Regulation of soluble guanylyl cyclase activity by oestradiol and progesterone in the hypothalamus but not hippocampus of female rats

Journal of Neuroendocrinology

Volumn 19, Issue 6, 2007, Pages 418-425

  Reyna Neyra, A ^a   Sarkar, G ^a   Etgen, A M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Cyclic GMP; Hypothalamus; Nitric oxide; Oestradiol; Progesterone; Soluble guanylyl cyclase

Indexed keywords

1 BENZYL 3 (5 HYDROXYMETHYL 2 FURYL)INDAZOLE; 3,3 BIS(2 AMINOETHYL) 1 HYDROXY 2 OXOTRIAZENE; 4 AMINO 5 CYCLOPROPYL 2 [1 (2 FLUOROBENZYL) 1H PYRAZOLO[3,4 B]PYRIDIN 3 YL]PYRIMIDINE; CYCLIC GMP; ESTRADIOL; GUANYLATE CYCLASE; NITRIC OXIDE; NITROPRUSSIDE SODIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; HORMONE ACTION; HYPOTHALAMUS; IN VIVO STUDY; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RAT; REGULATORY MECHANISM; REPRODUCTION; SOLUBILITY; SPRAGUE DAWLEY RAT; TISSUE DISTRIBUTION; TISSUE PREPARATION;

ANIMALS; CYCLIC GMP; ENZYME ACTIVATION; ESTRADIOL; ESTROUS CYCLE; FEMALE; GUANYLATE CYCLASE; HIPPOCAMPUS; HYPOTHALAMUS; NITRIC OXIDE; PROGESTERONE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SEXUAL BEHAVIOR, ANIMAL; STATISTICS, NONPARAMETRIC;

EID: 34248662114     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2007.01546.x     Document Type: Article

References (50)

