Effect of endogenous androgens on 17β-estradiol-mediated protection after spinal cord injury in male rats

Journal of Neurotrauma

Volumn 27, Issue 3, 2010, Pages 611-626

  Kachadroka, Supatra ^a,b   Hall, Alicia M ^a   Niedzielko, Tracy L ^a   Chongthammakun, Sukumal ^b   Floyd, Candace L ^a  

^a University of Alabama at Birmingham   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Apoptosis; Bax; Bcl xL; Estrogen; Serum levels

Indexed keywords

DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; ESTRADIOL; ESTROGEN; PROTEIN BAX; PROTEIN BCL XL; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BLADDER; BLADDER CAPACITY; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CRUSH TRAUMA; GEL ELECTROPHORESIS; GONADECTOMY; HINDLIMB; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; NEUROPROTECTION; NICK END LABELING; NONHUMAN; OPEN FIELD BEHAVIOR; OPTICAL DENSITY; ORGAN WEIGHT; PROTEIN EXPRESSION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; RAT; SPINAL CORD; SPINAL CORD INJURY; SPINAL CORD VENTRAL HORN; TESTOSTERONE BLOOD LEVEL; WESTERN BLOTTING; WHITE MATTER;

ANDROGENS; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; GAIT DISORDERS, NEUROLOGIC; MALE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; ORCHIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; SEX FACTORS; SPINAL CORD; SPINAL CORD INJURIES; URINARY BLADDER, NEUROGENIC; WALLERIAN DEGENERATION;

EID: 77950598169     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2009.1069     Document Type: Article

References (76)

