Enhanced response to pulmonary Streptococcus pneumoniae infection is associated with primary ciliary dyskinesia in mice lacking Pcdp1 and Spef2

Cilia

Volumn 2, Issue 1, 2013, Pages

  McKenzie, Casey W ^a   Klonoski, Joshua M ^b   Maier, Taylor ^a   Trujillo, Glenda ^c   Vitiello, Peter F ^a,d   Huber, Victor C ^b   Lee, Lance ^a,d  

^a SANFORD RESEARCH   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

Cilia; Lung; Primary ciliary dyskinesia; Streptococcus pneumoniae

Indexed keywords

ALPHA TUBULIN; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; PROSURFACTANT PROTEIN B; SURFACTANT PROTEIN B; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIUM DETECTION; BACTERIUM IDENTIFICATION; CELLULAR IMMUNITY; CILIARY DYSKINESIA; CILIARY MOTILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISEASE SEVERITY; FLOW CYTOMETRY; GENE; GENE DELETION; GENE IDENTIFICATION; HISTOPATHOLOGY; HOST PATHOGEN INTERACTION; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; INFLAMMATION; INFLAMMATORY CELL; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; LYMPHOCYTE FUNCTION; MOUSE; MOUSE MODEL; MUCOCILIARY CLEARANCE; NONHUMAN; PCDP1 GENE; PRIORITY JOURNAL; SPEF2 GENE; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; T LYMPHOCYTE;

EID: 84906329500     PISSN: None     EISSN: 20462530     Source Type: Journal    
DOI: 10.1186/2046-2530-2-18     Document Type: Article

References (64)

