Intraflagellar transport and cilia-dependent renal disease: The ciliary hypothesis of polycystic kidney disease

Journal of the American Society of Nephrology

Volumn 15, Issue 10, 2004, Pages 2528-2536

  Pazour, Gregory J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOSOMAL DOMINANT DISORDER; AUTOSOMAL RECESSIVE DISORDER; CELL DIFFERENTIATION; CELL PROLIFERATION; CILIARY MOTILITY; EPITHELIUM CELL; EUKARYOTIC FLAGELLUM; FLAGELLUM; GENE LOCATION; GENETIC DISORDER; HYPOTHESIS; KIDNEY DISEASE; KIDNEY NERVE; KIDNEY POLYCYSTIC DISEASE; KIDNEY TUBULE; MAMMAL; MUTATION; NEPHRON; NEPHRONOPHTHISIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ACTIVE TRANSPORT; ANIMAL; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; HUMAN; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RISK FACTOR; SENSITIVITY AND SPECIFICITY;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CELL PROLIFERATION; CILIA; FLAGELLA; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICE; MUTATION; POLYCYSTIC KIDNEY DISEASES; RISK FACTORS; SENSITIVITY AND SPECIFICITY;

EID: 16244368607     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.ASN.0000141055.57643.E0     Document Type: Review

References (111)

1. Zimmerman KW: [Contributions to knowledge of some glands and epithelium]. Arch Mikr Anat 52: 552-706, 1898
2. Wheatley DN: Primary cilia in normal and pathological tissues. Pathobiology 63: 222-238, 1995
3. Praetorius HA, Spring KR: Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 184: 71-79, 2001
4. Perkins LA, Hegecock EM, Thomson JN, Culotti JG: Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117:456-487, 1986
5. Witman GB: Cell motility: Deaf Drosophila keep the beat. Curr Biol 13: R796-R798, 2003
6. Tisher CC, Madsen KM: Anatomy of the kidney. In: Brenner & Rector's The Kidney, 6th Ed., edited by Brenner BM, Philadelphia, W.B. Saunders Company, 1996, pp 3-67
7. Guo P, Weinstein AM, Weinbaum S: A hydrodynamic mechanosensory hypothesis for brush border microvilli. Am J Physiol Renal Physiol 279: F698-F712, 2000
8. Schwartz EA, Leonard ML, Bizios R, Bowser SS: Analysis and modeling of the primary cilium bending response to fluid shear. Am J Physiol 272: F132-F138, 1997
9. Agrin NS, Leszyk JD, Green KM, Evans JE, Pazour GJ, Witman GB: Exploring the Chlamydomonas Flagellar Proteome. Mol Biol Cell 14: 434a, 2003
10. Ostrowski LE, Blackburn K, Radde KM, Moyer MB, Schlatzer DM, Moseley A, Boucher RC: A proteomic analysis of human cilia: Identification of novel components. Mol Cell Proteomics 1: 451-465, 2002
11. Bloodgood RA: Ciliary and Flagellar Membranes. New York, Plenum Press, 1990, pp 1-431
12. Gilula NB, Satir P: The ciliary necklace. A ciliary membrane specialization. J Cell Biol 53: 494-509, 1972
13. Bouck GB: The structure, origin, isolation and composition of the tubular mastigonemes of the Ochromonas flagellum. J Cell Biol 50: 362-384, 1971
14. Nakamura S, Tanaka G, Maeda T, Kamiya R, Matsunaga T, Nikaido O: Assembly and function of Chlamydomonas flagellar mastigonemes as probed with a monoclonal antibody. J Cell Sci 109: 57-62, 1996
15. Rosenbaum JL, Witman GB: Intraflagellar transport. Nat Rev Mol Cell Biol 3: 813-825, 2002
16. Papermaster DS, Schneider BG, Besharse JC: Vesicular transport of newly synthesized opsin from the Golgi apparatus toward the rod outer segment. Ultrastructural immunocytochemical and autoradiographic evidence in Xenopus retinas. Invest Ophthalmol Vis Sci 26: 1386-1404, 1985
