Superresolution pattern recognition reveals the architectural map of the ciliary transition zone

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Tony Yang, T ^a   Su, Jimmy ^b   Wang, Won Jing ^c   Craige, Branch ^d   Witman, George B ^d   Bryan Tsou, Meng Fu ^e   Liao, Jung Chi ^a  

^a INSTITUTE OF ATOMIC AND MOLECULAR SCIENCES   (Taiwan)

^b Northwestern University   (United States)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CEP290 PROTEIN, HUMAN; MEMBRANE PROTEIN; MKS1 PROTEIN, HUMAN; PROTEIN; RPGRIP1L PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TCTN2 PROTEIN, HUMAN; TMEM67 PROTEIN, HUMAN; TUMOR ANTIGEN; TUMOR PROTEIN;

CELL LINE; CHEMISTRY; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; EUKARYOTIC FLAGELLUM; HUMAN; METABOLISM; REPORTER GENE; ULTRASTRUCTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIGENS, NEOPLASM; CELL LINE; CILIA; GENES, REPORTER; HUMANS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NEOPLASM PROTEINS; PROTEINS;

EID: 84941686676     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14096     Document Type: Article

References (61)

1. Huangfu, D. and Anderson, K. V. Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA 102, 11325-11330 (2005).
2. Simons, M. et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Methods 37, 537-543 (2005).
3. Schneider, L. et al. PDGFRaa signaling is regulated through the primary cilium in fibroblasts. Curr. Biol. 15, 1861-1866 (2005).
4. Ezratty, E. J. et al. A role for the primary cilium in Notch signaling and epidermal differentiation during skin development. Cell 145, 1129-1141 (2011).
5. Badano, J. L., Mitsuma, N., Beales, P. L. and Katsanis, N. The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genom. Hum. Genet. 7, 125-148 (2006).
6. Opitz, J. M. and Howe, J. J. The Meckel syndrome (dysencephalia splanchnocystica, the Gruber syndrome). Birth Defects 5, 167 (1969).
7. Brancati, F., Dallapiccola, B. and Valente, E. Joubert Syndrome and related disorders. Orphanet J. Rare Dis. 5, 1-10 (2010).
8. Hildebrandt, F. and Zhou, W. Nephronophthisis-associated ciliopathies. J. Am. Soc. Nephrol. 18, 1855-1871 (2007).
9. Ansley, S. J. et al. Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425, 628-633 (2003).
10. Sang, L. et al. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 145, 513-528 (2011).
11. Szymanska, K. et al. Founder mutations and genotype-phenotype correlations in Meckel-Gruber syndrome and associated ciliopathies. Cilia 1, 18 (2012).
12. Fliegauf, M., Benzing, T. and Omran, H. When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8, 880-893 (2007).
13. Adams, M., Smith, U. M., Logan, C. V. and Johnson, C. A. Recent advances in the molecular pathology, cell biology and genetics of ciliopathies. J. Med. Genet. 45, 257-267 (2008).
14. Baker, K. and Beales, P. L. Making sense of cilia in disease: The human ciliopathies. Am. J. Med. Genet. C Semin. Med. Genet. 151C, 281-295 (2009).
15. Hildebrandt, F., Benzing, T. and Katsanis, N. Ciliopathies. New Engl. J. Med. 364, 1533-1543 (2011).
16. Williams, C. L. et al. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J. Cell Biol. 192, 1023-1041 (2011).
17. Garcia-Gonzalo, F. R. et al. A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat. Genet. 43, 776-784 (2011).
18. Chih, B. et al. A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nat. Cell Biol. 14, 61-72 (2011).
19. Kee, H. L. et al. A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat. Cell Biol. 14, 431-437 (2012).
20. Hu, Q. et al. A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329, 436-439 (2010).
21. Gilula, N. B. and Satir, P. The ciliary necklace: a ciliary membrane specialization. J. Cell Biol. 53, 494-509 (1972).
22. Craige, B. et al. CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J. Cell Biol. 190, 927-940 (2010).
23. Garcia-Gonzalo, F. R. and Reiter, J. F. Scoring a backstage pass: mechanisms of ciliogenesis and ciliary access. J. Cell Biol. 197, 697-709 (2012).
24. Remans, K., Bürger, M., Vetter, Ingrid R. and Wittinghofer, A. C2 domains as protein-protein interaction modules in the ciliary transition zone. Cell Reports 8, 1-9 (2014).
25. Gorden, N. T. et al. CC2D2A is mutated in Joubert syndrome and interacts with the ciliopathy-associated basal body protein CEP290. Am. J. Hum. Genet. 83, 559-571 (2008).
26. Wang, W.-J. et al. CEP162 is an axoneme-recognition protein promoting ciliary transition zone assembly at the cilia base. Nat. Cell Biol. 15, 591-601 (2013).
27. Tsang, W. Y. et al. CP110 suppresses primary cilia formation through its interaction with CEP290, a protein deficient in human ciliary disease. Dev. Cell 15, 187-197 (2008).
28. Schafer, T. et al. Genetic and physical interaction between the NPHP5 and NPHP6 gene products. Hum. Mol. Genet. 17, 3655-3662 (2008).
