The transition zone: An essential functional compartment of cilia

Cilia

Volumn 1, Issue , 2012, Pages

  Szymanska, Katarzyna ^a   Johnson, Colin A ^a  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

Cilia; Ciliopathies; IFT; Transition zone

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE;

AXONEME; BARDET BIEDL SYNDROME; CELL CYCLE REGULATION; CONGENITAL DISORDER; EUKARYOTIC FLAGELLUM; EXTRACELLULAR SPACE; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; JOUBERT SYNDROME; KINETOSOME; MECKEL SYNDROME; MICROTUBULE; NEPHRONOPHTHISIS; PHENOTYPIC VARIATION; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW; S PHASE CELL CYCLE CHECKPOINT; SENIOR LOKEN SYNDROME; SIGNAL TRANSDUCTION; TRANSITION ZONE; ULTRASTRUCTURE;

EID: 84874856739     PISSN: None     EISSN: 20462530     Source Type: Journal    
DOI: 10.1186/2046-2530-1-10     Document Type: Review

References (66)

1. Pan J, Snell W. The Primary Cilium: Keeper of the Key to Cell Division. Cell 2007, 129:1255-1257. 10.1016/j.cell.2007.06.018, 17604715.
2. Praetorius HA, Spring KR. A physiological view of the primary cilium. Annu Rev Physiol 2005, 67:515-529. 10.1146/annurev.physiol.67.040403.101353, 15709968.
3. Davis EE, Zhang Q, Liu Q, Diplas BH, Davey LM, Hartley J, Stoetzel C, Szymanska K, Ramaswami G, Logan CV, Muzny DM, Young AC, Wheeler DA, Cruz P, Morgan M, Lewis LR, Cherukuri P, Maskeri B, Hansen NF, Mullikin JC, Blakesley RW, Bouffard GG, Comparative Sequencing Program NISC, Gyapay G, Rieger S, Tönshoff B, Kern I, Soliman NA, Neuhaus TJ, Swoboda KJ, Kayserili H. TTC21B contributes both causal and modifying alleles across the ciliopathy spectrum. Nat Genet 2011, 43:189-196. 10.1038/ng.756, 3071301, 21258341.
4. Baala L, Romano S, Khaddour R, Saunier S, Smith UM, Audollent S, Ozilou C, Faivre L, Laurent N, Foliguet B, Munnich A, Lyonnet S, Salomon R, Encha-Razavi F, Gubler MC, Boddaert N, de Lonlay P, Johnson CA, Vekemans M, Antignac C, Attie-Bitach T. The Meckel-Gruber syndrome gene, MKS3, is mutated in Joubert syndrome. Am J Hum Genet 2007, 80:186-194. 10.1086/510499, 1785313, 17160906.
5. Bergmann C, Fliegauf M, Bruchle NO, Frank V, Olbrich H, Kirschner J, Schermer B, Schmedding I, Kispert A, Kranzlin B, Nürnberg G, Becker C, Grimm T, Girschick G, Lynch SA, Kelehan P, Senderek J, Neuhaus TJ, Stallmach T, Zentgraf H, Nürnberg P, Gretz N, Lo C, Lienkamp S, Schäfer T, Walz G, Benzing T, Zerres K, Omran H. Loss of nephrocystin-3 function can cause embryonic lethality, meckel-gruber-like syndrome, situs inversus, and renal-hepatic-pancreatic dysplasia. Am J Hum Genet 2008, 82:959-970. 10.1016/j.ajhg.2008.02.017, 2427297, 18371931.
6. Devuyst O, Arnould VJ. Mutations in RPGRIP1L: extending the clinical spectrum of ciliopathies. Nephrol Dial Transplant 2008, 23:1500-1503. 10.1093/ndt/gfn033, 18281315.
7. Mougou-Zerelli S, Thomas S, Szenker E, Audollent S, Elkhartoufi N, Babarit C, Romano S, Salomon R, Amiel J, Esculpavit C, Gonzales M, Escudier E, Leheup B, Loget P, Odent S, Roume J, Gérard M, Delezoide AL, Khung S, Patrier S, Cordier MP, Bouvier R, Martinovic J, Gubler MC, Boddaert N, Munnich A, Encha-Razavi F, Valente EM, Saad A, Saunier S, et al. CC2D2A Mutations in Meckel and Joubert Syndromes Indicate a Genotype-Phenotype Correlation. Hum Mutat 2009, 30:1574-1582. 10.1002/humu.21116, 2783384, 19777577.
8. Kotov N, Bates D, Gizatullina A, Gilaziev B, Khairullin R, Chen M, Drozdov I, Umezawa Y, Hundhausen C, Aleksandrov A, Yan XG, Spurgeon SK, Smales CM, Valeyev NV. Computational modelling elucidates the mechanism of ciliary regulation in health and disease. BMC Systems Biology 2011, 5:143. 10.1186/1752-0509-5-143, 3224258, 21920041.
9. Menini A (Ed: The Neurobiology of Olfaction Boca Raton, FL: CRC Press; 2010, Menini A (Ed:.
10. Fontilla MF, Peterson EH. Kinocilia heights on utricular hair cells. Hear Res 2000, 145:8-16. 10.1016/S0378-5955(00)00068-X, 10867272.
