Activity of protein kinase C is important for 3α,5α-THP's actions at dopamine type 1-like and/or GABAA receptors in the ventral tegmental area for lordosis of rats

Brain Research Bulletin

Volumn 77, Issue 2-3, 2008, Pages 91-97

  Frye, Cheryl A ^a   Walf, Alicia A ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

5 Pregnan 3 ol 20 one; Allopregnanolone; Midbrain; Neurosteroids; Phospholipase C

Indexed keywords

2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; 3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; BISINDOLYLMALEIMIDE; DOPAMINE 1 RECEPTOR; ESTRADIOL; GESTAGEN; MEMBRANE RECEPTOR; MUSCIMOL; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG INFUSION; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; LOCOMOTION; LORDOSIS; MOTOR ACTIVITY; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; SEXUAL BEHAVIOR; VENTRAL TEGMENTUM;

2,3,4,5-TETRAHYDRO-7,8-DIHYDROXY-1-PHENYL-1H-3-BENZAZEPINE; ANIMALS; DOPAMINE AGONISTS; ESTRADIOL; FEMALE; GABA AGONISTS; INDOLES; LORDOSIS; MALEIMIDES; MOTOR ACTIVITY; MUSCIMOL; OVARIECTOMY; PROGESTERONE; PROTEIN KINASE C; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS; RECEPTORS, DOPAMINE D1; RECEPTORS, GABA-A; VENTRAL TEGMENTAL AREA;

EID: 51749097947     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2008.07.002     Document Type: Article

References (83)

