17β-estradiol is protective in spinal cord injury in post- and pre-menopausal rats

Journal of Neurotrauma

Volumn 23, Issue 6, 2006, Pages 830-852

  Chaovipoch, Pimonporn ^a,c   Jelks, Karen A Bozak ^b   Gerhold, Lynnette M ^b   West, Eric J ^a   Chongthammakun, Sukumal ^c   Floyd, Candace L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Aging; Apoptosis; Estrogen; Menopause; Neuroprotection; TUNEL

Indexed keywords

ESTRADIOL; CRESYL VIOLET; FLUORESCENT DYE; FLUORO JADE; INDOLE DERIVATIVE; LUXOL FAST BLUE MBS; NEUROPROTECTIVE AGENT; ORGANIC COMPOUND; OXAZINE DERIVATIVE;

ADOLESCENT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN ISCHEMIA; CONTROLLED STUDY; FEMALE; MOTOR PERFORMANCE; NEUROPROTECTION; NONHUMAN; OVARIECTOMY; POSTMENOPAUSE; PREMENOPAUSE; RAT; SPINAL CORD INJURY; WHITE MATTER; ANIMAL; BODY WEIGHT; CELL COUNT; DRUG EFFECT; ESTRUS CYCLE; HINDLIMB; MICTURITION; MOTOR ACTIVITY; NICK END LABELING; PHYSIOLOGY; SEXUAL MATURATION;

ANIMALS; BODY WEIGHT; CELL COUNT; ESTRADIOL; ESTROUS CYCLE; FEMALE; FLUORESCENT DYES; HINDLIMB; IN SITU NICK-END LABELING; INDOLES; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; ORGANIC CHEMICALS; OVARIECTOMY; OXAZINES; RATS; SEXUAL MATURATION; SPINAL CORD INJURIES; URINATION;

EID: 33745501785     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2006.23.830     Document Type: Article

References (129)

1. ALKAYED, N.J., HARUKUNI, I., KIMES, A.S., LONDON, E.D., TRAYSTMAN, R.J., and HURN, P.D. (1998). Gender-linked brain injury in experimental stroke. Stroke 29, 159-166.
2. ALKAYED, N.J., MURPHY, S.J., TRAYSTMAN, R.J., HURN, P.D., and MILLER, V.M. (2000). Neuroprotective effects of female gonadal steroids in reproductively senescent female rats. Stroke 31, 161-168.
3. ANDERSON, K.D. (2004). Targeting recovery: priorities of the spinal cord-injured population. J. Neurotrauma 21, 1371-1383.
4. ANDERSON, K.J., FUGACCIA, I., and SCHEFF, S.W. (2003). Fluoro-jade B stains quiescent and reactive astrocytes in the rodent spinal cord. J. Neurotrauma 20, 1223-1231.
5. ANDERSON, K.J., MILLER, K.M., FUGACCIA, I., and SCHEFF, S.W. (2005). Regional distribution of fluoro-jade B staining in the hippocampus following traumatic brain injury. Exp. Neurol. 193, 125-130.
6. ASHCROFT, G.S., and ASHWORTH, J.J. (2003). Potential role of estrogens in wound healing. Am. J. Clin. Dermatol. 4, 737-743.
7. AUGOULEA, A., MASTORAKOS, G., LAMBRINOUDAKI, I., CHRISTODOULAKOS, G., and CREATSAS, G. (2005). Role of postmenopausal hormone replacement therapy on body fat gain and leptin levels. Gynecol. Endocrinol. 20, 227-235.
8. BAKE, S., and SOHRABJI, F. (2004). 17-Beta-estradiol differentially regulates blood-brain barrier permeability in young and aging female rats. Endocrinology 145, 5471-5475.
9. BAKER, K.A., and HAGG, T. (2005). An adult rat spinal cord contusion model of sensory axon degeneration: the estrus cycle or a preconditioning lesion do not affect outcome. J. Neurotrauma 22, 415-428.
10. 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.
