Inversin, Wnt signaling and primary cilia

Differentiation

Volumn 83, Issue 2, 2012, Pages

  Lienkamp, Soeren ^a   Ganner, Athina ^a   Walz, Gerd ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Cilia; Cystic kidney disease; Inversin; Nephronophthisis; Planar cell polarity

Indexed keywords

ANAPC2 PROTEIN; ANAPHASE PROMOTING COMPLEX; ANKYRIN; BETA CATENIN; DISHEVELLED PROTEIN; FRIZZLED 8 PROTEIN; FRIZZLED PROTEIN; INVERSIN; NEPHROCYSTIN; NEPHROCYSTIN 2; PROTEIN; PROTEIN DIEGO; PROTEIN FLAMINGO; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELL POLARITY; CILIARY MOTILITY; EUKARYOTIC FLAGELLUM; GENE MUTATION; GENE PRODUCT; HENLE LOOP; HUMAN; KIDNEY CYST; KIDNEY DEVELOPMENT; KIDNEY TUBULE; NEPHRONOPHTHISIS; NEPHRONOPHTHISIS TYPE 2; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PHOTORECEPTOR; PRIORITY JOURNAL; PRONEPHROS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RETINITIS PIGMENTOSA;

ANIMALS; CILIA; HUMANS; KIDNEY; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; WNT PROTEINS;

MAMMALIA; VERTEBRATA;

EID: 84856358351     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2011.11.012     Document Type: Article

References (70)

