DCDC2 mutations cause a renal-hepatic ciliopathy by disrupting Wnt signaling

American Journal of Human Genetics

Volumn 96, Issue 1, 2015, Pages 81-92

  Schueler, Markus ^a   Braun, Daniela A ^a   Chandrasekar, Gayathri ^b   Gee, Heon Yung ^a   Klasson, Timothy D ^c   Halbritter, Jan ^a   Bieder, Andrea ^b   Porath, Jonathan D ^a   Airik, Rannar ^a   Zhou, Weibin ^d   Loturco, Joseph J ^e   Che, Alicia ^e   Otto, Edgar A ^d   Böckenhauer, Detlef ^f   Sebire, Neil J ^g   Honzik, Tomas ^h   Harris, Peter C ⁱ   Koon, Sarah J ⁱ   Gunay Aygun, Meral ^j   Saunier, Sophie ^k   Zerres, Klaus ^l   Bruechle, Nadina Ortiz ^l   Drenth, Joost P H ^m   Pelletier, Laurence ^n,o   Tapia Páez, Isabel ^b   Lifton, Richard P ^p,q   Giles, Rachel H ^c   Kere, Juha ^b,r,s   Hildebrandt, Friedhelm ^a,q   more..

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF MICHIGAN   (United States)

^e UNIVERSITY OF CONNECTICUT   (United States)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^h CHARLES UNIVERSITY   (Czech Republic)

ⁱ MAYO CLINIC   (United States)

^j NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^k INSERM   (France)

^l UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^m RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

ⁿ MOUNT SINAI HOSPITAL   (Canada)

^o UNIVERSITY OF TORONTO   (Canada)

^p YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^q HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^r FOLKHÄLSAN INSTITUTE OF GENETICS   (Finland)

^s SCIENCE FOR LIFE LABORATORY   (Sweden)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DCDC2 PROTEIN, HUMAN; DCDC2 PROTEIN, MOUSE; DISHEVELLED PROTEINS; MICROTUBULE ASSOCIATED PROTEIN; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONEME; CELL CULTURE; CELL CYCLE; CONTROLLED STUDY; DCDC2 GENE; EMBRYO; END STAGE RENAL DISEASE; GENE; GENE MUTATION; GENETIC DISORDER; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROCEPHALUS; KIDNEY CYST; LIVER FIBROSIS; MITOSIS SPINDLE; MOUSE; NEPHRONOPHTHISIS; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; RENAL HEPATIC CILIOPATHY; WILD TYPE; WNT SIGNALING PATHWAY; ZEBRA FISH; 3T3 CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGY; EUKARYOTIC FLAGELLUM; EXON; GENETICS; HEK293 CELL LINE; KIDNEY; KIDNEY POLYCYSTIC DISEASE; METABOLISM; MUTATION; PATHOLOGY; TRANSMISSION ELECTRON MICROSCOPY;

DANIO RERIO;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BETA CATENIN; CILIA; COMPUTATIONAL BIOLOGY; EXONS; HEK293 CELLS; HUMANS; KIDNEY; KIDNEY DISEASES, CYSTIC; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; NIH 3T3 CELLS; PHENOTYPE; PHOSPHOPROTEINS; WNT SIGNALING PATHWAY; ZEBRAFISH;

EID: 84920729054     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2014.12.002     Document Type: Article

References (41)

