Experimental analysis of progressive necrosis after spinal cord trauma in the rat: Etiological role of the inflammatory response

Experimental Neurology

Volumn 143, Issue 1, 1997, Pages 141-152

  Zhang, Ziyin ^a,b   Krebs, Christopher J ^a   Guth, Lloyd ^a  

^a The College of William and Mary   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPURINOL; AMINOGUANIDINE; ANTIINFLAMMATORY AGENT; INDOMETACIN; NAPROXEN; PREGNENOLONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HISTOLOGY; INFLAMMATION; NECROSIS; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY;

EID: 0031033377     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1996.6355     Document Type: Article

References (68)

1. 1. ABDIH, H., C. J. KELLY, D. BOUCHIER-HAYES, R. WILLIAM, G. WATSON, H. P. REDMOND, P. BURKE, AND D. J. BOUCHIER-HAYES. 1994. Nitric oxide (endothelium-derived relaxing factor) attenuates revascularization-induced lung injury. J. Surg. Res. 57: 39-43.
2. 2. AGUAYO, A. J., G. M. BRAY, C. S. PERKINS, AND I. D. DUNCAN. 1979. Axon-sheath cell interactions in peripheral and central nervous system transplants. Soc. Neurosci. Symp. 4: 361-383.
3. 3. BALENTINE, J. D. 1978. Pathology of experimental spinal cord trauma. I. The necrotic lesion as a function of vascular injury. Lao. Invest. 39: 236-253.
4. 4. BARTHOLDI, D., AND M. E. SCHWAB. 1995. Methylprednisolone inhibits early inflammatory processes but not ischemic cell death after experimental spinal cord lesion in the rat. Brain Res. 672: 177-186.
5. 5. BEHRMANN, D. L., J. C. BRESNAHAN, AND M. S. BEATTIE. 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.
6. 6. BLIGHT, A. R. 1985. Delayed demyelination and macrophage invasion: A candidate for secondary cell damage in spinal cord injury. Cent. Nerv. Syst. Trauma 2: 299-315.
7. 7. BONVENTRE, J. V. 1993. Mechanisms of acute ischemic renal failure. Kidney Int. 43: 1160-1178.
8. 8. BRACKEN, M. B., M. J. SHEPARD, W. F. COLLINS, T. R. HOLFORD, W. YOUNG, D. S. BASKIN, H. M. EISENBERG, E. FLAMM, L. LEO-SUMMERS, J. MAROON, L. F. MARSHALL, P. L. PEROT, JR., J. PIEPMEIER, V. K. H. SONNTAG, F. C. WAGNER, J. E. WILBERGER, AND H. R. WINN. 1990. A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal cord injury. N. Engl. J. Med. 322: 1405-1411.
9. 9. CHIUEH, C. C., D. L. GILBERT, AND C. A. COLTON, EDS. 1994. The neurobiology of NO and OH. Ann. N. Y. Acad. Sci. 738: 1-167.
10. 10. CLEMENTE, C. D., AND W. F. WINDLE. 1954. Regeneration of severed nerve fibers in the spinal cord of the adult cat. J. Comp. Neurol. 101: 691-731.
11. 11. CURTIS, R., D. GREEN, R. M. LINDSAY, AND G. P. WILKIN. 1993. Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J. Neurocytol. 2: 51-64.
12. 12. DAS, D. K., ED. 1994. Cellular, biochemical and molecular aspects of reperfusion injury. Ann. N. Y. Acad. Sci. 723: 1-506.
13. 13. DAVID, S., AND A. J. AGUAYO. 1981. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214: 931-933.
14. 14. DIETRICH, W. D. 1994. Morphological manifestations of reperfusion injury in brain. Ann. N. Y. Acad. Sci. 723: 15-24.
15. 15. EIDELBERG, E., D. STRAEHLEY, R. ERSPAMER, AND C. J. WATKINS. 1977. Relationship between residual hindlimb-assisted locomotion and surviving axons after incomplete spinal cord injuries. Exp. Neurol. 56: 312-322.
