Estradiol induces physical association of neuronal nitric oxide synthase with NMDA receptor and promotes nitric oxide formation via estrogen receptor activation in primary neuronal cultures

Journal of Neurochemistry

Volumn 109, Issue 1, 2009, Pages 214-224

  D'Anglemont De Tassigny, Xavier ^a,b   Campagne, Céline ^a,b   Steculorum, Sophie ^a,b   Prevot, Vincent ^a,b  

^a JEAN PIERRE AUBERT RESEARCH CENTER   (France)

^b UNIV LILLE   (France)

Author keywords

Estradiol; Estrogen receptor; Hypothalamus; Neuronal nitric oxide synthase; NMDA receptor; Post synaptic density 95

Indexed keywords

ANTIESTROGEN; ANTISENSE OLIGODEOXYNUCLEOTIDE; ESTRADIOL; ESTROGEN RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; POSTSYNAPTIC DENSITY PROTEIN 95; RECEPTOR SUBUNIT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; FEMALE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MALE; NERVE CELL CULTURE; NEWBORN; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION;

RATTUS;

EID: 61849145822     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.05949.x     Document Type: Article

References (61)

1. Aarts M., Liu Y., Liu L., Besshoh S., Arundine M., Gurd J. W., Wang Y. T., Salter M. W. Tymianski M. (2002) Treatment of ischemic brain damage by perturbing NMDA receptor- PSD-95 protein interactions. Science 298, 846 850.
2. Abraham I. M., Todman M. G., Korach K. S. Herbison A. E. (2004) Critical in vivo roles for classical estrogen receptors in rapid estrogen actions on intracellular signaling in mouse brain. Endocrinology 145, 3055 3061.
3. Abu-Soud H. M., Yoho L. L. Stuehr D. J. (1994) Calmodulin controls neuronal nitric-oxide synthase by a dual mechanism. Activation of intra- and interdomain electron transfer. J. Biol. Chem. 269, 32047 32050.
4. Akama K. T. McEwen B. S. (2003) Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J. Neurosci. 23, 2333 2339.
5. Amateau S. K. McCarthy M. M. (2002) A novel mechanism of dendritic spine plasticity involving estradiol induction of prostaglandin-E2. J. Neurosci. 22, 8586 8596.
6. Amateau S. K. McCarthy M. M. (2004) Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior. Nat. Neurosci. 7, 643 650.
7. d'Anglemont de Tassigny X., Campagne C., Dehouck B., Leroy D., Holstein G. R., Beauvillain J. C., Buee-Scherrer V. Prevot V. (2007) Coupling of neuronal nitric oxide synthase to NMDA receptors via postsynaptic density-95 depends on estrogen and contributes to the central control of adult female reproduction. J. Neurosci. 27, 6103 6114.
8. Bhat G. K., Mahesh V. B., Lamar C. A., Ping L., Aguan K. Brann D. W. (1995) Histochemical localization of nitric oxide neurons in the hypothalamus: association with gonadotropin-releasing hormone neurons and co-localization with N-methyl-D-aspartate receptors. Neuroendocrinology 62, 187 197.
9. Boehning D. Snyder S. H. (2003) Novel neural modulators. Annu. Rev. Neurosci. 26, 105 131.
10. Bonavera J. J., Sahu A., Kalra P. S. Kalra S. P. (1993) Evidence that nitric oxide may mediate the ovarian steroid-induced luteinizing hormone surge: involvement of excitatory amino acids. Endocrinology 133, 2481 2487.
11. Brann D. W. Mahesh V. B. (1991) Endogenous excitatory amino acid involvement in the preovulatory and steroid-induced surge of gonadotropins in the female rat. Endocrinology 128, 1541 1547.
12. Bredt D. S. Snyder S. H. (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. Natl Acad. Sci. USA 86, 9030 9033.
13. Bredt D. S. Snyder S. H. (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl Acad. Sci. USA 87, 682 685.
14. Brenman J. E., Chao D. S., Gee S. H. et al. (1996) Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84, 757 767.
15. Brewer L. D., Thibault O., Staton J., Thibault V., Rogers J. T., Garcia-Ramos G., Kraner S., Landfield P. W. Porter N. M. (2007) Increased vulnerability of hippocampal neurons with age in culture: temporal association with increases in NMDA receptor current, NR2A subunit expression and recruitment of L-type calcium channels. Brain Res. 1151, 20 31.