1. Brandenburg JA, Marrie TJ, Coley CM, Singer DE, Obrosky DS, Kapoor WN, Fine MJ. Clinical presentation, processes and outcomes of care for patients with pneumococcal pneumonia. J Gen Intern Med 2000, 15:638-646. 10.1046/j.1525-1497.2000.04429.x, 1495594, 11029678.
2. Kadioglu A, Andrew PW. The innate immune response to pneumococcal lung infection: the untold story. Trends Immunol 2004, 25:143-149. 10.1016/j.it.2003.12.006, 15036042.
3. Ortqvist A, Hedlund J, Kalin M. Streptococcus pneumoniae: epidemiology, risk factors, and clinical features. Semin Respir Crit Care Med 2005, 26:563-574. 10.1055/s-2005-925523, 16388428.
4. Calbo E, Garau J. Of mice and men: innate immunity in pneumococcal pneumonia. Int J Antimicrob Agents 2010, 35:107-113. 10.1016/j.ijantimicag.2009.10.002, 20005681.
5. Knowles MR, Boucher RC. Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 2002, 109:571-577. 150901, 11877463.
6. Livraghi A, Randell SH. Cystic fibrosis and other respiratory diseases of impaired mucus clearance. Toxicol Pathol 2007, 35:116-129. 10.1080/01926230601060025, 17325980.
7. Randell SH, Boucher RC. Effective mucus clearance is essential for respiratory health. Am J Respir Cell Mol Biol 2006, 35:20-28. 10.1165/rcmb.2006-0082SF, 2658694, 16528010.
8. Afzelius BA. Cilia-related diseases. J Pathol 2004, 204:470-477. 10.1002/path.1652, 15495266.
9. Bush A, Chodhari R, Collins N, Copeland F, Hall P, Harcourt J, Hariri M, Hogg C, Lucas J, Mitchison HM, O'Callaghan C, Phillips G. Primary ciliary dyskinesia: current state of the art. Arch Dis Child 2007, 92:1136-1140. 10.1136/adc.2006.096958, 2066071, 17634184.
10. Ibanez-Tallon I, Heintz N, Omran H. To beat or not to beat: roles of cilia in development and disease. Hum Mol Genet 2003, 12(1):R27-R35.
11. Lee L. Mechanisms of mammalian ciliary motility: insights from primary ciliary dyskinesia genetics. Gene 2011, 473:57-66. 10.1016/j.gene.2010.11.006, 21111794.
12. Lee L. Riding the wave of ependymal cilia: genetic susceptibility to hydrocephalus in primary ciliary dyskinesia. J Neurosci Res 2013, 91:1117-1132. 10.1002/jnr.23238, 23686703.
13. 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. 10.1097/GIM.0b013e3181a53562, 3739704, 19606528.
14. Cowan MJ, Gladwin MT, Shelhamer JH. Disorders of ciliary motility. Am J Med Sci 2001, 321:3-10. 10.1097/00000441-200101000-00002, 11202477.
15. Ferkol T, Leigh M. Primary ciliary dyskinesia and newborn respiratory distress. Semin Perinatol 2006, 30:335-340. 10.1053/j.semperi.2005.11.001, 17142159.
16. Mall MA. Role of cilia, mucus, and airway surface liquid in mucociliary dysfunction: lessons from mouse models. J Aerosol Med Pulm Drug Deliv 2008, 21:13-24. 10.1089/jamp.2007.0659, 18518828.
17. Sagel SD, Davis SD, Campisi P, Dell SD. Update of respiratory tract disease in children with primary ciliary dyskinesia. Proc Am Thorac Soc 2011, 8:438-443. 10.1513/pats.201103-024SD, 3209579, 21926396.
18. Stannard W, O'Callaghan C. Ciliary function and the role of cilia in clearance. J Aerosol Med 2006, 19:110-115. 10.1089/jam.2006.19.110, 16551222.
19. Barlocco EG, Valletta EA, Canciani M, Lungarella G, Gardi C, De Santi MM, Mastella G. Ultrastructural ciliary defects in children with recurrent infections of the lower respiratory tract. Pediatr Pulmonol 1991, 10:11-17. 10.1002/ppul.1950100104, 2003040.
20. Ellerman A, Bisgaard H. Longitudinal study of lung function in a cohort of primary ciliary dyskinesia. Eur Respir J 1997, 10:2376-2379. 10.1183/09031936.97.10102376, 9387968.
21. Hellinckx J, Demedts M, De Boeck K. Primary ciliary dyskinesia: evolution of pulmonary function. Eur J Pediatr 1998, 157:422-426. 10.1007/s004310050843, 9625342.
22. Homma S, Kawabata M, Kishi K, Tsuboi E, Narui K, Nakatani T, Saiki S, Nakata K. Bronchiolitis in Kartagener's syndrome. Eur Respir J 1999, 14:1332-1339. 10.1183/09031936.99.14613329, 10624763.
23. Levison H, Mindorff CM, Chao J, Turner JA, Sturgess JM, Stringer DA. Pathophysiology of the ciliary motility syndromes. Eur J Respir Dis Suppl 1983, 127:102-117.
24. Magnin ML, Cros P, Beydon N, Mahloul M, Tamalet A, Escudier E, Clement A, Le Pointe HD, Blanchon S. Longitudinal lung function and structural changes in children with primary ciliary dyskinesia. Pediatr Pulmonol 2012, 47:816-825. 10.1002/ppul.22577, 22570319.
