Voltage-activated ion channels and Ca2+-induced Ca2+ release shape Ca2+ signaling in Merkel cells

Pflugers Archiv European Journal of Physiology

Volumn 457, Issue 1, 2008, Pages 197-209

  Piskorowski, Rebecca ^a   Haeberle, Henry ^a,b   Panditrao, Mayuri V ^a   Lumpkin, Ellen A ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

BK; Ca2+; CICR; Ion channel; Mechanotransduction; Merkel; Touch

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL; CALCIUM ION; POTASSIUM CHANNEL; PROTEIN ANTIBODY;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CALCIUM TRANSPORT; CONTROLLED STUDY; HAIR CELL; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MERKEL CELL; MOUSE; NEWBORN; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKIN; VOLTAGE CLAMP;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CALCIUM; CALCIUM SIGNALING; CELL MEMBRANE; CELL SEPARATION; CHLORIDE CHANNELS; DNA, COMPLEMENTARY; ELECTROPHYSIOLOGY; GREEN FLUORESCENT PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; ION CHANNEL GATING; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MERKEL CELLS; MICE; MICE, TRANSGENIC; PATCH-CLAMP TECHNIQUES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 52549087056     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-008-0496-3     Document Type: Article

References (71)

1. KO Johnson 2001 The roles and functions of cutaneous mechanoreceptors Curr Opin Neurobiol 11 455 461
2. A Iggo AR Muir 1969 The structure and function of a slowly adapting touch corpuscle in hairy skin J Physiol 200 763 796
3. CJ Woodbury HR Koerber 2007 Central and peripheral anatomy of slowly adapting type I low-threshold mechanoreceptors innervating trunk skin of neonatal mice J Comp Neurol 505 547 561
4. Z Halata M Grim KI Bauman 2003 Friedrich Sigmund Merkel and his "Merkel cell", morphology, development, and physiology: review and new results Anat Rec 271A 225 239
5. Y Yamashita H Ogawa K Taniguchi 1986 Differential effects of manganese and magnesium on two types of slowly adapting cutaneous mechanoreceptor afferent units in frogs Pflugers Arch 406 218 224
6. EG Pacitti GS Findlater 1988 Calcium channel blockers and Merkel cells Prog Brain Res 74 37 42
7. SS Senok KI Baumann 1997 Functional evidence for calcium-induced calcium release in isolated rat vibrissal Merkel cell mechanoreceptors J Physiol 500 Pt 1 29 37
8. Y Yamashita N Akaike M Wakamori I Ikeda H Ogawa 1992 Voltage-dependent currents in isolated single Merkel cells of rats J Physiol 450 143 162
9. H Haeberle M Fujiwara J Chuang MM Medina M Panditrao S Bechstedt J Howard EA Lumpkin 2004 Molecular profiling reveals synaptic release machinery in Merkel cells Proc Natl Acad Sci U S A 101 14503 14508
10. T Tachibana M Endoh R Kumakami T Nawa 2003 Immunohistochemical expressions of mGluR5, P2Y2 receptor, PLC-beta1, and IP3R-I and -II in Merkel cells in rat sinus hair follicles Histochem Cell Biol 120 13 21
11. G Sekerkova L Zheng PA Loomis B Changyaleket DS Whitlon E Mugnaini JR Bartles 2004 Espins are multifunctional actin cytoskeletal regulatory proteins in the microvilli of chemosensory and mechanosensory cells J Neurosci 24 5445 5456
12. C Hansel DJ Linden E D'Angelo 2001 Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum Nat Neurosci 4 467 475
13. EA Newman 2001 Propagation of intercellular calcium waves in retinal astrocytes and Muller cells J Neurosci 21 2215 2223
14. 2+ concentrations in intact Merkel cells of an isolated, functioning rat sinus hair preparation Exp Brain Res 108 357 366
15. M Tazaki T Suzuki 1998 Calcium inflow of hamster Merkel cells in response to hyposmotic stimulation indicate a stretch activated ion channel Neurosci Lett 243 69 72
16. 2+ signals in Merkel cells. PLoS ONE 3(3):e1750. DOI 10.1371/journal.pone.0001750
17. EA Lumpkin T Collisson P Parab A Omer-Abdalla H Haeberle P Chen A Doetzlhofer P White A Groves N Segil JE Johnson 2003 Math1-driven GFP expression in the developing nervous system of transgenic mice Gene Expr Patterns 3 389 395
18. M Koltzenburg CL Stucky GR Lewin 1997 Receptive properties of mouse sensory neurons innervating hairy skin J Neurophysiol 78 1841 1850
19. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana, Totowa, NJ, pp 365-386
20. LC Falke KD Gillis DM Pressel S Misler 1989 'Perforated patch recording' allows long-term monitoring of metabolite-induced electrical activity and voltage-dependent Ca2+ currents in pancreatic islet B cells FEBS Lett 251 167 172
