Putative roles of cilia in polycystic kidney disease

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1812, Issue 10, 2011, Pages 1256-1262

  Winyard, Paul ^a   Jenkins, Dagan ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cilia; Ciliopathy; Development; Hedgehog; MTOR; Wnt

Indexed keywords

BETA CATENIN; CAENORHABDITIS ELEGANS PROTEIN; CALCIUM; GUANOSINE TRIPHOSPHATASE; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; PHOSPHATIDYLINOSITOL 3 KINASE; POLYCYSTIN 1; PROTEIN KINASE B; PROTEIN PATCHED 1; RAPAMYCIN; RHEB PROTEIN; SONIC HEDGEHOG PROTEIN; TUBERIN; TYROSINE KINASE RECEPTOR; WNT PROTEIN; WNT11 PROTEIN; WNT9B PROTEIN;

BARDET BIEDL SYNDROME; CAENORHABDITIS ELEGANS; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL DISRUPTION; CELL INTERACTION; CELL MEMBRANE; CELL POLARITY; CELL STRUCTURE; CELL SURFACE; CYST; EUKARYOTIC FLAGELLUM; EXTRACELLULAR MATRIX; FLUID FLOW; GENE EXPRESSION; HUMAN; KIDNEY CELL; KIDNEY POLYCYSTIC DISEASE; KIDNEY TUBULE; KINETOPLASTIDA; NONHUMAN; PATHOGENESIS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM SIGNALING; CELL POLARITY; CILIA; HEDGEHOG PROTEINS; HUMANS; HYDRODYNAMICS; MICE; MODELS, BIOLOGICAL; POLYCYSTIC KIDNEY DISEASES; TOR SERINE-THREONINE KINASES; TRPP CATION CHANNELS; WNT PROTEINS;

CAENORHABDITIS ELEGANS; ERINACEIDAE; MAMMALIA; MUS;

EID: 80052270782     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.04.012     Document Type: Review

References (83)