1. Ahmed, Y., Lin, D.L., Ferguson, C., Esparza, N., and Damaser, M.S. (2006). Effect of estrogen on urethral function and nerve regeneration following pudendal nerve crush in the female rat. J. Urol. 175, 1948-1952.
2. Alonso, G., Guillemain, I., Dumoulin, A., Privat, A., and Patey, G. (1997). Immunolocalization of Bcl-xL=S in the central nervous system of neonatal and adult rats. Cell Tissue Res. 288, 59-68.
3. Anderson, K.D. (2004). Targeting recovery: Priorities of the spinal cord-injured population. J. Neurotrauma 21, 1371-1383.
4. Antignani, A., and Youle, R.J. (2006). How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr. Opin. Cell Biol. 18, 685-689.
5. Azcoitia, I., Sierra, A., Veiga, S., Honda, S., Harada, N., and Garcia-Segura, L.M. (2001). Brain aromatase is neuroprotective. J. Neurobiol. 47, 318-329.
6. Basso, D.M. (2000). Neuroanatomical substrates of functional recovery after experimental spinal cord injury: Implications of basic science research for human spinal cord injury. Phys. Ther. 80, 808-817.
7. Basso, D.M., Beattie, M.S., and Bresnahan, J.C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21.
8. Beattie, M.S. (2004). Inflammation and apoptosis: linked therapeutic targets in spinal cord injury. Trends Mol. Med. 10, 580-583.
9. Beattie, M.S., Farooqui, A.A., and Bresnahan, J.C. (2000). Review of current evidence for apoptosis after spinal cord injury. J. Neurotrauma 17, 915-925.
10. Bialek, M., Zaremba, P., Borowicz, K.K., and Czuczwar, S.J. (2004). Neuroprotective role of testosterone in the nervous system. Pol. J. Pharmacol. 56, 509-518.
11. Carr, B.G., Caplan, J.M., Pryor, J.P., and Branas, C.C. (2006). A meta-analysis of prehospital care times for trauma. Prehosp. Emerg. Care 10, 198-206.
12. Carson, F.L. (1990). Histotechnology: A Self-Instructional Text. Chicago: ASCP Press, pps. 170-171.
13. Caruso, A., Di Giorgi Gerevini, V., Castiglione, M., Marinelli, F., Tomassini, V., Pozzilli, C., Caricasole, A., Bruno, V., Caciagli, F., Moretti, A., Nicoletti, F., and Melchiorri, D. (2004). Testosterone amplifies excitotoxic damage of cultured oligodendrocytes. J. Neurochem. 88, 1179-1185.
14. Chang, B.S., Kelekar, A., Harris, M.H., Harlan, J.E., Fesik, S.W., and Thompson, C.B. (1999). The BH3 domain of Bcl-x(S) is required for inhibition of the antiapoptotic function of Bcl-x(L). Mol. Cell Biol. 19, 6673-6681.
15. Chaovipoch, P., Jelks, K.A., Gerhold, L.M., West, E.J., Chongthammakun, S., and Floyd, C.L. (2006). 17beta-estradiol is protective in spinal cord injury in post- and pre-menopausal rats. J. Neurotrauma 23, 830-852.
16. Chisu, V., Manca, P., Lepore, G., Gadau, S., Zedda, M., and Farina, V. (2006). Testosterone induces neuroprotection from oxidative stress. Effects on catalase activity and 3-nitro-ltyrosine incorporation into alpha-tubulin in a mouse neuroblastoma cell line. Arch. Ital. Biol. 144, 63-73.
17. Clark, M.J., Schopp, L.H., Mazurek, M.O., Zaniletti, I., Lammy, A.B., Martin, T.A., Thomas, F.P., and Acuff, M.E. (2008). Testosterone levels among men with spinal cord injury: Relationship between time since injury and laboratory values. Am. J. Phys. Med. Rehabil. 87, 758-767.
18. Cuzzocrea, S., Genovese, T., Mazzon, E., Esposito, E., Di, P. R., Muia, C., Crisafulli, C., Peli, A., Bramanti, P., and Chaudry, I.H. (2008). Effect of 17beta-estradiol on signal transduction pathways and secondary damage in experimental spinal cord trauma. Shock 29, 362-371.
19. De Groat,W.C.,Kawatani, M., Hisamitsu, T.,Cheng, C.L., Ma,C.P., Thor, K., Steers, W., and Roppolo, J.R. (1990). Mechanisms underlying the recovery of urinary bladder function following spinal cord injury. J. Auton. Nerv. Syst. 30 Suppl, S71-S77.
