An integrated model of electrical spiking, bursting, and calcium oscillations in GnRH neurons

Biophysical Journal

Volumn 96, Issue 11, 2009, Pages 4514-4524

  Fletcher, Patrick A ^a   Li, Yue Xian ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; GONADORELIN; ION CHANNEL; APAMIN; CYCLIC AMP; ENZYME INHIBITOR; FORSKOLIN; NEUROTOXIN; SODIUM; THAPSIGARGIN;

ARTICLE; BRAIN NERVE CELL; BRAIN SLICE; CALCIUM SIGNALING; CELL LINE; CELL MEMBRANE; CELL SURFACE; DYNAMICS; ELECTRIC ACTIVITY; EXPERIMENTAL STUDY; HORMONE RELEASE; HYPOTHALAMUS; INFORMATION PROCESSING; MEMBRANE POTENTIAL; MODEL; PREDICTION; ACTION POTENTIAL; ALGORITHM; BIOLOGICAL MODEL; CELL MEMBRANE POTENTIAL; DRUG EFFECT; METABOLISM; NERVE CELL; PHYSIOLOGY;

ACTION POTENTIALS; ALGORITHMS; APAMIN; CALCIUM; CYCLIC AMP; ENZYME INHIBITORS; FORSKOLIN; GONADOTROPIN-RELEASING HORMONE; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NEURONS; NEUROTOXINS; SODIUM; THAPSIGARGIN;

EID: 68949119568     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.03.037     Document Type: Article

References (39)

