Progesterone is neuroprotective after transient middle cerebral artery occlusion in male rats

Brain Research

Volumn 735, Issue 1, 1996, Pages 101-107

  Jiang, Ning ^a   Chopp, Michael ^a,b   Stein, Donald ^c   Feit, Howard ^a  

^a Henry Ford Health Science Center   (United States)

^b OAKLAND UNIVERSITY   (United States)

^c EMORY UNIVERSITY   (United States)

Author keywords

Cerebral ischemia; Neuronal damage; Progesterone; Rat

Indexed keywords

NEUROPROTECTIVE AGENT; PROGESTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN ISCHEMIA; CONTROLLED STUDY; HISTOLOGY; INTRAPERITONEAL DRUG ADMINISTRATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0030607198     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/0006-8993(96)00605-1     Document Type: Article

References (70)

1. [1] Backstorm, T., Zetterlund, B., Blom, S. and Romano, M., Effects of intravenous progesterone infusions on the epileptic discharge frequency in women with partial epilepsy, Acta Neurol. Scand., 69 (1984) 240-248.
2. [2] Barnes, A., Hajibeidl, A., Trent, A. and Matson, A., Expression of steroid metabolizing enzymes by aggregating fetal brain cells in culture: A model for developmental regulation of the progesterone 5α-reductase pathway, Endocrinology, 127 (1990) 500-504.
3. [3] Bederson, J.B., Pitts, L.H., Germano, S.M., Nishmura, M.C., Davis, R.L. and Martkowski, H.M., Evaluation of 2,3,5-triphenytetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats, Stroke, 17 (1986) 1304-1308.
4. [4] Betz, A.L. and Coester, H.C., Effect of steroid on edema and sodium uptake of the brain during focal ischemia in rats, Stroke, 21 (1990) 1199-1204.
5. [5] Betz, A.L., Ennis, S.R. and Schielke, G.P., Blood-brain barrier sodium transport limits development of brain edema during partial ischemia in gerbils, Stroke, 20 (1989) 1253-1259.
6. [6] Betz, A.L., Iannotti, F. and Hoff, J.T., Brain edema: A classification based on blood-brain barrier integrity, Cerebrovasc. Brain Metab. Rev., 1 (1989) 133-154.
7. A receptor, Brain Res., 561 (1991) 157-161.
8. [8] Bixo, M. and Backstorm, T., Regional distribution of progesterone and 5α-pregnane-3,20-dione in rat brain during progesterone-induced 'anesthesia', Pychoneuroendocrinology, 15 (1990) 159-162.
9. [9] Bullock, R., Graham, D.I., Chen, M.H., Lowe, D. and McCulloch, J., Focal cerebral ischemia in the cat: pretreatment with a competitive NMDA receptor antagonist D-CCPene, J. Cereb. Blood Flow Metab., 10 (1990) 668-674.
10. [10] Bureau, M. and Olsen, R.W., Multiple distinct subunits of the γ-aminobutyric acid-A receptor protein show different ligand binding affinities, Mol. Pharmacol., 37 (1990) 497-502.
11. [11] Chaplin, E.R., Free, R.G. and Goldstein, G.W., Inhibition by steroid of the uptake of potassium by capillaries isolated from rat brain, Biochem. Pharmacol., 30 (1981) 241-245.
12. [12] Chen, H., Chopp, M., Zhang, Z.G. and Garcia, J.H., The effect of hypothermia on transient cerebral artery occlusion in the rat, J. Cereb. Blood Flow Metab., 12 (1992) 621-628.
13. [13] Chen, M., Bullock, R., Graham, D.I., Frey, P., Lowe, D. and McCulloch, J., Evaluation of a competitive NMDA antagonist (D-CCPene) in feline focal cerebral ischemia, Ann. Neurol., 30 (1991) 62-70.
14. [14] Del Maestro, R., Thaw, H.H., Bjork, J., Planker, M. and Arfors, K.E., Free radicals as mediators of tissue injury, Acta Physiol. Scand. Suppl., 492 (1980) 43-57.