16. Calizo L. H. Flanagan-Cato L. M. (2000) Estrogen selectively regulates spine density within the dendritic arbor of rat ventromedial hypothalamic neurons. J. Neurosci. 20, 1589 1596.
17. Canabal D. D., Song Z., Potian J. G., Beuve A., McArdle J. J. Routh V. H. (2007) Glucose, insulin, and leptin signaling pathways modulate nitric oxide synthesis in glucose-inhibited neurons in the ventromedial hypothalamus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1418 R1428.
18. Christopherson K. S., Hillier B. J., Lim W. A. Bredt D. S. (1999) PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain. J. Biol. Chem. 274, 27467 27473.
19. Clasadonte J., Poulain P., Beauvillain J. C. Prevot V. (2008) Activation of neuronal nitric oxide release inhibits spontaneous firing in adult gonadotropin-releasing hormone neurons: a possible local synchronizing signal. Endocrinology 149, 587 596.
20. Cui H., Hayashi A., Sun H. S. et al. (2007) PDZ protein interactions underlying NMDA receptor-mediated excitotoxicity and neuroprotection by PSD-95 inhibitors. J. Neurosci. 27, 9901 9915.
21. Filardo E. J., Quinn J. A., Bland K. I. Frackelton A. R. Jr. (2000) Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 14, 1649 1660.
22. Filardo E. J., Quinn J. A., Frackelton A. R. Jr. Bland K. I. (2002) Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol. Endocrinol. 16, 70 84.
23. Finn P. D., McFall T. B., Clifton D. K. Steiner R. A. (1996) Sexual differentiation of galanin gene expression in gonadotropin-releasing hormone neurons. Endocrinology 137, 4767 4772.
24. Garthwaite J. Boulton C. L. (1995) Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 57, 683 706.
25. Garthwaite J., Charles S. L. Chess-Williams R. (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336, 385 388.
26. Gore A. C., Yeung G., Morrison J. H. Oung T. (2000) Neuroendocrine aging in the female rat: the changing relationship of hypothalamic gonadotropin-releasing hormone neurons and N-methyl-D-aspartate receptors. Endocrinology 141, 4757 4767.
27. Gould E., Woolley C. S., Frankfurt M. McEwen B. S. (1990) Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10, 1286 1291.
28. Haraguchi K., Satoh K., Yanai H., Hamada F., Kawabuchi M. Akiyama T. (2000) The hDLG-associated protein DAP interacts with dynein light chain and neuronal nitric oxide synthase. Genes Cells 5, 905 911.
29. Herbison A. E. Neill J. D. (2006) Physiology of the Gonadotropin- Releasing Hormone Neuronal Network, in Knobil and Neill's Physiology of Reproduction, 3rd Edn, pp. 1415 1482. Elsevier, Amsterdam.
30. Herbison A. E., Simonian S. X., Norris P. J. Emson P. C. (1996) Relationship of neuronal nitric oxide synthase immunoreactivity to GnRH neurons in the ovariectomized and intact female rat. J. Neuroendocrinol. 8, 73 82.
31. Hering H. Sheng M. (2001) Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2, 880 888.
32. Hisatsune C., Umemori H., Inoue T., Michikawa T., Kohda K., Mikoshiba K. Yamamoto T. (1997) Phosphorylation-dependent regulation of N-methyl-D-aspartate receptors by calmodulin. J. Biol. Chem. 272, 20805 20810.
33. Hollmann M. Heinemann S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31 108.
34. Ishii H., Shibuya K., Ohta Y., Mukai H., Uchino S., Takata N., Rose J. A. Kawato S. (2006) Enhancement of nitric oxide production by association of nitric oxide synthase with N-methyl-D-aspartate receptors via postsynaptic density 95 in genetically engineered Chinese hamster ovary cells: real-time fluorescence imaging using nitric oxide sensitive dye. J. Neurochem. 96, 1531 1539.
35. Itoh Y., Ma F. H., Hoshi H., Oka M., Noda K., Ukai Y., Kojima H., Nagano T. Toda N. (2000) Determination and bioimaging method for nitric oxide in biological specimens by diaminofluorescein fluorometry. Anal. Biochem. 287, 203 209.
36. Jarry H., Hirsch B., Leonhardt S. Wuttke W. (1992) Amino acid neurotransmitter release in the preoptic area of rats during the positive feedback actions of estradiol on LH release. Neuroendocrinology 56, 133 140.
