Mutation of CFAP57, a protein required for the asymmetric targeting of a subset of inner dynein arms in Chlamydomonas, causes primary ciliary dyskinesia


Autoři: Ximena M. Bustamante-Marin aff001;  Amjad Horani aff002;  Mihaela Stoyanova aff003;  Wu-Lin Charng aff003;  Mathieu Bottier aff005;  Patrick R. Sears aff001;  Wei-Ning Yin aff001;  Leigh Anne Daniels aff001;  Hailey Bowen aff002;  Donald F. Conrad aff003;  Michael R. Knowles aff001;  Lawrence E. Ostrowski aff001;  Maimoona A. Zariwala aff008;  Susan K. Dutcher aff003
Působiště autorů: Department of Medicine, Marsico Lung Institute, University of North Carolina, Chapel Hill, North Carolina, United States of America aff001;  Department of Pediatrics, Washington University School of Medicine, St. Louis, Missouri, United States of America aff002;  Department of Genetics, Washington University School of Medicine, St. Louis, Missouri, United States of America aff003;  Department of Neurology, Washington University School of Medicine, St. Louis, Missouri, United States of America aff004;  Department of Mechanical Engineering, Washington University, St. Louis, Missouri, United States of America aff005;  Division of Genetics, Oregon National Primate Research Center, Oregon Health & Science University, Beaverton, Oregon, United States of America aff006;  Department of Molecular and Medical Genetics, Oregon Health & Science University, Portland, Oregon, United States of America aff007;  Department of Pathology and Laboratory Medicine and the Marsico Lung Institute, University of North Carolina, Chapel Hill, North Carolina, United States of America aff008
Vyšlo v časopise: Mutation of CFAP57, a protein required for the asymmetric targeting of a subset of inner dynein arms in Chlamydomonas, causes primary ciliary dyskinesia. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008691
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008691

Souhrn

Primary ciliary dyskinesia (PCD) is characterized by chronic airway disease, reduced fertility, and randomization of the left/right body axis. It is caused by defects of motile cilia and sperm flagella. We screened a cohort of affected individuals that lack an obvious axonemal defect for pathogenic variants using whole exome capture, next generation sequencing, and bioinformatic analysis assuming an autosomal recessive trait. We identified one subject with an apparently homozygous nonsense variant [(c.1762C>T), p.(Arg588*)] in the uncharacterized CFAP57 gene. Interestingly, the variant results in the skipping of exon 11 (58 amino acids), which may be due to disruption of an exonic splicing enhancer. In normal human nasal epithelial cells, CFAP57 localizes throughout the ciliary axoneme. Nasal cells from the PCD patient express a shorter, mutant version of CFAP57 and the protein is not incorporated into the axoneme. The missing 58 amino acids include portions of WD repeats that may be important for loading onto the intraflagellar transport (IFT) complexes for transport or docking onto the axoneme. A reduced beat frequency and an alteration in ciliary waveform was observed. Knockdown of CFAP57 in human tracheobronchial epithelial cells (hTECs) recapitulates these findings. Phylogenetic analysis showed that CFAP57 is highly conserved in organisms that assemble motile cilia. CFAP57 is allelic with the BOP2/IDA8/FAP57 gene identified previously in Chlamydomonas reinhardtii. Two independent, insertional fap57 Chlamydomonas mutant strains show reduced swimming velocity and altered waveforms. Tandem mass tag (TMT) mass spectroscopy shows that FAP57 is missing, and the “g” inner dyneins (DHC7 and DHC3) and the “d” inner dynein (DHC2) are reduced, but the FAP57 paralog FBB7 is increased. Together, our data identify a homozygous variant in CFAP57 that causes PCD that is likely due to a defect in the inner dynein arm assembly process.

Klíčová slova:

Cilia – Dyneins – Epithelial cells – Homozygosity – Human genetics – Motor proteins – Pathogen motility – Swimming


Zdroje

1. Ferkol TW, Leigh MW. Ciliopathies: the central role of cilia in a spectrum of pediatric disorders. The Journal of pediatrics. 2012;160(3):366–71. doi: 10.1016/j.jpeds.2011.11.024 22177992

2. Horani A, Ferkol TW, Dutcher SK, Brody SL. Genetics and biology of primary ciliary dyskinesia. Paediatr Respir Rev. 2016;18:18–24. Epub 2015/10/20. doi: 10.1016/j.prrv.2015.09.001 26476603

3. Olcese C, Patel MP, Shoemark A, Kiviluoto S, Legendre M, Williams HJ, et al. X-linked primary ciliary dyskinesia due to mutations in the cytoplasmic axonemal dynein assembly factor PIH1D3. Nature communications. 2017;8:14279. Epub 2017/02/09. doi: 10.1038/ncomms14279 28176794