1. Alvarez-Jaimes L., Feliciano-Rivera M., Centeno-Gonzalez M., and Maldonado-Vlaar C.S. Contributions of the mitogen-activated protein kinase and protein kinase C cascades in spatial learning and memory mediated by the nucleus accumbens. J. Pharmacol. Exp. Therapeut. 314 (2005) 1144-1157
2. Akin D., Manier D.H., Sanders-Bush E., and Shelton R.C. Signal transduction abnormalities in melancholic depression. Int. J. Neuropsychopharmacol. 8 (2005) 5-16
3. Belmar J., Cuellar C., Llona I., Arancibia S., Kusch C., Tapia-Arancibia L., Pinter A., and Perez H. Allopregnanolone-induced modification of presynaptic basal and K+-induced [3H]-norepinephrine efflux from rat cortical slices during the estrous cycle. Neuroendocrinology 68 (1998) 264-271
4. Beyer C., Canchola E., and Larsson K. Facilitation of lordosis behavior in the ovariectomized estrogen primed rat by dibutyryl cAMP. Physiol. Behav. 26 (1988) 249-251
5. Buisson B., and Bertrand D. Nicotine addiction: the possible role of functional upregulation. Trends Pharmacol. Sci. 23 (2002) 130-136
6. Chu H.P., and Etgen A.M. A potential role of cyclic GMP in the regulation of lordosis behavior of female rats. Horm. Behav. 32 (1997) 125-132
7. Ciereszko R.E., Guan Z., Stokes B.T., Petroff B.K., Ottobre A.C., and Ottobre J.S. Arachidonic acid inhibits hCG-stimulated progesterone production by corpora lutea of primates: potential mechanism of action. Prostaglandins 50 (1995) 103-119
8. Compagnone N.A., and Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinol. 21 (2000) 1-56
9. DeBold J.F., and Malsbury C.W. Facilitation of sexual receptivity by hypothalamic and midbrain implants of progesterone in female hamsters. Physiol. Behav. 46 (1989) 655-660
10. Dunlop B.W., and Nemeroff C.B. The role of dopamine in the pathophysiology of depression. Arch. Gen. Psychiatry 64 (2007) 327-337
11. Dwivedi Y., Conley R.R., Roberts R.C., Tamminga C.A., and Pandey G.N. [(3)H]cAMP binding sites and protein kinase a activity in the prefrontal cortex of suicide victims. Am. J. Psychiatry 159 (2002) 66-73
12. Fancsik A., Linn D.M., and Tasker J.G. Neurosteroid modulation of GABA IPSCs is phosphorylation dependent. J. Neurosci. 20 (2000) 3067-3075
13. Frye C.A. The role of neurosteroids and non-genomic effects of progestins and androgens in mediating sexual receptivity of rodents. Brain Res. Brain Res. Rev. 37 (2001) 201-222
14. Frye C.A. The role of neurosteroids and nongenomic effects of progestins in the ventral tegmental area in mediating sexual receptivity of rodents. Horm. Behav. 40 (2001) 226-233
15. Frye C.A., and DeBold J.F. Evidence for a non-genomic action of progestins on sexual receptivity in hamster ventral tegmental area but not hypothalamus. Brain Res. 578 (1992) 87-93
16. Frye C.A., and DeBold J.F. Muscimol facilitates sexual receptivity in hamsters when infused into the ventral tegmentum. Pharmacol. Biochem. Behav. 42 (1992) 879-887
17. Frye C.A., and Gardiner S.G. Progestins can have a membrane-mediated action in rat midbrain for facilitation of sexual receptivity. Horm. Behav. 30 (1996) 682-691
18. Frye C.A., Mermelstein P.G., and DeBold J.F. Evidence for a non-genomic action of progestins on sexual receptivity in hamster ventral tegmental area but not hypothalamus. Brain Res. 578 (1992) 87-93
19. Frye C.A., Mermelstein P.G., and DeBold J.F. Bicuculline infused into the hamster ventral tegmentum inhibits, while sodium valproate facilitates, sexual receptivity. Pharmacol. Biochem. Behav. 46 (1993) 1-8
20. Frye C.A., Murphy R.E., and Platek S.M. Anti-sense oligonucleotides, for progestin receptors in the VMH and glutamic acid decarboxylase in the VTA, attenuate progesterone-induced lordosis in hamsters and rats. Behav. Brain Res. 115 (2000) 55-64
21. Frye C.A., Paris J.J., and Rhodes M.E. Engaging in paced mating, but neither exploratory, anti-anxiety, nor social behavior, increases 5α-reduced progestin concentrations in midbrain, hippocampus, striatum, and cortex. Reproduction 133 (2007) 663-674