16. 16. FADEN, A. I. 1988. Role of thyrotropin-releasing hormone and opiate receptor antagonists in limiting central nervous system injury. Adv. Neurol. 47: 531-546.
17. 17. FADEN, A. I., T. P. JACOBS, M. T. SMITH, AND J. W. HOLADAY. 1983. Comparison of thyrotropin-releasing hormone (TRH), naloxone, and dexamethasone treatments in experimental spinal cord injury. Neurology 33: 673-678.
18. s) that causes delayed Wallerian degeneration. J. Comp. Neurol., 371: 469-484.
19. 19. GIULIAN, D., M. CORPUZ, S. CHAPMAN, M. MANSOURI, AND C. ROBERTSON. 1993. Reactive mononuclear phagocytes release neurotoxins after ischemic and traumatic injury to the central nervous system. J. Neurosci. Res. 36: 681-693.
20. 20. GOETZL, E. J., R. A. LEWIS, AND M. ROLA-PLESZCZYNSKI, EDS. 1994. Cellular generation, transport, and effects of eiconosoids. Ann. N. Y. Acad. Sci. 744: 1-340.
21. 21. GRIFFITHS, M. J. D., M. MESSENT, R. J. MACALLISTER, AND T. W. EVANS. 1994. Aminoguanidine selectively inhibits inducible nitric oxide synthase. Br. J. Pharmacol. 110: 963-968.
22. 22. GUTH, L., E. X. ALBUQUERQUE, S. S. DESHPANDE, C. P. BARRETT, E. J. DONATI, AND J. W. WARNICK. 1980. Ineffectiveness of enzyme therapy on regeneration in the transected spinal cord of the rat. J. Neurosurg. 52: 73-86.
23. 23. GUTH, L., C. P. BARRETT, E. J. DONATI, S. S. DESHPANDE, AND E. X. ALBUQUERQUE. 1981. Histopathological reactions and axonal regeneration in the transected spinal cord of hibernating squirrels. J. Comp. Neurol. 203: 297-308.
24. 24. GUTH, L., C. P. BARRETT, E. J. DONATI, F. D. ANDERSON, M. V. SMITH, AND M. LIFSON. 1985. Essentiality of a specific cellular terrain for growth of axons into a spinal cord lesion. Exp. Neurol. 88: 1-12.
25. 25. GUTH, L., Z. ZHANG, N. A. DIPROSPERO, K. JOUBIN, AND M. T. FITCH. 1994. Spinal cord injury in the rat: Treatment with bacterial lipopolysaccharide and indomethacin enhances cellular repair and locomotor function. Exp. Neurol. 126: 76-87.
26. 26. GUTH, L., Z. ZHANG, AND E. ROBERTS. 1994. Key role for pregnenolone in combination therapy that promotes recovery after spinal cord injury. Proc. Natl. Acad. Sci. USA 91: 12308-12312.
27. 27. HACHIDA, M., AND D. L. MORTON. 1988. The protection of the ischemic lung with verapamil and hydralazine. J. Thoracic Cardiovasc. Surg. 95: 178-183.
28. 28. HAGLUND, U., G. B. BULKLEY, AND D. N. GRANGER. 1987. On the pathophysiology of intestinal ischemic injury. Acta Chir. Scand. 153: 321-324.
29. 29. HALL, E. D., D. L. WOLF, AND J. M. BRAUGHLER. 1986. Pathophysiology, consequences and pharmacological prevention of posttraumatic CNS ischemia. Pages 63-73 in G. Gilad, Ed., Processes of Recovery from Neural Trauma. Springer-Verlag, Berlin.
30. 30. HARVEY, J. E., AND H. H. SREBNIK. 1967. Locomotor activity and axon regeneration following spinal cord compression in rats treated with L-thyroxine. Neuropathol. Exp. Neurol. 26: 661-668.
31. 31. HAVERICH, A., AND M. KARCK. 1994. Role of calcium channel blockers in postischemic lungs. Ann. N. Y. Acad. Sci. 723: 51-58.
32. 32. HERNANDEZ, L. A., M. B. GRISHAM, B. TWOHIG, K. E. ARFORS, J. M. HARLAN, AND D. N. GRANGER. 1987. Role of neutrophils in ischemia-reperfusion induced microvascular injury. Am. J. Physiol. 253: H699-H703.
33. 33. HUNT, T. K., D. R. KNIGHTON, K. K. THAKRAL, W. H. GOODSON, AND W. S. ANDREWS. 1984. Studies on inflammation and wound healing: Angiogenesis and collagen synthesis stimulated in vivo by resident and activated wound macrophages. Surgery 96: 48-54.
