Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth

Journal of Neuroscience Research

Volumn 47, Issue 1, 1997, Pages 34-48

  Rabchevsky, A G ^a,b   Streit, W J ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b Lab Physiologie et Pharmacologie   (France)

Author keywords

brain macrophage; inflammation; OX 42; regeneration; transplantation

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL TRANSPLANTATION; MICROGLIA; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SCHWANN CELL; SPINAL CORD LESION;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BIOLOGICAL MARKERS; CELL COMMUNICATION; CELL DIVISION; CELLS, CULTURED; DATA INTERPRETATION, STATISTICAL; FLUORESCENT ANTIBODY TECHNIQUE; GELATIN SPONGE, ABSORBABLE; HOST VS GRAFT REACTION; LAMININ; LIPOPOLYSACCHARIDES; MICROCIRCULATION; MICROGLIA; NERVE REGENERATION; NEURITES; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES;

EID: 0031022698     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19970101)47:1<34::AID-JNR4>3.0.CO;2-G     Document Type: Article

References (70)

1. Aguayo A, David S, Richardson P, Bray G (1982): Axonal elongation in peripheral and central nervous system transplants. Adv Cell Neurobiol 3:215-234.
2. Bahr M, Przyrembel C, Bastmeyer M (1995): Astrocytes from adult optic nerves are nonpermissive for regenerating retinal ganglion cell axons. Exp Neurol 131:211-220.
3. Banati RB, Gerhmann J, Schubert P, Kreutzberg GW (1993): Cytotoxicity of microglia. Glia 7:111-118.
4. Bernstein JJ, Getz R, Jefferson M, Keleman M (1985): Astrocytes secrete basal lamina after hemisection of rat spinal cord. Brain Res 327:135-141.
5. Chamak B, Mallat M (1991): Fibronectin and laminin regulate the in vitro differentiation of microglial cells. Neuroscience 45:513-527.
6. Chamak B, Morandi V, Mallat M (1994): Brain macrophages stimulate neurite growth and regeneration by secreting thrombospondin. J Neurosci Res 38:221-233.
7. Chamak B, Dobbertin A, Mallat M (1995): Immunohistochemical detection of thrombospondin in microglia in the developing rat brain. Neuroscience 69:177-187.
8. Chao CC, Hu S, Molitor TW, Shaskan EG, Peterson PK (1992): Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol 149:2736-2741.
9. Colton CA, Gilbert DL (1987): Production of superoxide by a CNS macrophage, the microglia. FEBS Letts 223:284-288.
10. Constam DB, Phillip J, Malipiero UV, ten Dijke P, Schachner M, Fontana A (1992): Differential expression of transforming growth factor-β1, β2 and β3 by gliobastoma cells, astrocytes, and microglia. J Immunol 148:1404-1410.
11. David S, Bouchard C, Tsatas O, Giftochristos N (1990): Macrophages can modify the nonpermissive nature of the adult mammalian central nervous system. Neuron 5:463-469.
12. Dusart I, Schwab ME (1993): Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 6:712-724.
13. Eddleston M, Mucke L (1993): Molecular profile of reactive astrocytes-implications for their role in neurological disease. Neuroscience 54:15-36.
14. Elkabes S, DiCicco-Bloom EM, Black IB (1995): Brain microglia/ macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16:2505-2521.
15. Fagan AM, Gage FH (1990): Cholinergic sprouting in the hippocampus: a proposed role for IL-1. Exp Neurol 110:105-120.
16. Fagan AM, Gage FH (1994): Mechanisms of sprouting in the adult central nervous system: cellular responses in areas of terminal degeneration and reinnervation in the rat hippocampus. Neuroscience 58:705-725.
17. 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.
18. Frei K, Siepl C, Groscurth P, Bodmer S, Schwerdel C, Fontana A (1987): Antigen presentation and tumor cytotoxicity by interferon-g-treated microglial cells. Eur J Immunol 17:1271-1278.
19. Giulian D (1990): Microglia, cytokines, and cytotoxins: modulators of cellular responses after injury to the central nervous system. J Immunol Immunopharmacol 10:15-21.
20. Giulian D, Baker TJ, Shih L-CN, Lachman LB (1986): Interleukin-1 of the central nervous system is produced by ameboid microglia. J Exp Med 164:594-604.
21. Giulian D, Corpuz M, Chapman S, Mansouri M, Robertson C (1993): Reactive mononuclear phagocytes release neurotoxins after ischemic and traumatic injury to the central nervous system. J Neurosci Res 36:681-693.
