Macrophages and microglia in central nervous system injury: Are they helpful or harmful?

Journal of Cerebral Blood Flow and Metabolism

Volumn 23, Issue 4, 2003, Pages 385-394

  Schwartz, Michal ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

CNS disorder; Microglia; Neuroprotection; Protective autoimmunity; Therapeutic vaccination

Indexed keywords

GLATIRAMER; GLUTAMIC ACID; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL MODEL; AUTOIMMUNITY; BRAIN INJURY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; IMMUNE SYSTEM; INFLAMMATION; MACROPHAGE; MICROGLIA; NERVOUS SYSTEM INJURY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; STRESS; T LYMPHOCYTE; VACCINATION;

EID: 0037385159     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.WCB.0000061881.75234.5E     Document Type: Review

References (108)

1. Angelov DN, Waibel S, Guntinas-Lichius O, Lenzen M, Neiss WF, Tomov TL, Yoles E, Palgi O, Kipnis J, Schori H, Reuter A, Ludolph A, Schwartz M (2003) Therapeutic vaccine for acute and chronic motor neuron diseases: implications for ALS. Proc Natl Acad Sci U S A (in press)
2. Barouch R, Schwartz M (2002) Autoreactive T cells induce neurotrophin production by immune and neural cells in injured rat optic nerve: implications for protective autoimmunity. FASEB J 16:1304-1306
3. Basso DM, Beattie MS, Bresnahan JC (1996) Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 139:244-256
4. Bavetta S, Hamlyn PJ, Burnstock G, Lieberman AR, Anderson PN (1999) The effects of FK506 on dorsal column axons following spinal cord injury in adult rats: neuroprotection and local regeneration. Exp Neurol 158:382-393
5. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, Anderson DK, Faden AI, Hsu CY, Noble LJ, Salzman S, Young W (1997) Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148:453-463
6. Behrmann DL, Bresnahan JC, Beattie MS (1994) Modeling of acute spinal cord injury in the rat: neuroprotection and enhanced recovery with methylprednisolone, U-74006F and YM-14673. Exp Neurol 126:61-75
7. Bethea JR, Castro M, Keane RW, Lee TT, Dietrich WD, Yezierski RP (1998) Traumatic spinal cord injury induces nuclear factor-κB activation. J Neurosci 18:3251-3260
8. Bethea JR, Nagashima H, Acosta MC, Briceno C, Gomez F, Marcillo AE, Loor K, Green J, Dietrich WD (1999) Systemically administered interleukin-10 reduces tumor necrosis factor-α production and significantly improves functional recovery following traumatic spinal cord injury in rats. J Neurotrauma 16:851-863
9. Blight AR (1989) Effect of 4-aminopyridine on axonal conduction-block in chronic spinal cord injury. Brain Res Bull 22:47-52
10. Bracken MB (1991) Treatment of acute spinal cord injury with methylprednisolone: results of a multicenter, randomized clinical trial. J Neurotrauma 8(suppl 1):S47-S50; discussion S51-42
11. Bracken MB, Holford TR (1993) Effects of timing of methylprednisolone or naloxone administration on recovery of segmental and long-tract neurological function in NASCIS 2. J Neurosurg 79:500-507
12. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640
13. 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
14. Cai D, Deng K, Mellado W, Lee J, Ratan RR, Filbin MT (2002) Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 35:711-719
15. Caroni P, Schwab ME (1988) Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J Cell Biol 106:1281-1288
16. Chatzipanteli K, Yanagawa Y, Marcillo AE, Kraydieh S, Yezierski RP, Dietrich WD (2000) Posttraumatic hypothermia reduces polymorphonuclear leukocyte accumulation following spinal cord injury in rats. J Neurotrauma 17:321-332
17. Cheng H, Cao Y, Olsen L (1996) Spinal cord repair in adult paraplegic rats: Partial restoration of hind limb function. Science 273:510-513