15. [15] Dezsi, L., Greenberg, J.H., Sladky, J., Araki, N., Hamar, J. and Reivich, M., Prolonged effects of MK-801 in the cat during focal cerebral ischemia and recovery: survival, EEG activity and histopathology, J. Neurol. Sci., 121 (1994) 110-120.
16. [16] Gee, K.W., Steroid modulation of the GABA/benzodiazepine receptor-linked chloride ionophore, Mol. Neurobiol., 2 (1988) 291-317.
17. [17] George, C.P., Goldberg, M.P., Choi, D.W. and Steinberg, G.K., Dextromethorphan reduces neocortical ischemic neuronal damage in vivo, Brain Res., 440 (1988) 375-379.
18. [18] Gisvold, S.E. and Steen, P.A., Drug therapy in brain ischemia, Br. J. Anaesth., 57 (1985) 96-109.
19. [19] Green, A.R. and Cross, A.J., The neuroprotective actions of chlormethiazole, Prog. Neurobiol., 44 (1994) 463-484.
20. [20] Hanukoglu, I., Karavolas, H.J. and Goy, R.W., Progesterone metabolism in the pineal, brain stem, thalamus and corpus callosum of the female rat, Brain Res., 125 (1977) 313-324.
21. [21] Harrison, N.L., Majewska, M.D., Harrington, J.W. and Barker, J.L., Structure-activity relationships for steroid interaction with a γ-aminobutyric acid A receptor complex, J. Pharmacol. Exp. Ther., 241 (1987) 346-353.
22. [22] Harrison, N.L. and Simmonds, M.A., Modulation of the GABA receptor complex by a steroid anaesthetic, Brain Res., 323 (1984) 287-292.
23. [23] Karavolas, H.J., Bertics, P.J., Hodges, D.R. and Rudie, N., Progesterone processing by neuroendocrine structures. In F. Celotti, F. Naftolin and L. Martini (Eds.), Metabolism of Hormonal Steroids in Neuroendocrine Structures, Vol. 13, Serono Symposia Publications from Raven Press, New York, 1984, pp. 149-170.
24. 3H]5α-dihydro-progesterone by rat brain and pituitary and effects of estradiol and time: Tissue concentration of progesterone itself or specific metabolites? Endocrinology, 104(1979) 1418-1425.
25. [25] Koenig, H.L., Schumacher, M., Ferzaz, B., Do Thi, A.N., Ressouches, A., Rachida, G., Jung-Testas, I., Robel, P., Akwa, Y. and Baulieu, E.E., Progesterone synthesis and myelin formation by Schwann Cell, Science, 268 (1995) 1500-1504.
26. [26] Koizumi, J., Yoshida, Y., Nakazawa, T. and Oneda, G., Experimental studies of ischemic brain edema. 1. A new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area, Jpn. J. Stroke, 8 (1986) 1-8.
27. [27] Kokate, T.G., Svensson, B.E. and Rogawski, M.A., Anticonvulsant activity of neurosteroid: correlation with gamma-aminobutyric acid-evoked chloride current potentiation, J. Pharmacol. Exp. Ther., 270 (1994) 1223-1229.
28. A receptor complex: Electrophysiological studies. In D. Chadwick and K. Widdows (Eds.), Steroids and Neuronal Activity, Wiley, Chichester, 1990, pp. 56-71.
29. [29] Landgren, S.O.E., Pregnenolone (3α-hydroxy-5α-pregnane-20-one), a progesterone metabolite facilitates inhibition of synaptic transmission in the Schaffer collateral pathway of the guinea pig hippocampus in vitro, Epilepsy Res., 10 (1991) 156-165.
30. [30] Landgren, S., Aasly, J., Backstorm, T., Dubrovsky, B. and Danielsson, E., The effect of progesterone and its metabolites on interictal epileptiform discharge in the cat's cerebral cortex, Acta Physiol. Scand., 131 (1987) 33-42.
31. [31] Le Goascogne, C., Robel, P., Gouezou, M., Sananes, N., Baulieu, E.E. and Waterman, M., Neurosteroids: Cytochrome P-450scc in rat brain, Science, 237 (1987) 1212-1215.
32. [32] Litter, B.C, Matta, R.J. and Zahn, T.P., Physiological and psychological effects of progesterone in men, J. Nerv. Ment. Dis., 159 (1974) 256-267.
