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PMID: 19200523 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mutations in radial spoke head protein genes RSPH9 and RSPH4A cause primary ciliary dyskinesia with central-microtubular-pair abnormalities.

American journal of human genetics ·Vol. 84 ·No. 2 ·2009-02-00 ·Pages 197-209

Castleman VH, Romio L, Chodhari R, Hirst RA, de Castro SC, Parker KA, Ybot-Gonzalez P, Emes RD, Wilson SW, Wallis C, Johnson CA, Herrera RJ, Rutman A, Dixon M, Shoemark A, Bush A, Hogg C, Gardiner RM, Reish O, Greene ND, O'Callaghan C, Purton S, Chung EM, Mitchison HM

Abstract

Primary ciliary dyskinesia (PCD) is a genetically heterogeneous inherited disorder arising from dysmotility of motile cilia and sperm. This is associated with a variety of ultrastructural defects of the cilia and sperm axoneme that affect movement, leading to clinical consequences on respiratory-tract mucociliary clearance and lung function, fertility, and left-right body-axis determination. We performed whole-genome SNP-based linkage analysis in seven consanguineous families with PCD and central-microtubular-pair abnormalities. This identified two loci, in two families with intermittent absence of the central-pair structure (chromosome 6p21.1, Zmax 6.7) and in five families with complete absence of the central pair (chromosome 6q22.1, Zmax 7.0). Mutations were subsequently identified in two positional candidate genes, RSPH9 on chromosome 6p21.1 and RSPH4A on chromosome 6q22.1. Haplotype analysis identified a common ancestral founder effect RSPH4A mutation present in UK-Pakistani pedigrees. Both RSPH9 and RSPH4A encode protein components of the axonemal radial spoke head. In situ hybridization of murine Rsph9 shows gene expression restricted to regions containing motile cilia. Investigation of the effect of knockdown or mutations of RSPH9 orthologs in zebrafish and Chlamydomonas indicate that radial spoke head proteins are important in maintaining normal movement in motile, "9+2"-structure cilia and flagella. This effect is rescued by reintroduction of gene expression for restoration of a normal beat pattern in zebrafish. Disturbance in function of these genes was not associated with defects in left-right axis determination in humans or zebrafish.

