17β-estradiol increases astrocytic vascular endothelial growth factor (VEGF) in adult female rat hippocampus

Endocrinology

Volumn 152, Issue 5, 2011, Pages 1745-1751

  Barouk, Sharon ^a   Hintz, Tana ^a   Li, Ping ^a   Duffy, Aine M ^a   Maclusky, Neil J ^b   Scharfman, Helen E ^a,c  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b UNIVERSITY OF GUELPH   (Canada)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; VASCULOTROPIN;

ANTIBODY LABELING; ARTICLE; ASTROCYTE; CONFOCAL MICROSCOPY; ESTRUS CYCLE; EX VIVO STUDY; GLIA CELL; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MOUSE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; RAT; TISSUE SECTION;

ANIMALS; ASTROCYTES; ESTRADIOL; ESTROGENS; ESTROUS CYCLE; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NEUROGLIA; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 79955399440     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-1290     Document Type: Article

References (67)

1. Ribatti D 2005 The crucial role of vascular permeability factor/vascular endothelial growth factor in angiogenesis: a historical review. Br J Haematol 128:303-309 (Pubitemid 40216151)
2. Breen EC 2007 VEGF in biological control. J Cell Biochem 102:1358-1367 (Pubitemid 350223939)
3. Cullinan-Bove K, Koos RD 1993 Vascular endothelial growth factor/vascular permeability factor expression in the rat uterus: rapid stimulation by estrogen correlates with estrogen-induced increases in uterine capillary permeability and growth. Endocrinology 133:829-837 (Pubitemid 23238899)
4. Ferrara N, Chen H, Davis-Smyth T, Gerber HP, Nguyen TN, Peers D, Chisholm V, Hillan KJ, Schwall RH 1998 Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat Med 4:336-340 (Pubitemid 28144094)
5. Mueller MD, Vigne JL, Minchenko A, Lebovic DI, Leitman DC, Taylor RN 2000 Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors α and β. Proc Natl Acad Sci USA 97:10972-10977
6. Hoehn BD, Harik SI, Hudetz AG 2002 VEGF mRNA expressed in microvessels of neonatal and adult rat cerebral cortex. Mol Brain Res 101:103-108 (Pubitemid 34465566)
7. Rajah TT, Grammas P 2002 VEGF and VEGF receptor levels in retinal and brain-derived endothelial cells. Biochem Biophys Res Commun 293:710-713 (Pubitemid 34687245)
8. Wang Y, Kilic E, Kilic U, Weber B, Bassetti CL, Marti HH, Hermann DM 2005 VEGF overexpression induces post-ischaemic neuroprotection, but facilitates haemodynamic steal phenomena. Brain 128:52-63 (Pubitemid 40070520)
9. Alonso G, Galibert E, Duvoid-Guillou A, Vincent A 2005 Hyperosmotic stimulus induces reversible angiogenesis within the hypothalamic magnocellular nuclei of the adult rat: a potential role for neuronal vascular endothelial growth factor. BMC Neurosci 6:20
10. Jin KL, Mao XO, Nagayama T, Goldsmith PC, Greenberg DA 2000 Induction of vascular endothelial growth factor and hypoxia-inducible factor-1α by global ischemia in rat brain. Neuroscience 99:577-585 (Pubitemid 30612460)
11. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ 2004 VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36:827-835 (Pubitemid 39014099)
12. During MJ, Cao L 2006 VEGF a mediator of the effect of experience on hippocampal neurogenesis. Curr Alzheimer Res 3:29-33
13. Sköld MK, von Gertten C, Sandberg-Nordqvist AC, Mathiesen T, Holmin S 2005 VEGF and VEGF receptor expression after experimental brain contusion in rat. J Neurotrauma 22:353-367 (Pubitemid 40434684)
