A method for measuring electrical signals in a primary cilium

Cilia

Volumn 1, Issue , 2012, Pages

  Kleene, Nancy K ^a   Kleene, Steven J ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL ADHESION; CELL GROWTH; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; ELECTRIC POTENTIAL; ELECTRIC RESISTANCE; EUKARYOTIC FLAGELLUM; INTRACELLULAR RECORDING; INTRACELLULAR SIGNALING; MICROELECTRODE; MOUSE; NONHUMAN; PRIMARY CILIUM; PRIORITY JOURNAL; SECOND MESSENGER; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION;

EID: 84890345685     PISSN: None     EISSN: 20462530     Source Type: Journal    
DOI: 10.1186/2046-2530-1-17     Document Type: Article

References (71)

1. Wheatley DN, Wang AM, Strugnell GE. Expression of primary cilia in mammalian cells. Cell Biol Int 1996, 20:73-81. 10.1006/cbir.1996.0011, 8936410.
2. Veland IR, Awan A, Pedersen LB, Yoder BK, Christensen ST. Primary cilia and signaling pathways in mammalian development, health and disease. Nephron Physiol 2009, 111:39-53.
3. Lancaster MA, Gleeson JG. The primary cilium as a cellular signaling center: lessons from disease. Curr Opin Genet Dev 2009, 19:220-229. 10.1016/j.gde.2009.04.008, 2953615, 19477114.
4. Louvi A, Grove EA. Cilia in the CNS: the quiet organelle claims center stage. Neuron 2011, 69:1046-1060. 10.1016/j.neuron.2011.03.002, 3070490, 21435552.
5. Ware SM, Aygun MG, Hildebrandt F. Spectrum of clinical diseases caused by disorders of primary cilia. Proc Am Thorac Soc 2011, 8:444-450. 10.1513/pats.201103-025SD, 3209578, 21926397.
6. Gascue C, Katsanis N, Badano JL. Cystic diseases of the kidney: ciliary dysfunction and cystogenic mechanisms. Pediatr Nephrol 2011, 26:1181-1195. 10.1007/s00467-010-1697-5, 21113628.
7. Pazour GJ, Witman GB. The vertebrate primary cilium is a sensory organelle. Curr Opin Cell Biol 2003, 15:105-110. 10.1016/S0955-0674(02)00012-1, 12517711.
8. Gradilone SA, Masyuk AI, Splinter PL, Banales JM, Huang BQ, Tietz PS, Masyuk TV, LaRusso NF. Cholangiocyte cilia express TRPV4 and detect changes in luminal tonicity inducing bicarbonate secretion. Proc Natl Acad Sci USA 2007, 104:19138-19143. 10.1073/pnas.0705964104, 2141921, 18024594.
9. Moorman SJ, Shorr AZ. The primary cilium as a gravitational force transducer and a regulator of transcriptional noise. Dev Dyn 2008, 237:1955-1959. 10.1002/dvdy.21493, 18366139.
10. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK. The primary cilium as a complex signaling center. Curr Biol 2009, 19:R526-R535. 10.1016/j.cub.2009.05.025, 2814769, 19602418.
11. Satir P, Pedersen LB, Christensen ST. The primary cilium at a glance. J Cell Sci 2010, 123:499-503. 10.1242/jcs.050377, 2818190, 20144997.
12. Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AEH, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 2003, 33:129-137. 10.1038/ng1076, 12514735.
13. Raychowdhury MK, Ramos AJ, Zhang P, McLaughin M, Dai X-Q, Chen X-Z, Montalbetti N, Cantero MDR, Ausiello DA, Cantiello HF. Vasopressin receptor-mediated functional signaling pathway in primary cilia of renal epithelial cells. Am J Physiol 2009, 296:F87-F97.
14. Pazour GJ, San Agustin JT, Follit JA, Rosenbaum JL, Witman GB. Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Curr Biol 2002, 12:R378-R380. 10.1016/S0960-9822(02)00877-1, 12062067.
15. Yoder BK, Hou X, Guay-Woodford LM. The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. J Am Soc Nephrol 2002, 13:2508-2516. 10.1097/01.ASN.0000029587.47950.25, 12239239.
16. Raychowdhury MK, McLaughlin M, Ramos AJ, Montalbetti N, Bouley R, Ausiello DA, Cantiello HF. Characterization of single channel currents from primary cilia of renal epithelial cells. J Biol Chem 2005, 280:34718-34722. 10.1074/jbc.M507793200, 16079132.