4. Wallmeier J, Frank D, Shoemark A, Nothe-Menchen T, Cindric S, Olbrich H, et al. De Novo Mutations in FOXJ1 Result in a Motile Ciliopathy with Hydrocephalus and Randomization of Left/Right Body Asymmetry. American journal of human genetics. 2019;105(5):1030–9. Epub 2019/10/22. doi: 10.1016/j.ajhg.2019.09.022 31630787

5. Zariwala MA, Knowles MR, Leigh MW. Primary Ciliary Dyskinesia. Adam M, Ardinger H, Pagon R, Wallace S, Bean L, Stephen K, et al., editors. Seattle,Washington University of ezWashington 2020.

6. Shapiro AJ, Zariwala MA, Ferkol T, Davis SD, Sagel SD, Dell SD, et al. Diagnosis, monitoring, and treatment of primary ciliary dyskinesia: PCD foundation consensus recommendations based on state of the art review. Pediatr Pulmonol. 2016;51(2):115–32. Epub 2015/09/30. doi: 10.1002/ppul.23304 26418604.

7. Schwabe GC, Hoffmann K, Loges NT, Birker D, Rossier C, de Santi MM, et al. Primary ciliary dyskinesia associated with normal axoneme ultrastructure is caused by DNAH11 mutations. Human mutation. 2008;29(2):289–98. doi: 10.1002/humu.20656 18022865.

8. Knowles MR, Leigh MW, Carson JL, Davis SD, Dell SD, Ferkol TW, et al. Mutations of DNAH11 in patients with primary ciliary dyskinesia with normal ciliary ultrastructure. Thorax. 2012;67(5):433–41. doi: 10.1136/thoraxjnl-2011-200301 22184204.

9. Knowles MR, Leigh MW, Ostrowski LE, Huang L, Carson JL, Hazucha MJ, et al. Exome sequencing identifies mutations in CCDC114 as a cause of primary ciliary dyskinesia. American journal of human genetics. 2013;92(1):99–106. Epub 2012/12/25. doi: 10.1016/j.ajhg.2012.11.003 23261302

10. Hjeij R, Onoufriadis A, Watson CM, Slagle CE, Klena NT, Dougherty GW, et al. CCDC151 mutations cause primary ciliary dyskinesia by disruption of the outer dynein arm docking complex formation. American journal of human genetics. 2014;95(3):257–74. Epub 2014/09/06. doi: 10.1016/j.ajhg.2014.08.005 25192045

11. Alsaadi MM, Erzurumluoglu AM, Rodriguez S, Guthrie PA, Gaunt TR, Omar HZ, et al. Nonsense mutation in coiled-coil domain containing 151 gene (CCDC151) causes primary ciliary dyskinesia. Human mutation. 2014;35(12):1446–8. Epub 2014/09/17. doi: 10.1002/humu.22698 25224326

12. Hjeij R, Lindstrand A, Francis R, Zariwala MA, Liu X, Li Y, et al. ARMC4 mutations cause primary ciliary dyskinesia with randomization of left/right body asymmetry. American journal of human genetics. 2013;93(2):357–67. Epub 2013/07/16. doi: 10.1016/j.ajhg.2013.06.009 23849778

13. Onoufriadis A, Shoemark A, Schmidts M, Patel M, Jimenez G, Liu H, et al. Targeted NGS gene panel identifies mutations in RSPH1 causing primary ciliary dyskinesia and a common mechanism for ciliary central-pair agenesis due to radial spoke defects. Human molecular genetics. 2014. Epub 2014/02/13. doi: 10.1093/hmg/ddu046 24518672.

14. Wallmeier J, Shiratori H, Dougherty GW, Edelbusch C, Hjeij R, Loges NT, et al. TTC25 Deficiency Results in Defects of the Outer Dynein Arm Docking Machinery and Primary Ciliary Dyskinesia with Left-Right Body Asymmetry Randomization. American journal of human genetics. 2016;99(2):460–9. Epub 2016/08/04. doi: 10.1016/j.ajhg.2016.06.014 27486780

15. Mitchison HM, Schmidts M, Loges NT, Freshour J, Dritsoula A, Hirst RA, et al. Mutations in axonemal dynein assembly factor DNAAF3 cause primary ciliary dyskinesia. Nature genetics. 2012;44(4):381–9, S1–2. doi: 10.1038/ng.1106 22387996