14. Newton SS, Collier EF, Hunsberger J, Adams D, Terwilliger R, Selvanayagam E, Duman RS 2003 Gene profile of electroconvulsive seizures: Induction of neurotrophic and angiogenic factors. J Neurosci 23:10841-10851 (Pubitemid 37499691)
15. Nicoletti JN, Shah SK, McCloskey DP, Goodman JH, Elkady A, Atassi H, Hylton D, Rudge JS, Scharfman HE, Croll SD 2008 Vascular endothelial growth factor is up-regulated after status epilepticus and protects against seizure-induced neuronal loss in hippocampus. Neuroscience 151:232-241
16. Tanapat P, Hastings NB, Reeves AJ, Gould E 1999 Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792-5801 (Pubitemid 29327916)
17. Zhang JM, Konkle AT, Zup SL, McCarthy MM 2008 Impact of sex and hormones on new cells in the developing rat hippocampus: A novel source of sex dimorphism? Eur J Neurosci 27:791-800 (Pubitemid 351365183)
18. Dalla C, Papachristos EB, Whetstone AS, Shors TJ 2009 Female rats learn trace memories better than male rats and consequently retain a greater proportion of new neurons in their hippocampi. Proc Natl Acad Sci USA 106:2927-2932
19. Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ, Palmer TD 2003 VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18:2803-2812 (Pubitemid 37542133)
20. Warner-Schmidt JL, Duman RS 2007 VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc Natl Acad Sci USA 104:4647-4652 (Pubitemid 47186279)
21. Veliskova J, Velisek L, Galanopoulou AS, Sperber EF 2000 Neuroprotective effects of estrogens on hippocampal cells in adult female rats after status epilepticus. Epilepsia 41 (Suppl 6): S30-S35
22. Ledoux VA, Smejkalova T, May RM, Cooke BM, Woolley CS 2009 Estradiol facilitates the release of neuropeptide y to suppress hippocampus-dependent seizures. J Neurosci 29:1457-1468
23. Bake S, Ma L, Sohrabji F 2008 Estrogen receptor-α overexpression suppresses 17β-estradiol-mediated vascular endothelial growth factor expression and activation of survival kinases. Endocrinology 149:3881-3889
24. Brinton RD 2008 Estrogen regulation of glucose metabolism and mitochondrial function: Therapeutic implications for prevention of Alzheimer's disease. Adv Drug Deliv Rev 60:1504-1511
25. Brinton RD 2008 The healthy cell bias of estrogen action: Mitochondrial bioenergetics and neurological implications. Trends Neurosci 31:529-537
26. Croll SD, Goodman JH, Scharfman HE 2004 Vascular endothelial growth factor (VEGF) in seizures: a double-edged sword. Adv Exp Med Biol 548:57-68 (Pubitemid 38979613)
27. Lee C, Agoston DV 2009 Inhibition of VEGF receptor 2 increased cell death of dentate hilar neurons after traumatic brain injury. Exp Neurol 220:400-403
28. Scharfman HE, Hintz TM, Gomez J, Stormes KA, Barouk S, Malthankar-Phatak GH, McCloskey DP, Luine VN, Maclusky NJ 2007 Changes in hippocampal function of ovariectomized rats after sequential low doses of estradiol to simulate the preovulatory estrogen surge. Eur J Neurosci 26:2595-2612 (Pubitemid 350050429)
29. Scharfman HE, Mercurio TC, Goodman JH, Wilson MA, MacLusky NJ 2003 Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor. J Neurosci 23:11641-11652 (Pubitemid 38021291)
30. Scharfman HE, Sollas AL, Smith KL, Jackson MB, Goodman JH 2002 Structural and functional asymmetry in the normal and epileptic rat dentate gyrus. J Comp Neurol 454:424-439 (Pubitemid 35416801)
