LRRC6 Mutation Causes Primary Ciliary Dyskinesia with Dynein Arm Defects

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Horani, Amjad ^a   Ferkol, Thomas W ^a   Shoseyov, David ^b   Wasserman, Mollie G ^a   Oren, Yifat S ^c   Kerem, Batsheva ^c   Amirav, Israel ^d   Cohen Cymberknoh, Malena ^b   Dutcher, Susan K ^a   Brody, Steven L ^a   Elpeleg, Orly ^b   Kerem, Eitan ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d Rebecca Sieff Government Hospital   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; DYNEIN ADENOSINE TRIPHOSPHATASE; HISTIDINE; NITRIC OXIDE; SHORT HAIRPIN RNA;

ADOLESCENT; ADULT; ARTICLE; BRONCHIECTASIS; CHROMOSOME 8; CILIARY DYSKINESIA; CLINICAL ARTICLE; CLINICAL EVALUATION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME DEFECT; FEMALE; GENE; GENE FUNCTION; GENE LOCATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC LINKAGE; HAPLOTYPE; HOMOZYGOSITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LEUCINE RICH REPEAT CONTAINING PROTEIN 6 GENE; MALE; MISSENSE MUTATION; MUTATIONAL ANALYSIS; OTITIS MEDIA; PATHOGENESIS; PEDIGREE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHINOSINUSITIS; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; ADULT; AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ARABS; BASE SEQUENCE; CHROMOSOMES, HUMAN, PAIR 8; DYNEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; GENES, RECESSIVE; GENETIC LINKAGE; HEK293 CELLS; HUMANS; KARTAGENER SYNDROME; MALE; MICROSCOPY, ELECTRON; MICROSCOPY, VIDEO; MOLECULAR SEQUENCE DATA; NASAL MUCOSA; OLIGONUCLEOTIDES; PEDIGREE; PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA;

EID: 84875099215     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059436     Document Type: Article

References (52)

