Hyperpolarization-Activated Cation Channels Are Expressed in Rat Hypothalamic Gonadotropin-Releasing Hormone (GnRH) Neurons and Immortalized GnRH Neurons

Journal of the Society for Gynecologic Investigation

Volumn 13, Issue 6, 2006, Pages 442-450

  Arroyo, Armando ^a   Kim, Beomsu ^a   Rasmusson, Randall L ^a   Bett, Glenna ^a   Yeh, John ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

fluorescence immunohistochemistry; GnRH neurons; GT1 7; HCN; immunocytochemistry

Indexed keywords

CATION CHANNEL; GONADORELIN; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED 1 CHANNEL; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED 2 CHANNEL; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED 3 CHANNEL; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED 4 CHANNEL; UNCLASSIFIED DRUG; HCN2 POTASSIUM CHANNEL; HCN3 PROTEIN, RAT; HCN4 PROTEIN, RAT; HYPERPOLARIZATION ACTIVATED CATION CHANNEL; HYPERPOLARIZATION-ACTIVATED CATION CHANNEL; ION CHANNEL; MESSENGER RNA; POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL IMMORTALIZATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; FLUORESCENCE ANALYSIS; GENE EXPRESSION; HYPERPOLARIZATION; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MEMBRANE BIOLOGY; MEMBRANE CHANNEL; MOUSE; NEUROPHYSIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; CELL LINE; CHEMISTRY; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; NERVE CELL; PHYSIOLOGY; PREOPTIC AREA; SECRETION; SPRAGUE DAWLEY RAT;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TRANSFORMED; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; ION CHANNELS; NEURONS; POTASSIUM CHANNELS; PREOPTIC AREA; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 33749117162     PISSN: 10715576     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsgi.2006.05.010     Document Type: Article

References (51)