1. Guix FX, Uribesalgo I, Coma M, Munoz FJ. The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 2005; 76: 126-152.
2. Chu HP, Etgen AM. A potential role of cyclic GMP in the regulation of lordosis behavior of female rats. Horm Behav 1997; 32: 125-132.
3. 1 -adrenoceptor activation of the nitric oxide-cGMP pathway: Relevance for hormonal facilitation of lordosis behavior. J Neurosci 1999; 19: 7191-7197.
4. Mani SK, Allen JM, Rettori V, McCann SM, O'Malley BW, Clark JH. Nitric oxide mediates sexual behavior in female rats. Proc Natl Acad Sci USA 1994; 91: 6468-6472.
5. Ceccatelli S, Grandison L, Scott RE, Pfaff DW, Kow LM. Estradiol regulation of nitric oxide synthase mRNAs in rat hypothalamus. Neuroendocrinology 1996; 64: 357-363.
6. Okamura H, Yokosuka M, McEwen BS, Hayashi S. Colocalization of NADPH-diaphorase and estrogen receptor immunoreactivity in the rat ventromedial hypothalamic nucleus: Stimulatory effect of estrogen on NADPH-diaphorase activity. Endocrinology 1994; 135: 1705-1708.
7. Kimura F, Kawakami M, Nakano H, McCann SM. Changes in adenosine 3′,5′-monophosphate and guanosine 3′,5′-monophosphate concentrations in the anterior pituitary and hypothalamus during the rat estrous cycle and effects of administration of sodium pentobarbital in proestrus. Endocrinology 1980; 106: 631-635.
8. Lamar CA, Bhat GK, Mahesh VB, Brann DW. Evidence that neuronal nitric oxide synthase but not heme oxygenase increases in the hypothalamus on proestrus afternoon. Neuroendocrinology 1999; 70: 360-367.
9. Chu HP, Sarkar G, Etgen AM. Estradiol and progesterone modulate the nitric oxide/cyclic GMP pathway in the hypothalamus of female rats and in GT1-1 cells. Endocrine 2004; 24: 177-184.
10. Karanth S, Yu WH, Mastronardi CM, McCann SM. 17beta-estradiol stimulates ascorbic acid and LHRH release from the medial basal hypothalamus in adult male rats. Exp Biol Med (Maywood) 2004; 229: 926-934.
11. Bonavera JJ, Sahu A, Kalra PS, Kalra SP. Evidence that nitric oxide may mediate the ovarian steroid-induced luteinizing hormone surge: involvement of excitatory amino acids. Endocrinology 1993; 133: 2481-2487.
12. Rettori V, Belova N, Dees WL, Nyberg CL, Gimeno M, McCann SM. Role of nitric oxide in the control of luteinizing hormone-releasing hormone release in vivo and in vitro. Proc Natl Acad Sci USA 1993; 90: 10130-10134.
13. Pu S, Kalra PS, Kalra SP. Ovarian steroid-independent diurnal rhythm in cyclic GMP/nitric oxide efflux in the medial preoptic area: Possible role in preovulatory and ovarian steroid-induced LH surge. J Neuroendocrinol 1998; 10: 617-625.
14. Krumenacker JS, Hyder SM, Murad F. Estradiol rapidly inhibits soluble guanylyl cyclase expression in rat uterus. Proc Natl Acad Sci USA 2001; 98: 717-722.
15. Chen ZJ, Che D, Vetter M, Liu S, Chang CH. 17beta-estradiol inhibits soluble guanylate cyclase activity through a protein tyrosine phosphatase in PC12 cells. J Steroid Biochem Mol Biol 2001; 78: 451-458.
16. Zabel U, Hausler C, Weeger M, Schmidt HH. Homodimerization of soluble guanylyl cyclase subunits. Dimerization analysis using a glutathione s-transferase affinity tag. J Biol Chem 1999; 274: 18149-18152.
17. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, Chepenik KP, Waldman SA. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 2000; 52: 375-414.
18. Koesling D, Russwurm M, Mergia E, Mullershausen F, Friebe A. Nitric oxide-sensitive guanylyl cyclase: Structure and regulation. Neurochem Int 2004; 45: 813-819.
19. Pyriochou A, Papapetropoulos A. Soluble guanylyl cyclase: More secrets revealed. Cell Signal 2005; 17: 407-413.
20. Moncada S, Higgs EA. Endogenous nitric oxide: Physiology, pathology and clinical relevance. Eur J Clin Invest 1991; 21: 361-374.
21. Papapetropoulos A, Abou-Mohamed G, Marczin N, Murad F, Caldwell RW, Catravas JD. Downregulation of nitrovasodilator-induced cyclic GMP accumulation in cells exposed to endotoxin or interleukin-1 beta. Br J Pharmacol 1996; 118: 1359-1366.
22. Shi F, Stewart RL Jr, Perez E, Chen JY, LaPolt PS. Cell-specific expression and regulation of soluble guanylyl cyclase alpha 1 and beta 1 subunits in the rat ovary. Biol Reprod 2004; 70: 1552-1561.
23. Chang FJ, Lemme S, Sun Q, Sunahara RK, Beuve A. Nitric oxide-dependent allosteric inhibitory role of a second nucleotide binding site in soluble guanylyl cyclase. J Biol Chem 2005; 280: 11513-11519.
24. McEwen BS. Estrogens effects on the brain: Multiple sites and molecular mechanisms. J Appl Physiol 2001; 91: 2785-2801.
25. MacLusky NJ. Estrogen and Alzheimer's disease: The apolipoprotein connection. Endocrinology 2004; 145: 3062-3064.
26. Edwards DP. Regulation of signal transduction pathways by estrogen and progesterone. Annu Rev Physiol 2005; 67: 335-376.
