Progesterone in experimental permanent stroke: A dose-response and therapeutic time-window study

Brain

Volumn 137, Issue 2, 2014, Pages 486-502

  Wali, Bushra ^a   Ishrat, Tauheed ^a   Won, Soonmi ^a   Stein, Donald G ^a   Sayeed, Iqbal ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

dose response; functional recovery; progesterone; stroke; therapeutic time window

Indexed keywords

NEUROPROTECTIVE AGENT; P 0130; PLACEBO; PROGESTERONE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFARCTION SIZE; COGNITION; CONTROLLED STUDY; DOSE RESPONSE; EXPERIMENTAL STROKE; FOREFOOT; FORELIMB; FUNCTIONAL ASSESSMENT; GAIT DISORDER; GRIP STRENGTH; LATENT PERIOD; LOCOMOTION; MALE; MEMORY; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NEUROPROTECTION; NONHUMAN; OPTIMAL DRUG DOSE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RAT; ROTAROD TEST; SENSORIMOTOR FUNCTION; SHAM PROCEDURE; SOMATOSENSORY DISORDER; SPATIAL MEMORY; STUDY DESIGN; THERAPY DELAY; TIME TO TREATMENT; TIME WINDOW STUDY;

DOSE RESPONSE; FUNCTIONAL RECOVERY; PROGESTERONE; STROKE; THERAPEUTIC TIME WINDOW;

ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HAND STRENGTH; MALE; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; PROGESTERONE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; STROKE; TIME FACTORS;

EID: 84893876378     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt319     Document Type: Article

References (73)