18. Chong MS, Woolf CJ, Haque NS, Anderson PN (1999) Axonal regeneration from injured dorsal roots into the spinal cord of adult rats. J Comp Neurol 410:42-54
19. Constantini S, Young W (1994) The effects of methylprednisolone and the ganglioside GMI on acute spinal cord injury in rats. J Neurosurg 80:97-111
20. Coumans JV, Lin TT, Dai HN, MacArthur L, McAtee M, Nash C, Bregman BS (2001) Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J Neurosci 21:9334-9344
21. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS (1997) Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3:73-76
22. Cserr HF, Knopf PM (1992) Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: a new view. Immunol Today 13:507-512
23. Cserr HF, Harling-Berg CJ, Knopf PM (1992) Drainage of brain extracellular fluid into blood and deep cervical lymph and its immunological significance. Brain Pathol 2:269-276
24. Czech KA, Ryan JW, Sagen J, Pappas GD (1997) The influence of xenotransplant immunogenicity and immunosuppression on host MHC expression in the rat CNS. Exp Neurol 147:66-83
25. David S, Aguayo AJ (1981) Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214:931-933
26. Davies SJ, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-683
27. Eikelenboom P, Bate C, Van Gool WA, Hoozemans JJ, Rozemuller JM, Veerhuis R, Williams A (2002) Neuroinflammation in Alzheimer's disease and prion disease. Glia 40:232-239
28. Faden AI (1993) Experimental neurobiology of central nervous system trauma. Crit Rev Neurobiol 7:175-186
29. Fisher J, Levkovitch-Verbin H, Schori H, Yoles E, Butovsky O, Kaye JF, Ben-Nun A, Schwartz M (2001) Vaccination for neuroprotection in the mouse optic nerve: implications for optic neuropathies. J Neurosci 21:136-142
30. Flugel A, Berkowicz T, Ritter T, Labeur M, Jenne DE, Li Z, Ellwart JW, Willem M, Lassmann H, Wekerle H (2001) Migratory activity and functional changes of green fluorescent effector cells before and during experimental autoimmune encephalomyelitis. Immunity 14:547-560
31. Franzen R, Schoenen J, Leprince P, Joosten E, Moonen G, Martin D (1998) Effects of macrophage transplantation in the injured adult rat spinal cord: a combined immunocytochemical and biochemical study. J Neurosci Res 51:316-327
32. Ghirnikar RS, Lee YL, Eng LF (2000) Chemokine antagonist infusion promotes axonal sparing after spinal cord contusion injury in rat. J Neurosci Res 59:63-73
33. Grady MS, Steward O, Jane JA (1985) Transplantation of embryonic chick spinal cord into transection adult chicken spinal cords: a useful model for transplantation research. J Neurosci Res 14:403-414
34. Griffin D, Levine B, Tyor W, Ubol S, Despres P (1997) The role of antibody in recovery from alphavirus encephalitis. Immunol Rev 159:155-161
35. Gruner JA, Yee AK, Blight AR (1996) Histological and functional evaluation of experimental spinal cord injury: evidence of a stepwise response to graded compression. Brain Res 729:90-101
36. Hailer NP, Bechmann I, Heizmann S, Nitsch R (1997) Adhesion molecule expression on phagocytic microglial cells following anterograde degeneration of perforant path axons. Hippocampus 7:341-349
37. Harel A, Fainaru M, Shafer Z, Hernandez M, Cohen A, Schwartz M (1989) Optic nerve regeneration in adult fish and apolipoprotein A-I. Neurochem 52:1218-1228
38. Hauben E, Schwartz M (2003) Therapeutic vaccination for spinal cord injury: helping the body to cure itself. Trends Pharmacol Sci 24:7-12
39. Hauben E, Agranov E, Gothilf A, Nevo U, Cohen A, Smirnov I, Steinman L, Schwartz M (2001) Posttraumatic therapeutic vaccination with modified myelin self-antigen prevents complete paralysis while avoiding autoimmune disease. J Clin Invest 108:591-599
