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

Volumn 67, Issue , 2013, Pages 78-87

  Atif, Fahim ^a   Yousuf, Seema ^a   Sayeed, Iqbal ^a   Ishrat, Tauheed ^a   Hua, Fang ^a   Stein, Donald G ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BDNF TrkB Erk1 2 signaling; Cerebral ischemia; Combination treatment; Progesterone; Vitamin D

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CASPASE 3; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROPROTECTIVE AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE; PROTEIN BCL 2; PROTEIN KINASE B; UNCLASSIFIED DRUG; VITAMIN D HORMONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN BLOOD FLOW; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MONOTHERAPY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; BRAIN ISCHEMIA; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; DRUG THERAPY, COMBINATION; MALE; MAP KINASE KINASE 2; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEUROPROTECTIVE AGENTS; PROGESTERONE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; SIGNAL TRANSDUCTION; STROKE; TREATMENT OUTCOME; VITAMIN D;

EID: 84873392984     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.10.004     Document Type: Article

References (43)

1. K. Abe, and T. Hayashi Expression of the glial cell line-derived neurotrophic factor gene in rat brain after transient MCA occlusion Brain Res. 776 1997 230 234
2. F. Atif, I. Sayeed, T. Ishrat, and D.G. Stein Progesterone with vitamin D affords better neuroprotection against excitotoxicity in cultured cortical neurons than progesterone alone Mol. Med. 15 2009 328 336
3. R. Balden, A. Selvamani, and F. Sohrabji Vitamin D deficiency exacerbates experimental stroke injury and dysregulates ischemia-induced inflammation in adult rats Endocrinology 153 2012 2420 2435
4. M. Cekic, S.M. Cutler, J.W. VanLandingham, and D.G. Stein Vitamin D deficiency reduces the benefits of progesterone treatment after brain injury in aged rats Neurobiol. Aging 32 2011 864 874
5. M. Cekic, I. Sayeed, and D.G. Stein Combination treatment with progesterone and vitamin D hormone may be more effective than monotherapy for nervous system injury and disease Front. Neuroendocrinol 30 2009 158 172
6. T. Coughlan, C. Gibson, and S. Murphy Progesterone, BDNF and neuroprotection in the injured CNS Int. J. Neurosci. 119 2009 1718 1740
7. J. Dang, B. Mitkari, M. Kipp, and R.C. Beye Gonadal steroids prevent cell damage and stimulate behavioral recovery after transient middle cerebral artery occlusion in male and female rats Brain Behav. Immun. 25 2011 715 726
8. S. Dore, K. Sampei, S. Goto, N.J. Alkayed, D. Guastella, S. Blackshaw, M. Gallagher, R.J. Traystman, P.D. Hurn, R.C. Koehler, and S.H. Snyder Heme oxygenase-2 is neuroprotective in cerebral ischemia Mol. Med. 5 1999 656 663
9. M. Endres, D. Biniszkiewicz, R.W. Sobol, C. Harms, M. Ahmadi, A. Lipski, J. Katchanov, P. Mergenthaler, U. Dirnagl, S.H. Wilson, A. Meisel, and R. Jaenisch Increased postischemic brain injury in mice deficient in uracil-DNA glycosylase J. Clin. Invest. 113 2004 1711 1721
10. C.L. Gibson, D. Constantin, M.J. Prior, P.M. Bath, and S.P. Murphy Progesterone suppresses the inflammatory response and nitric oxide synthase-2 expression following cerebral ischemia Exp. Neurol. 193 2005 522 530
11. C.L. Gibson, B. Coomber, and S.P. Murphy Progesterone is neuroprotective following cerebral ischaemia in reproductively ageing female mice Brain 134 2011 2125 2133
12. C.L. Gibson, and S.P. Murphy Progesterone enhances functional recovery after middle cerebral artery occlusion in male mice J. Cereb. Blood Flow Metab. 24 2004 805 813
13. M.E. Greenberg, B. Xu, B. Lu, and B.L. Hempstead New insights in the biology of BDNF synthesis and release: implications in CNS function J. Neurosci. 29 2009 12764 12767
14. F. Hua, J. Wang, T. Ishrat, W. Wei, F. Atif, I. Sayeed, and D.G. Stein Genomic profile of toll-like receptor pathways in traumatically brain-injured mice: effect of exogenous progesterone J. Neuroinflamm. 8 2011 42
15. T. Ishrat, I. Sayeed, F. Atif, and D.G. Stein Effects of progesterone administration on infarct volume and functional deficits following permanent focal cerebral ischemia in rats Brain Res. 1257 2009 94 101
16. P.K. Jodha, P. Kaur, W. Underwood, J.P. Lydon, and M. Singh The differences in neuroprotective efficacy of progesterone and medroxyprogesterone acetate correlate with their effects on brain-derived neurotrophic factor expression Endocrinology 150 2009 3162 3168
17. G. Kojima, C. Bell, R.D. Abbott, L. Launer, R. Chen, H. Motonaga, G.W. Ross, J.D. Curb, and K. Masaki Low dietary vitamin d predicts 34-year incident stroke: the honolulu heart program Stroke 43 2012 2163 2167
