Elimination of basal lamina and the collagen 'scar' after spinal cord injury fails to augment corticospinal tract regeneration

Experimental Neurology

Volumn 160, Issue 1, 1999, Pages 40-50

  Weidner, N ^a   Grill, R J ^a   Tuszynski, M H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

2,2' bipyridine; Axonal regeneration; Collagen; Corticospinal; Scar formation; Spinal cord injury

Indexed keywords

2,2' BIPYRIDINE; COLLAGEN; COLLAGEN TYPE 3; COLLAGEN TYPE 4; IRON CHELATING AGENT; LAMININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GROWTH INHIBITION; NERVE CELL NETWORK; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RAT; SCAR FORMATION; SPINAL CORD INJURY;

EID: 0032727401     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.7200     Document Type: Article

References (47)

1. Aubert I., Ridet J. L., Gage F. H. Regeneration in the adult mammalian CNS: Guided by development. Curr. Opin. Neurobiol. 5:1995;625-635.
2. Azzi G., Jouis V., Godeau G., Groult N., Robert A. M. Immunolocalisation of extracellular matrix macromolecules in the rat spinal cord. Matrix. 9:1989;479-485.
3. Bartholdi D., Schwab M. E. Expression of proinflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: An in situ hybridization study. Eur. J. Neurosci. 9:1997;1422-1438.
4. 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., Young W. Endogenous repair after spinal cord contusion injuries in the rat. Exp. Neurol. 148:1997;453-463.
5. Bernstein J. J., Getz R., Jefferson M., Kelemen M. Astrocytes secrete basal lamina after hemisection of rat spinal cord. Brain. Res. 327:1985;135-141.
6. Berry M., Maxwell W. L., Logan A., Mathewson A., McConnell P., Ashhurst D. E., Thomas G. H. Deposition of scar tissue in the central nervous system. Acta Neurochir. Suppl. 32:1983;31-53.
7. Blesch A., Uy H. S., Grill R. J., Cheng J.-G., Patterson P. H., Tuszynski M. H. LIF augments neurotrophic expression and corticospinal axon growth after adult CNS injury. J. Neurosci. 19:1999;3556-3566.
8. Blurton-Jones M. M., Roberts J., Tuszynski M. H. Estrogen receptor immunoreactivity in the adult primate brain: Neuronal distribution and association with p75, trkA, and cholin acetyltransferase. J. Comp. Neurol. 405:1999;529-542.
9. Bregman B. S. Regeneration in the spinal cord. Curr. Opin. Neurobiol. 8:1998;800-807.
10. 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.
11. Brown J. C., Timpl R. The collagen superfamily. Int. Arch. Allergy Immunol. 107:1995;484-490.
12. Bunge R. P., Puckett W. R., Hiester E. D. Observations on the pathology of several types of human spinal cord injury, with emphasis on the astrocyte response to penetrating injuries. Adv. Neurol. 72:1997;305-315.
13. 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.
14. Fawcett J. W., Geller H. M. Regeneration in the CNS: optimism mounts. Trends Neurosci. 21:1998;179-180.
15. Feringa E. R., Kowalski T. F., Vahlsing H. L. Basal lamina formation at the site of spinal cord transection. Ann. Neurol. 8:1980;148-154.
16. Fernandez E., Pallini R. Connective tissue scarring in experimental spinal cord lesions: Significance of dural continuity and role of epidural tissues. Acta Neurochir. 76:1985;145-148.
17. 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.
18. Fitch M. T., Silver J. Beyond the glial scar. Tuszynski M. H., Kordower J. H. CNS Regeneration. 1999;55-88 Academic Press, San Diego.
19. Frisen J., Fried K., Sjögren A. M., Risling M. Growth of ascending spinal axons in CNS scar tissue. Int. J. Dev. Neurosci. 11:1993;461-475.
20. Frisen J., Risling M., Korhonen L., Zirrgiebel U., Johansson C. B., Cullheim S., Lindholm D. Nerve growth factor induces process formation in meningeal cells: Implications for scar formation in the injured CNS. J. Neurosci. 18:1998;5714-5722.
21. 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. Neurosci. 17:1997;5560-5572.
22. Ikeda H., Wu G. Y., Wu C. H. Evidence that an iron chelator regulates collagen synthesis by decreasing the stability of procollagen mRNA. Hepatology. 15:1992;282-287.
23. Ingber D., Folkman J. Inhibition of angiogenesis through modulation of collagen metabolism. Lab. Invest. 59:1988;44-51.