20. Dietz, V., Nakazawa, K., Wirz, M., and Erni, T. (1999). Level of spinal cord lesion determines locomotor activity in spinal man. Exp. Brain Res. 128, 405-409.
21. Doperalski, N.J., Sandhu, M.S., Bavis, R.W., Reier, P.J., and Fuller, D.D. (2008). Ventilation and phrenic output following high cervical spinal hemisection in male vs. female rats. Respir. Physiol. Neurobiol. 162, 160-167.
22. Faden, A.I., and Stoica, B. (2007). Neuroprotection: Challenges and opportunities. Arch. Neurol. 64, 794-800.
23. Farooque, M., Suo, Z., Arnold, P.M., Wulser, M.J., Chou, C.T., Vancura, R.W., Fowler, S., and Festoff, B.W. (2006). Genderrelated differences in recovery of locomotor function after spinal cord injury in mice. Spinal Cord 44, 182-187.
24. Fehlings, M.G., and Tator, C.H. (1995). The relationships among the severity of spinal cord injury, residual neurological function, axon counts, and counts of retrogradely labeled neurons after experimental spinal cord injury. Exp. Neurol. 132, 220-228.
25. Ferguson, A.R., Hook, M.A., Garcia, G., Bresnahan, J.C., Beattie, M.S., and Grau, J.W. (2004). A simple post hoc transformation that improves the metric properties of the BBB scale for rats with moderate to severe spinal cord injury. J. Neurotrauma 21, 1601-1613.
26. Gatson, J.W., and Singh, M. (2007). Activation of a membraneassociated androgen receptor promotes cell death in primary cortical astrocytes. Endocrinology 148, 2458-2464.
27. George, E.R., Scholten, D.J., Buechler, C.M., Jordan-Tibbs, J., Mattice, C., and Albrecht, R.M. (1995). Failure of methylprednisolone to improve the outcome of spinal cord injuries. Am. Surg. 61, 659-663.
28. Gold, S.M., and Voskuhl, R.R. (2006). Testosterone replacement therapy for the treatment of neurological and neuropsychiatric disorders. Curr. Opin. Investig. Drugs 7, 625-630.
29. Gorska, T., Chojnicka-Gittins, B., Majczynski, H., and Zmyslowski, W. (2007). Overground locomotion after incomplete spinal lesions in the rat: Quantitative gait analysis. J. Neurotrauma 24, 1198-1218.
30. Gorska, T., Chojnicka-Gittins, B., Majczynski, H., and Zmyslowski, W. (2009). Recovery of overground locomotion following partial spinal lesions of different extent in the rat. Behav. Brain Res. 196, 286-296.
31. Hall, E.D., and Springer, J.E. (2004). Neuroprotection and acute spinal cord injury: A reappraisal. NeuroRx 1, 80-100.
32. Hammond, J., Le, Q., Goodyer, C., Gelfand, M., Trifiro, M., and LeBlanc, A. (2001). Testosterone-mediated neuroprotection through the androgen receptor in human primary neurons. J. Neurochem. 77, 1319-1326.
33. Hamner, S., Skoglosa, Y., and Lindholm, D. (1999). Differential expression of bcl-w and bcl-x messenger RNA in the developing and adult rat nervous system. Neuroscience 91, 673-684.
34. Harris, M.H., and Thompson, C.B. (2000). The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability. Cell Death Differ. 7, 1182-1191.
35. Hauben, E., Mizrahi, T., Agranov, E., and Schwartz, M. (2002). Sexual dimorphism in the spontaneous recovery from spinal cord injury: A gender gap in beneficial autoimmunity? Eur. J. Neurosci. 16, 1731-1740.
36. Hugenholtz, H. (2003). Methylprednisolone for acute spinal cord injury: Not a standard of care. CMAJ 168, 1145-1146.
37. Huppenbauer, C.B., Tanzer, L., DonCarlos, L.L., and 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.
38. Keane, R.W., Davis, A.R., and Dietrich, W.D. (2006). Inflammatory and apoptotic signaling after spinal cord injury. J. Neurotrauma 23, 335-344.
39. Keirstead, H.S., Fedulov, V., Cloutier, F., Steward, O., and Duel, B.P. (2005). A noninvasive ultrasonographic method to evaluate bladder function recovery in spinal cord injured rats. Exp. Neurol. 194, 120-127.
