Effects of electrical stimulation and gonadal steroids on rat facial nerve regenerative properties

Restorative Neurology and Neuroscience

Volumn 27, Issue 6, 2009, Pages 633-644

  Sharma, Nijee ^a   Coughlin, Lisa ^a   Porter, Ryan G ^a   Tanzer, Lisa ^a   Wurster, Robert D ^b   Marzo, Sam J ^a   Jones, Kathryn J ^a,b   Foecking, Eileen M ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Electrical stimulation; Gonadal steroids; Peripheral nerve injury; Regeneration

Indexed keywords

ANDROSTANOLONE; ESTRADIOL; TESTOSTERONE PROPIONATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRUSH TRAUMA; ELECTROSTIMULATION; FACIAL NERVE INJURY; GONADECTOMY; HORMONE ACTION; MALE; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; TREATMENT OUTCOME;

ANIMALS; AXOTOMY; DIHYDROTESTOSTERONE; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ESTRADIOL; FACIAL NERVE DISEASES; LEUCINE; LYSINE; MALE; NERVE REGENERATION; RATS; RATS, SPRAGUE-DAWLEY; STEROIDS; TESTOSTERONE PROPIONATE; TIME FACTORS; TRITIUM;

EID: 74249110988     PISSN: 09226028     EISSN: None     Source Type: Journal    
DOI: 10.3233/RNN-2009-0489     Document Type: Article

References (52)