21. E Neher 1992 Correction for liquid junction potentials in patch clamp experiments Methods Enzymol 207 123 131
22. Hille B (2001) Ion channels of excitable membranes, 3rd edn. Sinauer, Sunderland, MA
23. AP Fox MC Nowycky RW Tsien 1987 Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones J Physiol 394 149 172
24. WA Kunze JC Bornstein JB Furness R Hendriks DS Stephenson 1994 Charybdotoxin and iberiotoxin but not apamin abolish the slow after-hyperpolarization in myenteric plexus neurons Pflugers Arch 428 300 306
25. JP Ding ZW Li CJ Lingle 1998 Inactivating BK channels in rat chromaffin cells may arise from heteromultimeric assembly of distinct inactivation- competent and noninactivating subunits Biophys J 74 268 289
26. K Ramanathan TH Michael PA Fuchs 2000 beta subunits modulate alternatively spliced, large conductance, calcium-activated potassium channels of avian hair cells J Neurosci 20 1675 1684
27. A Hafidi M Beurg D Dulon 2005 Localization and developmental expression of BK channels in mammalian cochlear hair cells Neuroscience 130 475 484
28. Baumann KI, Senok SS, Chan E, Yung WH (2000) Calcium influx and calcium-induced calcium release in mechanically stimulated Merkel cells of rat sinus hair type I mechanoreceptors. In: Suzuki H, Ono T (eds) Merkel cells, Merkel cell carcinoma and neurobiology of the skin. Elsevier, Amsterdam, pp 73-81
29. JW Xu MM Slaughter 2005 Large-conductance calcium-activated potassium channels facilitate transmitter release in salamander rod synapse J Neurosci 25 7660 7668
30. RS Lewis AJ Hudspeth 1983 Voltage- and ion-dependent conductances in solitary vertebrate hair cells Nature 304 538 541
31. DP Corey JM Dubinsky EA Schwartz 1984 The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina J Physiol 354 557 575
32. PA Fuchs T Nagai MG Evans 1988 Electrical tuning in hair cells isolated from the chick cochlea J Neurosci 8 2460 2467
33. LD Hirning AP Fox EW McCleskey BM Olivera SA Thayer RJ Miller RW Tsien 1988 Dominant role of N-type Ca2+ channels in evoked release of norepinephrine from sympathetic neurons Science 239 57 61
34. CA Reid JM Bekkers JD Clements 2003 Presynaptic Ca2+ channels: a functional patchwork Trends Neurosci 26 683 687
35. BM Fagan PM Cahusac 2001 Evidence for glutamate receptor mediated transmission at mechanoreceptors in the skin Neuroreport 12 341 347
36. L He RP Tuckett KB English 2003 5-HT2 and 3 receptor antagonists suppress the response of rat type I slowly adapting mechanoreceptor: an in vitro study Brain Res 969 230 236
37. PM Cahusac SS Senok IS Hitchcock PG Genever KI Baumann 2005 Are unconventional NMDA receptors involved in slowly adapting type I mechanoreceptor responses Neuroscience 133 763 773
38. PG Gillespie RG Walker 2001 Molecular basis of mechanosensory transduction Nature 413 194 202
39. LJ Drew JN Wood P Cesare 2002 Distinct mechanosensitive properties of capsaicin-sensitive and -insensitive sensory neurons J Neurosci 22 RC228
40. A Lelli P Perin M Martini CD Ciubotaru I Prigioni P Valli ML Rossi F Mammano 2003 Presynaptic calcium stores modulate afferent release in vestibular hair cells J Neurosci 23 6894 6903
41. AE Chavez JH Singer JS Diamond 2006 Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors Nature 443 705 708
42. A Suryanarayanan MM Slaughter 2006 Synaptic transmission mediated by internal calcium stores in rod photoreceptors J Neurosci 26 1759 1766
43. KM Cronk GA Wilkinson R Grimes EF Wheeler S Jhaveri BT Fundin I Silos-Santiago L Tessarollo LF Reichardt FL Rice 2002 Diverse dependencies of developing Merkel innervation on the trkA and both full-length and truncated isoforms of trkC Development 129 3739 3750
44. JJ Art R Fettiplace 1987 Variation of membrane properties in hair cells isolated from the turtle cochlea J Physiol 385 207 242
45. SJ Pyott E Glowatzki JS Trimmer RW Aldrich 2004 Extrasynaptic localization of inactivating calcium-activated potassium channels in mouse inner hair cells J Neurosci 24 9469 9474
46. CR Solaro M Prakriya JP Ding CJ Lingle 1995 Inactivating and noninactivating Ca(2+)- and voltage-dependent K+ current in rat adrenal chromaffin cells J Neurosci 15 6110 6123
47. P Langer S Grunder A Rusch 2003 Expression of Ca2+-activated BK channel mRNA and its splice variants in the rat cochlea J Comp Neurol 455 198 209
48. KP Rosenblatt ZP Sun S Heller AJ Hudspeth 1997 Distribution of Ca2+-activated K+ channel isoforms along the tonotopic gradient of the chicken's cochlea Neuron 19 1061 1075
