Hyperpolarization-activated cyclic nucleotide-gated channels in olfactory sensory neurons regulate axon extension and glomerular formation

Journal of Neuroscience

Volumn 30, Issue 49, 2010, Pages 16498-16508

  Mobley, Arie S ^a   Miller, Alexandra M ^a   Araneda, Ricardo C ^b   Maurer, Lydia R ^a   Müller, Frank ^c   Greer, Charles A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Bldg 142   (United States)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC NUCLEOTIDE GATED CHANNEL; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; GLOMERULUS; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE FIBER GROWTH; NONHUMAN; OLFACTORY MEMORY; OLFACTORY NERVE; OLFACTORY SENSORY NEURON; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL;

ANIMALS; ANIMALS, NEWBORN; ANTIDIARRHEALS; AXONS; BIOPHYSICS; CARDIOTONIC AGENTS; CELLS, CULTURED; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; ELECTRIC STIMULATION; EMBRYO, MAMMALIAN; GAP-43 PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; ION CHANNELS; LOPERAMIDE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL CELL ADHESION MOLECULES; NEUROGENESIS; OLFACTORY BULB; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; PYRIMIDINES; RECEPTORS, ODORANT; SENSORY RECEPTOR CELLS;

EID: 78650074381     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4225-10.2010     Document Type: Article

References (64)

