Selective estrogen receptor modulators (SERMs) enhance neurogenesis and spine density following focal cerebral ischemia

Journal of Steroid Biochemistry and Molecular Biology

Volumn 146, Issue , 2015, Pages 38-47

  Khan, Mohammad M ^a   Wakade, Chandramohan ^b,c   De Sevilla, Liesl ^c   Brann, Darrell W ^c  

^a Zaiwa University   (Libyan Arab Jamahiriya)

^b AUGUSTA UNIVERSITY   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Cerebral cortex; Cerebral ischemia; Estrogen; Neurogenesis; Plasticity; Raloxifene; Tamoxifen

Indexed keywords

BROXURIDINE; DIAMINOBENZIDINE; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SPINOPHILIN; TAMOXIFEN; TRIPHENYLTETRAZOLIUM; ESTRADIOL; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BRAIN CORTEX; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENSITY; FEMALE; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; REVIEW; SPINE; STEREOLOGY; SUBVENTRICULAR ZONE; ANIMAL; CEREBRAL ARTERY DISEASE; DENDRITIC SPINE; DRUG EFFECTS; LATERAL BRAIN VENTRICLE; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

ANIMALS; BRAIN ISCHEMIA; DENDRITIC SPINES; ESTRADIOL; FEMALE; INFARCTION, MIDDLE CEREBRAL ARTERY; LATERAL VENTRICLES; NEUROGENESIS; NEUROPROTECTIVE AGENTS; RALOXIFENE HYDROCHLORIDE; RATS, SPRAGUE-DAWLEY; SELECTIVE ESTROGEN RECEPTOR MODULATORS; TAMOXIFEN;

EID: 84918515722     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2014.05.001     Document Type: Review

References (48)

