The role of molecular genetic analysis in the diagnosis of primary ciliary dyskinesia

Annals of the American Thoracic Society

Volumn 11, Issue 3, 2014, Pages 351-359

  Kim, Raymond H ^a,b   Hall, David A ^c,d   Cutz, Ernest ^a,d   Knowles, Michael R ^e   Nelligan, Kathleen A ^a   Nykamp, Keith ^f   Zariwala, Maimoona A ^e   Dell, Sharon D ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c ST MICHAEL'S HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^f Prevention Genetics   (United States)

Author keywords

Diagnostic testing; Genetic analysis; Primary ciliary dyskinesia

Indexed keywords

NITRIC OXIDE; AXONEMAL DYNEIN; DNAH5 PROTEIN, HUMAN;

ADOLESCENT; ADULT; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BIOPSY; CHILD; CILIARY DYSKINESIA; CONTROLLED STUDY; DIAGNOSTIC TEST; DIAGNOSTIC VALUE; FEMALE; GENE MUTATION; GENETIC ANALYSIS; HUMAN; MAJOR CLINICAL STUDY; MALE; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; SENSITIVITY ANALYSIS; STRUCTURE ANALYSIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; URBAN AREA; VIDEO MICROSCOPY; GENETIC SCREENING; GENETICS; INFANT; KARTAGENER SYNDROME; MIDDLE AGED; MOLECULAR DIAGNOSIS; MUTATION; PRESCHOOL CHILD; REPRODUCIBILITY; RETROSPECTIVE STUDY; YOUNG ADULT;

ADOLESCENT; ADULT; AXONEMAL DYNEINS; CHILD; CHILD, PRESCHOOL; FEMALE; GENETIC TESTING; HUMANS; INFANT; KARTAGENER SYNDROME; MALE; MIDDLE AGED; MOLECULAR DIAGNOSTIC TECHNIQUES; MUTATION; REPRODUCIBILITY OF RESULTS; RETROSPECTIVE STUDIES; YOUNG ADULT;

EID: 84898756545     PISSN: 23256621     EISSN: None     Source Type: Journal    
DOI: 10.1513/AnnalsATS.201306-194OC     Document Type: Article

References (44)

