Disruption of IFT Complex a causes cystic kidneys without mitotic spindle misorientation

Journal of the American Society of Nephrology

Volumn 23, Issue 4, 2012, Pages 641-651

  Jonassen, Julie A ^a   SanAgustin, Jovenal ^a   Baker, Stephen P ^a   Pazour, Gregory J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CRE RECOMBINASE; INTRAFLAGELLAR TRANSPORT COMPLEX A PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIVISION; CELL PROLIFERATION; CENTROSOME; CONTROLLED STUDY; GENE; GENE DELETION; GENE FUNCTION; IFT140 GENE; INTRAFLAGELLAR TRANSPORT; KIDNEY COLLECTING TUBULE; KIDNEY CYST; KIDNEY DEVELOPMENT; KIDNEY DISEASE; KIDNEY DYSFUNCTION; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY POLYCYSTIC DISEASE; MITOSIS SPINDLE; MOUSE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL;

EID: 84859863721     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2011080829     Document Type: Article

References (66)

1. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK: The primary cilium as a complex signaling center. Curr Biol 19: R526-R535, 2009
2. Pedersen LB, Rosenbaum JL: Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85: 23-61, 2008
3. Satir P, Christensen ST: Structure and function of mammalian cilia. Histochem Cell Biol 129: 687-693, 2008
4. Pazour GJ: Intraflagellar transport and cilia-dependent renal disease: The ciliary hypothesis of polycystic kidney disease. J Am Soc Nephrol 15: 2528-2536, 2004
5. Gallagher AR,GerminoGG, Somlo S:Molecular advances in autosomal dominant polycystic kidney disease. Adv Chronic Kidney Dis 17: 118-130, 2010
6. Harris PC, Torres VE: Polycystic kidney disease. Annu RevMed 60: 321-337, 2009
7. 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 (Pubitemid 28243966)
8. Scholey JM: Intraflagellar transport motors in cilia: Moving along the cell's antenna. J Cell Biol 180: 23-29, 2008
9. Cole DG, Snell WJ: SnapShot: Intraflagellar transport. Cell 137: 784-784.e1, 2009
10. Ou G, KogaM, Blacque OE, Murayama T, Ohshima Y, Schafer JC, Li C, Yoder BK, LerouxMR, Scholey JM: Sensory ciliogenesis in Caenorhabditis elegans: Assignment of IFT components into distinct modules based on transport and phenotypic profiles. Mol Biol Cell 18: 1554-1569, 2007 (Pubitemid 46717540)
11. Follit JA, Xu F, Keady BT, Pazour GJ: Characterization of mouse IFT complex B. Cell Motil Cytoskeleton 66: 457-468, 2009
12. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG: Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117: 456-487, 1986
13. 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
14. 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 (Pubitemid 30386574)
15. 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 (Pubitemid 37432545)
16. Jonassen JA, San Agustin J, Follit JA, Pazour GJ: Deletion of IFT20 in the mouse kidney causes misorientation of the mitotic spindle and cystic kidney disease. J Cell Biol 183: 377-384, 2008
17. 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 USA 96: 5043-5048, 1999 (Pubitemid 29214532)
18. Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, Kanai Y, Kido M, HirokawaN: 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 (Pubitemid 29014462)
19. 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 USA 100: 5286-5291, 2003 (Pubitemid 36542697)