1. O.N. Kokiko, A.K. Murashov, M.R. Hoane, Administration of raloxifene reduces sensorimotor and working memory deficits following traumatic brain injury, Behav. Brain Res. 170 (2006) 233-240.
2. M. Morissette, S. Al Sweidi, S. Callier, T. Di Paolo, Estrogen and SERM neuroprotection in animal models of Parkinson's disease, Mol. Cell. Endocrinol. 290 (2008) 60-69.
3. E. Biewenga, L. Cabell, T. Audesirk, Estradiol and raloxifene protect cultured SN4741 neurons against oxidative stress, Neurosci. Lett. 373 (2005) 179-183.
4. K. O'Neill, S. Chen, R.D. Brinton, Impact of the selective estrogen receptor modulator, raloxifene, on neuronal survival and outgrowth following toxic insults associated with aging and Alzheimer's disease, Exp. Neurol. 185 (2004) 63-80.
5. I. Ciriza, P. Carrero, I. Azcoitia, S.G. Lundeen, L.M. Garcia-Segura, Selective estrogen receptor modulators protect hippocampal neurons from kainic acid excitotoxicity: differences with the effect of estradiol, J. Neurobiol. 61 (2004) 209-221.
6. S. Callier, M. Morissette, M. Grandbois, D. Pelaprat, T. Di Paolo, Neuroprotective properties of 17beta-estradiol, progesterone, and raloxifene in MPTP C57Bl/6 mice, Synapse 41 (2001) 131-138.
7. E.S. Lee, Z. Yin, D. Milatovic, H. Jiang, M. Aschner, Estrogen and tamoxifen protect against Mn-induced toxicity in rat cortical primary cultures of neurons and astrocytes, Toxicol. Sci. 110 (2009) 156-167.
8. K. Sharma, R.D. Mehra, Long-term administration of estrogen or tamoxifen to ovariectomized rats affords neuroprotection to hippocampal neurons by modulating the expression of Bcl-2 and Bax, Brain Res. 1204 (2008) 1-15.
9. C. Wakade, M.M. Khan, L.M. De Sevilla, Q.G. Zhang, V.B. Mahesh, D.W. Brann, Tamoxifen neuroprotection in cerebral ischemia involves attenuation of kinase activation and super-oxide production and potentiation of mitochondrial superoxide dismutase, Endocrinology 149 (2008) 367-379.
10. Y. Zhang, Y. Jin, M.J. Behr, P.J. Feustel, J.P. Morrison, H.K. Kimelberg, Behavioral and histological neuroprotection by tamoxifen after reversible focal cerebral ischemia, Exp. Neurol. 196 (2005) 41-46.
11. M.A. Arevalo, M. Santos-Galindo, N. Lagunas, I. Azcoitia, L.M. Garcia-Segura, Selective estrogen receptor modulators as brain therapeutic agents, J. Mol. Endocrinol. 46 (2011) R1-R9.
12. D.A. Velazquez-Zamora, L.M. Garcia-Segura, I. Gonzalez-Burgos, Effects of selective estrogen receptor modulators on allocentric working memory performance and on dendritic spines in medial prefrontal cortex pyramidal neurons of ovariectomized rats, Horm. Behav. 61 (2012) 512-517.
13. I. Gonzalez-Burgos, M.C. Rivera-Cervantes, D.A. Velazquez-Zamora, A. Feria-Velasco, L.M. Garcia-Segura, Selective estrogen receptor modulators regulate dendritic spine plasticity in the hippocampus of male rats, Neural Plast. 2012 (2012) 309494.
14. E. Scott, Q.G. Zhang, R. Wang, R. Vadlamudi, D. Brann, Estrogen neuroprotection and the critical period hypothesis, Front. Neuroendocrinol. 33 (2012) 85-104.
15. D.W. Brann, K. Dhandapani, C. Wakade, V.B. Mahesh, M.M. Khan, Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications, Steroids 72 (2007) 381-405.
16. J.W. Simpkins, M. Singh, C. Brock, A.M. Etgen, Neuroprotection and estrogen receptors, Neuroendocrinology 96 (2012) 119-130.
17. D.B. Dubal, M.L. Kashon, L.C. Pettigrew, J.M. Ren, S.P. Finklestein, S.W. Rau, et al., Estradiol protects against ischemic injury, J. Cereb. Blood Flow Metab. 18 (1998) 1253-1258.
18. M.M. Khan, K.M. Dhandapani, Q.G. Zhang, D.W. Brann, Estrogen regulation of spine density and excitatory synapses in rat prefrontal and somatosensory cerebral cortex, Steroids 78 (2013) 614-623.
19. Y. Tang, W.G. Janssen, J. Hao, J.A. Roberts, H. McKay, B. Lasley, et al., Estrogen replacement increases spinophilin-immunoreactive spine number in the prefrontal cortex of female rhesus monkeys, Cereb. Cortex 14 (2004) 215-223.
20. D.D. Murphy, M. Segal, Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones, J. Neurosci. 16 (1996) 4059-4068.
21. C.M. Brown, S. Suzuki, K.A. Jelks, P.M. Wise, Estradiol is a potent protective, restorative, and trophic factor after brain injury, Semin. Reprod. Med. 27 (2009) 240-249.
22. J. Li, M. Siegel, M. Yuan, Z. Zeng, L. Finnucan, R. Persky, et al., Estrogen enhances neurogenesis and behavioral recovery after stroke, J. Cereb. Blood Flow Metab. 31 (2011) 413-425.