33. [33] Luntz-Leybman, V., Freund, R.K. and Collins, A.C., 5α-Pregnan-3α-ol-20-one blocks nicotine-induced seizures and enhances paired-pulse inhibition, Eur. J. Pharmacol., 185 (1990) 239-242.
34. [34] MacDonald, P.C., Dombrosky, R.A. and Casey, M.L., Recurrent secretion of progesterone in large amounts: An endocrine/metabolic disorder unique to young women? Endocr. Rev., 12 (1991) 372-401.
35. [35] MacLusky, N.J. and McEwen, B.S., Oestrogen modulates progestin receptor concentrations in some rat brain regions but not in others, Nature, 274 (1978) 276-278.
36. [36] Majewska, M.D., Harrison, N.L., Schwartz, R.D., Barker, J.L. and Paul, S.M., Steroid hormone metabolites are barbiturate-like modulators of GABA receptor, Science, 232 (1986) 1004-1007.
37. [37] Miller, L.P. and Hsu, C., Therapeutic potential for adenosine receptor activation in ischemic brain injury, J. Neurotrauma, 9 (1992) S563-577.
38. [38] Mok, W.M. and Krieger, N.R., Evidence that 5α-pregnan-3α-ol-20-one is the metabolite responsible for progesterone anesthesia, Brain Res., 533 (1990) 42-45.
39. [39] Ogata, T., Nakamura, Y., Tsuji, K., Shibata, T. and Kataoka, K., Steroid hormones protect spinal cord neurons from glutamate toxicity, Neuroscience, 55 (1993) 445-449.
40. [40] Olsen, R.W., Discussion. In: D. Chadwick and K. Widdows (Eds.), Steroids and Neuronal Activity, Wiley, Chichester, 1990, pp. 72, 103-104, 221.
41. [41] Olson, J.J., Poor, M.M. and Beck, D.W., Methylprednisolone reduces the bulk flow of water across an in vitro blood-brain barrier, Brain Res., 439 (1988) 259-265.
42. [42] Park, C.K., McCulloch, J., Kang, J.K. and Choi, C.R., Pretreatment with a competitive NMDA antagonist D-CPPene attenuates focal cerebral infarction and brain swelling in awake rats, Acta Neurochir., 127 (1994) 220-226.
43. [43] Park, C.K., Nehls, D.G., Graham, D.I., Teasdale, G.M. and MacCulloch, J., The glutamate antagonist MK-801 reduces focal ischemic brain damage in the rat, Ann. Neurol., 24 (1988) 543-551.
44. [44] Paul, S.M. and Purdy, R.H., Neuroactive steroids, FASEB J., 6 (1992) 2311-2322.
45. [45] Pepe, G.J. and Rothchild, I., Metabolic clearance rate of progesterone: Comparison between ovariectomized, pregnant, pseudopregnant and deciduoma-bearing pseudopregnant rats, Endocrinology, 93 (1973) 1200-1205.
46. [46] Persson, L., Valtysson, I., Andine, P., Hagberg, H. and Hillered, L., Neuropathologic end points in experimental stroke therapy (MK-801): the importance of both early and late evaluation, Soc. Neurosci. Abstr., 1452 (1992).
47. [47] Pfaff, D.W. and McEwen, B.S., Actions of estrogens and progestins on nerve cells, Science, 219 (1983) 808-814.
48. [48] Phillis, J.W., Bender, A.S. and Marszalec, W., Estradiol and progesterone potentiate adenosine's depressant action on rat cerebral cortical neurons, Gen. Pharmacol., 16 (1985) 609-612.
49. [49] Powell, H., Morgan, M. and Sear, J.W., Pregnanolone: a new steroid intravenous anaesthetic. Dose-finding study, Anaesthesia, 47 (1992) 287-290.
50. A receptors, Neuron, 4 (1990) 759-765.
51. [51] Purdy, R.H., Moore, P.H. Jr., Rao, P.N., Hagino, M., Yamaguchi, T., Schmidt, P., Rubinow, D.R., Morrow, A.L. and Paul, S.M., Radioimmunoassay of 3α-hydroxy-5α-pregnane-20-one in rat and human plasma, Steroids, 55 (1990) 290-296.
