Primary ciliary dyskinesia: Recent advances in pathogenesis, diagnosis and treatment

Drugs

Volumn 67, Issue 13, 2007, Pages 1883-1892

  Lie, Hauw ^a   Ferkol, Thomas ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ST LOUIS CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; ARGININE; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CORTICOSTEROID; DORNASE ALFA; NITRIC OXIDE; SACCHARIN; URIDINE PHOSPHATE;

BRONCHIECTASIS; CHRONIC RHINITIS; CILIARY DYSKINESIA; CILIARY MOTILITY; CLINICAL FEATURE; CLINICAL TRIAL; EUKARYOTIC FLAGELLUM; GENE MUTATION; GENETIC SCREENING; HUMAN; IMMUNOFLUORESCENCE TEST; LUNG RESECTION; MUCOCILIARY CLEARANCE; NOSE SURGERY; OTITIS MEDIA; PATHOGENESIS; REVIEW; SINUSITIS; TRANSMISSION ELECTRON MICROSCOPY;

ADRENAL CORTEX HORMONES; ANTI-BACTERIAL AGENTS; ARGININE; CILIA; CILIARY MOTILITY DISORDERS; DEOXYRIBONUCLEASE I; HUMANS; URIDINE TRIPHOSPHATE;

EID: 34548341829     PISSN: 00126667     EISSN: 00126667     Source Type: Journal    
DOI: 10.2165/00003495-200767130-00006     Document Type: Review

References (100)