24. Kao C. C., Chang L. W., Bloodworth J. M. Jr. Axonal regeneration across transected mammalian spinal cords: An electron microscopic study of delayed microsurgical nerve grafting. Exp. Neurol. 54:1977;591-615.
25. Krikorian J. G., Guth L., Donati E. J. Origin of the connective tissue scar in the transected rat spinal cord. Exp. Neurol. 72:1981;698-707.
26. Logan A., Berry M. Transforming growth factor-beta 1 and basic fibroblast growth factor in the injured CNS. Trends Pharmacol. Sci. 14:1993;337-342.
27. Matthews M. A., St Onge M. F., Faciane C. L., Gelderd J. B. Axon sprouting into segments of rat spinal cord adjacent to the site of a previous transection. Neuropathol. Appl. Neurobiol. 5:1979;181-196.
28. Matthews M. A., St Onge M. F., Faciane C. L., Geldered J. B. Spinal cord transection: A quantitative analysis of elements of the connective tissue matrix formed within the site of lesion following administration of piromen, cytoxan or trypsin. Neuropathol. Appl. Neurobiol. 5:1979;161-180.
29. McKeon R. J., Höke A., Silver J. Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp. Neurol. 136:1995;32-43.
30. McKerracher L., David S., Jackson D. L., Kottis V., Dunn R. J., Braun P. E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron. 13:1994;805-811.
31. 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.
32. Mohajeri M. H., Bartsch U., van der Putten H., Sansig G., Mucke L., Schachner M. Neurite outgrowth on non-permissive substrates in vitro is enhanced by ectopic expression of the neural adhesion molecule L1 by mouse astrocytes. Eur. J. Neurosci. 8:1996;1085-1097.
33. Ness R., David S. Leptomeningeal cells modulate the neurite growth promoting properties of astrocytes in vitro. Glia. 19:1997;47-57.
34. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 1998;Academic Press, San Diego.
35. Risling M., Fried K., Linda H., Carlstedt T., Cullheim S. Regrowth of motor axons following spinal cord lesions: Distribution of laminin and collagen in the CNS scar tissue. Brain Res. Bull. 30:1993;405-414.
36. Schnell L., Klassen H. J., Schwab M. E., Perry V. H. Inflammatory responses in brain and spinal cord injury: Influence of recruited cells on secondary lesion area and BBB-damage. Soc. Neurosci. Abs. 23:1997;899.
37. Schwab M. E., Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76:1996;319-370.
38. Shellswell G. B., Restall D. J., Duance V. C., Bailey A. J. Identification and differential distribution of collagen types in the central and peripheral nervous systems. FEBS Lett. 106:1979;305-308.
39. Stichel C. C., Hermanns S., Luhmann H. J., Lausberg F., Niermann H., D'Urso D., Servos G., Hartwig H.-G., Müller H. W. Inhibition of collagen IV deposition promotes regeneration of injured CNS axons. Eur. J. Neurosci. 11:1999;632-646.
40. Stichel C. C., Müller H. W. The CNS lesion scar: New vistas on an old regeneration barrier. Cell Tissue Res. 294:1998;1-9.
41. Timpl R. Macromolecular organization of basement membranes. Curr. Opin. Cell Biol. 8:1996;618-624.
42. Tobin G. R., Chvapil M., Gildenberg P. L. Collagen biosynthesis in healing spinal cord wounds. Surg. Forum. 30:1979;454-456.
43. Tuszynski M. H., Gabriel K., Gage F. H., Suhr S., Meyer S., Rosetti A. Nerve growth factor delivery by gene transfer induces differential outgrowth of sensory, motor, and noradrenergic neurites after adult spinal cord injury. Exp. Neurol. 137:1996;157-173.
44. Tuszynski M. H., Kordower J. CNS Regeneration. 1999;Academic Press, San Diego.
45. Xu X. M., Guenard V., Kleitman N., Aebischer P., Bunge M. B. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp. Neurol. 134:1995;261-272.
46. Zgraggen W. J., Metz G. A. S., Kartje G. L., Thallmair M., Schwab M. E. Functional recovery and enhanced corticofugal plasticity after unilateral pyramidal tract lesion and blockade of myelin-associated neurite growth inhibitors in adult rats. J. Neurosci. 18:1998;4744-4757.
47. Zhang Y., Campbell G., Anderson P. N., Martini R., Schachner M., Lieberman A. R. Molecular basis of interactions between regenerating adult rat thalamic axons and Schwann cells in peripheral nerve grafts. I. Neural cell adhesion molecules. J. Comp. Neurol. 361:1995;193-209.