Control of the Wnt pathways by nephrocystin-4 is required for morphogenesis of the zebrafish pronephros

Human Molecular Genetics

Volumn 20, Issue 13, 2011, Pages 2611-2627

  Burcklé, Céline ^a,b,c,d   Gaudé, Helori Mael ^a,c   Vesque, Christine ^b,d   Silbermann, Flora ^a,c   Salomon, Rémi ^a,c   Jeanpierre, Cécile ^a,c   Antignac, Corinne ^a,c   Saunier, Sophie ^a,c   Schneider Maunoury, Sylvie ^b,d  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DISHEVELLED PROTEIN; GENE PRODUCT; INVERSIN; NEPHROCYSTIN 4; PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL POLARITY; CELLULAR DISTRIBUTION; CLOACA; CONTROLLED STUDY; EMBRYO; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CELL; MAMMAL CELL; MORPHOGENESIS; NEPHRONOPHTHISIS; NONHUMAN; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; ZEBRA FISH;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BETA CATENIN; CELL LINE; CILIA; DOGS; HEK293 CELLS; HUMANS; MITOSIS; MORPHOGENESIS; PHENOTYPE; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; WNT PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; MAMMALIA;

EID: 79958745491     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr164     Document Type: Article

References (67)

1. Davis, E.E., Zhang, Q., Liu, Q., Diplas, B.H., Davey, L.M., Hartley, J., Stoetzel, C., Szymanska, K., Ramaswami, G., Logan, C.V. et al. (2011) TTC21B contributes both causal and modifying alleles across the ciliopathy spectrum. Nat. Genet., 43, 189-196.
2. Hurd, T.W. and Hildebrandt, F. (2011) Mechanisms of nephronophthisis and related ciliopathies. Nephron Exp. Nephrol., 118, e9-14.
3. Cardenas-Rodriguez, M. and Badano, J.L. (2009) Ciliary biology: understanding the cellular and genetic basis of human ciliopathies. Am. J. Med. Genet. C: Semin. Med. Genet., 151C, 263-280.
4. Sharma, N., Berbari, N.F. and Yoder, B.K. (2008) Ciliary dysfunction in developmental abnormalities and diseases. Curr. Top. Dev. Biol., 85, 371-427.
5. Pedersen, L.B. and Rosenbaum, J.L. (2008) Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr. Top. Dev. Biol., 85, 23-61.
6. Jin, H. and Nachury, M.V. (2009) The BBSome. Curr. Biol., 19, R472-473.
7. Tammachote, R., Hommerding, C.J., Sinders, R.M., Miller, C.A., Czarnecki, P.G., Leightner, A.C., Salisbury, J.L., Ward, C.J., Torres, V.E., Gattone, V.H., II et al. (2009) Ciliary and centrosomal defects associated with mutation and depletion of the Meckel syndrome genes MKS1 and MKS3. Hum. Mol. Genet., 18, 3311-3323.
8. Williams, C.L., Masyukova, S.V. and Yoder, B.K. (2010) Normal ciliogenesis requires synergy between the cystic kidney disease genes MKS-3 and NPHP-4. J. Am. Soc. Nephrol., 21, 782-793.
9. Hoefele, J., Sudbrak, R., Reinhardt, R., Lehrack, S., Hennig, S., Imm, A., Muerb, U., Utsch, B., Attanasio, M., O'Toole, J.F. et al. (2005) Mutational analysis of the NPHP4 gene in 250 patients with nephronophthisis. Hum. Mutat., 25, 411.
10. Mollet, G., Salomon, R., Gribouval, O., Silbermann, F., Bacq, D., Landthaler, G., Milford, D., Nayir, A., Rizzoni, G., Antignac, C. et al. (2002) The gene mutated in juvenile nephronophthisis type 4 encodes a novel protein that interacts with nephrocystin. Nat. Genet., 32, 300-305.
11. Delous, M., Hellman, N.E., Gaude, H.M., Silbermann, F., Le Bivic, A., Salomon, R., Antignac, C. and Saunier, S. (2009) Nephrocystin-1 and nephrocystin-4 are required for epithelial morphogenesis and associate with PALS1/PATJ and Par6. Hum. Mol. Genet., 18, 4711-4723.
12. Mollet, G., Silbermann, F., Delous, M., Salomon, R., Antignac, C. and Saunier, S. (2005) Characterization of the nephrocystin/nephrocystin-4 complex and subcellular localization of nephrocystin-4 to primary cilia and centrosomes. Hum. Mol. Genet., 14, 645-656.
