Molecular control of physiological and pathological T-cell recruitment after mouse spinal cord injury

Journal of Neuroscience

Volumn 25, Issue 28, 2005, Pages 6576-6583

  Jones, T Bucky ^a   Hart, Ronald P ^b   Popovich, Phillip G ^a,c  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c Immunology   (United States)

Author keywords

Chemokines; Macrophage; Microglia; Myelin basic protein; Neuroinflammation; Spinal cord injury; T lymphocyte

Indexed keywords

MYELIN BASIC PROTEIN; RANTES;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEMYELINATION; DISEASE ACTIVITY; DISEASE COURSE; LYMPHOCYTE MIGRATION; MACROPHAGE ACTIVATION; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MOUSE; NEUROPATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD INJURY; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE;

ANIMALS; CHEMOKINES; CHEMOKINES, CC; CHEMOKINES, CXC; CHEMOTAXIS, LEUKOCYTE; CONTUSIONS; GENES, T-CELL RECEPTOR BETA; GROWTH SUBSTANCES; INSULIN-LIKE GROWTH FACTOR I; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; LYMPHOCYTE ACTIVATION; LYMPHOKINES; MACROPHAGES; MICE; MICE, TRANSGENIC; MICROGLIA; MYELIN BASIC PROTEINS; MYELITIS; RANTES; RNA, MESSENGER; SIALOGLYCOPROTEINS; SPINAL CORD INJURIES; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTE SUBSETS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 22244481544     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0305-05.2005     Document Type: Article

References (59)

