A potential neuroprotective and synaptic plasticity mechanism induced by estradiol through PI3K/GSK3beta in cerebral ischaemia;Mecanismo potencial de neuroprotección y plasticidad sináptica inducidas por el estradiol a través de PI3K/GSK3beta en la isquemia cerebral

Revista de Neurologia

Volumn 46, Issue 1, 2008, Pages 32-39

  Barrera Ocampo, A A ^a   Cespedes Rubio A E ^a   Cardona Gómez, Gloria Patricia ^a  

^a UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

Adhesion proteins; Beta catenin; Cerebral ischaemia; GSK 3beta; Neuroactive steroids; Protective therapy

Indexed keywords

BETA CATENIN; ESTRADIOL; PHOSPHATIDYLINOSITOL 3 KINASE;

BRAIN ISCHEMIA; CELL SURVIVAL; NERVE CELL; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; REVIEW;

EID: 38549154986     PISSN: 02100010     EISSN: None     Source Type: Journal    
DOI: 10.33588/rn.4601.2007094     Document Type: Review

References (80)

1. Ehrenreich H, Siren AL. Neuroprotection -what does it mean? What means do we have? Eur Arch Psychiatry Clin Neurosci 2001; 251: 149-51.
2. Vajda FJ. Neuroprotection and neurodegenerative disease. J Clin Neurosci 2002; 9: 4-8.
3. Arango-Dávila C, Escobar-Betancourt M, Cardona-Gómez GP, Pimienta-Jiménez H. Fisiopatología de la isquemia cerebral focal: aspectos básicos y proyección a la clínica. Rev Neurol 2004; 39: 156-65.
4. Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 2003; 4: 399-415.
5. Mathers CD, Bernard C, Iburg KM, Inoue M, Shibuya K, Tomijima N, et al. Global burden of disease in 2002: data sources, methods and results. 54 ed. Geneva:World Health Organization; 2003.
6. Ministerio de Salud de la República de Colombia. Situación de salud en Colombia: indicadores básicos 2002. Bogotá: Ministerio de Salud; 2002.
7. Lipton P. Ischemic cell death in brain neurons. Physiol Rev 1999; 79: 1431-568.
8. Martin RL, Lloyd HG, Cowan AI. The early events of oxygen and glucose deprivation: setting the scene for neuronal death? Trends Neurosci 1994; 17: 251-7.
9. Siesjo BK. A new perspective on ischemic brain damage? Prog Brain Res 1993; 96: 1-9.
10. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 1999; 22: 391-7.
11. Barone FC, Feuerstein GZ. Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 1999; 19: 819-34.
12. Kristian T, Siesjo BK. Calcium in ischemic cell death. Stroke 1998; 29: 705-18.
13. Mergenthaler P, Dirnagl U, Meisel A. Pathophysiology of stroke: lessons from animal models. Metab Brain Dis 2004; 19: 151-67.
14. Monnerie H, Shashidhara S, Le Roux PD. Decreased dendrite growth from cultured mouse cortical neurons surviving excitotoxic activation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate/kainate receptors. Neurosci Lett 2003; 345: 182-6.
15. Weinstein PR, Hong S, Sharp FR. Molecular identification of the ischemic penumbra. Stroke 2004; 35: 2666-70.
16. Kalaria RN, Bhatti SU, Lust WD, Perry G. The amyloid precursor protein in ischemic brain injury and chronic hypoperfusion. Ann N Y Acad Sci 1993; 695: 190-3.
17. Whitehead SN, Hachinski VC, Cechetto DF. Interaction between a rat model of cerebral ischemia and beta-amyloid toxicity: inflammatory responses. Stroke 2005; 36: 107-12.
18. Wen Y, Yang S, Liu R, Brun-Zinkernagel AM, Koulen P, Simpkins JW. Transient cerebral ischemia induces aberrant neuronal cell cycle re-entry and Alzheimer's disease-like tauopathy in female rats. J Biol Chem 2004; 279: 22684-92.
19. Friedhoff P, Von Bergen M, Mandelkow EM, Mandelkow E. Structure of tau protein and assembly into paired helical filaments. Biochim Biophys Acta 2000; 1502: 122-32.
20. Morishima-Kawashima M, Ihara Y. Alzheimer's disease: beta-amyloid protein and tau. J Neurosci Res 2002; 70: 392-401.
21. Iqbal K, Alonso AC, El Akkad E, Gong CX, Haque N, Khatoon S, et al. Alzheimer neurofibrillary degeneration: therapeutic targets and high-throughput assays. J Mol Neurosci 2003; 20: 425-9.
22. Plassart-Schiess E, Baulieu EE. Neurosteroids: recent findings. Brain Res Brain Res Rev 2001; 37: 133-40.
23. Amantea D, Russo R, Bagetta G, Corasaniti MT. From clinical evidence to molecular mechanisms underlying neuroprotection afforded by estrogens. Pharmacol Res 2005; 52: 119-32.
24. Won CK, Ha SJ, Noh HS, Kang SS, Cho GJ, Choi WS, et al. Estradiol prevents the injury-induced decrease of Akt activation and Bad phosphorylation. Neurosci Lett 2005; 387: 115-9.