22. Frye C.A., and Petralia S.M. Lordosis of rats is modified by neurosteroidogenic effects of membrane benzodiazepine receptors in the ventral tegmental area. Neuroendocrinology 77 (2003) 71-82
23. Frye C.A., and Petralia S.M. Mitochondrial benzodiazepine receptors in the ventral tegmental area modulate sexual behavior of cycling or hormone-primed hamsters. J. Neuroendocrinol. 15 (2001) 677-686
24. Frye C.A., and Petralia S.M. In the ventral tegmental area picrotoxin blocks FGIN 1-27-induced increases in sexual behavior of rats and hamsters. Psychopharmacology 178 (2005) 174-182
25. Frye C.A., Petralia S.M., Rhodes M.E., and Stein B. Fluoxetine may influence lordosis of rats through effects on midbrain 3α,5α-THP concentrations. Ann. NY Acad. Sci. 1007 (2001) 37-41
26. Frye C.A., and Rhodes M.E. Progestin concentrations are increased following paced mating in midbrain, hippocampus, diencephalon, and cortex of rats in behavioral estrus, but only in midbrain of diestrous rats. Neuroendocrinology 83 (2007) 336-347
27. Frye C.A., Rhodes M.E., Petralia S.M., Walf A.A., Sumida K., and Edinger K.L. 3α-hydroxy-5α-pregnan-20-one in the midbrain ventral tegmental area mediates social, sexual, and affective behaviors. Neuroscience 138 (2006) 1007-1014
28. Frye C.A., Sumida K., Zimmerberg B., and Brunelli S.A. Rats bred for high versus low anxiety responses neonatally demonstrate increases in lordosis, pacing behavior, and midbrain 3α,5α-THP levels as adults. Behav. Neurosci. 120 (2006) 281-289
29. 5, but not progestin receptor, antagonist and anti-sense oligonucleotide infusions to the ventral tegmental area of cycling rats and hamsters attenuate lordosis. Behav. Brain Res. 103 (1999) 23-34
30. Frye C.A., and Vongher J.M. Ventral tegmental area infusions of inhibitors of the biosynthesis and metabolism of 3α,5α-THP attenuate lordosis of hormone-primed and behavioural oestrous rats and hamsters. J. Neuroendocrinol. 13 (2001) 1076-1086
31. Frye C.A., and Walf A.A. Hippocampal 3α,5α-THP may alter depressive behavior of pregnant and lactating rats. Pharmacol. Biochem. Behav. 78 (2004) 531-540
32. Frye C.A., and Walf A.A. In the ventral tegmental area, progestins' membrane-mediated actions for lordosis of hormone-primed hamsters involve phospholipase C and protein kinase C. J. Neuroendocrinol. 19 (2007) 717-724
33. A receptors involve downstream signal transduction pathways. Steroids 73 (2008) 906-913
34. A receptors. Horm. Behav. 50 (2006) 332-337
35. A receptors in the ventral tegmental area may be G-protein-dependent. Behav. Brain Res. 172 (2006) 286-293
36. Frye C.A., Walf A.A., and Petralia S.M. Progestin facilitation of lordosis in rodents involves adenylyl cyclase activity in the ventral tegmental area. Horm. Behav. 50 (2006) 237-244
37. Frye C.A., Walf A.A., and Sumida K. Progestins' actions in the VTA to facilitate lordosis involve dopamine-like type 1 and 2 receptors. Pharmacol. Biochem. Behav. 78 (2004) 405-418
38. Gonzalez-Flores O., Ramirez-Orduna J.M., Lima-Hernandez F.J., Garcia-Juarez M., and Beyer C. Differential effect of kinase A and C blockers on lordosis facilitation by progesterone and its metabolites in ovariectomized estrogen-primed rats. Horm. Behav. 49 (2006) 398-404
39. Gonzalez-Flores O., Shu J., Camacho-Arroyo I., and Etgen A.M. Regulation of lordosis by cyclic 3′,5′-guanosine monophosphate, progesterone, and its 5α-reduced metabolites involves mitogen-activated protein kinase. Endocrinology 145 (2004) 5560-5567
40. Griffin L.D., and Mellon S.H. Selective serotonin reuptake inhibitors directly alter activity of neurosteroidogenic enzymes. PNAS 96 (1999) 13512-13517
41. Hardy D.F., and Debold J.F. Effects of mounts without intromission upon the behavior of female rats during the onset of estrogen-induced heat. Physiol. Behav. 7 (1971) 643-645