1. Appay V, Dunbar PR, Cerundolo V, McMichael A, Czaplewski L, Rowland-Jones S (2000) RANTES activates antigen-specific cytotoxic T lymphocytes in a mitogen-like manner through cell surface aggregation. Int Immunol 12:1173-1182.
2. Bacon KB, Premack BA, Gardner P, Schall TJ (1995) Activation of dual T cell signaling pathways by the chemokine RANTES. Science 269:1727-1730.
3. + T cells via CD40 ligand. Proc Natl Acad Sci USA 94:599-603.
4. + T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proc Natl Acad Sci USA 96:6873-6878.
5. Barbul A, Breslin RJ, Woodyard JP, Wasserkrug HL, Efron G (1989a) The effect of in vivo T helper and T suppressor lymphocyte depletion on wound healing. Ann Surg 209:479-483.
6. Barbul A, Shawe T, Rotter SM, Efron JE, Wasserkrug HL, Badawy SB (1989b) Wound healing in nude mice: a study on the regulatory role of lymphocytes in fibroplasia. Surgery 105:764-769.
7. Bartholdi D, Schwab ME (1997) Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur J Neurosci 9:1422-1438.
8. Bechmann I, Peter S, Beyer M, Gimsa U, Nitsch R (2001) Presence of B7-2 (CD86) and lack of B7-1 (CD80) on myelin phagocytosing MHC-II positive rat microglia is associated with nondestructive immunity in vivo. FASEB J 15:1086-1088.
9. Blight AR (1994) Effects of silica on the outcome from experimental spinal cord injury: implication of macrophages in secondary tissue damage. Neuroscience 60:263-273.
10. Boztug K, Carson MJ, Pham-Mitchell N, Asensio VC, DeMartino J, Campbell IL (2002) Leukocyte infiltration, but not neurodegeneration, in the CNS of transgenic mice with astrocyte production of the CXC chemokine ligand 10. J Immunol 169:1505-1515.
11. Butovsky O, Hauben E, Schwartz M (2001) Morphological aspects of spinal cord autoimmune neuroprotection: colocalization of T cells with B7-2 (CD86) and prevention of cyst formation. FASEB J 15:1065-1067.
12. Cross AH, Cannella B, Brosnan CF, Raine CS (1990) Homing to central nervous system vasculature by antigen specific lymphocytes. I. Localization of C14-labeled cells during acute, chronic, and relapsing experimental allergic encephalomyelitis. Lab Invest 63:162-170.
13. Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, Luster AD (2002) 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 168:3195-3204.
14. Efron JE, Frankel HL, Lazarou SA, Wasserkrug HL, Barbul A (1990) Wound healing and T-lymphocytes. J Surg Res 48:460-463.
15. Finch CE, Laping NJ, Morgan TE, Nichols NR, Pasinetti GM (1993) TGF-β1 is an organizer of responses to neurodegeneration. J Cell Biochem 53:314-322.
16. Genestier L, Kasibhatla S, Brunner T, Green DR (1999) Transforming growth factor beta1 inhibits Fas ligand expression and subsequent activation-induced cell death in T cells via downregulation of c-Myc. J Exp Med 189:231-239.
17. Glabinski AR, Balasingam V, Tani M, Kunkel SL, Strieter RM, Yong VW, Ransohoff RM (1996) Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. J Immunol 156:4363-4368.
18. Gonzalez R, Glaser J, Liu MT, Lane TE, Keirstead HS (2003) Reducing inflammation decreases secondary degeneration and functional deficit after spinal cord injury. Exp Neurol 184:456-463.
19. Hammarberg H, Lidman O, Lundberg C, Eltayeb SY, Gielen AW, Muhallab S, Svenningsson A, Linda H, Der Meide PH, Cullheim S, Olsson T, Piehl F (2000) Neuroprotection by encephalomyelitis: rescue of mechanically injured neurons and neurotrophin production by CNS-infiltrating T and natural killer cells. J Neurosci 20:5283-5291.
20. Huang D, Han Y, Rani MR, Glabinski A, Trebst C, Sorensen T, Tani M, Wang J, Chien P, O'Bryan S, Bielecki B, Zhou ZL, Majumder S, Ransohoff RM (2000) Chemokines and chemokine receptors in inflammation of the nervous system: manifold roles and exquisite regulation. Immunol Rev 177:52-67.
21. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM (2001) Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193:713-726.
22. Huaux F, Liu T, McGarry B, Ullenbruch M, Xing Z, Phan SH (2003) Eosinophils and T lymphocytes possess distinct roles in bleomycin-induced lung injury and fibrosis. J Immunol 171:5470-5481.
23. Huitinga I, van Rooijen N, de Groot CJ, Uitdehaag BM, Dijkstra CD (1990) Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J Exp Med 172:1025-1033.
24. Inman DM, Steward O (2003) Ascending sensory, but not other long-tract axons, regenerate into the connective tissue matrix that forms at the site of a spinal cord injury in mice. J Comp Neurol 462:431-449.
25. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD (2000) Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J Exp Med 192:1075-1080.
26. Jakeman LB, Guan Z, Wei P, Ponnappan R, Dzwonczyk R, Popovich PG, Stokes BT (2000) Traumatic spinal cord injury produced by controlled contusion in mouse. J Neurotrauma 17:299-319.
27. Jones TB, Basso DM, Sodhi A, Pan JZ, Hart RP, MacCallum RC, Lee S, Whitacre CC, Popovich PG (2002) Pathological CNS autoimmune disease triggered by traumatic spinal cord injury: implications for autoimmune vaccine therapy. J Neurosci 22:2690-2700.
28. Jones TB, Ankeny DP, Guan Z, McGaughy V, Fisher LC, Basso DM, Popovich PG (2004) Passive or active immunization with myelin basic protein impairs neurological function and exacerbates neuropathology after spinal cord injury in rats. J Neurosci 24:3752-3761.
29. Kawakami N, Lassmann S, Li Z, Odoardi F, Ritter T, Ziemssen T, Klinkert WE, Ellwart JW, Bradl M, Krivacic K, Lassmann H, Ransohoff RM, Volk HD, Wekerle H, Linington C, Flugel A (2004) The activation status of neuroantigen-specific T cells in the target organ determines the clinical outcome of autoimmune encephalomyelitis. J Exp Med 199:185-197.