17. Bai C-X, Giamarchi A, Rodat-Despoix L, Padilla F, Downs T, Tsiokas L, Delmas P. Formation of a new receptor-operated channel by heteromeric assembly of TRPP2 and TRPC1 subunits. EMBO Rep 2008, 9:472-479. 10.1038/embor.2008.29, 2373364, 18323855.
18. Köttgen M, Buchholz B, Garcia-Gonzalez MA, Kotsis F, Fu X, Doerken M, Boehlke C, Steffl D, Tauber R, Wegierski T, Nitschke R, Suzuki M, Kramer-Zucker A, Germino GG, Watnick T, Prenen J, Nilius B, Kuehn EW, Walz G. TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol 2008, 182:437-447. 10.1083/jcb.200805124, 2500130, 18695040.
19. Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, Tilly JL, Clapham DE. A sperm ion channel required for sperm motility and male fertility. Nature 2001, 413:603-609. 10.1038/35098027, 11595941.
20. Fujiu K, Nakayama Y, Yanagisawa A, Sokabe M, Yoshimura K. Chlamydomonas CAV2 encodes a voltage-dependent calcium channel required for the flagellar waveform conversion. Curr Biol 2009, 19:133-139. 10.1016/j.cub.2008.11.068, 19167228.
21. Biel M, Michalakis S. Cyclic nucleotide-gated channels. Handb Exp Pharmacol 2009, 191:111-136.
22. Nakamura T, Gold GH. A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 1987, 325:442-444. 10.1038/325442a0, 3027574.
23. Kleene SJ. Origin of the chloride current in olfactory transduction. Neuron 1993, 11:123-132. 10.1016/0896-6273(93)90276-W, 8393322.
24. Inglis PN, Boroevich KA, Leroux MR. Piecing together a ciliome. Trends Genet 2006, 22:491-500. 10.1016/j.tig.2006.07.006, 16860433.
25. Gherman A, Davis EE, Katsanis N. The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat Genet 2006, 38:961-962. 10.1038/ng0906-961, 16940995.
26. Li G, Vega R, Nelms K, Gekakis N, Goodnow C, McNamara P, Wu H, Hong NA, Glynne R. A role for Alström syndrome protein, alms1, in kidney ciliogenesis and cellular quiescence. PLoS Genet 2007, 3:e8. 10.1371/journal.pgen.0030008, 1761047, 17206865.
27. Arnaiz O, Malinowska A, Klotz C, Sperling L, Dadlez M, Koll F, Cohen J. Cildb: a knowledgebase for centrosomes and cilia. Database (Oxford) 2009, 2009:bap022.
28. Praetorius HA, Spring KR. Removal of the MDCK cell primary cilium abolishes flow sensing. J Membr Biol 2003, 191:69-76. 10.1007/s00232-002-1042-4, 12532278.
29. Hanaoka K, Qian F, Boletta A, Bhunia AK, Piontek K, Tsiokas L, Sukhatme VP, Guggino WB, Germino GG. Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 2000, 408:990-994. 10.1038/35050128, 11140688.
30. González-Perrett S, Kim K, Ibarra C, Damiano AE, Zotta E, Batelli M, Harris PC, Reisin IL, Arnaout MA, Cantiello HF. Polycystin-2, the protein mutated in autosomal dominant polycystic kidney disease (ADPKD), is a Ca2+-permeable nonselective cation channel. Proc Natl Acad Sci USA 2001, 98:1182-1187. 10.1073/pnas.98.3.1182, 14729, 11252306.
31. Vassilev PM, Guo L, Chen X-Z, Segal Y, Peng J-B, Basora N, Babakhanlou H, Cruger G, Kanazirska M, Ye C-P, Brown EM, Hediger MA, Zhou J. Polycystin-2 is a novel cation channel implicated in defective intracellular Ca2+ homeostasis in polycystic kidney disease. Biochem Biophys Res Commun 2001, 282:341-350. 10.1006/bbrc.2001.4554, 11264013.
32. Luo Y, Vassilev PM, Li X, Kawanabe Y, Zhou J. Native polycystin 2 functions as a plasma membrane Ca2+-permeable cation channel in renal epithelia. Mol Cell Biol 2003, 23:2600-2607. 10.1128/MCB.23.7.2600-2607.2003, 150742, 12640140.
33. Delmas P, Nauli SM, Li X, Coste B, Osorio N, Crest M, Brown DA, Zhou J. Gating of the polycystin ion channel signaling complex in neurons and kidney cells. FASEB J 2004, 18:740-742.
34. Koulen P, Cai Y, Geng L, Maeda Y, Nishimura S, Witzgall R, Ehrlich BE, Somlo S. Polycystin-2 is an intracellular calcium release channel. Nat Cell Biol 2002, 4:191-197. 10.1038/ncb754, 11854751.
