Dominant role of βγ subunits of G-proteins in oxytocin-evoked burst firing

Journal of Neuroscience

Volumn 27, Issue 8, 2007, Pages 1902-1912

  Wang, Yu Feng ^a   Hatton, Glenn I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Coimmunoprecipitation; G q 11 subunit; Milk ejection reflex; Oxytocin receptor; Signal transduction; Src family kinase

Indexed keywords

ANTIBODY; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE DIPHOSPHATE; IONOTROPIC RECEPTOR ANTAGONIST; OXYTOCIN; OXYTOCIN ANTAGONIST; OXYTOCIN RECEPTOR; PERTUSSIS TOXIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN TYROSINE KINASE; RHO KINASE; SURAMIN; TETANUS TOXIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; ISOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DISSOCIATION; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LACTATION; MILK EJECTION; NERVE CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SUCKLING; SUPRAOPTIC NUCLEUS; ANIMAL; DOSE RESPONSE; DRUG EFFECT; ELECTROPHYSIOLOGY; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; SYNAPSE; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHYSIOLOGY; FEMALE; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; LACTATION; NEURONS; OXYTOCIN; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OXYTOCIN; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33847216140     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5346-06.2007     Document Type: Article

References (53)

1. Bealer SL, Crowley WR (1999) Neurotransmitter interaction in release of intranuclear oxytocin in magnocellular nuclei of the hypothalamus. Ann NY Acad Sci 897:182-191.
2. 2+ channels by a G protein betagamma subunit-dependent mechanism. J Physiol (Lond) 556:121-134.
3. Buresi MC, Buret AG, Hollenberg MD, MacNaughton WK (2002) Activation of proteinase-activated receptor 1 stimulates epithelial chloride secretion through a unique MAP kinase- and cyclo-oxygenase-dependent pathway. FASEB J 16:1515-1525.
4. Cardona-Gomez GP, Mendez P, Garcia-Segura LM (2002) Synergistic interaction of estradiol and insulin-like growth factor-I in the activation of PI3K/Akt signaling in the adult rat hypothalamus. Brain Res Mol Brain Res 107:80-88.
5. Charpantier E, Wiesner A, Huh KH, Ogier R, Hoda JC, Allaman G, Raggenbass M, Feuerbach D, Bertrand D, Fuhrer C (2005) α7 neuronal nicotinic acetylcholine receptors are negatively regulated by tyrosine phosphorylation and Src-family kinases. J Neurosci 25:9836-9849.
6. Crowley WR, Armstrong WE (1992) Neurochemical regulation of oxytocin secretion in lactation. Endocr Rev 13:33-65.
7. Darbon P, Tscherter A, Yvon C, Streit J (2003) Role of the electrogenic Na/K pump in disinhibition-induced bursting in cultured spinal networks. J Neurophysiol 90:3119-3129.
8. Dunin-Barkowski WL, Escobar AL, Lovering AT, Orem JM (2003) Respiratory pattern generator model using Ca++-induced Ca++ release in neurons shows both pacemaker and reciprocal network properties. Biol Cybern 89:274-288.
9. Evans JJ, Forrest-Owen W, McArdle CA (1997) Oxytocin receptormediated activation of phosphoinositidase C and elevation of cytosolic calcium in the gonadotrope-derived alphaT3-1 cell line. Endocrinology 138:2049-2055.
10. Freund-Mercier MJ, Richard P (1984) Electrophysiological evidence for facilitatory control of oxytocin neurones by oxytocin during suckling in the rat. J Physiol (Lond) 352:447-466.
11. Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629-683.
12. Goff AK (2004) Steroid hormone modulation of prostaglandin secretion in the ruminant endometrium during the estrous cycle. Biol Reprod 71:11-16.
13. Goubaeva F, Ghosh M, Malik S, Yang J, Hinkle PM, Griendling KK, Neubig RR, Smrcka AV (2003) Stimulation of cellular signaling and G protein subunit dissociation by G protein betagamma subunit-binding peptides. J Biol Chem 278:19634-19641.
14. Hatton GI (1990) Emerging concepts of structure-function dynamics in adult brain: the hypothalamo-neurohypophysial system. Prog Neurobiol 34:437-504.
