Recurrent CNVs and SNVs at the NPHP1 locus contribute pathogenic alleles to Bardet-Biedl syndrome

American Journal of Human Genetics

Volumn 94, Issue 5, 2014, Pages 745-754

  Lindstrand, Anna ^a,g   Davis, Erica E ^a   Carvalho, Claudia M B ^b,c   Pehlivan, Davut ^b   Willer, Jason R ^a   Tsai, I Chun ^a   Ramanathan, Subhadra ^d   Zuppan, Craig ^d   Sabo, Aniko ^b   Muzny, Donna ^b   Gibbs, Richard ^b   Liu, Pengfei ^b   Lewis, Richard A ^b   Banin, Eyal ^e   Lupski, James R ^b,f   Clark, Robin ^d   Katsanis, Nicholas ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

^d LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^f TEXAS CHILDREN S HOSPITAL   (United States)

^g KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; LEUCINE; MESSENGER RNA; PROTEIN; PROTEIN NPHP1; UNCLASSIFIED DRUG; NEPHROCYSTIN 1;

ANIMAL EXPERIMENT; ARTICLE; AUTOSOMAL RECESSIVE INHERITANCE; BARDET BIEDL SYNDROME; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; COPY NUMBER VARIATION; DEVELOPMENTAL DISORDER; EMBRYO; FEMALE; GENE DELETION; GENE FREQUENCY; GENE LOCUS; GENETIC VARIABILITY; HETEROZYGOTE; HISPANIC; HOMOZYGOSITY; HUMAN; HYPOGONADISM; KIDNEY MALFORMATION; LOSS OF FUNCTION MUTATION; MAJOR CLINICAL STUDY; MALE; NONHUMAN; OBESITY; PEDIGREE; POINT MUTATION; POLYDACTYLY; PRIORITY JOURNAL; ANIMAL MODEL; GASTRULATION; GENE INTERACTION; GENE MUTATION; GENE REPRESSION; HOMOZYGOTE; MISSENSE MUTATION; PHENOTYPE; RECESSIVE INHERITANCE;

DANIO RERIO;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALLELES; ANIMALS; BARDET-BIEDL SYNDROME; DNA COPY NUMBER VARIATIONS; GASTRULATION; GENETIC LOCI; HETEROZYGOTE; HOMOZYGOTE; HUMANS; KIDNEY; MEMBRANE PROTEINS; MICE; PEDIGREE; SEQUENCE DELETION; ZEBRAFISH;

EID: 84899977171     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2014.03.017     Document Type: Article

References (39)

