The Primary cilium calcium channels and their role in flow sensing

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 1, 2015, Pages 157-165

  Patel, Amanda ^a  

^a Laboratory of Excellence in Ion Channel Science and Therapeutics   (France)

Author keywords

Ca2+ channels; Flow sensing; Polycystic kidney disease; Polycystins; Primary cilium

Indexed keywords

CALCIUM CHANNEL; POLYCYSTIN; POLYCYSTIN 1; POLYCYSTIN 2; SONIC HEDGEHOG PROTEIN; CALCIUM;

CELL ORGANELLE; EUKARYOTIC FLAGELLUM; FLOW KINETICS; FLOW SENSING; GENE MUTATION; HUMAN; KIDNEY CYST; KIDNEY POLYCYSTIC DISEASE; MOLECULAR PHYLOGENY; NONHUMAN; PATCH CLAMP TECHNIQUE; PROTEIN FUNCTION; RECORDING; REVIEW; ANIMAL; BIOLOGICAL MODEL; BODY FLUID; CHANNEL GATING; KIDNEY TUBULE; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; MICROFLUIDICS; MOUSE; PHYSIOLOGY; PROCEDURES; SHEAR STRENGTH;

ANIMALS; BODY FLUIDS; CALCIUM; CALCIUM CHANNELS; CILIA; HUMANS; ION CHANNEL GATING; KIDNEY TUBULES; MECHANOTRANSDUCTION, CELLULAR; MICE; MICROFLUIDICS; MODELS, BIOLOGICAL; SHEAR STRENGTH; STRESS, MECHANICAL;

EID: 84920083456     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1516-0     Document Type: Review

References (77)