1. Axelrod J.D. Progress and challenges in understanding planar cell polarity signaling. Seminars in Cell and Developmental Biology 2009, 20:964-971.
2. Benzing T., Simons M., Walz G. Wnt signaling in polycystic kidney disease. Journal of American Society of Nephrology 2007, 18:1389-1398.
3. Bergmann C., Fliegauf M., Bruchle N.O., Frank V., Olbrich H., Kirschner J., Schermer B., Schmedding I., Kispert A., Kranzlin B., et al. Loss of nephrocystin-3 function can cause embryonic lethality, Meckel-Gruber-like syndrome, situs inversus, and renal-hepatic-pancreatic dysplasia. American Journal of Human Genetics 2008, 82:959-970.
4. Burckle C., Gaude H.M., Vesque C., Silbermann F., Salomon R., Jeanpierre C., Antignac C., Saunier S., Schneider-Maunoury S. Control of the Wnt pathways by nephrocystin-4 is required for morphogenesis of the zebrafish pronephros. Human Molecular Genetics 2011, 20:2611-2627.
5. Corbit K.C., Shyer A.E., Dowdle W.E., Gaulden J., Singla V., Reiter J.F. Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nature Cell Biology 2008, 10:70-76.
6. Deblandre G.A., Wettstein D.A., Koyano-Nakagawa N., Kintner C. A two-step mechanism generates the spacing pattern of the ciliated cells in the skin of Xenopus embryos. Development 1999, 126:4715-4728.
7. Dishinger J.F., Kee H.L., Jenkins P.M., Fan S., Hurd T.W., Hammond J.W., Truong Y.N., Margolis B., Martens J.R., Verhey K.J. Ciliary entry of the kinesin-2 motor KIF17 is regulated by importin-beta2 and RanGTP. Nature Cell Biology 2010, 12:703-710.
8. Feiguin F., Hannus M., Mlodzik M., Eaton S. The ankyrin repeat protein Diego mediates Frizzled-dependent planar polarization. Developmental Cell 2001, 1:93-101.
9. Ganner A., Lienkamp S., Schafer T., Romaker D., Wegierski T., Park T.J., Spreitzer S., Simons M., Gloy J., Kim E., et al. Regulation of ciliary polarity by the APC/C. Proceedings of the National academy of Sciences of the United States of America 2009, 106:17799-17804.
10. Gerdes J.M., Liu Y., Zaghloul N.A., Leitch C.C., Lawson S.S., Kato M., Beachy P.A., Beales P.L., Demartino G.N., Fisher S., et al. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nature Genetics 2007, 39:1350-1360.
11. Goodrich L.V., Strutt D. Principles of planar polarity in animal development. Development 2011, 138:1877-1892.
12. Happe H., Leonhard W.N., van der Wal A., van de Water B., Lantinga-van Leeuwen I.S., Breuning M.H., de Heer E., Peters D.J. Toxic tubular injury in kidneys from Pkd1-deletion mice accelerates cystogenesis accompanied by dysregulated planar cell polarity and canonical Wnt signaling pathways. Human Molecular Genetics 2009, 18:2532-2542.
13. Haribaskar R., Putz M., Schupp B., Skouloudaki K., Bietenbeck A., Walz G., Schafer T. The planar cell polarity (PCP) protein Diversin translocates to the nucleus to interact with the transcription factor AF9. Biochemical and Biophysical Research Communications 2009.
14. Hildebrandt F., Zhou W. Nephronophthisis-associated ciliopathies. Journal of the American Socirty of Nephrology 2007, 18:1855-1871.
15. Huang P., Schier A.F. Dampened Hedgehog signaling but normal Wnt signaling in zebrafish without cilia. Development 2009, 136:3089-3098.
16. Iglesias D.M., Hueber P.A., Chu L., Campbell R., Patenaude A.M., Dziarmaga A.J., Quinlan J., Mohamed O., Dufort D., Goodyer P.R. Canonical WNT signaling during kidney development. American Journal of Physiology Renal Physiology 2007, 293:F494-F500.
17. Jenny A., Mlodzik M. Planar cell polarity signaling: a common mechanism for cellular polarization. Mt. Sinai J. Med. 2006, 73:738-750.
18. 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. Nature Genetics 2009, 41:793-799.
19. Kim I., Ding T., Fu Y., Li C., Cui L., Li A., Lian P., Liang D., Wang D.W., Guo C., et al. Conditional mutation of Pkd2 causes cystogenesis and upregulates beta-catenin. Journal of the American Society of Nephrology: JASN 2009, 20:2556-2569.
20. Lancaster M.A., Gleeson J.G. Cystic kidney disease: the role of Wnt signaling. Trends in Molecular Medicine 2010, 16:349-360.
21. Lancaster M.A., Louie C.M., Silhavy J.L., Sintasath L., Decambre M., Nigam S.K., Willert K., Gleeson J.G. Impaired Wnt-beta-catenin signaling disrupts adult renal homeostasis and leads to cystic kidney ciliopathy. Nature Medicine 2009, 15:1046-1054.
22. Lancaster M.A., Schroth J., Gleeson J.G. Subcellular spatial regulation of canonical Wnt signalling at the primary cilium. Nature Cell Biology 2011, 13:700-707.