23. S. Suzuki, L.M. Gerhold, M. Bottner, S.W. Rau, C. Dela Cruz, E. Yang, et al., Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta, J. Comp. Neurol. 500 (2007) 1064-1075.
24. C.G. Gross, Neurogenesis in the adult brain: death of a dogma, Nat. Rev. Neurosci. 1 (2000) 67-73.
25. F.H. Gage, Neurogenesis in the adult brain, J. Neurosci. 22 (2002) 612-613.
26. A. Alvarez-Buylla, J.M. Garcia-Verdugo, Neurogenesis in adult subventricular zone, J. Neurosci. 22 (2002) 629-634.
27. A. Arvidsson, T. Collin, D. Kirik, Z. Kokaia, O. Lindvall, Neuronal replacement from endogenous precursors in the adult brain after stroke, Nat. Med. 8 (2002) 963-970.
28. K. Jin, Y. Sun, L. Xie, A. Peel, X.O. Mao, S. Batteur, et al., Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum, Mol. Cell. Neurosci. 24 (2003) 171-189.
29. G.E. Goings, V. Sahni, F.G. Szele, Migration patterns of subventricular zone cells in adult mice change after cerebral cortex injury, Brain Res. 996 (2004) 213-226.
30. T. Yamashita, M. Ninomiya, P. Hernandez Acosta, J.M. Garcia-Verdugo, T. Sunabori, M. Sakaguchi, et al., Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum, J. Neurosci. 26 (2006) 6627-6636.
31. S.A. Shumaker, C. Legault, S.R. Rapp, L. Thal, R.B. Wallace, J.K. Ockene, et al., Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial, JAMA 289 (2003) 2651-2662.
32. S. Wassertheil-Smoller, S.L. Hendrix, M. Limacher, G. Heiss, C. Kooperberg, A. Baird, et al., Effect of estrogen plus progestin on stroke in postmenopausal women: the Women's Health Initiative: a randomized trial, JAMA 289 (2003) 2673-2684.
33. S.R. Rapp, M.A. Espeland, S.A. Shumaker, V.W. Henderson, R.L. Brunner, J.E. Manson, et al., Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial, JAMA 289 (2003) 2663-2672.
34. Q.G. Zhang, D. Han, R.M. Wang, Y. Dong, F. Yang, R.K. Vadlamudi, et al., C terminus of Hsc70-interacting protein (CHIP)-mediated degradation of hippocampal estrogen receptor-alpha and the critical period hypothesis of estrogen neuroprotection, Proc. Natl. Acad. Sci. U.S.A. 108 (2011) E617-E624.
35. Q.G. Zhang, M.D. Laird, D. Han, K. Nguyen, E. Scott, Y. Dong, et al., Critical role of NADPH oxidase in neuronal oxidative damage and microglia activation following traumatic brain injury, PLoS One 7 (2012) e34504.
36. J.S. Jacobsen, C.C. Wu, J.M. Redwine, T.A. Comery, R. Arias, M. Bowlby, et al., Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease, Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 5161-5166.
37. H. van Praag, G. Kempermann, F.H. Gage, Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus, Nat. Neurosci. 2 (1999) 266-270.
38. J. Zheng, P. Zhang, X. Li, S. Lei, W. Li, X. He, et al., Post-stroke estradiol treatment enhances neurogenesis in the subventricular zone of rats after permanent focal cerebral ischemia, Neuroscience 231 (2013) 82-90.
39. M.K. Sun, J. Hongpaisan, T.J. Nelson, D.L. Alkon, Poststroke neuronal rescue and synaptogenesis mediated in vivo by protein kinase C in adult brains, Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 13620-13625.
40. Z.G. Zhang, M. Chopp, Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic, Lancet Neurol. 8 (2009) 491-500.
41. P.B. Allen, C.C. Ouimet, P. Greengard, Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines, Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 9956-9961.
42. C. Isgor, S.J. Watson, Estrogen receptor alpha and beta mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone, Neuroscience 134 (2005) 847-856.
43. S. Couillard-Despres, B. Winner, S. Schaubeck, R. Aigner, M. Vroemen, N. Weidner, et al., Doublecortin expression levels in adult brain reflect neurogenesis, Eur. J. Neurosci. 21 (2005) 1-14.
44. M.I. Rossberg, S.J. Murphy, R.J. Traystman, P.D.L. Hurn, Y353381.HCl, a selective estrogen receptor modulator, and experimental stroke, Stroke 31 (2000) 3041-3046.
45. L.I. Benowitz, S.T. Carmichael, Promoting axonal rewiring to improve outcome after stroke, Neurobiol. Dis. 37 (2010) 259-266.
46. C.E. Brown, C. Wong, T.H. Murphy, Rapid morphologic plasticity of peri-infarct dendritic spines after focal ischemic stroke, Stroke 39 (2008) 1286-1291.
47. R. Mostany, C. Portera-Cailliau, Absence of large-scale dendritic plasticity of layer 5 pyramidal neurons in peri-infarct cortex, J. Neurosci. 31 (2011) 1734-1738.
48. G. Sulkowski, L. Struzynska, A. Lenkiewicz, U. Rafalowska, Changes of cytoskeletal proteins in ischaemic brain under cardiac arrest and reperfusion conditions, Folia Neuropathol. 44 (2006) 133-139.