1. Knobil E., and Neil J.D. The physiology of reproduction. 2nd ed (1994), Raven Press, New York
2. Terasawa E. Luteinizing hormone-releasing hormone (LHRH) neurons: Mechanism of pulsatile LHRH release. Vitam Horm 63 (2001) 91-129
3. Moenter S.M., DeFazio A.R., Pitts G.R., and Nunemaker C.S. Mechanisms underlying episodic gonadotropin-releasing hormone secretion. Front Neuroendocrinol 24 (2003) 79-93
4. Terasawa E., Keen K.L., Mogi K., and Claude P. Pulsatile release of luteinizing hormone-releasing hormone (LHRH) in cultured LHRH neurons derived from the embryonic olfactory placode of the rhesus monkey. Endocrinology 140 (1999) 1432-1441
5. Krsmanovic L.Z., Martinez-Fuentes A.J., Arora K.K., et al. Autocrine regulation of gonadotropin-releasing hormone secretion in cultured hypothalamic neurons. Endocrinology 140 (1999) 1423-1431
6. Funabashi T., Daikoku S., Shinohara K., and Kimura F. Pulsatile gonadotropin-releasing hormone (GnRH) secretion is an inherent function of GnRH neurons, as revealed by the culture of medial olfactory placode obtained from embryonic rats. Neuroendocrinology 71 (2000) 138-144
7. Martinez de la Escalera G., Choi A.L., and Weiner R.I. Generation and synchronization of gonadotropin-releasing hormone (GnRH) pulses: Intrinsic properties of the GT1-1 GnRH neuronal cell line. Proc Natl Acad Sci U S A 89 (1992) 1852-1855
8. Wetsel W.C., Valenca M.M., Merchenthaler I., et al. Intrinsic pulsatile secretory activity of immortalized luteinizing hormone-releasing hormone-secreting neurons. Proc Natl Acad Sci U S A 89 (1992) 4149-4153
9. Krsmanovic L.Z., Stojilkovic S.S., Merelli F., et al. Calcium signaling and episodic secretion of gonadotropin-releasing hormone in hypothalamic neurons. Proc Natl Acad Sci U S A 89 (1992) 8462-8466
10. Lagrange A.H., Ronnekleiv O.K., and Kelly M.J. Estradiol-17 beta and mu-opioid peptides rapidly hyperpolarize GnRH neurons: A cellular mechanism of negative feedback?. Endocrinology 136 (1995) 2341-2344
11. Kusano K., Fueshko S., Gainer H., and Wray S. Electrical and synaptic properties of embryonic luteinizing hormone-releasing hormone neurons in explant cultures. Proc Natl Acad Sci U S A 92 (1995) 3918-3922
12. Suter K.J., Song W.J., Sampson T.L., et al. Genetic targeting of green fluorescent protein to gonadotropin-releasing hormone neurons: Characterization of whole-cell electrophysiological properties and morphology. Endocrinology 141 (2000) 412-419
13. Sim J.A., Skynner M.J., and Herbison A.E. Heterogeneity in the basic membrane properties of postnatal gonadotropin-releasing hormone neurons in the mouse. J Neurosci 21 (2001) 1067-1075
14. Kato M., Ui-Tei K., Watanabe M., and Sakuma Y. Characterization of voltage-gated calcium currents in gonadotropin-releasing hormone neurons tagged with green fluorescent protein in rats. Endocrinology 144 (2003) 5118-5125
15. Abe H., and Terasawa E. Firing pattern and rapid modulation of activity by estrogen in primate luteinizing hormone releasing hormone-1 neurons. Endocrinology 146 (2005) 4312-4320
16. Suter K.J., Wuarin J.P., Smith B.N., Dudek F.E., and Moenter S.M. 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 (2000) 3731-3736
17. Kuehl-Kovarik M.C., Pouliot W.A., Halterman G.L., Handa R.J., Dudek F.E., and Partin K.M. 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 (2002) 2313-2322
18. Bosma M.M. Ion channel properties and episodic activity in isolated immortalized gonadotropin-releasing hormone (GnRH) neurons. J Membr Biol 136 (1993) 85-96
19. Van Goor F., Krsmanovic L.Z., Catt K.J., and Stojilkovic S.S. Coordinate regulation of gonadotropin-releasing hormone neuronal firing patterns by cytosolic calcium and store depletion. Proc Natl Acad Sci U S A 96 (1999) 4101-4106
20. DiFrancesco D. Pacemaker mechanisms in cardiac tissue. Annu Rev Physiol 55 (1993) 455-472
21. Luthi A., and McCormick D.A. H-current: Properties of a neuronal and network pacemaker. Neuron 21 (1998) 9-12
22. Maccaferri G., and McBain C.J. The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497 (1996) 119-130
23. Bal T., and McCormick D.A. Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current I(h). J Neurophysiol 77 (1997) 3145-3156
24. Chan C.S., Shigemoto R., Mercer J.N., and Surmeier D.J. HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J Neurosci 24 (2004) 9921-9932
