Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury

Experimental Neurology

Volumn 158, Issue 2, 1999, Pages 351-365

  Popovich, Phillip G ^a   Guan, Zhen ^a   Wei, Ping ^a   Huitinga, Inge ^b   Van Rooijen, Nico ^b   Stokes, Bradford T ^a  

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

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Immunosuppression; Liposomes; Macrophages; Microglia; Neuroinflammation; Regeneration; Spinal cord injury

Indexed keywords

CLODRONIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; FEMALE; GLIA; HINDLIMB; HOST RESISTANCE; IMMUNOMODULATION; INFLAMMATION; LEUKOCYTE; LOCOMOTION; MACROPHAGE; NERVE CELL; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY; TISSUE INJURY;

EID: 0032838089     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.7118     Document Type: Article

References (84)

1. Alberati-Giani D., Ricciardi-Castagnoli P., Kohler C., Cesura A. M. Regulation of the kynurenine metabolic pathway by interferon-γ in murine cloned macrophages and microglial cells. J. Neurochem. 66:1996;996-1004.
2. Balentine J. D. Pathology of experimental spinal cord trauma. II. Ultrastructure of axons and myelin. Lab. Invest. 39:1978;254-266.
3. Banati R. B., Rothe G., Valet G., Kreutzberg G. W. Respiratory burst activity in brain macrophages: a flow cytometric study on cultured rat microglia. Neuropathol. Appl. Neurobiol. 17:1991;223-230.
4. Barbeau H., Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res. 412:1987;84-95.
5. Bartholdi D., Schwab M. E. Methylprednisolone inhibits early inflammatory processes but not ischemic cell death after experimental spinal cord lesion in the rat. Brain Res. 672:1995;177-186.
6. Bartholdi D., Schwab M. E. Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: An in situ hybridization study. Eur. J. Neurosci. 9:1997;1422-1438.
7. Basso D. M., Beattie M. S., Bresnahan J. C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma. 12:1995;1-21.
8. Basso D. M., Beattie M. S., Bresnahan J. C. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp. Neurol. 139:1996;244-256.
9. Basso D. M., Murray M., Goldberger M. E. Differential recovery of bipedal and overground locomotion following complete spinal cord hemisection in cats. Res. Neurol. Neurosci. 7:1994;95-110.
10. Bauer J., Huitinga I., Zhao W., Lassmann H., Hickey W. F., Dijkstra C. D. The role of macrophages, perivascular cells, and microglial cells in the pathogenesis of experimental autoimmune encephalomyelitis. GLIA. 15:1995;437-446.
11. Beattie M. S., Bresnahan J. C., Komon J., Tovar C. A., Van Meter M., Anderson D. K., Faden A. I., Hsu C. Y., Noble L. J., Salzman S. K., Young W. Endogenous repair after spinal cord contusion injuries in the rat. Exp. Neurol. 148:1997;453-463.
12. Behrmann D. L., Bresnahan J. C., Beattie M. S. A comparison of YM-14673, U-50488H, and Nalmefene after spinal cord injury in the rat. Exp. Neurol. 119:1993;258-267.
13. Behrmann D. L., Bresnahan J. C., Beattie M. S. Modeling of acute spinal cord injury in the rat: Neuroprotection and enhanced recovery with methylprednisolone, U-74006F, and YM-14673. Exp. Neurol. 126:1994;1-16.
14. Behrmann D. L., Bresnahan J. C., Beattie M. S., Shah B. R. Spinal cord injury produced by consistent displacement of the cord in rats: behavioral and histologic analysis. J. Neurotrauma. 9:1992;197-217.
15. Blight A. R. Delayed demyelination and macrophage invasion: A candidate for secondary cell damage in spinal cord injury. CNS Trauma. 2:1985;299-315.
16. Blight A. R. Effects of silica on the outcome from experimental spinal cord injury: Implication of macrophages in secondary tissue damage. Neuroscience. 60:1994;263-273.
17. Blight A. R., Cohen T. I., Saito K., Heyes M. P. Quinolinic acid accumulation and functional deficits following experimental spinal cord injury. Brain. 118:1995;735-752.
18. Blight A. R., Saito K., Heyes M. P. Increased levels of the excitotoxin quinolinic acid in spinal cord following contusion injury. Brain Res. 632:1993;314-316.