11. BEHL, C., TRAPP, T., SKUTELLA, T., and HOLSBOER, F. (1997). Protection against oxidative stress-induced neuronal cell death-a novel role for RU486. Eur. J. Neurosci. 9, 912-920.
12. BRAMLETT, H.M. (2005). Sex differences and the effect of hormonal therapy on ischemic brain injury. Pathophysiology 12, 17-27.
13. BRAMLETT, H.M., and DIETRICH, W.D. (2001). Neuropathological protection after traumatic brain injury in intact female rats versus males or ovariectomized females. J. Neurotrauma 18, 891-900.
14. BURGER, H.G. (1999). The endocrinology of the menopause. J. Steroid Biochem. Mol. Biol. 69, 31-35.
15. CAI, D., QIU, J., CAO, Z., MCATEE, M., BREGMAN, B.S., and FILBIN, M.T. (2001). Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J. Neurosci. 21, 4731-4739.
16. CHAKRABORTY, T.R., and GORE, A.C. (2004). Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function. Exp. Biol. Med. (Maywood) 229, 977-987.
17. CUSHMAN, M. (2002). Effects of hormone replacement therapy and estrogen receptor modulators on markers of inflammation and coagulation. Am. J. Cardiol. 90, 7F-10F.
18. DE GROAT W.C., KAWATANI, M., HISAMITSU, T., et al. (1990). Mechanisms underlying the recovery of urinary bladder function following spinal cord injury. J. Auton. Nerv. Syst. 30, Suppl, S71-S77.
19. DONG, L., WANG, W., WANG, F., et al. (1999). Mechanisms of transcriptional activation of bcl-2 gene expression by 17beta-estradiol in breast cancer cells. J. Biol. Chem. 274, 32099-32107.
20. DRUCKMANN, R. (2001). Review. Female sex hormones, autoimmune diseases and immune response. Gynecol. Endocrinol. 15, Suppl 6, 69-76.
21. DRYDEN, D.M., SAUNDERS, L.D., ROWE, B.H., et al. (2003). The epidemiology of traumatic spinal cord injury in Alberta, Canada. Can. J. Neurol. Sci. 30, 113-121.
22. DUBAL, D.B., KASHON, M.L., PETTIGREW L.C., et al. (1998). Estradiol protects against ischemic injury. J. Cereb. Blood Flow Metab. 18, 1253-1258.
23. DUBAL, D.B., and WISE, P.M. (2001). Neuroprotective effects of estradiol in middle-aged female rats. Endocrinology 142, 43-48.
24. DUMONT, R.J., OKONKWO, D.O., VERMA, S., et al. (2001). Acute spinal cord injury. Part I. Pathophysiologic mechanisms. Clin. Neuropharmacol. 24, 254-264.
25. EISCH, A.J., SCHMUED, L.C., and MARSHALL, J.F. (1998). Characterizing cortical neuron injury with Fluoro-Jade labeling after a neurotoxic regimen of methamphetamine. Synapse 30, 329-333.
26. EMERSON, C.S., HENDRICK, J.P., and VINK, R. (1993). Estrogen improves biochemical and neurological outcome following traumatic brain injury in male rats, but not in females. Brain Res. 608, 95-100.
27. FARIN, A., DEUTSCH, R., BIEGON, A., and MARSHALL, L.F. (2003). Sex-related differences in patients with severe head injury: greater susceptibility to brain swelling in female patients 50 years of age and younger. J. Neurosurg. 98, 32-36.
28. FAROOQUE, M., SUO, Z., ARNOLD, P.M., et al. (2006). Gender-related differences in recovery of locomotor function after spinal cord injury in mice. Spinal Cord (in press).
29. 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.
30. FREEMAN, M.E. (1988). The ovarian cycle of the rat, in: Physiology of Reproduction. E. Knobil and J. Neil (eds), Raven Press: New York, pps. 1893-1928.
31. FURLAN, J.C., KRASSIOUKOV, A.V., and FEHLINGS, M.G. (2005). The effects of gender on clinical and neurological outcomes after acute cervical spinal cord injury. J. Neurotrauma 22, 368-381.