1. Beaumont V, Zucker RS (2000) Enhancement of synaptic transmission by cyclic AMP modulation of presynaptic Ih channels. Nat Neurosci 3:133-141. (Pubitemid 30126328)
2. Bender RA, Kirschstein T, Kretz O, Brewster AL, Richichi C, Rüschenschmidt C, Shigemoto R, Beck H, Frotscher M, Baram TZ (2007) Localization of HCN1 channels to presynaptic compartments: novel plasticity that may contribute to hippocampal maturation. J Neurosci 27:4697-4706. (Pubitemid 46663575)
3. Biju KC, Marks DR, Mast TG, Fadool DA (2008) Deletion of voltage-gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system. J Comp Neurol 506:161-179.
4. Bozza TC, Kauer JS (1998) Odorant response properties of convergent olfactory receptor neurons. J Neurosci 18:4560-4569. (Pubitemid 28280166)
5. Brewster AL, Chen Y, Bender RA, Yeh A, Shigemoto R, Baram TZ (2007) Quantitative analysis and subcellular distribution of mRNA and protein expression of the hyperpolarization-activated cyclic nucleotide-gated channels throughout development in rat hippocampus. Cereb Cortex 17:702-712. (Pubitemid 46254709)
6. Brunet LJ, Gold GH, Ngai J (1996) General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17:681-693.
7. Chen S, Wang J, Siegelbaum SA (2001) Properties of hyperpolarization- activated pacemaker current defined by coassembly of HCN1 and HCN2 subunits and basal modulation by cyclic nucleotide. J Gen Physiol 117:491-504.
8. Chen X, Shu S, Kennedy DP, Willcox SC, Bayliss DA (2009) Subunit-specific effects of isoflurane on neuronal Ih in HCN1 knock-out mice. J Neurophysiol 101:129-140.
9. Chesler AT, Zou DJ, Le Pichon CE, Peterlin ZA, Matthews GA, Pei X, Miller MC, Firestein S (2007) A G protein/cAMP signal cascade is required for axonal convergence into olfactory glomeruli. Proc Natl Acad Sci U S A 104:1039-1044. (Pubitemid 46154732)
10. Cho JH, Lépine M, Andrews W, Parnavelas J, Cloutier JF (2007) Requirement for Slit-1 and Robo-2 in zonal segregation of olfactory sensory neuron axons in the main olfactory bulb. J Neurosci 27:9094-9104.
11. Col JA, Matsuo T, Storm DR, Rodriguez I (2007) Adenylyl cyclase-dependent axonal targeting in the olfactory system. Development 134:2481-2489. (Pubitemid 47074142)
12. de Castro F, Hu L, Drabkin H, Sotelo C, Chédotal A (1999) Chemoattraction and chemorepulsion of olfactory bulb axons by different secreted semaphorins. J Neurosci 19:4428-4436. (Pubitemid 29241094)
13. Dibattista M, Mazzatenta A, Grassi F, Tirindelli R, Menini A (2008) Hyperpolarization-activated cyclic nucleotide-gated channels in mouse vomeronasal sensory neurons. J Neurophysiol 100:576-586.
14. Dubacq C, Jamet S, Trembleau A (2009) Evidence for developmentally regulated local translation of odorant receptor mRNAs in the axons of olfactory sensory neurons. J Neurosci 29:10184-10190.
15. Feinstein P, Mombaerts P (2004) Acontextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117:817-831.
16. Feinstein P, Bozza T, Rodriguez I, Vassalli A, Mombaerts P (2004) Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117:833-846. (Pubitemid 38748897)
17. Frings S, Lynch JW, Lindemann B (1992) Properties of cyclic nucleotide-gated channels mediating olfactory transduction: activation, selectivity, and blockage. J Gen Physiol 100:45-67.
18. Gasparini S, DiFrancesco D (1997) Action of the hyperpolarization- activated current (Ih) blocker ZD 7288 in hippocampal CA1 neurons. Pflugers Arch 435:99-106.
19. Gussing F, Bohm S (2004) NQO1 activity in the main and the accessory olfactory systems correlates with the zonal topography of projection maps. Eur J Neurosci 19:2511-2518. (Pubitemid 38621848)
20. Hanson MG, Landmesser LT (2004) Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 43:687-701.
21. Holderith NB, Shigemoto R, Nusser Z (2003) Cell type-dependent expression of HCN1 in the main olfactory bulb. Eur J Neurosci 18:344-354.
22. Imai T, Suzuki M, Sakano H (2006) Odorant receptor-derived cAMP signals direct axonal targeting. Science 314:657-661.
23. Kusch J, Biskup C, Thon S, Schulz E, Nache V, Zimmer T, Schwede F, Benndorf K (2010) Interdependence of receptor activation and ligand binding in HCN2 pacemaker channels. Neuron 67:75-85.
24. Lagostena L, Menini A (2003) Whole-cell recordings and photolysis of caged compounds in olfactory sensory neurons isolated from the mouse. Chem Senses 28:705-716. (Pubitemid 39144863)
25. Lee YT, Vasilyev DV, Shan QJ, Dunlop J, Mayer S, Bowlby MR (2008) Novel pharmacological activity of loperamide and CP-339,818 on human HCN channels characterized with an automated electrophysiology assay. Eur J Pharmacol 581:97-104.
26. Lin DM, Wang F, Lowe G, Gold GH, Axel R, Ngai J, Brunet L (2000) Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity. Neuron 26:69-80.
27. Lipscomb BW, Treloar HB, Klenoff J, Greer CA (2003) Cell surface carbohydrates and glomerular targeting of olfactory sensory neuron axons in the mouse. J Comp Neurol 467:22-31. (Pubitemid 37339755)
28. Lynch JW, Barry PH (1991) Inward rectification in rat olfactory receptor neurons. Proc Biol Sci 243:149-153.
29. Margalit T, Lancet D (1993) Expression of olfactory receptor and transduction genes during rat development. Brain Res Dev Brain Res 73:7-16.
30. 2+ increases. Proc Natl Acad Sci U S A 106:3537-3542.