16. Panizzi JR, Becker-Heck A, Castleman VH, Al-Mutairi DA, Liu Y, Loges NT, et al. CCDC103 mutations cause primary ciliary dyskinesia by disrupting assembly of ciliary dynein arms. Nature genetics. 2012;44(6):714–9. doi: 10.1038/ng.2277 22581229

17. Tarkar A, Loges NT, Slagle CE, Francis R, Dougherty GW, Tamayo JV, et al. DYX1C1 is required for axonemal dynein assembly and ciliary motility. Nature genetics. 2013;45(9):995–1003. doi: 10.1038/ng.2707 23872636

18. Horani A, Druley TE, Zariwala MA, Patel AC, Levinson BT, Van Arendonk LG, et al. Whole-Exome Capture and Sequencing Identifies HEATR2 Mutation as a Cause of Primary Ciliary Dyskinesia. American journal of human genetics. 2012;91(4):685–93. doi: 10.1016/j.ajhg.2012.08.022 23040496.

19. Horani A, Ferkol TW, Shoseyov D, Wasserman MG, Oren YS, Kerem B, et al. LRRC6 mutation causes primary ciliary dyskinesia with dynein arm defects. PloS one. 2013;8(3):e59436. doi: 10.1371/journal.pone.0059436 23527195

20. Horani A, Ustione A, Huang T, Firth AL, Pan J, Gunsten SP, et al. Establishment of the early cilia preassembly protein complex during motile ciliogenesis. Proceedings of the National Academy of Sciences of the United States of America. 2018;115(6):E1221–E8. Epub 2018/01/24. doi: 10.1073/pnas.1715915115 29358401

21. Knowles Michael R, Ostrowski Lawrence E, Loges Niki T, Hurd T, Leigh Margaret W, Huang L, et al. Mutations in SPAG1 Cause Primary Ciliary Dyskinesia Associated with Defective Outer and Inner Dynein Arms. American journal of human genetics. 2013;93(4):711–20. doi: 10.1016/j.ajhg.2013.07.025 24055112

22. Moore DJ, Onoufriadis A, Shoemark A, Simpson MA, zur Lage PI, de Castro SC, 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. American journal of human genetics. 2013;93(2):346–56. Epub 2013/07/31. doi: 10.1016/j.ajhg.2013.07.009 23891471

23. Kott E, Duquesnoy P, Copin B, Legendre M, Dastot-Le Moal F, Montantin G, 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. American journal of human genetics. 2012;91(5):958–64. doi: 10.1016/j.ajhg.2012.10.003 23122589

24. Paff T, Loges NT, Aprea I, Wu K, Bakey Z, Haarman EG, et al. Mutations in PIH1D3 Cause X-Linked Primary Ciliary Dyskinesia with Outer and Inner Dynein Arm Defects. American journal of human genetics. 2017;100(1):160–8. Epub 2017/01/04. doi: 10.1016/j.ajhg.2016.11.019 28041644

25. Wallmeier J, Al-Mutairi DA, Chen CT, Loges NT, Pennekamp P, Menchen T, et al. Mutations in CCNO result in congenital mucociliary clearance disorder with reduced generation of multiple motile cilia. Nature genetics. 2014;46(6):646–51. Epub 2014/04/22. doi: 10.1038/ng.2961 24747639.

26. Boon M, Wallmeier J, Ma L, Loges NT, Jaspers M, Olbrich H, et al. MCIDAS mutations result in a mucociliary clearance disorder with reduced generation of multiple motile cilia. Nature communications. 2014;5:4418. doi: 10.1038/ncomms5418 25048963.

27. Zariwala MA, Knowles MR, Leigh MW. Primary Ciliary Dyskinesia. In: Pagon RA, Adam MP, Ardinger HH, Wallace SE, Amemiya A, Bean LJH, et al., editors. GeneReviews(R) [Internet]. Seattle (WA): University of Washington, Seattle 1993–2016. http://www.ncbi.nlm.nih.gov/books/NBK1122/; 2007 [Updated 2015].

28. Olbrich H, Cremers C, Loges NT, Werner C, Nielsen KG, Marthin JK, et al. Loss-of-Function GAS8 Mutations Cause Primary Ciliary Dyskinesia and Disrupt the Nexin-Dynein Regulatory Complex. American journal of human genetics. 2015;97(4):546–54. Epub 2015/09/22. doi: 10.1016/j.ajhg.2015.08.012 26387594.

29. Edelbusch C, Cindric S, Dougherty GW, Loges NT, Olbrich H, Rivlin J, et al. Mutation of serine/threonine protein kinase 36 (STK36) causes primary ciliary dyskinesia with a central pair defect. Human mutation. 2017;38(8):964–9. Epub 2017/05/26. doi: 10.1002/humu.23261 28543983.