31. Paxinos G, Watson C 1986 The rat brain in stereotaxic coordinates. New York: Academic Press
32. Freeman ME 2006 Neuroendocrine control of the ovarian cycle in the rat. In: Knobil E, Neill JD, eds. Knobil and Neill's physiology of reproduction. New York: Academic Press; 2327-2388
33. Blurton-Jones M, Kuan PN, Tuszynski MH 2004 Anatomical evidence for transsynaptic influences of estrogen on brain-derived neurotrophic factor expression. J Comp Neurol 468:347-360 (Pubitemid 37549655)
34. Blurton-Jones M, Tuszynski MH 2006 Estradiol-induced modulation of estrogen receptor-β and GABA within the adult neocortex: a potential transsynaptic mechanism for estrogen modulation of BDNF. J Comp Neurol 499:603-612 (Pubitemid 44606766)
35. Reid AC, Teasdale GM, McCulloch J 1983 Hormonal influence on water permeability across the blood-brain barrier. Clin Exp Neurol 19:50-53
36. Ziylan YZ, Lefauconnier JM, Bernard G, Bourre JM 1990 Bloodbrain barrier permeability: regional alterations after acute and chronic administration of ethinyl estradiol. Neurosci Lett 118:181-184 (Pubitemid 20334875)
37. Bake S, Sohrabji F 2004 17β-Estradiol differentially regulates blood-brain barrier permeability in young and aging female rats. Endocrinology 145:5471-5475 (Pubitemid 39564586)
38. Moser EI, Kropff E, Moser MB 2008 Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 31:69-89
39. Wouterlood FG, Saldana E, Witter MP 1990 Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer phaseolus vulgaris-leucoagglutinin. J Comp Neurol 296:179-203 (Pubitemid 20169520)
40. Dolleman-Van der Weel MJ, Lopes da Silva FH, Witter MP 1997 Nucleus reuniens thalami modulates activity in hippocampal field CA1 through excitatory and inhibitory mechanisms. J Neurosci 17:5640-5650 (Pubitemid 27300328)
41. Chapman CA, Lacaille JC 1999 Cholinergic induction of theta-frequency oscillations in hippocampal inhibitory interneurons and pacing of pyramidal cell firing. J Neurosci 19:8637-8645 (Pubitemid 30226782)
42. Gibbs RB 2000 Oestrogen and the cholinergic hypothesis: Implications for oestrogen replacement therapy in postmenopausal women. Novartis Found Symp 230:94-107; discussion 107-111
43. Segi-Nishida E, Warner-Schmidt JL, Duman RS 2008 Electroconvulsive seizure and VEGF increase the proliferation of neural stemlike cells in rat hippocampus. Proc Natl Acad Sci USA 105:11352-11357
44. Jin KL, Mao XO, Greenberg DA 2000 Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci USA 97:10242-10247
45. Dumitriu D, Rapp PR, McEwen BS, Morrison JH 2010 Estrogen and the aging brain: an elixir for the weary cortical network. Ann NY Acad Sci 1204:104-112
46. Merchenthaler I, Dellovade TL, Shughrue PJ 2003 Neuroprotection by estrogen in animal models of global and focal ischemia. Ann NY Acad Sci 1007:89-100 (Pubitemid 38253657)
47. Svensson B, Peters M, König HG, Poppe M, Levkau B, Rothermundt M, Arolt V, Kögel D, Prehn JH 2002 Vascular endothelial growth factor protects cultured rat hippocampal neurons against hypoxic injury via an antiexcitotoxic, caspase-independent mechanism. J Cereb Blood Flow Metab 22:1170-1175
48. Hoffman GE, Merchenthaler I, Zup SL 2006 Neuroprotection by ovarian hormones in animal models of neurological disease. Endocrine 29:217-231 (Pubitemid 44097365)