1. Satir P., Christensen S.T. Structure and function of mammalian cilia. Histochem. Cell Biol. 2008, 129:687.
2. Bloodgood R.A. From central to rudimentary to primary: the history of an underappreciated organelle whose time has come. The primary cilium. Methods Cell Biol. 2009, 94:3.
3. Barr M.M., Sternberg P.W. A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 1999, 401:386.
4. Barr M.M., DeModena J., Braun D., Nguyen C.Q., Hall D.H., Sternberg P.W. The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Curr. Biol. 2001, 11:1341.
5. Murcia N.S., Richards W.G., Yoder B.K., Mucenski M.L., Dunlap J.R., Woychik R.P. The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 2000, 127:2347.
6. Sorokin S.P. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 1962, 15:363.
7. Gilula N.B., Satir P. The ciliary necklace. A ciliary membrane specialization. J. Cell Biol. 1972, 53:494.
8. Zhou J. Polycystins and primary cilia: primers for cell cycle progression. Annu. Rev. Physiol. 2009, 71:83.
9. Goetz S.C., Anderson K.V. The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 2010, 11:331.
10. Pedersen L.B., Veland I.R., Schroder J.M., Christensen S.T. Assembly of primary cilia. Dev. Dyn. 2008, 237:1993.
11. Lin F., Hiesberger T., Cordes K., Sinclair A.M., Goldstein L.S., Somlo S., Igarashi P. Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc. Natl. Acad. Sci. U. S. A 2003, 100:5286.
12. Pazour G.J., Dickert B.L., Vucica Y., Seeley E.S., Rosenbaum J.L., Witman G.B., Cole D.G. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell Biol. 2000, 151:709.
13. Nagalakshmi V.K., Ren Q., Pugh M.M., Valerius M.T., McMahon A.P., Yu J. Dicer regulates the development of nephrogenic and ureteric compartments in the mammalian kidney. Kidney Int. 2010.
14. Rohatgi R., Snell W.J. The ciliary membrane. Curr. Opin. Cell Biol. 2010, 22:541.
15. Rosenbaum J.L., Witman G.B. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 2002, 3:813.
16. Molla-Herman A., Ghossoub R., Blisnick T., Meunier A., Serres C., Silbermann F., Emmerson C., Romeo K., Bourdoncle P., Schmitt A., Saunier S., Spassky N., Bastin P., Benmerah A. The ciliary pocket: an endocytic membrane domain at the base of primary and motile cilia. J. Cell Sci. 2010, 123:1785.
17. Hu Q., Milenkovic L., Jin H., Scott M.P., Nachury M.V., Spiliotis E.T., Nelson W.J. A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 2010, 329:436.
18. Kim S.K., Shindo A., Park T.J., Oh E.C., Ghosh S., Gray R.S., Lewis R.A., Johnson C.A., ttie-Bittach T., Katsanis N., Wallingford J.B. Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 2010, 329:1337.
19. Barral Y. Cell biology. Septins at the nexus. Science 2010, 329:1289.
20. Jin H., White S.R., Shida T., Schulz S., Aguiar M., Gygi S.P., Bazan J.F., Nachury M.V. The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Glycobiology 2010, 141:1208.
21. Hildebrandt F., Attanasio M., Otto E. Nephronophthisis: disease mechanisms of a ciliopathy. J. Am. Soc. Nephrol. 2009, 20:23.
22. Zaghloul N.A., Katsanis N. Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy. J. Clin. Invest. 2009, 119:428.
23. Baker K., Beales P.L. Making sense of cilia in disease: the human ciliopathies. Am. J. Med. Genet. C Semin. Med. Genet. 2009, 151C:281.
24. Nauli S.M., Alenghat F.J., Luo Y., Williams E., Vassilev P., Li X., Elia A.E., Lu W., Brown E.M., Quinn S.J., Ingber D.E., Zhou J. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 2003, 33:129.
25. Pennekamp P., Karcher C., Fischer A., Schweickert A., Skryabin B., Horst J., Blum M., Dworniczak B. The ion channel polycystin-2 is required for left-right axis determination in mice. Curr. Biol. 2002, 12:938.
26. Schottenfeld J., Sullivan-Brown J., Burdine R.D. Zebrafish curly up encodes a Pkd2 ortholog that restricts left-side-specific expression of southpaw. Development 2007, 134:1605.
27. Praetorius H.A., Spring K.R. Bending the MDCK cell primary cilium increases intracellular calcium. J. Membr. Biol. 2001, 184:71.
