Basic fibroblast growth factor increases long-term survival of spinal motor neurons and improves respiratory function after experimental spinal cord injury

Journal of Neuroscience

Volumn 19, Issue 16, 1999, Pages 7037-7047

  Teng, Yang Dong ^a   Mocchetti, Italo ^a   Taveira DaSilva, Angelo M ^a   Gillis, Richard A ^a   Wrathall, Jean R ^a  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ChAT; FGF2; Minute ventilation; Motor neurons; Plethysmograph; Rat; Respiratory rate; Tidal volume

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CARBON DIOXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREATHING RATE; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; FEMALE; INTRAVENOUS DRUG ADMINISTRATION; MOTONEURON; NEUROPROTECTION; NONHUMAN; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; RAT; RESPIRATORY FUNCTION; SPINAL CORD INJURY; SPINAL CORD VENTRAL HORN; SYMPATHETIC NERVE CELL; TIDAL VOLUME; TREATMENT OUTCOME;

EID: 0006495387     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-16-07037.1999     Document Type: Article

References (68)

1. Baker HJ, Lindsey JR, Weisbroth SH (1979) The laboratory rat, biology and diseases, pp 411-412. Orlando, FL: Academic.
2. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21.
3. Basso DM, Beattie MS, Bresnahan JC, Anderson DK, Faden AI, Gruner JA, Holford TR, Hsu CY, Noble LJ, Nockels R, Perot PL, Salzman SK, Young W (1996) MASCIS evaluation of open field locomotor scores: effects of experience and teamwork on reliability. Multicenter Animal Spinal Cord Injury Study. J Neurotrauma 13:343-359.
4. BΦgin R, Bureau MA, Lupien L, Lemieux B (1980) Control of breathing in Duchenne's muscular dystrophy. Am J Med 69:227-234.
5. Behrmann DL, Bresnahan JC, Beattie MS, Shah BR (1992) Spinal cord injury produced by consistent mechanical displacement of the cord in rats: behavioral and histologic analysis. J Neurotrauma 9:197-217.
6. Blottner D, Baumgarten HG (1992) Basic fibroblast growth factor prevents neuronal death and atrophy of retrogradely labeled preganglionic neurons in vivo. Exp Neurol 118:35-46.
7. Blottner D, Stapf C, Meisinger C, Grothe C (1997) Localization, differential expression and retrograde axonal transport suggest physiological role of FGF-2 in spinal autonomie neurons of the rat. Eur J Neurosci 9:368-377.
8. Bluechardt MH, Wiens M, Thomas SG, Plyley MJ (1992) Repeated measurements of pulmonary function following spinal cord injury. Paraplegia 30:768-774.
9. Bracken MB, Shepard MJ, Collins WF, Holford TR, Young W, Baskin DS, Eisenberg HM, Flamm E, Leo-Summers L, Maroon PH, Marshall LF, Perot PL, Piepmeier J, Sonntag VKH, Wagner FC, Wilberger JE, Winn HR (1990) A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal cord injury. N Engl J Med 322:1405-1411.
10. Brandoli C, Sanna A, De Bernardi MA, Follesa P, Brooker G, Mocchetti I (1998) Brain-derived neurotrophic factor and basic fibroblast growth factor downregulate NMDA receptor function in cerebellar granule cells. J Neurosci 18:7953-7961.
11. Caro CG, Butler J, DuBois AB (1960) Some effects of restriction of chest cage expansion on pulmonary function in man: an experimental study. J Clin Invest 39:573-583.
12. Chadi G, Tinner B, Agnati LF, Fuxe K (1993) Basic fibroblast growth factor (bFGF, FGF-2) immunoreactivity exists in the noradrenaline, adrenaline and 5-HT nerve cells of the rat brain. Neurosci Lett 160:171-176.
13. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS (1997) Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3:73-76.
14. Dorato MA, Carlson KH, Copple DL (1983) Pulmonary mechanics in conscious Fischer 344 rats: multiple evaluations using nonsurgical techniques. Toxicol Appl Pharmacol 68:344-353.
15. El-Bohy AA, Schrimsher GW, Reier PJ, Goshgarian HG (1998) Quantitative assessment of respiratory function following contusion injury of the cervical spinal cord. Exp Neurol 150:143-152.
16. Fagan AM, Suhr ST, Lucidi-Phillipi CA, Peterson DA, Holtzman DM, Gage FH (1997) Endogenous FGF-2 is important for cholinergic sprouting in the denervated hippocampus. J Neurosci 17:2499-2511.
17. Feldman JL, McCrimmon DR (1999) Neural control of breathing. In: Fundamental neuroscience (Zigmond MJ, Bloom FE, Landis SC, Roberts JL, Squire LR, eds), pp 1063-1090. San Diego: Academic.