40. Hauben E, Butovsky O, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Leibowitz-Amit R, Pevsner E, Akselrod S, Neeman M, Cohen IR, Schwartz M (2000a) Passive or active immunization with myelin basic protein promotes recovery from spinal cord contusion. J Neurosci 20:6421-6430
41. Hauben E, Nevo U, Yoles E, Moalem G, Agranov E, Leibowitz-Amit R, Mor F, Pevsner E, Akselrod S, Neeman M, Cohen IR, Schwartz M (2000b) Autoimmune T cells - potential neuroprotection therapy for spinal cord injury. Lancet 355:286-287
42. Hess PR, Sellon RK (1997) Steroid-responsive, cervical, pyogranulomatous pachymeningitis in a dog. J Am Anim Hosp Assoc 33:461-468
43. Heumann R, Lindholm D, Bandtlow C, Meyer M, Radeke MJ, Misko TP, Shooter E, Thoenen H (1987) Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc Natl Acad Sci U S A 84:8735-8739
44. Hickey WF, Hsu BL, Kimura H (1991) T-lymphocyte entry into the central nervous system. J Neurosci Res 28:254-260
45. Ignatius MJ, Skene JH, Muller HW, Shooter EM (1987) Examination of a nerve injury-induced, 37 kDa protein: purification and characterization. Neurochem Res 12:967-976
46. Kalb LY (1995) Recovery from spinal cord injury: new approaches. Neuroscientist 1:321-327
47. Kerchensteiner M, Gallmeier E, Behrens L, Leal VV, Misgeld T, Klinkert WE, Kolbeck R, Hoppe E, Oropeza-Wekerle RL, Bartke I, Stadelmann C, Lassmann H, Wekerle H, Hohlfeld R (1999) Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: a neuroprotective role of inflammation? J Exp Med 189:865-870.
48. + regulatory T cells suppress the ability to withstand injury to the central nervous system. Proc Natl Acad Sci U S A 99:15620-15625
49. Kipnis J, Mizrahi T, Yoles E, Ben-Nun A, Schwartz M (2002b) Myelin specific Th1 cells are necessary for post-traumatic protective autoimmunity. J Neuroimmunol. 130:78-85
50. Kipnis J, Schwartz M (2002) Dual action of glatiramer acetate (Cop-I) in the treatment of CNS autoimmune and neurodegenerative disorders. Trends Mol Med 8:319-323
51. Kipnis J, Yoles E, Porat Z, Cohen A, Mor F, Sela M, Cohen IR, Schwartz M (2000) T cell immunity to copolymer I confers neuroprotection on the damaged optic nerve: possible therapy for optic neuropathies. Proc Natl Acad Sci U S A 97:7446-7451
52. Kipnis J, Yoles E, Schori H, Hauben E, Shaked I, Schwartz M (2001) Neuronal survival after CNS insult is determined by a genetically encoded autoimmune response. J Neurosci 21:4564-4571
53. Lazarov-Spiegler O, Solomon AS, Zeev-Brann AB, Hirschberg DL, Lavie V, Schwartz M (1996) Transplantation of activated macrophages overcomes central nervous system regrowth failure. FASEB J 10:1296-1302
54. Li Y, Field PM, Raisman G (1997) Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277:2000-2002
55. Lindholm D, Heumann R, Hengerer B, Thoenen H (1988) Interleukin-1 increases stability and transcription of mRNA encoding nerve growth factor in cultured rat fibroblasts. J Biol Chem 263:16348-16351
56. Lindholm D, Heumann R, Meyer M, Thoenen H (1987) Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciatic nerve. Nature 330:658-659
57. Lotan M, Schwartz M (1994) Cross talk between the immune system and the nervous system in response to injury: implications for regeneration. FASEB J 8:1026-1033
58. Lue LF, Walker DG (2002) Modeling Alzheimer's disease immune therapy mechanisms: interactions of human postmortem microglia with antibody-opsonized amyloid beta peptide. J Neurosci Res 70:599-610
59. Magnus T, Chan A, Linker RA, Toyka KV, Gold R (2002) Astrocytes are less efficient in the removal of apoptotic lymphocytes than microglia cells: implications for the role of glial cells in the inflamed central nervous system. J Neuropathol Exp Neurol 61:760-766
60. McGeer PL, McGeer EG (2002) Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 26:459-470
61. McKerracher L (2002) Ganglioside rafts as MAG receptors that mediate blockade of axon growth. Proc Natl Acad Sci U S A 99:7811-7813
62. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994) Identification of myelin-derived inhibitor of neurite growth. Neuron 13:805-811
63. Medawar PB (1948) Immunity to homologous grafted skin. Part III: the fate of skin homografts transplanted to the brain, to subcutaneus tissue and to the anterior chamber of the eye. Br J Exp Pathol 29:58
64. Miwa T, Furukawa S, Nakajima K, Furukawa Y, Kohsaka S (1997) Lipopolysaccharide enhances synthesis of brain-derived neurotrophic factor in cultured rat microglia. J Neurosci Res 50:1023-1029
65. Mizrahi T, Hauben E, Schwartz M (2002) The tissue-specific self-pathogen is the protective self-antigen: the case of uveitis. J Immunol 169:5971-5977
66. Moalem G, Gdalyahu A, Shani Y, Otten U, Lazarovici P, Cohen IR, Schwartz M (2000) Production of neurotrophins by activated T cells: implications for neuroprotective autoimmunity. J Autoimmun 15:331-345
67. Moalem G, Leibowitz-Amit R, Yoles E, Mor F, Cohen IR, Schwartz M (1999a) Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy. Nat Med 5:49-55
68. Moalem G, Monsonego A, Shani Y, Cohen IR, Schwartz M (1999b) Differential T cell response in central and peripheral nerve injury: connection with immune privilege. FASEB J 13:1207-1217
69. 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
70. Neumann S, Woolf CJ (1999) Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23:83-91
71. Nevo U, Hauben E, Yoles E, Agranov E, Akselrod S, Schwartz M, Neeman M (2001) Diffusion anisotropy MRI for quantitative assessment of recovery in injured rat spinal cord. Magn Reson Med 45:1-9
72. Olsson T, Lidman O, Piehl F (2003) Harm or heal - divergent effects of autoimmune neuroinflammation? Trends Immunol 24:5-6
73. Polazzi E, Contesabile A (2002) Reciprocal interactions between microglia and neurons: from survival to neuropathology. Rev Neurosci 13:221-242
74. 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
75. Popovich PG, Stokes BT, Whitacre CC (1996) Concept of autoimmunity following spinal cord injury: possible roles for T lymphocytes in the traumatized central nervous system. J Neurosci Res 45:349-363
76. Popovich PG, Stuckman S, Gienapp IE, Whitacre CC (2001) Alterations in immune cell phenotype and function after experimental spinal cord injury. J Neurotrauma 18:957-966.
77. Povlishock JT, Jenkins LW (1995) Are the pathological changes evoked by traumatic brain injury immediate and irreversible? Brain Pathol 5:415-426
78. Prewitt C, Niesman I, Kane CJ, Houle JD (1997) Activated macrophage/microglial cells can promote the regeneration of sensory axons into the injured spinal cord. Exp Neurol 148:433-443
79. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT (2002) Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895-903
80. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, Hadani M, Schwartz M (1998) Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 4:814-821
81. Reier PJ, Stokes BT, Thompson FJ, Anderson DK (1992) Fetal cell grafts into resection and contusion/compression injuries of the rat and cat spinal cord. Exp Neurol 115:177-188
82. Rudge JS, Silver J (1990) Inhibition of neurite outgrowth on astroglial scars in vitro. J Neurosci 10:3594-3603
83. Sanner C, Elliott JL, Snider WD (1994) Upregulation of NMDARI mRNA induced by MK-801 is associated with massive death of axotomized motor neurones in adult rats. Neurobiol Dis 1:121-129
84. Schnell L, Schwab ME (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343:269-272
85. Schori H, Kipnis J, Yoles E, WoldeMussie E, Ruiz G, Wheeler LA, Schwartz M (2001a) Vaccination for protection of retinal ganglion cells against death from glutamate cytotoxicity and ocular hypertension: implications for glaucoma. Proc Nad Acad Sci U S A 98:3398-3403