1. AbouAlaiwi WA, Takahashi M, Mell BR, Jones TJ, Ratnam S, Kolb RJ, Nauli SM (2009) Ciliary polycystin-2 is a mechanosensitive calcium channel involved in nitric oxide signaling cascades. Circ Res 104:860–869. doi:10.1161/CIRCRESAHA.108.192765
2. Bai C, Giamarchi A, Rodat-Despoix L, Padilla F, Downs T, Tsiokas L, Delmas P (2008) Formation of a novel receptor-operated channel by heteromeric assembly of TRPP2 and TRPC1 subunits. EMBO Rep 9:472–479
3. Barr MM, DeModena J, Braun D, Nguyen CQ, Hall DH, Sternberg PW (2001) The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Curr Biol 11:1341–1346
4. Barr MM, Sternberg PW (1999) A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401:386–389
5. Cai Y, Maeda Y, Cedzich A, Torres VE, Wu G, Hayashi T, Mochizuki T, Park JH, Witzgall R, Somlo S (1999) Identification and characterization of polycystin-2, the PKD2 gene product. J Biol Chem 274:28557–28565
6. Coste B, Mathur J, Schmidt M, Earley TJ, Ranade S, Petrus MJ, Dubin AE, Patapoutian A (2010) Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330:55–60. doi:10.1126/science.1193270
7. DeCaen PG, Delling M, Vien TN, Clapham DE (2013) Direct recording and molecular identification of the calcium channel of primary cilia. Nature 504:315–318. doi:10.1038/nature12832
8. Delling M, DeCaen PG, Doerner JF, Febvay S, Clapham DE (2013) Primary cilia are specialized calcium signalling organelles. Nature 504:311–314. doi:10.1038/nature12833
9. Delmas P, Nauli SM, Li X, Coste B, Osorio N, Crest M, Brown DA, Zhou J (2004) Gating of the polycystin ion channel signaling complex in neurons and kidney cells. FASEB J 18:740–742
10. Eisenhoffer GT, Loftus PD, Yoshigi M, Otsuna H, Chien CB, Morcos PA, Rosenblatt J (2012) Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 484:546–549. doi:10.1038/nature10999
11. Field S, Riley KL, Grimes DT, Hilton H, Simon M, Powles-Glover N, Siggers P, Bogani D, Greenfield A, Norris DP (2011) Pkd1l1 establishes left-right asymmetry and physically interacts with Pkd2. Development 138:1131–1142. doi:10.1242/dev.058149
12. Foggensteiner L, Bevan AP, Thomas R, Coleman N, Boulter C, Bradley J, Ibraghimov-Beskrovnaya O, Klinger K, Sandford R (2000) Cellular and subcellular distribution of polycystin-2, the protein product of the PKD2 gene. J Am Soc Nephrol 11:814–827
13. Geng L, Okuhara D, Yu Z, Tian X, Cai Y, Shibazaki S, Somlo S (2006) Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. J Cell Sci 119:1383–1395
14. Geng L, Segal Y, Pavlova A, Barros EJ, Lohning C, Lu W, Nigam SK, Frischauf AM, Reeders ST, Zhou J (1997) Distribution and developmentally regulated expression of murine polycystin. Am J Physiol 272:F451–459
15. Geng L, Segal Y, Peissel B, Deng N, Pei Y, Carone F, Rennke HG, Glucksmann-Kuis AM, Schneider MC, Ericsson M, Reeders ST, Zhou J (1996) Identification and localization of polycystin, the PKD1 gene product. J Clin Invest 98:2674–2682. doi:10.1172/JCI119090
16. Gherman A, Davis EE, Katsanis N (2006) The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat Genet 38:961–962. doi:10.1038/ng0906-961
17. Gonzalez-Perrett S, Kim K, Ibarra C, Damiano AE, Zotta E, Batelli M, Harris PC, Reisin IL, Arnaout MA, Cantiello HF (2001) Polycystin-2, the protein mutated in autosomal dominant polycystic kidney disease (ADPKD), is a Ca2+-permeable nonselective cation channel. Proc Natl Acad Sci U S A 98:1182–1187
18. Guo L, Chen M, Basora N, Zhou J (2000) The human polycystic kidney disease 2-like (PKDL) gene: exon/intron structure and evidence for a novel splicing mechanism. Mamm Genome 11:46–50
19. Hanaoka K, Qian F, Boletta A, Bhunia AK, Piontek K, Tsiokas L, Sukhatme VP, Guggino WB, Germino GG (2000) Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 408:990–994