19. Bracken M. B., Shepard M. J., Collins W. F., Holford T. R., Young W., Baskin D. S., Eisenberg H. M., Flamm E., Leo-Summers L., Maroon J. A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal-cord injury: Results of the Second National Acute Spinal Cord Injury Study. N. Engl. J. Med. 322:1990;1405-1411.
20. Bracken M. B., Shepard M. J., Holford T. R., Leo-Summers L., Aldrich E. F., Fazl M., Fehlings M., Herr D. L., Hitchon P. W., Marshall L. F. Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury: Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial - National Acute Spinal Cord Injury Study. JAMA. 277:1997;1597-1604.
21. Bregman B. S., Kunkel-Bagden E., Schnell L., Dai H. N., Gao D., Schwab M. E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature. 378:1995;498-501.
22. Bresnahan J. C., Beattie M. S., Todd F. D. III, Noyes D. H. A behavioral and anatomical analysis of spinal cord injury produced by a feedback-controlled impaction device. Exp. Neurol. 95:1987;548-570.
23. Bresnahan J. C., King J. S., Martin G. F., Yashon D. A neuroanatomical analysis of spinal cord injury in the rhesus monkey (Macaca mulatta). J. Neurol. Sci. 28:1976;521-542.
24. Bruck W., Huitinga I., Dijkstra C. D. Liposome-mediated monocyte depletion during wallerian degeneration defines the role of hematogenous phagocytes in myelin removal. J. Neurosci. Res. 46:1996;477-484.
25. Carlson S. L., Parrish M. E., Springer J. E., Doty K., Dossett L. Acute inflammatory response in spinal cord following impact injury. Exp. Neurol. 151:1998;77-88.
26. Cheng H., Cao Y. H., Olson L. Spinal cord repair in adult paraplegic rats: Partial restoration of hind limb function. Science. 273:1996;510-513.
27. Crowe M. J., Bresnahan J. C., Shuman S. L., Masters J. N., Beattie M. S. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nature Med. 3:1997;73-76.
28. Damoiseaux J. G., Dopp E. A., Calame W., Chao D., MacPherson G. G., Dijkstra C. D. Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1. Immunology. 83:1994;140-147.
29. Davies S. J., Fitch M. T., Memberg S. P., Hall A. K., Raisman G., Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature. 390:1997;680-683.
30. DeJong B. A., Smith M. E. A role for complement in phagocytosis of myelin. Neurochem. Res. 22:1997;491-498.
31. DeWitt D. A., Perry G., Cohen M., Doller C., Silver J. Astrocytes regulate microglial phagocytosis of senile plaque cores of Alzheimer's disease. Exp. Neurol. 149:1998;329-340.
32. Dusart I., Schwab M. E. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur. J. Neurosci. 6:1993;712-724.
33. Edgerton V. R., Roy R. R., Hodgson J. A., Prober R. J., de Guzman C. P., de Leon R. Potential of adult mammalian lumbosacral spinal cord to execute and acquire improved locomotion in the absence of supraspinal input. J. Neurotrauma. 9:1992;S119-S128.
34. Eidelberg E., Straehley D., Erspamer R., Watkins C. J. Relationship between residual hindlimb-assisted locomotion and surviving axons after incomplete spinal cord injuries. Exp. Neurol. 56:1977;312-322.
35. Elkabes S., DiCicco-Bloom E. M., Black I. B. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J. Neurosci. 16:1996;2508-2521.
36. Fitch M. T., Silver J. Activated macrophages and the blood-brain barrier: inflammation after CNS injury leads to increases in putative inhibitory molecules. Exp. Neurol. 148:1997;587-603.
37. Franzen R., Schoenen J., Leprince P., Joosten E., Moonen G., Martin D. Effects of macrophage transplantation in the injured adult rat spinal cord: A combined immunocytochemical and biochemical study. J. Neurosci. Res. 51:1998;316-327.
38. Giulian D. Ameboid microglia as effectors of inflammation in the central nervous system. J. Neurosci. Res. 18:1987;155-171.
39. Giulian D., Chen J., Ingeman J. E., George J. K., Noponen M. The role of mononuclear phagocytes in wound healing after traumatic injury to adult mammalian brain. J. Neurosci. 9:1989;4416-4429.
40. Giulian D., Corpuz M., Chapman S., Mansouri M., Robertson C. Reactive mononuclear phagocytes release neurotoxins after ischemic and traumatic injury to the central nervous system. J. Neurosci. Res. 36:1993;681-693.
