Low dose of dopamine may stimulate prolactin secretion by increasing fast potassium currents
Tóm tắt
Dopamine (DA) released from the hypothalamus tonically inhibits pituitary lactotrophs. DA (at micromolar concentration) opens potassium channels, hyperpolarizing the lactotrophs and thus preventing the calcium influx that triggers prolactin hormone release. Surprisingly, at concentrations ∼1000 lower, DA can stimulate prolactin secretion. Here, we investigated whether an increase in a K+ current could mediate this stimulatory effect. We considered the fast K+ currents flowing through large-conductance BK channels and through A-type channels. We developed a minimal lactotroph model to investigate the effects of these two currents. Both I
BK and I
A could transform the electrical pattern of activity from spiking to bursting, but through distinct mechanisms. I
BK always increased the intracellular Ca2+ concentration, while I
A could either increase or decrease it. Thus, the stimulatory effects of DA could be mediated by a fast K+ conductance which converts tonically spiking cells to bursters. In addition, the study illustrates that a heterogeneous distribution of fast K+ conductances could cause heterogeneous lactotroph firing patterns.
Tài liệu tham khảo
Arey BJ, Burris TP, Basco P, Freeman ME (1993) Infusion of dopamine at low concentrations stimulates the release of prolactin from Alpha-Methyl-P-Tyrosine-treated rats. Proc. Soc. Exp. Biol. Med. 203: 60–63.
Ben Jonathan N, Hnasko R (2001) Dopamine as a prolactin (PRL) inhibitor. Endocr. Rev. 22: 724–763.
Bertram R, Butte MJ, Kiemel T, Sherman A (1995) Topological and phenomenological classification of bursting oscillations. Bull. Math. Biol. 57: 413–439.
Burris TP, Freeman ME (1993) Low concentrations of dopamine increase cytosolic calcium in lactotrophs. Endocrinol. 133: 63–68.
Burris TP, Nguyen DN, Smith SG, Freeman ME (1992) The stimulatory and inhibitory effects of dopamine on prolactin secretion involve different G-Proteins. Endocrinol. 130: 926–932.
Burris TP, Stringer LC, Freeman ME (1991) Pharmacological evidence that a D2-Receptor subtype mediates dopaminergic stimulation of prolactin secretion from the anterior-pituitary gland. Neuroendocrinol. 54: 175–183.
Chang A, Shin SH (1999) Dopamine agonists both stimulate and inhibit prolactin release in GH(4)ZR(7) cells. Eur. J. Endocrinol. 141: 387–395.
Chang A, Shin SH, Pang SC (1997) Dopamine D-2 receptor mediates both inhibitory and stimulatory actions on prolactin release. Endocrine 7: 177–182.
Chay TR, Keizer J (1983) Minimal model for membrane oscillations in the pancreatic beta-cell. Biophys. J. 42: 181–189.
Denef C, Manet D, Dewals R (1980) Dopaminergic stimulation of prolactin-release. Nature 285: 243–246.
Dodge FA, Rahamimoff R (1967) Co-operative action of calcium ions in transmitter release at neuromuscular junction. J. Physiol. Lond. 193: 419–432.
Doiron B, Laing C, Longtin A, Maler L (2002) Ghostbursting: A novel neuronal burst mechanism. J. Comput. Neurosci. 12: 5–25.
Einhorn LC, Gregerson KA, Oxford GS (1991) D2 dopamine receptor activation of potassium channels in identified rat lactotrophs—whole-cell and single-channel recording. J. Neurosci. 11: 3727–3737.
Ermentrout B (2002) Simulating, analyzing, and animating dynamical systems SIAM.
Gregerson KA, Flagg TP, O'Neill TJ, Anderson M, Lauring O, Horel JS, Welling PA (2001) Identification of G protein-coupled, inward rectifier potassium channel gene products from the rat anterior pituitary gland. Endocrinol. 142: 2820–2832.
Helmchen F, Imoto K, Sakmann B (1996) Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. Biophys. J. 70: 1069–1081.
Herrington J, Lingle CJ (1994) Multiple components of voltage-dependent potassium current in normal rat anterior-pituitary-cells. J. Neurophys. 72: 719–729.