18. Follesa P, Wrathall JR, Mocchetti I (1994) Increased basic fibroblast growth factor mRNA following contusive spinal cord injury. Brain Res Mol Brain Res 22:1-8.
19. Frankel HL, Coll JR, Charlifue SW, Whitenect GG, Gardner BP, Jamous MA, Krishnan KR, Nuseibeh I, Savic G, Sett P (1998) Long-term survival in spinal cord injury: a fifty year investigation. Spinal Cord 36:266-274.
20. Frim DM, Uhler TA, Short MP, Ezzedine ZD, Klagsbrun M, Breakefield XO, Isacson O (1993) Effects of biologically delivered NGF, BDNF and bFGF on striatal excitotoxic lesions. NeuroReport 4:367-370.
21. Gale K, Kerasidis H, Wrathall JR (1985) Spinal cord contusion in the rat: behavioral analysis of functional neurological impairment. Exp Neurol 88:123-134.
22. Gibson JG, Pride NB, Newsom Davis J, Loh LC (1977) Pulmonary mechanics in patients with respiratory muscle weakness. Am Rev Respir Dis 115:389-395.
23. Gomez-Pinilla F, Tram H, Cotman CW, Nieto-Sampedro M (1989) Neuroprotective effect of MK-801 and U-50488H after contusive spinal cord injury. Exp Neurol 104:118-124.
24. Guth L (1976) Functional plasticity in the respiratory pathway of the mammalian spinal cord. Exp Neurol 51:414-420.
25. Guyton AC (1991) Pulmonary ventilation. In: Textbook of medical physiology, 8th Edition, pp 402-412. Philadelphia: Saunders.
26. Holstege G (1991) Descending motor pathways and the spinal motor system: limbic and nonlimbic components. Prog Brain Res 87:307-421.
27. Kerasidis H, Wrathall JR, Gale K (1987) Behavioral assessment of functional deficit in rats with contusive spinal cord injury. J Neurosci Methods 20:167-189.
28. Kinkead R, Zhan WZ, Prakash YS, Bach KB, Sieck GC, Mitchell GS (1998) Cervical dorsal rhizotomy enhances serotonergic innervation of phrenic motoneurons and serotonin-dependent long-term facilitation of respiratory motor output in rats. J Neurosci 18:8436-8443.
29. Kirschner PB, Henshaw R, Weise J, Trubetskoy V, Finklestein S, Schulz JB, Beal MF (1995) Basic fibroblast growth factor protects against excitotoxicity and chemical hypoxia in both neonatal and adult rats. J Cereb Blood Flow Metab 15:619-623.
30. Koo EH, Hoffman PN, Price DL (1988) Levels of neurotransmitter and cytoskeletal protein mRNAs during nerve regeneration in sympathetic ganglia. Brain Res 449:361-363.
31. Kurtzke JF (1977) Epidemiology of spinal cord injury. Neurol Neurocir Psiquiatr 18:157-191.
32. Ledsome JR, Sharp JM (1981) Pulmonary function in acute cervical spinal cord injury. Am Rev Respir Dis 124:41-44.
33. Lewis LJ, Brookhart JM (1951) Significance of the crossed phrenic phenomenon. Am J Physiol 166:241-254.
34. Liou WW, Goshgarian GH (1994) Quantitative assessment of the effect of chronic phrenicotomy on the induction of the crossed phrenic phenomenon. Exp Neurol 127:145-153.
35. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, Dong HX, Wu YJ, Fan GS, Jacquin MF, Hsu CY, Choi DW (1997) Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 17:5395-5406.
36. Mansel JK, Norman JR (1990) Respiratory complications and management of spinal cord injuries. Chest 97:1446-1452.
37. 2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J Neurochem 65:1740-1751.
38. McCrimmon DR, Dekin MS, Mitchell GS (1995) Glutamate, GABA, and serotonin in ventilatory control. In: Regulation of breathing (Dempsey JA, Pack AI, eds), pp 151-218. New York: Dekker.
39. Mocchetti I, Rabin SJ, Colangelo AM, Whittemore SR, Wrathall JR (1996) Increased basic fibroblast growth factor expression following contusive spinal cord injury. Exp Neurol 141:154-164.
40. Monteau R, Hilaire G (1991) Spinal respiratory motoneurons. Prog Neurobiol 37:83-144.
41. Moreno DE, Yu XJ, Goshgarian HG (1992) Identification of the axon pathways which mediate functional recovery of a paralyzed hemidiaphragm following spinal cord hemisection in the adult rat. Exp Neurol 116:219-228.
42. Moyer JA, Wood A, Zaleska MM, Ay I, Finklestein SP, Protter AA (1998) Basic fibroblast growth factor: a potential therapeutic agent for the treatment of acute neurodegenerative disorders and vascular insufficiency. Exp Opin Ther Patents 8:1425-1445.
43. Nakamura M, Fujimura Y, Yato Y, Watanabe M (1996) Muscle reorganization following incomplete cervical spinal cord injury in rats. Spinal Cord 34:752-756.
