CiliaCarta: An integrated and validated compendium of ciliary genes

Abstract

The cilium is an essential organelle at the surface of mammalian cells whose dysfunction causes a wide range of genetic diseases collectively called ciliopathies. The current rate at which new ciliopathy genes are identified suggests that many ciliary components remain undiscovered. We generated and rigorously analyzed genomic, proteomic, transcriptomic and evolutionary data and systematically integrated these using Bayesian statistics into a predictive score for ciliary function. This resulted in 285 candidate ciliary genes. We generated independent experimental evidence of ciliary associations for 24 out of 36 analyzed candidate proteins using multiple cell and animal model systems (mouse, zebrafish and nematode) and techniques. For example, we show that OSCP1, which has previously been implicated in two distinct non-ciliary processes, causes ciliogenic and ciliopathy-associated tissue phenotypes when depleted in zebrafish. The candidate list forms the basis of CiliaCarta, a comprehensive ciliary compendium covering 956 genes. The resource can be used to objectively prioritize candidate genes in whole exome or genome sequencing of ciliopathy patients and can be accessed at http://bioinformatics.bio.uu.nl/john/syscilia/ciliacarta/.

Full text

Its licence does not allow us to show the full text. Read it at PubMed Central:

References 100

1. 1.

   Yuan S, Sun Z. Expanding horizons: ciliary proteins reach beyond cilia. Annu Rev Genet. Annual Reviews; 2013;47: 353–76.

   Not in our library10.1146/annurev-genet-111212-133243

2. 2.

   Reiter JF, Leroux MR. Genes and molecular pathways underpinning ciliopathies. Nat Rev Mol Cell Biol. Nature Publishing Group; 2017;18: 533–547.

   Not in our library10.1038/nrm.2017.60

3. 3.

   Waters AM, Beales PL. Ciliopathies: an expanding disease spectrum. Pediatr Nephrol. Springer Berlin / Heidelberg; 2011; 1–18–18.

   Not in our library10.1007/s00467-010-1731-7

4. 4.

   Tyler KM, Fridberg A, Toriello KM, Olson CL, Cieslak JA, Hazlett TL, et al Flagellar membrane localization via association with lipid rafts. J Cell Sci. 2009;122: 859–66.

   Not in our library10.1242/jcs.037721

5. 5.

   Takao D, Verhey KJ. Gated entry into the ciliary compartment. Cell Mol Life Sci. 2015;

   Not in our library10.1007/s00018-015-2058-0

6. 6.

   Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. Nature America Inc.; 2000;25: 25–9.

   Not in our library10.1038/75556

7. 7.
   The SYSCILIA gold standard (SCGSv1) of known ciliary components and its applications within a systems biology consortium · 2013

   No notice
8. 8.

   Josic D, Clifton JG. Mammalian plasma membrane proteomics. Proteomics. 2007;7: 3010–29.

   Not in our library10.1002/pmic.200700139

9. 9.

   Tabach Y, Billi AC, Hayes GD, Newman MA, Zuk O, Gabel H, et al Identification of small RNA pathway genes using patterns of phylogenetic conservation and divergence. Nature. 2013;493: 694–8.

   Not in our library10.1038/nature11779

10. 10.
    Integrative Genomics-Based Discovery of Novel Regulators of the Innate Antiviral Response. · 2015

    Not checked
11. 11.

    Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong S-E, et al A mitochondrial protein compendium elucidates complex I disease biology. Cell. 2008;134: 112–23.

    Not in our library10.1016/j.cell.2008.06.016

12. 12.
    MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins · 2015

    No notice
13. 13.

    Avidor-Reiss T, Maer AM, Koundakjian E, Polyanovsky A, Keil T, Subramaniam S, et al Decoding Cilia FunctionDefining Specialized Genes Required for Compartmentalized Cilia Biogenesis. Cell. 2004;117: 527–539.

    Not in our library10.1016/s0092-8674(04)00412-x

14. 14.

    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: 541–552.