30. Wallmeier J, Shiratori H, Dougherty Gerard W, Edelbusch C, Hjeij R, Loges Niki T, et al. TTC25 Deficiency Results in Defects of the Outer Dynein Arm Docking Machinery and Primary Ciliary Dyskinesia with Left-Right Body Asymmetry Randomization. The American Journal of Human Genetics. 2016;99(2):460–9. https://doi.org/10.1016/j.ajhg.2016.06.014 27486780

31. Olcese C, Patel MP, Shoemark A, Kiviluoto S, Legendre M, Williams HJ, et al. X-linked primary ciliary dyskinesia due to mutations in the cytoplasmic axonemal dynein assembly factor PIH1D3. 2017;8:14279. https://www.nature.com/articles/ncomms14279#supplementary-information.

32. Paff T, Loges NT, Aprea I, Wu K, Bakey Z, Haarman EG, et al. Mutations in PIH1D3 Cause X-Linked Primary Ciliary Dyskinesia with Outer and Inner Dynein Arm Defects. The American Journal of Human Genetics. 2017;100(1):160–8. https://doi.org/10.1016/j.ajhg.2016.11.019 28041644

33. Bustamante-Marin XM, Yin W-N, Sears PR, Werner ME, Brotslaw EJ, Mitchell BJ, et al. Lack of GAS2L2 Causes PCD by Impairing Cilia Orientation and Mucociliary Clearance. The American Journal of Human Genetics. 2019. https://doi.org/10.1016/j.ajhg.2018.12.009.

34. El Khouri E, Thomas L, Jeanson L, Bequignon E, Vallette B, Duquesnoy P, et al. Mutations in DNAJB13, Encoding an HSP40 Family Member, Cause Primary Ciliary Dyskinesia and Male Infertility. The American Journal of Human Genetics. 2016;99(2):489–500. https://doi.org/10.1016/j.ajhg.2016.06.022 27486783

35. Merveille AC, Davis EE, Becker-Heck A, Legendre M, Amirav I, Bataille G, 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. Nature genetics. 2011;43(1):72–8. doi: 10.1038/ng.726 21131972.

36. Becker-Heck A, Zohn IE, Okabe N, Pollock A, Lenhart KB, Sullivan-Brown J, et al. The coiled-coil domain containing protein CCDC40 is essential for motile cilia function and left-right axis formation. Nature genetics. 2011;43(1):79–84. doi: 10.1038/ng.727 21131974

37. Cindric S, Dougherty GW, Olbrich H, Hjeij R, Loges NT, Amirav I, et al. SPEF2- and HYDIN-mutant Cilia Lack the Central Pair Associated Protein SPEF2 Aiding PCD Diagnostics. Am J Respir Cell Mol Biol. 2019. Epub 2019/09/24. doi: 10.1165/rcmb.2019-0086OC 31545650.

38. Omran H, Kobayashi D, Olbrich H, Tsukahara T, Loges NT, Hagiwara H, et al. Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins. Nature. 2008;456(7222):611–6. doi: 10.1038/nature07471 19052621

39. Wirschell M, Olbrich H, Werner C, Tritschler D, Bower R, Sale WS, et al. The nexin-dynein regulatory complex subunit DRC1 is essential for motile cilia function in algae and humans. Nature genetics. 2013;45(3):262–8. doi: 10.1038/ng.2533 23354437.

40. Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, May-Simera H, et al. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell. 2004;117(4):541–52. doi: 10.1016/s0092-8674(04)00450-7 15137946.

41. Silflow CD, Lefebvre PA. Assembly and motility of eukaryotic cilia and flagella. Lessons from Chlamydomonas reinhardtii. Plant Physiol. 2001;127(4):1500–7. 11743094.

42. Patel-King RS, Sakato-Antoku M, Yankova M, King SM. WDR92 is required for axonemal dynein heavy chain stability in cytoplasm. Mol Biol Cell. 2019;30(15):1834–45. Epub 2019/05/23. doi: 10.1091/mbc.E19-03-0139 31116681

43. Pazour GJ, Agrin N, Leszyk J, Witman GB. Proteomic analysis of a eukaryotic cilium. The Journal of cell biology. 2005;170(1):103–13. Epub 2005/07/07. doi: 10.1083/jcb.200504008 15998802.

44. Piperno G, Ramanis Z, Smith EF, Sale WS. Three distinct inner dynein arms in Chlamydomonas flagella: molecular composition and location in the axoneme. The Journal of cell biology. 1990;110(2):379–89. doi: 10.1083/jcb.110.2.379 2137128.