40. Kloos, A.D., Fisher, L.C., Detloff, M.R., Hassenzahl, D.L., and Basso, D.M. (2005). Stepwise motor and all-or-none sensory recovery is associated with nonlinear sparing after incremental spinal cord injury in rats. Exp. Neurol. 191, 251-265.
41. Kujawa, K.A., Emeric, E., and Jones, K.J. (1991). Testosterone differentially regulates the regenerative properties of injured hamster facial motoneurons. J. Neurosci. 11, 3898-3906.
42. Kujawa, K.A., Kinderman, N.B., and 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.
43. Kujawa, K.A., Tanzer, L., and 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.
44. Lee, H.C., Cho, D.Y., Lee, W.Y., and Chuang, H.C. (2007). Pitfalls in treatment of acute cervical spinal cord injury using highdose methylprednisolone: A retrospect audit of 111 patients. Surg. Neurol. 68 Suppl 1, S37-S41.
45. Motoyama, N., Wang, F., Roth, K.A., Sawa, H., Nakayama, K., Nakayama, K., Negishi, I., Senju, S., Zhang, Q., Fujii, S., and Lon, D.Y. (1995). Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267, 1506-1510.
46. National Spinal Cord Injury Statistical Center (2008). Spinal cord injury information network.
47. Nesic-Taylor, O., Cittelly, D., Ye, Z., Xu, G.Y., Unabia, G., Lee, J.C., Svrakic, N.M., Liu, X.H., Youle, R.J., Wood, T.G., McAdoo, D., Westlund, K.N., Hulsebosch, C.E., and Perez-Polo, J.R. (2005). Exogenous Bcl-xL fusion protein spares neurons after spinal cord injury. J. Neurosci. Res. 79, 628-637.
48. Nguyen, T.V., Yao, M., and Pike, C.J. (2005). Androgens activate mitogen-activated protein kinase signaling: Role in neuroprotection. J. Neurochem. 94, 1639-1651.
49. Noble, L.J., and Wrathall, J.R. (1987). An inexpensive apparatus for producing graded spinal cord contusive injury in the rat. Exp. Neurol. 95, 530-533.
50. Nout, Y.S., Leedy, G.M., Beattie, M.S., and Bresnahan, J.C. (2006). Alterations in eliminative and sexual reflexes after spinal cord injury: Defecatory function and development of spasticity in pelvic floor musculature. Prog. Brain Res. 152, 359-372.
51. Ogata, T., Nakamura, Y., Tsuji, K., Shibata, T., and Kataoka, K. (1993). Steroid hormones protect spinal cord neurons from glutamate toxicity. Neuroscience 55, 445-449.
52. Orlando, R., Caruso, A., Molinaro, G., Motolese, M., Matrisciano, F., Togna, G., Melchiorri, D., Nicoletti, F., and Bruno, V. (2007). Nanomolar concentrations of anabolic-androgenic steroids amplify excitotoxic neuronal death in mixed mouse cortical cultures. Brain Res. 1165, 21-29.
53. Parsadanian, A.S., Cheng, Y., Keller-Peck, C.R., Holtzman, D.M., and Snider, W.D. (1998). Bcl-xL is an antiapoptotic regulator for postnatal CNS neurons. J. Neurosci. 18, 1009-1019.
54. Pike, C.J., Nguyen, T.V., Ramsden, M., Yao, M., Murphy, M.P., & Rosario, E.R. (2008). Androgen cell signaling pathways involved in neuroprotective actions. Horm. Behav. 53, 693-705.
55. Pikov, V., and Wrathall, J.R. (2001). Coordination of the bladder detrusor and the external urethral sphincter in a rat model of spinal cord injury: Effect of injury severity. J. Neurosci. 21, 559-569.
56. Pikov, V., and Wrathall, J. R. (2002). Altered glutamate receptor function during recovery of bladder detrusor-external urethral sphincter coordination in a rat model of spinal cord injury. J. Pharmacol. Exp. Ther. 300, 421-427.
57. Pikov, V., Gillis, R.A., Jasmin, L., and Wrathall, J.R. (1998). Assessment of lower urinary tract functional deficit in rats with contusive spinal cord injury. J. Neurotrauma 15, 375-386.
58. Qiu, J., Nesic, O., Ye, Z., Rea, H., Westlund, K.N., Xu, G.Y., McAdoo, D., Hulsebosch, C.E., and Perez-Polo, J.R. (2001). Bcl-xL expression after contusion to the rat spinal cord. J. Neurotrauma 18, 1267-1278.