    Not in our library10.1016/s0092-8674(04)00450-7

15. 15.

    Piasecki BP, Burghoorn J, Swoboda P. Regulatory Factor X (RFX)-mediated transcriptional rewiring of ciliary genes in animals. Proc Natl Acad Sci U S A. 2010;107: 12969–74.

    Not in our library10.1073/pnas.0914241107

16. 16.

    Ivliev AE, ‘t Hoen PAC, van Roon-Mom WMC, Peters DJM, Sergeeva MG. Exploring the Transcriptome of Ciliated Cells Using In Silico Dissection of Human Tissues. Dias-Neto E, editor. PLoS One. Public Library of Science; 2012;7: e35618

    Not in our library10.1371/journal.pone.0035618

17. 17.

    Arnaiz O, Malinowska A, Klotz C, Sperling L, Dadlez M, Koll F, et al Cildb: a knowledgebase for centrosomes and cilia. Database. 2009;2009: bap022.

    Not in our library10.1093/database/bap022

18. 18.

    Touw WG, Bayjanov JR, Overmars L, Backus L, Boekhorst J, Wels M, et al Data mining in the Life Sciences with Random Forest: a walk in the park or lost in the jungle? Brief Bioinform. 2013;14: 315–26.

    Not in our library10.1093/bib/bbs034

19. 19.
    An organelle-specific protein landscape identifies novel diseases and molecular mechanisms · 2016

    No notice
20. 20.

    Kobayashi Y, Tsuchiya A, Hayashi T, Kohyama N, Ohbayashi M, Yamamoto T. Isolation and characterization of polyspecific mouse organic solute carrier protein 1 (mOscp1). Drug Metab Dispos. 2007;35: 1239–45.

    Not in our library10.1124/dmd.107.014795

21. 21.

    Nie X, Zhang B, Li X, Xiang J, Xiao B, Ma J, et al Cloning, expression, and mutation analysis of NOR1, a novel human gene down-regulated in HNE1 nasopharyngeal carcinoma cell line. J Cancer Res Clin Oncol. 2003;129: 410–4.

    Not in our library10.1007/s00432-003-0451-9

22. 22.

    Lindblad-Toh K, Garber M, Zuk O, Lin MF, Parker BJ, Washietl S, et al A high-resolution map of human evolutionary constraint using 29 mammals. Nature. Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.; 2011;478: 476–82.

    Not in our library10.1038/nature10530

23. 23.

    Liu Q, Tan G, Levenkova N, Li T, Pugh EN, Rux JJ, et al The proteome of the mouse photoreceptor sensory cilium complex. Mol Cell Proteomics. 2007;6: 1299–317.

    Not in our library10.1074/mcp.m700054-mcp200

24. 24.

    Ross AJ, Dailey LA, Brighton LE, Devlin RB. Transcriptional profiling of mucociliary differentiation in human airway epithelial cells. Am J Respir Cell Mol Biol. 2007;37: 169–85.

    Not in our library10.1165/rcmb.2006-0466oc

25. 25.

    Inglis PN, Ou G, Leroux MR, Scholey JM. The sensory cilia of Caenorhabditis elegans. WormBook. 2007; 1–22.

    Not in our library10.1895/wormbook.1.126.2

26. 26.

    Starich TA, Herman RK, Kari CK, Yeh WH, Schackwitz WS, Schuyler MW, et al Mutations affecting the chemosensory neurons of Caenorhabditis elegans. Genetics. 1995;139: 171–188.

    Not in our library10.1093/genetics/139.1.171

27. 27.

    Sanders AAWM, Kennedy J, Blacque OE. Image analysis of Caenorhabditis elegans ciliary transition zone structure, ultrastructure, molecular composition, and function. Methods Cell Biol. 2015;127: 323–47.

    Not in our library10.1016/bs.mcb.2015.01.010

28. 28.

    Coon BG, Hernandez V, Madhivanan K, Mukherjee D, Hanna CB, Barinaga-Rementeria Ramirez I, et al The Lowe syndrome protein OCRL1 is involved in primary cilia assembly. Hum Mol Genet. 2012;21: 1835–47.