37. Kiedrowski L., Costa E. Wroblewski J. T. (1992) Glutamate receptor agonists stimulate nitric oxide synthase in primary cultures of cerebellar granule cells. J. Neurochem. 58, 335 341.
38. Kojima H., Urano Y., Kikuchi K., Higuchi T., Hirata Y. Nagano T. (1999) Fluorescent indicators for imaging nitric oxide production. Angew. Chem. Int. Ed. Engl. 38, 3209 3212.
39. Kornau H. C., Schenker L. T., Kennedy M. B. Seeburg P. H. (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737 1740.
40. Lamar C. A., Bhat G. K., Mahesh V. B. Brann D. W. (1999) Evidence that neuronal nitric oxide synthase but not heme oxygenase increases in the hypothalamus on proestrus afternoon. Neuroendocrinology 70, 360 367.
41. Liu X. B., Murray K. D. Jones E. G. (2004) Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J. Neurosci. 24, 8885 8895.
42. Maggi A., Ciana P., Belcredito S. Vegeto E. (2004) Estrogens in the nervous system: mechanisms and nonreproductive functions. Annu. Rev. Physiol. 66, 291 313.
43. McCann S. M., Haens G., Mastronardi C., Walczewska A., Karanth S., Rettori V. Yu W. H. (2003) The role of nitric oxide (NO) in control of LHRH release that mediates gonadotropin release and sexual behavior. Curr. Pharm. Des. 9, 381 390.
44. Ojeda S. R., Urbanski H. F., Costa M. E., Hill D. F. Moholt-Siebert M. (1990) Involvement of transforming growth factor alpha in the release of luteinizing hormone-releasing hormone from the developing female hypothalamus. Proc. Natl Acad. Sci. USA 87, 9698 9702.
45. Ojeda S. R., Terasawa E., Pfaff D., Arnold A., Etgen A., Fahrbach S., Moss R. Rubin R. (2002) Neuroendocrine Regulation of Puberty, pp. 589 659. Elsevier, New York.
46. Osborne C. K., Wakeling A. Nicholson R. I. (2004) Fulvestrant: an oestrogen receptor antagonist with a novel mechanism of action. Br. J. Cancer 90 (Suppl 1 S2 S6.
47. Panatier A., Theodosis D. T., Mothet J. P., Touquet B., Pollegioni L., Poulain D. A. Oliet S. H. (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775 784.
48. Prast H. Philippu A. (2001) Nitric oxide as modulator of neuronal function. Prog. Neurobiol. 64, 51 68.
49. Prossnitz E. R., Oprea T. I., Sklar L. A. Arterburn J. B. (2008) The ins and outs of GPR30: a transmembrane estrogen receptor. J. Steroid Biochem. Mol. Biol. 109, 350 353.
50. Sans N., Petralia R. S., Wang Y. X., Blahos J. 2nd. Hell J. W. Wenthold R. J. (2000) A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci. 20, 1260 1271.
51. Sato S., Braham C. S., Putnam S. K. Hull E. M. (2005) Neuronal nitric oxide synthase and gonadal steroid interaction in the MPOA of male rats: co-localization and testosterone-induced restoration of copulation and nNOS-immunoreactivity. Brain Res. 1043, 205 213.
52. Sattler R., Xiong Z., Lu W. Y., Hafner M., MacDonald J. F. Tymianski M. (1999) Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 284, 1845 1848.
53. Savchenko A., Barnes S. Kramer R. H. (1997) Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390, 694 698.
54. Scordalakes E. M., Shetty S. J. Rissman E. F. (2002) Roles of estrogen receptor alpha and androgen receptor in the regulation of neuronal nitric oxide synthase. J. Comp Neurol. 453, 336 344.
55. Swanson L. W. (1996) Structure of the Rat Brain. Elsevier Science Publishers, Amsterdam.
56. Thomas P., Pang Y., Filardo E. J. Dong J. (2005) Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146, 624 632.
57. Wang H. G., Lu F. M., Jin I., Udo H., Kandel E. R., de Vente J., Walter U., Lohmann S. M., Hawkins R. D. Antonova I. (2005) Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron 45, 389 403.
58. Warner M. Gustafsson J. A. (2006) Nongenomic effects of estrogen: why all the uncertainty? Steroids 71, 91 95.
59. Williams K. (1993) Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol. Pharmacol. 44, 851 859.
60. Woolley C. S. (2007) Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 47, 657 680.
61. Woolley C. S. McEwen B. S. (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12, 2549 2554.