17. Snapp EL, Landfear SM: Characterization of a targeting motif for a flagellar membrane protein in Leishmania enriettii. J Biol Chem 274: 29543-29548, 1999
18. Tam BM, Moritz OL, Hurd LB, Papermaster DS: Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis. J Cell Biol 151: 1369-1380, 2000
19. Tai AW, Chuang J-Z, Bode C, Wolfrum U, Sung C-H: Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1. Cell 97: 877-887, 1999
20. Ringo DL: Flagellar motion and fine structure of the flagellar apparatus in Chlamydomonas. J Cell Biol 33: 543-571, 1967
21. O'Toole ET, Giddings TH, McIntosh JR, Dutcher SK: Three-dimensional organization of basal bodies from wild-type and delta-tubulin deletion strains of Chlamydomonas reinhardtii. Mol Biol Cell 14: 2999-3012, 2003
22. Hinchcliffe EH, Miller FJ, Cham M, Khodjakov A, Sluder G: Requirement of a centrosomal activity for cell cycle progression through G1 into S phase. Science 291: 1547-1550, 2001
23. Khodjakov A, Rieder CL: Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J Cell Biol 153: 237-242, 2001
24. Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M: Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426: 570-574, 2003
25. Hinchcliffe EH, Li C, Thompson EA, Maller JL, Sluder G: Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283: 851-854, 1999
26. Lacey KR, Jackson PK, Stearns T: Cyclin-dependent kinase control of centrosome duplication. Proc Natl Acad Sci U S A 96: 2817-2822, 1999
27. Ouchi M, Fujiuchi N, Sasai K, Katayama H, Minamimori YA, Ongusaha PP, Deng C, Sen S, Lee SW, Ouchi T: BRCA1 phosphorylation by Aurora-A in the regulation of G2 to M transition. J Biol Chem 279: 19643-19648, 2004
28. Chen D, Purohit A, Halilovic E, Doxsey SJ, Newton AC: Centrosomal anchoring of protein kinase C βII by pericentrin controls microtubule organization, spindle function, and cytokinesis. J Biol Chem 279: 4829-4839, 2004
29. Doxsey SJ: Centrosomes as command centres for cellular control. Nat Cell Biol 3: E105-E108, 2001
30. Doxsey S: Re-evaluating centrosome function. Nat Rev Mol Cell Biol 2: 688-698, 2001
31. Kozminski KG, Johnson KA, Forscher P, Rosenbaum JL: A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci U S A 90: 5519-5523, 1993
32. Cole DG: The intraflagellar transport machinery of Chlamydomonas reinhardtii. Traffic 4: 435-442, 2003
33. Scholey JM: Intraflagellar transport. Annu Rev Cell Dev Biol 19: 423-443, 2003
34. Piperno G, Mead K: Transport of a novel complex in the cytoplasmic matrix of Chlamydomonas flagella. Proc Natl Acad Sci U S A 94: 4457-4462, 1997
35. Cole DG, Diener DR, Himelblau AL, Beech PL, Fuster JC, Rosenbaum JL: Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J Cell Biol 141: 993-1008, 1998
36. Pazour GJ, Baker SA, Deane JA, Cole DG, Dickert BL, Rosenbaum JL, Witman GB, Besharse JC: The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J Cell Biol 157: 103-113, 2002
37. Pazour GJ, Dickert BL, Vucica Y, Seeley ES, Rosenbaum JL, Witman GB, Cole DG: Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene Tg737, are required for assembly of cilia and flagella. J Cell Biol 151: 709-718, 2000
38. Haycraft CJ, Swoboda P, Taulman PD, Thomas JH, Yoder BK: The C. elegans homolog of the murine cystic kidney disease gene Tg737 functions in a ciliogenic pathway and is disrupted in osm-5 mutant worms. Development 128: 1493-1505, 2001
39. Qin H, Rosenbaum JL, Barr MM: An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons. Curr Biol 11: 457-461, 2001