42. Harrison N.L., and Simmonds M.A. Modulation of the GABA receptor complex by a steroid anesthetic. Brain Res. 323 (1984) 287-292
43. Jo Y., King S.R., Khan S.A., and Stocco D.M. Involvement of protein kinase C and cyclic adenosine 3′,5′-monophosphate-dependent kinase in steroidogenic acute regulatory protein expression and steroid biosynthesis in Leydig cells. Biol. Reprod. 73 (2005) 244-255
44. Johnson J., and Capco D.G. Progesterone acts through protein kinase C to remodel the cytoplasm as the amphibian oocyte becomes the fertilization-competent egg. Mech. Dev. 67 (1997) 215-226
45. Kostellow A.B., Chien E.J., and Morrill G.A. Calcium-dependent phosphorylation of the amphibian oocyte plasma membrane: an early event in initiating the meiotic divisions. Biochem. Biophys. Res. Commun. 147 (1987) 863-869
46. Kow L.M., Brown H.E., and Pfaff D.W. Activation of protein kinase C in the hypothalamic ventromedial nucleus or the midbrain central gray facilitates lordosis. Brain Res. 660 (1994) 241-248
47. Kow L.M., and Pfaff D.W. Mapping of neural and signal transduction pathways for lordosis in the search for estrogen actions on the central nervous system. Behav. Brain Res. 92 (1998) 169-180
48. Kubli-Garfias C., Azpeitia E., Villanueva-Tello T., and Ponce-Monter H. Inhibition of noradrenaline release by 5α-progestins in cerebral cortex slices. Proc. Western Pharmacol. Soc. 26 (1983) 135-138
49. A receptors. Cell. Mol. Neurobiol. 16 (1996) 155-174
50. Lange C.A. Integration of progesterone receptor action with rapid signaling events in breast cancer models. J. Steroid Biochem. Mol. Biol. 108 (2008) 203-212
51. Maggi A., and Perez J. Progesterone and estrogens in rat brain: modulation of GABA (gamma-aminobutyric acid) receptor activity. Eur. J. Pharmacol. 103 (1984) 165-168
52. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., and Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232 (1986) 1004-1007
53. Mani S.K., Fienberg A.A., O'Callaghan J.P., Snyder G.L., Allen P.B., Dash P.K., Moore A.N., Mitchell A.J., Bibb J., Greengard P., and O'Malley B.W. Requirement for DARPP-32 in progesterone-facilitated sexual receptivity in female rats and mice. Science 287 (2000) 1053-1056
54. Marazziti D., Perez J., and Cassano G.B. Is obsessive-compulsive disorder caused by a second-messenger imbalance?. CNS Spectrums 6 (2001) 206-209
55. Marazziti D., Dell'Osso L., Masala I., Baroni S., Presta S., Giannaccini G., Di Nasso E., Mungai F., Lucacchini A., and Cassano G.B. Decreased inhibitory activity of PKC in OCD patients after six months of treatment. Psychoneuroendocrinology 27 (2002) 769-776
56. Marshall J.F., and Teitelbaum P. Further analysis of sensory inattention following lateral hypothalamic damage in rats. J Comp Physiol Psychol 86 (1974) 375-395
57. Maurice T., Phan V.L., Urani A., Kamei H., Noda Y., and Nabeshima T. Neuroactive neurosteroids as endogenous effectors for the sigma1 (sigma1) receptor: pharmacological evidence and therapeutic opportunities. Jpn. J. Pharmacol. 81 (1999) 125-155
58. Meizel S. Amino acid neurotransmitter receptor/chloride channels of mammalian sperm and the acrosome reaction. Biol. Reprod. 56 (1997) 569-574
59. Mobbs C.V., Rothfeld J.M., Saluja R., and Pfaff D.W. Phorbol esters and forskolin infused into midbrain central gray facilitate lordosis. Pharmacol. Biochem. Behav. 34 (1989) 665-667
60. 3H]noradrenaline release: modulation by calcium channel blockers. J. Neuroendocrinol. 14 (2002) 955-962
61. Nemeroff C.B., and Vale W.W. The neurobiology of depression: inroads to treatment and new drug discovery. J. Clin. Psychol. 66 (2005) 5-13
62. Pandey G.N., Dwivedi Y., Sridhararao J., Ren X., Janicak P.G., and Sharma R. Protein kinase C and phospholipase C activity and expression of their specific isozymes is decreased and expression of MARCKS is increased in platelets of bipolar but not in unipolar patients. Neuropsychopharmacology 26 (2002) 216-228