28. Abou Alaiwi W.A., Takahashi M., Mell B.R., Jones T.J., Ratnam S., Kolb R.J., Nauli S.M. Ciliary polycystin-2 is a mechanosensitive calcium channel involved in nitric oxide signaling cascades. Circ. Res. 2009, 104:860.
29. Nonaka S., Shiratori H., Saijoh Y., Hamada H. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 2002, 418:96.
30. Sarmah B., Latimer A.J., Appel B., Wente S.R. Inositol polyphosphates regulate zebrafish left-right asymmetry. Dev. Cell 2005, 9:133.
31. Praetorius H.A., Spring K.R. Removal of the MDCK Cell Primary Cilium Abolishes Flow Sensing. J. Membr. Biol. 2003, 191:69.
32. Sammels E., Devogelaere B., Mekahli D., Bultynck G., Missiaen L., Parys J.B., Cai Y., Somlo S., De Smedt H. Polycystin-2 activation by inositol 1,4,5-trisphosphate-induced Ca2+ release requires its direct association with the inositol 1,4,5-trisphosphate receptor in a signaling microdomain. J. Biol. Chem. 2010, 285:18794.
33. Li Y., Santoso N.G., Yu S., Woodward O.M., Qian F., Guggino W.B. Polycystin-1 interacts with inositol 1,4,5-trisphosphate receptor to modulate intracellular Ca2+ signaling with implications for polycystic kidney disease. J. Biol. Chem. 2009, 284:36431.
34. Cowley B.D. Calcium, cyclic AMP, and MAP kinases: dysregulation in polycystic kidney disease. Kidney Int. 2008, 73:251.
35. Wang X., Ward C.J., Harris P.C., Torres V.E. Cyclic nucleotide signaling in polycystic kidney disease. Kidney Int. 2010, 77:129.
36. Xia S., Li X., Johnson T., Seidel C., Wallace D.P., Li R. Polycystin-dependent fluid flow sensing targets histone deacetylase 5 to prevent the development of renal cysts. Development 2010, 137:1075.
37. Hellman N.E., Liu Y., Merkel E., Austin C., Le C.S., Beier D.R., Sun Z., Sharma N., Yoder B.K., Drummond I.A. The zebrafish foxj1a transcription factor regulates cilia function in response to injury and epithelial stretch. Proc. Natl. Acad. Sci. U. S. A 2010, 107:18499.
38. European chromosome 16 tuberous sclerosis consortium, Identification and characterization of the tuberous sclerosis gene on chromosome 16. Glycobiology 1993, 75:1305.
39. van S.M., de H.R., Hermans C., Nellist M., Janssen B., Verhoef S., Lindhout D., van den O.A., Halley D., Young J., Burley M., Jeremiah S., Woodward K., Nahmias J., Fox M., Ekong R., Osborne J., Wolfe J., Povey S., Snell R.G., Cheadle J.P., Jones A.C., Tachataki M., Ravine D., Sampson J.R., Reeve M.P., Richardson P., Wilmer F., Munro C., Hawkins T.L., Sepp T., Ali J.B., Ward S., Green A.J., Yates J.R., Kwiatkowska J., Henske E.P., Short M.P., Haines J.H., Jozwiak S., Kwiatkowski D.J. Identification of the tuberous sclerosis gene TSC1 on chromosome 9q34. Science 1997, 277:805.
40. Hartman T.R., Liu D., Zilfou J.T., Robb V., Morrison T., Watnick T., Henske E.P. The tuberous sclerosis proteins regulate formation of the primary cilium via a rapamycin-insensitive and polycystin 1-independent pathway. Hum. Mol. Genet. 2009, 18:151.
41. Bonnet C.S., Aldred M., von R.C., Harris R., Sandford R., Cheadle J.P. Defects in cell polarity underlie TSC and ADPKD-associated cystogenesis. Hum. Mol. Genet. 2009, 18:2166.
42. Yoder B.K., Hou X., Guay-Woodford L.M. 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.
43. Brook-Carter P.T., Peral B., Ward C.J., Thompson P., Hughes J., Maheshwar M.M., Nellist M., Gamble V., Harris P.C., Sampson J.R. Deletion ot the TSC2 and PKD1 genes associated with severe infantile polycystic kidney disease-a contiguous gene syndrome. Nat. Genet. 1994, 8:328.
44. Shillingford J.M., Murcia N.S., Larson C.H., Low S.H., Hedgepeth R., Brown N., Flask C.A., NoVick A.C., Goldfarb D.A., Kramer-Zucker A., Walz G., Piontek K.B., Germino G.G., Weimbs T. The mTOR pathway is regulated by polycystin-1, and its inhibition reverses renal cystogenesis in polycystic kidney disease. Proc. Natl. Acad. Sci. U. S. A 2006, 103:5466.
45. Dere R., Wilson P.D., Sandford R.N., Walker C.L. Carboxy terminal tail of polycystin-1 regulates localization of TSC2 to repress mTOR. PLoS One 2010, 5:e9239.