41. Giulian D., Li J., Bartel S., Broker J., Li X., Kirkpatrick J. B. Cell surface morphology identifies microglia as a distinct class of mononuclear phagocyte. J. Neurosci. 15:1995;7712-7726.
42. Giulian D., Robertson C. Inhibition of mononuclear phagocytes reduces ischemic injury in the spinal cord. Ann. Neurol. 27:1990;33-42.
43. Goldberger M. E., Bregman B. S., Vierck C. J. Jr., Brown M. Criteria for assessing recovery of function after spinal cord injury: behavioral methods. Exp. Neurol. 107:1990;113-117.
44. Grill R., Murai K., Blesch A., Gage F. H., Tuszynski M. H. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neuroscience. 17:1997;5560-5572.
45. Guth L., Barrett C. P., Donati E. J., Anderson F. D., Smith M. V., Lifson M. Essentiality of a specific cellular terrain for growth of axons into a spinal cord lesion. Exp. Neurol. 88:1985;1-12.
46. Guth L., Zhang Z., DiProspero N. A., Joubin K., Fitch M. T. Spinal cord injury in the rat: Treatment with bacterial lipopolysaccharide and indomethacin enhances cellular repair and locomotor function. Exp. Neurol. 126:1994;76-87.
47. Guth L., Zhang Z., Roberts E. Key role for pregnenolone in combination therapy that promotes recovery after spinal cord injury. Proc. Natl. Acad. Sci. USA. 91:1994;12308-12312.
48. Hirschberg D. L., Schwartz M. Macrophage recruitment to acutely injured central nervous system is inhibited by a resident factor: Basis for an immune-brain barrier. J. Neuroimmunol. 61:1995;89-96.
49. Huitinga I., Damoiseaux J. G., van Rooijen N., Döpp E. A., Dijkstra C. D. Liposome mediated affection of monocytes. Immunobiology. 185:1992;11-19.
50. Huitinga I., van Rooijen N., de Groot C. J., Uitdehaag B. M., Dijkstra C. D. Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J. Exp. Med. 172:1990;1025-1033.
51. Kerasidis H., Wrathall J. R., Gale K. Behavioral assessment of functional deficit in rats with contusive spinal cord injury. J. Neurosci. Methods. 20:1987;167-189.
52. Kunkel-Bagden E., Dai H. N., Bregman B. S. Methods to assess the development and recovery of locomotor function after spinal cord injury in rats. Exp. Neurol. 119:1993;153-164.
53. Lazarov-Spiegler O., Rapalino O., Agranov G., Schwartz M. Restricted inflammatory response in the CNS: A key impediment to axonal regeneration. Mol. Med. Today. 4:1998;337-342.
54. Lazarov-Spiegler O., Solomon A. S., Zeev-Brann A. B., Hirschberg D. L., Lavie V., Schwartz M. Transplantation of activated macrophages overcomes central nervous system regrowth failure. FASEB J. 10:1996;1296-1302.
55. McTigue D. M., Horner P. J., Stokes B. T., Gage F. H. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J. Neurosci. 18:1998;5354-5365.
56. McTigue D. M., Tani M., Krivacic K., Chernosky A., Kelner G. S., Maciejewski D., Maki R., Ransohoff R. M., Stokes B. T. Selective chemokine mRNA accumulation in the rat spinal cord after contusion injury. J. Neurosci. Res. 53:1998;368-376.
57. Means E. D., Anderson D. K. Neuronophagia by leukocytes in experimental spinal cord injury. J. Neuropathol. Exp. Neurol. 42:1983;707-719.
58. Micklus M. J., Greig N. H., Tung J., Rapoport S. I. Organ distribution of liposomal formulations following intracarotid infusion in rats. Biochim. Biophys. Acta. 1124:1992;7-12.
59. Mosley K., Cuzner M. L. Receptor-mediated phagocytosis of myelin by macrophages and microglia: effect of opsonization and receptor blocking agents. Neurochem. Res. 21:1996;481-487.
60. Noble L. J., Wrathall J. R. Distribution and time course of protein extravasation in the rat spinal cord after contusive injury. Brain Res. 482:1989;57-66.
61. Popovich P. G., Horner P. J., Mullin B. B., Stokes B. T. A quantitative spatial analysis of the blood-spinal cord barrier. I. Permeability changes after experimental spinal contusion injury. Exp. Neurol. 142:1996;258-275.
62. Popovich P. G., Reinhard J. F. Jr., Flanagan E. M., Stokes B. T. Elevation of the neurotoxin quinolinic acid occurs following spinal contusion injury. Brain Res. 633:1994;348-352.