52. [52] Purdy, R.H., Morrow, A.L., Blinn, J.R. and Paul, S.M., Synthesis, metabolism, and pharmacological activity of 3α-hydroxy steroids which potentiate GABA-receptor-mediated chloride ion uptake in rat cerebral cortical synaptoneurosomes, J. Med. Chem., 33 (1990) 1572-1581.
53. [53] Raisingham, K.H., Dorfman, R.I.L., Forchielli, E., Gyermak, L. and Genther, G., Uptake of intravenously administered progesterone, pregnanedione and pregnenolone by the rat brain. Acta Endocrinol., 51 (1968) 395-404.
54. [54] Robel, P. and Baulieu, E.E., Neurosteroids: 3β-hydroxy-delta 5-derivatives in the rodent brain, Neurochem Int., 7 (1985) 953-958.
55. [55] Robel, P. and Baulieu, E.E., Neurosteroids: Biosynthesis and function, Trends Endocrinol. Metab., 5 (1994) 1-8.
56. [56] Robel, P., Bourreau, E., Corpechot, C., Dangt, D.C., Halberg, F., Clarke, C., Haug, M., Schlegel, M.L., Synguelakis, M., Vourch, C. and Baulieu, E.E., Neurosteroids: 3β-hydroxy-delta 5-derivatives in rat and monkey brain, J. Steroid Biochem., 27 (1987) 649-655.
57. [57] Robel, P., Young, J., Corpechot, C., Mayo, W., Perche, F., Haug, M., Simon, H. and Baulieu, E.E., Biosynthesis and assay of neurosteroids in rats and mice: Functional correlates, J. Steroid Biochem. Mol. Biol., 53 (1995) 355-360.
58. [58] Rodolphi, K.A., Schubert, P., Parkinson, F.E. and Fredholm, B.B., Neuroprotective role of adenosine in cerebral ischemia. Trends Pharmacol. Sci., 13 (1992) 439-445.
59. [59] Roof, R.L., Duvdevani, R., Braswell, L. and Stein, D.G., Progesterone treatment attenuated brain edema following contusion injury in male and female rats, Restor. Neurol. Neurosci., 4 (1992) 425-427.
60. [60] Roof, R.L., Duvdevani, R., Braswell, L. and Stein, D.G., Progesterone facilitates cognitive recovery and reduces secondary neuronal loss caused by cortical contusion injury in male rat, Exp. Neurol., 129 (1994) 64-69.
61. [61] Roof, R.L., Duvdevani, R. and Stein, D.G., Gender influences outcome of brain injury: progesterone plays a protective role, Brain Res., 607 (1993) 333-336.
62. A receptor complex, Neuropharmacology, 23 (1984) 877-878.
63. [63] Simon, R. and Shiraishi, K., N-Methyl-D-aspartate antagonist reduces stroke size and regional glucose metabolism, Ann. Neurol., 27 (1990) 606-611.
64. [64] Smith, S.S., Progesterone administration attenuates excitatory amino acid responses of cerebellar Purkinje cells, Neuroscience, 42 (1991) 309-320.
65. [65] Smith, S.S., Female sex steroid hormones: from receptors to networks to performance-actions on the sensorimotor system, Prog. Neurobiol., 44 (1994) 55-88.
66. [66] Smith, S.S., Waterhouse, B.D. and Woodward, D.J., Locally applied progesterone metabolites alter neuronal responsiveness to iontophoretically applied glutamate in the cerebellum, Brain Res. Bull., 18 (1987) 739-747.
67. [67] Steinberg, G.K., George, C.P., DeLaPaz, R.D., Shibata, D.K. and Gross, T., Dextromethorphan protects against cerebral injury following transient focal ischemia in rabbits, Stroke, 19 (1988) 1112-1118.
68. [68] Swanson, R.A., Morton, M.T., Tsao-Wu, G., Davidson, C. and Sharp, F.R., A semiautomated method for measuring brain infarct volume, J. Cereb. Blood Flow Metab., 10 (1990) 290-293.
69. [69] Wilson, M.A., Influences of gender, gonadectomy and estrous cycle on GABA/BZ receptors and benzodiazepine responses in rats, Brain Res. Bull, 29 (1992) 165-172.
70. [70] Zea Longa, Z., Weinstein, P.R., Carlson, S. and Cummins, R., Reversible middle cerebral artery occlusion without craniectomy in rats, Stroke, 20 (1989) 84-91.