Effects of Macrophage Transplantation in the Injured Adult Rat Spinal Cord: A Combined Immunocytochemical and Biochemical Study

Franzen, Rachelle; Schoenen, Jean; Leprince, Pierre; Joosten, Elbert; Moonen, Gustave; Martin, Didier

doi:10.1002/(SICI)1097-4547(19980201)51:3<316::AID-JNR5>3.0.CO;2-J

Article (Scientific journals)

Effects of Macrophage Transplantation in the Injured Adult Rat Spinal Cord: A Combined Immunocytochemical and Biochemical Study

Franzen, Rachelle; Schoenen, Jean; Leprince, Pierre et al.

1998 • In Journal of Neuroscience Research, 51 (3), p. 316-27

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https://hdl.handle.net/2268/7235

DOI
10.1002/(SICI)1097-4547(19980201)51:3<316::AID-JNR5>3.0.CO;2-J

PubMed
9486767

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Abstract :

[en] Early and robust invasion by macrophages may be one of the reasons why axonal regeneration is more effective in the PNS than in the CNS. Therefore, we have grafted autologous peritoneal macrophages labeled with fluorescent latex microspheres into spinal cord compression lesions. At various survival times, we have studied their effect on the expression of neuronal (neurofilaments [NF], calcitonin gene-related peptide [CGRP], 5-hydroxytryptamine [5-HT]) and nonneuronal markers (myelin-associated glycoprotein [MAG], glial fibrillary acidic protein [GFAP], laminin) by using semiquantitative Western blot and immunohistochemical techniques. After 1 month, we observed a significant decrease of the expression of MAG as well as an important invasion of the lesion site by neurites, chiefly peptidergic axons of presumed dorsal root origin, in macrophage-grafted animals compared with controls. In addition, angiogenesis and Schwann cell infiltration were more pronounced after macrophage grafts, providing an increase in laminin, a favorable substrate for axonal regrowth. By using reverse transcription-polymerase chain reaction (RT-PCR), mRNAs for tumor necrosis factor-alpha (TNF-alpha) were detected in the transplanted cells, whereas results were negative for nerve growth factor (NGF), neurotrophin-3 (NT-3), brain-derived neurotrophic factor (BDNF), or acidic fibroblast growth factor (aFGF) and basic fibroblast growth factor (bFGF). Thus, macrophage grafts may represent an interesting strategy to promote axonal regeneration in the CNS. Our study suggests that they may exert their beneficial effects by degrading myelin products, which inhibit axonal regrowth, and by promoting a permissive extracellular matrix containing notably laminin. No evidence for a direct synthesis of neurotrophic factors by the transplanted macrophages was found in this study, but resident glial cells could secrete such factors as a result of stimulation by macrophage-released cytokines.

Disciplines :

Surgery

Author, co-author :

Franzen, Rachelle ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Neuro-anatomie

Schoenen, Jean ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Neuro-anatomie

Leprince, Pierre ; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.

Joosten, Elbert

Moonen, Gustave ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie - Doyen de la Faculté de Médecine

Martin, Didier ; Université de Liège - ULiège > Département des sciences cliniques > Neurochirurgie

Language :

English

Title :

Effects of Macrophage Transplantation in the Injured Adult Rat Spinal Cord: A Combined Immunocytochemical and Biochemical Study

Publication date :

01 February 1998

Journal title :

Journal of Neuroscience Research

ISSN :

0360-4012

eISSN :

1097-4547

Publisher :

John Wiley & Sons, Hoboken, United States - New York

Volume :

Issue :

Pages :

316-27

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 27 February 2009

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Bibliography

Aguayo AJ, David S (1981): Axonal elongation into PNS "bridges" after CNS injury in adult rat. Science 214:931-933.
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.
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.
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.
Bernstein JJ, Getz R, Jefferson M, Keleman M (1985): Astrocytes secrete basal lamina after hemisection of rat spinal cord. Brain Res 327:135-141.
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.
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.
Chamak B, Morandi V, Mallat M (1994): Brain macrophages stimulate neurite growth and regeneration by secreting thrombospondin. J Neurosci Res 38:221-233.
Chen S, Bisby MA (1993): Impaired motor axons regeneration in the C57BL/Ola mouse. J Comp Neurol 333:449-454.
Chomczynski P, Sacchi N (1987): Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
Dahlin LB (1995): Prevention of macrophage invasion impairs regeneration in nerve grafts. Brain Res 679:274-280.
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.
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.
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.
Filbin MT (1995): Myelin-associated glycoprotein: A role in myelination and in the inhibition of axonal regeneration. Curr Opin Neurobiol 5:588-595.
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.
Fryer HJL, Davis GE, Manthorpe M, Varon S (1986): Lowry protein assay using an automatic microtiter plate spectrophotometer. Anal Biochem 153:262-266.
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.
Giulian D, Robertson C (1990): Inhibition of mononuclear phagocytes reduces ischemic injury in the spinal cord. Ann Neurol 27: 33-42.
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.
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.
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.
Gundersen RW, Barren JN (1979): Neuronal chemotaxis: Chick dorsal root axons turn toward high concentrations of nerve growth factor. Science 206:1079-1080.
Guth L, Reier PJ, Barren CP, Donati EJ (1983): Repair of the mammalian spinal cord. Trends Neurosci: 20-24.
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.
Hikawa N, Horie H, Takenaka T (1993): Macrophage-enhanced neurite regeneration of adult dorsal root ganglia neurones in culture. Neuroreport 5:41-44.
Jaffe EA, Ruggiero JT, Falcone DJ (1985): Monocytes and macrophages synthesize and secrete thrombospondin. Blood 65: 79-84.
Jelsma T, Aguayo AJ (1994): Trophic factors. Current Biol 4:717-725.
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.
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.
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.
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.
Liesi P, Kaakkola S, Dahl D, Vaheri A (1984): Laminin is induced in astrocytes of adult brain by injury. EMBO J 3:683-686.
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.
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.
Ludwin SK, Bisby MA (1991): Wallerian degeneration is delayed in the central nervous system of Ola mice. J Neuropathol Exp Neurol 50:330.
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.
Mallat M, Houlgatte R, Brachet P, Prochiantz A (1989): Lipopolysac-charide-stimulated rat brain macrophages release NGF in vitro. Dev Biol 133:309-311.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Perry VH, Brown MC, Gordon S (1987): The macrophage response to central and peripheral nerve injury. J Exp Med 165:1218-1223.
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.
Ranion Y, Cajal S (1928): Degeneration and Regeneration of the Nervous System. London: Oxford University Press.
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.
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.
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.
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.
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.