40. Han YG, Kwok BH, Kernan MJ: Intraflagellar transport is required in Drosophila to differentiate sensory cilia but not sperm. Curr Biol 13: 1679-1686, 2003
41. Moyer JH, Lee-Tischler MJ, Kwon H-Y, Schrick JJ, Avner ED, Sweeney WE, Godfrey VL, Cacheiro NLA, Wilkinson JE, Woychik RP: Candidate gene associated with a mutation causing recessive polycystic kidney disease in mice. Science 264: 1329-1333, 1994
42. Sommardahl C, Cottrell M, Wilkinson JE, Woychik RP, Johnson DK: Phenotypic variations of orpk mutation and chromosomal localization of modifiers influencing kidney phenotype. Physiol Genomics 7: 127-134, 2001
43. Cano DA, Murcia NS, Pazour GJ, Hebrok M: orpk mouse model of polycystic kidney disease reveals essential role of primary cilia in pancreatic tissue organization. Development 131: 3457-3467, 2004
44. Murcia NS, Richards WG, Yoder BK, Mucenski ML, Dunlap JR, Woychik RP: The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 127: 2347-2355, 2000
45. Huangfu D, Liu A, Rakeman AS, Murcia NS, Niswander L, Anderson KV: Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426: 83-87, 2003
46. Ibanez-Tallon I, Gorokhova S, Heintz N: Loss of function of axonemal dynein Mdnah5 causes primary ciliary dyskinesia and hydrocephalus. Hum Mol Genet 11: 715-721, 2002
47. Bryan JHD: Abnormal cilia in a male-sterile mutant mouse. Virchows Arch 400: 77-86, 1983
48. Shimizu A, Koto M: Ultrastructure and movement of the ependymal and tracheal cilia in congenitally hydrocephalic WIC-Hyd rats. Childs Nerv Syst 8: 25-32, 1992
49. Afzelius BA: Role of cilia in human health. Cell Motil Cytoskel 32: 95-97, 1995
50. Taulman PD, Haycraft CJ, Balkovetz DF, Yoder BK: Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol Biol Cell 12: 589-599, 2001
51. Zhang Q, Murcia NS, Chittenden LR, Richards WG, Michaud EJ, Woychik RP, Yoder BK: Loss of the Tg737 protein results in skeletal patterning defects. Dev Dyn 227: 78-90, 2003
52. Afzelius BA: A human syndrome caused by immotile cilia. Science 193: 317-319, 1976
53. Takeda S, Yonekawa Y, Tanaka Y, Okada Y, Nonaka S, Hirokawa N: Left-right asymmetry and kinesin superfamily protein KIF3A: New insights in determination of laterality and mesoderm induction by kif3A-/- mice analysis. J Cell Biol 145: 825-836, 1999
54. Nonaka S, Tanaka Y, Okada Y, Takada S, Harada A, Kanai Y, Kido M, Hirokawa N: 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, 1998
55. Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR, Goldstein LSB: Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci U S A 96: 5043-5048, 1999
56. Culotti JG, Russell RL: Osmotic avoidance defective mutants of the nematode Caenorhabditis elegans. Genetics 90: 243-256, 1978
57. Morris RL, Scholey JM: Heterotrimeric kinesin-II is required for the assembly of motile 9+2 ciliary axonemes on sea urchin embryos. J Cell Biol 138: 1009-1022, 1997
58. Kozminski KG, Beech PL, Rosenbaum JL: The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J Cell Biol 131: 1517-1527, 1995
59. Brown JM, Marsala C, Kosoy R, Gaertig J: Kinesin-II is preferentially targeted to assembling cilia and is required for ciliogenesis and normal cytokinesis in Tetrahymena. Mol Biol Cell 10: 3081-3096, 1999
60. Signor D, Wedaman KP, Rose LS, Scholey JM: Two heterotrimeric kinesin complexes in chemosensory neurons and sensory cilia of Caenorhabditis elegans. Mol Biol Cell 10: 345-360, 1999
61. Marszalek JR, Liu X, Roberts E, Chui D, Marth J, Williams DS, Goldstein LSB: Tissue specific deletion of KIF3A from photoreceptors results in their degradation. Mol Biol Cell 9: 131a, 1998