1. Afzelius BA, Eliasson R, Johnson O, et al. Lack of dyein arms in immotile human spermatozoa. J Cell Biol 1975; 66: 225-32
2. Pedersen H, Rebbe H. Absence of arms in the axoneme of immobile human spermatozoa. Biol Reprod 1975; 12: 541-4
3. Eliasson R, Mossberg B, Camner P, et al. The immotile-cilia syndrome: a congenital ciliary abnormality as an etiologic factor in chronic airway infections and male sterility. N Engl J Med 1977; 297: 1-6
4. Rossman CM, Forrest JB, Lee RM, et al. The dyskinetic cilia syndrome: ciliary motility in immotile cilia syndrome. Chest 1980; 78: 580-2
5. Wanner A, Salathé M, O'Riordan TG. Mucociliary clearance in the airways. Am J Respir Crit Care Med 1996; 154: 1868-902
6. Knowles MR, Boucher RC. Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 2002; 109: 571-7
7. Beisson J, Wright M. Basal body/centriole assembly and continuity. Curr Opin Cell Biol 2003; 15: 96-104
8. Luck DJL. Genetic and biochemical dissection of the eukaryotic flagellum. J Cell Biol 1984; 98: 789-94
9. Ostrowski LE, Blackburn K, Radde KM, et al. A proteomic analysis of human cilia: identification of novel components. Mol Cell Proteomics 2002; 1: 451-65
10. Houtmeyers E, Gosselink R, Gayan-Ramirez G, et al. Regulation of mucociliary clearance in health and disease. Eur Respir J 1999; 13: 1177-88
11. Afzelius BA. Cilia-related diseases. J Pathol 2004; 204: 470-7
12. Ibañez-Tallon I, Heintz N, Omran H. To beat or not to beat: roles of cilia in development and disease. Hum Mol Genet 2003; 12: R27-35
13. Eley L, Yates LM, Goodship JA. Cilia and disease. Curr Opin Genet Dev 2005; 15: 308-14
14. Davenport JR, Yoker BK. An incredible decade for the primary cilium: a look at a once-forgotten organelle. Am J Physiol Renal Physiol 2005; 289: F1159-69
15. Badano JL, Mitsuma N, Beales PL, et al. The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 2006; 7: 125-48
16. Cano DA, Sekine S, Hebrok M. Primary cilia deletion in pancreatic epithelial cells results in cyst formation and pancreatitis. Gastroenterology 2006; 131: 1856-9
17. Nonaka S, Tanaka Y, Okada Y, et al. Randomization of left-right asymmetry due to loss of nodal cilia generative leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 1998; 95: 829-37
18. McGrath J, Somlo S, Makova S, et al. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 2003; 114: 61-73
19. Okada Y, Nonaka S, Tanaka Y, et al. Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol Cell 1999; 4: 459-68
20. Krawczynski MR, Dmenska H, Witt M. Apparent X-linked primary ciliary dyskinesia associated with retinitis pigmentosa and a hearing loss. J Appl Genet 2004; 45: 107-10
21. Moore A, Escudier E, Roger G, et al. RPGR is mutated in patients with a complex X-linked phenotype combining primary ciliary dyskinesia and retinitis pigmentosa. J Med Genet 2005; 43: 326-33
22. Torgersen J. Situs inversus, asymmetry, and twinning. Am J Hum Genet 1950; 2: 361-70
23. Katsuhara K, Kawamoto S, Wakabayashi T, et al. Situs inversus totalis and Kartagener's syndrome in a Japanese population. Chest 1972; 61: 56-61
24. Afzeluis BA, Mossberg B. Immotile cilia syndrome (primary ciliary dyskinesia) including Kartagener syndrome. New York: McGraw-Hill, 1995
25. Afzeluis BA. Genetics and pulmonary medicine. 6. Immotile cilia syndrome: past, present, and prospects for the future. Thorax 1998; 53: 894-7
26. Blouin JL, Meeks M, Radhakrishna U, et al. Primary ciliary dyskinesia: a genome-wide linkage analysis reveals extensive locus heterogeneity. Eur J Hum Genet 2000; 8: 109-18
27. Geremek M, Witt M. Primary ciliary dyskinesia: genes, candidate genes and chromosomal regions. J Appl Genet 2004; 45: 347-61
28. Blair DF, Dutcher SK. Flagella in prokaryotes and lower eukaryotes. Curr Opin Genet Dev 1992; 2: 756-67
29. Gibbons IR. Dynein family of motor proteins: present status and future questions. Cell Motil Cytoskeleton 1995; 32: 136-44
30. Harrison A, King SM. The molecular anatomy of dynein. Essays Biochem 2000; 35: 75-87
31. Li JB, Gerdes JM, Haycraft CJ, et al. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 2004; 117: 541-52
32. Pazour GJ, Agrin N, Leszyk J, et al. Proteomic analysis of a eukaryotic cilium. J Cell Biol 2005; 170: 103-13
33. Maiti AK, Mattel MG, Jorissen M, et al. Identification, tissue specific expression, and chromosomal localization of several human dynein heavy chain genes. Eur J Hum Genet 2000; 8: 923-32
34. Wilkerson CG, King SM, Witman GB. Molecular analysis of the gamma heavy chain of Chlamydomonas flagellar outer arm dynein. J Cell Sci 1994; 107: 497-506
35. Pennarun G, Escudier E, Chapelin C, et al. 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: 1508-19
36. Guichard C, Harricane MC, Lafitte JJ, et al. Axonemal dynein intermediate-chain gene (DNAI1) mutations result in situs inversus and primary ciliary dyskinesia (Kartagener syndrome). Am J Hum Genet 2001; 68: 1030-5