29. Stowe, T. R., Wilkinson, C. J., Iqbal, A. and Stearns, T. The centriolar satellite proteins Cep72 and Cep290 interact and are required for recruitment of BBS proteins to the cilium. Mol. Biol. Cell 23, 3322-3335 (2012).
30. Rachel, R. A. et al. Combining Cep290 and Mkks ciliopathy alleles in mice rescues sensory defects and restores ciliogenesis. J. Clin. Invest. 122, 1233-1245 (2012).
31. Kim, J., Krishnaswami, S. R. and Gleeson, J. G. CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum. Mol. Genet. 17, 3796-3805 (2008).
32. Chang, B. et al. In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum. Mol. Genet. 15, 1847-1857 (2006).
33. Sayer, J. A. et al. The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat. Genet. 38, 674-681 (2006).
34. Ludington, W. B., Wemmer, K. A., Lechtreck, K. F., Witman, G. B. and Marshall, W. F. Avalanche-like behavior in ciliary import. Proc. Natl. Acad. Sci. USA 110, 3925-3930 (2013).
35. Kozminski, K. G., Johnson, K. A., Forscher, P. and Rosenbaum, J. L. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc. Natl. Acad. Sci. USA 90, 5519-5523 (1993).
36. Rosenbaum, J. L. and Witman, G. B. Intraflagellar transport. Nat. Methods 3, 813-825 (2002).
37. Snow, J. J. et al. Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat. Cell Biol. 6, 1109-1113 (2004).
38. Nachury, M. V., Seeley, E. S. and Jin, H. Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu. Rev. Cell. Dev. Biol. 26, 59-87 (2010).
39. Ishikawa, H. and Marshall, W. F. Ciliogenesis: building the cells antenna. Nat. Rev. Mol. Cell Biol. 12, 222-234 (2011).
40. Deane, J. A., Cole, D. G., Seeley, E. S., Diener, D. R. and Rosenbaum, J. L. Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr. Biol. 11, 1586-1590 (2001).
41. Liem, K. F. et al. The IFT-A complex regulates Shh signaling through cilia structure and membrane protein trafficking. J. Cell Biol. 197, 789-800 (2012).
42. Christensen, S. T., Pedersen, L. B., Schneider, L. and Satir, P. Sensory cilia and integration of signal transduction in human health and disease. Traffic 8, 97-109 (2007).
43. Huang, L. 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. 89, 713-730 (2011).
44. Yang, T. T. et al. Superresolution STED microscopy reveals differential localization in primary cilia. Cytoskeleton (Hoboken, N.J.) 70, 54-65 (2013).
45. Cole, D. G. et al. Chlamydomonas kinesin-II dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J. Cell Biol. 141, 993-1008 (1998).
46. Nathwani, B., Yang, T. T. and Liao, J.-C. Towards a subdiffraction view of motor-mediated transport in primary cilia. Cell. Mol. Bioeng. 6, 82-97 (2013).
47. Hell, S. and Wichmann, J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19, 780-782 (1994).
48. Klar, T. A., Jakobs, S., Dyba, M., Egner, A. and Hell, S. W. Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc. Natl. Acad. Sci. USA. 97, 8206-8210 (2000).
49. Donnert, G. et al. Two-color far-field fluorescence nanoscopy. Biophys. J. 92, L67-L69 (2007).
50. Huang, B., Wang, W., Bates, M. and Zhuang, X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319, 810-813 (2008).
51. Harke, B., Ullal, C. K., Keller, J. and Hell, S. W. Three-dimensional nanoscopy of colloidal crystals. Nano Lett. 8, 1309-1313 (2008).
52. Wildanger, D., Medda, R., Kastrup, L. and Hell, S. W. A compact STED microscope providing 3D nanoscale resolution. J. Microsc. 236, 35-43 (2009).
53. Graser, S. et al. Cep164, a novel centriole appendage protein required for primary cilium formation. J. Cell Biol. 179, 321-330 (2007).
54. Ou, Y. et al. Adenylate cyclase regulates elongation of mammalian primary cilia. Exp. Cell Res. 315, 2802-2817 (2009).
55. Williams, C. L., Winkelbauer, M. E., Schafer, J. C., Michaud, E. J. and Yoder, B. K. Functional redundancy of the B9 proteins and nephrocystins in Caenorhabditis elegans ciliogenesis. Mol. Biol. Cell 19, 2154-2168 (2008).
56. Kyttälä, M. et al. MKS1, encoding a component of the flagellar apparatus basal body proteome, is mutated in Meckel syndrome. Nat. Methods 38, 155-157 (2006).
57. Smith, U. M. et al. The transmembrane protein meckelin (MKS3) is mutated in Meckel-Gruber syndrome and the wpk rat. Nat. Genet. 38, 191-196 (2006).
58. Goetz, Sarah C., Liem, Karel F, Jr. and Anderson, Kathryn V. The spinocerebellar ataxia-associated gene tau tubulin kinase 2 controls the initiation of ciliogenesis. Cell 151, 847-858 (2012).
59. Shiba, D., Manning, D. K., Koga, H., Beier, D. R. and Yokoyama, T. Inv acts as a molecular anchor for Nphp3 and Nek8 in the proximal segment of primary cilia. Cytoskeleton 67, 112-119 (2010).
60. Wang, W.-J., Soni, R. K., Uryu, K. and Bryan Tsou, M.-F. The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J. Cell Biol. 193, 727-739 (2011).
61. Tikhonov, A. and Arsenin, V. Solutions of ill-posed problems. (Winston and Sons, Washington, 1977).