27. van Steveren WC, Markerink-van Ittersum M, Steinbusch HW, Behrends S, de Vente J. Localization and characterization of cGMP-immunoreactive structures in rat brain slices after NO-dependent and NO-independent stimulation of soluble guanylyl cyclase. Brain Res 2005; 1036: 77-89.
28. Chu HP, Morales JC, Etgen AM. Cyclic GMP may potentiate lordosis behaviour by progesterone receptor activation. J Neuroendocrinol 1999; 11: 107-113.
29. Fleischmann A, Etgen AM, Makman MH. Estradiol plus progesterone promote glutamate-induced release of gamma-aminobutyric acid from preoptic area synaptosomes. Neuropharmacology 1992; 31: 799-807.
30. Keefer LK, Nims RW, Davies KM. Wink DA. 'NONOates'(1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: Convenient nitric oxide dosage forms. Meth Enzymol 1996; 268: 281-293.
31. Martin E, Lee YC, Murad F. YC-1 activation of human soluble guanylyl cyclase has both heme-dependent and heme-independent components. Proc Natl Acad Sci USA 2001; 98: 12938-12942.
32. Lamothe M, Chang FJ, Balashova N, Shirokov R, Beuve A. Functional characterization of nitric oxide and YC-1 activation of soluble guanylyl cyclase: Structural implication for the YC-1 binding site? Biochemistry 2004; 43: 3039-3048.
33. Wedel B, Harteneck C, Foerster J, Friebe A, Schultz G, Koesling D. Functional domains of soluble guanylyl cyclase. J Biol Chem 1995; 270: 24871-24875.
34. Cary SP, Winger JA, Marletta MA. Tonic and acute nitric oxide signaling through soluble guanylate cyclase is mediated by nonheme nitric oxide, ATP, and GTP. Proc Natl Acad Sci USA 2005; 102: 13064-13069.
35. Koesling D, Mullershausen F, Lange A, Friebe A, Mergia E, Wagner C, Russwurm M. Negative feedback in NO/cGMP signalling. Biochem Soc Trans 2005; 33: 1119-1122.
36. Cary SP, Winger JA, Derbyshire ER, Marletta MA. Nitric oxide signaling: no longer simply on or off. Trends Biochem Sci 2006; 31: 231-239.
37. Roy B, Garthwaite J. Nitric oxide activation of guanylyl cyclase in cells revisited. Proc Nat Acad Sci USA 2006; 103: 12185-12190.
38. Louis JC, Revel MO, Zwiller J. Activation of soluble guanylate cyclase through phosphorylation by protein kinase C in intact PC12 cells. Biochim Biophys Acta 1993; 1177: 299-306.
39. Ferrero R, Rodriguez-Pascual F, Miras-Portugal MT, Torres M. Nitric oxide-sensitive guanylyl cyclase activity inhibition through cyclic GMP-dependent dephosphorylation. J Neurochem 2000; 75: 2029-2039.
40. Burette A, Zabel U, Weinberg RJ, Schmidt HH, Valtschanoff JG. Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J Neurosci 2002; 22: 8961-8970.
41. Bellamy TC, Wood J, Goodwin DA, Garthwaite J. Rapid desensitization of the nitric oxide receptor, soluble guanylyl cyclase, underlies diversity of cellular cGMP responses. Proc Natl Acad Sci USA 2000; 97: 2928-2933.
42. Bellamy TC, Garthwaite J. Sub-second kinetics of the nitric oxide receptor, soluble guanylyl cyclase, in intact cerebellar cells. J Biol Chem 2001; 276: 4287-4292.
43. Nedvetsky PI, Kleinschnitz C, Schmidt HH. Regional distribution of protein and activity of the nitric oxide receptor, soluble guanylyl cyclase, in rat brain suggests multiple mechanisms of regulation. Brain Res 2002; 950: 148-154.
44. Wagner C, Russwurm M, Jager R, Friebe A, Koesling D. Dimerization of nitric oxide-sensitive guanylyl cyclase requires the alpha 1 N terminus. J Biol Chem 2005; 280: 17687-17693.
45. Calka J. The role of nitric oxide in the hypothalamic control of LHRH and oxytocin release, sexual behavior and aging of the LHRH and oxytocin neurons. Folia Histoch Cytobiol 2006; 44: 3-12.
46. Gotti S, Sica M, Viglietti-Panzica C, Panzica GC. The distribution of nitric oxide synthase immunoreactivity in the Mouse brain. Microsc Res Tech 2005; 68: 13-25.
47. Panzica GC, Viglietti-Panzica C, Sica M, Gotti S, Martini M, Pinos H, Carrillo B, Collado P. Effects of gonadal hormones on central nitric oxide producing systems. Neuroscience 2006; 138: 987-995.
48. Tafoya MA, Chen JY, Stewart RL, Lapolt PS. Activation of soluble guanylyl cyclase inhibits estradiol production and cyclic AMP accumulation from cultured rat granulosa cells. Fertil Steril 2004; 82 (Suppl. 3): 1154-1159.
49. Velardez MO, Del Carmen Diaz M, Lasaga M, Franchi AM, Duvilanski BH. Estrogen decreases the sensitivity of anterior pituitary to the inhibitory effect of nitric oxide on prolactin release. Horm Res 2003; 60: 111-115.
50. Cabilla JP, Diaz MC, Machiavelli LI, Poliandri AH, Quinteros FA, Lasaga M, Duvilanski BH. 17β-estradiol modifies nitric oxide-sensitive guanylyl cyclase expression and down-regulates its activity in rat anterior pituitary gland. Endocrinology 2006; 147: 4311-4318.