Neuroprotection by progesterone after transient cerebral ischemia in stroke-prone spontaneously hypertensive rats

Hormones and Behavior

Volumn 84, Issue , 2016, Pages 29-40

  Yousuf, Seema ^a   Atif, Fahim ^a   Sayeed, Iqbal ^a   Wang, Jun ^a   Stein, Donald G ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Functional recovery; Neuroprotection; Progesterone; Stroke prone spontaneously hypertensive rats (SHRSP); Transient cerebral ischemia

Indexed keywords

INTERLEUKIN 1BETA; PROGESTERONE; SUPEROXIDE; VASCULOTROPIN; NEUROPROTECTIVE AGENT; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; ASTROCYTE; BODY WEIGHT; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; GRIP STRENGTH; HYPERTENSION; MACROPHAGE; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SENSORY DYSFUNCTION; STROKE PRONE SPONTANEOUSLY HYPERTENSIVE RAT; SYSTOLIC BLOOD PRESSURE; WISTAR KYOTO RAT; ANIMAL; BLOOD PRESSURE; CEREBRAL ARTERY DISEASE; CEREBROVASCULAR ACCIDENT; DRUG EFFECTS; METABOLISM; PATHOLOGY; SPONTANEOUSLY HYPERTENSIVE RAT; TRANSIENT ISCHEMIC ATTACK;

ANIMALS; APOPTOSIS; BLOOD PRESSURE; INFARCTION, MIDDLE CEREBRAL ARTERY; ISCHEMIC ATTACK, TRANSIENT; MALE; MICROGLIA; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PROGESTERONE; RATS; RATS, INBRED SHR; RATS, INBRED WKY; STROKE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84973319912     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2016.06.002     Document Type: Article

References (68)