25. Montella S, Santamaria F, Salvatore M, Maglione M, Iacotucci P, De Santi MM, Mollica C. Lung disease assessment in primary ciliary dyskinesia: a comparison between chest high-field magnetic resonance imaging and high-resolution computed tomography findings. Ital J Pediatr 2009, 35:24. 10.1186/1824-7288-35-24, 2737542, 19660117.
26. Mossberg B, Camner P, Afzelius BA. The immotile-cilia syndrome compared to other obstructive lung diseases: a clue to their pathogenesis. Eur J Respir Dis Suppl 1983, 127:129-136.
27. 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. 10.1164/rccm.200303-365OC, 14656747.
28. Pedersen M, Stafanger G. Bronchopulmonary symptoms in primary ciliary dyskinesia. A clinical study of 27 patients. Eur J Respir Dis Suppl 1983, 127:118-128.
29. Pifferi M, Bush A, Pioggia G, Caramella D, Tartarisco G, Di Cicco M, Zangani M, Chinellato I, Maggi F, Tezza G, Macchia P, Boner A. Evaluation of pulmonary disease using static lung volumes in primary ciliary dyskinesia. Thorax 2012, 67:993-999. 10.1136/thoraxjnl-2011-200137, 22771515.
30. Santamaria F, Montella S, Tiddens HA, Guidi G, Casotti V, Maglione M, de Jong PA. Structural and functional lung disease in primary ciliary dyskinesia. Chest 2008, 134:351-357. 10.1378/chest.07-2812, 18403663.
31. Turner JA, Corkey CW, Lee JY, Levison H, Sturgess J. Clinical expressions of immotile cilia syndrome. Pediatrics 1981, 67:805-810.
32. Marthin JK, Petersen N, Skovgaard LT, Nielsen KG. Lung function in patients with primary ciliary dyskinesia: a cross-sectional and 3-decade longitudinal study. Am J Respir Crit Care Med 2010, 181:1262-1268. 10.1164/rccm.200811-1731OC, 20167855.
33. Bush A, Payne D, Pike S, Jenkins G, Henke MO, Rubin BK. Mucus properties in children with primary ciliary dyskinesia: comparison with cystic fibrosis. Chest 2006, 129:118-123. 10.1378/chest.129.1.118, 16424421.
34. Zhang Z, Sapiro R, Kapfhamer D, Bucan M, Bray J, Chennathukuzhi V, McNamara P, Curtis A, Zhang M, Blanchette-Mackie EJ, Strauss JF. A sperm-associated WD repeat protein orthologous to Chlamydomonas PF20 associates with Spag6, the mammalian orthologue of Chlamydomonas PF16. Mol Cell Biol 2002, 22:7993-8004. 10.1128/MCB.22.22.7993-8004.2002, 134734, 12391165.
35. Zhang Z, Tang W, Zhou R, Shen X, Wei Z, Patel AM, Povlishock JT, Bennett J, Strauss JF. Accelerated mortality from hydrocephalus and pneumonia in mice with a combined deficiency of SPAG6 and SPAG16L reveals a functional interrelationship between the two central apparatus proteins. Cell Motil Cytoskeleton 2007, 64:360-376. 10.1002/cm.20189, 17323374.
36. Sapiro R, Kostetskii I, Olds-Clarke P, Gerton GL, Radice GL, Strauss IJ. Male infertility, impaired sperm motility, and hydrocephalus in mice deficient in sperm-associated antigen 6. Mol Cell Biol 2002, 22:6298-6305. 10.1128/MCB.22.17.6298-6305.2002, 134010, 12167721.
37. Zhang Z, Kostetskii I, Tang W, Haig-Ladewig L, Sapiro R, Wei Z, Patel AM, Bennett J, Gerton GL, Moss SB, Radice GL, Strauss JF. Deficiency of SPAG16L causes male infertility associated with impaired sperm motility. Biol Reprod 2006, 74:751-759. 10.1095/biolreprod.105.049254, 16382026.
38. Teves ME, Zhang Z, Costanzo RM, Henderson SC, Corwin FD, Zweit J, Sundaresan G, Subler M, Salloum FN, Rubin BK, Strauss JF. Sperm-associated antigen-17 gene is essential for motile cilia function and neonatal survival. Am J Respir Cell Mol Biol 2013, 48:765-772. 10.1165/rcmb.2012-0362OC, 23418344.
39. Love D, Li FQ, Burke MC, Cyge B, Ohmitsu M, Cabello J, Larson JE, Brody SL, Cohen JC, Takemaru K. Altered lung morphogenesis, epithelial cell differentiation and mechanics in mice deficient in the Wnt/beta-catenin antagonist Chibby. PLoS One 2010, 5:e13600. 10.1371/journal.pone.0013600, 2963606, 21049041.
40. Voronina VA, Takemaru K, Treuting P, Love D, Grubb BR, Hajjar AM, Adams A, Li FQ, Moon RT. Inactivation of Chibby affects function of motile airway cilia. J Cell Biol 2009, 185:225-233. 10.1083/jcb.200809144, 2700371, 19364920.
41. Lee L, Campagna DR, Pinkus JL, Mulhern H, Wyatt TA, Sisson JH, Pavlik JA, Pinkus GS, Fleming MD. Primary ciliary dyskinesia in mice lacking the novel ciliary protein Pcdp1. Mol Cell Biol 2008, 28:949-957. 10.1128/MCB.00354-07, 2223405, 18039845.