46. Fischer D.C., Jacoby U., Pape L., Ward C.J., Kuwertz-Broeking E., Renken C., Nizze H., Querfeld U., Rudolph B., Mueller-Wiefel D.E., Bergmann C., Haffner D. Activation of the AKT/mTOR pathway in autosomal recessive polycystic kidney disease (ARPKD). Nephrol. Dial. Transplant. 2009, 24:1819.
47. Becker J.U., Saez A.O., Zerres K., Witzke O., Hoyer P.F., Schmid K.W., Kribben A., Bergmann C., Nurnberger J. The mTOR pathway is activated in human autosomal-recessive polycystic kidney disease. Kidney Blood Press. Res. 2010, 33:129.
48. Wu M., Arcaro A., Varga Z., Vogetseder A., Le H.M., Wuthrich R.P., Serra A.L. Pulse mTOR inhibitor treatment effectively controls cyst growth but leads to severe parenchymal and glomerular hypertrophy in rat polycystic kidney disease. Am. J. Physiol. Renal Physiol. 2009, 297:F1597-F1605.
49. Shillingford J.M., Piontek K.B., Germino G.G., Weimbs T. Rapamycin ameliorates PKD resulting from conditional inactivation of Pkd1. J. Am. Soc. Nephrol. 2010, 21:489.
50. Zafar I., Ravichandran K., Belibi F.A., Doctor R.B., Edelstein C.L. Sirolimus attenuates disease progression in an orthologous mouse model of human autosomal dominant polycystic kidney disease. Kidney Int. 2010, 78:754.
51. Zullo A., Iaconis D., Barra A., Cantone A., Messaddeq N., Capasso G., Dolle P., Igarashi P., Franco B. Kidney-specific inactivation of Ofd1 leads to renal cystic disease associated with upregulation of the mTOR pathway. Hum. Mol. Genet. 2010, 19:2792.
52. Boehlke C., Kotsis F., Patel V., Braeg S., Voelker H., Bredt S., Beyer T., Janusch H., Hamann C., Godel M., Muller K., Herbst M., Hornung M., Doerken M., Kottgen M., Nitschke R., Igarashi P., Walz G., Kuehn E.W. Primary cilia regulate mTORC1 activity and cell size through Lkb1. Nat. Cell Biol. 2010, 12:1115.
53. Grumolato L., Liu G., Mong P., Mudbhary R., Biswas R., Arroyave R., Vijayakumar S., Economides A.N., Aaronson S.A. Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev. 2010, 24:2517.
54. Lancaster M.A., Gleeson J.G. Cystic kidney disease: the role of Wnt signaling. Trends Mol. Med. 2010, 16:349.
55. Saadi-Kheddouci S., Berrebi D., Romagnolo B., Cluzeaud F., Peuchmaur M., Kahn A., Vandewalle A., Perret C. Early development of polycystic kidney disease in transgenic mice expressing an activated mutant of the beta-catenin gene. Oncogene 2001, 20:5972.
56. Kim E., Arnould T., Sellin L.K., Benzing T., Fan M.J., Gruning W., Sokol S.Y., Drummond I., Walz G. The polycystic kidney disease 1 gene product modulates Wnt signaling. J. Biol. Chem. 1999, 274:4947.
57. Lal M., Song X., Pluznick J.L., Di G., Merrick D.M., Rosenblum N.D., Chauvet V., Gottardi C.J., Pei Y., M.J.Caplan M.J. Polycystin-1C-terminal tail associates with beta-catenin and inhibits canonical Wnt signaling. Hum. Mol. Genet. 2008, 17:3105.
58. Liu M., Shi S., Senthilnathan S., Yu J., Wu E., Bergmann C., Zerres K., Bogdanova N., Coto E., Deltas C., Pierides A., Demetriou K., Devuyst O., Gitomer B., Laakso M., Lumiaho A., Lamnissou K., Magistroni R., Parfrey P., Breuning M., Peters D.J., Torra R., Winearls C.G., Torres V.E., Harris P.C., Paterson A.D., Pei Y. Genetic variation of DKK3 may modify renal disease severity in ADPKD. J. Am. Soc. Nephrol. 2010, 21:1510.
59. Romaker D., Puetz M., Teschner S., Donauer J., Geyer M., Gerke P., Rumberger B., Dworniczak B., Pennekamp P., Buchholz B., Neumann H.P., Kumar R., Gloy J., Eckardt K.U., Walz G. Increased expression of secreted frizzled-related protein 4 in polycystic kidneys. J. Am. Soc. Nephrol. 2009, 20:48.
60. Majumdar A., Vainio S., Kispert A., McMahon J., McMahon A.P. Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 2003, 130:3175.
61. Karner C.M., Chirumamilla R., Aoki S., Igarashi P., Wallingford J.B., Carroll T.J. Wnt9b signaling regulates planar cell polarity and kidney tubule morphogenesis. Nat. Genet. 2009, 41:793.
62. Saburi S., Hester I., Fischer E., Pontoglio M., Eremina V., Gessler M., Quaggin S.E., Harrison R., Mount R., McNeill H. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet. 2008, 40:1010.