1. Aronowski J., Samways E., Strong R., Rhoades H.M., Grotta J.C. An alternative method for the quantitation of neuronal damage after experimental middle cerebral artery occlusion in rats: analysis of behavioral deficit. J. Cereb. Blood Flow Metab. 1996, 16:705-713.
2. Ashafaq M., Raza S.S., Khan M.M., Ahmad A., Javed H., Ahmad M.E., Tabassum R., Islam F., Siddiqui M.S., Safhi M.M. Catechin hydrate ameliorates redox imbalance and limits inflammatory response in focal cerebral ischemia. Neurochem. Res. 2012, 37:1747-1760.
3. Atif F., Yousuf S., Sayeed I., Ishrat T., Hua F., Stein D.G. 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. Borlongan C.V., Hida H., Nishino H. Early assessment of motor dysfunctions aids in successful occlusion of the middle cerebral artery. Neuroreport 1998, 9:3615-3621.
5. Boutin H., LeFeuvre R.A., Horai R., Asano M., Iwakura Y., Rothwell N.J. Role of IL-1alpha and IL-1beta in ischemic brain damage. J. Neurosci. 2001, 21:5528-5534.
6. Carswell H.V., Anderson N.H., Clark J.S., Graham D., Jeffs B., Dominiczak A.F., Macrae I.M. Genetic and gender influences on sensitivity to focal cerebral ischemia in the stroke-prone spontaneously hypertensive rat. Hypertension 1999, 33:681-685.
7. Centers for Disease Control Prevention. Prevalence of stroke-United States, 2006-2010. MMWR 2012, 61:379082.
8. Ceulemans A.G., Zgavc T., Kooijman R., Hachimi-Idrissi S., Sarre S., Michotte Y. The dual role of the neuroinflammatory response after ischemic stroke: modulatory effects of hypothermia. J. Neuroinflamm. 2010, 7:74.
9. Chiba T., Itoh T., Tabuchi M., Nakazawa T., Satou T. Interleukin-1beta accelerates the onset of stroke in stroke-prone spontaneously hypertensive rats. Mediat. Inflamm. 2012, 2012:701976.
10. Danton G.H., Dietrich W.D. Inflammatory mechanisms after ischemia and stroke. J. Neuropathol. Exp. Neurol. 2003, 62:127-136.
11. DeVries A.C., Nelson R.J., Traystman R.J., Hurn P.D. Cognitive and behavioral assessment in experimental stroke research: will it prove useful?. Neurosci. Biobehav. Rev. 2001, 25:325-342.
12. Dheen S.T., Kaur C., Ling E.A. Microglial activation and its implications in the brain diseases. Curr. Med. Chem. 2007, 14:1189-1197.
13. Dinarello C.A., Simon A., van der Meer J.W. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat. Rev. Drug Discov 2012, 11:633-652.
14. Dziennis S., Akiyoshi K., Subramanian S., Offner H., Hurn P.D. Role of dihydrotestosterone in post-stroke peripheral immunosuppression after cerebral ischemia. Brain Behav. Immun. 2011, 25:685-695.
15. Emsley H.C., Smith C.J., Gavin C.M., Georgiou R.F., Vail A., Barberan E.M., Illingworth K., Scarth S., Wickramasinghe V., Hoadley M.E., Rothwell N.J., Tyrrell P.J., Hopkins S.J. Clinical outcome following acute ischaemic stroke relates to both activation and autoregulatory inhibition of cytokine production. BMC Neurol. 2007, 7:5.
16. Farhat M.Y., Lavigne M.C., Ramwell P.W. The vascular protective effects of estrogen. FASEB J. 1996, 10:615-624.
17. Fisher M., Feuerstein G., Howells D.W., Hurn P.D., Kent T.A., Savitz S.I., Lo E.H. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009, 40:2244-2250.
18. Gibson C.L., Constantin D., Prior M.J., Bath P.M., Murphy S.P. Progesterone suppresses the inflammatory response and nitric oxide synthase-2 expression following cerebral ischemia. Exp. Neurol. 2005, 193:522-530.
19. Grossman K.J., Goss C.W., Stein D.G. Effects of progesterone on the inflammatory response to brain injury in the rat. Brain Res. 2004, 1008:29-39.
20. Howard R.B., Sayeed I., Stein D. Suboptimal dosing parameters as possible factors in the negative phase III clinical trials of progesterone in TBI. J. Neurotrauma 2015, E pub 2015/09/16. 10.1089/neu.2015.4179.
21. Howard V.J., Tanner R.M., Anderson A., Irvin M.R., Calhoun D.A., Lackland D.T., Oparil S., Muntner P. Apparent treatment-resistant hypertension among individuals with history of stroke or transient ischemic attack. Am. J. Med. 2015, 128(707-714).
22. Iadecola C., Davisson R.L. Hypertension and cerebrovascular dysfunction. Cell Metab. 2008, 7:476-484.
