Morphological characterization of the action potential initiation segment in GnRH neuron dendrites and axons of male mice

Endocrinology (United States)

Volumn 156, Issue 11, 2015, Pages 4174-4186

  Herde, Michel K ^a,b   Herbison, Allan E ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN G; GONADORELIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL BODY; CELL DENSITY; CELL STRUCTURE; CELL SUBPOPULATION; CIRCUMVENTRICULAR ORGAN; DENDRITE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTRACELLULAR SPACE; MALE; MEDIAN EMINENCE; MOUSE; NERVE FIBER; NEURITE; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; CONFOCAL MICROSCOPY; CYTOLOGY; METABOLISM; NERVE CELL; PHYSIOLOGY; TRANSGENIC MOUSE;

ACTION POTENTIALS; ANIMALS; AXONS; DENDRITES; GONADOTROPIN-RELEASING HORMONE; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; NEURONS;

EID: 84946028369     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1284     Document Type: Article

References (53)

1. Campbell RE, Suter KJ. Redefining the gonadotrophin-releasing hormone neurone dendrite. J Neuroendocrinol. 2010;22:650-658.
2. Herbison AE. Physiology of the adult GnRH neuronal network. In: Plant TM, Zeleznik AJ, eds. Knobil and Neill's Physiology of Reproduction. 4th ed. New York: Academic Press; 2014:399-467.
3. Herde MK, Iremonger KJ, Constantin S, Herbison AE. GnRH neurons elaborate a long-range projection with shared axonal and dendritic functions. J Neurosci. 2013;33:12689-12697.
4. Iremonger KJ, Herbison AE. Multitasking in gonadotropin-releas-ing hormone neuron dendrites. [published online ahead of print October 3, 2014]. Neuroendocrinology.
5. Chen X, Iremonger K, Herbison A, Kirk V, Sneyd J. Regulation of electrical bursting in a spatiotemporal model of a GnRH neuron. Bull Math Biol. 2013;75:1941-1960.
6. Herde MK, Geist K, Campbell RE, Herbison AE. Gonadotropin-releasing hormone neurons extend complex highly branched dendritic trees outside the blood-brain barrier. Endocrinology. 2011; 152:3832-3841.
7. Lehman MN, Silverman AJ. Ultrastructure of luteinizing hormone-releasing hormone (LHRH) neurons and their projections in the golden hamster. Brain Res Bull. 1988;20:211-221.
8. Leranth C, Segura LM, Palkovits M, MacLusky NJ, Shanabrough M, Naftolin F. The LH-RH-containing neuronal network in the preoptic area of the rat: demonstration of LH-RH-containing nerve terminals in synaptic contact with LH-RH neurons. Brain Res. 1985; 345:332-336.
9. Chen WP, Witkin JW, Silverman AJ./3-Endorphin and gonadotro-pin-releasing hormone synaptic input to gonadotropin-releasing hormone neurosecretory cells in the male rat. J Comp Neurol. 1989; 286:85-95.
10. Langub MC Jr, Maley BE, Watson RE Jr. Ultrastructural evidence for luteinizing hormone-releasing hormone neuronal control of estrogen responsive neurons in the preoptic area. Endocrinology. 1991;128:27-36.
11. Kalló I, Vida B, Bardóczi Z, et al. Gonadotropin-releasing hormone neurones innervate kisspeptin neurones in the female mouse brain. Neuroendocrinology. 2013;98:281-289.
12. Palmer LM, Stuart GJ. Site of action potential initiation in layer 5 pyramidal neurons. J Neurosci. 2006;26:1854-1863.
13. v 1. 2 in action potential initiation and backpropa-gation. Nat Neurosci. 2009;12:996-1002.
14. Kole MH, Stuart GJ. Signal processing in the axon initial segment. Neuron. 2012;73:235-247.
15. Kordeli E, Lambert S, Bennett V. Ankyrin G. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J Biol Chem. 1995;270:2352-2359.