15. Hatton GI (2004) Morphological plasticity of astroglial/neuronal interactions: functional implications. In: Glial neuronal signaling (Hatton GI, Parpura V, eds), pp 99-124. Boston: Kluwer Academic.
16. Hatton GI, Wang Y-F (2005) Signal transduction pathway underlying oxytocin-evoked burst firing in oxytocin neurons. Soc Neurosci Abstr 31:993.8.
17. Hirasawa M, Kombian SB, Pittman QJ (2001) Oxytocin retrogradely inhibits evoked, but not miniature, EPSCs in the rat supraoptic nucleus: role of N- and P/Q-type calcium channels. J Physiol (Lond) 532:595-607.
18. Hoare S, Copland JA, Strakova Z, Ives K, Jeng YJ, Hellmich MR, Soloff MS (1999) The proximal portion of the COOH terminus of the oxytocin receptor is required for coupling to g(q), but not g(i). Independent mechanisms for elevating intracellular calcium concentrations from intracellular stores. J Biol Chem 274:28682-28689.
19. Jelsema CL, Axelrod J (1987) Stimulation of phospholipase A2 activity in bovine rod outer segments by the beta gamma subunits of transducin and its inhibition by the alpha subunit. Proc Natl Acad Sci USA 84:3623-3627.
20. Jourdain P, Israel JM, Dupouy B, Oliet SH, Allard M, Vitiello S, Theodosis DT, Poulain DA (1998) Evidence for a hypothalamic oxytocin-sensitive pattern-generating network governing oxytocin neurons in vitro. J Neurosci 18:6641-6649.
21. Kow LM, Johnson AE, Ogawa S, Pfaff DW (1991) Electrophysiological actions of oxytocin on hypothalamic neurons in vitro: neuropharmacological characterization and effects of ovarian steroids. Neuroendocrinology 54:526-535.
22. Kuriyama K, Nakashima T, Kawarabayashi T, Kiyohara T (1993) Oxytocin inhibits nonphasically firing supraoptic and paraventricular neurons in the virgin female rat. Brain Res Bull 31:681-687.
23. Leng G, Brown CH, Russell JA (1999) Physiological pathways regulating the activity of magnocellular neurosecretory cells. Prog Neurobiol 57:625-655.
24. Lin SY, Cui H, Yusta B, Belsham DD (2004) IGF-I signaling prevents dehydroepiandrosterone (DHEA)-induced apoptosis in hypothalamic neurons. Mol Cell Endocrinol 214:127-135.
25. Ludwig M, Sabatier N, Bull PM, Landgraf R, Dayanithi G, Leng G (2002) Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites. Nature 418:85-89.
26. Macrez N, Mironneau C, Carricaburu V, Quignard JF, Babich A, Czupalla C, Nurnberg B, Mironneau J (2001) Phosphoinositide 3-kinase isoforms selectively couple receptors to vascular L-type Ca(2+) channels. Circ Res 89:692-699.
27. Malik S, Ghosh M, Bonacci TM, Tall GG, Smrcka AV (2005) Ric-8 enhances G protein βγ-dependent signaling in response to βγ-binding peptides in intact cells. Mol Pharmacol 68:129-136.
28. Moos F, Poulain DA, Rodriguez F, Guerne Y, Vincent JD, Richard P (1989) Release of oxytocin within the supraoptic nucleus during the milk ejection reflex in rats. Exp Brain Res 76:593-602.
29. Neumann I, Russell JA, Landgraf R (1993) Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: a microdialysis study. Neuroscience 53:65-75.
30. Parker SL, Crowley WR (1993a) Stimulation of oxytocin release in the lactating rat by central excitatory amino acid mechanisms: evidence for specific involvement of R,S-alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid-sensitive glutamate receptors. Endocrinology 133:2847-2854.
31. Parker SL, Crowley WR (1993b) Stimulation of oxytocin release in the lactating rat by a central interaction of alpha 1-adrenergic and alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid-sensitive excitatory amino acid mechanisms. Endocrinology 133:2855-2860.
32. Paul S, Nairn AC, Wang P, Lombroso PJ (2003) NMDA-mediated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling. Nat Neurosci 6:34-42.
33. Pittman QJ, Hirasawa M, Mouginot D, Kombian SB (2000) Neurohypophysial peptides as retrograde transmitters in the supraoptic nucleus of the rat. Exp Physiol 85:139S-143S.