1. Al-Majed, A. A., Neumann, C. M., Brushart, T. M., & Gordon, T. (2000a) Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci, 20, 2602-2608.
2. Al-Majed, A. A., Brushart, T. M., & Gordon, T. (2000b) Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. Eur J Neurosci, 12, 4381-4390.
3. Al-Majed, A. A., Tam, S. L., & Gordon, T. (2004) Electrical stimulation accelerates and enhances expression of regenerationassociated genes in regenerating rat femoral motoneurons. Cell Mol Neurobiol, 24, 379-402.
4. Bialek, M., Zaremba, P., Borowicz, K. K., & Czuczwar, S. J. (2004) Neuroprotective role of testosterone in the nervous system. Pol J Pharmacol, 56, 509-518.
5. Bisby, M. A. (1979) Differences in incorporation of axonally transported protein in regenerating motor and sensory axons. Exp Neurol, 65, 680-684.
6. Bisby, M. A. (1978) Fast axonal transport of labeled protein in sensory axons during regeneration. Exp Neurol, 61, 281-300.
7. Borgens, R. B. (1999) Electrically mediated regeneration and guidance of adult mammalian spinal axons into polymeric channels. Neuroscience, 91, 251-264.
8. Borgens, R. B., Roederer, E., & Cohen, M. J. (1981) Enhanced spinal cord regeneration in lamprey by applied electric fields. Science, 213, 611-617.
9. Brown, T. J., Khan, T., & Jones, K. J. (1999) Androgen induced acceleration of functional recovery after rat sciatic nerve injury. Restor Neurol Neurosci, 15, 289-295.
10. Brushart, T. M., Hoffman, P. N., Royall, R. M., Murinson, B. B., Witzel, C., & Gordon, T. (2002) Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. J Neurosci, 22, 6631-6638.
11. De Nicola, A. F. (1993) Steroid hormones and neuronal regeneration. Adv Neurol, 59, 199-206.
12. Drengler, S. M., Handa, R. J., & Jones, K. J. (1996) Regulation of androgen receptor mRNA expression in hamster facial motoneurons: differential effects of non-aromatizable and aromatizable androgens. Brain Res Mol Brain Res, 41, 8-15.
13. Fargo, K. N., Alexander, T. D., Tanzer, L., Poletti, A., & Jones, K. J. (2008) Androgen regulates neuritin mRNA levels in an in vivo model of steroid-enhanced peripheral nerve regeneration. J Neurotrauma, 25, 561-566.
14. Forman, D. S., & Berenberg, R. A. (1978) Regeneration of motor axons in the rat sciatic nerve studied by labeling with axonally transported radioactive proteins. Brain Res, 156, 213-225.
15. Forman, D. S., McQuarrie, I. G., Labore, F.W.,Wood, D. K., Stone, L. S., Braddock, C. H., & Fuchs, D. A. (1980) Time course of the conditioning lesion effect on axonal regeneration. Brain Res, 182, 180-185.
16. Hayashi, S. (1994) Immunocytochemical detection of estrogen receptor in the facial nucleus of the newborn rat by three antibodies with distinct epitopes. Horm Behav, 28, 530-536.
17. Hetzler, L. E., Sharma, N., Tanzer, L., Wurster, R. D., Leonetti, J., Marzo, S. J., Jones, K. J., & Foecking, E. M. (2008) Accelerating functional recovery after rat facial nerve injury: Effects of gonadal steroids and electrical stimulation. Otolaryngol Head Neck Surg, 139, 62-67.
18. Huppenbauer, C. B., Tanzer, L., DonCarlos, L. L., & Jones, K. J. (2005) Gonadal steroid attenuation of developing hamster facial motoneuron loss by axotomy: equal efficacy of testosterone, dihydrotestosterone, and 17-beta estradiol. J Neurosci, 25, 4004-4013.
19. Islamov, R. R., Hendricks, W. A., Jones, R. J., Lyall, G. J., Spanier, N. S., & Murashov, A. K. (2002) 17Beta-estradiol stimulates regeneration of sciatic nerve in female mice. Brain Res, 943, 283-286.
20. Jones, K. J. (1994) Androgenic enhancement of motor neuron regeneration. Ann N Y Acad Sci, 743, 141-61; discussion 161-164
21. Jones, K. J. (1993a) Gonadal steroids and neuronal regeneration. A therapeutic role. Adv Neurol, 59, 227-240.
22. Jones, K. J. (1993b) Recovery from facial paralysis following crush injury of the facial nerve in hamsters: differential effects of gender and androgen exposure. Exp Neurol, 121, 133-138.
23. Jones, K. J., Alexander, T. D., Brown, T. J., & Tanzer, L. (2000) Gonadal steroid enhancement of facial nerve regeneration: role of heat shock protein 70. J Neurocytol, 29, 341-349.
24. Jones, K. J., Drengler, S. M., & Oblinger, M. M. (1997) Gonadal steroid regulation of growth-associated protein GAP-43 mRNA expression in axotomized hamster facial motor neurons. Neurochem Res, 22, 1367-1374.
25. Jones, K. J., Storer, P. D., Drengler, S. M.,&Oblinger, M.M. (1999) Differential regulation of cytoskeletal gene expression in hamster facial motoneurons: effects of axotomy and testosterone treatment. J Neurosci Res, 57, 817-823.
26. Jung-Testas, I., Renoir, M., Bugnard, H., Greene, G. L., & Baulieu, E. E. (1992) Demonstration of steroid hormone receptors and steroid action in primary cultures of rat glial cells. J Steroid Biochem Mol Biol, 41, 621-631.