1. Alkayed NJ, Murphy SJ, Traystman RJ, Hurn PD, Miller VM. Neuroprotective effects of female gonadal steroids in reproductively senescent female rats. Stroke 2000; 31: 161-8
2. Asbury ET, Fritts ME, Horton JE, Isaac WL. Progesterone facilitates the acquisition of avoidance learning and protects against subcortical neuronal death following prefrontal cortex ablation in the rat. Behav Brain Res 1998; 97: 99-106
3. Atif F, Yousuf S, Sayeed I, Ishrat T, Hua F, Stein DG. Combination treatment with progesterone and vitamin D hormone is more effective than monotherapy in ischemic stroke: The role of BDNF/TrkB/Erk1/2 signaling in neuroprotection. Neuropharmacology 2013; 67: 78-87
4. Betz AL, Coester HC. Effect of steroids on edema and sodium uptake of the brain during focal ischemia in rats. Stroke 1990; 21: 1199-204
5. Bitran D, Dowd JA. Ovarian steroids modify the behavioral and neurochemical responses of the central benzodiazepine receptor. Psychopharmacology (Berl) 1996; 125: 65-73
6. Bitran D, Purdy RH, Kellogg CK. Anxiolytic effect of progesterone is associated with increases in cortical allopregnanolone and GABAA receptor function. Pharmacol Biochem Behav 1993; 45: 423-8
7. Bitran D, Shiekh M, McLeod M. Anxiolytic effect of progesterone is mediated by the neurosteroid allopregnanolone at brain GABAA receptors. J Neuroendocrinol 1995; 7: 171-7
8. Bixo M, Backstrom T. Regional distribution of progesterone and 5 alphapregnane-3,20-dione in rat brain during progesterone-induced anesthesia Psychoneuroendocrinology 1990; 15: 159-62
9. Cekic M, Cutler SM, VanLandingham JW, Stein DG. Vitamin D deficiency reduces the benefits of progesterone treatment after brain injury in aged rats. Neurobiol Aging 2011; 32: 864-74
10. Cekic M, Sayeed I, Stein DG. Combination treatment with progesterone and vitamin D hormone may be more effective than monotherapy for nervous system injury and disease. Front Neuroendocrinol 2009; 30: 158-72
11. Chen J, Chopp M, Li Y. Neuroprotective effects of progesterone after transient middle cerebral artery occlusion in rat. J Neurol Sci 1999; 171: 24-30
12. Cutler SM, Cekic M, Miller DM, Wali B, VanLandingham JW, Stein DG. Progesterone improves acute recovery after traumatic brain injury in the aged rat. J Neurotrauma 2007; 24: 1475-86
13. Delcker A, Diener HC, Timmann D, Faustmann P. The role of vertebral and internal carotid artery disease in the pathogenesis of vertebrobasilar transient ischemic attacks. Eur Arch Psychiatry Clin Neurosci 1993; 242: 179-83
14. Djebaili M, Hoffman SW, Stein DG. Allopregnanolone and progesterone decrease cell death and cognitive deficits after a contusion of the rat pre-frontal cortex. Neuroscience 2004; 123: 349-59
15. Durukan A, Tatlisumak T. Acute ischemic stroke: Overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia. Pharmacol Biochem Behav 2007; 87: 179-97
16. Encarnacion A, Horie N, Keren-Gill H, Bliss TM, Steinberg GK, Shamloo M. Long-Term behavioral assessment of function in an experimental model for ischemic stroke. J Neurosci Methods 2011; 196: 247-57
17. Fisher M. Recommendations for advancing development of acute stroke therapies: Stroke Therapy Academic Industry Roundtable 3. Stroke 2003; 34: 1539-46
18. Fisher M, Albers GW, Donnan GA, Furlan AJ, Grotta JC, Kidwell CS, et al. Enhancing the development and approval of acute stroke therapies: Stroke Therapy Academic Industry roundtable. Stroke 2005; 36: 1808-13
19. Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA, Savitz SI, et al. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009; 40: 2244-50
20. Gibson CL, Constantin D, Prior MJ, Bath PM, Murphy SP. Progesterone suppresses the inflammatory response and nitric oxide synthase-2 expression following cerebral ischemia. Exp Neurol 2005; 193: 522-30
21. Gibson CL, Coomber B, Murphy SP. Progesterone is neuroprotective following cerebral ischaemia in reproductively ageing female mice. Brain 2011; 134 (Pt 7): 2125-33
22. Gibson CL, Gray LJ, Bath PM, Murphy SP. Progesterone for the treatment of experimental brain injury; a systematic review. Brain 2008; 131 (Pt 2): 318-28
23. Gibson CL, Murphy SP. Progesterone enhances functional recovery after middle cerebral artery occlusion in male mice. J Cereb Blood Flow Metab 2004; 24: 805-13
24. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, et al. Heart disease and stroke statistics-2013 update: A report from the American Heart Association. Circulation 2013; 127: E6-e245
25. Goss CW, Hoffman SW, Stein DG. Behavioral effects and anatomic correlates after brain injury: A progesterone dose-response study. Pharmacol Biochem Behav 2003; 76: 231-42