1. S. Saunier, J. Calado, F. Benessy, F. Silbermann, R. Heilig, J. Weissenbach, and C. Antignac Characterization of the NPHP1 locus: mutational mechanism involved in deletions in familial juvenile nephronophthisis Am. J. Hum. Genet. 66 2000 778 789
2. F. Hildebrandt, E. Otto, C. Rensing, H.G. Nothwang, M. Vollmer, J. Adolphs, H. Hanusch, and M. Brandis A novel gene encoding an SH3 domain protein is mutated in nephronophthisis type 1 Nat. Genet. 17 1997 149 153
3. G. Caridi, L. Murer, R. Bellantuono, P. Sorino, D.A. Caringella, R. Gusmano, and G.M. Ghiggeri Renal-retinal syndromes: association of retinal anomalies and recessive nephronophthisis in patients with homozygous deletion of the NPH1 locus Am. J. Kidney Dis. 32 1998 1059 1062
4. M.A. Parisi, C.L. Bennett, M.L. Eckert, W.B. Dobyns, J.G. Gleeson, D.W. Shaw, R. McDonald, A. Eddy, P.F. Chance, and I.A. Glass The NPHP1 gene deletion associated with juvenile nephronophthisis is present in a subset of individuals with Joubert syndrome Am. J. Hum. Genet. 75 2004 82 91
5. M. Delous, N.E. Hellman, H.M. Gaudé, F. Silbermann, A. Le Bivic, R. Salomon, C. Antignac, and S. Saunier Nephrocystin-1 and nephrocystin-4 are required for epithelial morphogenesis and associate with PALS1/PATJ and Par6 Hum. Mol. Genet. 18 2009 4711 4723
6. K. Slanchev, M. Pütz, A. Schmitt, A. Kramer-Zucker, and G. Walz Nephrocystin-4 is required for pronephric duct-dependent cloaca formation in zebrafish Hum. Mol. Genet. 20 2011 3119 3128
7. E.A. Otto, B. Schermer, T. Obara, J.F. O'Toole, K.S. Hiller, A.M. Mueller, R.G. Ruf, J. Hoefele, F. Beekmann, and D. Landau 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 Nat. Genet. 34 2003 413 420
8. G. Mollet, R. Salomon, O. Gribouval, F. Silbermann, D. Bacq, G. Landthaler, D. Milford, A. Nayir, G. Rizzoni, C. Antignac, and S. Saunier The gene mutated in juvenile nephronophthisis type 4 encodes a novel protein that interacts with nephrocystin Nat. Genet. 32 2002 300 305
9. H. Olbrich, M. Fliegauf, J. Hoefele, A. Kispert, E. Otto, A. Volz, M.T. Wolf, G. Sasmaz, U. Trauer, and R. Reinhardt et al. Mutations in a novel gene, NPHP3, cause adolescent nephronophthisis, tapeto-retinal degeneration and hepatic fibrosis Nat. Genet. 34 2003 455 459
10. R.J. Ferland, W. Eyaid, R.V. Collura, L.D. Tully, R.S. Hill, D. Al-Nouri, A. Al-Rumayyan, M. Topcu, G. Gascon, and A. Bodell et al. Abnormal cerebellar development and axonal decussation due to mutations in AHI1 in Joubert syndrome Nat. Genet. 36 2004 1008 1013
11. C.M. Louie, G. Caridi, V.S. Lopes, F. Brancati, A. Kispert, M.A. Lancaster, A.M. Schlossman, E.A. Otto, M. Leitges, and H.J. Gröne et al. AHI1 is required for photoreceptor outer segment development and is a modifier for retinal degeneration in nephronophthisis Nat. Genet. 42 2010 175 180
12. J.L. Badano, J.C. Kim, B.E. Hoskins, R.A. Lewis, S.J. Ansley, D.J. Cutler, C. Castellan, P.L. Beales, M.R. Leroux, and N. Katsanis Heterozygous mutations in BBS1, BBS2 and BBS6 have a potential epistatic effect on Bardet-Biedl patients with two mutations at a second BBS locus Hum. Mol. Genet. 12 2003 1651 1659
13. J.L. Badano, C.C. Leitch, S.J. Ansley, H. May-Simera, S. Lawson, R.A. Lewis, P.L. Beales, H.C. Dietz, S. Fisher, and N. Katsanis Dissection of epistasis in oligogenic Bardet-Biedl syndrome Nature 439 2006 326 330
14. N. Katsanis, S.J. Ansley, J.L. Badano, E.R. Eichers, R.A. Lewis, B.E. Hoskins, P.J. Scambler, W.S. Davidson, P.L. Beales, and J.R. Lupski Triallelic inheritance in Bardet-Biedl syndrome, a Mendelian recessive disorder Science 293 2001 2256 2259
15. N.A. Zaghloul, and N. Katsanis Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy J. Clin. Invest. 119 2009 428 437
16. E.E. Davis, and N. Katsanis The ciliopathies: a transitional model into systems biology of human genetic disease Curr. Opin. Genet. Dev. 22 2012 290 303
17. R. Hjeij, A. Lindstrand, R. Francis, M.A. Zariwala, X. Liu, Y. Li, R. Damerla, G.W. Dougherty, M. Abouhamed, and H. Olbrich et al. ARMC4 mutations cause primary ciliary dyskinesia with randomization of left/right body asymmetry Am. J. Hum. Genet. 93 2013 357 367
18. C.M. Carvalho, F. Zhang, P. Liu, A. Patel, T. Sahoo, C.A. Bacino, C. Shaw, S. Peacock, A. Pursley, and Y.J. Tavyev et al. Complex rearrangements in patients with duplications of MECP2 can occur by fork stalling and template switching Hum. Mol. Genet. 18 2009 2188 2203
19. A. Itsara, G.M. Cooper, C. Baker, S. Girirajan, J. Li, D. Absher, R.M. Krauss, R.M. Myers, P.M. Ridker, and D.I. Chasman et al. Population analysis of large copy number variants and hotspots of human genetic disease Am. J. Hum. Genet. 84 2009 148 161
20. E.E. Davis, Q. Zhang, Q. Liu, B.H. Diplas, L.M. Davey, J. Hartley, C. Stoetzel, K. Szymanska, G. Ramaswami, C.V. Logan NISC Comparative Sequencing Program TTC21B contributes both causal and modifying alleles across the ciliopathy spectrum Nat. Genet. 43 2011 189 196