Horta J, Hiriart M, Cota G (1991) Differential expression of Na channels in functional subpopulations of rat lactotropes. Am. J. Physiol. 261: C865–C871.
Kanyicska B, Freeman ME, Dryer SE (1997) Endothelin activates large-conductance K+ channels in rat lactotrophs: Reversal by long-term exposure to dopamine agonist. Endocrinol. 138: 3141–3153.
Liu LX, Shen RY, Kapatos G, Chiodo LA (1994) Dopamine neuron membrane physiology—characterization of the transient outward current (I-A) and demonstration of a common signal-transduction pathway for I-A and I-K. Synapse 17: 230–240.
Lledo PM, Guerineau N, Mollard P, Vincent JD, Israel JM (1991) Physiological characterization of 2 functional-states in subpopulations of prolactin cells from lactating rats. J. Physiol.- Lond. 437: 477–494.
Lledo PM, Legendre P, Israel JM, Vincent JD (1990a) Dopamine inhibits 2 characterized voltage-dependent calcium currents in identified rat lactotroph cells. Endocrinol. 127: 990–1001.
Lledo PM, Legendre P, Zhang J, Israel JM, Vincent JD (1990b) Effects of dopamine on voltage-dependent potassium currents in identified rat lactotroph cells. Neuroendocrinology 52: 545–555.
Neher E, Augustine GJ (1992) Calcium gradients and buffers in bovine chromaffin cells. J. Physiol. Lond. 450: 273–301.
Oxford GS, Tse A (1993) Modulation of ion channels underlying excitation-secretion coupling in identified lactotrophs and gonadotrophs. Biol. Reprod. 48: 1–7.
Porter TE, Grandy D, Bunzow J, Wiles CD, Civelli O, Frawley LS (1994) Evidence that stimulatory dopamine-receptors may be involved in the regulation of prolactin secretion. Endocrinol. 134: 1263–1268.
Prakriya M, Lingle CJ (2000) Activation of BK channels in rat chromaffin cells requires summation of Ca2+ influx from multiple Ca2+ channels. J. Neurophysiol. 84: 1123–1135.
Rinzel J, Ermentrout GB (1998) Analysis of neural excitability and oscillations. In: C Koch, I Segev, eds. Methods in Neuronal Modeling. MIT Press, Cambridge.
Roberts WM, Jacobs RA, Hudspeth AJ (1990) Colocalization of ion channels involved in frequency-selectivity and synaptic transmission at presynaptic active zones of hair-cells. J. Neurosci. 10: 3664–3684.
Roussel C, Erneux T, Schiffmann SN, Gall D (2006) Modulation of neuronal excitability by intracellular calcium buffering: From spiking to bursting. Cell Calcium 39: 455–466.
Rush ME, Rinzel J (1995) The potassium A-current, low firing rates and rebound excitation in hodgkin-huxley models. Bull. Math. Biol. 57: 899–929.
Sharp AA, Oneil MB, Abbott LF, Marder E (1993) Dynamic clamp—Computer-generated conductances in real neurons. J. Neurophysiol. 69: 992–995.
Tagawa R, Takahara J, Sato M, Niimi M, Murao K, Ishida T (1992) Stimulatory effects of quinpirole hydrochloride, D2-dopamine receptor agonist, at low concentrations on prolactin-release in female rats invitro. Life Sci. 51: 727–732.
Van Goor F, Li YX, Stojilkovic SS (2001a) Paradoxical role of large-conductance calcium-activated K+ (BK) channels in controlling action potential-driven Ca2+ entry in anterior pituitary cells. J. Neurosci. 21: 5902–5915.
Van Goor F, Zivadinovic D, Martinez-Fuentes AJ, Stojilkovic SS (2001b) Dependence of pituitary hormone secretion on the pattern of spontaneus voltage-gated calcium influx—Cell type-specific action potential secretion coupling. J. Biol. Chem. 276: 33840–33846.
Van Goor F, Zivadinovic D, Stojilkovic SS (2001c) Differential expression of ionic channels in rat anterior pituitary cells. Mol. Endocrinol. 15: 1222–1236.