1. Ferkol TW, Leigh MW, (2012) Ciliopathies: the central role of cilia in a spectrum of pediatric disorders. J Pediatr 160: 366-371.
2. Knowles MR, Boucher RC, (2002) Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 109: 571-577.
3. Afzelius BA, (1976) A human syndrome caused by immotile cilia. Science 193: 317-319.
4. Chilvers MA, Rutman A, O'Callaghan C, (2003) Ciliary beat pattern is associated with specific ultrastructural defects in primary ciliary dyskinesia. J Allergy Clin Immunol 112: 518-524.
5. Kennedy MP, Omran H, Leigh MW, Dell S, Morgan L, et al. (2007) Congenital heart disease and other heterotaxic defects in a large cohort of patients with primary ciliary dyskinesia. Circulation 115: 2814-2821.
6. Leigh MW, Pittman JE, Carson JL, Ferkol TW, Dell SD, et al. (2009) Clinical and genetic aspects of primary ciliary dyskinesia/Kartagener syndrome. Genet Med 11: 473-487.
7. Wessels MW, den Hollander NS, Willems PJ, (2003) Mild fetal cerebral ventriculomegaly as a prenatal sonographic marker for Kartagener syndrome. Prenat Diagn 23: 239-242.
8. Olbrich H, Haffner K, Kispert A, Volkel A, Volz A, et al. (2002) Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat Genet 30: 143-144.
9. Guichard C, Harricane MC, Lafitte JJ, Godard P, Zaegel M, et al. (2001) Axonemal dynein intermediate-chain gene (DNAI1) mutations result in situs inversus and primary ciliary dyskinesia (Kartagener syndrome). Am J Hum Genet 68: 1030-1035.
10. Loges NT, Olbrich H, Fenske L, Mussaffi H, Horvath J, et al. (2008) DNAI2 mutations cause primary ciliary dyskinesia with defects in the outer dynein arm. Am J Hum Genet 83: 547-558.
11. Duriez B, Duquesnoy P, Escudier E, Bridoux AM, Escalier D, et al. (2007) A common variant in combination with a nonsense mutation in a member of the thioredoxin family causes primary ciliary dyskinesia. Proc Natl Acad Sci U S A 104: 3336-3341.
12. Horvath J, Fliegauf M, Olbrich H, Kispert A, King SM, et al. (2005) Identification and analysis of axonemal dynein light chain 1 in primary ciliary dyskinesia patients. Am J Respir Cell Mol Biol 33: 41-47.
13. Horani A, Druley TE, Zariwala MA, Patel AC, Levinson BT, et al. (2012) Whole-Exome Capture and Sequencing Identifies HEATR2 Mutation as a Cause of Primary Ciliary Dyskinesia. Am J Hum Genet 91: 685-693.
14. Omran H, Kobayashi D, Olbrich H, Tsukahara T, Loges NT, et al. (2008) Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins. Nature 456: 611-616.
15. Castleman VH, Romio L, Chodhari R, Hirst RA, de Castro SC, et al. (2009) Mutations in radial spoke head protein genes RSPH9 and RSPH4A cause primary ciliary dyskinesia with central-microtubular-pair abnormalities. Am J Hum Genet 84: 197-209.
16. Blanchon S, Legendre M, Copin B, Duquesnoy P, Montantin G, et al. (2012) Delineation of CCDC39/CCDC40 mutation spectrum and associated phenotypes in primary ciliary dyskinesia. J Med Genet 49: 410-416.
17. Knowles MR, Leigh MW, Carson JL, Davis SD, Dell SD, et al. (2011) Mutations of DNAH11 in patients with primary ciliary dyskinesia with normal ciliary ultrastructure. Thorax 67: 433-441.
18. Pennarun G, Escudier E, Chapelin C, Bridoux AM, Cacheux V, et al. (1999) Loss-of-function mutations in a human gene related to Chlamydomonas reinhardtii dynein IC78 result in primary ciliary dyskinesia. Am J Hum Genet 65: 1508-1519.
19. Bartoloni L, Blouin JL, Pan Y, Gehrig C, Maiti AK, et al. (2002) Mutations in the DNAH11 (axonemal heavy chain dynein type 11) gene cause one form of situs inversus totalis and most likely primary ciliary dyskinesia. Proc Natl Acad Sci U S A 99: 10282-10286.
20. Mitchison HM, Schmidts M, Loges NT, Freshour J, Dritsoula A, et al. (2012) Mutations in axonemal dynein assembly factor DNAAF3 cause primary ciliary dyskinesia. Nat Genet 44: 381-389.
21. Merveille AC, Davis EE, Becker-Heck A, Legendre M, Amirav I, et al. (2011) CCDC39 is required for assembly of inner dynein arms and the dynein regulatory complex and for normal ciliary motility in humans and dogs. Nat Genet 43: 72-78.
22. Becker-Heck A, Zohn IE, Okabe N, Pollock A, Lenhart KB, et al. (2011) The coiled-coil domain containing protein CCDC40 is essential for motile cilia function and left-right axis formation. Nat Genet 43: 79-84.
23. Panizzi JR, Becker-Heck A, Castleman VH, Al-Mutairi DA, Liu Y, et al. (2012) CCDC103 mutations cause primary ciliary dyskinesia by disrupting assembly of ciliary dynein arms. Nat Genet 44: 714-719.
24. Olbrich H, Schmidts M, Werner C, Onoufriadis A, Loges NT, et al. (2012) Recessive HYDIN mutations cause primary ciliary dyskinesia without randomization of left-right body asymmetry. Am J Hum Genet 91: 672-684.