1. L. Sang, J.J. Miller, K.C. Corbit, R.H. Giles, M.J. Brauer, E.A. Otto, L.M. Baye, X. Wen, S.J. Scales, and M. Kwong Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways Cell 145 2011 513 528
2. F. Hildebrandt, T. Benzing, and N. Katsanis Ciliopathies N. Engl. J. Med. 364 2011 1533 1543
3. 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
4. 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 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
5. M. Attanasio, N.H. Uhlenhaut, V.H. Sousa, J.F. O'Toole, E. Otto, K. Anlag, C. Klugmann, A.C. Treier, J. Helou, and J.A. Sayer Loss of GLIS2 causes nephronophthisis in humans and mice by increased apoptosis and fibrosis Nat. Genet. 39 2007 1018 1024
6. M. Chaki, R. Airik, A.K. Ghosh, R.H. Giles, R. Chen, G.G. Slaats, H. Wang, T.W. Hurd, W. Zhou, and A. Cluckey Exome capture reveals ZNF423 and CEP164 mutations, linking renal ciliopathies to DNA damage response signaling Cell 150 2012 533 548
7. W. Zhou, E.A. Otto, A. Cluckey, R. Airik, T.W. Hurd, M. Chaki, K. Diaz, F.P. Lach, G.R. Bennett, and H.Y. Gee FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair Nat. Genet. 44 2012 910 915
8. H. Olbrich, M. Fliegauf, J. Hoefele, A. Kispert, E. Otto, A. Volz, M.T. Wolf, G. Sasmaz, U. Trauer, and R. Reinhardt Mutations in a novel gene, NPHP3, cause adolescent nephronophthisis, tapeto-retinal degeneration and hepatic fibrosis Nat. Genet. 34 2003 455 459
9. E. Otto, J. Hoefele, R. Ruf, A.M. Mueller, K.S. Hiller, M.T. Wolf, M.J. Schuermann, A. Becker, R. Birkenhäger, and R. Sudbrak A gene mutated in nephronophthisis and retinitis pigmentosa encodes a novel protein, nephroretinin, conserved in evolution Am. J. Hum. Genet. 71 2002 1161 1167
10. 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
11. E. Otto, B. Loeys, H. Khanna, J. Hellemans, R. Sudbrak, S. Fan, U. Muerb, J.F. O'Toole, J. Helou, and M. Attanasio A novel ciliary IQ domain protein, NPHP5, is mutated in Senior-Loken syndrome (nephronophthisis with retinitis pigmentosa), and interacts with RPGR and calmodulin Nat. Genet. 37 2005 282 288
12. J.A. Sayer, E.A. Otto, J.F. O'Toole, G. Nurnberg, M.A. Kennedy, C. Becker, H.C. Hennies, J. Helou, M. Attanasio, and B.V. Fausett The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4 Nat. Genet. 38 2006 674 681
13. E.M. Valente, J.L. Silhavy, F. Brancati, G. Barrano, S.R. Krishnaswami, M. Castori, M.A. Lancaster, E. Boltshauser, L. Boccone, L. Al-Gazali International Joubert Syndrome Related Disorders Study Group Mutations in CEP290, which encodes a centrosomal protein, cause pleiotropic forms of Joubert syndrome Nat. Genet. 38 2006 623 625
14. M. Delous, L. Baala, R. Salomon, C. Laclef, J. Vierkotten, K. Tory, C. Golzio, T. Lacoste, L. Besse, and C. Ozilou The ciliary gene RPGRIP1L is mutated in cerebello-oculo-renal syndrome (Joubert syndrome type B) and Meckel syndrome Nat. Genet. 39 2007 875 881
15. E.A. Otto, M.L. Trapp, U.T. Schultheiss, J. Helou, L.M. Quarmby, and F. Hildebrandt NEK8 mutations affect ciliary and centrosomal localization and may cause nephronophthisis J. Am. Soc. Nephrol. 19 2008 587 592
16. J. Halbritter, K. Diaz, M. Chaki, J.D. Porath, B. Tarrier, C. Fu, J.L. Innis, S.J. Allen, R.H. Lyons, and C.J. Stefanidis High-throughput mutation analysis in patients with a nephronophthisis-associated ciliopathy applying multiplexed barcoded array-based PCR amplification and next-generation sequencing J. Med. Genet. 49 2012 756 767
17. J. Halbritter, J.D. Porath, K.A. Diaz, D.A. Braun, S. Kohl, M. Chaki, S.J. Allen, N.A. Soliman, F. Hildebrandt, E.A. Otto GPN Study Group Identification of 99 novel mutations in a worldwide cohort of 1,056 patients with a nephronophthisis-related ciliopathy Hum. Genet. 132 2013 865 884
18. L. Kruglyak, M.J. Daly, M.P. Reeve-Daly, and E.S. Lander Parametric and nonparametric linkage analysis: a unified multipoint approach Am. J. Hum. Genet. 58 1996 1347 1363
19. K. Strauch, R. Fimmers, T. Kurz, K.A. Deichmann, T.F. Wienker, and M.P. Baur Parametric and nonparametric multipoint linkage analysis with imprinting and two-locus-trait models: application to mite sensitization Am. J. Hum. Genet. 66 2000 1945 1957