22. Guth LJ, Barrett CP, Donati EJ, Anderson FD, Smith MV, Lifson M (1985): Essentiality of a specific cellular terrain for growth of axons into a spinal cord lesion. Exp Neurol 88:1-12.
23. Harvey AR, Fan Y, Connor AM, Grounds MD, Beilharz MW (1993): The migration and intermixing of donor and host glia on nitrocellulose polymers implanted into cortical lesion cavities in adult mice and rats. Int J Dev Neurosci 11:569-581.
24. Metier E, Ayala J, Denefle P, Bousseau A, Rouget P, Mallat M, Prochiantz A (1988): Brain macrophages synthesize interleukin-1 and interleukin-1 mRNAs in vitro. J Neurosci Res 21: 391-397.
25. Hoffman JR, Dixit VM, O'Shea SK (1994): Expression of thrombospondin in the adult nervous system. J Comp Neurol 340:126-139.
26. Houle JD, Kane CJM (1995): Macrophage-related effects on the regeneration of sensory axons into the injured spinal cord. Soc Neurosci Abstr 21:819.
27. Kiefer R, Gold R, Gehrmann J, Lindholm D, Wekerle H, Kreutzberg GW (1993): Transforming growth factor-beta expression in reactive spinal cord microglia and meningeal inflammatory cells during experimental allergic neuritis. J Neurosci Res 36:391-398.
28. Kiefer R, Streit WJ, Toyka KV, Kreutzberg GW, Hartung HP (1995): Transforming growth factor-beta: a lesion-associated cytokine of the nervous system. Int J Dev Neurosci 13:331-339.
29. Klagsbrun M, D'Amore PA (1991): Regulators of angiogenesis. Annu Rev Physiol 53:217-239.
30. Kohsaka S, Nakajima K, Hamanoue M, Koizumi S, Inoue K (1994): Microglia-derived plasminogen has neurotrophic effects on the CNS neurons in vitro (abstract). Neuropathol Appl Neurobiol 20:190.
31. Li Y, Raisman G (1995): Sprouts from cut corticospinal axons persist in the presence of astrocytic scarring in longterm lesions of the adult rat spinal cord. Exp Neurol 134:102-111.
32. Liesi P, Kaakkola S, Dahl D, Vaheri A (1984): Laminin is induced in astrocytes of adult brain by injury. EMBO J 3:683-686.
33. Liuzzi FJ, Lasek RJ (1987): Astrocytes block axonal regeneration in mammals by activating the physiological stop pathway. Science 237:642-645.
34. Lu X, Richardson PM (1991): Inflammation near the nerve cell body enhances axonal regeneration. J Neurosci 11:972-978.
35. Lu X, Richardson PM (1993): Responses of macrophages in rat dorsal root ganglia following peripheral nerve injury. J Neurocytol 22:334-341.
36. Mallat M, Houlgatte R, Brachet P, Prochiantz A (1989): Lipopolysaccharide-stimulated rat brain macrophages release NGF in vitro. Dev Biol 133:309-311.
37. Marty S, Dusart I, Peschanski M (1991): Glial changes following an exitotoxic lesion in the CNS. I. Microglia/macrophages. neuroscience 45:529-539.
38. Masuda-Nakagawa LM, Muller KJ, Nicholls JG (1993): Axonal sprouting and laminin appearance after destruction of glial sheathes. Proc Natl Acad Sci USA 90:4966-4970.
39. McCarthy KD, De Vellis J (1980): Preparation of separate astroglial and oligodendrogial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
40. McKeon RJ, Schreiber RC, Rudge JS, Silver J (1991): Reduction of neunte outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398-3411.
41. McKeon RJ, Hoke A, Silver J (1995): Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp Neurol 136:32-43.
42. Morshead CM, VanderKooy D (1990): Separate blood and brain origins of proliferating cells during gliosis in adult brain. Brain Res 535:237-244.
43. Nagata K, Nakajima K, Takemoto N, Saito H, Kohsaka S (1993a): Microglia-derived plasminogen enhances neunte outgrowth from explant culture of rat brain. Int J Dev Neurosci 11:227-237.
44. Nagata K, Takei N, Nakajima K, Saito H, Kohsaka S (1993b): Microglia conditioned medium promotes survival and development of cultured mesencephalic neurons from embryonic rat brain. J Neurosci Res 34:357-363.
45. Nakajima K, Hamanoue M, Shimojo M, Takei N, Kohsaka S (1989): Characterization of microglia isolated from a primary culture of embryonic rat brain by a simplified method. Biomed Res 10: 411-423.
46. Nakajima K, Nagata K, Hamanoue M, Takemoto N, Kohsaka S (1993): Microglia-derived elastase produces a low-molecular weight plasminogen that enhances neunte outgrowth in rat neocortical explant cultures. J Neurochem 61:2155-2163.