63. Popovich P. G., Wei P., Stokes B. T. The cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 377:1997;443-464.
64. Popovich P. G., Yu J. Y., Whitacre C. C. Spinal cord neuropathology in rat experimental autoimmune encephalomyelitis: Modulation by oral administration of myelin basic protein. J. Neuropathol. Exp. Neurol. 56:1997;1323-1338.
65. Qian Q., Jutila M. A., van Rooijen N., Cutler J. E. Elimination of mouse splenic macrophages correlates with increased susceptibility to experimental disseminated candidiasis. J. Immunol. 152:1994;5000-5008.
66. Rabchevsky A. G., Streit W. J. Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J. Neurosci. Res. 47:1997;34-48.
67. Rapalino O., Lazarov-Spiegler O., Agranov E., Velan G. J., Yoles E., Fraidakis M., Solomon A., Gepstein R., Katz A., Belkin A. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nature Med. 4:1998;814-821.
68. Schroeter M., Jander S., Huitinga I., Witte O. W., Stoll G. Phagocytic response in photochemically induced infarction of rat cerebral cortex: The role of resident microglia. Stroke. 28:1997;382-386.
69. Semple-Rowland S. L., Mahatme A., Popovich P. G., Green D. A., Hassler G., Stokes B. T., Streit W. J. Analysis of TGF-β1 gene expression in contused rat spinal cord using quantitative RT-PCR. J. Neurotrauma. 12:1995;1003-1014.
70. Shuman S. L., Bresnahan J. C., Beattie M. S. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J. Neurosci. Res. 50:1997;798-808.
71. Stokes B. T., Noyes D. H., Behrmann D. L. An electromechanical spinal injury device with dynamic sensitivity. J. Neurotrauma. 9:1992;187-195.
72. Streit W. J., Semple-Rowland S. L., Hurley S. D., Miller R. C., Popovich P. G., Stokes B. T. Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 152:1998;74-87.
73. Taoka Y., Okajima K., Uchiba M., Murakami K., Harada N., Johno M., Naruo M. Activated protein C reduces the severity of compression-induced spinal cord injury in rats by inhibiting activation of leukocytes. J. Neurosci. 18:1998;1393-1398.
74. Taoka Y., Okajima K., Uchiba M., Murakami K., Kushimoto S., Johno M., Naruo M., Okabe H., Takatsuki K. Role of neutrophils in spinal cord injury in the rat. Neuroscience. 79:1997;1177-1182.
75. van Rooijen N., Sanders A. Liposome mediated depletion of macrophages: Mechanism of action, preparation of liposomes and applications. J. Immunol. Methods. 174:1994;83-93.
76. van Rooijen N., Sanders A., van den Berg T. K. Apoptosis of macrophages induced by liposome-mediated intracellular delivery of clodronate and propamidine. J. Immunol. Methods. 193:1996;93-99.
77. van Rooijen N., van Nieuwmegen R. Elimination of phagocytic cells in the spleen after intravenous injection of liposome-encapsulated dichloromethylene diphosphonate: An enzyme-histochemical study. Cell Tissue Res. 238:1984;355-358.
78. Windle W. F., Smart J., Beers J. Residual function after subtotal spinal cord transection in adult cats. Neurology. 8:1958;518-521.
79. Wrathall J. R., Choiniere D., Teng Y. D. Dose-dependent reduction of tissue loss and functional impairment after spinal cord trauma with the AMPA/kainate antagonist NBQX. J. Neurosci. 14:1994;6598-6607.
80. Zeev-Brann A. B., Lazarov-Spiegler O., Brenner T., Schwartz M. Differential effects of central and peripheral nerves on macrophages and microglia. GLIA. 23:1998;181-190.
81. Zhang S. C., Fedoroff S. Neuron-microglia interactions in vitro. Acta Neuropathol. (Berl.). 91:1996;385-395.
82. Zhang Z., Guth L. Experimental spinal cord injury: Wallerian degeneration in the dorsal column is followed by revascularization, glial proliferation, and nerve regeneration. Exp. Neurol. 147:1997;159-171.
83. Zhang Z., Guth L., Steward O. Mechanisms of motor recovery after subtotal spinal cord injury: Insights from the study of mice carrying a mutation (WldS) that delays cellular responses to injury. Exp. Neurol. 149:1998;221-229.
84. Zhang Z., Krebs C. J., Guth L. Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp. Neurol. 143:1997;141-152.