20. D.F. Gudbjartsson, K. Jonasson, M.L. Frigge, and A. Kong Allegro, a new computer program for multipoint linkage analysis Nat. Genet. 25 2000 12 13
21. F. Hildebrandt, S.F. Heeringa, F. Rüschendorf, M. Attanasio, G. Nürnberg, C. Becker, D. Seelow, N. Huebner, G. Chernin, and C.N. Vlangos A systematic approach to mapping recessive disease genes in individuals from outbred populations PLoS Genet. 5 2009 e1000353
22. L.M. Boyden, M. Choi, K.A. Choate, C.J. Nelson-Williams, A. Farhi, H.R. Toka, I.R. Tikhonova, R. Bjornson, S.M. Mane, and G. Colussi Mutations in kelch-like 3 and cullin 3 cause hypertension and electrolyte abnormalities Nature 482 2012 98 102
23. M.A. Zariwala, H.Y. Gee, M. Kurkowiak, D.A. Al-Mutairi, M.W. Leigh, T.W. Hurd, R. Hjeij, S.D. Dell, M. Chaki, and G.W. Dougherty ZMYND10 is mutated in primary ciliary dyskinesia and interacts with LRRC6 Am. J. Hum. Genet. 93 2013 336 345
24. E.A. Otto, T.W. Hurd, R. Airik, M. Chaki, W. Zhou, C. Stoetzel, S.B. Patil, S. Levy, A.K. Ghosh, and C.A. Murga-Zamalloa Candidate exome capture identifies mutation of SDCCAG8 as the cause of a retinal-renal ciliopathy Nat. Genet. 42 2010 840 850
25. J. Odenthal, and C. Nüsslein-Volhard fork head domain genes in zebrafish Dev. Genes Evol. 208 1998 245 258
26. B. Thisse, V. Heyer, A. Lux, V. Alunni, A. Degrave, I. Seiliez, J. Kirchner, J.P. Parkhill, and C. Thisse Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening Methods Cell Biol. 77 2004 505 519
27. G. Chandrasekar, L. Vesterlund, K. Hultenby, I. Tapia-Páez, and J. Kere The zebrafish orthologue of the dyslexia candidate gene DYX1C1 is essential for cilia growth and function PLoS ONE 8 2013 e63123
28. W. Zhou, and F. Hildebrandt Molecular cloning and expression of phospholipase C epsilon 1 in zebrafish Gene Expr. Patterns 9 2009 282 288
29. D.T. Truong, A. Che, A.R. Rendall, C.E. Szalkowski, J.J. LoTurco, A.M. Galaburda, and R. Holly Fitch Mutation of Dcdc2 in mice leads to impairments in auditory processing and memory ability Genes Brain Behav. 13 2014 802 811
30. A. Shmueli, A. Gdalyahu, S. Sapoznik, T. Sapir, M. Tsukada, and O. Reiner Site-specific dephosphorylation of doublecortin (DCX) by protein phosphatase 1 (PP1) Mol. Cell. Neurosci. 32 2006 15 26
31. S. Massinen, M.E. Hokkanen, H. Matsson, K. Tammimies, I. Tapia-Páez, V. Dahlström-Heuser, J. Kuja-Panula, J. Burghoorn, K.E. Jeppsson, and P. Swoboda Increased expression of the dyslexia candidate gene DCDC2 affects length and signaling of primary cilia in neurons PLoS ONE 6 2011 e20580
32. T. Watnick, and G. Germino From cilia to cyst Nat. Genet. 34 2003 355 356
33. R.H. Giles, J.H. van Es, and H. Clevers Caught up in a Wnt storm: Wnt signaling in cancer Biochim. Biophys. Acta 1653 2003 1 24
34. F.M. Coquelle, T. Levy, S. Bergmann, S.G. Wolf, D. Bar-El, T. Sapir, Y. Brody, I. Orr, N. Barkai, G. Eichele, and O. Reiner Common and divergent roles for members of the mouse DCX superfamily Cell Cycle 5 2006 976 983
35. J. Yasuda, A.J. Whitmarsh, J. Cavanagh, M. Sharma, and R.J. Davis The JIP group of mitogen-activated protein kinase scaffold proteins Mol. Cell. Biol. 19 1999 7245 7254
36. A. Jaeschke, M.P. Czech, and R.J. Davis An essential role of the JIP1 scaffold protein for JNK activation in adipose tissue Genes Dev. 18 2004 1976 1980
37. M. Caspi, R. Atlas, A. Kantor, T. Sapir, and O. Reiner Interaction between LIS1 and doublecortin, two lissencephaly gene products Hum. Mol. Genet. 9 2000 2205 2213
38. K.Y. Renkema, M.F. Stokman, R.H. Giles, and N.V. Knoers Next-generation sequencing for research and diagnostics in kidney disease Nat. Rev. Nephrol. 10 2014 433 444
39. A.F. Hurlstone, A.P. Haramis, E. Wienholds, H. Begthel, J. Korving, F. Van Eeden, E. Cuppen, D. Zivkovic, R.H. Plasterk, and H. Clevers The Wnt/beta-catenin pathway regulates cardiac valve formation Nature 425 2003 633 637
40. R.K. Miller, and P.D. McCrea Wnt to build a tube: contributions of Wnt signaling to epithelial tubulogenesis Developmental dynamics: an official publication of the American Association of Anatomists 239 2010 77 93
41. W.S. Ge, Y.J. Wang, J.X. Wu, J.G. Fan, Y.W. Chen, and L. Zhu Beta-catenin is overexpressed in hepatic fibrosis and blockage of Wnt/beta-catenin signaling inhibits hepatic stellate cell activation Molecular medicine reports 9 2014 2145 2151