47. O'Shea KS, Liu L-H, Dixit VM (1991): Thrombospondin and a 140 kD fragment promote adhesion and neunte outgrowth from embryonic central and peripheral neurons and PC 12 cells. Neuron 7:231-237.
48. Paino CL, Fernandez-Valle C, Bates ML, Bunge MB (1994): Regrowth of axons in lesioned adult rat spinal cord: promotion by implants of cultured Schwann cells. J Neurocytol 23:433-452.
49. Piani D, Frei K, Do KQ, Cuenod M, Fontana A (1991): Murine brain macrophages induce NMDA receptor mediated neurotoxicity in vitro by secreting glutamate. Neurosci Lett 133:159-162.
50. Rabchevsky AG, Streit WJ, Reier PJ (1993): Transplantation of fluorescently-labeled microglia into the adult rat spinal cord. Soc Neurosci Abstr 19:57.
51. Rabchevsky AG, Streit WJ, Reier PJ (1994): Intraspinal transplantation of enriched microglia seeded within biodegradable polymeric tubes: evidence for neuritic ingrowth. Soc Neurosci Abstr 20:879.
52. Rabchevsky AG, Streit WJ, Reier PJ (1995): Transplantation of brain macrophages (BrM) embedded in gelfoam into the injured rat spinal cord: evidence for neuritic ingrowth and the presence of extracellular matrix (abstr). J Neurotrauma 12:136.
53. Reier PJ, Stensaas LJ, Guth L (1983): The astrocytic scar as an impediment to regeneration in the central nervous system. In Kao CC, Bunge RP, Reier PJ (eds): "Spinal Cord Reconstruction." New York: Raven Press, pp 163-195.
54. Remick DG, Scales WE, May MA, Spengler M, Nguyen D, Kunkel SL (1988): In situ hybridization analysis of macrophage-derived tumor necrosis factor and interleukin-1 mRNA. Lab Invest 59:809-816.
55. Ridley AJ, Davis JB, Stroobant P, Land H (1989): Transforming growth factors-β1 and -β2 are mitogens for rat Schwann cells. J Cell Biol 109:3419-3424.
56. Risling M, Cullheim S, Hildebrand C (1983): Reinnervation of the ventral root L7 from ventral horn neurons following intramedullary axotomy in adult cats. Brain Res 2801:15-23.
57. Sanes J (1983): Role of extracellular matrix in neural development. Ann Rev Physiol 45:581-600.
58. Semple-Rowland SL Mahatme A, Popovich PG, Green DA, Hassler G Jr, Stokes BT, Streit WJ (1995): Analysis of TGF-β1 gene expression in contused rat spinal cord using quantitative RT-PCR. J Neurotrauma 12:1003-1014.
59. Shimojo M, Nakajima K, Takei N, Hamanoue M, Kohsaka S (1991): Production of basic fibroblast growth factor in cultured rat brain microglia. Neurosci Lett. 123:229-231.
60. Stichel CC, Muller HW (1994a): Extension and long-lasting changes of glial cells following transection of the postcommissural fornix in the adult rat. Glia 10:89-100.
61. Stichel CC, Muller HW (1994b): Relationship between injury-induced astrogliosis, laminin expression and axonal sprouting in the adult rat brain. J Neurocytol 23:615-630.
62. Streit WJ (1993): Microglial-neuronal interactions. J Chem Neuroanat 6:261-266.
63. Streit WJ, Graeber MB (1991): Perivascular location and phenotypic heterogeneity of microglial cells in the rat brain. J Neuroimmunol 33:87.
64. Streit WJ, Graeber MB (1993): Heterogeneity of microglial and perivascular cell populations: insights gained from the facial nucleus paradigm. Glia 7:68-74.
65. Streit WJ, Kreutzberg GW (1988): Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J Comp Neurol 268:248-263.
66. Thanos S, Mey J, Wild M (1993): Treatment of the adult retina with microglia-suppressing factors retards axotomy induced neuronal degeneration and enhances axonal regeneration in vivo and in vitro. J Neurosci 13:455-466.
67. Vaca K, Wendt E (1992): Divergent effects of astroglial and microglial secretions on neuron growth and survival. Exp Neurol 118:62-72.
68. Wang JJ, Chuah MI, Yew DTW, Leung PC, Tsang DSC (1995): Effects of astrocyte implantation into the hemisected adult rat spinal cord. Neuroscience 65:973-981.
69. Woodroofe MN, Sarna GS, Wadhwa M, Hayes GM, Loughlin AJ, Tinker A, Cuzner ML (1991): Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: evidence of a role for microglia in cytokine production. J Neuroimmunol 33:227-236.
70. Xu XM, Guenard V, Chen A, Kleitman N, Bunge MB (1995): Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J Comp Neurol 351:145-160.