25. Puia G, Belelli D. Neurosteroids on our minds. Trends Pharmacol Sci 2001; 22: 266-7.
26. Hall JM, Couse JF, Korach KS. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 2001; 276: 36869-72.
27. Driggers PH, Segars JH. Estrogen action and cytoplasmic signaling pathways. Part II: the role of growth factors and phosphorylation in estrogen signaling. Trends Endocrinol Metab 2002; 13: 422-7.
28. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ, et al. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 1997; 51: 535-41.
29. Bucolo C, Drago F. Effects of neurosteroids on ischemia-reperfusion injury in the rat retina: role of sigma1 recognition sites. Eur J Pharmacol 2004; 498: 111-4.
30. Anderson MF, Aberg MA, Nilsson M, Eriksson PS. Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Brain Res Dev Brain Res 2002; 134: 115-22.
31. Bondy CA, Cheng CM. Signaling by insulin-like growth factor 1 in brain. Eur J Pharmacol 2004; 490: 25-31.
32. Frederick TJ, Wood TL. IGF-I and FGF-2 coordinately enhance cyclin D1 and cyclin E-cdk2 association and activity to promote G1 progression in oligodendrocyte progenitor cells. Mol Cell Neurosci 2004; 25: 480-92.
33. Russo VC, Kobayashi K, Najdovska S, Baker NL, Werther GA. Neuronal protection from glucose deprivation via modulation of glucose transport and inhibition of apoptosis: a role for the insulin-like growth factor system. Brain Res 2004; 1009: 40-53.
34. Clemmons DR, Maile LA. Minireview: integral membrane proteins that function coordinately with the insulin-like growth factor I receptor to regulate intracellular signaling. Endocrinology 2003; 144: 1664-70.
35. LeRoith D. Insulin-like growth factor I receptor signaling -overlapping or redundant pathways? Endocrinology 2000; 141: 1287-8.
36. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002; 296: 1655-7.
37. Brazil DP, Yang ZZ, Hemmings BA. Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 2004; 29: 233-42.
38. Hemmings BA. Akt signaling: linking membrane events to life and death decisions. Science 1997; 275: 628-30.
39. Frame S, Cohen P. GSK3 takes centre stage more than 20 years after its discovery. Biochem J 2001; 359: 1-16.
40. Yao HB, Shaw PC, Wong CC, Wan DC. Expression of glycogen synthase kinase-3 isoforms in mouse tissues and their transcription in the brain. J Chem Neuroanat 2002; 23: 291-7.
41. Kaytor MD, Orr HT. The GSK3 beta signaling cascade and neurodegenerative disease. Curr Opin Neurobiol 2002; 12: 275-8.
42. Dajani R, Fraser E, Roe SM, Young N, Good V, Dale TC, et al. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 2001; 105: 721-32.
43. Hetman M, Cavanaugh JE, Kimelman D, Xia Z. Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J Neurosci 2000; 20: 2567-74.
44. Lucas JJ, Hernández F, Gómez-Ramos P, Morán MA, Hen R, Ávila J. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J 2001; 20: 27-39.
45. Wen Y, Yang SH, Liu R, Pérez EJ, Brun-Zinkernagel AM, Koulen P, et al. Cdk5 is involved in NFT-like tauopathy induced by transient cerebral ischemia in female rats. Biochim Biophys Acta 2007; 1772: 473-83.
46. Cardona-Gómez GP, Arango-Dávila C, Gallego-Gómez JC, Barrera-Ocampo A, Pimienta H, García-Segura LM. Estrogen dissociates Tau and alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor subunit in postischemic hippocampus. Neuroreport 2006; 17: 1337-41.
47. Ferrer I, Barrachina M, Puig B. Glycogen synthase kinase-3 is associated with neuronal and glial hyperphosphorylated tau deposits in Alzheimer's disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Acta Neuropathol (Berl) 2002; 104: 583-91.
48. Takashima A, Murayama M, Murayama O, Kohno T, Honda T, Yasutake K, et al. Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc Natl Acad Sci U S A 1998; 95: 9637-41.
49. Murayama M, Tanaka S, Palacino J, Murayama O, Honda T, Sun X, et al. Direct association of presenilin-1 with beta-catenin. FEBS Lett 1998; 433: 73-7.
50. Moon RT, Bowerman B, Boutros M, Perrimon N. The promise and perils of Wnt signaling through beta-catenin. Science 2002; 296: 1644-6.
51. De Ferrari GV, Inestrosa NC. Wnt signaling function in Alzheimer's disease. Brain Res Brain Res Rev 2000; 33: 1-12.
52. Yu X, Malenka RC. Beta-catenin is critical for dendritic morphogenesis. Nat Neurosci 2003; 6: 1169-77.