49. Bushnell CD, Hurn P, Colton C, Miller VM, del Zoppo G, Elkind MS, Stern B, Herrington D, Ford-Lynch G, Gorelick P, James A, Brown CM, Choi E, Bray P, Newby LK, Goldstein LB, Simpkins J 2006 Advancing the study of stroke in women: summary and recommendations for future research from an NINDS-sponsored multidisciplinary working group. Stroke 37:2387-2399 (Pubitemid 44337191)
50. Hyvärinen M, Qiao Q, Tuomilehto J, Söderberg S, Eliasson M, Stehouwer CD 2010 The difference between acute coronary heart disease and ischaemic stroke risk with regard to gender and age in Finnish and Swedish populations. Int J Stroke 5:152-156
51. Vagnerova K, Koerner IP, Hurn PD 2008 Gender and the injured brain. Anesth Analg 107:201-214
52. Herson PS, Koerner IP, Hurn PD 2009 Sex, sex steroids, and brain injury. Semin Reprod Med 27:229-239
53. Hansen TM, Moss AJ, Brindle NP 2008 Vascular endothelial growth factor and angiopoietins in neurovascular regeneration and protection following stroke. Curr Neurovasc Res 5:236-245
54. Krum JM, Mani N, Rosenstein JM 2008 Roles of the endogenous VEGF receptors flt-1 and flk-1in astroglial and vascular remodeling after brain injury. Exp Neurol 212:108-117
55. Suzuki S, Brown CM, Dela Cruz CD, Yang E, Bridwell DA, Wise PM 2007 Timing of estrogen therapy after ovariectomy dictates the efficacy of its neuroprotective and antiinflammatory actions. Proc Natl Acad Sci USA 104:6013-6018 (Pubitemid 47175650)
56. Sibug RM, Helmerhorst FM, Tijssen AM, de Kloet ER, de Koning J 2002 Estrogen reduces vascular endothelial growth factor (164) expression in the mouse nucleus paraventricularis of the hypothalamus. Neurosci Lett 333:199-202 (Pubitemid 35335776)
57. Ardelt AA, McCullough LD, Korach KS, Wang MM, Munzenmaier DH, Hum PD 2005 Estradiol regulates angiopoietin-1 mRNA expression through estrogen receptor-α in a rodent experimental stroke model. Stroke 36:337-341 (Pubitemid 40170819)
58. Newton SS, Duman RS 2004 Regulation of neurogenesis and angiogenesis in depression. Curr Neurovasc Res 1:261-267
59. MacGregor EA 2005 Female sex hormones and migraine. Rev Neurol (Paris) 161:677-678 (Pubitemid 40934004)
60. MacGregor EA 2008 Menstrual migraine. Curr Opin Neurol 21:309-315 (Pubitemid 351653981)
61. MacGregor EA 2004 Oestrogen and attacks of migraine with and without aura. Lancet Neurol 3:354-361 (Pubitemid 38648856)
62. Krause DN, Duckles SP, Pelligrino DA 2006 Influence of sex steroid hormones on cerebrovascular function. J Appl Physiol 101:1252-1261 (Pubitemid 44497571)
63. Puri V, Puri S, Svojanovsky SR, Mathur S, Macgregor RR, Klein RM, Welch KM, Berman NE 2006 Effects of oestrogen on trigeminal ganglia in culture: Implications for hormonal effects on migraine. Cephalalgia 26:33-42
64. Welch KM, Brandes JL, Berman NE 2006 Mismatch in how oestrogen modulates molecular and neuronal function may explain menstrual migraine. Neurol Sci 27 (Suppl 2): S190-S192 (Pubitemid 44390140)
65. Scharfman HE, MacLusky NJ 2008 Estrogen-growth factor interactions and their contributions to neurological disorders. Headache 48 (Suppl 2): S77-S89 (Pubitemid 351990909)
66. Garcia-Segura LM, McCarthy MM 2004 Minireview: role of glia in neuroendocrine function. Endocrinology 145:1082-1086 (Pubitemid 38280986)
67. Mong JA, Blutstein T 2006 Estradiol modulation of astrocytic form and function: Implications for hormonal control of synaptic communication. Neuroscience 138:967-975