano M, Yovel G, Rolls A, Mack M, Pluchino S, Martino G, Jung S, Schwartz M. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med 2009, 6:e1000113. 10.1371/journal.pmed.1000113, 2707628, 19636355.
68. Barrette B, Hebert MA, Filali M, Lafortune K, Vallieres N, Gowing G, Julien JP, Lacroix S. Requirement of myeloid cells for axon regeneration. J Neurosci 2008, 28:9363-9376. 10.1523/JNEUROSCI.1447-08.2008, 18799670.
69. Vargas ME, Watanabe J, Singh SJ, Robinson WH, Barres BA. Endogenous antibodies promote rapid myelin clearance and effective axon regeneration after nerve injury. Proc Natl Acad Sci U S A 2010, 107:11993-11998. 10.1073/pnas.1001948107, 2900702, 20547838.
70. Hikawa N, Takenaka T. Myelin-stimulated macrophages release neurotrophic factors for adult dorsal root ganglion neurons in culture. Cell Mol Neurobiol 1996, 16:517-528. 10.1007/BF02150231, 8879753.
71. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 2009, 29:13435-13444. 10.1523/JNEUROSCI.3257-09.2009, 2788152, 19864556.
72. Lu D, Goussev A, Chen J, Pannu P, Li Y, Mahmood A, Chopp M. Atorvastatin reduces neurological deficit and increases synaptogenesis, angiogenesis, and neuronal survival in rats subjected to traumatic brain injury. J Neurotrauma 2004, 21:21-32. 10.1089/089771504772695913, 14987462.
73. Pannu R, Barbosa E, Singh AK, Singh I. Attenuation of acute inflammatory response by atorvastatin after spinal cord injury in rats. J Neurosci Res 2005, 79:340-350. 10.1002/jnr.20345, 15605375.
74. Angelov DN, Waibel S, Guntinas-Lichius O, Lenzen M, Neiss WF, Tomov TL, Yoles E, Kipnis J, Schori H, Reuter A, Ludolph A, Schwartz M. Therapeutic vaccine for acute and chronic motor neuron diseases: implications for amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 2003, 100:4790-4795. 10.1073/pnas.0530191100, 153634, 12668759.
75. Sicotte M, Tsatas O, Jeong SY, Cai CQ, He Z, David S. Immunization with myelin or recombinant Nogo-66/MAG in alum promotes axon regeneration and sprouting after corticospinal tract lesions in the spinal cord. Mol Cell Neurosci 2003, 23:251-263. 10.1016/S1044-7431(03)00053-8, 12812757.
76. Huang DW, McKerracher L, Braun PE, David S. A therapeutic vaccine approach to stimulate axon regeneration in the adult mammalian spinal cord. Neuron 1999, 24:639-647. 10.1016/S0896-6273(00)81118-6, 10595515.
77. Wolf SA, Fisher J, Bechmann I, Steiner B, Kwidzinski E, Nitsch R. Neuroprotection by T-cells depends on their subtype and activation state. J Neuroimmunol 2002, 133:72-80. 10.1016/S0165-5728(02)00367-3, 12446010.
78. Aarli JA. Role of cytokines in neurological disorders. Curr Med Chem 2003, 10:1931-1937. 10.2174/0929867033456918, 12871095.
79. Dahle C, Ekerfelt C, Vrethem M, Samuelsson M, Ernerudh J. T helper type 2 like cytokine responses to peptides from P0 and P2 myelin proteins during the recovery phase of Guillain-Barre syndrome. J Neurol Sci 1997, 153:54-60. 10.1016/S0022-510X(97)00178-0, 9455979.
80. Inoue A, Iwahashi T, Koh CS, Yanagisawa N. A study on subpopulation of helper T cells in chronic inflammatory demyelinating polyneuropathy. Arerugi 1994, 43:1270-1276.
81. Deretzi G, Pelidou SH, Zou LP, Quiding C, Zhu J. Local effects of recombinant rat interleukin-6 on the peripheral nervous system. Immunology 1999, 97:582-587. 10.1046/j.1365-2567.1999.00808.x, 2326882, 10457210.
82. Malandrini A, Villanova M, Dotti MT, Federico A. Acute inflammatory neuropathy in Charcot-Marie-Tooth disease. Neurology 1999, 52:859-861. 10.1212/WNL.52.4.859, 10078742.
83. Shy ME, Arroyo E, Sladky J, Menichella D, Jiang H, Xu W, Kamholz J, Scherer SS. Heterozygous P0 knockout mice develop a peripheral neuropathy that resembles chronic inflammatory demyelinating polyneuropathy (CIDP). J Neuropathol Exp Neurol 1997, 56:811-821.
84. Schmid CD, Stienekemeier M, Oehen S, Bootz F, Zielasek J, Gold R, Toyka KV, Schachner M, Martini R. Immune deficiency in mouse models for inherited peripheral neuropathies leads to improved myelin maintenance. J Neurosci 2000, 20:729-735.
85. Carenini S, Maurer M, Werner A, Blazyca H, Toyka KV, Schmid CD, Raivich G, Martini R. The role of macrophages in demyelinating peripheral nervous system of mice heterozygously deficient in p0. J Cell Biol 2001, 152:301-308. 10.1083/jcb.152.2.301, 2199607, 11266447.
86. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 2002, 34:895-903. 10.1016/S0896-6273(02)00730-4, 12086638.
87. Kuo HS, Tsai MJ, Huang MC, Chiu CW, Tsai CY, Lee MJ, Huang WC, Lin YL, Kuo WC, Cheng H. Acid fibroblast growth factor and peripheral nerve grafts regulate Th2 cytokine expression, macrophage activation, polyamine synthesis, and neurotrophin expression in transected rat spinal cords. J Neurosci 2011, 31:4137-4147. 10.1523/JNEUROSCI.2592-10.2011, 21411654.
88. Lee YS, Hsiao I, Lin VW. Peripheral nerve grafts and aFGF restore partial hindlimb function in adult paraplegic rats. J Neurotrauma 2002, 19:1203-1216. 10.1089/08977150260338001, 12427329.
89. Kaji R, Kiyoshima-Shibata J, Nagaoka M, Nanno M, Shida K. Bacterial teichoic acids reverse predominant IL-12 production induced by certain lactobacillus strains into predominant IL-10 production via TLR2-dependent ERK activation in macrophages. J Immunol 2010, 184:3505-3513. 10.4049/jimmunol.0901569, 20190136.
90. Redecke V, Hacker H, Datta SK, Fermin A, Pitha PM, Broide DH, Raz E. Cutting edge: activation of Toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma. J Immunol 2004, 172:2739-2743.