37. Zariwala M, Noone PG, Sannuti A, et al. Germline mutations in an intermediate chain dynein causes primary ciliary dyskinesia. Am J Respir Cell Mol Biol 2001; 25: 577-83
38. Zariwala MA, Leigh MW, Ceppa F, et al. Mutations of DNAI1 in primary ciliary dyskinesia: evidence of founder effect in a common mutation. Am J Respir Crit Care Med 2006; 174: 858-66
39. Ibanez-Tallon I, Gorokhova S, Heintz N. Loss of function of axonemal Mdnah5 causes primary ciliary dyskinesia and hydrocephalus. Hum Mol Genet 2002; 15: 715-21
40. Olbrich H, Haffner K, Kispert A, et al. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat Genet 2002; 30: 143-4
41. Kispert A, Petry M, Olbrich H, et al. Genotype-phenotype correlations in PCD patients carrying DNAH5 mutations. Thorax 2003; 58: 552-4
42. Fliegauf M, Olbrich H, Horvath J, et al. Mislocalization of DNAH5 and DNAH9 in respiratory cells from patients with primary ciliary dyskinesia. Am J Respir Crit Care Med 2005; 171: 1343-9
43. Hornef N, Olbrich H, Horvath J, 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: 120-6
44. Bartoloni L, Blouin JL, Pan Y, et al. Mutations in the DNAH11 (axonemal heavy chain dynein arm type 11) gene cause one form of situs inversus totalis and most likely primary ciliary dyskinesia. Proc Natl Acad Sci U S A 2002; 99: 10282-6
45. Pan Y, McCaskill CD, Thompson KH, et al. Paternal isodisomy of chromosome 7 associated with complete situs inversus and immotile cilia. Am J Hum Genet 1998; 62: 1551-5
46. Sleigh MA, Blake JR, Liron N. The propulsion of mucus by cilia. Am Rev Respir Dis 1988; 137: 726-41
47. Bush A, Cole P, Hariri M, et al. Primary ciliary dyskinesia: diagnosis and standards of care. Eur Respir J 1998; 12: 982-8
48. Noone PG, Leigh MW, Sannuti A, et al. Primary ciliary dyskinesia: diagnostic and phenotypic features. Am J Respir Crit Care Med 2004; 169: 459-67
49. Hossain T, Kappelman MD, Perez-Atayde AR, et al. Primary ciliary dyskinesia as a cause of neonatal respiratory distress: implications for the neonatologist. J Perinatal 2003; 23: 684-7
50. Holzmann D, Felix H. Neonatal respiratory distress syndrome: a sign of primary ciliary dyskinesia? Eur J Pediatr 2000; 159: 857-60
51. Bromiker R, Neeman Z, Bar-Oz B, et al. Early diagnosis of primary ciliary dyskinesia in a newborn without situs inversus. Acta Paediatr 2002; 91: 1002-11
52. Coren ME, Meeks M, Morrison I, et al. Primary ciliary dyskinesia: age at diagnosis and symptom history. Acta Paediatr 2002; 91: 667-9
53. Morini F, Cozzi DA, Conforti A, et al. An infant with respiratory distress and failure to thrive. Eur Respir J 2002; 20: 500-3
54. van der Baan S, Veerman AJ, Heidendahl GA, et al. Primary ciliary dyskinesia and nasal mucociliary clearance. Respiration 1987; 52: 68-75
55. Greenstone M, Rutman A, Dewar A, et al. Primary ciliary dyskinesia: cytological and clinical features. Q J Med 1988; 67: 405-30
56. Turner JA, Corkey CW, Lee JY, et al. Clinical expressions of immotile cilia syndrome. Pediatrics 1981; 67: 805-10
57. El Zein L, Omran H, Bouvagnet P. Lateralization defects and ciliary dyskinesia: lessons from algae. Trends Genet 2003; 19: 162-7
58. Brueckner M. Cilia propel the embryo in the right direction. Am J Med Genet 2001; 101: 339-44
59. Raman R, Al-Ali SY, Poole CA, et al. Isomerism of the right atrial appendages: clinical, anatomical, and microscopic study of a long-surviving case with asplenia and ciliary abnormalities. Clin Anat 2003; 16: 269-76
60. Munro NC, Currie DC, Lindsay KS, et al. Fertility in men with primary ciliary dyskinesia presenting with respiratory infection. Thorax 1994; 49: 684-7
61. Halbert SA, Patton DL, Zarutskie PW, et al. Function and structure of cilia in the fallopian tube of an infertile woman with Kartagener's syndrome. Hum Reprod 1997; 12: 55-8
62. Afzelius BA, Eliasson R. Male and female infertility problems in the immotile cilia syndrome. Eur J Respir Dis 1983; 64: 144-7
63. Greenstone MA, Jones RW, Dewar A, et al. Hydrocephalus and primary ciliary dyskinesia. Arch Dis Child 1984; 59: 481-2
64. De Santi MM, Magni A, Valletta EA, et al. Hydrocephalus, bronchiectasis, and ciliary aplasia. Arch Dis Child 1990; 65: 543-4
65. Zito I, Downes SM, Patel RJ, et al. RPGR mutation associated with retinitis pigmentosa, impaired hearing, and sinorespiratory infections. J Med Genet 2003; 40: 609-15
66. Engesaeth VG, Warner JO, Bush A. New associations of primary ciliary dyskinesia syndrome. Pediatr Pulmonol 1993; 16: 9-12
67. Carson JL, Collier AM. Ciliary defects: cell biology and clinical perspectives. Adv Pediatr 1988; 35: 139-65
68. Bertrand B, Collet S, Eloy P, et al. Secondary ciliary dyskinesia in upper respiratory tract. Acta Otorhinolaryngol Belg 2000; 54: 309-16
69. Carson JL, Collier AM, Fernald GW, et al. Microtubular discontinuities as acquired ciliary defects in airway epithelium of patients with chronic respiratory diseases. Ultrastruct Pathol 1994; 18: 327-32