32. GARCIA-SEGURA, L.M., AZCOITIA, I., and DONCARLOS, L.L. (2001). Neuroprotection by estradiol. Prog. Neurobiol. 63, 29-60.
33. GARCIA-SEGURA, L.M., CARDONA-GOMEZ, P., NAFTOLING, F., and CHOWEN, J.A. (1998). Estradiol upregulates Bcl-2 expression in adult brain neurons. Neuroreport 9, 593-597.
34. GOODMAN, Y., BRUCE, A.J., CHENG, B., and MATTSON, M.P. (1996). Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J. Neurochem. 66, 1836-1844.
35. GREEN, P.S., and SIMPKINS, J.W. (2000). Neuroprotective effects of estrogens: potential mechanisms of action. Int. J. Dev. Neurosci. 18, 347-358.
36. GUNDERSON, H.J. (1986). Stereology of arbitrary particles: a review of unbiased number and size estimator and the presentation of some new ones, in memory of William R. Thompson. J. Microscop. 143, 3-45.
37. HALL, E.D., GIBSON, T.R., and PAVEL, K.M. (2005). Lack of a gender difference in post-traumatic neurodegeneration in the mouse controlled cortical impact injury model. J. Neurotrauma 22, 669-679.
38. HALL, P.A. (1999). Assessing apoptosis: a critical survey. Endocrinol. Relat. Cancer 6, 3-8.
39. HALLAM, T.M., FLOYD, C.L., FOLKERTS, M.M., et al. (2004). Comparison of behavioral deficits and acute neuronal degeneration in rat lateral fluid percussion and weight-drop brain injury models. J. Neurotrauma 21, 521-539.
40. HAUSMANN, O.N. (2003). Post-traumatic inflammation following spinal cord injury. Spinal Cord 41, 369-378.
41. HOULE, J.D., and YE, J.H. (1999). Survival of chronically-injured neurons can be prolonged by treatment with neurotrophic factors. Neuroscience 94, 929-936.
42. HOUWELING, D.A., VAN ASSELDONK, J.T., LANKHORST, A.J., et al. (1998). Local application of collagen containing brain-derived neurotrophic factor decreases the loss of function after spinal cord injury in the adult rat. Neurosci. Lett. 251, 193-196.
43. HUGHES, S.E. (2003). Detection of apoptosis using in situ markers for DNA strand breaks in the failing human heart. Fact or epiphenomenon? J. Pathol. 201, 181-186.
44. HURN, P.D., and BRASS, L.M. (2003). Estrogen and stroke: a balanced analysis. Stroke 34, 338-341.
45. IMAI, K., KADOWAKI, T., AIZAWA, Y., and FUKUTOMI, K. (1994). Morbidity rates of complications in persons with spinal cord injury according to the site of injury and with special reference to hypertension. Paraplegia 32, 246-252.
46. JACKSON, A.B., DIJKERS, M., DEVIVO, M.J., and POCZATEK, R.B. (2004). A demographic profile of new traumatic spinal cord injuries: change and stability over 30 years. Arch. Phys. Med. Rehabil. 85, 1740-1748.
47. JAKEMAN, L.B., WEI, P., GUAN, Z., and STOKES, B.T. (1998). Brain-derived neurotrophic factor stimulates hindlimb stepping and sprouting of cholinergic fibers after spinal cord injury. Exp. Neurol. 154, 170-184.
48. JEZIERSKI, M.K., and SOHRABJI, F. (2001). Neurotrophin expression in the reproductively senescent forebrain is refractory to estrogen stimulation. Neurobiol. Aging 22, 309-319.
49. 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.
50. KIM, D., SCHALLERT, T., LIU, Y., et al. (2001). Transplantation of genetically modified fibroblasts expressing BDNF in adult rats with a subtotal hemisection improves specific motor and sensory functions. Neurorehabil. Neural Repair 15, 141-150.
51. 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.
