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

Volumn 34, Issue 4, 2003, Pages 413-420

  Otto, Edgar A ^a   Schermer, Bernhard ^b   Obara, Tomoko ^c   O'Toole, John F ^a   Hiller, Karl S ^a   Mueller, Adelheid M ^a   Ruf, Rainer G ^a   Hoefele, Julia ^a   Beekmann, Frank ^a   Landau, Daniel ^d   Foreman, John W ^e   Goodship, Judith A ^f   Strachan, Tom ^f   Kispert, Andreas ⁱ   Wolf, Matthias T ^a   Gagnadoux, Marie F ^g   Nivet, Hubert ^h   Antignac, Corinne ^g   Walz, Gerd ^b   Drummond, Iain A ^c   Benzing, Thomas ^b   Hildebrandt, Friedhelm ^a   more..

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f NEWCASTLE UNIVERSITY   (United Kingdom)

^g INSERM   (France)

^h UNIVERSITY HOSPITAL OF TOURS   (France)

ⁱ NONE

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; GENE PRODUCT; INVERSIN; NEPHROCYSTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXIS; CELLULAR DISTRIBUTION; CLINICAL FEATURE; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; EUKARYOTIC FLAGELLUM; GENE; GENE EXPRESSION; GENE MAPPING; GENE MUTATION; HUMAN; HUMAN CELL; INVS GENE; KIDNEY POLYCYSTIC DISEASE; KIDNEY TUBULE CELL; MOLECULAR INTERACTION; NEPHRONOPHTHISIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SITUS INVERSUS; ZEBRA FISH;

ANIMALS; BASE SEQUENCE; BODY PATTERNING; CHILD; CILIA; DNA; FEMALE; GENE TARGETING; HUMANS; KIDNEY DISEASES, CYSTIC; MALE; MOLECULAR SEQUENCE DATA; MUTATION; POLYCYSTIC KIDNEY, AUTOSOMAL RECESSIVE; PROTEINS; SITUS INVERSUS; TRANSCRIPTION FACTORS; TUBULIN; ZEBRAFISH;

ANIMALIA; DANIO RERIO; EUKARYOTA;

EID: 0041592700     PISSN: 10614036     EISSN: None     Source Type: Journal    
DOI: 10.1038/ng1217     Document Type: Article

References (49)