13. Wiik, A.C., Wade, C., Biagi, T., Ropstad, E.O., Bjerkas, E., Lindblad-Toh, K. and Lingaas, F. (2008) A deletion in nephronophthisis 4 (NPHP4) is associated with recessive cone-rod dystrophy in standard wire-haired dachshund. Genome Res., 18, 1415-1421.
14. Won, J., Marin de Evsikova, C., Smith, R.S., Hicks, W.L., Edwards, M.M., Longo-Guess, C., Li, T., Naggert, J.K. and Nishina, P.M. (2011) NPHP4 is necessary for normal photoreceptor ribbon synapse maintenance and outer segment formation, and for sperm development. Hum. Mol. Genet., 20, 482-496.
15. Lin, F., Hiesberger, T., Cordes, K., Sinclair, A.M., Goldstein, L.S., Somlo, S. and Igarashi, P. (2003) 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.
16. Murcia, N.S., Richards, W.G., Yoder, B.K., Mucenski, M.L., Dunlap, J.R. and Woychik, R.P. (2000) The Oak Ridge Polycystic Kidney (ORPK) disease gene is required for left-right axis determination. Development, 127, 2347-2355.
17. Otto, E.A., Schermer, B., Obara, T., O'Toole, J.F., Hiller, K.S., Mueller, A.M., Ruf, R.G., Hoefele, J., Beekmann, F., Landau, D. et al. (2003) 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.
18. Pazour, G.J., Dickert, B.L., Vucica, Y., Seeley, E.S., Rosenbaum, J.L., Witman, G.B. and Cole, D.G. (2000) 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.
19. Menezes, L.F. and Germino, G.G. (2009) Polycystic kidney disease, cilia, and planar polarity. Methods Cell Biol., 94, 273-297.
20. Kramer-Zucker, A.G., Olale, F., Haycraft, C.J., Yoder, B.K., Schier, A.F. and Drummond, I.A. (2005) Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development, 132, 1907-1921.
21. Obara, T., Mangos, S., Liu, Y., Zhao, J., Wiessner, S., Kramer-Zucker, A.G., Olale, F., Schier, A.F. and Drummond, I.A. (2006) Polycystin-2 immunolocalization and function in zebrafish. J. Am. Soc. Nephrol., 17, 2706-2718.
22. Sayer, J.A., Otto, E.A., O'Toole, J.F., Nurnberg, G., Kennedy, M.A., Becker, C., Hennies, H.C., Helou, J., Attanasio, M., Fausett, B.V. et al. (2006) The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat. Genet., 38, 674-681.
23. Sun, Z., Amsterdam, A., Pazour, G.J., Cole, D.G., Miller, M.S. and Hopkins, N. (2004) A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development, 131, 4085-4093.
24. Tsujikawa, M. and Malicki, J. (2004) Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron, 42, 703-716.
25. Zhou, W., Dai, J., Attanasio, M. and Hildebrandt, F. (2010) Nephrocystin-3 is required for ciliary function in zebrafish embryos. Am. J. Physiol. Renal Physiol., 299, F55-62.
26. Liu, Y., Pathak, N., Kramer-Zucker, A. and Drummond, I.A. (2007) Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros. Development, 134, 1111-1122.
27. Ma, M. and Jiang, Y.J. (2007) Jagged2a-notch signaling mediates cell fate choice in the zebrafish pronephric duct. PLoS Genet., 3, e18.
28. Sullivan-Brown, J., Schottenfeld, J., Okabe, N., Hostetter, C.L., Serluca, F.C., Thiberge, S.Y. and Burdine, R.D. (2008) Zebrafish mutations affecting cilia motility share similar cystic phenotypes and suggest a mechanism of cyst formation that differs from pkd2 morphants. Dev. Biol., 314, 261-275.
29. Karner, C.M., Chirumamilla, R., Aoki, S., Igarashi, P., Wallingford, J.B. and Carroll, T.J. (2009) Wnt9b signaling regulates planar cell polarity and kidney tubule morphogenesis. Nat. Genet., 41, 793-799.
30. Saburi, S., Hester, I., Fischer, E., Pontoglio, M., Eremina, V., Gessler, M., Quaggin, S.E., Harrison, R., Mount, R. and McNeill, H. (2008) Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet., 40, 1010-1015.
31. Wallingford, J.B. (2010) Planar cell polarity signaling, cilia and polarized ciliary beating. Curr. Opin. Cell Biol., 22, 597-604.