25. Santoro B., Liu D.T., Yao H., et al. Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain. Cell 93 (1998) 717-729
26. Ludwig A., Zong X., Jeglitsch M., Hofmann F., and Biel M. A family of hyperpolarization-activated mammalian cation channels. Nature 393 (1998) 587-591
27. Gauss R., Seifert R., and Kaupp U.B. Molecular identification of a hyperpolarization-activated channel in sea urchin sperm. Nature 393 (1998) 583-587
28. Pape H.C. Queer current and pacemaker: The hyperpolarization-activated cation current in neurons. Annu Rev Physiol 58 (1996) 299-327
29. Robinson R.B., and Siegelbaum S.A. Hyperpolarization-activated cation currents: From molecules to physiological function. Annu Rev Physiol 65 (2003) 453-480
30. Monteggia L.M., Eisch A.J., Tang M.D., Kaczmarek L.K., and Nestler E.J. Cloning and localization of the hyperpolarization-activated cyclic nucleotide-gated channel family in rat brain. Brain Res Mol Brain Res 81 (2000) 129-139
31. Notomi T., and Shigemoto R. Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J Comp Neurol 471 (2004) 241-276
32. Mistrik P., Mader R., Michalakis S., Weidinger M., Pfeifer A., and Biel M. The murine HCN3 gene encodes a hyperpolarization-activated cation channel with slow kinetics and unique response to cyclic nucleotides. J Biol Chem 280 (2005) 27056-27061
33. Mellon P.L., Windle J.J., Goldsmith P.C., Padula C.A., Roberts J.L., and Weiner R.I. Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 5 (1990) 1-10
34. Santoro B., Chen S., Luthi A., et al. Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci 20 (2000) 5264-5275
35. Liposits Z., Merchenthaler I., Wetsel W.C., et al. Morphological characterization of immortalized hypothalamic neurons synthesizing luteinizing hormone-releasing hormone. Endocrinology 129 (1991) 1575-1583
36. Hsu L.J., Sagara Y., Arroyo A., et al. Alpha-synuclein promotes mitochondrial deficit and oxidative stress. Am J Pathol 157 (2000) 401-410
37. Harris-Warrick R.M. Voltage-sensitive ion channels in rhythmic motor systems. Curr Opin Neurobiol 12 (2002) 646-651
38. Ashcroft F.M., and Rorsman P. Electrophysiology of the pancreatic beta-cell. Prog Biophys Mol Biol 54 (1989) 87-143
39. 2+-mobilizing and adenylyl cyclase-coupled receptors. J Neurosci 20 (2000) 9290-9297
40. Charles A., Weiner R., and Costantin J. cAMP modulates the excitability of immortalized H=hypothalamic (GT1) neurons via a cyclic nucleotide gated channel. Mol Endocrinol 15 (2001) 997-1009
41. Oka Y., and Matsushima T. Gonadotropin-releasing hormone (GnRH)-immunoreactive terminal nerve cells have intrinsic rhythmicity and project widely in the brain. J Neurosci 13 (1993) 2161-2176
42. + current underlying pacemaker potentials of fish gonadotrophin-releasing hormone neurones. J Physiol 482 (1995) 1-6
43. + currents underlying pacemaker potentials of fish gonadotropin-releasing hormone cells. J Neurophysiol 81 (1999) 643-653
44. Qiu D.L., Chu C.P., Shirasaka T., et al. Neuromedin U depolarizes rat hypothalamic paraventricular nucleus neurons in vitro by enhancing IH channel activity. J Neurophysiol 90 (2003) 843-850
45. Kamondi A., and Reiner P.B. Hyperpolarization-activated inward current in histaminergic tuberomammillary neurons of the rat hypothalamus. J Neurophysiol 66 (1991) 1902-1911
46. Ghamari-Langroudi M., and Bourque C.W. Excitatory role of the hyperpolarization-activated inward current in phasic and tonic firing of rat supraoptic neurons. J Neurosci 20 (2000) 4855-4863
47. Yu X., Duan K.L., Shang C.F., Yu H.G., and Zhou Z. Calcium influx through hyperpolarization-activated cation channels (I(h) channels) contributes to activity-evoked neuronal secretion. Proc Natl Acad Sci U S A 101 (2004) 1051-1056
48. Charles A.C., and Hales T.G. Mechanisms of spontaneous calcium oscillations and action potentials in immortalized hypothalamic (GT1-7) neurons. J Neurophysiol 73 (1995) 56-64
49. Costantin J.L., and Charles A.C. Modulation of Ca(2+) signaling by K(+) channels in a hypothalamic neuronal cell line (GT1-1). J Neurophysiol 85 (2001) 295-304
50. Wetsel W.C. Immortalized hypothalamic luteinizing hormone-releasing hormone (LHRH) neurons: A new tool for dissecting the molecular and cellular basis of LHRH physiology. Cell Mol Neurobiol 15 (1995) 43-78
51. Martinez de la Escalera G., and Clapp C. Regulation of gonadotropin-releasing hormone secretion: Insights from GT1 immortal GnRH neurons. Arch Med Res 32 (2001) 486-498