70. Pifferi M, Cangiotti AM, Ragazzo V, et al. Primary ciliary dyskinesia: diagnosis in children with inconclusive ultrastructural findings. Pediatr Allergy Immunol 2001; 12: 274-82
71. Greenstone MA, Dewar A, Cole PJ. Ciliary dyskinesia with normal ultrastructure. Thorax 1983; 38: 875-6
72. Carda C, Armengot M, Escribano A, et al. Ultrastructural patterns of primary ciliary dyskinesia syndrome. Ultrastruct Pathol 2005; 29: 3-8
73. Jorissen M, Willems T. Success rates of respiratory epithelial cell culture techniques with ciliogenesis for diagnosing primary ciliary dyskinesia. Acta Otorhinolaryngol Belg 2000; 54: 357-65
74. Stanley P, MacWilliam L, Greenstone M, et al. Efficacy of a saccharin test for screening to detect abnormal mucociliary clearance. Br J Dis Chest 1984; 78: 9-26
75. Stannard W, Rutman A, Wallis C, et al. Central microtubular agenesis causing primary ciliary dyskinesia. Am J Respir Crit Care Med 2004; 169: 634-7
76. Chilvers MA, Rutman A, O'Callaghan C. Ciliary beat pattern is associated with specific ultrastructural defects in primary ciliary dyskinesia. J Allergy Clin Immunol 2003; 112: 518-24
77. Wodehouse T, Kharitonov SA, Mackay IS, et al. Nasal nitric oxide measurements for the screening of primary ciliary dyskinesia. Eur Respir J 2003; 21: 43-7
78. Corbelli R, Bringolf-Isler B, Amacher A, et al. Nasal nitric oxide measurements to screen children for primary ciliary dyskinesia. Chest 2004; 126: 1054-9
79. Jain B, Rubinstein I, Robbins RA, et al. Modulation of airway epithelial cell ciliary beat frequency by nitric oxide. Biochem Biophys Res Commun 1993; 191: 83-8
80. Xue C, Botkin SJ, Johns RA. Localization of endothelial NOS at the basal microtubule membrane in ciliated epithelium of the rat lung. J Histochem Cytochem 1996; 44: 463-71
81. Kawamoto H, Takeno S, Yajin K. Increased expression of inducible nitric oxide synthase in nasal epithelial cells in patients with allergic rhinitis. Laryngoscope 1999; 109: 2015-20
82. Baraldi E, Pasquale MF, Cangiotti AM, et al. Nasal nitric oxide is low early in life: case study of two infants with primary ciliary dyskinesia. Eur Respir J 2004; 24: 881-3
83. Bush A, Ferkol T. Movement: the emerging genetics of primary ciliary dyskinesia. Am J Respir Crit Care Med 2006; 174: 109-10
84. Ellerman A, Bisgaard H. Longitudinal study of lung function in a cohort of primary ciliary dyskinesia. Eur Respir J 1997; 10: 2376-9
85. Corkey CW, Levison H, Turner JA. The immotile cilia syndrome: a longitudinal survey. Am Rev Respir Dis 1981; 124: 544-8
86. Hellinckx J, Demedts M, De Boeck K. Primary ciliary dyskinesia: evolution of pulmonary function. Eur J Pediatr 1998; 157: 422-6
87. Gibson RL, Burns JL, Ramsey BW. Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med 2003; 168: 918-51
88. Phillips GE, Thomas S, Heather S, et al. Airway response of children with primary ciliary dyskinesia to exercise and β2-agonist challenge. Eur Respir J 1998; 11: 1389-91
89. Shak S, Capon DJ, Hellmiss R, et al. Recombinant human DNase I reduces the viscosity of cystic fibrosis sputum. Proc Natl Acad Sci U S A 1990; 87: 9188-92
90. Phipps RJ, Nadel JA, Davis B. Effect of alpha-adrenergic stimulation on mucus secretion and on ion transport in cat trachea in vitro. Am Rev Respir Dis 1980; 121: 359-65
91. Phipps RJ, Williams IP, Richardson PS, et al. Sympathomimetic drugs stimulate the output of secretory glycoproteins from human bronchi in vitro. Clin Sci Lond 1982; 63: 23-8
92. Bennett WD. Effect of β-adrenergic agonists on mucociliary clearance. J Allergy Clin Immunol 2002; 110: S291-7
93. Grasemann H, Gartig SS, Wiesemann HG, et al. Effect of L-arginine infusion on airway NO in cystic fibrosis and primary ciliary dyskinesia syndrome. Eur Respir J 1999; 13: 114-8
94. Noone PG, Bennett WD, Regnis JA, et al. Effect of aerosolized uridine-5′-triphosphate on airway clearance with cough in patients with primary ciliary dyskinesia. Am J Respir Crit Care Med 1999; 160: 144-9
95. Smit HJ, Schreurs AJ, van den Bosch JM, et al. Is resection of bronchiectasis beneficial in patients with primary ciliary dyskinesia? Chest 1996; 109: 1541-4
96. Macchiarini P, Chapelier A, Vouhe P, et al. Double lung transplantation in situs inversus with Kartagener's syndrome. Paris-Sud University Lung Transplant Group. J Thorac Cardiovasc Surg 1994; 108: 86-91
97. Rabago G, Copeland JG, Rosapepe F, et al. Heart-lung transplantation in situs inversus. Ann Thorac Surg 1996; 62: 296-8
98. Hadfield PJ, Rowe-Jones JM, Bush A, et al. Treatment of otitis media with effusion in children with primary ciliary dyskinesia. Clin Otolayrngol 1997; 22: 302-6
99. Majithia A, Fong J, Hariri M, et al. Hearing outcomes in children with primary ciliary dyskinesia: a longitudinal study. Int J Pediatr Otorhinolaryngol 2005; 69: 1061-4
100. Parsons DS, Greene BA. A treatment for primary ciliary dyskinesia: efficacy of functional endoscopic sinus surgery. Laryngoscope 1993; 103: 1269-72