    Not in our library10.1093/hmg/ddr615

29. 29.

    Hernandez-Hernandez V, Pravincumar P, Diaz-Font A, May-Simera H, Jenkins D, Knight M, et al Bardet-Biedl syndrome proteins control the cilia length through regulation of actin polymerization. Hum Mol Genet. 2013;22: 3858–68.

    Not in our library10.1093/hmg/ddt241

30. 30.

    Kok FO, Shin M, Ni C-W, Gupta A, Grosse AS, van Impel A, et al Reverse Genetic Screening Reveals Poor Correlation between Morpholino-Induced and Mutant Phenotypes in Zebrafish. Dev Cell. 2015;32: 97–108.

    Not in our library10.1016/j.devcel.2014.11.018

31. 31.

    McClintock TS, Glasser CE, Bose SC, Bergman DA. Tissue expression patterns identify mouse cilia genes. Physiol Genomics. 2008;32: 198–206.

    Not in our library10.1152/physiolgenomics.00128.2007

32. 32.

    Koschützke L, Bertram J, Hartmann B, Bartsch D, Lotze M, von Bohlen und Halbach O. SrGAP3 knockout mice display enlarged lateral ventricles and specific cilia disturbances of ependymal cells in the third ventricle. Cell Tissue Res. 2015;361: 645–50.

    Not in our library10.1007/s00441-015-2224-6

33. 33.

    Fujiwara M, Sengupta P, McIntire SL. Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron. 2002;36: 1091–102.

    Not in our library10.1016/s0896-6273(02)01093-0

34. 34.

    Masyukova S V, Winkelbauer ME, Williams CL, Pieczynski JN, Yoder BK. Assessing the pathogenic potential of human Nephronophthisis disease-associated NPHP-4 missense mutations in C. elegans. Hum Mol Genet. 2011;20: 2942–54.

    Not in our library10.1093/hmg/ddr198

35. 35.

    Williams CL, Winkelbauer ME, Schafer JC, Michaud EJ, Yoder BK. Functional redundancy of the B9 proteins and nephrocystins in Caenorhabditis elegans ciliogenesis. Mol Biol Cell. 2008;19: 2154–68.

    Not in our library10.1091/mbc.e07-10-1070

36. 36.
    Coordinated genomic control of ciliogenesis and cell movement by RFX2 · 2014

    No notice
37. 37.

    Pausch H, Venhoranta H, Wurmser C, Hakala K, Iso-Touru T, Sironen A, et al A frameshift mutation in ARMC3 is associated with a tail stump sperm defect in Swedish Red (Bos taurus) cattle. BMC Genet. BioMed Central; 2016;17: 49

    Not in our library10.1186/s12863-016-0356-7

38. 38.

    Firat-Karalar EN, Sante J, Elliott S, Stearns T. Proteomic analysis of mammalian sperm cells identifies new components of the centrosome. J Cell Sci. 2014;127: 4128–33.

    Not in our library10.1242/jcs.157008

39. 39.

    Huu NT, Yoshida H, Yamaguchi M. Tumor suppressor gene OSCP1/NOR1 regulates apoptosis, proliferation, differentiation, and ROS generation during eye development of Drosophila melanogaster. FEBS J. 2015;282: 4727–46.

    Not in our library10.1111/febs.13528

40. 40.

    Shan Z, Hou Q, Zhang N, Guo L, Zhang X, Ma Y, et al Overexpression of oxidored-nitro domain containing protein 1 induces growth inhibition and apoptosis in human prostate cancer PC3 cells. Oncol Rep. 2014;32: 1939–46.

    Not in our library10.3892/or.2014.3407

41. 41.

    Izuno H, Kobayashi Y, Sanada Y, Nihei D, Suzuki M, Kohyama N, et al Rat organic solute carrier protein 1 (rOscp1) mediated the transport of organic solutes in Xenopus laevis oocytes: isolation and pharmacological characterization of rOscp1. Life Sci. 2007;81: 1183–92.