62. Lin F, Hiesberger T, Cordes K, Sinclair AM, Goldstein LS, 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 100: 5286-5291, 2003
63. Wong RW, Setou M, Teng J, Takei Y, Hirokawa N: Overexpression of motor protein KIF17 enhances spatial and working memory in transgenic mice. Proc Natl Acad Sci U S A 99: 14500-14505, 2002
64. Gibbons BH, Asai DJ, Tang W-JY, Hays TS, Gibbons IR: Phylogeny and expression of axonemal and cytoplasmic dynein genes in sea urchins. Mol Biol Cell 5: 57-70, 1994
65. Pazour GJ, Dickert BL, Witman GB: The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J Cell Biol 144: 473-481, 1999
66. Porter ME, Bower R, Knott JA, Byrd P, Dentier W: Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol Biol Cell 10: 693-712, 1999
67. Signor D, Wedaman KP, Orozco JT, Dwyer ND, Bargmann CI, Rose LS, Scholey JM: Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. J Cell Biol 147: 519-530, 1999
68. Schafer JC, Haycraft CJ, Thomas JH, Yoder BK, Swoboda P: XBX-1 encodes a dynein light intermediate chain required for retrograde intraflagellar transport and cilia assembly in Caenorhabditis elegans. Mol Biol Cell 14: 2057-2070, 2003
69. Hou Y, Pazour GJ, Witman GB: A dynein light intermediate chain, D1bLIC, is required for retrograde intraflagellar transport (IFT). Mol Biol Cell 15: 2004, in press
70. Pazour GJ, Wilkerson CG, Witman GB: A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT). J Cell Biol 141: 979-992, 1998
71. Vaisberg EA, Grissom PM, McIntosh JR: Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles. J Cell Biol 133: 831-842, 1996
72. Grissom PM, Vaisberg EA, McIntosh JR: Identification of a novel light intermediate chain (D2LIC) for mammalian cytoplasmic dynein 2. Mol Biol Cell 13: 817-829, 2002
73. Mikami A, Tynan SH, Hama T, Luby-Phelps K, Saito T, Crandall JE, Besharse JC, Vallee RB: Molecular structure of cytoplasmic dynein 2 and its distribution in neuronal and ciliated cells. J Cell Sci 115: 4801-4808, 2002
74. Murcia NS, Sweeney WE Jr, Avner ED: New insights into the molecular pathophysiology of polycystic kidney disease. Kidney Int 55: 1187-1197, 1999
75. Hirokawa N: Stirring up development with the heterotrimeric kinesin KIF3. Traffic 1: 29-34, 2000
76. Sun Z, Amsterdam A, Pazour GJ, Cole DG, Miller MS, Hopkins N: A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development 131: 4085-4093, 2004
77. Pazour GJ, Witman GB: The vertebrate primary cilium is a sensory organeile. Curr Opin Cell Biol 15: 105-110, 2003
78. 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 12: R378-R380, 2002
79. 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 13: 2508-2516, 2002
80. Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, 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 33: 129-137, 2003
81. The International Polycystic Kidney Disease Consortium: Polycystic kidney disease: The complete structure of the PKD1 gene and its protein. Cell 81: 289-298, 1995
82. 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: PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 272: 1339-1342, 1996
83. Cai Y, Anyatonwu G, Okuhara D, Lee KB, Yu Z, Onoe T, Mei CL, Qian Q, Geng L, Witzgall R, Ehrlich BE, Somlo S: Calcium dependence of polycystin-2 channel activity is modulated by phosphorylation at Ser812. J Biol Chem 279: 19,987-19,995, 2004
84. 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 12: 938-943, 2002
85. Torikata C, Kijimoto C, Koto M: Ultrastructure of respiratory cilia of WIC-Hyd male rats. Am J Pathol 138: 341-347, 1991
