Home LiteratureArticle Details
PMID: 22019273 Published · ppublish English Case Reports Journal Article Research Support, Non-U.S. Gov't

Ciliopathies with skeletal anomalies and renal insufficiency due to mutations in the IFT-A gene WDR19.

American journal of human genetics ·Vol. 89 ·No. 5 ·2011-11-11 ·Pages 634-43

Bredrup C, Saunier S, Oud MM, Fiskerstrand T, Hoischen A, Brackman D, Leh SM, Midtbø M, Filhol E, Bole-Feysot C, Nitschké P, Gilissen C, Haugen OH, Sanders JS, Stolte-Dijkstra I, Mans DA, Steenbergen EJ, Hamel BC, Matignon M, Pfundt R, Jeanpierre C, Boman H, Rødahl E, Veltman JA, Knappskog PM, Knoers NV, Roepman R, Arts HH

Abstract

A subset of ciliopathies, including Sensenbrenner, Jeune, and short-rib polydactyly syndromes are characterized by skeletal anomalies accompanied by multiorgan defects such as chronic renal failure and retinitis pigmentosa. Through exome sequencing we identified compound heterozygous mutations in WDR19 in a Norwegian family with Sensenbrenner syndrome. In a Dutch family with the clinically overlapping Jeune syndrome, a homozygous missense mutation in the same gene was found. Both families displayed a nephronophthisis-like nephropathy. Independently, we also identified compound heterozygous WDR19 mutations by exome sequencing in a Moroccan family with isolated nephronophthisis. WDR19 encodes IFT144, a member of the intraflagellar transport (IFT) complex A that drives retrograde ciliary transport. We show that IFT144 is absent from the cilia of fibroblasts from one of the Sensenbrenner patients and that ciliary abundance and morphology is perturbed, demonstrating the ciliary pathogenesis. Our results suggest that isolated nephronophthisis, Jeune, and Sensenbrenner syndromes are clinically overlapping disorders that can result from a similar molecular cause.