23. Lester J.T., DeLuca N.A. Herpes simplex virus 1 ICP4 forms complexes with TFIID and mediator in virus-infected cells. Journal of Virology 2011, 85:5733-5744.
24. Lienkamp S., Ganner A., Boehlke C., Schmidt T., Arnold S.J., Schafer T., Romaker D., Schuler J., Hoff S., Powelske C., et al. Inversin relays Frizzled-8 signals to promote proximal pronephros development. Proceedings of the National academy of Sciences of the United States of America 2010, 107:20388-20393.
25. 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. Proceedings of the National academy of Sciences of the United States of America 2003, 100:5286-5291.
26. Macca M., Franco B. The molecular basis of oral-facial-digital syndrome, type 1. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics 2009, 151C:318-325.
27. Maretto S., Cordenonsi M., Dupont S., Braghetta P., Broccoli V., Hassan A.B., Volpin D., Bressan G.M., Piccolo S. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proceedings of the National academy of Sciences of the United States of America 2003, 100:3299-3304.
28. McNeill H. Planar cell polarity: keeping hairs straight is not so simple. Cold Spring Harbor Perspectives in Biology 2010, 2:a003376.
29. Mitchell B., Jacobs R., Li J., Chien S., Kintner C. A positive feedback mechanism governs the polarity and motion of motile cilia. Nature 2007, 447:97-101.
30. Mochizuki T., Saijoh Y., Tsuchiya K., Shirayoshi Y., Takai S., Taya C., Yonekawa H., Yamada K., Nihei H., Nakatsuji N., et al. Cloning of inv, a gene that controls left/right asymmetry and kidney development. Nature 1998, 395:177-181.
31. Morgan D., Eley L., Sayer J., Strachan T., Yates L.M., Craighead A.S., Goodship J.A. 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. Human Molecular Genetics 2002, 11:3345-3350.
32. Morgan D., Goodship J., Essner J.J., Vogan K.J., Turnpenny L., Yost H.J., Tabin C.J., Strachan T. The left-right determinant inversin has highly conserved ankyrin repeat and IQ domains and interacts with calmodulin. Human Genetics 2002, 110:377-384.
33. Morgan D., Turnpenny L., Goodship J., Dai W., Majumder K., Matthews L., Gardner A., Schuster G., Vien L., Harrison W., et al. Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse. Nature Genetics 1998, 20:149-156.
34. Nonaka S., Tanaka Y., Okada Y., Takeda 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 1998, 95:829-837.
35. Nurnberger J., Bacallao R.L., Phillips C.L. Inversin forms a complex with catenins and N-cadherin in polarized epithelial cells. Molecular Biology of the Cell 2002, 13:3096-3106.
36. Nurnberger J., Kribben A., Opazo Saez A., Heusch G., Philipp T., Phillips C.L. The Invs gene encodes a microtubule-associated protein. Journal of the American Society of Nephrology 2004, 15:1700-1710.
37. O'Toole J.F., Otto E.A., Frishberg Y., Hildebrandt F. Retinitis pigmentosa and renal failure in a patient with mutations in INVS. Nephrology, dialysis, transplantation: Official Publication of the European Dialysis and Transplant Association-European Renal Association 2006, 21:1989-1991.
38. Ocbina P.J., Tuson M., Anderson K.V. Primary cilia are not required for normal canonical Wnt signaling in the mouse embryo. PLoS One 2009, 4:e6839.
39. Okada M., Sugimoto K., Shimada Y., Fujita S., Yanagida H., Yagi K., Takemura T. Association of INVS (NPHP2) mutation in an adolescent exhibiting nephronophthisis (NPH) and complete situs inversus. Clinical Nephrology 2008, 69:135-141.
40. Okada Y., Takeda S., Tanaka Y., Belmonte J.C., Hirokawa N. Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 2005, 121:633-644.
41. Otto E.A., Helou J., Allen S.J., O'Toole J.F., Wise E.L., Ashraf S., Attanasio M., Zhou W., Wolf M.T., Hildebrandt F. Mutation analysis in nephronophthisis using a combined approach of homozygosity mapping, CEL I endonuclease cleavage, and direct sequencing. Human Mutation 2008, 29:418-426.
42. 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. Mutations in INVS encoding inversin cause nephronophthisis type 2, linking renal cystic disease to the function of primary cilia and left-right axis determination. Nature Genetics 2003, 34:413-420.
43. Park T.J., Gray R.S., Sato A., Habas R., Wallingford J.B. Subcellular localization and signaling properties of dishevelled in developing vertebrate embryos. Current Biology 2005, 15:1039-1044.
44. Park T.J., Mitchell B.J., Abitua P.B., Kintner C., Wallingford J.B. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nature Genetics 2008, 40:871-879.
45. 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. Human Molecular Genetics 2008.