30. Kipnis J, Mizrahi T, Yoles E, Ben-Nun A, Schwartz M (2002) Myelin specific Th1 cells are necessary for post-traumatic protective autoimmunity. J Neuroimmunol 130:78-85.
31. Lagord C, Berry M, Logan A (2002) Expression of TGFbeta2 but not TGFbeta1 correlates with the deposition of scar tissue in the lesioned spinal cord. Mol Cell Neurosci 20:69-92.
32. Logan A, Berry M, Gonzalez AM, Frautschy SA, Sporn MB, Baird A (1994) Effects of transforming growth factor beta 1 on scar production in the injured central nervous system of the rat. Eur J Neurosci 6:355-363.
33. Ma M, Wei T, Boring L, Charo IF, Ransohoff RM, Jakeman LB (2002) Monocyte recruitment and myelin removal are delayed following spinal cord injury in mice with CCR2 chemokine receptor deletion. J Neurosci Res 68:691-702.
34. Ma M, Wei P, Wei T, Ransohoff RM, Jakeman LB (2004) Enhanced axonal growth into a spinal cord contusion injury site in a strain of mouse (129X1/SvJ) with a diminished inflammatory response. J Comp Neurol 474:469-486.
35. Mabon PJ, Weaver LC, Dekaban GA (2000) Inhibition of monocyte/macrophage migration to a spinal cord injury site by an antibody to the integrin alphaD: a potential new anti-inflammatory treatment. Exp Neurol 166:52-64.
36. McTigue DM, Tani M, Krivacic K, Chernosky A, Keiner GS, Maciejewski D, Maki R, Ransohoff RM, Stokes BT (1998) Selective chemokine mRNA accumulation in the rat spinal cord after contusion injury. J Neurosci Res 53:368-376.
37. McTigue DM, Popovich PG, Morgan TE, Stokes BT (2000) Localization of transforming growth factor-beta1 and receptor mRNA after experimental spinal cord injury. Exp Neurol 163:220-230.
38. Mennicken F, Maki R, de Souza EB, Quirion R (1999) Chemokines and chemokine receptors in the CNS: a possible role in neuroinflammation and patterning. Trends Pharmacol Sci 20:73-78.
39. Moser B, Wolf M, Walz A, Loetscher P (2004) Chemokines: multiple levels of leukocyte migration control. Trends Immunol 25:75-84.
40. Muhallab S, Lundberg C, Gielen AW, Lidman O, Svenningsson A, Piehl F, Olsson T (2002) Differential expression of neurotrophic factors and inflammatory cytokines by myelin basic protein-specific and other recruited T cells infiltrating the central nervous system during experimental autoimmune encephalomyelitis. Scand J Immunol 55:264-273.
41. Neumann H, Boucraut J, Hahnel C, Misgeld T, Wekerle H (1996) Neuronal control of MHC class II inducibility in rat astrocytes and microglia. Eur J Neurosci 8:2582-2590.
42. Popovich PG (2000) Immunological regulation of neuronal degeneration and regeneration in the injured spinal cord. Prog Brain Res 128:43-58.
43. Popovich PG, Wei P, Stokes BT (1997) The cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J Comp Neurol 377:443-464.
44. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, Stokes BT (1999) Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 158:351-365.
45. Pu SF, Zhuang HX, Marsh DJ, Ishii DN (1999) Insulin-like growth factor-II increases and IGF is required for postnatal rat spinal motoneuron survival following sciatic nerve axotomy. J Neurosci Res 55:9-16.
46. Pulford BE, Whalen LR, Ishii DN (1999) Peripherally administered insulin-like growth factor-I preserves hindlimb reflex and spinal cord noradrenergic circuitry following a central nervous system lesion in rats. Exp Neurol 159:114-123.
47. Ririe KM, Rasmussen RP, Wittwer CT (1997) Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal Biochem 245:154-160.
48. Sallusto F, Lanzavecchia A, Mackay CR (1998) Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunol Today 19:568-574.
49. Sallusto F, Mackay CR, Lanzavecchia A (2000) The role of chemokine receptors in primary, effector, and memory immune responses. Annu Rev Immunol 18:593-620.
50. Schaffer M, Barbul A (1998) Lymphocyte function in wound healing and following injury. Br J Surg 85:444-460.
51. Schwartz M, Kipnis J (2001) Protective autoimmunity: regulation and prospects for vaccination after brain and spinal cord injuries. Trends Mol Med 7:252-258.
52. Sorensen TL, Tani M, Jensen J, Pierce V, Lucchinetti C, Folcik VA, Qin S, Rottman J, Sellebjerg F, Strieter RM, Frederiksen JL, Ransohoff RM (1999) Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest 103:807-815.
53. Sroga JM, Jones TB, Kigerl KA, McGaughy VM, Popovich PG (2003) Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J Comp Neurol 462:223-240.
54. Steinman L (1996) A few autoreactive cells in an autoimmune infiltrate control a vast population of nonspecific cells: a tale of smart bombs and the infantry. Proc Natl Acad Sci USA 93:2253-2256.
55. Tran EH, Hoekstra K, van Rooijen N, Dijkstra CD, Owens T (1998) Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice. J Immunol 161:3767-3775.
56. Trifilo MJ, Lane TE (2003) Adenovirus-mediated expression of CXCL10 in the central nervous system results in T-cell recruitment and limited neuropathology. J Neurovirol 9:315-324.
57. Tylaska LA, Boring L, Weng W, Aiello R, Charo IF, Rollins BJ, Gladue RP (2002) Ccr2 regulates the level of MCP-1/CCL2 in vitro and at inflammatory sites and controls T cell activation in response to alloantigen. Cytokine 18:184-190.
58. Walsh PT, O'Connor R (2000) The insulin-like growth factor-I receptor is regulated by CD28 and protects activated T cells from apoptosis. Eur J Immunol 30:1010-1018.
59. Wynn TA (2004) Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat Rev Immunol 4:583-594.