    Not in our library10.1016/j.lfs.2007.08.012

42. 42.

    Hiratsuka K, Yin S-A, Ohtomo T, Fujita M, Ohtsuki K, Isaka H, et al Intratesticular localization of the organic solute carrier protein, OSCP1, in spermatogenic cells in mice. Mol Reprod Dev. 2008;75: 1495–504.

    Not in our library10.1002/mrd.20893

43. 43.

    Huu NT, Yoshida H, Umegawachi T, Miyata S, Yamaguchi M. Structural characterization and subcellular localization of Drosophila organic solute carrier partner 1. BMC Biochem. 2014;15: 11

    Not in our library10.1186/1471-2091-15-11

44. 44.

    Hiratsuka K, Momose A, Takagi N, Sasaki H, Yin S-A, Fujita M, et al Neuronal expression, cytosolic localization, and developmental regulation of the organic solute carrier partner 1 in the mouse brain. Histochem Cell Biol. 2011;135: 229–38.

    Not in our library10.1007/s00418-011-0790-6

45. 45.

    Jensen VL, Li C, Bowie R V, Clarke L, Mohan S, Blacque OE, et al Formation of the transition zone by Mks5/Rpgrip1L establishes a ciliary zone of exclusion (CIZE) that compartmentalises ciliary signalling proteins and controls PIP2 ciliary abundance. EMBO J. 2015;34: 2537–56.

    Not in our library10.15252/embj.201488044

46. 46.

    Gherman A, Davis EE, Katsanis N. The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat Genet. 2006;38: 961–2.

    Not in our library10.1038/ng0906-961

47. 47.

    Chevrier V, Bruel A-L, Van Dam TJP, Franco B, Lo Scalzo M, Lembo F, et al OFIP/KIAA0753 forms a complex with OFD1 and FOR20 at pericentriolar satellites and centrosomes and is mutated in one individual with oral-facial-digital syndrome. Hum Mol Genet. 2016;25: 497–513.

    Not in our library10.1093/hmg/ddv488

48. 48.

    Slaats GG, Wheway G, Foletto V, Szymanska K, van Balkom BWM, Logister I, et al Screen-based identification and validation of four new ion channels as regulators of renal ciliogenesis. J Cell Sci. 2015;128: 4550–9.

    Not in our library10.1242/jcs.176065

49. 49.

    Seeley ES, Nachury M V. Constructing and deconstructing roles for the primary cilium in tissue architecture and cancer. Methods Cell Biol. 2009;94: 299–313.

    Not in our library10.1016/s0091-679x(08)94015-2

50. 50.

    Michaud EJ, Yoder BK. The primary cilium in cell signaling and cancer. Cancer Res. 2006;66: 6463–7.

    Not in our library10.1158/0008-5472.can-06-0462

51. 51.
    Functional aspects of primary cilia in signaling, cell cycle and tumorigenesis · 2013

    No notice
52. 52.
    Rare disruptive mutations in ciliary function genes contribute to testicular cancer susceptibility · 2016

    Not checked
53. 53.
    Ensembl 2016 · 2015

    No notice
54. 54.

    Kent WJ. BLAT—the BLAST-like alignment tool. Genome Res. 2002;12: 656–64. Article published online before March 2002

    Not in our library10.1101/gr.229202

55. 55.

    Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, et al The human genome browser at UCSC. Genome Res. 2002;12: 996–1006. Article published online before print in May 2002

    Not in our library10.1101/gr.229102

56. 56.

    Letteboer SJF, Roepman R. Versatile screening for binary protein-protein interactions by yeast two-hybrid mating. Methods Mol Biol. 2008;484: 145–59.

    Not in our library10.1007/978-1-59745-398-1_10

57. 57.

    Boldt K, Mans DA, Won J, van Reeuwijk J, Vogt A, Kinkl N, et al Disruption of intraflagellar protein transport in photoreceptor cilia causes Leber congenital amaurosis in humans and mice. J Clin Invest. 2011;121: 2169–80.