86. Ward CJ, Yuan D, Masyuk TV, Wang X, Punyashthiti R, Whelan S, Bacallao R, Torra R, LaRusso NF, Torres VE, Harris PC: Cellular and subcellular localization of the ARPKD protein; fibrocystin is expressed on primary cilia. Hum Mol Genet 12: 2703-2710, 2003
87. Wang S, Luo Y, Wilson PD, Witman GB, Zhou J: The autosomal recessive polycystic kidney disease protein is localized to primary cilia, with concentration in the basal body area. J Am Soc Nephrol 15: 592-602, 2004
88. Zhang MZ, Mai W, Li C, Cho SY, Hao C, Moeckel G, Zhao R, Kim I, Wang J, Xiong H, Wang H, Sato Y, Wu Y, Nakanuma Y, Lilova M, Pei Y, Harris RC, Li S, Coffey RJ, Sun L, Wu D, Chen XZ, Breyer MD, Zhao ZJ, McKanna JA, Wu G: PKHD1 protein encoded by the gene for autosomal recessive polycystic kidney disease associates with basal bodies and primary cilia in renal epithelial cells. Proc Natl Acad Sci U S A 101: 2311-2316, 2004
89. Masyuk TV, Huang BQ, Ward CJ, Masyuk AI, Yuan D, Splinter PL, Punyashthiti R, Ritman EL, Torres VE, Harris PC, LaRusso NF: Defects in cholangiocyte fibrocystin expression and ciliary structure in the PCK rat. Gastroenterology 125: 1303-1310, 2003
90. Ward CJ, Hogan MC, Rossetti S, Walker D, Sneddon T, Wang X, Kubly V, Cunningham JM, Bacallao R, Ishibashi M, Milliner DS, Torres VE, Harris PC: The gene mutated in autosomal recessive polycystic kidney disease encodes a large, receptor-like protein. Nat Genet 30: 159-269, 2002
91. Onuchic LF, Furu L, Nagasawa Y, Hou X, Eggermann T, Ren Z, Bergmann C, Senderek J, Esquivel E, Zeltner R, Rudnik-Schoneborn S, Mrug M, Sweeney W, Avner ED, Zerres K, Guay-Woodford LM, Somlo S, Germino GG: PKHD1, the polycystic kidney and hepatic disease 1 gene, encodes a novel large protein containing multiple immunoglobulin-like plexin-transcription-factor domains and parallel beta-helix I repeats. Am J Hum Genet 70: 1305-1317, 2002
92. Kamiya R, Kurimoto E, Muto E: Two types of Chlamydomonas flagellar mutants missing different components of inner-arm dynein. J Cell Biol 112: 441-447, 1991
93. Hildebrandt F, Otto E, Rensing C, Nothwang HG, Vollmer M, Adolphs J, Hanusch H, Brandis M: A novel gene encoding an SH3 domain protein is mutated in nephronophthisis type 1. Nat Genet 17: 149-153, 1997
94. Otto EA, Schermer B, Obara T, O'Toole JF, Hiller KS, Mueller AM, Ruf RG, Hoefele J, Beekmann F, Landau D, Foreman JW, Goodship JA, Strachan T, Kispert A, Wolf MT, Gagnadoux MF, Nivet H, Antignac C, Walz G, Drummond IA, Benzing T, Hildebrandt F: Mutations in INVS encoding inversin cause nephronophthisis type 2, linking renal cystic disease to the function of primary cilia and left-right axis determination. Nat Genet 34: 413-420, 2003
95. Mochizuki T, Saijoh Y, Tsuchiya K, Shirayoshi Y, Takai S, Taya C, Yonekawa H, Yamada K, Nihei H, Nakatsuji N, Overbbek PA, Hamada H, Yokoyama T: Cloning of inv, a gene that controls left/right asymmetry and kidney development. Nature 395: 177-181, 1998
96. Morgan D, Turnpenny L, Goodship J, Dai W, Majumder K, Matthews L, Gardner A, Schuster G, Vien L, Harrison W, Elder FFB, Pneman-Splitt M, Overbeek P, Strachan T: Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse. Nat Genet 20: 149-156, 1998
97. Eley L, Turnpenny L, Yates LM, Craighead AS, Morgan D, Whistler C, Goodship JA, Strachan T: A perspective on inversin. Cell Biol Int 28: 119-124, 2004
98. Watanabe D, Saijoh Y, Nonaka S, Sasaki G, Ikawa Y, Yokoyama T, Hamada H: The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia. Development 130: 1725-1734, 2003