MeSH Terms
Animals Chlamydomonas/genetics Chromosome Aberrations Chromosome Mapping Chromosomes, Human/genetics Chromosomes, Human, Pair 1 Cilia/genetics,pathology Congenital Abnormalities/genetics Cytoskeletal Proteins/genetics DNA-Binding Proteins/genetics Female Humans In Situ Hybridization Kartagener Syndrome/genetics Male Mutation Pedigree Polymorphism, Single Nucleotide Zebrafish/genetics
Chemicals
Cytoskeletal Proteins DNA-Binding Proteins RSPH1 protein, human RSPH9 protein, human
Authors & Affiliations
24 authors, click to expand affiliations / ORCID
Castleman Victoria H
General and Adolescent Paediatric Unit, University College London Institute of Child Health, Rayne Building, 5 University Street, London WC1E 6JJ, UK.
Romio Leila
Chodhari Rahul
Hirst Robert A
de Castro Sandra C P
Parker Keith A
Ybot-Gonzalez Patricia
Emes Richard D
Wilson Stephen W
Wallis Colin
Johnson Colin A
Herrera Rene J
Rutman Andrew
Dixon Mellisa
Shoemark Amelia
Bush Andrew
Hogg Claire
Gardiner R Mark
Reish Orit
Greene Nicholas D E
O'Callaghan Christopher
Purton Saul
Chung Eddie M K
Mitchison Hannah M
References (44)
44 references, click to expand
  1. DNAI1 mutations explain only 2% of primary ciliary dykinesia.
    Respiration. 2008;76(2):198-204 PMID: 18434704
  2. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry.
    Nat Genet. 2002 Feb;30(2):143-4 PMID: 11788826
  3. Sequence analysis of 21 genes located in the Kartagener syndrome linkage region on chromosome 15q.
    Eur J Hum Genet. 2008 Jun;16(6):688-95 PMID: 18270537
  4. A study of possible deleterious effects of consanguinity.
    Clin Genet. 1997 Mar;51(3):167-73 PMID: 9137881
  5. Trans-splicing mutants of Chlamydomonas reinhardtii.
    Mol Gen Genet. 1990 Sep;223(3):417-25 PMID: 2270082
  6. Mutations of DNAI1 in primary ciliary dyskinesia: evidence of founder effect in a common mutation.
    Am J Respir Crit Care Med. 2006 Oct 15;174(8):858-66 PMID: 16858015
  7. Ciliary beat pattern is associated with specific ultrastructural defects in primary ciliary dyskinesia.
    J Allergy Clin Immunol. 2003 Sep;112(3):518-24 PMID: 13679810
  8. Genome-wide transcriptional analysis of flagellar regeneration in Chlamydomonas reinhardtii identifies orthologs of ciliary disease genes.
    Proc Natl Acad Sci U S A. 2005 Mar 8;102(10):3703-7 PMID: 15738400
  9. Faster multipoint linkage analysis using Fourier transforms.
    J Comput Biol. 1998 Spring;5(1):1-7 PMID: 9541867
  10. A locus for primary ciliary dyskinesia maps to chromosome 19q.
    J Med Genet. 2000 Apr;37(4):241-4 PMID: 10745040
  11. Y-chromosome diversity characterizes the Gulf of Oman.
    Eur J Hum Genet. 2008 Mar;16(3):374-86 PMID: 17928816
  12. The 9 + 2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility.
    J Cell Biol. 2000 Nov 27;151(5):F37-42 PMID: 11086017
  13. Immotile cilia syndrome associated with polycystic kidney.
    J Urol. 1984 Dec;132(6):1165-6 PMID: 6502812
  14. DNAH5 mutations are a common cause of primary ciliary dyskinesia with outer dynein arm defects.
    Am J Respir Crit Care Med. 2006 Jul 15;174(2):120-6 PMID: 16627867
  15. A novel X-linked recessive mental retardation syndrome comprising macrocephaly and ciliary dysfunction is allelic to oral-facial-digital type I syndrome.
    Hum Genet. 2006 Sep;120(2):171-8 PMID: 16783569
  16. Absent inner dynein arms in a fetus with familial hydrocephalus-situs abnormality.
    Am J Med Genet A. 2004 Sep 1;129A(3):308-11 PMID: 15326634
  17. Primary ciliary dyskinesia: genes, candidate genes and chromosomal regions.
    J Appl Genet. 2004;45(3):347-61 PMID: 15306728
  18. The radial spokes and central apparatus: mechano-chemical transducers that regulate flagellar motility.
    Cell Motil Cytoskeleton. 2004 Jan;57(1):8-17 PMID: 14648553
  19. Flagellar motility is required for the viability of the bloodstream trypanosome.
    Nature. 2006 Mar 9;440(7081):224-7 PMID: 16525475
  20. easyLINKAGE-Plus--automated linkage analyses using large-scale SNP data.