20. Harris PC, Torres VE (2009) Polycystic kidney disease. Annu Rev Med 60:321–337
21. Hildebrandt F, Benzing T, Katsanis N (2011) Ciliopathies. N Engl J Med 364:1533–1543. doi:10.1056/NEJMra1010172
22. Huan Y, van Adelsberg J (1999) Polycystin-1, the PKD1 gene product, is in a complex containing E-cadherin and the catenins. J Clin Invest 104:1459–1468
23. Hughes J, Ward CJ, Aspinwall R, Butler R, Harris PC (1999) Identification of a human homologue of the sea urchin receptor for egg jelly: a polycystic kidney disease-like protein. Hum Mol Genet 8:543–549
24. Hughes J, Ward CJ, Peral B, Aspinwall R, Clark K, San Millan JL, Gamble V, Harris PC (1995) The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat Genet 10:151–160
25. Irigoin F, Badano JL (2011) Keeping the balance between proliferation and differentiation: the primary cilium. Curr Genomics 12:285–297. doi:10.2174/138920211795860134
26. Ishikawa H, Thompson J, Yates JR 3rd, Marshall WF (2012) Proteomic analysis of mammalian primary cilia. Curr Biol 22:414–419. doi:10.1016/j.cub.2012.01.031
27. Karcher C, Fischer A, Schweickert A, Bitzer E, Horie S, Witzgall R, Blum M (2005) Lack of a laterality phenotype in Pkd1 knock-out embryos correlates with absence of polycystin-1 in nodal cilia. Differentiation 73:425–432. doi:10.1111/j.1432-0436.2005.00048.x
28. Ko JY, Park JH (2013) Mouse models of polycystic kidney disease induced by defects of ciliary proteins. BMB Rep 46:73–79
29. Kottgen 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 (2008) TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol 182:437–447
30. Koulen P, Cai Y, Geng L, Maeda Y, Nishimura S, Witzgall R, Ehrlich BE, Somlo S (2002) Polycystin-2 is an intracellular calcium release channel. Nat Cell Biol 4:191–197
31. Lee H, Iida T, Mizuno A, Suzuki M, Caterina MJ (2005) Altered thermal selection behavior in mice lacking transient receptor potential vanilloid 4. J Neurosci 25:1304–1310. doi:10.1523/JNEUROSCI.4745.04.2005
32. Li A, Tian X, Sung SW, Somlo S (2003) Identification of two novel polycystic kidney disease-1-like genes in human and mouse genomes. Genomics 81:596–608
33. Liedtke W, Tobin DM, Bargmann CI, Friedman JM (2003) Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proc Natl Acad Sci U S A 100(Suppl 2):14531–14536
34. Luo Y, Vassilev PM, Li X, Kawanabe Y, Zhou J (2003) Native polycystin 2 functions as a plasma membrane Ca2+s-permeable cation channel in renal epithelia. Mol Cell Biol 23:2600–2607
35. Ma M, Tian X, Igarashi P, Pazour GJ, Somlo S (2013) Loss of cilia suppresses cyst growth in genetic models of autosomal dominant polycystic kidney disease. Nat Genet 45:1004–1012. doi:10.1038/ng.2715
36. McGrath J, Somlo S, Makova S, Tian X, Brueckner M (2003) Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114:61–73
37. Mizuno A, Matsumoto N, Imai M, Suzuki M (2003) Impaired osmotic sensation in mice lacking TRPV4. Am J Physiol Cell Physiol 285:C96–101. doi:10.1152/ajpcell.00559.2002
38. Mochizuki T, Wu G, Hayashi T, Xenophontos SL, Veldhuisen B, Saris JJ, Reynolds DM, Cai Y, Gabow PA, Pierides A, Kimberling WJ, Breuning MH, Deltas CC, Peters DJ, Somlo S (1996) PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 272:1339–1342
39. Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33:129–137
40. Nauli SM, Kawanabe Y, Kaminski JJ, Pearce WJ, Ingber DE, Zhou J (2008) Endothelial cilia are fluid shear sensors that regulate calcium signaling and nitric oxide production through polycystin-1. Circulation 117:1161–1171
41. Newby LJ, Streets AJ, Zhao Y, Harris PC, Ward CJ, Ong AC (2002) Identification, characterization, and localization of a novel kidney polycystin-1-polycystin-2 complex. J Biol Chem 277:20763–20773
42. Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, Kanai Y, Kido M, Hirokawa N (1998) Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95:829–837
43. Obermuller N, Gallagher AR, Cai Y, Gassler N, Gretz N, Somlo S, Witzgall R (1999) The rat pkd2 protein assumes distinct subcellular distributions in different organs. Am J Physiol 277:F914–925
44. Ong AC, Harris PC (2005) Molecular pathogenesis of ADPKD: the polycystin complex gets complex. Kidney Int 67:1234–1247. doi:10.1111/j.1523-1755.2005.00201.x
45. Pazour GJ, Bloodgood RA (2008) Targeting proteins to the ciliary membrane. Curr Top Dev Biol 85:115–149. doi:10.1016/S0070-2153(08)00805-3
46. Pazour GJ, San Agustin JT, Follit JA, Rosenbaum JL, Witman GB (2002) Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Curr Biol 12:R378–380
47. Pennekamp P, Karcher C, Fischer A, Schweickert A, Skryabin B, Horst J, Blum M, Dworniczak B (2002) The ion channel polycystin-2 is required for left-right axis determination in mice. Curr Biol 12:938–943
48. Peyronnet R, Martins JR, Duprat F, Demolombe S, Arhatte M, Jodar M, Tauc M, Duranton C, Paulais M, Teulon J, Honore E, Patel A (2013) Piezo1-dependent stretch-activated channels are inhibited by Polycystin-2 in renal tubular epithelial cells. EMBO Rep 14:1143–1148. doi:10.1038/embor.2013.170
49. Peyronnet R, Sharif-Naeini R, Folgering JH, Arhatte M, Jodar M, El Boustany C, Gallian C, Tauc M, Duranton C, Rubera I, Lesage F, Pei Y, Peters DJ, Somlo S, Sachs F, Patel A, Honore E, Duprat F (2012) Mechanoprotection by polycystins against apoptosis is mediated through the opening of stretch-activated K(2P) Channels. Cell Rep 1:241–250. doi:10.1016/j.celrep.2012.01.006
50. Plotnikova OV, Pugacheva EN, Golemis EA (2011) Aurora A kinase activity influences calcium signaling in kidney cells. J Cell Biol 193:1021–1032. doi:10.1083/jcb.201012061
51. Praetorius HA, Spring KR (2001) Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 184:71–79
52. Praetorius HA, Spring KR (2003) Removal of the MDCK cell primary cilium abolishes flow sensing. J Membr Biol 191:69–76. doi:10.1007/s00232-002-1042-4
53. Praetorius HA, Spring KR (2005) A physiological view of the primary cilium. Annu Rev Physiol 67:515–529
54. Qian F, Germino FJ, Cai Y, Zhang X, Somlo S, Germino GG (1997) PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat Genet 16:179–183. doi:10.1038/ng0697-179
55. Raychowdhury MK, McLaughlin M, Ramos AJ, Montalbetti N, Bouley R, Ausiello DA, Cantiello HF (2005) Characterization of single channel currents from primary cilia of renal epithelial cells. J Biol Chem 280:34718–34722
56. Rossetti S, Consugar MB, Chapman AB, Torres VE, Guay-Woodford LM, Grantham JJ, Bennett WM, Meyers CM, Walker DL, Bae K, Zhang QJ, Thompson PA, Miller JP, Harris PC (2007) Comprehensive molecular diagnostics in autosomal dominant polycystic kidney disease. J Am Soc Nephrol 18:2143–2160. doi:10.1681/ASN.2006121387
57. Scheffers MS, van der Bent P, Prins F, Spruit L, Breuning MH, Litvinov SV, de Heer E, Peters DJ (2000) Polycystin-1, the product of the polycystic kidney disease 1 gene, co-localizes with desmosomes in MDCK cells. Hum Mol Genet 9:2743–2750
58. Schneider MC, Rodriguez AM, Nomura H, Zhou J, Morton CC, Reeders ST, Weremowicz S (1996) A gene similar to PKD1 maps to chromosome 4q22: a candidate gene for PKD2. Genomics 38:1–4. doi:10.1006/geno.1996.0584
59. Schwartz EA, Leonard ML, Bizios R, Bowser SS (1997) Analysis and modeling of the primary cilium bending response to fluid shear. Am J Physiol 272:F132–138
60. Sharif Naeini R, Folgering J, Bichet D, Duprat F, Lauritzen I, Arhatte M, Jodar M, Dedman A, Chatelain FC, Schulte U, Retailleau K, Loufrani L, Patel A, Sachs F, Delmas P, Peters DJ, Honoré E (2009) Polycystin-1 and -2 dosage regulates pressure sensing. Cell 139:587–596