59. Ritz, M.F., and Hausmann, O.N. (2008). Effect of 17beta-estradiol on functional outcome, release of cytokines, astrocyte reactivity and inflammatory spreading after spinal cord injury in male rats. Brain Res. 1203, 177-188.
60. Roselli, C.F. (2007). Brain aromatase: Roles in reproduction and neuroprotection. J. Steroid Biochem. Mol. Biol. 106, 143-150.
61. Rosse, T., Olivier, R., Monney, L., Rager, M., Conus, S., Fellay, I., Jansen, B., and Borner, C. (1998). Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 391, 496-499.
62. Rouleau, P., Ung, R.V., Lapointe, N.P., and Guertin, P.A. (2007). Hormonal and immunological changes in mice after spinal cord injury. J. Neurotrauma 24, 367-378.
63. Schopp, L.H., Clark, M., Mazurek, M.O., Hagglund, K.J., Acuff, M.E., Sherman, A.K., and Childers, M.K. (2006). Testosterone levels among men with spinal cord injury admitted to inpatient rehabilitation. Am. J. Phys. Med. Rehabil. 85, 678-684.
64. Springer, J.E. (2002). Apoptotic cell death following traumatic injury to the central nervous system. J. Biochem. Mol. Biol. 35, 94-105.
65. Sribnick, E.A., Matzelle, D.D., Ray, S.K., and Banik, N.L. (2006). Estrogen treatment of spinal cord injury attenuates calpain activation and apoptosis. J. Neurosci. Res. 84, 1064-1075.
66. Sribnick, E.A., Wingrave, J.M., Matzelle, D.D., Wilford, G.G., Ray, S.K., and Banik, N.L. (2005). Estrogen attenuated markers of inflammation and decreased lesion volume in acute spinal cord injury in rats. J. Neurosci. Res. 82, 283-293.
67. Suberviola, B., Gonzalez-Castro, A., Llorca, J., Ortiz-Melon, F., and Minambres, E. (2008). Early complications of high-dose methylprednisolone in acute spinal cord injury patients. Injury 39, 748-752.
68. Swartz, K.R., Fee, D.B., Joy, K.M., Roberts, K.N., Sun, S., Scheff, N.N., Wilson, M.E., and Scheff, S.W. (2007). Gender differences in spinal cord injury are not estrogen-dependent. J. Neurotrauma 24, 473-480.
69. Webb, A.A., Chan, C.B., Brown, A., and Saleh, T.M. (2006). Estrogen reduces the severity of autonomic dysfunction in spinal cord-injured male mice. Behav. Brain Res. 171, 338-349.
70. Wise, P.M., Dubal, D.B., Wilson, M.E., Rau, S.W., and Liu, Y. (2001). Estrogens: Trophic and protective factors in the adult brain. Front. Neuroendocrinol. 22, 33-66.
71. Yang, E., and Korsmeyer, S.J. (1996). Molecular thanatopsis: A discourse on the BCL2 family and cell death. Blood 88, 386-401.
72. Yang, S.H., Liu, R., Wen, Y., Perez, E., Cutright, J., Brun-Zinkernagel, A.M., Singh, M., Day, A.L., and Simpkins, J.W. (2005). Neuroendocrine mechanism for tolerance to cerebral ischemia-reperfusion injury in male rats. J. Neurobiol. 62, 341-351.
73. Yang, S.H., Perez, E., Cutright, J., Liu, R., He, Z., Day, A.L., and Simpkins, J.W. (2002). Testosterone increases neurotoxicity of glutamate in vitro and ischemia-reperfusion injury in an animal model. J. Appl. Physiol. 92, 195-201.
74. Yune, T.Y., Kim, S.J., Lee, S.M., Lee, Y.K., Oh, Y.J., Kim, Y.C., Markelonis, G.J., and Oh, T.H. (2004). Systemic administration of 17beta-estradiol reduces apoptotic cell death and improves functional recovery following traumatic spinal cord injury in rats. J. Neurotrauma 21, 293-306.
75. Yune, T.Y., Park, H.G., Lee, J.Y., and Oh, T.H. (2008). Estrogeninduced Bcl-2 expression after spinal cord injury is mediated through Phosphoinositide-3-Kinase=Akt-dependent CREB activation. J. Neurotrauma 25, 1121-1131.
76. Zhang, X., Chen, Y., Jenkins, L.W., Kochanek, P.M., and Clark, R.S. (2005). Bench-to-bedside review: Apoptosis=programmed cell death triggered by traumatic brain injury. Crit. Care 9, 66-75. (Pubitemid 40246773)