    Bioinformatics. 2005 Sep 1;21(17):3565-7 PMID: 16014370
  21. Expression pattern of glypican-4 suggests multiple roles during mouse development.
    Dev Dyn. 2005 Jul;233(3):1013-7 PMID: 15830372
  22. FOXP2 expression during brain development coincides with adult sites of pathology in a severe speech and language disorder.
    Brain. 2003 Nov;126(Pt 11):2455-62 PMID: 12876151
  23. Analysis of ciliary beat pattern and beat frequency using digital high speed imaging: comparison with the photomultiplier and photodiode methods.
    Thorax. 2000 Apr;55(4):314-7 PMID: 10722772
  24. Radial spokes of Chlamydomonas flagella: genetic analysis of assembly and function.
    J Cell Biol. 1981 Jan;88(1):80-8 PMID: 7204490
  25. High-frequency nuclear transformation of Chlamydomonas reinhardtii.
    Proc Natl Acad Sci U S A. 1990 Feb;87(3):1228-32 PMID: 2105499
  26. Radial spoke proteins of Chlamydomonas flagella.
    J Cell Sci. 2006 Mar 15;119(Pt 6):1165-74 PMID: 16507594
  27. Proteomic analysis of a eukaryotic cilium.
    J Cell Biol. 2005 Jul 4;170(1):103-13 PMID: 15998802
  28. Merlin--rapid analysis of dense genetic maps using sparse gene flow trees.
    Nat Genet. 2002 Jan;30(1):97-101 PMID: 11731797
  29. 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 Dec 11;95(6):829-37 PMID: 9865700
  30. Sequences controlling transcription of the Chlamydomonas reinhardtii beta 2-tubulin gene after deflagellation and during the cell cycle.
    Mol Cell Biol. 1994 Aug;14(8):5165-74 PMID: 8035797
  31. Molecular cloning and characterization of a radial spoke head protein of sea urchin sperm axonemes: involvement of the protein in the regulation of sperm motility.
    Mol Biol Cell. 1998 Feb;9(2):513-22 PMID: 9450971
  32. Dysfunction of axonemal dynein heavy chain Mdnah5 inhibits ependymal flow and reveals a novel mechanism for hydrocephalus formation.
    Hum Mol Genet. 2004 Sep 15;13(18):2133-41 PMID: 15269178
  33. Central microtubular agenesis causing primary ciliary dyskinesia.
    Am J Respir Crit Care Med. 2004 Mar 1;169(5):634-7 PMID: 14982824
  34. Sequence analysis reveals homology between two proteins of the flagellar radial spoke.
    Mol Cell Biol. 1992 Sep;12(9):3967-77 PMID: 1508197
  35. Kartagener's syndrome and the syndrome of immotile cilia.
    Hum Genet. 1979 Feb 15;46(3):249-61 PMID: 155641
  36. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  37. DNAI2 mutations cause primary ciliary dyskinesia with defects in the outer dynein arm.
    Am J Hum Genet. 2008 Nov;83(5):547-58 PMID: 18950741
  38. Congenital heart disease and other heterotaxic defects in a large cohort of patients with primary ciliary dyskinesia.
    Circulation. 2007 Jun 5;115(22):2814-21 PMID: 17515466
  39. Primary ciliary dyskinesia: current state of the art.
    Arch Dis Child. 2007 Dec;92(12):1136-40 PMID: 17634184
  40. The Chlamydomonas Sourcebook. A Comprehensive Guide to Biology and Laboratory Use. Elizabeth H. Harris. Academic Press, San Diego, CA, 1989. xiv, 780 pp., illus. $145.
    Science. 1989 Dec 15;246(4936):1503-4 PMID: 17756009
  41. Loci for primary ciliary dyskinesia map to chromosome 16p12.1-12.2 and 15q13.1-15.1 in Faroe Islands and Israeli Druze genetic isolates.
    J Med Genet. 2004 Mar;41(3):233-40 PMID: 14985390
  42. Comparative genomics of trypanosomatid parasitic protozoa.
    Science. 2005 Jul 15;309(5733):404-9 PMID: 16020724
  43. RPGR is mutated in patients with a complex X linked phenotype combining primary ciliary dyskinesia and retinitis pigmentosa.
    J Med Genet. 2006 Apr;43(4):326-33 PMID: 16055928
  44. Innate pulmonary immunity: cilia.
    Pediatr Pulmonol Suppl. 2004;26:72-3 PMID: 15029603
Article Info
Journal
American journal of human genetics
Abbr.
Am J Hum Genet
ISSN
1537-6605
Published
2009-02-00
Epub
2009-00-05
Pages
197-209
Language
English
Region
United States
NLM ID
0370475
PMCID
PMC2668031
Subset
IM
Grants
Wellcome Trust · United Kingdom
Medical Research Council · G0700073 · United Kingdom
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