1. Smith, C. & Graham, J. Congenital medullary cysts of the kidneys with severe refractory anemia. Am. J. Dis. Child. 69, 369-377 (1945).
2. Fanconi, G., Hanhart, E. & Albertini, A. Die familiäre juvenile Nephronophthise. Hel. Pediatr. Acta 6, 1-49 (1951).
3. Hildebrandt, F. Juvenile nephronophthisis, in Pediatric nephrology (eds. Barratt, T.M., Avner, E.D. & Harmon, W.E.) (Williams & Wilkins, Baltimore. 1999).
4. Hildebrandt, F. et al. A novel gene encoding an SH3 domain protein is mutated in nephronophthisis type 1. Nat. Genet. 17, 149-153 (1997).
5. Saunier, S. et al. A novel gene that encodes a protein with a putative src homology 3 domain is a candidate gene for familial juvenile nephronophthisis. Hum. Mol. Genet. 6, 2317-2323 (1997).
6. Otto, E. et al. A gene mutated in nephronophthisis and retinitis pigmentosa encodes a novel protein, nephroretinin, conserved in evolution. Am. J. Hum. Genet. 71, 1167-1171 (2002).
7. Mollet, G. et al. The gene mutated in juvenile nephronophthisis type 4 encodes a novel protein that interacts with nephrocystin. Nat. Genet. 32, 300-305 (2002).
8. Waldherr, R., Lennert, T., Weber, H.P., Fodisch, H.J. & Scharer, K. The nephronophthisis complex. A clinicopathologic study in children. Virchows Arch. [Pathol. Anat.] 394, 235-254 (1982).
9. Zeisberg, M., Strutz, F. & Muller, G.A. Renal fibrosis: an update. Curr. Opin. Nephrol. Hypertens. 10, 315-320 (2001).
10. Otto, E. et al. Nephrocystin: gene expression and sequence conservation between human, mouse, and Caenorhabditis elegans. J. Am. Soc. Nephrol. 11, 270-282 (2000).
11. Donaldson, J.C. et al. Crk-associated substrate p130(Cas) interacts with nephrocystin and both proteins localize to cell-cell contacts of polarized epithelial cells. Exp. Cell Res. 256, 168-178 (2000).
12. Donaldson, J.C., Dise, R.S., Ritchie, M.D. & Hanks, S.K. Nephrocystin-conserved domains involved in targeting to epithelial cell-cell junctions, interaction with filamins, and establishing cell polarity. J. Biol. Chem. 277, 29028-29035 (2002).
13. Benzing, T. et al. Nephrocystin interacts with Pyk2, p130(Cas), and tensin and triggers phosphorylation of Pyk2. Proc. Natl. Acad. Sci. USA 98, 9784-9789 (2001).
14. Hildebrandt, F. & Otto, E. Molecular genetics of nephronophthisis and medullary cystic kidney disease. J. Am. Soc. Nephrol. 11, 1753-1761 (2000).
15. Omran, H. et al. Identification of a new gene locus for adolescent nephronophthisis, on chromosome 3q22 in a large Venezuelan pedigree. Am. J. Hum. Genet. 66, 118-127 (2000).
16. Haider, N.B., Carmi, R., Shalev, H., Sheffield, V.C. & Landau, D. A Bedouin kindred with infantile nephronophthisis demonstrates linkage to chromosome 9 by homozygosity mapping. Am. J. Hum. Genet. 63, 1404-1410 (1998).
17. Gagnadoux, M.F., Bacri, J.L., Broyer, M. & Habib, R. Infantile chronic tubulo-interstitial nephritis with cortical microcysts: variant of nephronophthisis or new disease entity? Pediatr. Nephrol. 3, 50-55 (1989).
18. Mochizuki, T. et al. Cloning of inv, a gene that controls left/right asymmetry and kidney development. Nature 395, 177-181 (1998).
19. Morgan, D. et al. Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse. Nat. Genet. 20, 149-156 (1998).
20. Igarashi, P. & Somlo, S. Genetics and pathogenesis of polycystic kidney disease. J. Am. Soc. Nephrol. 13, 2384-2398 (2002).
21. Nauli, S.M. et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33, 129-137 (2003).
22. Morgan, D. et al. The left-right determinant inversin has highly conserved ankyrin repeat and IQ domains and interacts with calmodulin. Hum. Genet. 110, 377-384 (2002).
23. Morgan, D. et al. 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).
24. Ostrowski, L.E. et al. A proteomic analysis of human cilia: identification of novel components. Mol. Cell. Proteomics 1, 451-465 (2002).
25. Yokoyama, T. et al. Reversal of left-right asymmetry: a situs inversus mutation. Science 260, 679-682 (1993).
26. Okada, Y. et al. Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol. Cell 4, 459-468 (1999).
27. Olbrich, H. et al. Mutations in a novel gene, NPHP3, cause adolescent nephronophthisis, tapeto-retinal degeneration and hepatic fibrosis. Nat. Genet. advance online publication, 20 July 2003 (doi:10.1038/ng1216).
28. Bhunia, A.K. et al. PKD1 induces p21(waf1) and regulation of the cell cycle via direct activation of the JAK-STAT signaling pathway in a process requiring PKD2. Cell 109, 157-168 (2002).
29. Taulman, P.D., Haycraft, C.J., Balkovetz, D.F. & Yoder, B.K. Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol. Biol. Cell 12, 589-599 (2001).
30. Haycraft, C.J., Swoboda, P., Taulman, P.D., Thomas, J.H. & Yoder, B.K. 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).
31. Barr, M.M. et al. The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Curr. Biol. 11, 1341-1346 (2001).
32. 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. 13, 2508-2516 (2002).
33. Hou, X. et al. Cystin, a novel cilia-associated protein, is disrupted in the cpk mouse model of polycystic kidney disease. J. Clin. Invest. 109, 533-540 (2002).
34. Calvet, J.P. Ciliary signaling goes down the tubes. Nat. Genet. 33, 113-114 (2003).
35. Nurnberger, J., Bacallao, R.L. & Phillips, C.L. Inversin forms a complex with catenins and N-cadherin in polarized epithelial cells. Mol. Biol. Cell. 13, 3096-3106 (2002).
36. Woo, D.D., Miao, S.Y., Pelayo, J.C. & Woolf, A.S. Taxol inhibits progression of congenital polycystic kidney disease. Nature 368, 750-753 (1994).
37. Woo, D.D., Tabancay, A.P., Jr. & Wang, C.J. Microtubule active taxanes inhibit polycystic kidney disease progression in cpk mice. Kidney. Int. 51, 1613-1618 (1997).
38. McQuinn, T.C., Miga, D.E., Mjaatvedt, C.H., Phelps, A.L. & Wessels, A. Cardiopulmonary malformations in the inv/inv mouse. Anat. Rec. 263, 62-71 (2001).
39. Hirokawa, N., Noda, Y. & Okada, Y. Kinesin and dynein superfamily proteins in organelle transport and cell division. Curr. Opin. Cell. Biol. 10, 60-73 (1998).
40. Pennekamp, P. et al. The ion channel polycystin-2 is required for left-right axis determination in mice. Curr. Biol. 12, 938-943 (2002).
41. Wu, G. et al. Somatic inactivation of Pkd2 results in polycystic kidney disease. Cell 93, 177-188 (1998).
42. Wu, G. et al. Cardiac defects and renal failure in mice with targeted mutations in Pkd2. Nat. Genet. 24, 75-78 (2000).
43. Moyer, J.H. et al. Candidate gene associated with a mutation causing recessive polycystic kidney disease in mice. Science 264, 1329-1333 (1994).
44. Woo, D.D., Nguyen, D.K., Khatibi, N. & Olsen, P. Genetic identification of two major modifier loci of polycystic kidney disease progression in pcy mice. J. Clin. Invest. 100, 1934-1940 (1997).
45. Kuida, S. & Beier, D.R. Genetic localization of interacting modifiers affecting severity in a murine model of polycystic kidney disease. Genome Res. 10, 49-54 (2000).
46. Omran, H. et al. Human adolescent nephronophthisis: gene locus synteny with polycystic kidney disease in pcy mice. J. Am. Soc. Nephrol. 12, 107-113 (2001).
47. Benzing, T. et al. 14-3-3 interacts with regulator of G protein signaling proteins and modulates their activity. J. Biol. Chem. 275, 28167-28172 (2000).
48. Benzing, T. et al. Upregulation of RGS7 may contribute to tumor necrosis factor-induced changes in central nervous function. Nat. Med. 5, 913-918 (1999).
49. Drummond, I.A. et al. Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 125, 4655-4667 (1998).