45. Kagami O, Kamiya R. Separation of dynein species by high-pressure liquid chromatography. Methods Cell Biol. 1995;47:487–9. doi: 10.1016/s0091-679x(08)60849-3 7476533.

46. Kamiya R. Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants. Int Rev Cytol. 2002;219:115–55. doi: 10.1016/s0074-7696(02)19012-7 12211628.

47. Bui KH, Yagi T, Yamamoto R, Kamiya R, Ishikawa T. Polarity and asymmetry in the arrangement of dynein and related structures in the Chlamydomonas axoneme. The Journal of cell biology. 2012;198(5):913–25. doi: 10.1083/jcb.201201120 22945936

48. Heuser T, Barber CF, Lin J, Krell J, Rebesco M, Porter ME, et al. Cryoelectron tomography reveals doublet-specific structures and unique interactions in the I1 dynein. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(30):E2067–76. doi: 10.1073/pnas.1120690109 22733763

49. Yagi T, Uematsu K, Liu Z, Kamiya R. Identification of dyneins that localize exclusively to the proximal portion of Chlamydomonas flagella. Journal of cell science. 2009;122(Pt 9):1306–14. doi: 10.1242/jcs.045096 19351714.

50. Dutcher SK, Gibbons W, Inwood WB. A genetic analysis of suppressors of the PF10 mutation in Chlamydomonas reinhardtii. Genetics. 1988;120(4):965–76. 3224813.

51. King SJ, Inwood WB, O’Toole ET, Power J, Dutcher SK. The bop2-1 mutation reveals radial asymmetry in the inner dynein arm region of Chlamydomonas reinhardtii. The Journal of cell biology. 1994;126(5):1255–66. doi: 10.1083/jcb.126.5.1255 8063862.

52. Lin J, Le TV, Augspurger K, Tritschler D, Bower R, Fu G, et al. FAP57/WDR65 targets assembly of a subset of inner arm dyneins and connects to regulatory hubs in cilia. Mol Biol Cell. 2019;30(21):2659–80. Epub 2019/09/05. doi: 10.1091/mbc.E19-07-0367 31483737

53. Antony D, Becker-Heck A, Zariwala MA, Schmidts M, Onoufriadis A, Forouhan M, et al. Mutations in CCDC39 and CCDC40 are the major cause of primary ciliary dyskinesia with axonemal disorganization and absent inner dynein arms. Human mutation. 2013;34(3):462–72. Epub 2012/12/21. doi: 10.1002/humu.22261 23255504

54. Wilfert AB, Chao KR, Kaushal M, Jain S, Zollner S, Adams DR, et al. Genome-wide significance testing of variation from single case exomes. Nature genetics. 2016;48(12):1455–61. Epub 2016/11/01. doi: 10.1038/ng.3697 27776118

55. Leigh MW, Hazucha MJ, Chawla KK, Baker BR, Shapiro AJ, Brown DE, et al. Standardizing Nasal Nitric Oxide Measurement as a Test for Primary Ciliary Dyskinesia. Annals of the American Thoracic Society. 2013;10(6):574–81. doi: 10.1513/AnnalsATS.201305-110OC 24024753.

56. Griffith M, Miller CA, Griffith OL, Krysiak K, Skidmore ZL, Ramu A, et al. Optimizing cancer genome sequencing and analysis. Cell Syst. 2015;1(3):210–23. Epub 2015/12/09. doi: 10.1016/j.cels.2015.08.015 26645048

57. Fulcher ML, Randell SH. Human nasal and tracheo-bronchial respiratory epithelial cell culture. Methods Mol Biol. 2013;945:109–21. Epub 2012/10/26. doi: 10.1007/978-1-62703-125-7_8 23097104.

58. Blackburn K, Bustamante-Marin X, Yin W, Goshe MB, Ostrowski LE. Quantitative Proteomic Analysis of Human Airway Cilia Identifies Previously Uncharacterized Proteins of High Abundance. J Proteome Res. 2017;16(4):1579–92. Epub 2017/03/11. doi: 10.1021/acs.jproteome.6b00972 28282151

59. Gentzsch M, Boyles SE, Cheluvaraju C, Chaudhry IG, Quinney NL, Cho C, et al. Pharmacological Rescue of Conditionally Reprogrammed Cystic Fibrosis Bronchial Epithelial Cells. American journal of respiratory cell and molecular biology. 2017;56(5):568–74. doi: 10.1165/rcmb.2016-0276MA 27983869.