32. Cao, Y., Park, A. and Sun, Z. (2010) Intraflagellar transport proteins are essential for cilia formation and for planar cell polarity. J. Am. Soc. Nephrol., 21, 1326-1333.
33. Skouloudaki, K., Puetz, M., Simons, M., Courbard, J.R., Boehlke, C., Hartleben, B., Engel, C., Moeller, M.J., Englert, C., Bollig, F. et al. (2009) Scribble participates in Hippo signaling and is required for normal zebrafish pronephros development. Proc. Natl Acad. Sci. USA, 106, 8579-8584.
34. Simons, M., Gloy, J., Ganner, A., Bullerkotte, A., Bashkurov, M., Kronig, C., Schermer, B., Benzing, T., Cabello, O.A., Jenny, A. et al. (2005) Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet., 37, 537-543.
35. Gerdes, J.M., Davis, E.E. and Katsanis, N. (2009) The vertebrate primary cilium in development, homeostasis, and disease. Cell, 137, 32-45.
36. Yin, C., Ciruna, B. and Solnica-Krezel, L. (2009) Convergence and extension movements during vertebrate gastrulation. Curr. Top. Dev. Biol., 89, 163-192.
37. Shu, X., Zeng, Z., Gautier, P., Lennon, A., Gakovic, M., Patton, E.E. and Wright, A.F. (2010) Zebrafish Rpgr is required for normal retinal development and plays a role in dynein-based retrograde transport processes. Hum. Mol. Genet., 19, 657-670.
38. Wingert, R.A., Selleck, R., Yu, J., Song, H.D., Chen, Z., Song, A., Zhou, Y., Thisse, B., Thisse, C., McMahon, A.P. et al. (2007) The cdx genes and retinoic acid control the positioning and segmentation of the zebrafish pronephros. PLoS Genet., 3, 1922-1938.
39. Pyati, U.J., Cooper, M.S., Davidson, A.J., Nechiporuk, A. and Kimelman, D. (2006) Sustained Bmp signaling is essential for cloaca development in zebrafish. Development, 133, 2275-2284.
40. van der Hoeven, F., Sordino, P., Fraudeau, N., Izpisua-Belmonte, J.C. and Duboule, D. (1996) Teleost HoxD and HoxA genes: comparison with tetrapods and functional evolution of the HOXD complex. Mech. Dev., 54, 9-21.
41. Jessen, J.R., Topczewski, J., Bingham, S., Sepich, D.S., Marlow, F., Chandrasekhar, A. and Solnica-Krezel, L. (2002) Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell Biol., 4, 610-615.
42. Tada, M. and Smith, J.C. (2000) Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development, 127, 2227-2238.
43. Dorsky, R.I., Sheldahl, L.C. and Moon, R.T. (2002) A transgenic Lef1/beta-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev. Biol., 241, 229-237.
44. Vasilyev, A., Liu, Y., Mudumana, S., Mangos, S., Lam, P.Y., Majumdar, A., Zhao, J., Poon, K.L., Kondrychyn, I., Korzh, V. et al. (2009) Collective cell migration drives morphogenesis of the kidney nephron. PLoS Biol., 7, e9.
45. Davenport, J.R., Watts, A.J., Roper, V.C., Croyle, M.J., van Groen, T., Wyss, J.M., Nagy, T.R., Kesterson, R.A. and Yoder, B.K. (2007) Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr. Biol., 17, 1586-1594.
46. Happe, H., Leonhard, W.N., van der Wal, A., van de Water, B., Lantinga-van Leeuwen, I.S., Breuning, M.H., de Heer, E. and Peters, D.J. (2009) Toxic tubular injury in kidneys from Pkd1-deletion mice accelerates cystogenesis accompanied by dysregulated planar cell polarity and canonical Wnt signaling pathways. Hum. Mol. Genet., 18, 2532-2542.
47. Lancaster, M.A., Louie, C.M., Silhavy, J.L., Sintasath, L., Decambre, M., Nigam, S.K., Willert, K. and Gleeson, J.G. (2009) Impaired Wnt-beta-catenin signaling disrupts adult renal homeostasis and leads to cystic kidney ciliopathy. Nat. Med., 15, 1046-1054.
48. Varelas, X., Miller, B.W., Sopko, R., Song, S., Gregorieff, A., Fellouse, F.A., Sakuma, R., Pawson, T., Hunziker, W., McNeill, H. et al. (2010) The Hippo pathway regulates Wnt/beta-catenin signaling. Dev. Cell, 18, 579-591.