49. DS Navaratnam TJ Bell TD Tu EL Cohen JC Oberholtzer 1997 Differential distribution of Ca2+-activated K+ channel splice variants among hair cells along the tonotopic axis of the chick cochlea Neuron 19 1077 1085
50. ML Andermann J Ritt MA Neimark CI Moore 2004 Neural correlates of vibrissa resonance; band-pass and somatotopic representation of high-frequency stimuli Neuron 42 451 463
51. PA Fuchs MG Evans 1990 Potassium currents in hair cells isolated from the cochlea of the chick J Physiol 429 529 551
52. K Ramanathan TH Michael GJ Jiang H Hiel PA Fuchs 1999 A molecular mechanism for electrical tuning of cochlear hair cells Science 283 215 217
53. M Beurg A Hafidi LJ Skinner J Ruel R Nouvian M Henaff JL Puel JM Aran D Dulon 2005 Ryanodine receptors and BK channels act as a presynaptic depressor of neurotransmission in cochlear inner hair cells Eur J Neurosci 22 1109 1119
54. ZW Wang O Saifee ML Nonet L Salkoff 2001 SLO-1 potassium channels control quantal content of neurotransmitter release at the C. elegans neuromuscular junction Neuron 32 867 881
55. W Greffrath W Magerl U Disque-Kaiser E Martin S Reuss G Boehmer 2004 Contribution of Ca2+-activated K+ channels to hyperpolarizing after-potentials and discharge pattern in rat supraoptic neurones J Neuroendocrinol 16 577 588
56. M Sausbier H Hu C Arntz S Feil S Kamm H Adelsberger U Sausbier CA Sailer R Feil F Hofmann M Korth MJ Shipston HG Knaus DP Wolfer CM Pedroarena JF Storm P Ruth 2004 Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2+-activated K+ channel deficiency Proc Natl Acad Sci U S A 101 9474 9478
57. G Raffaelli C Saviane MH Mohajerani P Pedarzani E Cherubini 2004 BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus J Physiol 557 147 157
58. GV Petkov AD Bonev TJ Heppner R Brenner RW Aldrich MT Nelson 2001 Beta1-subunit of the Ca2+-activated K+ channel regulates contractile activity of mouse urinary bladder smooth muscle J Physiol 537 443 452
59. ME Werner P Zvara AL Meredith RW Aldrich MT Nelson 2005 Erectile dysfunction in mice lacking the large-conductance calcium-activated potassium (BK) channel J Physiol 567 545 556
60. KS Thorneloe AL Meredith AM Knorn RW Aldrich MT Nelson 2005 Urodynamic properties and neurotransmitter dependence of urinary bladder contractility in the BK channel deletion model of overactive bladder Am J Physiol Renal Physiol 289 F604 F610
61. AL Meredith KS Thorneloe ME Werner MT Nelson RW Aldrich 2004 Overactive bladder and incontinence in the absence of the BK large conductance Ca2+-activated K+ channel J Biol Chem 279 36746 36752
62. N Harada A Ernst HP Zenner 1994 Intracellular calcium changes by hyposmotic activation of cochlear outer hair cells in the guinea pig Acta Otolaryngol 114 510 515
63. N Alessandri-Haber JJ Yeh AE Boyd CA Parada X Chen DB Reichling JD Levine 2003 Hypotonicity induces TRPV4-mediated nociception in rat Neuron 39 497 511
64. J Kim YD Chung DY Park S Choi DW Shin H Soh HW Lee W Son J Yim CS Park MJ Kernan C Kim 2003 A TRPV family ion channel required for hearing in Drosophila Nature 424 81 84
65. Z Gong W Son YD Chung J Kim DW Shin CA McClung Y Lee HW Lee DJ Chang BK Kaang H Cho U Oh J Hirsh MJ Kernan C Kim 2004 Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila J Neurosci 24 9059 9066
66. JM Pattillo B Yazejian DA DiGregorio JL Vergara AD Grinnell SD Meriney 2001 Contribution of presynaptic calcium-activated potassium currents to transmitter release regulation in cultured Xenopus nerve-muscle synapses Neuroscience 102 229 240
67. LJ Skinner V Enee M Beurg HH Jung AF Ryan A Hafidi JM Aran D Dulon 2003 Contribution of BK Ca2+-activated K+ channels to auditory neurotransmission in the Guinea pig cochlea J Neurophysiol 90 320 332
68. L Warbington T Hillman C Adams M Stern 1996 Reduced transmitter release conferred by mutations in the slowpoke-encoded Ca2(+)-activated K+ channel gene of Drosophila Invert Neurosci 2 51 60
69. MJ Berridge MD Bootman HL Roderick 2003 Calcium signalling: dynamics, homeostasis and remodelling Nat Rev Mol Cell Biol 4 517 529
70. M Weskamp W Seidl S Grissmer 2000 Characterization of the increase in [Ca(2+)](i) during hypotonic shock and the involvement of Ca(2+)-activated K(+) channels in the regulatory volume decrease in human osteoblast-like cells J Membr Biol 178 11 20
71. M Jakab M Ritter 2006 Cell volume regulatory ion transport in the regulation of cell migration Contrib Nephrol 152 161 180