34. 34. JENSEN, J. A., T. K. HUNT, H. SCHEUENSTUHL, AND M. J. BANDA. 1986. Effect of lactate, pyruvate and pH on secretion of angiogenesis and mitogenesis factors by macrophages. Lab. Invest. 54: 574-578.
35. 35. JOHNSON, W. J., AND C. P. SUNG. 1987. Rat macrophage treatment with lipopolysaccharide leads to a reduction in respiratory burst product secretion and a decrease in NADPH oxidase affinity. Cell. Immunol. 108: 109-119.
36. 36. JOOSTEN, E. A., R. L. SCHUITMAN, M. E. VERMELIS, AND P. J. DEDEREN. 1992. Postnatal development of the ipsilateral corticospinal component in rat spinal cord: A light and electron microscopic anterograde HRP study. J. Comp. Neurol. 326: 133-146.
37. 37. KOCH, A. E., P. J. POLVERINI, AND S. J. LEIBOVICH. 1986. Induction of neovascularization by activated human monocytes. J. Leukocyte Biol. 39: 233-238.
38. 38. KOIKE, K., F. A. MOORE, E. E. MOORE, R. S. POGGETTI, R. M. TUDER, AND A. BANNERJEE. 1992. Endotoxin after gut ischemia/ reperfusion causes irreversible lung injury. J. Surg. Res. 52: 656-662.
39. 39. KUROSE, I., AND D. N. GRANGER. 1994. Evidence implicating xanthine oxidase and neutrophils in reperfusion-induced microvascular dysfunction. Ann. N. Y. Acad. Sci. 723: 158-179.
40. 40. LIESI, P., AND J. SILVER. 1988. Is astrocyte laminin involved in axonal guidance in the mammalian CNS? Dev. Neurol. 130: 774-785.
41. 41. LINDHOLM, D., E. CASTREN, R. KIEFER, F. ZAFRA, AND H. THOENEN. 1992. Transforming growth factor-beta 1 in the rat brain: Increase after injury and inhibition of astrocyte proliferation. J. Cell Biol. 117: 395-400.
42. 42. LIPTON, W. A., Y. B. CHOI, Z. H. PAN, S. Z. LEI, H. S. V. CHEN, N. J. SUCHER, J. LOSCALZO, D. J. SIEGEL, AND J. S. STAMLER. 1993. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364: 626-632.
43. 2+ homeostasis in hearts reperfused after prolonged episodes of ischemia. Ann. N. Y. Acad. Sci. 723: 38-50.
44. 44. MCCULLOUGH, A. W. 1959. Studies on peripheral nerve regeneration. I. Peripheral nerve regeneration in white rats of various ages when treated with a pyrogenic bacterial polysaccharide complex in various dosage. J. Comp. Neurol. 113: 471-490.
45. 45. MISKO, T. P., W. M. MOORE, T. P. KASTEN, G. A. NICKOLS, J. A. CORBETT, R. G. TILTON, M. L. MCDANIEL, J. R. WILLIAMSON, AND M. G. CURRIE. 1993. Selective inhibition of the inducible nitic oxide synthase by aminoguanidine. Eur. J. Pharmacol. 233: 119-125.
46. 46. MITCHELL, J. A., P. AKARASEREENONT, C. THIEMERMANN, R. J. FLOWER, AND J. R. VANE. 1993. Selectivity of nonsteroidal antiinflammatory drugs as inhibitors of constitutive and inducible cyclooxygenase. Proc. Natl. Acad. Sci. USA 90: 11693-11697.
47. 47. NATHAN, C. F. 1987. Secretory products of macrophages. J. Clin. Invest. 79: 319-326.
48. 48. PALLER, M. S., AND D. L. GREENE. 1994. Role of calcium in reperfusion injury of the kidney. Ann. N. Y. Acad. Sci. 723: 59-70.
49. 49. PARK, P. O., U. HAGLUND, G. B. BULKLEY, AND K. FALT. 1990. The sequence of development of intestinal tissue injury after strangulation ischemia and reperfusion. Surgery 107: 574-580.
50. 50. PIPPENGER, M. A., T. J. SIMS, AND S. A. GILMORE. 1990. Development of the rat corticospinal tract through an altered glial environment. Brain Res. 55: 43-50.