44. Noble LJ, Wrathall JR (1985) Spinal cord contusion in the rat: morphometric analyses of alterations in the spinal cord. Exp Neurol 88:135-149.
45. Noble LJ, Wrathall JR (1989a) Correlative analysis of lesion development and functional status after graded spinal cord contusive injuries in the rat. Exp Neurol 103:34-40.
46. Noble LJ, Wrathall JR (1989b) Distribution and time course of protein extravasation in the spinal cord after contusive injury. Brain Res 482:57-66.
47. O'Hara TE, Goshgarian GH (1991) Quantitative assessment of phrenic nerve functional recovery mediated by the crossed phrenic reflex at various time intervals after spinal cord injury. Exp Neurol 111:244-250.
48. Panjabi M, Wrathall JR (1988) Biomechanical analysis of spinal cord injury and functional loss. Spine 13:1365-1370.
49. Prakash UBS (1989) Neurologic diseases. In: Textbook of pulmonary diseases, 4th Edition, Vol 2 (Baum GL, Wolinsky E, eds), pp 1409-1436. Boston: Little, Brown.
50. Riggins RS, Kraus JF (1977) The risk of neurologic damage with fractures of the vertebrae. J Trauma 17:126-133.
51. Saji M, Miura M (1990) Thoracic excitatory motor neurons of the rats: localization and sites of origin of their premotor neurons. Brain Res 507:247-253.
52. Schramm LP, Adair JR, Stribling JM, Gray LP (1975) Preganglionic innervation of the adrenal gland of the rat: a study using horseradish peroxidase. Exp Neurol 49:540-553.
53. Shapiro S, Kubek M, Siemers E, Daly E, Callahan J, Putty T (1995) Quantification of thyrotropin-releasing hormone changes and serotonin content changes following graded spinal cord injury. J Surg Res 59:393-398.
54. Shapiro SS, Wilk MB (1965) An analysis of variance test of normality. Biometrika 52:591-612.
55. Slaok RS, Shuoart W (1994) Respiratory dysfunction associated with traumatic injury to the central nervous system. Clin Chest Med 15:739-749.
56. Sofroniew MV, Cooper JD, Svendsen CN, Crossman P, Ip NY, Lindsay RM, Zafra F, Lindholm D (1993) Atrophy but not death of adult septal cholinergic neurons after ablation of target capacity to produce mRNAs for NGF, BDNF, and NT3. J Neurosci 13:5263-5276.
57. Teng YD, Wrathall JR (1997) Local blockade of sodium channels by tetrodotoxin ameliorates tissue loss and long-term functional deficits resulting from experimental spinal cord injury. J Neurosci 17:4359-4366.
58. Teng YD, Mocchetti I, Taveira-DaSilva AM, Gillis RA, Wrathall JR (1998a) Basic and acidic fibroblast growth factor (FGF2) improves respiratory function after contusive spinal cord injury - a dose-response study. J Neurotrauma 15:899.
59. Teng YD, Mocchetti I, Wrathall JR (1998b) Basic and acidic fibroblast growth factors protect spinal motor neurons in vivo after experimental spinal cord injury. Eur J Neurosci 10:798-802.
60. Troyer AD, Heilporn A (1980) Respiratory mechanics in quadriplegia. The respiratory function of the intercostal muscles. Am Rev Respir Dis 122:591-600.
61. Turner DL, Bach KB, Martin PA, Olsen EB, Brownfield M, Foley KT, Mitchell GS (1997) Modulation of ventilatory control during exercise. Respir Physiol 110:277-285.
62. Vitacca M, Clini E, Facchetti D, Pagani M, Poloni M, Porta R, Ambrosino N (1997) Breathing pattern and respiratory mechanics in patients with amyotrophic lateral sclerosis. Eur Respir J 10:1614-1621.
63. Wrathall JR (1996) Weight-drop models of experimental spinal cord injury. In: Neurotrauma (Narayan RK, Wilberger JE, Povlishock JT, eds), pp 1381-1394. New York: McGraw.
64. Wrathall JR, Pettegrew R, Harvey F (1985) Spinal cord contusion in the rat: production of graded, reproducible injury groups. Exp Neurol 88:108-122.
65. Wrathall JR, Teng YD, Choiniere D, Mundt D (1992) Evidence that local non-NMDA receptors contribute to functional deficits in contusive spinal cord injury. Brain Res 586:140-143.
66. Wrathall JR, Choiniere D, Teng YD (1994) Dose-dependent reduction of tissue loss and functional impairment after spinal cord trauma with the AMPA/kainate antagonist NBQX. J Neurosci 14:6598-6607.
67. Wrathall JR, Li W, Hudson LD (1998) Myelin gene expression after experimental contusive spinal cord injury. J Neurosci 18:8780-8793.
68. Young W (1993) Secondary injury mechanisms in acute spinal cord injury. J Emerg Med 11:13-22.