23. Ishrat T., Sayeed I., Atif F., Hua F., Stein D.G. Progesterone and allopregnanolone attenuate blood-brain barrier dysfunction following permanent focal ischemia by regulating the expression of matrix metalloproteinases. Exp. Neurol. 2010, 226:183-190.
24. Ishrat T., Sayeed I., Atif F., Hua F., Stein D.G. Progesterone is neuroprotective against ischemic brain injury through its effects on the phosphoinositide 3-kinase/protein kinase B signaling pathway. Neuroscience 2012, 210:442-450.
25. Jickling G.C., Manolescu B.N. Breaking down barriers to identify hemorrhagic transformation in ischemic stroke. Neurology 2012, 79:1632-1633.
26. Jin R., Yang G., Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J. Leukoc. Biol. 2010, 87:779-789.
27. Kannan K., Jain S.K. Oxidative stress and apoptosis. Pathophysiology: ISP 2000, 7:153-163.
28. Kuboyama K., Harada H., Tozaki-Saitoh H., Tsuda M., Ushijima K., Inoue K. Astrocytic P2Y(1) receptor is involved in the regulation of cytokine/chemokine transcription and cerebral damage in a rat model of cerebral ischemia. J. Cereb. Blood Flow Metab. 2011, 31:1930-1941.
29. Lakhan S.E., Kirchgessner A., Hofer M. Inflammatory mechanisms in ischemic stroke: therapeutic approaches. J. Transl. Med. 2009, 7:97.
30. Lankhorst S., Saleh L., Danser A.J., van den Meiracker A.H. Etiology of angiogenesis inhibition-related hypertension. Curr. Opin. Pharmacol. 2015, 21:7-13.
31. Li Z., Wang B., Kan Z., Zhang B., Yang Z., Chen J., Wang D., Wei H., Zhang J.N., Jiang R. Progesterone increases circulating endothelial progenitor cells and induces neural regeneration after traumatic brain injury in aged rats. J. Neurotrauma 2012, 29:343-353.
32. Liu J., Wang Y., Akamatsu Y., Lee C.C., Stetler R.A., Lawton M.T., Yang G.Y. Vascular remodeling after ischemic stroke: mechanisms and therapeutic potentials. Prog. Neurobiol. 2014, 115:138-156.
33. Longa E.Z., Weinstein P.R., Carlson S., Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989, 20:84-91.
34. Margaritescu O., Pirici D., Margaritescu C. VEGF expression in human brain tissue after acute ischemic stroke. Romanian J. Morphol. Embryol. 2011, 52:1283-1292.
35. Minshall R.D., Pavcnik D., Browne D.L., Hermsmeyer K. Nongenomic vasodilator action of progesterone on primate coronary arteries. J. Appl. Physiol. (1985) 2002, 92:701-708.
36. Muradian K., Schachtschabel D.O. The role of apoptosis in aging and age-related disease: update. Z. Gerontol. Geriatr. 2001, 34:441-446.
37. Murray K.N., Parry-Jones A.R., Allan S.M. Interleukin-1 and acute brain injury. Front. Cell. Neurosci. 2015, 9:18.
38. Offner H., Subramanian S., Parker S.M., Wang C., Afentoulis M.E., Lewis A., Vandenbark A.A., Hurn P.D. Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. J. Immunol. 2006, 176:6523-6531.
39. Okamoto K., Yamori Y., Nagaoka A. Establishment of the stroke-prone spontaneously hypertensive rat (SHR). Circ. Res. 1974, 34:I-143-I-153.
40. Peeling J., Corbett D., Del Bigio M.R., Hudzik T.J., Campbell T.M., Palmer G.C. Rat middle cerebral artery occlusion: correlations between histopathology, T2-weighted magnetic resonance imaging, and behavioral indices. J. Stroke Cerebrovasc. Dis. 2001, 10:166-177.
41. Perusquia M., Hernandez R., Morales M.A., Campos M.G., Villalon C.M. Role of endothelium in the vasodilating effect of progestins and androgens on the rat thoracic aorta. Gen. Pharmacol. 1996, 27:181-185.
42. Ramirez-Rosas M.B., Cobos-Puc L.E., Sanchez-Lopez A., Gutierrez-Lara E.J., Centurion D. Pharmacological characterization of the mechanisms involved in the vasorelaxation induced by progesterone and 17beta-estradiol on isolated canine basilar and internal carotid arteries. Steroids 2014, 89:33-40.
43. Remus E.W., Sayeed I., Won S., Lyle A.N., Stein D.G. Progesterone protects endothelial cells after cerebrovascular occlusion by decreasing MCP-1- and CXCL1-mediated macrophage infiltration. Exp. Neurol. 2015, 271:401-408.
44. Sayeed I., Stein D.G. Progesterone as a neuroprotective factor in traumatic and ischemic brain injury. Prog. Brain Res. 2009, 175:219-237.
45. Sharp F.R., Jickling G.C. Modeling immunity and inflammation in stroke: differences between rodents and humans?. Stroke 2014, 45:e179-e180.
46. Simoncini T., Mannella P., Fornari L., Caruso A., Varone G., Genazzani A.R. In vitro effects of progesterone and progestins on vascular cells. Steroids 2003, 68:831-836.