86. Schori H, Yoles E, Schwartz M (2001b) T-cell-based immunity counteracts the potential toxicity of glutamate in the central nervous system. J Neuroimmunol 119:199-204
87. Schwab ME, Bartholdi D (1996) Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 76:319-370
88. Schwab ME, Caroni P (1988) Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. J Neurosci 8:2381-2393
89. Schwab ME, Thoenen H (1985) Dissociated neurons regenerate into sciatic but not optic nerve explants in culture irrespective of neurotrophic factors. J Neurosci 5:2415-2423
90. Schwartz M, Hauben E (2002) Differing views on spinal cord repair. Science 296:1400.
91. Schwartz M, Kipnis J (2002a) Autoimmunity on alert: naturally occurring regulatory CD4+CD25+ T cells as part of the evolutionary compromise between a "need" and a "risk". Trends Immunol 23:530-534
92. Schwartz M, Kipnis J (2002b) Multiple sclerosis as a by-product of the failure to sustain protective autoimmunity: a paradigm shift. Neuroscientist 8:405-413
93. Schwartz M, Cohen I, Lazarov-Spiegler O, Moalem G, Yoles E (1999a) The remedy may lie in ourselves: prospects for immune cell therapy in central nervous system protection and repair [InProcess Citation]. J Mol Med 77:713-717
94. Schwartz M, Moalem G, Leibowitz-Amit R, Cohen IR (1999b) Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci 22:295-299
95. Shibata A, Wright MV, David S, McKerracher L, Braun PE, Kater SB (1998) Unique responses of differentiating neuronal growth cones to inhibitory cures presented by oligodendrocytes. J Cell Biol 142:191-202
96. Shrikant P, Benveniste EN (1996) The central nervous system as an immunocompetent organ: role of glial cells in antigen presentation. J Immunol 157:1819-1822
97. Srebro Z, Dziobek K (2001) Neuroprotection: the role of neuroglia. Folia Med Cracov 42:113-121
98. Streilein JW (1993) Immune privilege as the result of local tissue barriers and immunosuppressive microenvironments. Curr Opin Immunol 5:428-432
99. Streilein JW (1995) Unraveling immune privilege. Science 270:1158-1159
100. Taylor DL, Diemel LT, Cuzner ML, Pocock JM (2002) Activation of group II metabotropic glutamate receptors underlies microglial reactivity and neurotoxicity following stimulation with chromogranin A, a peptide up-regulated in Alzheimer's disease. J Neurochem 82:1179-1191
101. Tuszynski MH, Gage FH (1995) Bridging grafts and transient nerve growth factor infusions promote long-term central nervous system neuronal rescue and partial functional recovery. Proc Natl Acad Sci U S A 92:4621-4625
102. Wang XM, Terman JR, Martin GF (1998) Regeneration of supraspinal axons after transection of the thoracic spinal cord in the developing opossum, Didelphis virginiana. J Comp Neurol 398:83-97
103. Xu XM, Chen A, Guenard V, Kleitman N, Bunge MB (1997) Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J Neurocytol 26:1-16
104. Yoles E, Hauben E, Palgi O, Agranov E, Gothilf A, Cohen A, Kuchroo V, Cohen IR, Weiner H, Schwartz M (2001) Protective autoimmunity is a physiological response to CNS trauma. J Neurosci 21:3740-3748
105. Yoles E, Schwartz M (1998) Degeneration of spared axons following partial white matter lesion: implications for optic nerve neuropathies. Exp Neurol 153:1-7
106. Yong C, Arnold PM, Zoubine MN, Citron BA, Watanabe I, Berman NE, Festoff BW (1998) Apoptosis in cellular compartments of rat spinal cord after severe contusion injury. J Neurotrauma 15:459-472
107. Young W, Kume-Kick J, Constantini S (1994) Glucocorticoid therapy of spinal cord injury. Ann NY Acad Sci 743:241-263
108. Zuo J, Ferguson TA, Hernandez YJ, Stetler-Stevenson WG, Muir D (1998) Neuronal matrix metalloproteinase-2 degrades and inactivates a neurite-inhibiting chondroitin sulfate proteoglycan. J Neurosci 18:5203-5211