21. L. de Pontual, N.A. Zaghloul, S. Thomas, E.E. Davis, D.M. McGaughey, H. Dollfus, C. Baumann, S.L. Bessling, C. Babarit, and A. Pelet et al. Epistasis between RET and BBS mutations modulates enteric innervation and causes syndromic Hirschsprung disease Proc. Natl. Acad. Sci. USA 106 2009 13921 13926
22. H. Khanna, E.E. Davis, C.A. Murga-Zamalloa, A. Estrada-Cuzcano, I. Lopez, A.I. den Hollander, M.N. Zonneveld, M.I. Othman, N. Waseem, and C.F. Chakarova et al. A common allele in RPGRIP1L is a modifier of retinal degeneration in ciliopathies Nat. Genet. 41 2009 739 745
23. C.C. Leitch, N.A. Zaghloul, E.E. Davis, C. Stoetzel, A. Diaz-Font, S. Rix, M. Alfadhel, R.A. Lewis, W. Eyaid, and E. Banin et al. Hypomorphic mutations in syndromic encephalocele genes are associated with Bardet-Biedl syndrome Nat. Genet. 40 2008 443 448
24. A. Putoux, S. Thomas, K.L. Coene, E.E. Davis, Y. Alanay, G. Ogur, E. Uz, D. Buzas, C. Gomes, and S. Patrier et al. KIF7 mutations cause fetal hydrolethalus and acrocallosal syndromes Nat. Genet. 43 2011 601 606
25. C. Stoetzel, V. Laurier, E.E. Davis, J. Muller, S. Rix, J.L. Badano, C.C. Leitch, N. Salem, E. Chouery, and S. Corbani et al. BBS10 encodes a vertebrate-specific chaperonin-like protein and is a major BBS locus Nat. Genet. 38 2006 521 524
26. N.A. Zaghloul, Y. Liu, J.M. Gerdes, C. Gascue, E.C. Oh, C.C. Leitch, Y. Bromberg, J. Binkley, R.L. Leibel, and A. Sidow et al. Functional analyses of variants reveal a significant role for dominant negative and common alleles in oligogenic Bardet-Biedl syndrome Proc. Natl. Acad. Sci. USA 107 2010 10602 10607
27. J.M. Gerdes, Y. Liu, N.A. Zaghloul, C.C. Leitch, S.S. Lawson, M. Kato, P.A. Beachy, P.L. Beales, G.N. DeMartino, and S. Fisher et al. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response Nat. Genet. 39 2007 1350 1360
28. C. Li, P.N. Inglis, C.C. Leitch, E. Efimenko, N.A. Zaghloul, C.A. Mok, E.E. Davis, N.J. Bialas, M.P. Healey, and E. Héon et al. An essential role for DYF-11/MIP-T3 in assembling functional intraflagellar transport complexes PLoS Genet. 4 2008 e1000044
29. E.M. Valente, C.V. Logan, S. Mougou-Zerelli, J.H. Lee, J.L. Silhavy, F. Brancati, M. Iannicelli, L. Travaglini, S. Romani, and B. Illi et al. Mutations in TMEM216 perturb ciliogenesis and cause Joubert, Meckel and related syndromes Nat. Genet. 42 2010 619 625
30. J.C. McIntyre, E.E. Davis, A. Joiner, C.L. Williams, I.C. Tsai, P.M. Jenkins, D.P. McEwen, L. Zhang, J. Escobado, S. Thomas NISC Comparative Sequencing Program Gene therapy rescues cilia defects and restores olfactory function in a mammalian ciliopathy model Nat. Med. 18 2012 1423 1428
31. I.A. Drummond, and A.J. Davidson Zebrafish kidney development Methods Cell Biol. 100 2010 233 260
32. F. Hildebrandt, M. Attanasio, and E. Otto Nephronophthisis: disease mechanisms of a ciliopathy J. Am. Soc. Nephrol. 20 2009 23 35
33. C. Redin, S. Le Gras, O. Mhamdi, V. Geoffroy, C. Stoetzel, M.C. Vincent, P. Chiurazzi, D. Lacombe, I. Ouertani, and F. Petit et al. Targeted high-throughput sequencing for diagnosis of genetically heterogeneous diseases: efficient mutation detection in Bardet-Biedl and Alström syndromes J. Med. Genet. 49 2012 502 512
34. P.L. Beales, N. Elcioglu, A.S. Woolf, D. Parker, and F.A. Flinter New criteria for improved diagnosis of Bardet-Biedl syndrome: results of a population survey J. Med. Genet. 36 1999 437 446
35. L. Huang, K. Szymanska, V.L. Jensen, A.R. Janecke, A.M. Innes, E.E. Davis, P. Frosk, C. Li, J.R. Willer, and B.N. Chodirker et al. TMEM237 is mutated in individuals with a Joubert syndrome related disorder and expands the role of the TMEM family at the ciliary transition zone Am. J. Hum. Genet. 89 2011 713 730
36. M. Ma, X. Tian, P. Igarashi, G.J. Pazour, and S. Somlo Loss of cilia suppresses cyst growth in genetic models of autosomal dominant polycystic kidney disease Nat. Genet. 45 2013 1004 1012
37. J.F. O'Toole, Y. Liu, E.E. Davis, C.J. Westlake, M. Attanasio, E.A. Otto, D. Seelow, G. Nurnberg, C. Becker, and M. Nuutinen et al. Individuals with mutations in XPNPEP3, which encodes a mitochondrial protein, develop a nephronophthisis-like nephropathy J. Clin. Invest. 120 2010 791 802
38. R.A. Rachel, H.L. May-Simera, S. Veleri, N. Gotoh, B.Y. Choi, C. Murga-Zamalloa, J.C. McIntyre, J. Marek, I. Lopez, and A.N. Hackett et al. Combining Cep290 and Mkks ciliopathy alleles in mice rescues sensory defects and restores ciliogenesis J. Clin. Invest. 122 2012 1233 1245
39. W. Wiszniewski, J.V. Hunter, N.A. Hanchard, J.R. Willer, C. Shaw, Q. Tian, A. Illner, X. Wang, S.W. Cheung, and A. Patel et al. TM4SF20 ancestral deletion and susceptibility to a pediatric disorder of early language delay and cerebral white matter hyperintensities Am. J. Hum. Genet. 93 2013 197 210