63. Park-Chung M., Wu F.S., and Farb D.H. 3α-Hydroxy-5α-pregnan-20-one sulfate: a negative modulator of the NMDA-induced current in cultured neurons. Mol. Pharmacol. 46 (1994) 146-150
64. Paxinos G., and Watson C. The Rat Brain (1986), Academic Press, New York
65. Petralia S.M., and Frye C.A. In the ventral tegmental area, cAMP mediates progesterone's actions at dopamine type 1 receptors for lordosis of rats and hamsters. J. Neuroendocrinol. 18 (2006) 902-914
66. Petralia S.M., and Frye C.A. In the ventral tegmental area, G-proteins and cAMP mediate the neurosteroid 3α,5α-THP's actions at dopamine type 1 receptors for lordosis of rats. Neuroendocrinology 80 (2004) 233-243
67. Petralia S.M., Jahagirdar V., and Frye C.A. Inhibiting biosynthesis and/or metabolism of progestins in the ventral tegmental area attenuates lordosis of rats in behavioural oestrus. J. Neuroendocrinol. 17 (2005) 545-552
68. Petralia S.M., Walf A.A., and Frye C.A. In the ventral tegmental area, progestins' membrane-mediated actions for lordosis of hamsters and rats involve protein kinase A. Neuroendocrinology 84 (2006) 405-414
69. Pfaus J.G., Smith W.J., Byrne N., and Stephens G. Appetitive and consummatory sexual behaviors of female rats in bilevel chambers. II. Patterns of estrus termination following vaginocervical stimulation. Horm. Behav. 37 (2000) 96-107
70. Rausch J.L., Gillespie C.F., Fei Y., Hobby H.M., Stoming T., Ganapathy V., and Leibach F.H. Antidepressant effects on kinase gene expression patterns in rat brain. Neurosci. Lett. 334 (2002) 91-94
71. Raw R.E., and Silvia W.J. Activity of phospholipase C and release of prostaglandin F2 alpha by endometrial tissue from ovariectomized ewes receiving progesterone and estradiol. Biol. Reprod. 44 (1991) 404-412
72. Reddy D.S., and Kulkarni S.K. Chronic neurosteroid treatment prevents the development of morphine tolerance and attenuates abstinence behavior in mice. Eur. J. Pharmacol. 337 (1997) 19-25
73. Riemer R.K., Goldfien A., and Roberts J.M. Estrogen increases adrenergic- but not cholinergic-mediated production of inositol phosphates in rabbit uterus. Mol. Pharmacol. 32 (1987) 663-668
74. Ross C.A., MacCumber M.W., Glatt C.E., and Snyder S.H. Brain phospholipase C isozymes: differential mRNA localizations by in situ hybridisation. PNAS 86 (1989) 2923-2927
75. Rubinow D.R., and Schmidt P.J. Gonadal steroid regulation of mood: the lessons of premenstrual syndrome. Front. Neuroendocrinol. 27 (2006) 210-216
76. Rupprecht R., and Holsboer F. Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci. 22 (1999) 410-416
77. Smith F.L., Javed R.R., Smith P.A., Dewey W.L., and Gabra B.H. PKC and PKA inhibitors reinstate morphine-induced behaviors in morphine tolerant mice. Pharmacol. Res. 54 (2006) 474-480
78. Sumida K., Walf A.A., and Frye C.A. Progestin-facilitated lordosis of hamsters may involve dopamine-like type 1 receptors in the ventral tegmental area. Behav. Brain Res. 161 (2005) 1-7
79. Ueda H., Inoue M., Yoshida A., Mizuno K., Yamamoto H., Maruo J., Matsuno K., and Mita S. Metabotropic neurosteroid/sigma-receptor involved in stimulation of nociceptor endings of mice. J. Pharmacol. Exp. Therapeut. 298 (2001) 703-710
80. Uzunova V., Sampson L., and Uzunov D.P. Relevance of endogenous 3α-reduced neurosteroids to depression and antidepressant action. Psychopharmacology 186 (2006) 351-361
81. Vathy I.U., Etgen A.M., and Barfield R.J. Actions of RU 38486 on progesterone facilitation and sequential inhibition of rat estrous behavior: correlation with neural progestin receptor levels. Horm. Behav. 23 (1989) 43-56
82. Winfree C.J., Coombs D.W., DeLeo J.A., and Colburn R.W. Analgesic effects of intrathecally-administered 3α-hydroxy-5α-pregnan-20-one in a rat mechanical visceral pain model. Life Sci. 50 (1992) 1007-1012
83. Yaghoubi N., Malayev A., Russek S.J., Gibbs T.T., and Farb D.H. Neurosteroid modulation of recombinant ionotropic glutamate receptors. Brain Res. 803 (1998) 153-160