52. KLUVERA, H., and BARRERA, E. (1953). A method for the combined staining of cells and fibers in the nervous system. J. Neuropathol. Exp. Neurol. 4, 400-403.
53. KODA, M., HASHIMOTO, M., MURAKAMI, M., et al. (2004). Adenovirus vector-mediated in vivo gene transfer of brain-derived neurotrophic factor (BDNF) promotes rubrospinal axonal regeneration and functional recovery after complete transection of the adult rat spinal cord. J. Neurotrauma 21, 329-337.
54. KODA, M., MURAKAMI, M., INO, H., et al. (2002). Brain-derived neurotrophic factor suppresses delayed apoptosis of oligodendrocytes after spinal cord injury in rats. J. Neurotrauma 19, 777-785.
55. KRASSIOUKOV, A.V., FURLAN, J.C., and FEHLINGS, M.G. (2003). Medical co-morbidities, secondary complications, and mortality in elderly with acute spinal cord injury. J. Neurotrauma 20, 391-399.
56. KRISTENSEN, K., PEDERSEN, S.B., VESTERGAARD, P., MOSEKILDE, L., and RICHELSEN, B. (1999). Hormone replacement therapy affects body composition and leptin differently in obese and non-obese postmenopausal women. J. Endocrinol. 163, 55-62.
57. KUNDROTIENE, J., WAGNER, A., and LILJEQUIST, S. (2004). Fluoro-Jade and TUNEL staining as useful tools to identify ischemic brain damage following moderate extradural compression of sensorimotor cortex. Acta Neurobiol. Exp. (Warsaw) 64, 153-162.
58. KUPINA, N.C., DETLOFF, M.R., BOBROWSKI, W.F., SNYDER, B.J., and HALL, E.D. (2003). Cytoskeletal protein degradation and neurodegeneration evolves differently in males and females following experimental head injury. Exp. Neurol. 180, 55-73.
59. LI, G.L., BRODIN, G., FAROOQUE, M., et al. (1996). Apoptosis and expression of Bcl-2 after compression trauma to rat spinal cord. J. Neuropathol. Exp. Neurol. 55, 280-289.
60. LINFORD, N.J., and DORSA, D.M. (2002). 17-Beta-Estradiol and the phytoestrogen genistein attenuate neuronal apoptosis induced by the endoplasmic reticulum calcium-ATPase inhibitor thapsigargin. Steroids 67, 1029-1040.
61. LIU, Y., HIMES, B.T., MURRAY, M., TESSLER, A., and FISCHER, I. (2002). Grafts of BDNF-producing fibroblasts rescue axotomized rubrospinal neurons and prevent their atrophy. Exp. Neurol. 178, 150-164.
62. LOVEJOY, J.C. (2003). The menopause and obesity. Primary Care 30, 317-325.
63. LU, P., YANG, H., JONES, L.L., FILBIN, M.T., and TUSZYNSKI, M.H. (2004). Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J. Neurosci. 24, 6402-6409.
64. LUNA, L. (1968). AFIP Mannual of Histological Staining Methods. McGraw Hill: New York.
65. LYETH, E.G., GONG, Q.Z., SHIELDS, S., MUIZELAAR, J.P., and BERMAN, R.F. (2001). Group I metabotropic glutamate antagonist reduces acute neuronal degeneration and behavioral deficits after traumatic brain injury in rats. Exp. Neurol. 169, 191-199.
66. MARCONDES, F.K., BIANCHI, F.J., and TANNO, A.P. (2002). Determination of the estrous cycle phases of rats: some helpful considerations. Braz. J. Biol. 62, 609-614.
67. MATTSON, M.P. (2003). Excitotoxic and excitoprotective mechanisms: abundant targets for the prevention and treatment of neurodegenerative disorders. Neuromol. Med. 3, 65-94.
68. MATTSON, M.P., and CHAN, S.L. (2003). Calcium orchestrates apoptosis. Nat. Cell Biol. 5, 1041-1043.
69. MCCULLOUGH, L.D., and HURN, P.D. (2003). Estrogen and ischemic neuroprotection: an integrated view. Trends Endocrinol. Metab. 14, 228-235.