16. Zhou D, Lambert S, Malen PL, Carpenter S, Boland LM, Bennett V. AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol. 1998;143:1295-1304.
17. Garrido JJ, Giraud P, Carlier E, et al. A targeting motif involved in sodium channel clustering at the axonal initial segment. Science. 2003;300:2091-2094.
18. Roberts CB, Campbell RE, Herbison AE, Suter KJ. Dendritic action potential initiation in hypothalamic gonadotropin-releasing hormone neurons. Endocrinology. 2008;149:3355-3360.
19. Iremonger KJ, Herbison AE. Initiation and propagation of action potentials in gonadotropin-releasing hormone neuron dendrites. J Neurosci. 2012;32:151-158.
20. Spergel DJ, Krüth U, Hanley DF, Sprengel R, Seeburg PH. GABA-And glutamate-Activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J Neurosci. 1999;19:2037-2050.
21. Constantin S, Piet R, Iremonger K, et al. GnRH neuron firing and response to GABA in vitro depend on acute brain slice thickness and orientation. Endocrinology. 2012;153:3758-3769.
22. Iremonger J, Herbison AE. Elucidating the structure and function of GnRH neuron dendrites. In: Armstrong WE, Tasker JG, eds. Neurophysiology of Neuroendocrine Neurons. Hoboken, NJ: John Wiley & Sons; 2015:273-299.
23. Van Wart A, Trimmer JS, Matthews G. Polarized distribution of ion channels within microdomains of the axon initial segment. J Comp Neurol. 2007;500:339-352.
24. Bennett V, Lambert S. Physiological roles of axonal ankyrins in survival of premyelinated axons and localization of voltage-gated sodium channels. J Neurocytol. 1999;28:303-318.
25. Atherton JF, Wokosin DL, Ramanathan S, Bevan MD. Autonomous initiation and propagation of action potentials in neurons of the subthalamic nucleus. J Physiol. 2008;586:5679-5700.
26. Preibisch S, Saalfeld S, Tomancak P. Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics. 2009;25: 1463-1465.
27. Campbell RE, Han SK, Herbison AE. Biocytin filling of adult gonadotropin-releasing hormone neurons in situ reveals extensive, spiny, dendritic processes. Endocrinology. 2005;146:1163-1169.
28. Cottrell EC, Campbell RE, Han SK, Herbison AE. Postnatal remodeling of dendritic structure and spine density in gonadotropin-releasing hormone neurons. Endocrinology. 2006;147:3652-3661.
29. Chan H, Prescott M, Ong Z, Herde MK, Herbison AE, Campbell RE. Dendritic spine plasticity in gonadatropin-releasing hormone (GnRH) neurons activated at the time of the preovulatory surge. Endocrinology. 2011;152:4906-4914.
30. Campbell RE, Gaidamaka G, Han SK, Herbison AE. Dendro-den-dritic bundling and shared synapses between gonadotropin-releasing hormone neurons. Proc Natl Acad Sci US A. 2009;106:10835-10840.
31. Ybarra N, Hemond PJ, O'Boyle MP, Suter KJ. Spatially selective, testosterone-independent remodeling of dendrites in gonadotropin-releasing hormone (GnRH) neurons prepubertally in male rats. Endocrinology. 2011;152:2011-2019.
32. + channel distribution at the axon initial segment. Nature. 2010;465: 1075-1078.
33. Kaphzan H, Buffington SA, Jung JI, Rasband MN, Klann E. Alterations in intrinsic membrane properties and the axon initial segment in a mouse model of Angelman syndrome. J Neurosci. 2011;31: 17637-17648.
34. Duflocq A, Chareyre F, Giovannini M, Couraud F, Davenne M. Characterization of the axon initial segment (AIS) of motor neurons and identification of a para-AIS and a juxtapara-AIS, organized by protein 4. 1B. BMC Biol. 2011;9:66.