1. Knobil, E. 1980. The neuroendocrine control of the menstrual cycle. Recent Prog. Horm. Res. 36:63-88.
2. Suter, K. J., J. P. Wuarin, B. N. Smith, F. E. Dudek, and S. M. Moenter. 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.
3. 2+ oscillations in luteinizing hormone-releasing hormone neurons derived from the embryonic olfactory placode of the rhesus monkey. J. Neurosci. 19:5898-5909.
4. Moore, Jr., J. P., E. Shang, and S. Wray. 2002. In situ GABAergic modulation of synchronous gonadotropin releasing hormone-1 neuronal activity. J. Neurosci. 22:8932-8941.
5. Woller, M., E. Nichols, T. Herdendorf, and D. Tutton. 1998. Release of luteinizing hormone-releasing hormone from enzymatically dispersed rat hypothalamic explants is pulsatile. Biol. Reprod. 59:587-590.
6. Martinez-Fuentes, A. J., L. Hu, L. Z. Krsmanovic, and K. J. Catt. 2004. Gonadotropin-releasing hormone (GnRH) receptor expression and membrane signaling in early embryonic GnRH neurons: role in pulsatile neurosecretion. Mol. Endocrinol. 18:1808-1817.
7. Krsmanovic, L. Z., N. Mores, C. E. Navarro, K. K. Arora, and K. J. Catt. 2003. An agonist-induced switch in G protein coupling of the gonadotropin-releasing hormone receptor regulates pulsatile neuropeptide secretion. Proc. Natl. Acad. Sci. USA. 100:2969-2974.
8. Khadra, A., and Y. X. Li. 2006. A model for the pulsatile secretion of gonadotropin-releasing hormone from synchronized hypothalamic neurons. Biophys. J. 91:74-83.
9. Li, Y. X., and A. Khadra. 2008. Robust synchrony and rhythmogenesis in endocrine neurons via autocrine regulations in vitro and in vivo. Bull. Math. Biol. 70:2103-2125.
10. 2+ signaling in GnRH-secreting neurons. Biophys. J. 79:1310-1323.
11. 2+-mobilizing and adenylyl cyclase-coupled receptors. J. Neurosci. 20:9290-9297.
12. Jasoni, C. L., M. G. Todman, M. M. Strumia, and A. E. Herbison. 2007. Cell type-specific expression of a genetically encoded calcium indicator reveals intrinsic calcium oscillations in adult gonadotropin-releasing hormone neurons. J. Neurosci. 27:860-867.
13. Van Goor, F., L. Z. Krsmanovic, K. J. Catt, and S. S. Stojilkovic. 1999. Control of action potential-driven calcium influx in GT1 neurons by the activation status of sodium and calcium channels. Mol. Endocrinol. 13:587-603.
14. Hu, L., K. Wada, N. Mores, L. Z. Krsmanovic, and K. J. Catt. 2006. Essential role of G protein-gated inwardly rectifying potassium channels in gonadotropin-induced regulation of GnRH neuronal firing and pulsatile neurosecretion. J. Biol. Chem. 281:25231-25240.
15. Van Goor, F., L. Z. Krsmanovic, K. J. Catt, and S. S. Stojilkovic. 1999. Coordinate regulation of gonadotropin-releasing hormone neuronal firing patterns by cytosolic calcium and store depletion. Proc. Natl. Acad. Sci. USA. 96:4101-4106.
16. 2+ concentration and gonadotropin-releasing hormone (GnRH) release in immortalized GnRH neurons in an Na+ -dependent manner. Endocrinology. 143:4210-4217.
17. Yoshida, H., S. Paruthiyil, P. Butler, and R. I. Weiner. 2004. Role of cAMP signaling in the mediation of dopamine-induced stimulation of GnRH secretion via D1 dopamine receptors in GT1-7 cells. Neuroendocrinology. 80:2-10.
18. Kuehl-Kovarik, M. C., W. A. Pouliot, G. L. Halterman, R. J. Handa, F. E. Dudek, et al. 2002. Episodic bursting activity and response to excitatory amino acids in acutely dissociated gonadotropin-releasing hormone neurons genetically targeted with green fluorescent protein. J. Neurosci. 22:2313-2322.
19. Kuehl-Kovarik, M. C., K. M. Partin, R. J. Handa, and F. E. Dudek. 2005. Spike-dependent depolarizing afterpotentials contribute to endogenous bursting in gonadotropin releasing hormone neurons. Neuroscience. 134:295-300.
20. Liu, X., and A. E. Herbison. 2008. Small-conductance calcium-activated potassium channels control excitability and firing dynamics in gonadotropin-releasing hormone (GnRH) neurons. Endocrinology. 149:3598-3604.
21. Charles, A. C., and T. G. Hales. 1995. Mechanisms of spontaneous calcium oscillations and action potentials in immortalized hypothalamic (GT1-7) neurons. J. Neurophysiol. 73:56-64.
22. Li, Y. X. 2003. Tango waves in a bidomain model of fertilization calcium waves. Physica D. 186:27-49.
23. i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism. J. Theor. Biol. 166:461-473.
24. Li, Y. X., S. S. Stojilkovic, J. Keizer, and J. Rinzel. 1997. Sensing and refilling calcium stores in an excitable cell. Biophys. J. 72:1080-1091.
25. Allbritton, N. L., T. Meyer, and L. Stryer. 1992. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science. 258:1812-1815.
26. Lewis, R. S. 2007. The molecular choreography of a store-operated calcium channel. Nature. 446:284-287.
27. Spergel, D. J., K. J. Catt, and E. Rojas. 1996. Immortalized GnRH neurons express large-conductance calcium-activated potassium channels. Neuroendocrinology. 63:101-111.
28. Xu, C., T. A. Roepke, C. Zhang, O. K. Ronnekleiv, and M. J. Kelly. 2008. GnRH activates the M-current in GnRH neurons: an autoregulatory negative feedback mechanism? Endocrinology. 149:2459-2466.
29. Chay, T. R. 1996. Modeling slowly bursting neurons via calcium store and voltage-independent calcium current. Neural Comput. 8:951-978.
30. + entry in anterior pituitary cells. J. Neurosci. 21:5902-5915.
31. Kelly, M. J., and E. J. Wagner. 2002. GnRH neurons and episodic bursting activity. Trends Endocrinol. Metab. 13:409-410.
32. Nunemaker, C. S., R. A. DeFazio, M. E. Geusz, E. D. Herzog, G. R. Pitts, et al. 2001. Long-term recordings of networks of immortalized GnRH neurons reveal episodic patterns of electrical activity. J. Neurophysiol. 86:86-93.
33. Nunemaker, C. S., M. Straume, R. A. DeFazio, and S. M. Moenter. 2003. Gonadotropin-releasing hormone neurons generate interacting rhythms in multiple time domains. Endocrinology. 144:823-831.
34. Terasawa, E., T. A. Richter, and K. L. Keen. 2002. A role for nonneuronal cells in synchronization of intracellular calcium oscillations in primate LHRH neurons. Prog. Brain Res. 141:283-291.
35. Woller, M. J., S. Meyer, A. Ada-Nguema, and D. Waechter-Brulla. 2004. Dissecting autocrine effects on pulsatile release of gonadotropin-releasing hormone in cultured rat hypothalamic tissue. Exp. Biol. Med. (Maywood). 229:56-64.
36. Krsmanovic, L. Z., S. S. Stojilkovic, L. M. Mertz, M. Tomic, and K. J. Catt. 1993. Expression of gonadotropin-releasing hormone receptors and autocrine regulation of neuropeptide release in immortalized hypothalamic neurons. Proc. Natl. Acad. Sci. USA. 90:3908-3912.
37. Krsmanovic, L. Z., A. J. Martinez-Fuentes, K. K. Arora, N. Mores, C. E. Navarro, et al. 1999. Autocrine regulation of gonadotropin-releasing hormone secretion in cultured hypothalamic neurons. Endocrinology. 140:1423-1431.
38. Xu, C., X. Z. Xu, C. S. Nunemaker, and S. M. Moenter. 2004. Dose-dependent switch in response of gonadotropin-releasing hormone (GnRH) neurons to GnRH mediated through the type I GnRH receptor. Endocrinology. 145:728-735.
39. Todman, M. G., S. K. Han, and A. E. Herbison. 2005. Profiling neurotransmitter receptor expression in mouse gonadotropin-releasing hormone neurons using green fluorescent protein-promoter transgenics and microarrays. Neuroscience. 132:703-712.