1. Zariwala MA, Knowles MR, Leigh MW. Primary ciliary dyskinesia. 2007 Jan 24 [accessed 28 Feb 2013]. In: Pagon RA, Adam MP, Bird TD, et al. GeneReviews [Internet]. University of Washington, Seattle, 1993. Available from: http://www.ncbi.nlm.nih.gov/books/NBK1122/.
2. Leigh MW, Pittman JE, Carson JL, Ferkol TW, Dell SD, Davis SD, Knowles MR, Zariwala MA. Clinical and genetic aspects of primary ciliary dyskinesia/Kartagener syndrome. Genet Med 2009;11: 473-487.
3. Barbato A, Frischer T, Kuehni CE, Snijders D, Azevedo I, Baktai G, Bartoloni L, Eber E, Escribano A, Haarman E, et al . Primary ciliary dyskinesia: a consensus statement on diagnostic and treatment approaches in children. Eur Respir J 2009;34: 1264-1276.
4. Olin JT, Burns K, Carson JL, Metjian H, Atkinson JJ, Davis SD, Dell SD, Ferkol TW, Milla CE, Olivier KN, et al.; for the Genetic Disorders of Mucociliary Clearance Consortium. Diagnostic yield of nasal scrape biopsies in primary ciliary dyskinesia: a multicenter experience. Pediatr Pulmonol 2011;46:483-488.
5. Shoemark A, Dixon M, Corrin B, Dewar A. Twenty-year review of quantitative transmission electron microscopy for the diagnosis of primary ciliary dyskinesia. J Clin Pathol 2012;65:267-271.
6. Duriez B, Duquesnoy P, Escudier E, Bridoux AM, Escalier D, Rayet I, Marcos E, Vojtek AM, Bercher JF, Amselem S. A common variant in combination with a nonsense mutation in a member of the thioredoxin family causes primary ciliary dyskinesia. Proc Natl Acad Sci USA 2007;104:3336-3341. (Pubitemid 46364160)
7. Knowles MR, Leigh MW, Ostrowski LE, Huang L, Carson JL, Hazucha MJ, Yin W, Berg JS, Davis SD, Dell SD, et al.; Genetic Disorders of Mucociliary Clearance Consortium. Exome sequencing identifies mutations in CCDC114 as a cause of primary ciliary dyskinesia. Am J Hum Genet 2013;92:99-106.
8. Loges NT, Olbrich H, Fenske L, Mussaffi H, Horvath J, Fliegauf M, Kuhl H, Baktai G, Peterffy E, Chodhari R, et al . DNAI2 mutations cause primary ciliary dyskinesia with defects in the outer dynein arm. Am J Hum Genet 2008;83:547-558.
9. Mazor M, Alkrinawi S, Chalifa-Caspi V, Manor E, Sheffield VC, Aviram M, Parvari R. Primary ciliary dyskinesia caused by homozygous mutation in DNAL1, encoding dynein light chain 1. Am J Hum Genet 2011;88:599 -607.
10. Olbrich H, Häffner K, Kispert A, Völkel A, Volz A, Sasmaz G, Reinhardt R, Hennig S, Lehrach H, Konietzko N, et al. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat Genet 2002;30:143-144.
11. Onoufriadis A, Paff T, Antony D, Shoemark A, Micha D, Kuyt B, Schmidts M, Petridi S, Dankert-Roelse JE, Haarman EG, et al.; UK10K. Splice-site mutations in the axonemal outer dynein arm docking complex gene CCDC114 cause primary ciliary dyskinesia. Am J Hum Genet 2013;92:88-98.
12. Pennarun G, Escudier E, Chapelin C, Bridoux AM, Cacheux V, Roger G, Clément A, Goossens M, Amselem S, Duriez B. Loss-of-function mutations in a human gene related to Chlamydomonas reinhardtii dynein IC78 result in primary ciliary dyskinesia. Am J Hum Genet 1999;65:1508-1519. (Pubitemid 30468663)
13. Hjeij R, Lindstrand A, Francis R, Zariwala MA, Liu X, Li Y, Damerla R, Dougherty GW, Abouhamed M, Olbrich H, et al. ARMC4 mutations cause primary ciliary dyskinesia with randomization of left/right body asymmetry. Am J Hum Genet 2013;93:357-367.
14. Duquesnoy P, Escudier E, Vincensini L, Freshour J, Bridoux AM, Coste A, Deschildre A, de Blic J, Legendre M, Montantin G, et al. Loss-offunction mutations in the human ortholog of Chlamydomonas reinhardtii ODA7 disrupt dynein arm assembly and cause primary ciliary dyskinesia. Am J Hum Genet 2009;85:890-896.