34. Ponzio TA, Ni Y, Montana V, Parpura V, Hatton GI (2006) Vesicular glutamate transporter expression in supraoptic neurones suggests a glutamatergic phenotype. J Neuroendocrinol 18:253-265.
35. Quignard JF, Mironneau J, Carricaburu V, Fournier B, Babich A, Nurnberg B, Mironneau C, Macrez N (2001) Phosphoinositide 3-kinase gamma mediates angiotensin II-induced stimulation of L-type calcium channels in vascular myocytes. J Biol Chem 276:32545-32551.
36. Sahu A (2003) Leptin signaling in the hypothalamus: emphasis on energy homeostasis and leptin resistance. Front Neuroendocrinol 24:225-253.
37. Smithson KG, Hatton GI (1990) Immunocytochemical identification of electrophysiologically characterized cells in brain slices. In: Handbook of chemical neuroanatomy (Hokfelt T, ed), pp 305-350. Amsterdam: Elsevier.
38. Stern JE, Armstrong WE (1997) Sustained outward rectification of oxytocinergic neurones in the rat supraoptic nucleus: ionic dependence and pharmacology. J Physiol (Lond) 500:497-508.
39. Su H, Alroy G, Kirson ED, Yaari Y (2001) Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J Neurosci 21:4173-4182.
40. Suter KJ, Wuarin J-P, Smith BN, Dudek FE, Moenter SM (2000) Whole-cell recordings from preoptic/hypothalamic slices reveal burst firing in gonadotropin-releasing hormone neurons identified with green fluorescent protein in transgenic mice. Endocrinology 141:3731-3736.
41. Tsunoda Y, Owyang C (1994) A newly cloned phospholipase A2-activating protein elicits Ca2+ oscillations and pancreatic amylase secretion via mediation of G protein beta/phospholipase A2/arachidonic acid cascades. Biochem Biophys Res Commun 203:1716-1724.
42. Viard P, Exner T, Maier U, Mironneau J, Nurnberg B, Macrez N (1999) Gbetagamma dimers stimulate vascular L-type Ca2+ channels via phosphoinositide 3-kinase. FASEB J 13:685-694.
43. Vogt S, Grosse R, Schultz G, Offermanns S (2003) Receptor-dependent RhoA activation in G12/G13-deficient cells: genetic evidence for an involvement of Gq/G11. J Biol Chem 278:28743-28749.
44. Wakerley JB, Lincoln DW (1973) The milk-ejection reflex of the rat: a 20- to 40-fold acceleration in the firing of paraventricular neurones during oxytocin release. J Endocrinol 57:477-493.
45. Wakerley JB, Clarke G, Summerlee AJ (1994) Milk ejection and its control. In: The physiology of reproduction (Knobil E, Neill JD, eds), pp 1131-1177. New York: Raven.
46. Wang YF, Hatton GI (2004) Milk ejection burst-like electrical activity evoked in supraoptic oxytocin neurons in slices from lactating rats. J Neurophysiol 91:2312-2321.
47. Wang YF, Hatton GI (2005) Burst firing of oxytocin neurons in male rat hypothalamic slices. Brain Res 1032:36-43.
48. Wang YF, Hatton GI (2006) Mechanisms underlying oxytocin-induced excitation of supraoptic neurons: prostaglandin mediation of actin polymerization. J Neurophysiol 95:3933-3947.
49. Wang YF, Negoro H, Honda K (1997) Effect of interhemispheric sections of the hypothalamus on milk-ejection bursts of supraoptic oxytocin neurones during bilateral and unilateral suckling in the rat. Neurosci Lett 227:17-20.
50. Wang YF, Gao XB, van den Pol AN (2001) Membrane properties underlying patterns of GABA-dependent action potentials in developing mouse hypothalamic neurons. J Neurophysiol 86:1252-1265.
51. Wang YF, Ponzio TA, Hatton GI (2006) Autofeedback effects of progressively rising oxytocin concentrations on supraoptic oxytocin neuronal activity in slices from lactating rats. Am J Physiol Regul Integr Comp Physiol 290:R1191-R1198.
52. Yevenes GE, Peoples RW, Tapia JC, Parodi J, Soto X, Olate J, Aguayo LG (2003) Modulation of glycine-activated ion channel function by G-protein betagamma subunits. Nat Neurosci 6:819-824.
53. Zhong M, Yang M, Sanborn BM (2003) Extracellular signal-regulated kinase 1/2 activation by myometrial oxytocin receptor involves Galpha(q)Gbetagamma and epidermal growth factor receptor tyrosine kinase activation. Endocrinology 144:2947-2956.