53. Cardona-Gómez P, Pérez M, Ávila J, García-Segura LM, Wandosell F. Estradiol inhibits GSK3 and regulates interaction of estrogen receptors, GSK3, and beta-catenin in the hippocampus. Mol Cell Neurosci 2004; 25: 363-73.
54. Shimamura K, Takeichi M. Local and transient expression of E-cadherin involved in mouse embryonic brain morphogenesis. Development 1992; 116: 1011-9.
55. Nelson WJ, Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004; 303: 1483-7.
56. Lickert H, Bauer A, Kemler R, Stappert J. Casein kinase II phosphorylation of E-cadherin increases E-cadherin/beta-catenin interaction and strengthens cell-cell adhesion. J Biol Chem 2000; 275: 5090-5.
57. De Lacalle S. Estrogen effects on neuronal morphology. Endocrine 2006; 29: 185-90.
58. Carswell HV, Macrae IM, Gallagher L, Harrop E, Horsburgh KJ. Neuroprotection by a selective estrogen receptor beta agonist in a mouse model of global ischemia. Am J Physiol Heart Circ Physiol 2004; 287: H1501-4.
59. Cardona-Gómez GP, Trejo JL, Fernández AM, García-Segura LM. Estrogen receptors and insulin-like growth factor-I receptors mediate estrogen-dependent synaptic plasticity. Neuroreport 2000; 11: 1735-8.
60. García-Segura LM, Baetens D, Naftolin F. Synaptic remodelling in arcuate nucleus after injection of estradiol valerate in adult female rats. Brain Res 1986; 366: 131-6.
61. Horvath TL, García-Segura LM, Naftolin F. Lack of gonadotropin-positive feedback in the male rat is associated with lack of estrogen-induced synaptic plasticity in the arcuate nucleus. Neuroendocrinology 1997; 65: 136-40.
62. Parducz A, Pérez J, García-Segura LM. Estradiol induces plasticity of gabaergic synapses in the hypothalamus. Neuroscience 1993; 53: 395-401.
63. Frankfurt M, McEwen BS. Estrogen increases axodendritic synapses in the VMN of rats after ovariectomy. Neuroreport 1991; 2: 380-2.
64. Nishizuka M, Pfaff DW. Intrinsic synapses in the ventromedial nucleus of the hypothalamus: an ultrastructural study. J Comp Neurol 1989; 286: 260-8.
65. Gould E, Woolley CS, Frankfurt M, McEwen BS. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 1990; 10: 1286-91.
66. Woolley CS, McEwen BS. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 1992; 12: 2549-54.
67. Woolley CS, McEwen BS. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 1993; 336: 293-306.
68. Woolley CS, Wenzel HJ, Schwartzkroin PA. Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region of the adult female rat. J Comp Neurol 1996; 373: 108-17.
69. Xu X, Zhang Z. Effects of estradiol benzoate on learning-memory behavior and synaptic structure in ovariectomized mice. Life Sci 2006; 79: 1553-60.
70. Smith CC, McMahon LL. Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci 2006; 26: 8517-22.
71. Yokomaku D, Numakawa T, Numakawa Y, Suzuki S, Matsumoto T, Adachi N, et al. Estrogen enhances depolarization-induced glutamate release through activation of phosphatidylinositol 3-kinase and mitogen-activated protein kinase in cultured hippocampal neurons. Mol Endocrinol 2003; 17: 831-44.
72. Daoudal G, Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 2003; 10: 456-65.
73. Ozawa S, Kamiya H, Tsuzuki K. Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 1998; 54: 581-618.
74. Phillips SM, Sherwin BB. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology 1992; 17: 485-95.
75. Phillips SM, Sherwin BB. Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology 1992; 17: 497-506.
76. Good M, Day M, Muir JL. Cyclical changes in endogenous levels of oestrogen modulate the induction of LTD and LTP in the hippocampal CA1 region. Eur J Neurosci 1999; 11: 4476-80.
77. MacLusky NJ, Luine VN, Hajszan T, Leranth C. The 17alpha and 17beta isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 2005; 146: 287-93.
78. Rudick CN, Woolley CS. Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat. J Neurosci 2001; 21: 6532-43.
79. Brake WG, Alves SE, Dunlop JC, Lee SJ, Bulloch K, Allen PB, et al. Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 2001; 142: 1284-9.
80. Choi JM, Romeo RD, Brake WG, Bethea CL, Rosenwaks Z, McEwen BS. Estradiol increases pre- and post-synaptic proteins in the CA1 region of the hippocampus in female rhesus macaques (Macaca mulatta). Endocrinology 2003; 144: 4734-8.