18. A. Liu, I. Margaill, S. Zhang, F. Labombarda, B. Coqueran, B. Delespierre, P. Liere, C. Marchand-Leroux, B.W. O'Malley, J.P. Lydon, A.F. De Nicola, R. Sitruk-Ware, C. Mattern, M. Plotkine, M. Schumacher, and R. Guennoun Progesterone receptors: a key for neuroprotection in experimental stroke Endocrinology 153 2012 3747 3757
19. L. Liu, L. Zhao, H. She, S. Chen, J.M. Wang, C. Wong, K. McClure, R. Sitruk-Ware, and R.D. Brinton Clinically relevant progestins regulate neurogenic and neuroprotective responses in vitro and in vivo Endocrinology 151 2010 5782 5794
20. E.Z. Longa, P.R. Weinstein, S. Carlson, and R. Cummins Reversible middle cerebral artery occlusion without craniectomy in rats Stroke 20 1989 84 91
21. E. Losem-Heinrichs, B. Gorg, C. Redecker, A. Schleicher, O.W. Witte, K. Zilles, and H.J. Bidmon 1alpha,25-dihydroxy-vitamin D3 in combination with 17beta-estradiol lowers the cortical expression of heat shock protein-27 following experimentally induced focal cortical ischemia in rats Arch. Biochem. Biophys. 439 2005 70 79
22. B. Lu BDNF and activity-dependent synaptic modulation Learn. Mem. 10 2003 86 98
23. M.D. Maines The heme oxygenase system: a regulator of second messenger gases Annu. Rev. Pharmacol. Toxicol. 37 1997 517 554
24. S.E. Makariou, P. Michel, M.S. Tzoufi, A. Challa, and H.J. Milionis Vitamin D and stroke: promise for prevention and better outcome Curr. Vasc. Pharmacol. 2012 Jun 22 (Epub ahead of print)
25. S. Margulies, and R. Hicks Combination therapies for traumatic brain injury: prospective considerations J. Neurotrauma. 26 2009 925 939
26. M.P. Mattson, S. Maudsley, and B. Martin BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders Trends Neurosci. 27 2004 589 594
27. M. Mizuno, K. Yamada, A. Olariu, H. Nawa, and T. Nabeshima Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats J. Neurosci. 20 2000 7116 7121
28. J. Nilsen, and R.D. Brinton Impact of progestins on estrogen-induced neuroprotection: synergy by progesterone and 19-norprogesterone and antagonism by medroxyprogesterone acetate Endocrinology 143 2002 205 212
29. J. Nilsen, and R.D. Brinton Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling Proc. Natl. Acad. Sci. U S A 100 2003 10506 10511
30. E. Oermann, H.J. Bidmon, O.W. Witte, and K. Zilles Effects of 1alpha,25 dihydroxyvitamin D3 on the expression of HO-1 and GFAP in glial cells of the photothrombotically lesioned cerebral cortex J. Chem. Neuroanat. 28 2004 225 238
31. S. Pilz, W. Marz, B. Wellnitz, U. Seelhorst, A. Fahrleitner-Pammer, H.P. Dimai, B.O. Boehm, and H. Dobnig Association of vitamin D deficiency with heart failure and sudden cardiac death in a large cross-sectional study of patients referred for coronary angiography J. Clin. Endocrinol. Metab. 93 2008 3927 3935
32. P.P. Roux, and J. Blenis ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions Microbiol. Mol. Biol. Rev. 68 2004 320 344
33. I. Sayeed, Q. Guo, S.W. Hoffman, and D.G. Stein Allopregnanolone, a progesterone metabolite, is more effective than progesterone in reducing cortical infarct volume after transient middle cerebral artery occlusion Ann. Emerg. Med. 47 2006 381 389
34. I. Sayeed, and D.G. Stein Progesterone as a neuroprotective factor in traumatic and ischemic brain injury Prog. Brain Res. 175 2009 219 237
35. I. Sayeed, B. Wali, and D.G. Stein Progesterone inhibits ischemic brain injury in a rat model of permanent middle cerebral artery occlusion Restor. Neurol. Neurosci. 25 2007 151 159
36. Q. Shi, P. Zhang, J. Zhang, X. Chen, H. Lu, Y. Tian, T.L. Parker, and Y. Liu Adenovirus-mediated brain-derived neurotrophic factor expression regulated by hypoxia response element protects brain from injury of transient middle cerebral artery occlusion in mice Neurosci. Lett. 465 2009 220 225
37. M.V. Sofroniew, C.L. Howe, and W.C. Mobley Nerve growth factor signaling, neuroprotection, and neural repair Annu. Rev. Neurosci. 24 2001 1217 1281
38. D.G. Stein Progesterone exerts neuroprotective effects after brain injury Brain Res. Rev. 57 2008 386 397
39. D.G. Stein Is progesterone a worthy candidate as a novel therapy for traumatic brain injury? Dialogues Clin. Neurosci. 13 2011 352 359
40. Q. Sun, A. Pan, F.B. Hu, J.E. Manson, and K.M. Rexrode 25-Hydroxyvitamin D levels and the risk of stroke: a prospective study and meta-analysis Stroke 43 2012 1470 1477
41. J. Wang, Y. Zhao, C. Liu, C. Jiang, C. Zhao, and Z. Zhu Progesterone inhibits inflammatory response pathways after permanent middle cerebral artery occlusion in rats Mol. Med. Rep. 4 2011 319 324
42. X.L. Yao, J. Liu, E. Lee, G.S. Ling, and J.T. McCabe Progesterone differentially regulates pro- and anti-apoptotic gene expression in cerebral cortex following traumatic brain injury in rats J. Neurotrauma. 22 2005 656 668
43. Y. Zeng, M. Tan, J. Kohyama, M. Sneddon, J.B. Watson, Y.E. Sun, and C.W. Xie Epigenetic enhancement of BDNF signaling rescues synaptic plasticity in aging J. Neurosci. 31 2011 17800 17810