    Not in our library10.1172/jci45627

58. 58.

    Gloeckner CJ, Boldt K, Ueffing M. Strep/FLAG tandem affinity purification (SF-TAP) to study protein interactions. Curr Protoc Protein Sci. 2009;Chapter 19: Unit19.20

    Not in our library10.1002/0471140864.ps1920s57

59. 59.

    Boldt K, van Reeuwijk J, Gloeckner CJ, Ueffing M, Roepman R. Tandem affinity purification of ciliopathy-associated protein complexes. Methods Cell Biol. 2009;91: 143–60.

    Not in our library10.1016/s0091-679x(08)91009-8

60. 60.

    Olsen J V, de Godoy LMF, Li G, Macek B, Mortensen P, Pesch R, et al Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics. 2005;4: 2010–21.

    Not in our library10.1074/mcp.t500030-mcp200

61. 61.

    Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26: 1367–72.

    Not in our library10.1038/nbt.1511

62. 62.
    Active transport and diffusion barriers restrict Joubert Syndrome-associated ARL13B/ARL-13 to an Inv-like ciliary membrane subdomain. · 2013

    Not checked
63. 63.

    Dona M, Bachmann-Gagescu R, Texier Y, Toedt G, Hetterschijt L, Tonnaer EL, et al NINL and DZANK1 Co-function in Vesicle Transport and Are Essential for Photoreceptor Development in Zebrafish. PLoS Genet. 2015;11: e1005574

    Not in our library10.1371/journal.pgen.1005574

64. 64.

    Chaki M, Airik R, Ghosh AK, Giles RH, Chen R, Slaats GG, et al Exome capture reveals ZNF423 and CEP164 mutations, linking renal ciliopathies to DNA damage response signaling. Cell. 2012;150: 533–48.

    Not in our library10.1016/j.cell.2012.06.028

65. 65.

    Coene KLM, Roepman R, Doherty D, Afroze B, Kroes HY, Letteboer SJF, et al OFD1 Is Mutated in X-Linked Joubert Syndrome and Interacts with LCA5-Encoded Lebercilin. Am J Hum Genet. 2009;85: 465–481.

    Not in our library10.1016/j.ajhg.2009.09.002

66. 66.

    Roepman R, Bernoud-Hubac N, Schick DE, Maugeri A, Berger W, Ropers HH, et al The retinitis pigmentosa GTPase regulator (RPGR) interacts with novel transport-like proteins in the outer segments of rod photoreceptors. Hum Mol Genet. 2000;9: 2095–105.

    Not in our library10.1093/hmg/9.14.2095

67. 67.

    Roepman R, Letteboer SJF, Arts HH, van Beersum SEC, Lu X, Krieger E, et al Interaction of nephrocystin-4 and RPGRIP1 is disrupted by nephronophthisis or Leber congenital amaurosis-associated mutations. Proc Natl Acad Sci. 2005;102: 18520–18525.

    Not in our library10.1073/pnas.0505774102

68. 68.

    Otto EA, Hurd TW, Airik R, Chaki M, Zhou W, Stoetzel C, et al Candidate exome capture identifies mutation of SDCCAG8 as the cause of a retinal-renal ciliopathy. Nat Genet. 2010;42: 840–850.

    Not in our library10.1038/ng.662

69. 69.

    Kersten FF, van Wijk E, Hetterschijt L, Bauβ K, Peters TA, Aslanyan MG, et al The mitotic spindle protein SPAG5/Astrin connects to the Usher protein network postmitotically. Cilia. 2012;1: 2

    Not in our library10.1186/2046-2530-1-2

70. 70.

    Eblimit A, Nguyen T-MT, Chen Y, Esteve-Rudd J, Zhong H, Letteboer S, et al Spata7 is a retinal ciliopathy gene critical for correct RPGRIP1 localization and protein trafficking in the retina. Hum Mol Genet. 2015;24: 1584–601.