20. Absalon S, Blisnick T, Kohl L, Toutirais G, Doré G, Julkowska D, Tavenet A, Bastin P: Intraflagellar transport and functional analysis of genes required for flagellum formation in trypanosomes. Mol Biol Cell 19: 929-944, 2008 (Pubitemid 351481809)
21. 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 (Pubitemid 32241525)
22. Absalon S, Blisnick T, Bonhivers M, Kohl L, Cayet N, Toutirais G, Buisson J, Robinson D, Bastin P: Flagellum elongation is required for correct structure, orientation and function of the flagellar pocket in Trypanosoma brucei. J Cell Sci 121: 3704-3716, 2008
23. Lee E, Sivan-Loukianova E, Eberl DF, Kernan MJ: An IFT-A protein is required to delimit functionally distinct zones in mechanosensory cilia. Curr Biol 18: 1899-1906, 2008
24. Blacque OE, Li C, Inglis PN, Esmail MA, Ou G, Mah AK, Baillie DL, Scholey JM, Leroux MR: The WD repeat-containing protein IFTA-1 is required for retrograde intraflagellar transport.Mol Biol Cell 17: 5053-5062, 2006 (Pubitemid 44907350)
25. Iomini C, Babaev-Khaimov V, Sassaroli M, Piperno G: Protein particles in Chlamydomonas flagella undergo a transport cycle consisting of four phases. J Cell Biol 153: 13-24, 2001 (Pubitemid 34280190)
26. Iomini C, Li L, Esparza JM, Dutcher SK: Retrograde intraflagellar transport mutants identify complex A proteins with multiple genetic interactions in Chlamydomonas reinhardtii. Genetics 183: 885-896, 2009
27. Mukhopadhyay S, Wen X, Chih B, Nelson CD, Lane WS, Scales SJ, Jackson PK: TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia. Genes Dev 24: 2180-2193, 2010
28. Tran PV, Haycraft CJ, Besschetnova TY, Turbe-Doan A, Stottmann RW, Herron BJ, Chesebro AL, Qiu H, Scherz PJ, Shah JV, Yoder BK, Beier DR: THM1 negatively modulates mouse sonic hedgehog signal transduction and affects retrograde intraflagellar transport in cilia. Nat Genet 40: 403-410, 2008 (Pubitemid 351450878)
29. Cortellino S, Wang C, Wang B, Bassi MR, Caretti E, Champeval D, Calmont A, Jarnik M, Burch J, Zaret KS, Larue L, Bellacosa A: Defective ciliogenesis, embryonic lethality and severe impairment of the Sonic Hedgehog pathway caused by inactivation of the mouse complex A intraflagellar transport gene Ift122/Wdr10, partially overlapping with the DNA repair gene Med1/Mbd4. Dev Biol 325: 225-237, 2009
30. Qin J, Lin Y, Norman RX, Ko HW, Eggenschwiler JT: Intraflagellar transport protein 122 antagonizes Sonic Hedgehog signaling and controls ciliary localization of pathway components. Proc Natl Acad Sci USA 108: 1456-1461, 2011
31. Mill P, Lockhart PJ, Fitzpatrick E, Mountford HS, Hall EA, Reijns MA, Keighren M, Bahlo M, Bromhead CJ, Budd P, Aftimos S, Delatycki MB, Savarirayan R, Jackson IJ, Amor DJ: Human and mouse mutations in WDR35 cause short-rib polydactyly syndromes due to abnormal ciliogenesis. Am J Hum Genet 88: 508-515, 2011
32. Walczak-Sztulpa J, Eggenschwiler J, Osborn D, Brown DA, Emma F, Klingenberg C, Hennekam RC, Torre G, Garshasbi M, Tzschach A, Szczepanska M, Krawczynski M, Zachwieja J, Zwolinska D, Beales PL, Ropers HH, Latos-Bielenska A, Kuss AW: Cranioectodermal Dysplasia, Sensenbrenner syndrome, is a ciliopathy caused by mutations in the IFT122 gene. Am J Hum Genet 86: 949-956, 2010