MeSH Terms
Adolescent Adult Child Cilia/genetics,pathology Craniofacial Abnormalities/genetics Cytoskeletal Proteins Ectodermal Dysplasia/genetics Exome/genetics Female Fibroblasts/metabolism Flagella/genetics,pathology Humans Intracellular Signaling Peptides and Proteins Male Molecular Sequence Data Morocco Mutation, Missense Netherlands Norway Oligonucleotide Array Sequence Analysis Pedigree Polycystic Kidney Diseases/congenital,genetics Proteins/genetics Short Rib-Polydactyly Syndrome/genetics Thoracic Diseases/genetics Young Adult
Chemicals
Cytoskeletal Proteins Intracellular Signaling Peptides and Proteins Proteins WDR19 protein, human
Authors & Affiliations
28 authors, click to expand affiliations / ORCID
Bredrup Cecilie
Department of Ophthalmology, Haukeland University Hospital, N-5021 Bergen, Norway.
Saunier Sophie
Oud Machteld M
Fiskerstrand Torunn
Hoischen Alexander
Brackman Damien
Leh Sabine M
Midtbø Marit
Filhol Emilie
Bole-Feysot Christine
Nitschké Patrick
Gilissen Christian
Haugen Olav H
Sanders Jan-Stephan F
Stolte-Dijkstra Irene
Mans Dorus A
Steenbergen Eric J
Hamel Ben C J
Matignon Marie
Pfundt Rolph
Jeanpierre Cécile
Boman Helge
Rødahl Eyvind
Veltman Joris A
Knappskog Per M
Knoers Nine V A M
Roepman Ronald
Arts Heleen H
References (44)
44 references, click to expand
  1. Expanded phenotype of cranioectodermal dysplasia (Sensenbrenner syndrome)
    Am J Med Genet. 1997 Jun 27;70(4):349-52 PMID: 9182772
  2. Mutation in IFT80 in a fetus with the phenotype of Verma-Naumoff provides molecular evidence for Jeune-Verma-Naumoff dysplasia spectrum.
    J Med Genet. 2011 Feb;48(2):88-92 PMID: 19648123
  3. Primary cilia of odontoblasts: possible role in molar morphogenesis.
    J Dent Res. 2009 Oct;88(10):910-5 PMID: 19783798
  4. Analysis of hedgehog signaling in mouse intraflagellar transport mutants.
    Methods Cell Biol. 2009;93:347-69 PMID: 20409825
  5. IFT80, which encodes a conserved intraflagellar transport protein, is mutated in Jeune asphyxiating thoracic dystrophy.
    Nat Genet. 2007 Jun;39(6):727-9 PMID: 17468754
  6. Cystic diseases of the kidney: ciliary dysfunction and cystogenic mechanisms.
    Pediatr Nephrol. 2011 Aug;26(8):1181-95 PMID: 21113628
  7. Cranioectodermal dysplasia (Sensenbrenner's syndrome).
    J Med Genet. 1989 Jun;26(6):393-6 PMID: 2661822
  8. Fast and accurate short read alignment with Burrows-Wheeler transform.
    Bioinformatics. 2009 Jul 15;25(14):1754-60 PMID: 19451168
  9. Mechanisms of nephronophthisis and related ciliopathies.
    Nephron Exp Nephrol. 2011;118(1):e9-14 PMID: 21071979
  10. TTC21B contributes both causal and modifying alleles across the ciliopathy spectrum.
    Nat Genet. 2011 Mar;43(3):189-96 PMID: 21258341
  11. Clinical and epidemiological assessment of steroid-resistant nephrotic syndrome associated with the NPHS2 R229Q variant.
    Kidney Int. 2009 Apr;75(7):727-35 PMID: 19145239
  12. Complex interactions between genes controlling trafficking in primary cilia.
    Nat Genet. 2011 Jun;43(6):547-53 PMID: 21552265
  13. Connective tissue involvement in two patients with features of cranioectodermal dysplasia.
    Am J Med Genet A. 2009 Oct;149A(10):2212-5 PMID: 19760620
  14. Ciliopathies: an expanding disease spectrum.
    Pediatr Nephrol. 2011 Jul;26(7):1039-56 PMID: 21210154
  15. Human and mouse mutations in WDR35 cause short-rib polydactyly syndromes due to abnormal ciliogenesis.
    Am J Hum Genet. 2011 Apr 8;88(4):508-15 PMID: 21473986
  16. The intraflagellar transport machinery of Chlamydomonas reinhardtii.
    Traffic. 2003 Jul;4(7):435-42 PMID: 12795688
  17. Intraflagellar transport and functional analysis of genes required for flagellum formation in trypanosomes.
    Mol Biol Cell. 2008 Mar;19(3):929-44 PMID: 18094047
  18. Evidence of oligogenic inheritance in nephronophthisis.
    J Am Soc Nephrol. 2007 Oct;18(10):2789-95 PMID: 17855640
  19. Mutations in the gene encoding the basal body protein RPGRIP1L, a nephrocystin-4 interactor, cause Joubert syndrome.
    Nat Genet. 2007 Jul;39(7):882-8 PMID: 17558407