11. Fliegauf M, Benzing T, Omran H. When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 2007, 8:880-893. 10.1038/nrm2278, 17955020.
12. Paintrand M, Moudjou M, Delacroix H, Bornens M. Centrosome organization and centriole architecture: Their sensitivity to divalent cations. J Struct Biol 1992, 108:107-128. 10.1016/1047-8477(92)90011-X, 1486002.
13. Satir P. Studies on cilia. J Cell Biol 1968, 39:77-94. 10.1083/jcb.39.1.77, 2107504, 5678451.
14. Sorokin SP. Reconstructions of Centriole Formation and Ciliogenesis in Mammalian Lungs. J Cell Sci 1968, 3:207-230.
15. Pedersen LB, Veland IR, Schroder JM, Christensen ST. Assembly of primary cilia. Dev Dyn 2008, 237:1993-2006. 10.1002/dvdy.21521, 18393310.
16. Omran H. NPHP proteins: gatekeepers of the ciliary compartment. J Cell Biol 2010, 190:715-717. 10.1083/jcb.201008080, 2935579, 20819931.
17. Gibbons IR, Grimstone AV. On Flagellar Structure in Certain Flagellates. J Biophys Biochem Cytol 1960, 7:697-716. 10.1083/jcb.7.4.697, 2224891, 13827900.
18. Ringo DL. Flagellar motion and fine structure of the flagellar apparatus in Chlamydomonas. J Cell Biol 1967, 33:543-571. 10.1083/jcb.33.3.543, 2107204, 5341020.
19. Williams CL, Li C, Kida K, Inglis PN, Mohan S, Semenec L, Bialas NJ, Stupay RM, Chen N, Blacque OE, Yoder BK, Leroux MR. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. The Journal of Cell Biology 2011, 192:1023-1041. 10.1083/jcb.201012116, 3063147, 21422230.
20. Gilula NB, Satir P. The ciliary necklace. J Cell Biol 1972, 53:494-509. 10.1083/jcb.53.2.494, 2108734, 4554367.
21. Fisch C, Dupuis-Williams P. Ultrastructure of cilia and flagella - back to the future!. Biol Cell 2011, 103:249-270. 10.1042/BC20100139, 21728999.
22. Quinlan RJ, Tobin JL, Beales PL. Modeling ciliopathies: primary cilia in development and disease. Curr Top Dev Biol 2008, 84:249-310.
23. Liu Q, Tan G, Levenkova N, Li T, Pugh EN, Rux JJ, Speicher DW, Pierce EA. The Proteome of the Mouse Photoreceptor Sensory Cilium Complex. Mol Cell Proteomics 2007, 6:1299-1317. 10.1074/mcp.M700054-MCP200, 2128741, 17494944.
24. Kilburn CL, Pearson CG, Romijn EP, Meehl JB, Giddings TH, Culver BP, Yates JR, Winey M. New Tetrahymena basal body protein components identify basal body domain structure. J Cell Biol 2007, 178:905-912. 10.1083/jcb.200703109, 2064616, 17785518.
25. Graser S, Stierhof Y-D, Lavoie SB, Gassner OS, Lamla S, Le Clech M, Nigg EA. Cep164, a novel centriole appendage protein required for primary cilium formation. J Cell Biol 2007, 179:321-330. 10.1083/jcb.200707181, 2064767, 17954613.
26. Ishikawa H, Kubo A, Tsukita S, Tsukita S. Odf2-deficient mother centrioles lack distal/subdistal appendages and the ability to generate primary cilia. Nat Cell Biol 2005, 7:517-524. 10.1038/ncb1251, 15852003.
27. Deane JA, Cole DG, Seeley ES, Diener DR, Rosenbaum JL. Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr Biol 2001, 11:1586-1590. 10.1016/S0960-9822(01)00484-5, 11676918.
28. Rosenbaum JL, Witman GB. Intraflagellar transport. Nat Rev Mol Cell Biol 2002, 3:813-825. 10.1038/nrm952, 12415299.
29. O'Toole ET, Giddings TH, Dutcher SK. Understanding Microtubule Organizing Centers by Comparing Mutant and Wild-Type Structures with Electron Tomography. Methods in Cell Biology 2007, 125-143. Academic Press, Waltham, MS, McIntosh JR.
30. Reese TS. Olfactory cilia in the frog. J Cell Biol 1965, 25:209-230. 2106683, 5840799.
31. Anderson RGW. Isolation of ciliated or inciliated basal bodies from the rabbit oviduct. J Cell Biol 1974, 60:393-404. 10.1083/jcb.60.2.393, 2109169, 4204973.
32. Cavalier-Smith T. Basal Body and Flagellar Development During the Vegetative Cell Cycle and the Sexual Cycle of Chlamydomonas Reinhardii. J Cell Sci 1974, 16:529-556.
33. Dute R, Kung C. Ultrastructure of the proximal region of somatic cilia in Paramecium tetraurelia. J Cell Biol 1978, 78:451-464. 10.1083/jcb.78.2.451, 2110115, 690175.