63. Fischer E., Legue E., Doyen A., Nato F., Nicolas J.F., Torres V., Yaniv M., Pontoglio M. Defective planar cell polarity in polycystic kidney disease. Nat. Genet. 2006, 38:21.
64. Simons M., Gloy J., Ganner A., Bullerkotte A., Bashkurov M., Kronig C., Schermer B., Benzing T., Cabello O.A., Jenny A., Mlodzik M., Polok B., Driever W., Obara T., Walz G. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 2005, 37:537.
65. Jenkins D. Hedgehog signalling: emerging evidence for non-canonical pathways. Cell. Signal. 2009, 21:1023.
66. Pathi S., Pagan-Westphal S., Baker D.P., Garber E.A., Rayhorn P., Bumcrot D., Tabin C.J., Blake P.R., Williams K.P. Comparative biological responses to human Sonic, Indian, and Desert hedgehog. Mech. Dev. 2001, 106:107.
67. Rohatgi R., Milenkovic L., Corcoran R.B., Scott M.P. Hedgehog signal transduction by Smoothened: pharmacologic evidence for a 2-step activation process. Proc. Natl. Acad. Sci. U. S. A 2009, 106:3196.
68. Rohatgi R., Milenkovic L., Scott M.P. Patched1 regulates hedgehog signaling at the primary cilium. Science 2007, 317:372.
69. Kim J., Kato M., Beachy P.A. Gli2 trafficking links Hedgehog-dependent activation of Smoothened in the primary cilium to transcriptional activation in the nucleus. Proc. Natl. Acad. Sci. U. S. A 2009, 106:21666.
70. Caspary T., Larkins C.E., Anderson K.V. The graded response to Sonic Hedgehog depends on cilia architecture. Dev. Cell 2007, 12:767.
71. Kelley R.I., Hennekam R.C. The Smith-Lemli-Opitz syndrome. J. Med. Genet. 2000, 37:321.
72. Lee J.J., Ekker S.C., von Kessler D.P., Porter J.A., Sun B.I., Beachy P.A. Autoproteolysis in hedgehog protein biogenesis. Science 1994, 266:1528.
73. Porter J.A. D.P.von Kessler, S.C. Ekker, K.E. Young, J.J. Lee, K. Moses, and P.A. Beachy, The product of hedgehog autoproteolytic cleavage active in local and long-range signalling. Nature 1995, 374:363.
74. Cooper M.K., Wassif C.A., Krakowiak P.A., Taipale J., Gong R., Kelley R.I., Porter F.D., Beachy P.A. A defective response to Hedgehog signaling in disorders of cholesterol biosynthesis. Nat. Genet. 2003, 33:508.
75. Hu M.C., Mo R., Bhella S., Wilson C.W., Chuang P.T., Hui C.C., Rosenblum N.D. GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development 2006, 133:569.
76. Yu J., Carroll T.J., McMahon A.P. Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 2002, 129:5301.
77. Chan S.K., Riley P.R., Price K.L., McElduff F., Winyard P.J., Welham S.J., Woolf A.S., Long D.A. Corticosteroid-induced kidney dysmorphogenesis is associated with deregulated expression of known cystogenic molecules, as well as Indian hedgehog. Am. J. Physiol. Renal Physiol. 2010, 298:F346-F356.
78. Wilson P.D. Polycystin: new aspects of structure, function, and regulation. J. Am. Soc. Nephrol. 2001, 12:834.
79. Israeli S., Amsler K., Zheleznova N., Wilson P.D. Abnormalities in focal adhesion complex formation, regulation, and function in human autosomal recessive polycystic kidney disease epithelial cells. Am. J. Physiol. Cell Physiol. 2010, 298:C831-C846.
80. May-Simera H.L., Ross A., Rix S., Forge A., Beales P.L., Jagger D.J. Patterns of expression of Bardet-Biedl syndrome proteins in the mammalian cochlea suggest noncentrosomal functions. J. Comp. Neurol. 2009, 514:174.
81. Kim J.C., Badano J.L., Sibold S., Esmail M.A., Hill J., Hoskins B.E., Leitch C.C., Venner K., Ansley S.J., Ross A.J., Leroux M.R., Katsanis N., Beales P.L. The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat. Genet. 2004, 36:462.
82. Walz G., Budde K., Mannaa M., Nurnberger J., Wanner C., Sommerer C., Kunzendorf U., Banas B., Horl W.H., Obermuller N., Arns W., Pavenstadt H., Gaedeke J., Buchert M., May C., Gschaidmeier H., Kramer S., Eckardt K.U. Everolimus in patients with autosomal dominant polycystic kidney disease. N. Engl. J. Med. 2010, 363:830.
83. Serra A.L., Poster D., Kistler A.D., Krauer F., Raina S., Young J., Rentsch K.M., Spanaus K.S., Senn O., Kristanto P., Scheffel H., Weishaupt D., Wuthrich R.P. Sirolimus and kidney growth in autosomal dominant polycystic kidney disease. N. Engl. J. Med. 2010, 363:820.