    Not in our library10.1093/hmg/ddu573

71. 71.

    Huang L, Szymanska K, Jensen VL, Janecke AR, Innes AM, Davis EE, et al TMEM237 is mutated in individuals with a Joubert syndrome related disorder and expands the role of the TMEM family at the ciliary transition zone. Am J Hum Genet. 2011;89: 713–30.

    Not in our library10.1016/j.ajhg.2011.11.005

72. 72.
    A Computational Screen for Regulators of Oxidative Phosphorylation Implicates SLIRP in Mitochondrial RNA Homeostasis · 2009

    Corrected
73. 73.

    Lambacher NJ, Bruel A-L, van Dam TJP, Szymańska K, Slaats GG, Kuhns S, et al TMEM107 recruits ciliopathy proteins to subdomains of the ciliary transition zone and causes Joubert syndrome. Nat Cell Biol. Nature Publishing Group; 2016;18: 122–31.

    Not in our library10.1038/ncb3273

74. 74.

    Szklarczyk R, Megchelenbrink W, Cizek P, Ledent M, Velemans G, Szklarczyk D, et al WeGET: predicting new genes for molecular systems by weighted co-expression. Nucleic Acids Res. Oxford University Press; 2015; gkv1228.

    Not in our library10.1093/nar/gkv1228

75. 75.

    Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30: 207–10.

    Not in our library10.1093/nar/30.1.207

76. 76.

    van Dam TJP, Townsend MJ, Turk M, Schlessinger A, Sali A, Field MC, et al Evolution of modular intraflagellar transport from a coatomer-like progenitor. Proc Natl Acad Sci U S A. 2013;110: 6943–8.

    Not in our library10.1073/pnas.1221011110

77. 77.

    Barker AR, Renzaglia KS, Fry K, Dawe HR. Bioinformatic analysis of ciliary transition zone proteins reveals insights into the evolution of ciliopathy networks. BMC Genomics. 2014;15: 531

    Not in our library10.1186/1471-2164-15-531

78. 78.

    Briggs LJ, Davidge JA, Wickstead B, Ginger ML, Gull K. More than one way to build a flagellum: comparative genomics of parasitic protozoa. Curr Biol. 2004;14: R611–2.

    Not in our library10.1016/j.cub.2004.07.041

79. 79.

    Kensche PR, van Noort V, Dutilh BE, Huynen MA. Practical and theoretical advances in predicting the function of a protein by its phylogenetic distribution. J R Soc Interface. 2008;5: 151–70.

    Not in our library10.1098/rsif.2007.1047

80. 80.

    Swoboda P, Adler HT, Thomas JH. The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol Cell. 2000;5: 411–21.

    Not in our library10.1016/s1097-2765(00)80436-0

81. 81.

    You Y, Huang T, Richer EJ, Schmidt J-EH, Zabner J, Borok Z, et al Role of f-box factor foxj1 in differentiation of ciliated airway epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2004;286: L650–7.

    Not in our library10.1152/ajplung.00170.2003

82. 82.

    Efimenko E, Bubb K, Mak HY, Holzman T, Leroux MR, Ruvkun G, et al Analysis of xbx genes in C. elegans. Development. 2005;132: 1923–34.

    Not in our library10.1242/dev.01775

83. 83.

    Chen N, Mah A, Blacque OE, Chu J, Phgora K, Bakhoum MW, et al Identification of ciliary and ciliopathy genes in Caenorhabditis elegans through comparative genomics. Genome Biol. 2006;7: R126

    Not in our library10.1186/gb-2006-7-12-r126

84. 84.

    Laurençon A, Dubruille R, Efimenko E, Grenier G, Bissett R, Cortier E, et al Identification of novel regulatory factor X (RFX) target genes by comparative genomics in Drosophila species. Genome Biol. 2007;8: R195

    Not in our library10.1186/gb-2007-8-9-r195

85. 85.

    Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, Marshall A, et al Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science. American Association for the Advancement of Science; 2010;328: 1036–40.