35. Cantiello HF. Regulation of calcium signaling by polycystin-2. Am J Physiol 2004, 286:F1012-F1029.
36. Tsiokas L, Kim S, Ong E-C. Cell biology of polycystin-2. Cell Signal 2007, 19:444-453. 10.1016/j.cellsig.2006.09.005, 1817723, 17084592.
37. Witzgall R. TRPP2 channel regulation. Handb Exp Pharmacol 2007, 179:363-375. 10.1007/978-3-540-34891-7_22, 17217069.
38. Kleene SJ, Gesteland RC. Transmembrane currents in frog olfactory cilia. J Membr Biol 1991, 120:75-81. 10.1007/BF01868593, 1850487.
39. Rauchman MI, Nigam SK, Delpire E, Gullans SR. An osmotically tolerant inner medullary collecting duct cell line from an SV40 transgenic mouse. Am J Physiol 1993, 265:F416-F424.
40. Kleene SJ. Patch-clamping of whole olfactory cilia 1995, 347-352. CRC Press, Boca Raton, FL, Spielman AI, Brand JG.
41. Barnes BG. Ciliated secretory cells in the pars distalis of the mouse hypophysis. J Ultrastruc Res 1961, 5:453-467.
42. Takeuchi H, Kurahashi T. Distribution, amplification, and summation of cyclic nucleotide sensitivities within single olfactory sensory cilia. J Neurosci 2008, 28:766-775. 10.1523/JNEUROSCI.3531-07.2008, 18199776.
43. LeDizet M, Piperno G. Detection of acetylated α-tubulin by specific antibodies. Meth Enzymol 1991, 196:264-274.
44. Zhou J. Polycystins and primary cilia: primers for cell cycle progression. Annu Rev Physiol 2009, 71:83-113. 10.1146/annurev.physiol.70.113006.100621, 19572811.
45. Rossetti S, Consugar MB, Chapman AB, Torres VE, Guay-Woodford LM, Grantham JJ, Bennett WM, Meyers CM, Walker DL, Bae K, Zhang Q, Thompson PA, Miller JP, Harris PC, the CRISP Consortium Comprehensive molecular diagnostics in autosomal dominant polycystic kidney disease. J Am Soc Nephrol 2007, 18:2143-2160. 10.1681/ASN.2006121387, 17582161, the CRISP Consortium.
46. Tsiokas L, Kim E, Arnould T, Sukhatme VP, Walz G. Homo- and heterodimeric interactions between the gene products of PKD1 and PKD2. Proc Natl Acad Sci USA 1997, 94:6965-6970. 10.1073/pnas.94.13.6965, 21268, 9192675.
47. Qian F, Germino FJ, Cai Y, Zhang X, Somlo S, Germino GG. PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat Genet 1997, 16:179-183. 10.1038/ng0697-179, 9171830.
48. Roth KE, Rieder CL, Bowser SS. Flexible-substratum technique for viewing cells from the side: some in vivo properties of primary (9 + 0) cilia in cultured kidney epithelia. J Cell Sci 1988, 89:457-466.
49. Suchyna TM, Markin VS, Sachs F. Biophysics and structure of the patch and the gigaseal. Biophys J 2009, 97:738-747. 10.1016/j.bpj.2009.05.018, 2718145, 19651032.
50. Kleene SJ. Basal conductance of frog olfactory cilia. Pflugers Arch 1992, 421:374-380. 10.1007/BF00374226, 1408661.
51. Dovichi NJ, Hu S, Michels D, Mao D, Dambrowitz A. Single cell proteomics 2009, 69-89. WILEY-VCH Verlag GmbH & Co, Weinheim, Germany, Anselmetti D.
52. Mitchell KAP, Szabo G, Otero AS. Methods for the isolation of sensory and primary cilia-an overview. Methods Cell Biol 2009, 94:87-101.
53. Low SH, Vasanth S, Larson CH, Mukherjee S, Sharma N, Kinter MT, Kane ME, Obara T, Weimbs T. Polycystin-1, STAT6, and P100 function in a pathway that transduces ciliary mechanosensation and is activated in polycystic kidney disease. Dev Cell 2006, 10:57-69. 10.1016/j.devcel.2005.12.005, 16399078.
54. Domire JS, Green JA, Lee KG, Johnson AD, Askwith CC, Mykytyn K. Dopamine receptor 1 localizes to neuronal cilia in a dynamic process that requires the Bardet-Biedl syndrome proteins. Cell Mol Life Sci 2011, 68:2951-2960. 10.1007/s00018-010-0603-4, 3368249, 21152952.