70. MERCHENTHALER, I., DELLOVADE, T.L., and SHUGHRUE, P.J. (2003). Neuroprotection by estrogen in animal models of global and focal ischemia. Ann. N.Y. Acad. Sci. 1007, 89-100.
71. MIRANDA, P., WILLIAMS, C.L., and EINSTEIN, G. (1999). Granule cells in aging rats are sexually dimorphic in their response to estradiol. J. Neurosci. 19, 3316-3325.
72. MOOSMANN, B., and BEHL, C. (2002). Antioxidants as treatment for neurodegenerative disorders. Expert. Opin. Invest. Drugs 11, 1407-1435.
73. NEUMANN, S., BRADKE, F., TESSIER-LAVIGNE, M., and BASBAUM, A.I. (2002). Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34, 885-893.
74. NILSEN, J., and BRINTON, R.D. (2003). Mechanism of estrogen-mediated neuroprotection: regulation of mitrochondrial calcium and bcl-2 expression. Proc. Natl. Acad. Sci. USA 100, 2842-2847.
75. NILSEN, J., CHEN, S., and BRINTON, R.D. (2002). Dual action of estrogen on glutamate-induced calcium signaling: mechanisms requiring interaction between estrogen receptors and src/mitogen activated protein kinase pathway. Brain Res. 930, 216-234.
76. NOBLE, L.J., and WRATHALL, J.R. (1989). Correlative analyses of lesion development and functional status after graded spinal cord contusive injuries in the rat. Exp. Neurol. 103, 34-40.
77. NOBUNAGA, A.I., GO, B.K., and KARUNAS, R.B. (1999). Recent demographic and injury trends in people served by the Model Spinal Cord Injury Care Systems. Arch. Phys. Med. Rehabil. 80, 1372-1382.
78. NORDELL, V.L., SCARBOROUGH, M.M., BUCHANAN, A.K., and SOHRABJI, F. (2003). Differential effects of estrogen in the injured forebrain of young adult and reproductive senescent animals. Neurobiol. Aging 24, 733-743.
79. NOUT, Y.S., SCHMIDT, M.H., TOVAR, C.A., GULP, E., BEATTIE, M.S., and BRESNAHAN, J.C. (2005). Telemetric monitoring of corpus spongiosum penis pressure in conscious rats for assessment of micturition and sexual function following spinal cord contusion injury. J. Neurotrauma 22, 429-441.
80. OBERNIER, J.A., BOULDIN, T.W., and CREWS, F.T. (2002). Binge ethanol exposure in adult rats causes necrotic cell death. Alcohol Clin. Exp. Res. 26, 547-557.
81. PATIST, C.M., MULDER, M.B., GAUTIER, S.E., MAQUET, V., JEROME, R., and OUDEGA, M. (2004). Freeze-dried poly(D,L-lactic acid) macroporous guidance scaffolds impregnated with brain-derived neurotrophic factor in the transected adult rat thoracic spinal cord. Biomaterials 25, 1569-1582.
82. PICKETT, W., SIMPSON, K., WALKER, J., and BRISON, R.J. (2003). Traumatic spinal cord injury in Ontario, Canada. J. Trauma 55, 1070-1076.
83. 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.
84. 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.
85. POEHLMAN, E.T., TOTH, M.J., and GARDNER, A.W. (1995). Changes in energy balance and body composition at menopause: a controlled longitudinal study. Ann. Intern. Med. 123, 673-675.
86. PRICE, T.M., O'BRIEN, S.N., WELTER, B.H., GEORGE, R., ANADDJIWALA, J., and KILGORE, M. (1998). Estrogen regulation of adipose tissue lipoprotein lipase-possible mechanism of body fat distribution. Am. J. Obstet. Gynecol. 178, 101-107.
87. QIU, J., CAI, D., DAI, H., et al. (2002a). Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34, 895-903.
88. QIU, J., CAI, D., and FILBIN, M.T. (2002b). A role for cAMP in regeneration during development and after injury. Prog. Brain Res. 137, 381-387.