47. Skolnick, B.E., Maas, A.I., Narayan, R.K., van der Hoop, R.G., MacAllister, T., Ward, J.D., Nelson, N.R., Stocchetti, N., the, S.T.I., 2014. A clinical trial of progesterone for severe traumatic brain injury. N. Engl. J. Med. 371, 2467-2476.
48. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
49. Stein D.G. Is progesterone a worthy candidate as a novel therapy for traumatic brain injury?. Dialogues Clin. Neurosci. 2011, 13:352-359.
50. Stein D.G. Embracing failure: what the phase III progesterone studies can teach about TBI clinical trials. Brain Inj. 2015, 29:1259-1272.
51. Stroke Therapy Academic Industry Roundtable, S. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 1999, 30:2752-2758.
52. Sun D., Jakobs T.C. Structural remodeling of astrocytes in the injured CNS. Neuroscientist 2012, 18:567-588.
53. Tagami M., Ikeda K., Yamagata K., Nara Y., Fujino H., Kubota A., Numano F., Yamori Y. Vitamin E prevents apoptosis in hippocampal neurons caused by cerebral ischemia and reperfusion in stroke-prone spontaneously hypertensive rats. Lab. Investig. 1999, 79:609-615.
54. Taraborrelli S. Physiology, production and action of progesterone. Acta Obstet. Gynecol. Scand. 2015, 94(Suppl. 161):8-16.
55. Touyz R.M. Reactive oxygen species and angiotensin II signaling in vascular cells - implications in cardiovascular disease. Braz. J. Med. Biol. Res. 2004, 37:1263-1273.
56. Tsivgoulis G., Katsanos A.H., Alexandrov A.V. Reperfusion therapies of acute ischemic stroke: potentials and failures. Front. Neurol. 2014, 5:215.
57. Wahl F., Allix M., Plotkine M., Boulu R.G. Neurological and behavioral outcomes of focal cerebral ischemia in rats. Stroke 1992, 23:267-272.
58. Wali B., Ishrat T., Won S., Stein D.G., Sayeed I. Progesterone in experimental permanent stroke: a dose-response and therapeutic time-window study. Brain 2014, 137:486-502.
59. Wallace A.E., Kline A.E., Montanez S., Hernandez T.D. Impact of the novel anti-convulsant vigabatrin on functional recovery following brain lesion. Rest. Neurol Neurosci. 1999, 14:35-45.
60. Wang M.M., Klaus J.A., Joh H.D., Traystman R.J., Hurn P.D. Postischemic angiogenic factor expression in stroke-prone rats. Exp. Neurol. 2002, 173:283-288.
61. Wong R., Renton C., Gibson C.L., Murphy S.J., Kendall D.A., Bath P.M., Progesterone Pre-Clinical Stroke Pooling Project, C. Progesterone treatment for experimental stroke: an individual animal meta-analysis. J. Cereb. Blood Flow Metab. 2013, 33:1362-1372.
62. Wright D.W., Yeatts S.D., Silbergleit R., Palesch Y.Y., Hertzberg V.S., Frankel M., Goldstein F.C., Caveney A.F., Howlett-Smith H., Bengelink E.M., Manley G.T., Merck L.H., Janis L.S., Barsan W.G., Investigators N.E.T.T. Very early administration of progesterone for acute traumatic brain injury. N. Engl. J. Med. 2014, 371:2457-2466.
63. Yamagata K. Pathological alterations of astrocytes in stroke-prone spontaneously hypertensive rats under ischemic conditions. Neurochem. Int. 2012, 60:91-98.
64. Yamagata K., Kitazawa T., Shinoda M., Tagawa C., Chino M., Matsufuji H. Stroke status evoked adhesion molecule genetic alterations in astrocytes isolated from stroke-prone spontaneously hypertensive rats and the apigenin inhibition of their expression. Stroke Res. Treat. 2010, Epub 2009 Dec 20. 10.4061/2010/386389.
65. Yousuf S., Atif F., Sayeed I., Tang H., Stein D.G. Progesterone in transient ischemic stroke: a dose-response study. Psychopharmacology 2014, 231:3313-3323.
66. Yousuf S., Atif F., Sayeed I., Wang J., Stein D.G. Post-stroke infections exacerbate ischemic brain injury in middle-aged rats: immunomodulation and neuroprotection by progesterone. Neuroscience 2013, 239:92-102.
67. Yousuf S., Sayeed I., Atif F., Tang H., Wang J., Stein D.G. Delayed progesterone treatment reduces brain infarction and improves functional outcomes after ischemic stroke: a time-window study in middle-aged rats. J. Cereb. Blood Flow Metab. 2014, 34:297-306.
68. Zhang X.H., Lei H., Liu A.J., Zou Y.X., Shen F.M., Su D.F. Increased oxidative stress is responsible for severer cerebral infarction in stroke-prone spontaneously hypertensive rats. CNS Neurosci. Ther. 2011, 17:590-598.