33. Tsujikawa M, Malicki J: Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron 42: 703-716, 2004 (Pubitemid 38748786)
34. Gilissen C, Arts HH, Hoischen A, Spruijt L, Mans DA, Arts P, van Lier B, Steehouwer M, van Reeuwijk J, Kant SG, Roepman R, Knoers NV, Veltman JA, BrunnerHG: Exome sequencing identifiesWDR35 variants involved in Sensenbrenner syndrome. Am J Hum Genet 87: 418-423, 2010
35. Arts HH, Bongers EM, Mans DA, van Beersum SE, Oud MM, Bolat E, Spruijt L, Cornelissen EA, Schuurs-Hoeijmakers JH, de Leeuw N, Cormier-Daire V, Brunner HG, Knoers NV, Roepman R: C14ORF179 encoding IFT43 is mutated in Sensenbrenner syndrome. J Med Genet 48: 390-395, 2011
36. Zaffanello M, Diomedi-Camassei F, Melzi ML, Torre G, Callea F, Emma F: Sensenbrenner syndrome: A new member of the hepatorenal fibrocystic family. Am J Med Genet A 140: 2336-2340, 2006 (Pubitemid 44684961)
37. Austin CP, Battey JF, Bradley A, Bucan M, Capecchi M, Collins FS, Dove WF, Duyk G, Dymecki S, Eppig JT, Grieder FB, Heintz N, Hicks G, Insel TR, Joyner A, Koller BH, Lloyd KC, Magnuson T, Moore MW, Nagy A, Pollock JD, Roses AD, Sands AT, Seed B, Skarnes WC, Snoddy J, Soriano P, Stewart DJ, Stewart F, Stillman B, Varmus H, Varticovski L, Verma IM, Vogt TF, von Melchner H, Witkowski J, Woychik RP, Wurst W, Yancopoulos GD, Young SG, Zambrowicz B: The knockout mouse project. Nat Genet 36: 921-924, 2004 (Pubitemid 351319639)
38. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M, Harrow J, Cox T, Jackson D, Severin J, Biggs P, Fu J, Nefedov M, de Jong PJ, Stewart AF, Bradley A: A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474: 337-342, 2011
39. Deane JA, Cole DG, Seeley ES, Diener DR, Rosenbaum JL: Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr Biol 11: 1586-1590, 2001
40. Follit JA, Tuft RA, Fogarty KE, Pazour GJ: The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol Biol Cell 17: 3781-3792, 2006 (Pubitemid 44330865)
41. Robert A, Margall-Ducos G, Guidotti JE, Brégerie O, Celati C, Bréchot C, Desdouets C: The intraflagellar transport component IFT88/polaris is a centrosomal protein regulating G1-S transition in non-ciliated cells. J Cell Sci 120: 628-637, 2007 (Pubitemid 46437897)
42. Delaval B, Bright A, Lawson ND, Doxsey S: The cilia protein IFT88 is required for spindle orientation in mitosis. Nat Cell Biol 13: 461-468, 2011
43. Yu J, Carroll TJ, McMahon AP: Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 129: 5301-5312, 2002 (Pubitemid 35460691)
44. Costantini F, Kopan R: Patterning a complex organ: Branching morphogenesis and nephron segmentation in kidney development. Dev Cell 18: 698-712, 2010
45. Fischer E, Legue E, Doyen A, Nato F, Nicolas JF, Torres V, Yaniv M, Pontoglio M: Defective planar cell polarity in polycystic kidney disease. Nat Genet 38: 21-23, 2006 (Pubitemid 43011877)
46. Saburi S, Hester I, Fischer E, Pontoglio M, Eremina V, Gessler M, Quaggin SE, Harrison R, Mount R,McNeill H: Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat Genet 40: 1010-1015, 2008
47. Goilav B: Apoptosis in polycystic kidney disease. BiochimBiophys Acta 1812: 1272-1280, 2011
48. Saadi-Kheddouci S, Berrebi D, Romagnolo B, Cluzeaud F, Peuchmaur M, Kahn A, Vandewalle A, Perret C: Early development of polycystic kidney disease in transgenicmice expressing an activatedmutant of the beta-catenin gene. Oncogene 20: 5972-5981, 2001 (Pubitemid 32955039)