89. RAMIREZ, I., (1981). Estradiol-induced changes in lipoprotein lipase, eating, and body weight in rats. Am. J. Physiol. 240, E533-E538.
90. ROOF, R.L., and HALL, E.D. (2000). Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone. J. Neurotrauma 17, 367-388.
91. ROY, E.J., and WADE, G.N. (1977). Role of food intake in estradiol-induced body weight changes in female rats. Horm. Behav. 8, 265-274.
92. 2+ channels in smooth muscle cells. FASEB J. 12, 613-619.
93. SAAVEDRA, R.A., MURRAY, M., DE LACALLE, S., and TESSLER, A. (2000). In vivo neuroprotection of injured CNS neurons by a single injection of a DNA plasmid encoding the Bcl-2 gene. Prog. Brain Res. 128, 365-372.
94. SATO, M., CHANG, E., IGARASHI, T., and NOBLE, L.J. (2001). Neuronal injury and loss after traumatic brain injury: time course and regional variability. Brain Res. 917, 45-54.
95. SCHMUED, L.C., ALBERTSON, C., and SLIKKER, W., JR. (1997). Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 751, 37-46.
96. SCHMUED, L.C., and HOPKINS, K.J. (2000). Fluoro-Jade B: a high-affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 874, 123-130.
97. SEKHON, L.H., and FEHLINGS, M.G. (2001). Epidemiology, demographics, and pathophysiology of acute spinal cord injury. Spine 26, S2-S12.
98. SEKI, T., HIDA, K., TADA, M., KOYANAGI, I., and IWASAKI, Y. (2003). Role of the bcl-2 gene after contusive spinal cord injury in mice. Neurosurgery 53, 192-198.
99. SHIBATA, M., MURRAY, M., TESSLER, A., LJUBETIC, C., CONNORS, T., and SAAVEDRA, R.A. (2000). Single injections of a DNA plasmid that contains the human Bcl-2 gene prevent loss and atrophy of distinct neuronal populations after spinal cord injury in adult rats. Neurorehabil. Neural Repair 14, 319-330.
100. SINGER, C.A., ROGERS, K.L., and DORSA, D.M. (1998). Modulation of Bcl-2 expression: a potential component of estrogen protection in NT2 neurons. Neuroreport 9, 2565-2568.
101. SINGH, M., MEYER, E.M., MILLARD, W.J., and SIMPKINS, J.W. (1994). Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res. 644, 305-312.
102. SIPSKI, M.L., JACKSON, A.B., GOMEZ-MARIN, O., ESTORES, I., and STEIN, A. (2004). Effects of gender on neurologic and functional recovery after spinal cord injury. Arch. Phys. Med. Rehabil. 85, 1826-1836.
103. SMITH, M.S., FREEMAN, M.E., and NEILL, J.D. (1975). The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96, 219-226.
104. SOHRABJI, F., MIRANDA, R.C., and TORAN-ALLERAND, C.D. (1995). Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 92, 11110-11114.
105. SOUSTIEL, J. F., PALZUR, E., NEVO, O., THALER, I., and VLODAVSKY, E. (2005). Neuroprotective anti-apoptosis effect of estrogens in traumatic brain injury. J. Neurotrauma 22, 345-352.
106. 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.
107. STEIN, D.G., and HOFFMAN, S.W. (2003). Estrogen and progesterone as neuroprotective agents in the treatment of acute brain injuries. Pediatr. Rehabil. 6, 13-22.
108. i during metabolic inhibition. J. Mol. Cell Cardiol. 35, 331-336.
109. SUZUKI, T., BRAMLETT, H.M., RUENES, G., and DIETRICH, W.D. (2004). The effects of early post-traumatic hyperthermia in female and ovariectomized rats. J. Neurotrauma 21, 842-853.
110. SVENDSEN, O.L., HASSAGER, C., and CHRISTIANSEN, C. (1995). Age- and menopause-associated variations in body composition and fat distribution in healthy women as measured by dual-energy x-ray absorptiometry. Metabolism 44, 369-373.