55. Schneider L, Clement CA, Teilmann SC, Pazour GJ, Hoffmann EK, Satir P, Christensen ST. PDGFRαα signaling is regulated through the primary cilium in fibroblasts. Curr Biol 2005, 15:1861-1866. 10.1016/j.cub.2005.09.012, 16243034.
56. Praetorius HA, Spring KR. Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 2001, 184:71-79. 10.1007/s00232-001-0075-4, 11687880.
57. Ma R, Li W-P, Rundle D, Kong J, Akbarali HI, Tsiokas L. PKD2 functions as an epidermal growth factor-activated plasma membrane channel. Mol Cell Biol 2005, 25:8285-8298. 10.1128/MCB.25.18.8285-8298.2005, 1234340, 16135816.
58. González-Perrett S, Batelli M, Kim K, Essafi M, Timpanaro G, Moltabetti N, Reisin IL, Arnaout MA, Cantiello HF. Voltage dependence and pH regulation of human polycystin-2-mediated cation channel activity. J Biol Chem 2002, 277:24959-24966. 10.1074/jbc.M105084200, 11991947.
59. McGrath J, Somlo S, Makova S, Tian X, Brueckner M. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 2003, 114:61-73. 10.1016/S0092-8674(03)00511-7, 12859898.
60. Teilmann SC, Byskov AG, Pedersen PA, Wheatley DN, Pazour GJ, Christensen ST. Localization of transient receptor potential ion channels in primary and motile cilia of the female murine reproductive organs. Mol Reprod Dev 2005, 71:444-452. 10.1002/mrd.20312, 15858826.
61. Masyuk AI, Masyuk TV, Splinter PL, Huang BQ, Stroope AJ, LaRusso NF. Cholangiocyte cilia detect changes in luminal fluid flow and transmit them into intracellular Ca2+ and cAMP signaling. Gastroenterology 2006, 131:911-920. 10.1053/j.gastro.2006.07.003, 1866168, 16952559.
62. Lu CJ, Du H, Wu J, Jansen DA, Jordan KL, Xu N, Sieck GC, Qian Q. Non-random distribution and sensory functions of primary cilia in vascular smooth muscle cells. Kidney Blood Press Res 2008, 31:171-184. 10.1159/000132462, 2814154, 18483460.
63. AbouAlaiwi WA, Takahashi M, Mell BR, Jones TJ, Ratnam S, Kolb RJ, Nauli SM. Ciliary polycystin-2 is a mechanosensitive calcium channel involved in nitric oxide signaling cascades. Circ Res 2009, 104:860-869. 10.1161/CIRCRESAHA.108.192765, 3085025, 19265036.
64. Berbari NF, Johnson AD, Lewis JS, Askwith CC, Mykytyn K. Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors. Mol Biol Cell 2008, 19:1540-1547. 10.1091/mbc.E07-09-0942, 2291422, 18256283.
65. Eberle AN, Mild G, Zumsteg U. Cellular models for the study of the pharmacology and signaling of melanin-concentrating hormone receptors. J Recept Signal Transduct Res 2010, 30:385-402. 10.3109/10799893.2010.524223, 21083507.
66. Tao B, Bu S, Yang Z, Siroky B, Kappes JC, Kispert A, Guay-Woodford LM. Cystin localizes to primary cilia via membrane microdomains and a targeting motif. J Am Soc Nephrol 2009, 20:2570-2580. 10.1681/ASN.2009020188, 2794227, 19850956.
67. Jenkins PM, Hurd TW, Zhang L, McEwen DP, Brown RL, Margolis B, Verhey KJ, Martens JR. Ciliary targeting of olfactory CNG channels requires the CNGB1b subunit and the kinesin-2 motor protein, KIF17. Curr Biol 2006, 16:1211-1216. 10.1016/j.cub.2006.04.034, 16782012.
68. Domire JS, Mykytyn K. Markers for neuronal cilia. Methods Cell Biol 2009, 91:111-121.
69. Marley A, von Zastrow M. DISC1 regulates primary cilia that display specific dopamine receptors. PLoS One 2010, 5:e10902. 10.1371/journal.pone.0010902, 2878344, 20531939.
70. Rabito CA. Occluding junctions in a renal cell line (LLC-PK1) with characteristics of proximal tubular cells. Am J Physiol 1986, 250:F734-F743.
71. Volk KA, Sigmund RD, Snyder PM, McDonald FJ, Welsh MJ, Stokes JB. rENaC is the predominant Na+ channel in the apical membrane of the rat renal inner medullary collecting duct. J Clin Invest 1995, 96:2748-2757. 10.1172/JCI118344, 185984, 8675644.