35. Grubb MS, Shu Y, Kuba H, Rasband MN, Wimmer VC, Bender KJ. Short-And long-term plasticity at the axon initial segment. J Neurosci. 2011;31:16049-16055.
36. Westrum LE. Observations on initial segments of axons in the prepy-riform cortex of the rat. J Comp Neurol. 1970;139:337-356.
37. DeFelipe J, Hendry SH, Jones EG, Schmechel D. Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory-motor cortex. J Comp Neurol. 1985;231:364-384.
38. Lahjouji F, Bras H, Barbe A, Chmykhova N, Chazal G. Electron microscopic serial analysis of GABA presynaptic terminals on the axon hillock and initial segment of labeled abducens motoneurons in the rat. Neurosci Res. 1997;27:143-153.
39. Howard A, Tamas G, Soltesz I. Lighting the chandelier: new vistas for axo-Axonic cells. Trends Neurosci. 2005;28:310-316.
40. Moore AM, Prescott M, Marshall CJ, Yip SH, Campbell RE. Enhancement of a robust arcuate GABAergic input to gonadotropin-releasing hormone neurons in a model of polycystic ovarian syndrome. Proc Natl Acad Sci USA. 2015;112:596-601.
41. Williams SR, Stuart GJ. Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science. 2002;295: 1907-1910.
42. Lee K, Duan W, Sneyd J, Herbison AE. Two slow calcium-Activated afterhyperpolarization currents control burst firing dynamics in gonadotropin-releasing hormone neurons. J Neurosci. 2010;30: 6214-6224.
43. Cuevas P, Gimenez-Gallego G, Martinez-Murillo R, Carceller F. Immunohistochemical localization of basic fibroblast growth factor in ependymal cells of the rat lateral and third ventricles. Acta Anat. 1991;141:307-310.
44. Tooyama I, Hara Y, Yasuhara O, et al. Production of antisera to acidic fibroblast growth factor and their application to immunohistochemical study in rat brain. Neuroscience. 1991;40:769-779.
45. Gonzalez AM, Logan A, Ying W, Lappi DA, Berry M, Baird A. Fibroblast growth factor in the hypothalamic-pituitary axis: differential expression of fibroblast growth factor-2 and a high affinity receptor. Endocrinology. 1994;134:2289-2297.
46. Rousselet A, Fetler L, Chamak B, Prochiantz A. Rat mesencephalic neurons in culture exhibit different morphological traits in the presence of media conditioned on mesencephalic or striatal astroglia. Dev Biol. 1988;129:495-504.
47. Zhou D, DiFiglia M. Basic fibroblast growth factor enhances the growth of postnatal neostriatal GABAergic neurons in vitro. Exp Neurol. 1993;122:171-188.
48. Patel MN, McNamaraJO. Selective enhancementofaxonal branching of cultured dentate gyrus neurons by neurotrophic factors. Neu-roscience. 1995;69:763-770.
49. Gibson MJ, Ingraham L, Dobrjansky A. Soluble factors guide go-nadotropin-releasing hormone axonal targeting to the median eminence. Endocrinology. 2000;141:3065-3071.
50. Tsai PS, Moenter SM, Postigo HR, et al. Targeted expression of a dominant-negative fibroblast growth factor (FGF) receptor in go-nadotropin-releasing hormone (GnRH) neurons reduces FGF responsiveness and the size of GnRH neuronal population. Mol En-docrinol. 2005;19:225-236.
51. Gill JC, Tsai PS. Expression of a dominant negative FGF receptor in developingGNRH1neuronsdisruptsaxonoutgrowthandtargeting to the median eminence. Biol Reprod. 2006;74:463-472.
52. Chen WP, Witkin JW, Silverman AJ. Sexual dimorphism in the syn-Aptic input to gonadotropin releasing hormone neurons. Endocrinology. 1990;126:695-702.
53. Campos P, Herbison AE. Optogenetic activation of GnRH neurons reveals minimal requirements for pulsatile luteinizing hormone secretion. Proc Natl Acad Sci USA. 2014;111:18387-18392.