42. Sironen A, Kotaja N, Mulhern H, Wyatt TA, Sisson JH, Pavlik JA, Miiluniemi M, Fleming MD, Lee L. Loss of SPEF2 function in mice results in spermatogenesis defects and primary ciliary dyskinesia. Biol Reprod 2011, 85:690-701. 10.1095/biolreprod.111.091132, 3184289, 21715716.
43. Martin TR, Frevert CW. Innate immunity in the lungs. Proc Am Thorac Soc 2005, 2:403-411. 10.1513/pats.200508-090JS, 2713330, 16322590.
44. Mitzner W, Fallica J, Bishai J. Anisotropic nature of mouse lung parenchyma. Ann Biomed Eng 2008, 36:2111-2120. 10.1007/s10439-008-9538-4, 18633711.
45. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012, 9:671-675. 10.1038/nmeth.2089, 22930834.
46. Sanchez CJ, Hinojosa CA, Shivshankar P, Hyams C, Camberlein E, Brown JS, Orihuela CJ. Changes in capsular serotype alter the surface exposure of pneumococcal adhesins and impact virulence. PLoS One 2011, 6:e26587. 10.1371/journal.pone.0026587, 3197518, 22028914.
47. DiPetrillo CG, Smith EF. Pcdp1 is a central apparatus protein that binds Ca(2+)-calmodulin and regulates ciliary motility. J Cell Biol 2010, 189:601-612. 10.1083/jcb.200912009, 2867295, 20421426.
48. Sironen A, Hansen J, Thomsen B, Andersson M, Vilkki J, Toppari J, Kotaja N. Expression of SPEF2 during mouse spermatogenesis and identification of IFT20 as an interacting protein. Biol Reprod 2010, 82:580-590. 10.1095/biolreprod.108.074971, 19889948.
49. Zhang H, Mitchell DR. Cpc1, a Chlamydomonas central pair protein with an adenylate kinase domain. J Cell Sci 2004, 117:4179-4188. 10.1242/jcs.01297, 1525021, 15292403.
50. Gillespie SH, Balakrishnan I. Pathogenesis of pneumococcal infection. J Med Microbiol 2000, 49:1057-1067.
51. Kadioglu A, Gingles NA, Grattan K, Kerr A, Mitchell TJ, Andrew PW. Host cellular immune response to pneumococcal lung infection in mice. Infect Immun 2000, 68:492-501. 10.1128/IAI.68.2.492-501.2000, 97168, 10639409.
52. Monton C, Torres A, El-Ebiary M, Filella X, Xaubet A, de la Bellacasa JP. Cytokine expression in severe pneumonia: a bronchoalveolar lavage study. Crit Care Med 1999, 27:1745-1753. 10.1097/00003246-199909000-00008, 10507593.
53. Rincon M, Irvin CG. Role of IL-6 in asthma and other inflammatory pulmonary diseases. Int J Biol Sci 2012, 8:1281-1290. 3491451, 23136556.
54. van der Poll T, Keogh CV, Guirao X, Buurman WA, Kopf M, Lowry SF. Interleukin-6 gene-deficient mice show impaired defense against pneumococcal pneumonia. J Infect Dis 1997, 176:439-444. 10.1086/514062, 9237710.
55. Chu WM. Tumor necrosis factor. Cancer Lett 2013, 328:222-225. 10.1016/j.canlet.2012.10.014, 23085193.
56. Liao W, Lin JX, Leonard WJ. Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. Immunity 2013, 38:13-25. 10.1016/j.immuni.2013.01.004, 23352221.
57. Martin JG, Suzuki M, Ramos-Barbon D, Isogai S. T cell cytokines: animal models. Paediatr Respir Rev 2004, 5(A):S47-S51.
58. Nembrini C, Marsland BJ, Kopf M. IL-17-producing T cells in lung immunity and inflammation. J Allergy Clin Immunol 2009, 123:986-994. Quiz 995-996, 10.1016/j.jaci.2009.03.033, 19410688.
59. Reynolds JM, Angkasekwinai P, Dong C. IL-17 family member cytokines: regulation and function in innate immunity. Cytokine Growth Factor Rev 2010, 21:413-423. 10.1016/j.cytogfr.2010.10.002, 3008409, 21074482.
60. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, Shellito JE, Bagby GJ, Nelson S, Charrier K, Peschon JJ, Kolls JK. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001, 194:519-527. 10.1084/jem.194.4.519, 2193502, 11514607.
61. Fujio K, Okamura T, Yamamoto K. The family of IL-10-secreting CD4+ T cells. Adv Immunol 2010, 105:99-130.
62. Moore KW, de Waal MR, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001, 19:683-765. 10.1146/annurev.immunol.19.1.683, 11244051.
63. Urry Z, Xystrakis E, Hawrylowicz CM. Interleukin-10-secreting regulatory T cells in allergy and asthma. Curr Allergy Asthma Rep 2006, 6:363-371. 10.1007/s11882-996-0005-8, 16899197.
64. van der Poll T, Marchant A, Keogh CV, Goldman M, Lowry SF. Interleukin-10 impairs host defense in murine pneumococcal pneumonia. J Infect Dis 1996, 174:994-1000. 10.1093/infdis/174.5.994, 8896500.