60. Anna A, Monika G. Splicing mutations in human genetic disorders: examples, detection, and confirmation. Journal of applied genetics. 2018;59(3):253–68. Epub 04/21. doi: 10.1007/s13353-018-0444-7 29680930.

61. Knowles MR, Ostrowski LE, Leigh MW, Sears PR, Davis SD, Wolf WE, et al. Mutations in RSPH1 Cause Primary Ciliary Dyskinesia with a Unique Clinical and Ciliary Phenotype. American journal of respiratory and critical care medicine. 2014;189(6):707–17. doi: 10.1164/rccm.201311-2047OC 24568568

62. Feng Y, Nie L, Thakur MD, Su Q, Chi Z, Zhao Y, et al. A multifunctional lentiviral-based gene knockdown with concurrent rescue that controls for off-target effects of RNAi. Genomics Proteomics Bioinformatics. 8(4):238–45. doi: 10.1016/S1672-0229(10)60025-3 21382592.

63. Horani A, Nath A, Wasserman MG, Huang T, Brody SL. Rho-associated protein kinase inhibition enhances airway epithelial Basal-cell proliferation and lentivirus transduction. Am J Respir Cell Mol Biol. 2013;49(3):341–7. Epub 2013/05/30. doi: 10.1165/rcmb.2013-0046TE 23713995

64. Horani A, Druley TE, Zariwala MA, Patel AC, Levinson BT, Van Arendonk LG, et al. Whole-Exome Capture and Sequencing Identifies HEATR2 Mutation as a Cause of Primary Ciliary Dyskinesia. American journal of human genetics. 2012;91(4):685–93. doi: 10.1016/j.ajhg.2012.08.022 23040496

65. Wickstead B, Gull K. Dyneins across eukaryotes: a comparative genomic analysis. Traffic. 2007;8(12):1708–21. Epub 2007/09/28. doi: 10.1111/j.1600-0854.2007.00646.x 17897317

66. Yachdav G, Kloppmann E, Kajan L, Hecht M, Goldberg T, Hamp T, et al. PredictProtein—an open resource for online prediction of protein structural and functional features. Nucleic acids research. 2014;42(Web Server issue):W337–43. Epub 2014/05/07. doi: 10.1093/nar/gku366 24799431

67. Dutcher SK. Chlamydomonas reinhardtii: biological rationale for genomics. The Journal of eukaryotic microbiology. 2000;47(4):340–9. doi: 10.1111/j.1550-7408.2000.tb00059.x 11140447.

68. Li X, Zhang R, Patena W, Gang SS, Blum SR, Ivanova N, et al. An Indexed, Mapped Mutant Library Enables Reverse Genetics Studies of Biological Processes in Chlamydomonas reinhardtii. The Plant cell. 2016;28(2):367–87. Epub 2016/01/15. doi: 10.1105/tpc.15.00465 26764374

69. Zhang R, Patena W, Armbruster U, Gang SS, Blum SR, Jonikas MC. High-Throughput Genotyping of Green Algal Mutants Reveals Random Distribution of Mutagenic Insertion Sites and Endonucleolytic Cleavage of Transforming DNA. The Plant cell. 2014;26 (4):1398–409. doi: 10.1105/tpc.114.124099 24706510.

70. Bayly PV, Lewis BL, Kemp PS, Pless RB, Dutcher SK. Efficient spatiotemporal analysis of the flagellar waveform of Chlamydomonas reinhardtii. Cytoskeleton. 2010;67(1):56–69. doi: 10.1002/cm.20424 20169530

71. Bottier M, Thomas KA, Dutcher SK, Bayly PV. How Does Cilium Length Affect Beating? Biophysical Journal. 2019;116(7):1292–304. https://doi.org/10.1016/j.bpj.2019.02.012 30878201

72. Lin H, Guo S, Dutcher SK. RPGRIP1L helps to establish the ciliary gate for entry of proteins. Journal of cell science. 2018;131(20): jcs220905. Epub 2018/09/22. doi: 10.1242/jcs.220905 30237221

73. Bower R, Tritschler D, Vanderwaal K, Perrone CA, Mueller J, Fox L, et al. The N-DRC forms a conserved biochemical complex that maintains outer doublet alignment and limits microtubule sliding in motile axonemes. Mol Biol Cell. 2013;24(8):1134–52. doi: 10.1091/mbc.E12-11-0801 23427265

74. Awata J, Takada S, Standley C, Lechtreck KF, Bellve KD, Pazour GJ, et al. NPHP4 controls ciliary trafficking of membrane proteins and large soluble proteins at the transition zone. Journal of cell science. 2014;127(Pt 21):4714–27. doi: 10.1242/jcs.155275 25150219