31. Matsuzaki O, Bakin RE, Cai X, Menco BP, Ronnett GV (1999) Localization of the olfactory cyclic nucleotide-gated channel subunit 1 in normal, embryonic and regenerating olfactory epithelium. Neuroscience 94:131-140.
32. Ming GL, Song HJ, Berninger B, Holt CE, Tessier-Lavigne M, Poo MM (1997) cAMP-dependent growth cone guidance by netrin-1. Neuron 19:1225-1235.
33. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675-686.
34. Moosmang S, Biel M, Hofmann F, Ludwig A (1999) Differential distribution of four hyperpolarization-activated cation channels in mouse brain. Biol Chem 380:975-980. (Pubitemid 29412758)
35. Müller F, Scholten A, Ivanova E, Haverkamp S, Kremmer E, Kaupp UB (2003) HCN channels are expressed differentially in retinal bipolar cells and concentrated at synaptic terminals. Eur J Neurosci 17:2084-2096.
36. Notomi T, Shigemoto R (2004) Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J Comp Neurol 471:241-276.
37. Potter SM, Zheng C, Koos DS, Feinstein P, Fraser SE, Mombaerts P (2001) Structure and emergence of specific olfactory glomeruli in the mouse. J Neurosci 21:9713-9723.
38. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453-480.
39. Rodriguez-Gil DJ, Treloar HB, Zhang X, Miller AM, Two A, Iwema C, Firestein SJ, Greer CA (2010) Chromosomal location-dependent nonstochastic onset of odor receptor expression. J Neurosci 30:10067-10075.
40. Rodríguez-Menchaca AA, Navarro-Polanco RA, Ferrer-Villada T, Rupp J, Sachse FB, Tristani-Firouzi M, Sánchez-Chapula JA (2008) The molecular basis of chloroquine block of the inward rectifier Kir2.1 channel. Proc Natl Acad Sci U S A 105:1364-1368.
41. Sakano H (2010) Neural map formation in the mouse olfactory system. Neuron 67:530-542.
42. Schwarting GA, Raitcheva D, Crandall JE, Burkhardt C, Püschel AW (2004) Semaphorin 3A-mediated axon guidance regulates convergence and targeting of P2 odorant receptor axons. Eur J Neurosci 19:1800-1810.
43. Serizawa S, Miyamichi K, Takeuchi H, Yamagishi Y, Suzuki M, Sakano H (2006) A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127:1057-1069.
44. Shay EL, Greer CA, Treloar HB (2008) Dynamic expression patterns of ECM molecules in the developing mouse olfactory pathway. Dev Dyn 237:1837-1850.
45. Singh KK, Miller FD (2005) Activity regulates positive and negative neurotrophin-derived signals to determine axon competition. Neuron 45:837-845.
46. Surges R, Brewster AL, Bender RA, Beck H, Feuerstein TJ, Baram TZ (2006) Regulated expression of HCN channels and cAMP levels shape the properties of the h current in developing rat hippocampus. Eur J Neurosci 24:94-104.
47. Suto F, Murakami Y, Nakamura F, Goshima Y, Fujisawa H (2003) Identification and characterization of a novel mouse plexin, plexin-A4. Mech Dev 120:385-396.
48. Treloar HB, Feinstein P, Mombaerts P, Greer CA (2002) Specificity of glomerular targeting by olfactory sensory axons. J Neurosci 22:2469-2477.
49. Treloar HB, Miller AM, Ray A, Greer CA (2009) Development of the olfactory system. In: The neurobiology of olfaction (Menini A, ed), pp 131-156. Boca Raton, FL: CRC.
50. Vargas G, Lucero MT (1999) Dopamine modulates inwardly rectifying hyperpolarization-activated current (Ih) in cultured rat olfactory receptor neurons. J Neurophysiol 81:149-158.
51. Vasilyev DV, Shan Q, Lee Y, Mayer SC, Bowlby MR, Strassle BW, Kaftan EJ, Rogers KE, Dunlop J (2007) Direct inhibition of Ih by analgesic loperamide in rat DRG neurons. J Neurophysiol 97:3713-3721.
52. Wainger BJ, DeGennaro M, Santoro B, Siegelbaum SA, Tibbs GR (2001) Molecular mechanism of cAMP modulation of HCN pacemaker channels. Nature 411:805-810.
53. Walz A, Mombaerts P, Greer CA, Treloar HB (2006) Disrupted compartmental organization of axons and dendrites within olfactory glomeruli of mice deficient in the olfactory cell adhesion molecule, OCAM. Mol Cell Neurosci 32:1-14. (Pubitemid 43868092)
54. Wang F, Nemes A, Mendelsohn M, Axel R (1998) Odorant receptors govern the formation of a precise topographic map. Cell 93:47-60.
55. Williams DK, Cohan CS (1995) Calcium transients in growth cones and axons of cultured Helisoma neurons in response to conditioning factors. J Neurobiol 27:60-75.
56. Ye B, Nerbonne JM (2009) Proteolytic processing of HCN2 and coassembly with HCN4 in the generation of cardiac pacemaker channels. J Biol Chem 284:25553-25559.
57. Yu CR, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553-566.
58. Zagotta WN, Siegelbaum SA (1996) Structure and function of cyclic nucleotide-gated channels. Annu Rev Neurosci 19:235-263.
59. Zhao H, Reed RR (2001) X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104:651-660.
60. Zheng C, Feinstein P, Bozza T, Rodriguez I, Mombaerts P (2000) Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotide-gated channel subunit. Neuron 26:81-91.
61. Zheng JQ (2000) Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature 403:89-93.
62. Zhou L, Olivier NB, Yao H, Young EC, Siegelbaum SA (2004) A conserved tripeptide in CNG and HCN channels regulates ligand gating by controlling C-terminal oligomerization. Neuron 44:823-834.
63. Zou DJ, Chesler AT, Le Pichon CE, Kuznetsov A, Pei X, Hwang EL, Firestein S (2007) Absence of adenylyl cyclase 3 perturbs peripheral olfactory projections in mice. J Neurosci 27:6675-6683.
64. Zou DJ, Chesler A, Firestein S (2009) How the olfactory bulb got its glomeruli: a just so story. Nat Rev Neurosci 10:611-618.