111. TAKAHASHI, K., SCHWARZ, E., LJUBETIC, C., MURRAY, M., TESSLER, A., and SAAVEDRA, R.A. (1999). DNA plasmid that codes for human Bcl-2 gene preserves axotomized Clarke's nucleus neurons and reduces atrophy after spinal cord hemisection in adult rats. J. Comp. Neurol. 404, 159-171.
112. THOMPSON, C.B. (1995). Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456-1462.
113. TONG, W., IGARASHI, T., FERRIERO, D.M., and NOBLE, L.J. (2002). Traumatic brain injury in the immature mouse brain: characterization of regional vulnerability. Exp. Neurol. 176, 105-116.
114. VAGENAKIS, A.G. (1989). Endocrine aspects of menopause. Clin. Rheumatol. 8, Suppl 2, 48-51.
115. WAGNER, A.K., WILLARD, L.A., KLINE, A.E., et al. (2004). Evaluation of estrous cycle stage and gender on behavioral outcome after experimental traumatic brain injury. Brain Res. 998, 113-121.
116. WATTERS, J.J., CAMPBELL, J.S., CUNNINGHAM, M.J., KREBS, E.G., and DORSA, D.M. (1997). Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signaling cascade and c-fos immediate early gene transcription. Endocrinology 138, 4030-4033.
117. WATTERS, J.J., and DORSA, D.M. (1998). Transcriptional effects of estrogen on neuronal neurotensin gene expression involve cAMP/protein kinase A-dependent signaling mechanisms. J. Neurosci. 18, 6672-6680.
118. WEISSMAN, B.A., DALY, J.W., and SKOLNICK, P. (1975). Diethylstilbestrol- elicited accumulation of cyclic AMP in incubated rat hypothalamus. Endocrinology 97, 1559-1566.
119. WEST, M.J., SLOMIANKA, L., and GUNDERSON, H.J. (1991). Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Record 231, 482-497.
120. WISE, P.M. (2003). Impact of menopause on the brain. Alzheimer Dis. Assoc. Disord. 17, Suppl 2, S48-S50.
121. WISE, P.M., SMITH, M.J., DUBAL, D.B., WILSON, M.E., KRAJNAK, K.M., and ROSEWELL, K.L. (1999). Neuroendocrine influences and repercussions of the menopause. Endocrinol. Rev. 20, 243-248.
122. WISE, P.M., SMITH, M.J., DUBAL, D.B., et al. (2002). Neuroendocrine modulation and repercussions of female reproductive aging. Recent Prog. Horm. Res. 57, 235-256.
123. YEKUTIEL, M., BROOKS, M.E., OHRY, A., YAROM, J., and CAREL, R. (1989). The prevalence of hypertension, ischaemic heart disease and diabetes in traumatic spinal cord injured patients and amputees. Paraplegia 27, 58-62.
124. YOUNG, W. (1986). Ca paradox in neural injury: a hypothesis. Cent. Nerv. Syst. Trauma 3, 235-251.
125. YUNE, T.Y., KIM, S.J., LEE, S.M., et al. (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.
126. ZHANG, Z., and GUTH, L. (1997). Experimental spinal cord injury: Wallerian degeneration in the dorsal column is followed by revascularization, glial proliferation, and nerve regeneration. Exp. Neurol. 147, 159-171.
127. ZHANG, Z., KREBS, C.J., and GUTH, L. (1997). Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp. Neurol. 143, 141-152.
128. ZHAO, X., AHRAM, A., BERMAN, R.F., MUIZELAAR, J.P., and LYETH, B.G. (2003). Early loss of astrocytes after experimental traumatic brain injury. Glia 44, 140-152.
129. ZSOMBOK, A., TOTH, Z., and GALLYAS, F. (2005). Basophilia, acidophilia and argyrophilia of "dark" (compacted) neurons during their formation, recovery or death in an otherwise undamaged environment. J. Neurosci. Methods 142, 145-152.