25. Loges NT, Olbrich H, Becker-Heck A, Haffner K, Heer A, et al. (2009) Deletions and point mutations of LRRC50 cause primary ciliary dyskinesia due to dynein arm defects. Am J Hum Genet 85: 883-889.
26. Gherman A, Davis EE, Katsanis N, (2006) The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat Genet 38: 961-962.
27. Serluca FC, Xu B, Okabe N, Baker K, Lin SY, et al. (2009) Mutations in zebrafish leucine-rich repeat-containing six-like affect cilia motility and result in pronephric cysts, but have variable effects on left-right patterning. Development 136: 1621-1631.
28. Kobe B, Kajava AV, (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11: 725-732.
29. Edvardson S, Shaag A, Kolesnikova O, Gomori JM, Tarassov I, et al. (2007) Deleterious mutation in the mitochondrial arginyl-transfer RNA synthetase gene is associated with pontocerebellar hypoplasia. Am J Hum Genet 81: 857-862.
30. Dejima K, Randell SH, Stutts MJ, Senior BA, Boucher RC, (2006) Potential role of abnormal ion transport in the pathogenesis of chronic sinusitis. Arch Otolaryngol Head Neck Surg 132: 1352-1362.
31. You Y, Richer EJ, Huang T, Brody SL, (2002) Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am J Physiol Lung Cell Mol Physiol 283: L1315-1321.
32. Feng Y, Nie L, Thakur MD, Su Q, Chi Z, et al. (2010) A multifunctional lentiviral-based gene knockdown with concurrent rescue that controls for off-target effects of RNAi. Genomics Proteomics Bioinformatics 8: 238-245.
33. Stewart SA, Dykxhoorn DM, Palliser D, Mizuno H, Yu EY, et al. (2003) Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 9: 493-501.
34. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D, (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295: 868-872.
35. Pan J, You Y, Huang T, Brody SL, (2007) RhoA-mediated apical actin enrichment is required for ciliogenesis and promoted by Foxj1. J Cell Sci 120: 1868-1876.
36. Ostrowski LE, Yin W, Rogers TD, Busalacchi KB, Chua M, et al. (2010) Conditional deletion of dnaic1 in a murine model of primary ciliary dyskinesia causes chronic rhinosinusitis. Am J Respir Cell Mol Biol 43: 55-63.
37. Jain R, Ray JM, Pan JH, Brody SL, (2012) Sex hormone-dependent regulation of cilia beat frequency in airway epithelium. Am J Respir Cell Mol Biol 46: 446-453.
38. Barbato A, Frischer T, Kuehni CE, Snijders D, Azevedo I, et al. (2009) Primary ciliary dyskinesia: a consensus statement on diagnostic and treatment approaches in children. Eur Respir J 34: 1264-1276.
39. Sisson JH, Stoner JA, Ammons BA, Wyatt TA, (2003) All-digital image capture and whole-field analysis of ciliary beat frequency. J Microsc 211: 103-111.
40. Walker WT, Jackson CL, Lackie PM, Hogg C, Lucas JS, (2012) Nitric oxide in primary ciliary dyskinesia. Eur Respir J 40: 1024-1032.
41. Noone PG, Leigh MW, Sannuti A, Minnix SL, Carson JL, et al. (2004) Primary ciliary dyskinesia: diagnostic and phenotypic features. Am J Respir Crit Care Med 169: 459-467.
42. Xue JC, Goldberg E, (2000) Identification of a novel testis-specific leucine-rich protein in humans and mice. Biol Reprod 62: 1278-1284.
43. UniProt Consortium, (2012) Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40: D71-75.
44. Price SR, Evans PR, Nagai K, (1998) Crystal structure of the spliceosomal U2B"-U2A' protein complex bound to a fragment of U2 small nuclear RNA. Nature 394: 645-650.
45. Dutcher SK, (1995) Flagellar assembly in two hundred and fifty easy-to-follow steps. Trends Genet 11: 398-404.
46. Kavlie RG, Kernan MJ, Eberl DF Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility. Genetics 185: 177-188.
47. Morgan GW, Denny PW, Vaughan S, Goulding D, Jeffries TR, et al. (2005) An evolutionarily conserved coiled-coil protein implicated in polycystic kidney disease is involved in basal body duplication and flagellar biogenesis in Trypanosoma brucei. Mol Cell Biol 25: 3774-3783.
48. Fliegauf M, Olbrich H, Horvath J, Wildhaber JH, Zariwala MA, et al. (2005) Mislocalization of DNAH5 and DNAH9 in respiratory cells from patients with primary ciliary dyskinesia. Am J Respir Crit Care Med 171: 1343-1349.
49. Brody SL, Yan XH, Wuerffel MK, Song SK, Shapiro SD, (2000) Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am J Respir Cell Mol Biol 23: 45-51.
50. Kott E, Duquesnoy P, Copin B, Legendre M, Dastot-Le Moal F, et al. (2012) Loss-of-Function Mutations in LRRC6, a Gene Essential for Proper Axonemal Assembly of Inner and Outer Dynein Arms, Cause Primary Ciliary Dyskinesia. Am J Hum Genet 91: 958-964.
51. Pazour GJ, Agrin N, Leszyk J, Witman GB, (2005) Proteomic analysis of a eukaryotic cilium. J Cell Biol 170: 103-113.
52. Ostrowski LE, Blackburn K, Radde KM, Moyer MB, Schlatzer DM, et al. (2002) A proteomic analysis of human cilia: identification of novel components. Mol Cell Proteomics 1: 451-465.