26. Guo Q, Sayeed I, Baronne LM, Hoffman SW, Guennoun R, Stein DG. Progesterone administration modulates AQP4 expression and edema after traumatic brain injury in male rats. Exp Neurol 2006; 198: 469-78
27. Hacke W, Schwab S, Horn M, Spranger M, De Georgia M, von Kummer R. ?Malignant? middle cerebral artery territory infarction: Clinical course and prognostic signs. Arch Neurol 1996; 53: 309-15
28. Hankey GJ. Stroke: How large a public health problem, and how can the neurologist help? Arch Neurol 1999; 56: 748-54
29. Hetze S, Romer C, Teufelhart C, Meisel A, Engel O. Gait analysis as a method for assessing neurological outcome in a mouse model of stroke. J Neurosci Methods 2012; 206: 7-14
30. Hua F, Reiss JI, Tang H, Wang J, Fowler X, Sayeed I, et al. Progesterone and low-dose vitamin D hormone treatment enhances sparing of memory following traumatic brain injury. Horm Behav 2012; 61: 642-51
31. Hua F, Wang J, Ishrat T, Wei W, Atif F, Sayeed I, et al. Genomic profile of Toll-like receptor pathways in traumatically brain-injured mice: Effect of exogenous progesterone. J Neuroinflammation 2011; 8: 42
32. Ishrat T, Sayeed I, Atif F, Hua F, Stein DG. Progesterone and allopregnanolone attenuate blood-brain barrier dysfunction following permanent focal ischemia by regulating the expression of matrix metalloproteinases. Exp Neurol 2010; 226: 183-90
33. Ishrat T, Sayeed I, Atif F, Hua F, Stein DG. Progesterone is neuroprotective against ischemic brain injury through its effects on the phosphoinositide 3-kinase/protein kinase B signaling pathway. Neuroscience 2012; 210: 442-50
34. Ishrat T, Sayeed I, Atif F, Stein DG. Effects of progesterone administration on infarct volume and functional deficits following permanent focal cerebral ischemia in rats. Brain Res 2009; 1257: 94-101
35. Jiang N, Chopp M, Stein D, Feit H. Progesterone is neuroprotective after transient middle cerebral artery occlusion in male rats. Brain Res 1996; 735: 101-7
36. Kissela BM, Khoury JC, Alwell K, Moomaw CJ, Woo D, Adeoye O, et al. Age at stroke: Temporal trends in stroke incidence in a large, biracial population. Neurology 2012; 79: 1781-7
37. Kitagawa H, Hayashi T, Mitsumoto Y, Koga N, Itoyama Y, Abe K. Reduction of ischemic brain injury by topical application of glial cell line-derived neurotrophic factor after permanent middle cerebral artery occlusion in rats. Stroke 1998; 29: 1417-22
38. Kumon Y, Kim SC, Tompkins P, Stevens A, Sakaki S, Loftus CM. Neuroprotective effect of postischemic administration of progesterone in spontaneously hypertensive rats with focal cerebral ischemia. J Neurosurg 2000; 92: 848-52
39. Labombarda F, Gonzalez S, Lima A, Roig P, Guennoun R, Schumacher M, et al. Progesterone attenuates astro-And microgliosis and enhances oligodendrocyte differentiation following spinal cord injury. Exp Neurology 2011; 231: 135-46
40. Liu A, Margaill I, Zhang S, Labombarda F, Coqueran B, Delespierre B, et al. Progesterone receptors: A key for neuroprotection in experimental stroke. Endocrinology 2012; 153: 3747-57
41. Lubjuhn J, Gastens A, von Wilpert G, Bargiotas P, Herrmann O, Murikinati S, et al. Functional testing in a mouse stroke model induced by occlusion of the distal middle cerebral artery. J Neurosci Methods 2009; 184: 95-103
42. Muntner P, DeSalvo KB, Wildman RP, Raggi P, He J, Whelton PK. Trends in the prevalence, awareness, treatment, and control of cardiovascular disease risk factors among noninstitutionalized patients with a history of myocardial infarction and stroke. Am J Epidemiol 2006; 163: 913-20
43. Murphy SJ, Littleton-Kearney MT, Hurn PD. Progesterone administration during reperfusion, but not preischemia alone, reduces injury in ovariectomized rats. J Cereb Blood Flow Metab 2002; 22: 1181-8
44. Murray CJ, Lopez AD. Mortality by cause for eight regions of the world: Global Burden of Disease Study. Lancet 1997; 349: 1269-76
45. Parkkinen S, Ortega FJ, Kuptsova K, Huttunen J, Tarkka I, Jolkkonen J. Gait impairment in a rat model of focal cerebral ischemia. Stroke Res Treat 2013; 2013: 410972
46. Pettus EH, Wright DW, Stein DG, Hoffman SW. Progesterone treatment inhibits the inflammatory agents that accompany traumatic brain injury. Brain Res 2005; 1049: 112-9
47. Reddy DS, Kulkarni SK. Differential anxiolytic effects of neurosteroids in the mirrored chamber behavior test in mice. Brain Res 1997; 752: 61-71
48. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, et al. Heart disease and stroke statistics-2012 update: A report from the American Heart Association. Circulation 2012; 125: E2-e220