75. Consortium GT. Human genomics. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science. 2015;348(6235):648–60. Epub 2015/05/09. doi: 10.1126/science.1262110 25954001

76. Kasak L, Punab M, Nagirnaja L, Grigorova M, Minajeva A, Lopes AM, et al. Bi-allelic Recessive Loss-of-Function Variants in FANCM Cause Non-obstructive Azoospermia. Am J Hum Genet. 2018;103(2):200–12. Epub 2018/08/04. doi: 10.1016/j.ajhg.2018.07.005 30075111

77. Lechtreck KF. IFT-Cargo Interactions and Protein Transport in Cilia. Trends Biochem Sci. 2015;40(12):765–78. Epub 2015/10/27. doi: 10.1016/j.tibs.2015.09.003 26498262

78. Bhogaraju S, Cajanek L, Fort C, Blisnick T, Weber K, Taschner M, et al. Molecular basis of tubulin transport within the cilium by IFT74 and IFT81. Science. 2013;341(6149):1009–12. doi: 10.1126/science.1240985 23990561.

79. Ahmed NT, Mitchell DR. ODA16p, a Chlamydomonas flagellar protein needed for dynein assembly. Mol Biol Cell. 2005;16(10):5004–12. doi: 10.1091/mbc.e05-07-0627 16093345.

80. Gao C, Wang G, Amack JD, Mitchell DR. Oda16/Wdr69 is essential for axonemal dynein assembly and ciliary motility during zebrafish embryogenesis. Developmental dynamics: an official publication of the American Association of Anatomists. 2010;239(8):2190–7. doi: 10.1002/dvdy.22355 20568242

81. Ahmed NT, Gao C, Lucker BF, Cole DG, Mitchell DR. ODA16 aids axonemal outer row dynein assembly through an interaction with the intraflagellar transport machinery. The Journal of cell biology. 2008;183(2):313–22. Epub 2008/10/15. doi: 10.1083/jcb.200802025 18852297.

82. Hunter EL, Lechtreck K, Fu G, Hwang J, Lin H, Gokhale A, et al. The IDA3 adapter, required for intraflagellar transport of I1 dynein, is regulated by ciliary length. Mol Biol Cell. 2018;29(8):886–96. Epub 2018/02/23. doi: 10.1091/mbc.E17-12-0729 29467251

83. Yanagisawa HA, Kamiya R. Association between actin and light chains in Chlamydomonas flagellar inner-arm dyneins. Biochemical and biophysical research communications. 2001;288(2):443–7. doi: 10.1006/bbrc.2001.5776 11606062.

84. Oltean A, Schaffer AJ, Bayly PV, Brody SL. Quantifying Ciliary Dynamics during Assembly Reveals Stepwise Waveform Maturation in Airway Cells. American journal of respiratory cell and molecular biology. 2018;59(4):511–22. Epub 2018/06/01. doi: 10.1165/rcmb.2017-0436OC 29851510

85. Dutcher SK. Asymmetries in the cilia of Chlamydomonas Philos Trans R Soc Lond B Biol Sci. 2019.

86. Dinkel H, Michael S, Weatheritt RJ, Davey NE, Van Roey K, Altenberg B, et al. ELM—the database of eukaryotic linear motifs. Nucleic acids research. 2012;40(Database issue):D242–51. doi: 10.1093/nar/gkr1064 22110040

87. Lin J, Nicastro D. Asymmetric distribution and spatial switching of dynein activity generates ciliary motility. Science. 2018;360(6387). Epub 2018/04/28. doi: 10.1126/science.aar1968 29700238.

88. Oda T, Yanagisawa H, Kamiya R, Kikkawa M. A molecular ruler determines the repeat length in eukaryotic cilia and flagella. Science. 2014;346(6211):857–60. Epub 2014/11/15. doi: 10.1126/science.1260214 25395538.