15. Horani A, Druley TE, Zariwala MA, Patel AC, Levinson BT, Van Arendonk LG, Thornton KC, Giacalone JC, Albee AJ, Wilson KS, et al. Whole-exome capture and sequencing identifies HEATR2 mutation as a cause of primary ciliary dyskinesia. Am J Hum Genet 2012;91:685-693.
16. Kott E, Duquesnoy P, Copin B, Legendre M, Dastot-Le Moal F, Montantin G, Jeanson L, Tamalet A, Papon JF, Siffroi JP, et al. 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 2012;91:958-964.
17. Loges NT, Olbrich H, Becker-Heck A, Häffner K, Heer A, Reinhard C, Schmidts M, Kispert A, Zariwala MA, Leigh MW, et al. Deletions and point mutations of LRRC50 cause primary ciliary dyskinesia due to dynein arm defects. Am J Hum Genet 2009;85:883-889.
18. Mitchison HM, Schmidts M, Loges NT, Freshour J, Dritsoula A, Hirst RA, O'Callaghan C, Blau H, Al Dabbagh M, Olbrich H, et al. Mutations in axonemal dynein assembly factor DNAAF3 cause primary ciliary dyskinesia. Nat Genet 2012;44:381-389, S1-S2.
19. Omran H, Kobayashi D, Olbrich H, Tsukahara T, Loges NT, Hagiwara H, Zhang Q, Leblond G, O'Toole E, Hara C, et al. Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins. Nature 2008;456:611-616.
20. Panizzi JR, Becker-Heck A, Castleman VH, Al-Mutairi DA, Liu Y, Loges NT, Pathak N, Austin-Tse C, Sheridan E, Schmidts M, et al. CCDC103 mutations cause primary ciliary dyskinesia by disrupting assembly of ciliary dynein arms. Nat Genet 2012;44:714-719.
21. Zariwala MA, Gee HY, Kurkowiak M, Al-Mutairi DA, Leigh MW, Hurd TW, Hjeij R, Dell SD, Chaki M, Dougherty GW, et al. ZMYND10 is mutated in primary ciliary dyskinesia and interacts with LRRC6. Am J Hum Genet 2013;93:336-345.
22. Moore DJ, Onoufriadis A, Shoemark A, Simpson MA, zur Lage PI, de Castro SC, Bartoloni L, Gallone G, Petridi S, Woollard WJ, et al. Mutations in ZMYND10, a gene essential for proper axonemal assembly of inner and outer dynein arms in humans and flies, cause primary ciliary dyskinesia. Am J Hum Genet 2013;93:346-356.
23. Castleman VH, Romio L, Chodhari R, Hirst RA, de Castro SC, Parker KA, Ybot-Gonzalez P, Emes RD, Wilson SW, Wallis C, et al. Mutations in radial spoke head protein genes RSPH9 and RSPH4A cause primary ciliary dyskinesia with central-microtubular-pair abnormalities. Am J Hum Genet 2009;84:197-209.
24. Kott E, Legendre M, Copin B, Papon JF, Dastot-Le Moal F, Montantin G, Duquesnoy P, Piterboth W, Amram D, Bassinet L, et al. Loss-of-function mutations in RSPH1 cause primary ciliary dyskinesia with central-complex and radial-spoke defects. Am J Hum Genet 2013;93:561-570.
25. Antony D, Becker-Heck A, Zariwala MA, Schmidts M, Onoufriadis A, Forouhan M, Wilson R, Taylor-Cox T, Dewar A, Jackson C, et al.; UK10K. Mutations in CCDC39 and CCDC40 are the major cause of primary ciliary dyskinesia with axonemal disorganization and absent inner dynein arms. Hum Mutat 2013;34:462-472.
26. Becker-Heck A, Zohn IE, Okabe N, Pollock A, Lenhart KB, Sullivan-Brown J, McSheene J, Loges NT, Olbrich H, Haeffner K, et al. The coiled-coil domain containing protein CCDC40 is essential for motile cilia function and left-right axis formation. Nat Genet 2011;43:79-84.
27. Merveille AC, Davis EE, Becker-Heck A, Legendre M, Amirav I, Bataille G, Belmont J, Beydon N, Billen F, Clément A, et al. 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 2011;43:72-78.
28. Knowles MR, Leigh MW, Carson JL, Davis SD, Dell SD, Ferkol TW, Olivier KN, Sagel SD, Rosenfeld M, Burns KA, et al.; Genetic Disorders of Mucociliary Clearance Consortium. Mutations of DNAH11 in patients with primary ciliary dyskinesia with normal ciliary ultrastructure. Thorax 2012;67:433-441.