49. Merkel CE, Karner CM, Carroll TJ: Molecular regulation of kidney development: is the answer blowing in the Wnt? Pediatr Nephrol 22: 1825-1838, 2007 (Pubitemid 47506222)
50. Reidy KJ, Rosenblum ND: Cell and molecular biology of kidney development. Semin Nephrol 29: 321-337, 2009
51. Wong SY, Reiter JF: The primary ciliumat the crossroads of mammalian hedgehog signaling. Curr Top Dev Biol 85: 225-260, 2008
52. Happé H, van der Wal AM, Leonhard WN, Kunnen SJ, Breuning MH, de Heer E, Peters DJ: Altered Hippo signalling in polycystic kidney disease. J Pathol 224: 133-142, 2011
53. Mrug M, Zhou J,Woo Y, Cui X, Szalai AJ, Novak J, Churchill GA, Guay- Woodford LM: Overexpression of innate immune response genes in a model of recessive polycystic kidney disease. Kidney Int 73: 63-76, 2008 (Pubitemid 350273645)
54. Pigino G, Geimer S, Lanzavecchia S, Paccagnini E, Cantele F, Diener DR, Rosenbaum JL, Lupetti P: Electron-tomographic analysis of intraflagellar transport particle trains in situ. J Cell Biol 187: 135-148, 2009
55. Nishio S, Tian X, Gallagher AR, Yu Z, Patel V, Igarashi P, Somlo S: Loss of oriented cell division does not initiate cyst formation. JAmSocNephrol 21: 295-302, 2010
56. Hu B, He X, Li A, Qiu Q, Li C, Liang D, Zhao P, Ma J, Coffey RJ, Zhan Q, Wu G: Cystogenesis in ARPKD results from increased apoptosis in collecting duct epithelial cells of Pkhd1 mutant kidneys. Exp Cell Res 317: 173-187, 2011
57. Ostrom L, Tang MJ, Gruss P, Dressler GR: Reduced Pax2 gene dosage increases apoptosis and slows the progression of renal cystic disease. Dev Biol 219: 250-258, 2000 (Pubitemid 30152603)
58. Soucek L, Evan GI: The ups and downs of Myc biology. CurrOpinGenet Dev 20: 91-95, 2010
59. Habbig S, Bartram MP, Müller RU, Schwarz R, Andriopoulos N, Chen S, Sägmüller JG, Hoehne M, Burst V, Liebau MC, Reinhardt HC, Benzing T, Schermer B: NPHP4, a cilia-associated protein, negatively regulates the Hippo pathway. J Cell Biol 193: 633-642, 2011
60. Norman J: Fibrosis and progression of autosomal dominant polycystic kidney disease (ADPKD). Biochim Biophys Acta 1812: 1327-1336, 2011
61. Zhou J, Ouyang X, Cui X, Schoeb TR, Smythies LE, Johnson MR, Guay-Woodford LM, Chapman AB, Mrug M: Renal CD14 expression correlateswith the progression of cystic kidneydisease. Kidney Int 78: 550-560, 2010
62. Davenport JR, Watts AJ, Roper VC, Croyle MJ, van Groen T, Wyss JM, Nagy TR, Kesterson RA, Yoder BK: Disruption of intraflagellar transport in adultmice leads to obesity and slow-onset cystic kidney disease. Curr Biol 17: 1586-1594, 2007 (Pubitemid 47380400)
63. Patel V, Li L, Cobo-Stark P, Shao X, Somlo S, Lin F, Igarashi P: Acute kidney injury and aberrant planar cell polarity induce cyst formation in mice lacking renal cilia. Hum Mol Genet 17: 1578-1590, 2008 (Pubitemid 351737162)
64. O'Gorman S, Dagenais NA, Qian M, Marchuk Y: Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. ProcNatl Acad Sci USA 94: 14602-14607, 1997 (Pubitemid 28041420)
65. Farley FW, Soriano P, Steffen LS, Dymecki SM: Widespread recombinase expression using FLPeR (flipper) mice. Genesis 28: 106-110, 2000
66. PazourGJ, SanAgustin 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 (Pubitemid 34689219)