89. Lin H, Zhang Z, Guo S, Chen F, Kessler JM, Wang YM, et al. A NIMA-Related Kinase Suppresses the Flagellar Instability Associated with the Loss of Multiple Axonemal Structures. PLoS Genet. 2015;11(9):e1005508. doi: 10.1371/journal.pgen.1005508 26348919

90. Fu G, Wang Q, Phan N, Urbanska P, Joachimiak E, Lin J, et al. The I1 dynein-associated tether and tether head complex is a conserved regulator of ciliary motility. Mol Biol Cell. 2018;29(9):1048–59. Epub 2018/03/09. doi: 10.1091/mbc.E18-02-0142 29514928

91. Kubo T, Hou Y, Cochran DA, Witman GB, Oda T. A microtubule-dynein tethering complex regulates the axonemal inner dynein f (I1). Mol Biol Cell. 2018;29(9):1060–74. Epub 2018/03/16. doi: 10.1091/mbc.E17-11-0689 29540525

92. Urbanska P, Joachimiak E, Bazan R, Fu G, Poprzeczko M, Fabczak H, et al. Ciliary proteins Fap43 and Fap44 interact with each other and are essential for proper cilia and flagella beating. Cellular and molecular life sciences: CMLS. 2018;75(24):4479–93. Epub 2018/04/25. doi: 10.1007/s00018-018-2819-7 29687140.

93. Muller L, Brighton LE, Carson JL, Fischer WA 2nd, Jaspers I. Culturing of human nasal epithelial cells at the air liquid interface. J Vis Exp. 2013;(80). doi: 10.3791/50646 24145828

94. Lin H, Kwan AL, Dutcher SK. Synthesizing and salvaging NAD: lessons learned from Chlamydomonas reinhardtii. PLoS Genet. 2010;6(9):e1001105. Epub 2010/09/15. doi: 10.1371/journal.pgen.1001105 20838591

95. Pan J, You Y, Huang T, Brody SL. RhoA-mediated apical actin enrichment is required for ciliogenesis and promoted by Foxj1. Journal of cell science. 2007;120(Pt 11):1868–76. doi: 10.1242/jcs.005306 17488776.

96. You Y, Richer EJ, Huang T, Brody SL. Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am J Physiol Lung Cell Mol Physiol. 2002;283(6):L1315–21. Epub 2002/10/22. doi: 10.1152/ajplung.00169.2002 12388377.

97. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nature methods. 2012;9:676. https://www.nature.com/articles/nmeth.2019#supplementary-information 22743772

98. Onishi M, Pringle JR. Robust Transgene Expression from Bicistronic mRNA in the Green Alga Chlamydomonas reinhardtii. G3: Genes|Genomes|Genetics. 2016;6(12):4115–25. doi: 10.1534/g3.116.033035 27770025.

99. Yamano T, Iguchi H, Fukuzawa H. Rapid transformation of Chlamydomonas reinhardtii without cell-wall removal. J Biosci Bioeng. 2013;115(6):691–4. Epub 2013/01/22. doi: 10.1016/j.jbiosc.2012.12.020 23333644.

100. Witman GB. Isolation of Chlamydomonas flagella and flagellar axonemes. Methods in enzymology. 1986;134:280–90. doi: 10.1016/0076-6879(86)34096-5 3821567.

101. Batth TS, Francavilla C, Olsen JV. Off-line high-pH reversed-phase fractionation for in-depth phosphoproteomics. J Proteome Res. 2014;13(12):6176–86. Epub 2014/10/23. doi: 10.1021/pr500893m 25338131.

102. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Analytical chemistry. 2002;74(20):5383–92. Epub 2002/10/31. doi: 10.1021/ac025747h 12403597.

103. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Analytical chemistry. 2003;75(17):4646–58. Epub 2003/11/25. doi: 10.1021/ac0341261 14632076.

104. Holmes JA, Dutcher SK. Cellular asymmetry in Chlamydomonas reinhardtii. Journal of cell science. 1989;94 (Pt 2):273–85. 2621224.

105. Lux FG 3rd, Dutcher SK. Genetic interactions at the FLA10 locus: suppressors and synthetic phenotypes that affect the cell cycle and flagellar function in Chlamydomonas reinhardtii. Genetics. 1991;128(3):549–61. 1874415.

106. Sears PR, Yin WN, Ostrowski LE. Continuous mucociliary transport by primary human airway epithelial cells in vitro. American journal of physiology Lung cellular and molecular physiology. 2015;309(2):L99–108. Epub 2015/05/17. doi: 10.1152/ajplung.00024.2015 25979076

107. Sisson JH, Stoner JA, Ammons BA, Wyatt TA. All-digital image capture and whole-field analysis of ciliary beat frequency. Journal of microscopy. 2003;211(Pt 2):103–11. Epub 2003/07/31. doi: 10.1046/j.1365-2818.2003.01209.x 12887704.

108. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature methods. 2012;9(7):671–5. Epub 2012/08/30. doi: 10.1038/nmeth.2089 22930834

109. Dutcher SK. Flagellar assembly in two hundred and fifty easy-to-follow steps. Trends in genetics: TIG. 1995;11(10):398–404. doi: 10.1016/s0168-9525(00)89123-4 7482766.


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