  20. Loss of the Tg737 protein results in skeletal patterning defects.
    Dev Dyn. 2003 May;227(1):78-90 PMID: 12701101
  21. Anomalies in the permanent dentition and other oral findings in 29 individuals with Laurence-Moon-Bardet-Biedl syndrome.
    J Oral Pathol Med. 1996 Feb;25(2):86-9 PMID: 8667262
  22. NEK1 mutations cause short-rib polydactyly syndrome type majewski.
    Am J Hum Genet. 2011 Jan 7;88(1):106-14 PMID: 21211617
  23. Hierarchical interactions of homeodomain and forkhead transcription factors in regulating odontogenic gene expression.
    J Biol Chem. 2011 Jun 17;286(24):21372-83 PMID: 21504905
  24. Primary cilia regulate Shh activity in the control of molar tooth number.
    Development. 2009 Mar;136(6):897-903 PMID: 19211681
  25. Cranioectodermal Dysplasia, Sensenbrenner syndrome, is a ciliopathy caused by mutations in the IFT122 gene.
    Am J Hum Genet. 2010 Jun 11;86(6):949-56 PMID: 20493458
  26. Jeune asphyxiating thoracic dystrophy and short-rib polydactyly type III (Verma-Naumoff) are variants of the same disorder.
    Am J Med Genet. 2000 Feb 14;90(4):310-4 PMID: 10710229
  27. Dissection of epistasis in oligogenic Bardet-Biedl syndrome.
    Nature. 2006 Jan 19;439(7074):326-30 PMID: 16327777
  28. Retrograde intraflagellar transport mutants identify complex A proteins with multiple genetic interactions in Chlamydomonas reinhardtii.
    Genetics. 2009 Nov;183(3):885-96 PMID: 19720863
  29. Nephrocystins and MKS proteins interact with IFT particle and facilitate transport of selected ciliary cargos.
    EMBO J. 2011 May 20;30(13):2532-44 PMID: 21602787
  30. NPHS2 variation in focal and segmental glomerulosclerosis.
    BMC Nephrol. 2008 Sep 29;9:13 PMID: 18823551
  31. [Asphyxiating thoracic dystrophy with familial characteristics].
    Arch Fr Pediatr. 1955;12(8):886-91 PMID: 13292988
  32. SnapShot: Intraflagellar transport.
    Cell. 2009 May 15;137(4):784-784.e1 PMID: 19450523
  33. Exome sequencing identifies WDR35 variants involved in Sensenbrenner syndrome.
    Am J Hum Genet. 2010 Sep 10;87(3):418-23 PMID: 20817137
  34. PLINK: a tool set for whole-genome association and population-based linkage analyses.
    Am J Hum Genet. 2007 Sep;81(3):559-75 PMID: 17701901
  35. Oral manifestations in Ellis-van Creveld syndrome: report of a case and review of the literature.
    J Oral Maxillofac Surg. 2010 Feb;68(2):456-60 PMID: 20116723
  36. C14ORF179 encoding IFT43 is mutated in Sensenbrenner syndrome.
    J Med Genet. 2011 Jun;48(6):390-5 PMID: 21378380
  37. Exome sequencing identifies truncating mutations in human SERPINF1 in autosomal-recessive osteogenesis imperfecta.
    Am J Hum Genet. 2011 Mar 11;88(3):362-71 PMID: 21353196
  38. DYNC2H1 mutations cause asphyxiating thoracic dystrophy and short rib-polydactyly syndrome, type III.
    Am J Hum Genet. 2009 May;84(5):706-11 PMID: 19442771
  39. New syndrome of skeletal, dental and hair anomalies.
    Birth Defects Orig Artic Ser. 1975;11(2):372-9 PMID: 1227553
  40. Intraflagellar transport molecules in ciliary and nonciliary cells of the retina.
    J Cell Biol. 2010 Apr 5;189(1):171-86 PMID: 20368623
  41. Jeune syndrome: description of 13 cases and a proposal for follow-up protocol.
    Eur J Pediatr. 2010 Jan;169(1):77-88 PMID: 19430947
  42. Detection of nonneutral substitution rates on mammalian phylogenies.
    Genome Res. 2010 Jan;20(1):110-21 PMID: 19858363
  43. Distinct mutants of retrograde intraflagellar transport (IFT) share similar morphological and molecular defects.
    J Cell Biol. 1998 Dec 14;143(6):1591-601 PMID: 9852153
  44. Disruption of intraflagellar protein transport in photoreceptor cilia causes Leber congenital amaurosis in humans and mice.
    J Clin Invest. 2011 Jun;121(6):2169-80 PMID: 21606596
Article Info
Journal
American journal of human genetics
Abbr.
Am J Hum Genet
ISSN
1537-6605
Published
2011-11-11
Epub
2011-00-20
Pages
634-43
Language
English
Region
United States
NLM ID
0370475
PMCID
PMC3213394
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]