61. Sharma N, Berbari NF, Yoder BK (2008) Ciliary dysfunction in developmental abnormalities and diseases. Curr Top Dev Biol 85:371–427. doi:10.1016/S0070-2153(08)00813-2
62. Shimizu T, Janssens A, Voets T, Nilius B (2009) Regulation of the murine TRPP3 channel by voltage, pH, and changes in cell volume. Pflugers Arch 457:795–807. doi:10.1007/s00424-008-0558-6
63. Shiratori H, Hamada H (2006) The left-right axis in the mouse: from origin to morphology. Development 133:2095–2104. doi:10.1242/dev.02384
64. Streets AJ, Wessely O, Peters DJ, Ong AC (2013) Hyperphosphorylation of polycystin-2 at a critical residue in disease reveals an essential role for polycystin-1-regulated dephosphorylation. Hum Mol Genet 22:1924–1939. doi:10.1093/hmg/ddt031
65. Torres VE, Harris PC, Pirson Y (2007) Autosomal dominant polycystic kidney disease. Lancet 369:1287–1301. doi:10.1016/S0140-6736(07)60601-1
66. Tsiokas L, Arnould T, Zhu C, Kim E, Walz G, Sukhatme VP (1999) Specific association of the gene product of PKD2 with the TRPC1 channel. Proc Natl Acad Sci U S A 96:3934–3939
67. Tsiokas L, Kim E, Arnould T, Sukhatme VP, Walz G (1997) Homo- and heterodimeric interactions between the gene products of PKD1 and PKD2. Proc Natl Acad Sci U S A 94:6965–6970
68. Vogel P, Read R, Hansen GM, Freay LC, Zambrowicz BP, Sands AT (2010) Situs inversus in Dpcd/Poll-/-, Nme7-/-, and Pkd1l1-/- mice. Vet Pathol 47:120–131. doi:10.1177/0300985809353553
69. Wang Q, Dai XQ, Li Q, Wang Z, Cantero Mdel R, Li S, Shen J, Tu JC, Cantiello H, Chen XZ (2012) Structural interaction and functional regulation of polycystin-2 by filamin. PLoS One 7:e40448. doi:10.1371/journal.pone.0040448
70. Wilson PD (2004) Polycystic kidney disease. N Engl J Med 350:151–164
71. Wu L, Gao X, Brown RC, Heller S, O'Neil RG (2007) Dual role of the TRPV4 channel as a sensor of flow and osmolality in renal epithelial cells. Am J Physiol Ren Physiol 293:F1699–1713. doi:10.1152/ajprenal.00462.2006
72. Wu G, Hayashi T, Park JH, Dixit M, Reynolds DM, Li L, Maeda Y, Cai Y, Coca-Prados M, Somlo S (1998) Identification of PKD2L, a human PKD2-related gene: tissue-specific expression and mapping to chromosome 10q25. Genomics 54:564–568. doi:10.1006/geno.1998.5618
73. Xu C, Rossetti S, Jiang L, Harris PC, Brown-Glaberman U, Wandinger-Ness A, Bacallao R, Alper SL (2007) Human ADPKD primary cyst epithelial cells with a novel, single codon deletion in the PKD1 gene exhibit defective ciliary polycystin localization and loss of flow-induced Ca2+ signaling. Am J Physiol Ren Physiol 292:F930–945. doi:10.1152/ajprenal.00285.2006
74. Yoder BK, Hou X, Guay-Woodford LM (2002) The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. J Am Soc Nephrol 13:2508–2516
75. Yoshiba S, Shiratori H, Kuo IY, Kawasumi A, Shinohara K, Nonaka S, Asai Y, Sasaki G, Belo JA, Sasaki H, Nakai J, Dworniczak B, Ehrlich BE, Pennekamp P, Hamada H (2012) Cilia at the node of mouse embryos sense fluid flow for left-right determination via Pkd2. Science 338:226–231. doi:10.1126/science.1222538
76. Yuasa T, Venugopal B, Weremowicz S, Morton CC, Guo L, Zhou J (2002) The sequence, expression, and chromosomal localization of a novel polycystic kidney disease 1-like gene, PKD1L1, in human. Genomics 79:376–386. doi:10.1006/geno.2002.6719
77. Zhang P, Luo Y, Chasan B, Gonzalez-Perrett S, Montalbetti N, Timpanaro GA, Cantero Mdel R, Ramos AJ, Goldmann WH, Zhou J, Cantiello HF (2009) The multimeric structure of polycystin-2 (TRPP2): structural-functional correlates of homo- and hetero-multimers with TRPC1. Hum Mol Genet 18:1238–1251. doi:10.1093/hmg/ddp024