Effects of macrophage transplantation in the injured adult rat spinal cord: A combined immunocytochemical and biochemical study

Journal of Neuroscience Research

Volumn 51, Issue 3, 1998, Pages 316-327

  Franzen, Rachelle ^a   Schoenen, Jean ^a,c   Leprince, Pierre ^a   Joosten, Elbert ^b   Moonen, Gustave ^a   Martin, Didier ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Angiogenesis; Axonal regeneration; CNS; Macrophages; Myelin; Neural transplantation

Indexed keywords

ACIDIC FIBROBLAST GROWTH FACTOR; BASIC FIBROBLAST GROWTH FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCITONIN GENE RELATED PEPTIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; MYELIN; MYELIN ASSOCIATED GLYCOPROTEIN; NERVE GROWTH FACTOR; NEUROFILAMENT PROTEIN; NEUROTROPHIN 3; SEROTONIN; TUMOR NECROSIS FACTOR ALPHA;

ANGIOGENESIS; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; IMMUNOCYTOCHEMISTRY; MACROPHAGE; NERVE FIBER REGENERATION; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD INJURY;

ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CELLS, CULTURED; FEMALE; GROWTH SUBSTANCES; IMMUNOHISTOCHEMISTRY; MACROPHAGES, PERITONEAL; MICROSPHERES; NEURONS; POLYMERASE CHAIN REACTION; RATS; RATS, WISTAR; RNA, MESSENGER; SPINAL CORD INJURIES; TRANSCRIPTION, GENETIC;

EID: 0032006114     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19980201)51:3<316::AID-JNR5>3.0.CO;2-J     Document Type: Article

References (57)