49. Saadi-Kheddouci, S., Berrebi, D., Romagnolo, B., Cluzeaud, F., Peuchmaur, M., Kahn, A., Vandewalle, A. and Perret, C. (2001) Early development of polycystic kidney disease in transgenic mice expressing an activated mutant of the beta-catenin gene. Oncogene, 20, 5972-5981.
50. Sansom, O.J., Griffiths, D.F., Reed, K.R., Winton, D.J. and Clarke, A.R. (2005) Apc deficiency predisposes to renal carcinoma in the mouse. Oncogene, 24, 8205-8210.
51. Gottardi, C.J., Wong, E. and Gumbiner, B.M. (2001) E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J. Cell. Biol., 153, 1049-1060.
52. Morgan, D., Eley, L., Sayer, J., Strachan, T., Yates, L.M., Craighead, A.S. and Goodship, J.A. (2002) 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.
53. Lienkamp, S., Ganner, A., Boehlke, C., Schmidt, T., Arnold, S.J., Schafer, T., Romaker, D., Schuler, J., Hoff, S., Powelske, C. et al. (2010) Inversin relays Frizzled-8 signals to promote proximal pronephros development. Proc. Natl Acad. Sci. USA, 107, 20388-20393.
54. Matsumoto, S., Fumoto, K., Okamoto, T., Kaibuchi, K. and Kikuchi, A. (2010) Binding of APC and dishevelled mediates Wnt5a-regulated focal adhesion dynamics in migrating cells. EMBO J., 29, 1192-1204.
55. Elbert, M., Cohen, D. and Musch, A. (2006) PAR1b promotes cell-cell adhesion and inhibits dishevelled-mediated transformation of Madin-Darby canine kidney cells. Mol. Biol. Cell, 17, 3345-3355.
56. Park, T.J., Mitchell, B.J., Abitua, P.B., Kintner, C. and Wallingford, J.B. (2008) Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat. Genet., 40, 871-879.
57. Tory, K., Rousset-Rouviere, C., Gubler, M.C., Moriniere, V., Pawtowski, A., Becker, C., Guyot, C., Gie, S., Frishberg, Y., Nivet, H. et al. (2009) Mutations of NPHP2 and NPHP3 in infantile nephronophthisis. Kidney Int., 75, 839-847.
58. Bellavia, S., Dahan, K., Terryn, S., Cosyns, J.P., Devuyst, O. and Pirson, Y. (2010) A homozygous mutation in INVS causing juvenile nephronophthisis with abnormal reactivity of the Wnt/beta-catenin pathway. Nephrol. Dial. Transplant., 25, 4097-4102.
59. Haas, P. and Gilmour, D. (2006) Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev. Cell, 10, 673-680.
60. Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B. and Schilling, T.F. (1995) Stages of embryonic development of the zebrafish. Dev. Dyn., 203, 253-310.
61. Zufferey, R., Dull, T., Mandel, R.J., Bukovsky, A., Quiroz, D., Naldini, L. and Trono, D. (1998) Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol., 72, 9873-9880.
62. Park, M. and Moon, R.T. (2002) The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat. Cell Biol., 4, 20-25.
63. Carreira-Barbosa, F., Concha, M.L., Takeuchi, M., Ueno, N., Wilson, S.W. and Tada, M. (2003) Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development, 130, 4037-4046.
64. Lecaudey, V., Anselme, I., Rosa, F. and Schneider-Maunoury, S. (2004) The zebrafish Iroquois gene iro7 positions the r4/r5 boundary and controls neurogenesis in the rostral hindbrain. Development, 131, 3121-3131.
65. Bisgrove, B.W., Snarr, B.S., Emrazian, A. and Yost, H.J. (2005) Polaris and Polycystin-2 in dorsal forerunner cells and Kupffer's vesicle are required for specification of the zebrafish left-right axis. Dev. Biol., 287, 274-288.
66. Khelfaoui, M., Denis, C., van Galen, E., de Bock, F., Schmitt, A., Houbron, C., Morice, E., Giros, B., Ramakers, G., Fagni, L. et al. (2007) Loss of X-linked mental retardation gene oligophrenin1 in mice impairs spatial memory and leads to ventricular enlargement and dendritic spine immaturity. J. Neurosci., 27, 9439-9450.
67. Drummond, I.A. (2005) Kidney development and disease in the zebrafish. J. Am. Soc. Nephrol., 16, 299-304.