51. 51. QAYUMI, A. K., M. T. JANUSZ, K. DOROVINI-ZIS, D. M. LYSTER, W. R. JAMIESON, A. POOSTIZADEH, E. J. FEELEY, AND M. NIKBAKHT-SANGAI. 1994. Additive effect of allopurinol and deferoxamine in the prevention of spinal cord injury caused by aortic crossclamping. J. Thoracic Cardiovasc. Surg. 107: 1203-1209.
52. 52. RAMON Y CAJAL, S. 1913. Degeneration and Regeneration of the Nervous System. English translation by R. M. May, 1928. Oxford Univ. Press, London. English edition reprinted, 1959, Hafner, New York.
53. 53. RAPPOLEE, D. A., D. MARK, M. J. BANDA, AND Z. WERE. 1988. Wound macrophages express TGF-α and other growth factors in vivo: Analysis by mRNA phenotyping. Science 241: 708-712.
54. 54. RICHARDSON, P. M., U. M. MCGUINNESS, AND A. J. AGUAYO. 1980. Axons from CNS neurons regenerate into PNS grafts. Nature 284: 264-265.
55. 55. SIMPSON, P. J., AND B. R. LUCCHESI. 1987. Free radicals and myocardial ischemia and reperfusion injury. J. Lab. Clin Med. 110: 13-30.
56. 56. SMITH, G. M., R. H. MILLER, AND J. SILVER. 1986. Changing role of forebrain astrocytes during development, regenerative failure and induced regeneration upon transplantation. J. Comp. Neurol. 251: 23-43.
57. 57. SPORN, M. B., AND A. B. ROBERTS, EDS. 1990. Peptide Growth Factors and Their Receptors. Springer-Verlag, Berlin.
58. 58. STRASSMAN, G., T. A. SPRINGER, S. J. HASKILL, C. C. MIRAGLIA, L. L. LANIER, AND D. O. ADAMS. 1985. Antigens associated with the activation of murine mononuclear macrophages in vivo: Differential expression of lymphocyte function-associated antigen in the several stages of development. Cell. Immunol. 94: 265-275.
59. 59. SUSSMAN, M. S., AND G. B. BULKLEY. 1990. Oxygen-derived free radicals in reperfusion injury. Pages 711-723 in L. Packer and A. N. Glazer, Eds., Methods in Enzymology: Oxygen Radicals in Biological Systems, Vol. 186, Part B. Academic Press, San Diego.
60. 60. TERASHIMA, T., T. OCHIISHI, AND T. YAMAUCHI. 1994. Immunohistochemical detection of calcium/calmodulin-dependent protein kinase II in the spinal cord of the rat and monkey with special reference to the corticospinal tract. J. Comp. Neurol. 340: 469-479.
61. 61. TREMBLEY, B., AND W. SLIKKER, JR., EDS. 1995. Neuroprotective agents: clinical and experimental aspects. Ann. N. Y. Acad. Sci. 7865: 1-348.
62. 62. TSAO, P. S., AND A. M. LEFER. 1990. Time course and mechanism of endothelial dysfunction in isolated ischemic-and hypoxic-perfused rat hearts. Am. J. Physiol. 259: H1660-H1666.
63. 63. WEINBERG, J. M. 1991. The cell biology of ischemic renal injury. Kidney Int. 39: 476-500.
64. 64. WINDLE, W. F. 1956. Regeneration of axons in the vertebrate central nervous system. Physiol. Rev. 36: 427-440.
65. 65. WINDLE, W. F., AND W. W. CHAMBERS. 1950. Regeneration in the spinal cord of the cat and dog. J. Comp. Neurol. 93: 241-257.
66. 66. WINDLE, W. F., D. C. CLEMENTE, AND W. W. CHAMBERS. 1952. Inhibition of formation of glial barrier as means of permitting peripheral nerve to grow into brain. J. Comp. Neurol. 96: 359-369.
67. 67. WRATHALL, J. R., R. K. PETTEGREW, AND F. HARVEY. 1985. Spinal cord contusion in the rat: Production of graded, reproducible, injury groups. Exp. Neurol. 88: 108-122.
68. s) that causes delayed Wallerian degeneration. J. Comp. Neurol., 371: 485-495.