1. Aguayo AJ, David S (1981): Axonal elongation into PNS "bridges" after CNS injury in adult rat. Science 214:931-933.
2. Araujo DM, Cotman CWW (1992): Basic FGF in ustroglial, microglial and neuronal cultures: Characterization of binding sites and modulation of release by lymphokines and trophic factors. Dev Biol 133:309-311.
3. Avellino AM, Hart D, Dailey AT, Mackinnon M, Ellegala D, Kliot M (1995): Differential macrophage responses in the peripheral and central nervous system during Wallerian degeneration of axons. Exp Neurol 136:183-198.
4. Bedi KS, Winter J, Berry M, Cohen J (1992): Adult rat dorsal root ganglion neurons extend neurites on predegenerated but not on normal peripheral nerves in vitro. Eur J Neurosci 4:193-200.
5. Bernstein JJ, Getz R, Jefferson M, Keleman M (1985): Astrocytes secrete basal lamina after hemisection of rat spinal cord. Brain Res 327:135-141.
6. Bisby MA, Chen S (1990): Delayed Wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons. Brain Res 530:117-120.
7. Brown MC, Perry VH, Hunt SP, Lapper SR (1994): Further studies on motor and sensory nerve regeneration in mice with delayed Wallerian degeneration. Eur J Neurosci 6:420-128.
8. Chamak B, Morandi V, Mallat M (1994): Brain macrophages stimulate neurite growth and regeneration by secreting thrombospondin. J Neurosci Res 38:221-233.
9. Chen S, Bisby MA (1993): Impaired motor axons regeneration in the C57BL/Ola mouse. J Comp Neurol 333:449-454.
10. Chomczynski P, Sacchi N (1987): Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
11. Dahlin LB (1995): Prevention of macrophage invasion impairs regeneration in nerve grafts. Brain Res 679:274-280.
12. 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.
13. David S, Braun PE, Jackson DL, Kottis V, McKerracher L (1995): Laminin overrides the inhibitory effects of PNS and CNS myelin-derived inhibitors of neurite growth. J Neurosci Res 42:594-602.
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. Filbin MT (1995): Myelin-associated glycoprotein: A role in myelination and in the inhibition of axonal regeneration. Curr Opin Neurobiol 5:588-595.
16. Frei K, Malipiero UV, Leist TP, Zinkernagel RM, Schwab ME, Fontana A (1989): On the cellular source and function of interleukin 6 produced in the central nervous system in viral diseases. Eur J Immunol 19:689-694.
17. Fryer HJL, Davis GE, Manthorpe M, Varon S (1986): Lowry protein assay using an automatic microtiter plate spectrophotometer. Anal Biochem 153:262-266.
18. George R, Griffin JW (1994): Delayed macrophage responses and myelin clearance during Wallerian degeneration in the central nervous system: the dorsal radiculotomy model. Exp Neurol 129:225-236.
19. Giulian D, Robertson C (1990): Inhibition of mononuclear phagocytes reduces ischemic injury in the spinal cord. Ann Neurol 27: 33-42.
20. Giulian D, Chen J, Ingeman JE, George JK, Noponen M (1989): The role of mononuclear phagocytes in wound healing after traumatic injury to adult mammalian brain. J Neurosci 9:4416-4429.
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. Griffin JW, George R, Lobato C, Tyor WR, Chun Van L, Glass JD (1992): Macrophage responses ans myelin clearance during Wallerian degeneration: Relevance to immune-mediated demyelinalion. Neuroimmunol 40:153-166.
23. Gundersen RW, Barren JN (1979): Neuronal chemotaxis: Chick dorsal root axons turn toward high concentrations of nerve growth factor. Science 206:1079-1080.
24. Guth L, Reier PJ, Barren CP, Donati EJ (1983): Repair of the mammalian spinal cord. Trends Neurosci: 20-24.
25. Hikawa N, Takenaka T (1996): Myelin-stimulated macrophages release neurotrophic factors for adult dorsal root ganglion neurons in culture. Cell Mol Neurobiol 16:517-528.
26. Hikawa N, Horie H, Takenaka T (1993): Macrophage-enhanced neurite regeneration of adult dorsal root ganglia neurones in culture. Neuroreport 5:41-44.
27. Jaffe EA, Ruggiero JT, Falcone DJ (1985): Monocytes and macrophages synthesize and secrete thrombospondin. Blood 65: 79-84.
28. Jelsma T, Aguayo AJ (1994): Trophic factors. Current Biol 4:717-725.
29. 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.
30. Lazarov-Spiegler O, Solomon AS, Zeev-Brann AB, Hirschberg DL, Lavie V, Schwanz M (1996): Transplantation of activated macrophages overcomes central nervous system regrowth failure. FASEB J 10:1296-1302.
31. Leibovich SJ, Polverini PJ, Shepard HM, Wiseman DM, Shively V, Nuseir N (1987): Macrophage-induced angiogenesis is mediated by tumor necrosis factor alpha. Nature 329:630-635.
32. Li Y, Raisman G (1995): Sprouts from cutcorticospinal axons persist in the presence of astrocytic scarring in longterm lesions of the adult rat spinal cord. Exp Neurol 134:102-111.
33. Liesi P, Kaakkola S, Dahl D, Vaheri A (1984): Laminin is induced in astrocytes of adult brain by injury. EMBO J 3:683-686.
34. 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.
35. Lotan M, Solomon A, Ben-Bassat S, Schwartz M (1994): Cytokines modulate the inflammatory response and change permissiveness to neuronal adhesion in injured mammalian central nervous system. Exp Neurol 126:284-290.
36. Ludwin SK, Bisby MA (1991): Wallerian degeneration is delayed in the central nervous system of Ola mice. J Neuropathol Exp Neurol 50:330.
37. Ludwin SK, Bisby MA (1992): Delayed Wallerian degeneration in the central nervous system of Ola mice: An ultrastructural study. J Neurol Sci 109:140-147.
38. Mallat M, Houlgatte R, Brachet P, Prochiantz A (1989): Lipopolysac-charide-stimulated rat brain macrophages release NGF in vitro. Dev Biol 133:309-311.
39. Mansour H, Asher R, Dahl D, Labkovsky B, Perides G, Bignami A (1990): Permissive and non-permissive reactive astrocytes: Immunofluorescence study with antibodies to the glial hyaluronate-binding protein. J Neurosci Res 25:300-311.
40. Manthorpe M, Engvall E, Rouslahti E, Longo FM, Davis GE, Varon S (1983): Laminin promotes neuritic regeneration from cultured, peripheral and central neurons. J Cell Biol 97:1882-1890.
41. Martin D, Schoenen J, Delree P, Leprince P, Rogister B, Moonen G (1991): Grafts of syngenic cultured, adult dorsal root ganglion-derived Schwann cells to the injured spinal cord of adult rats: Preliminary morphological studies. Neurosci Lett 124:44-48.
42. Martin D, Schoenen J, Delree P, Gilson V, Rogister B, Leprince P, Stevenaert A, Moonen G (1992): Experimental acute traumatic-injury of the adult rat spinal cord by a subdural inflatable balloon: Methodology, behavioral, analysis and histopathology. J Neurosci Res 32:539-550.
43. Martin D, Schoenen J, Delree P, Rigo JM, Rogister B, Leprince P, Moonen G (1993): Syngeneic grafting of adult rat DRG-derived Schwann cells to the injured spinal cord. Brain Res Bull 30:507-514.
44. Martin D, Robe P, Franzen R, Delree P, Schoenen J, Stevenaert A, Moonen G (1996): Effects of Schwann cell transplantation in a contusion model of rat spinal cord injury. J Neurosci Res 45:588-597.
45. McKeon RJ, Schreiber RC, Rudge JS, Silver J (1991): Reduction of neurite 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.
46. McKeon RJ, Hoke A, Silver J (1995): Injury-induced proteoglycans inhibit the potential for laminin-medialed axon growth on astrocytic scars. Exp Neurol 136:32-43.
47. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994): Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13:805-811.
48. Mukhopadhyay G, Doherty P, Walsch FS, Crocker PR, Filbin MT (1994): A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13:757-767.
49. Ng WP, Cartel N, Li C, Roder J, Lozano A (1996): Myelin from MAG-deficient mice is a strong inhibitor of neurite outgrowth. Neuroreport 7:861-864.
50. Perry VH, Brown MC, Gordon S (1987): The macrophage response to central and peripheral nerve injury. J Exp Med 165:1218-1223.
51. Rabchevsky AG, Streit WJ (1997): Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J Neurosci Res 47:34-48.
52. Ranion Y, Cajal S (1928): Degeneration and Regeneration of the Nervous System. London: Oxford University Press.
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. 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.
55. 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.
56. Shimojo M, Nakajima K, Takei N, Hamanoue M, Koshsaka S (1991): Production of basic fibroblast growth factor in cultured rat brain microglia. Neurosci Lett 123:229-231.
57. Spranger M, Lindholm D, Bandtlow C (1990): Regulation of NGF synthesis in the rat central nervous system: Comparison between the effects of interleukin-1 and various growth factors in astrocyte cultures and in vivo. Eur J Neurosci 2:69-76.