27. Kujawa, K. A., Emeric, E., & Jones, K. J. (1991) Testosterone differentially regulates the regenerative properties of injured hamster facial motoneurons. J Neurosci, 11, 3898-3906.
28. Kujawa, K. A., Kinderman, N. B., & Jones, K. J. (1989) Testosterone-induced acceleration of recovery from facial paralysis following crush axotomy of the facial nerve in male hamsters. Exp Neurol, 105, 80-85.
29. Kujawa, K. A., Tanzer, L., & Jones, K. J. (1995) Inhibition of the accelerative effects of testosterone on hamster facial nerve regeneration by the antiandrogen flutamide. Exp Neurol, 133, 138-143.
30. Lal, D., Hetzler, L. T., Sharma, N., Wurster, R. D., Marzo, S. J., Jones, K. J., & Foecking, E. M. (2008) Electrical stimulation facilitates rat facial nerve recovery from a crush injury. Otolaryngol Head Neck Surg, 139, 68-73.
31. Manivannan, S.,&Terakawa, S. (1994) Rapid sprouting of filopodia in nerve terminals of chromaffin cells, PC12 cells, and dorsal root neurons induced by electrical stimulation. J Neurosci, 14, 5917-5928.
32. McMurray, R., Islamov, R., & Murashov, A. K. (2003) Raloxifene analog LY117018 enhances the regeneration of sciatic nerve in ovariectomized female mice. Brain Res, 980, 140-145.
33. McQuarrie, I. G., & Grafstein, B. (1981) Effect of a conditioning lesion on optic nerve regeneration in goldfish. Brain Res, 216, 253-264.
34. Morimoto, T., Miyoshi, T., Fujikado, T., Tano, Y., & Fukuda, Y. (2002) Electrical stimulation enhances the survival of axotomized retinal ganglion cells in vivo. Neuroreport, 13, 227-230.
35. Oblinger, M. M., & Lasek, R. J. (1984) A conditioning lesion of the peripheral axons of dorsal root ganglion cells accelerates regeneration of only their peripheral axons. J Neurosci, 4, 1736-1744.
36. Patel, N., & Poo, M. M. (1982) Orientation of neurite growth by extracellular electric fields. J Neurosci, 2, 483-496.
37. Paxinos, G.,&Watson, C. S. (2007). The rat brain in stereotaxic coordinates: Compact 6th edition, sixth edition Academic Press.
38. Pockett, S., & Gavin, R. M. (1985) Acceleration of peripheral nerve regeneration after crush injury in rat. Neurosci Lett, 59, 221-224.
39. Santagati, S., Melcangi, R. C., Celotti, F., Martini, L., & Maggi, A. (1994) Estrogen receptor is expressed in different types of glial cells in culture. J Neurochem, 63, 2058-2064.
40. Schumacher, M., Robel, P., & Baulieu, E. E. (1996) Development and regeneration of the nervous system: a role for neurosteroids. Dev Neurosci, 18, 6-21.
41. Tanzer, L.,& Jones, K. J. (1997) Gonadal steroid regulation of hamster facial nerve regeneration: effects of dihydrotestosterone and estradiol. Exp Neurol, 146, 258-264.
42. Tetzlaff, J.,Tanzer, L.,&Jones, K. J. (2007a) Cellular localization of androgen and estrogen receptors in mouse-derived motoneuron hybrid cells and mouse facial motoneurons. Dev Neurobiol,67, 1362-1370.
43. Tetzlaff, J., Tanzer, L., & Jones, K. J. (2007b) Exogenous androgen treatment delays the stress response following hamster facial nerve injury. J Neuroendocrinol, 19, 383-389.
44. Tetzlaff, J. E., Huppenbauer, C. B., Tanzer, L., Alexander, T. D., & Jones, K. J. (2006) Motoneuron injury and repair: New perspectives on gonadal steroids as neurotherapeutics. J Mol Neurosci, 28, 53-64.
45. Udina, E., Furey, M., Busch, S., Silver, J., Gordon, T., & Fouad, K. (2008) Electrical stimulation of intact peripheral sensory axons in rats promotes outgrowth of their central projections. Exp Neurol, 210, 238-247.
46. Valero-Cabre, A., Tsironis, K., Skouras, E., Navarro, X., & Neiss, W. F. (2004) Peripheral and spinal motor reorganization after nerve injury and repair. J Neurotrauma, 21, 95-108.
47. Vivo, M., Puigdemasa, A., Casals, L., Asensio, E., Udina, E., & Navarro, X. (2008) Immediate electrical stimulation enhances regeneration and reinnervation and modulates spinal plastic changes after sciatic nerve injury and repair. Exp Neurol, 211, 180-193.
48. Yu, W. H. (1982) Effect of testosterone on the regeneration of the hypoglossal nerve in rats. Exp Neurol, 77, 129-141.
49. Yu, W. H., & McGinnis, M. Y. (2001) Androgen receptors in cranial nerve motor nuclei of male and female rats. J Neurobiol, 46, 1-10.
50. Yu, W. H., & Srinivasan, R. (1981) Effect of testosterone and 5 alpha-dihydrotestosterone on regeneration of the hypoglossal nerve in rats. Exp Neurol, 71, 431-435. (Pubitemid 11179639)
51. Yu, W. H., & Yu, M. C. (1983) Acceleration of the regeneration of the crushed hypoglossal nerve by testosterone. Exp Neurol, 80, 349-360.
52. Zhou, Z. X., Lane, M. V., Kemppainen, J. A., French, F. S., & Wilson, E. M. (1995) Specificity of ligand-dependent androgen receptor stabilization: receptor domain interactions influence ligand dissociation and receptor stability. Mol Endocrinol, 9, 208-218.