49. Roof RL, Duvdevani R, Braswell L, Stein DG. Progesterone facilitates cognitive recovery and reduces secondary neuronal loss caused by cortical contusion injury in male rats. Exp Neurol 1994; 129: 64-9
50. Roof RL, Stein DG. Gender differences in Morris water maze performance depend on task parameters. Physiol Behav 1999; 68: 81-6
51. Savitz SI, Chopp M, Deans R, Carmichael ST, Phinney D, Wechsler L. Stem Cell Therapy as an Emerging Paradigm for Stroke (STEPS) II. Stroke 2011; 42: 825-9
52. Sayeed I, Guo Q, Hoffman SW, Stein DG. Allopregnanolone, a progesterone metabolite, is more effective than progesterone in reducing cortical infarct volume after transient middle cerebral artery occlusion. Ann Emerg Med 2006; 47: 381-9
53. Sayeed I, Stein DG. progesterone as a neuroprotective factor in traumatic and ischemic brain injury. In: Verhaagen J, Hol EM, Huitinga I, Wijnholds W, Bergen AB, Boer GJ, et al. editors. Neurotherapy. New York: Elsevier; 2009. p. 219-37
54. Sayeed I, Wali B, Stein DG. Progesterone inhibits ischemic brain injury in a rat model of permanent middle cerebral artery occlusion. Restor Neurol Neurosci 2007; 25: 151-9
55. Schumacher M, Guennoun R, Stein DG, De Nicola AF. Progesterone: Therapeutic opportunities for neuroprotection and myelin repair. Pharmacol Ther 2007; 116: 77-106
56. Shear DA, Galani R, Hoffman SW, Stein DG. Progesterone protects against necrotic damage and behavioral abnormalities caused by traumatic brain injury. Exp Neurol 2002; 178: 59-67
57. Stein DG. A clinical/translational perspective: Can a developmental hormone play a role in the treatment of traumatic brain injury? Horm Behav 2013; 63: 291-300
58. Stein DG, Wright DW, Kellermann AL. Does progesterone have neuroprotective propertieš Ann Emerg Med 2008; 51: 164-72
59. Tamura A, Graham DI, McCulloch J, Teasdale GM. Focal cerebral ischaemia in the rat: 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cereb Blood Flow Metab 1981; 1: 53-60
60. Thomas AJ, Nockels RP, Pan HQ, Shaffrey CI, Chopp M. Progesterone is neuroprotective after acute experimental spinal cord trauma in rats. Spine 1999; 24: 2134-8
61. VanLandingham JW, Cekic M, Cutler S, Hoffman SW, Stein DG. Neurosteroids reduce inflammation after TBI through CD55 induction. Neurosci Lett 2007; 425: 94-8
62. VanLandingham JW, Cekic M, Cutler SM, Hoffman SW, Washington ER, Johnson SJ, et al. Progesterone and its metabolite allopregnanolone differentially regulate hemostatic proteins after traumatic brain injury. J Cereb Blood Flow Metab 2008; 28: 1786-94
63. Vanlandingham JW, Cutler SM, Virmani S, Hoffman SW, Covey DF, Krishnan K, et al. The enantiomer of progesterone acts as a molecular neuroprotectant after traumatic brain injury. Neuropharmacology 2006; 51: 1078-85
64. Wali B, Sayeed I, Stein DG. Improved behavioral outcomes after progesterone administration in aged male rats with traumatic brain injury. Restor Neurol Neurosci 2011; 29: 61-71
65. Wang J, Jiang C, Liu C, Li X, Chen N, Hao Y. Neuroprotective effects of progesterone following stroke in aged rats. Behav Brain Res 2010; 209: 119-22
66. Wang Y, Bontempi B, Hong SM, Mehta K, Weinstein PR, Abrams GM, et al. A comprehensive analysis of gait impairment after experimental stroke and the therapeutic effect of environmental enrichment in rats. J Cereb Blood Flow Metab 2008; 28: 1936-50
67. Won S, Wali B, Sayeed I, Stein DG. Progesterone prevents hemorrhagic transformation after tPAa treatment in experimental stroke. International Stroke Conference: February 2013; Honolulu, HI. Stroke 2013; 44: ATMP33
68. Wong R, Renton C, Gibson CL, Murphy SJ, Kendall DA, Bath PM. Progesterone treatment for experimental stroke: An individual animal meta-Analysis. J Cereb Blood Flow Metab 2013a; 33: 1362-72
69. Wong R, Bath PM, Kendall D, Gibson CL. Progesterone and cerebral ischaemia: The relevance of ageing. J Neuroendocrinol 2013b, in press
70. Wright DW, Kellermann AL, Hertzberg VS, Clark PL, Frankel M, Goldstein FC, et al. ProTECT: A randomized clinical trial of progesterone for acute traumatic brain injury. Ann Emerg Med 2007; 49: 391-402
71. Xiao G, Wei J, Yan W, Wang W, Lu Z. Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: A randomized controlled trial. Crit Care 2008; 12: R61
72. Yamamoto M, Tamura A, Kirino T, Shimizu M, Sano K. Behavioral changes after focal cerebral ischemia by left middle cerebral artery occlusion in rats. Brain Res 1988; 452: 323-8
73. Yousuf S, Atif F, Sayeed I, Wang J, Stein DG. Post-stroke infections exacerbate ischemic brain injury in middle-Aged rats: Immunomodulation neuroprotection by progesterone. Neuroscience 2013; 239: 92-102