    Not in our library10.1126/science.1186176

86. 86.

    Sorokin S. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J Cell Biol. 1962;15: 363–77.

    Not in our library10.1083/jcb.15.2.363

87. 87.

    Hoyer-Fender S. Centriole maturation and transformation to basal body. Semin Cell Dev Biol. 2010;21: 142–7.

    Not in our library10.1016/j.semcdb.2009.07.002

88. 88.

    Graser S, Stierhof Y-D, Lavoie SB, Gassner OS, Lamla S, Le Clech M, et al Cep164, a novel centriole appendage protein required for primary cilium formation. J Cell Biol. 2007;179: 321–30.

    Not in our library10.1083/jcb.200707181

89. 89.

    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. Am J Hum Genet. 2014;95: 257–74.

    Not in our library10.1016/j.ajhg.2014.08.005

90. 90.

    Trojan P, Krauss N, Choe H-W, Giessl A, Pulvermüller A, Wolfrum U. Centrins in retinal photoreceptor cells: regulators in the connecting cilium. Prog Retin Eye Res. 2008;27: 237–59.

    Not in our library10.1016/j.preteyeres.2008.01.003

91. 91.

    Yang J, Liu X, Yue G, Adamian M, Bulgakov O, Li T. Rootletin, a novel coiled-coil protein, is a structural component of the ciliary rootlet. J Cell Biol. 2002;159: 431–40.

    Not in our library10.1083/jcb.200207153

92. 92.

    Overlack N, Kilic D, Bauss K, Märker T, Kremer H, van Wijk E, et al Direct interaction of the Usher syndrome 1G protein SANS and myomegalin in the retina. Biochim Biophys Acta. 2011;1813: 1883–92.

    Not in our library10.1016/j.bbamcr.2011.05.015

93. 93.

    Trojan P, Krauss N, Choe H-W, Gießl A, Pulvermüller A, Wolfrum U. Centrins in retinal photoreceptor cells: Regulators in the connecting cilium. Prog Retin Eye Res. Pergamon; 2008;27: 237–259.

    Not in our library10.1016/j.preteyeres.2008.01.003

94. 94.

    Blanks JC, Johnson L V. Specific binding of peanut lectin to a class of retinal photoreceptor cells. A species comparison. Invest Ophthalmol Vis Sci. 1984;25: 546–57.

    Not in our library

95. 95.

    Reiners J, Märker T, Jürgens K, Reidel B, Wolfrum U. Photoreceptor expression of the Usher syndrome type 1 protein protocadherin 15 (USH1F) and its interaction with the scaffold protein harmonin (USH1C). Mol Vis. 2005;11: 347–55.

    Not in our library

96. 96.

    Wunderlich KA, Tanimoto N, Grosche A, Zrenner E, Pekny M, Reichenbach A, et al Retinal functional alterations in mice lacking intermediate filament proteins glial fibrillary acidic protein and vimentin. FASEB J. 2015;29: 4815–28.

    Not in our library10.1096/fj.15-272963

97. 97.

    Sedmak T, Wolfrum U. Intraflagellar transport molecules in ciliary and nonciliary cells of the retina. J Cell Biol. 2010;189: 171–186.

    Not in our library10.1083/jcb.200911095

98. 98.

    Maerker T, van Wijk E, Overlack N, Kersten FFJ, McGee J, Goldmann T, et al A novel Usher protein network at the periciliary reloading point between molecular transport machineries in vertebrate photoreceptor cells. Hum Mol Genet. 2008;17: 71–86.

    Not in our library10.1093/hmg/ddm285

99. 99.

    Sedmak T, Sehn E, Wolfrum U. Immunoelectron microscopy of vesicle transport to the primary cilium of photoreceptor cells. Methods Cell Biol. 2009;94: 259–72.

    Not in our library10.1016/s0091-679x(08)94013-9

100. 100.

     Westerfield M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio Rerio*). Paperback. Institute of Neuro Science; 1994.

     Not in our library

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.