46. Phillips C.L., Miller K.J., Filson A.J., Nurnberger J., Clendenon J.L., Cook G.W., Dunn K.W., Overbeek P.A., Gattone V.H., Bacallao R.L. Renal cysts of inv/inv mice resemble early infantile nephronophthisis. Journal of the American Society of Nephrology 2004, 15:1744-1755.
47. Qian C.N., Knol J., Igarashi P., Lin F., Zylstra U., Teh B.T., Williams B.O. Cystic renal neoplasia following conditional inactivation of APC in mouse renal tubular epithelium. Journal of Biological Chemistry 2005, 280:3938-3945.
48. Raciti D., Reggiani L., Geffers L., Jiang Q., Bacchion F., Subrizi A.E., Clements D., Tindal C., Davidson D.R., Kaissling B., et al. Organization of the pronephric kidney revealed by large-scale gene expression mapping. Genome Biology 2008, 9:R84.
49. Roepman R., Wolfrum U. Protein networks and complexes in photoreceptor cilia. Subcell Biochemistry 2007, 43:209-235.
50. Ross A.J., May-Simera H., Eichers E.R., Kai M., Hill J., Jagger D.J., Leitch C.C., Chapple J.P., Munro P.M., Fisher S., et al. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nature Genetics 2005.
51. 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, 20:5972-5981.
52. 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. Nature Genetics 2008, 40:1010-1015.
53. Sang L., Miller J.J., Corbit K.C., Giles R.H., Brauer M.J., Otto E.A., Baye L.M., Wen X., Scales S.J., Kwong M., et al. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 2011, 145:513-528.
54. Shiba D., Manning D.K., Koga H., Beier D.R., Yokoyama T. Inv acts as a molecular anchor for Nphp3 and Nek8 in the proximal segment of primary cilia. Cytoskeleton 2010, 67:112-119.
55. Shiba D., Yamaoka Y., Hagiwara H., Takamatsu T., Hamada H., Yokoyama T. Localization of Inv in a distinctive intraciliary compartment requires the C-terminal ninein-homolog-containing region. Journal of Cell Science 2009, 122:44-54.
56. Simons M., Gloy J., Ganner A., Bullerkotte A., Bashkurov M., Kronig C., Schermer B., Benzing T., Cabello O.A., Jenny A., et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nature Genetics 2005, 37:537-543.
57. Strutt H., Strutt D. Asymmetric localisation of planar polarity proteins: mechanisms and consequences. Seminars in Cell and Developmental Biology 2009, 20:957-963.
58. Strutt H., Warrington S.J., Strutt D. Dynamics of core planar polarity protein turnover and stable assembly into discrete membrane subdomains. DevelopmentalCell 2011, 20:511-525.
59. Stubbs J.L., Davidson L., Keller R., Kintner C. Radial intercalation of ciliated cells during Xenopus skin development. Development 2006, 133:2507-2515.
60. Sugiyama N., Tsukiyama T., Yamaguchi T.P., Yokoyama T. The canonical Wnt signaling pathway is not involved in renal cyst development in the kidneys of inv mutant mice. Kidney International 2011, 79:957-965.
61. 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. Journal of Cell Biology 1999, 145:825-836.
62. Tory K., Rousset-Rouviere C., Gubler M.C., Moriniere V., Pawtowski A., Becker C., Guyot C., Gie S., Frishberg Y., Nivet H., et al. Mutations of NPHP2 and NPHP3 in infantile nephronophthisis. Kidney International 2009, 75:839-847.
63. Vasilyev A., Liu Y., Mudumana S., Mangos S., Lam P.Y., Majumdar A., Zhao J., Poon K.L., Kondrychyn I., Korzh V., et al. Collective cell migration drives morphogenesis of the kidney nephron. PLoS Biology 2009, 7:e9.
64. Verghese E., Weidenfeld R., Bertram J.F., Ricardo S.D., Deane J.A. Renal cilia display length alterations following tubular injury and are present early in epithelial repair. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association-European Renal Association 2008, 23:834-841.
65. Ward H.H., Wang J., Phillips C. Analysis of multiple Invs transcripts in mouse and MDCK cells. Genomics 2004, 84:991-1001.
66. 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 2003, 130:1725-1734.
67. Yasuhiko Y., Imai F., Ookubo K., Takakuwa Y., Shiokawa K., Yokoyama T. Calmodulin binds to inv protein: implication for the regulation of inv function. Development Growth and Differentiation 2001, 43:671-681.
68. Yokoyama T., Copeland N.G., Jenkins N.A., Montgomery C.A., Elder F.F., Overbeek P.A. Reversal of left-right asymmetry: a situs inversus mutation. Science 1993, 260:679-682.
69. Zallen J.A. Planar polarity and tissue morphogenesis. Cell 2007, 129:1051-1063.
70. Zhao C., Malicki J. Nephrocystins and MKS proteins interact with IFT particle and facilitate transport of selected ciliary cargos. The EMBO Journal 2011, 30:2532-2544.