29. Olbrich H, Schmidts M, Werner C, Onoufriadis A, Loges NT, Raidt J, Banki NF, Shoemark A, Burgoyne T, Al Turki S, et al.; UK10K Consortium. Recessive HYDIN mutations cause primary ciliary dyskinesia without randomization of left-right body asymmetry. Am J Hum Genet 2012;91:672-684.
30. Wirschell M, Olbrich H, Werner C, Tritschler D, Bower R, Sale WS, Loges NT, Pennekamp P, Lindberg S, Stenram U, et al. The nexindynein regulatory complex subunit DRC1 is essential for motile cilia function in algae and humans. Nat Genet 2013;45:262-268.
31. Horani A, Brody SL, Ferkol TW, Shoseyov D, Wasserman MG, Tashma A, Wilson KS, Bayly PV, Amirav I, Cohen-Cymberknoh M, et al. CCDC65 mutation causes primary ciliary dyskinesia with normal ultrastructure and hyperkinetic cilia. PLoS ONE 2013;8:e72299.
32. American Thoracic Society; European Respiratory Society. ATS/ ERS recommendations for standardized procedures for the online and of fline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med 2005;171:912-930.
33. Struben VM, Wieringa MH, Mantingh CJ, Bommeljé C, Don M, Feenstra L, de Jongste JC. Nasal NO: normal values in children age 6 through to 17 years. Eur Respir J 2005;26:453 -457.
34. Noone PG, Leigh MW, Sannuti A, Minnix SL, Carson JL, Hazucha M, Zariwala MA, Knowles MR. Primary ciliary dyskinesia: diagnostic and phenotypic features. Am J Respir Crit Care Med 2004;169:459-467. (Pubitemid 38187117)
35. Piacentini GL, Bodini A, Peroni D, Rigotti E, Pigozzi R, Pradal U, Boner AL. Nasal nitric oxide for early diagnosis of primary ciliary dyskinesia: practical issues in children. Respir Med 2008;102:541-547.
36. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. A method and server for predicting damaging missense mutations. Nat Methods 2010;7:248-249.
37. Kumar P, Henikoff S, Ng PC. Predicting the effects of coding nonsynonymous variants on protein function using the SIFT algorithm. Nat Protoc 2009;4:1073-1081.
38. Schwarz JM, Rödelsperger C, Schuelke M, Seelow D. MutationTaster evaluates disease-causing potential of sequence alterations. Nat Methods 2010;7:575-576.
39. Hornef N, Olbrich H, Horvath J, Zariwala MA, Fliegauf M, Loges NT, Wildhaber J, Noone PG, Kennedy M, Antonarakis SE, et al. DNAH5 mutations are a common cause of primary ciliary dyskinesia with outer dynein arm defects. Am J Respir Crit Care Med 2006;174:120-126. (Pubitemid 44015384)
40. Failly M, Saitta A, Muñoz A, Falconnet E, Rossier C, Santamaria F, de Santi MM, Lazor R, DeLozier-Blanchet CD, Bartoloni L, et al. DNAI1 mutations explain only 2% of primary ciliary dykinesia. Respiration 2008;76:198-204.
41. Failly M, Bartoloni L, Letourneau A, Munoz A, Falconnet E, Rossier C, de Santi MM, Santamaria F, Sacco O, DeLozier-Blanchet CD, et al. Mutations in DNAH5 account for only 15% of a non-preselected cohort of patients with primary ciliary dyskinesia. J Med Genet 2009;46:281-286.
42. Djakow J, Svobodová T, Hrach K, Uhlík J, Cinek O, Pohunek P. Effectiveness of sequencing selected exons of DNAH5 and DNAI1 in diagnosis of primary ciliary dyskinesia. Pediatr Pulmonol 2012;47:864-875.
43. Lucas JS, Adam EC, Goggin PM, Jackson CL, Powles-Glover N, Patel SH, Humphreys J, Fray MD, Falconnet E, Blouin JL, et al. Static respiratory cilia associated with mutations in Dnahc11/DNAH11: a mouse model of PCD. Hum Mutat 2012;33:495-503.
44. O'Callaghan C, Rutman A, Williams GM, Hirst RA. Inner dynein arm defects causing primary ciliary dyskinesia: repeat testing required. Eur Respir J 2011;38:603-607.