99. Morgan D, Eley L, Sayer J, Strachan T, Yates LM, Craighead AS, Goodship JA: Expression analyses and interaction with the anaphase promoting complex protein Apc2 suggest a role for inversin in primary cilia and involvement in the cell cycle. Hum Mol Genet 11: 3345-3350, 2002
100. Olbrich H, Fliegauf M, Hoefele J, Kispert A, Otto E, Volz A, Wolf MT, Sasmaz G, Trauer U, Reinhard! R, Sudbrak R, Antignac C, Gretz N, Walz G, Schermer B, Benzing T, Hildebrandt F, Omran H: Mutations in a novel gene, NPHP3, cause adolescent nephronophthisis, tapeto-retinal degeneration and hepatic fibrosis. Nat Genet 34: 455-459, 2003
101. Otto E, Hoefele J, Ruf R, Mueller AM, Hiller KS, Wolf MT, Schuermann MJ, Becker A, Birkenhager R, Sudbrak R, Hennies HC, Nurnberg P, Hildebrandt F: A gene mutated in nephronophthisis and retinitis pigmentosa encodes a novel protein, nephroretinin, conserved in evolution. Am J Hum Genet 71: 1161-1167, 2002
102. Mollet G, Salomon R, Gribouval O, Silbermann F, Bacq D, Landthaler G, Milford D, Nayir A, Rizzoni G, Antignac C, Saunier S: The gene mutated in juvenile nephronophthisis type 4 encodes a novel protein that interacts with nephrocystin. Nat Genet 32: 300-305, 2002
103. Stone DL, Slavotinek A, Bouffard GG, Banerjee-Basu S, Baxevanis AD, Barr M, Biesecker LG: Mutation of a gene encoding a putative chaperonin causes McKusick-Kaufman syndrome. Nat Genet 25: 79-82, 2000
104. Ansley SJ, Badano JL, Blacque OE, Hill J, Hoskins BE, Leitch CC, Kim JC, Ross AJ, Eichers ER, Teslovich TM, Mah AK, Johnsen RC, Cavender JC, Lewis RA, Leroux MR, Beales PL, Katsanis N: Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425: 628-633, 2003
105. Kim JC, Badano JL, Sibold S, Esmail MA, Hill J, Hoskins BE, Leitch CC, Venner K, Ansley SJ, Ross AJ, Leroux MR, Katsanis N, Beales PL: The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat Genet 36: 462-470, 2004
106. Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, May-Simera H, Li H, Blacque OE, Li L, Leitch CC, Lewis RA, Green JS, Parfrey PS, Leroux MR, Davidson WS, Beales PL, Guay-Woodford LM, Yoder BK, Stormo GD, Katsanis N, Dutcher SK: Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117: 541-552, 2004
107. Blacque OE, Reardon MJ, Li C, McCarthy J, Mahjoub MR, Ansley SJ, Badano JL, Mah AK, Beales PL, Davidson WS, Johnsen RC, Audeh M, Plasterk RHA, Maillie DL, Katsanis N, Quarmby LM, Wicks SR, Leroux MR: Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. Genes Dev 18: 1630-1642, 2004
108. Mykytyn K, Mullins RF, Andrews M, Chiang AP, Swiderski RE, Yang B, Braun T, Casavant T, Stone EM, Sheffield VC: Bardet-Biedl syndrome type 4 (BBS4)-null mice implicate Bbs4 in flagella formation but not global cilia assembly. Proc Natl Acad Sci U S A 101: 8664-8669, 2004
109. Romio L, Wright V, Price K, Winyard PJ, Donnai D, Porteous ME, Franco B, Giorgio G, Malcolm S, Woolf AS, Feather SA: OFD1, the gene mutated in oral-facial-digital syndrome type 1, is expressed in the metanephros and in human embryonic renal mesenchymal cells. J Am Soc Nephrol 14: 680-689, 2003
110. Ferrante MI, Giorgio G, Feather SA, Bulfone A, Wright V, Ghiani M, Selicorni A, Gammaro L, Scolari F, Woolf AS, Sylvie O, Bernard L, Malcolm S, Winter R, Ballabio A, Franco B: Identification of the gene for oral-facial-digital type I syndrome. Am J Hum Genet 68: 569-576, 2001
111. Lacy ER, Luciano L, Reale E: Flagellar cells and ciliary cells in the renal tubule of elasmobranchs. J Exp Zool Suppl 2: 186-192, 1989