34. Geimer S, Melkonian M. Centrin Scaffold in Chlamydomonas reinhardtii Revealed by Immunoelectron Microscopy. Eukaryot Cell 2005, 4:1253-1263. 10.1128/EC.4.7.1253-1263.2005, 1168961, 16002651.
35. Horst CJ, Forestner DM, Besharse JC. Cytoskeletal-membrane interactions: a stable interaction between cell surface glycoconjugates and doublet microtubules of the photoreceptor connecting cilium. J Cell Biol 1987, 105:2973-2987. 10.1083/jcb.105.6.2973, 2114726, 3693403.
36. Craige B, Tsao C-C, Diener DR, Hou Y, Lechtreck K-F, Rosenbaum JL, Witman GB. CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 2010, 190:927-940. 10.1083/jcb.201006105, 2935561, 20819941.
37. Silflow CD, Liu B, LaVoie M, Richardson EA, Palevitz BA. γ-tubulin in Chlamydomonas: Characterization of the gene and localization of the gene product in cells. Cell Motil Cytoskeleton 1999, 42:285-297. 10.1002/(SICI)1097-0169(1999)42:4<285::AID-CM3>3.0.CO;2-Z, 10223635.
38. Hu Q, Milenkovic L, Jin H, Scott MP, Nachury MV, Spiliotis ET, Nelson WJ. A Septin Diffusion Barrier at the Base of the Primary Cilium Maintains Ciliary Membrane Protein Distribution. Science 2010, 329:436-439. 10.1126/science.1191054, 3092790, 20558667.
39. Ishikawa H, Marshall WF. Ciliogenesis: building the cell's antenna. Nat Rev Mol Cell Biol 2011, 12:222-234. 10.1038/nrm3085, 21427764.
40. Hu Q, Nelson WJ. Ciliary diffusion barrier: The gatekeeper for the primary cilium compartment. Cytoskeleton 2011, 68:313-324. 10.1002/cm.20514, 3143192, 21634025.
41. Nachury MV, Seeley ES, Jin H. Trafficking to the Ciliary Membrane: How to Get Across the Periciliary Diffusion Barrier?. Annu Rev Cell Dev Biol 2010, 26:59-87. 10.1146/annurev.cellbio.042308.113337, 2952038, 19575670.
42. Deretic D, Williams AH, Ransom N, Morel V, Hargrave PA, Arendt A. Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proc Natl Acad Sci U S A 2005, 102:3301-3306. 10.1073/pnas.0500095102, 552909, 15728366.
43. Mazelova J, Astuto-Gribble L, Inoue H, Tam BM, Schonteich E, Prekeris R, Moritz OL, Randazzo PA, Deretic D. Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J 2009, 28:183-192. 10.1038/emboj.2008.267, 2637330, 19153612.
44. Geng L, Okuhara D, Yu Z, Tian X, Cai Y, Shibazaki S, Somlo S. Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. J Cell Sci 2006, 119:1383-1395. 10.1242/jcs.02818, 16537653.
45. Jahn R, Scheller RH. SNAREs - engines for membrane fusion. Nat Rev Mol Cell Biol 2006, 7:631-643. 10.1038/nrm2002, 16912714.
46. Follit JA, Tuft RA, Fogarty KE, Pazour GJ. The Intraflagellar Transport Protein IFT20 Is Associated with the Golgi Complex and Is Required for Cilia Assembly. Mol Biol Cell 2006, 17:3781-3792. 10.1091/mbc.E06-02-0133, 1593158, 16775004.
47. Ang AL, Taguchi T, Francis S, Fölsch H, Murrells LJ, Pypaert M, Warren G, Mellman I. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J Cell Biol 2004, 167:531-543. 10.1083/jcb.200408165, 2172492, 15534004.
48. Hsiao Y-C, Tong ZJ, Westfall JE, Ault JG, Page-McCaw PS, Ferland RJ. Ahi1, whose human ortholog is mutated in Joubert syndrome, is required for Rab8a localization, ciliogenesis and vesicle trafficking. Hum Mol Genet 2009, 18:3926-3941. 10.1093/hmg/ddp335, 2748898, 19625297.
49. Yoshimura S-I, Egerer J, Fuchs E, Haas AK, Barr FA. Functional dissection of Rab GTPases involved in primary cilium formation. J Cell Biol 2007, 178:363-369. 10.1083/jcb.200703047, 2064854, 17646400.
50. Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peränen J, Merdes A, Slusarski DC, Scheller RH, Bazan JF, Sheffield VC, Jackson PK. A Core Complex of BBS Proteins Cooperates with the GTPase Rab8 to Promote Ciliary Membrane Biogenesis. Cell 2007, 129:1201-1213. 10.1016/j.cell.2007.03.053, 17574030.
51. Follit JA, Li L, Vucica Y, Pazour GJ. The cytoplasmic tail of fibrocystin contains a ciliary targeting sequence. J Cell Biol 2010, 188:21-28. 10.1083/jcb.200910096, 2812845, 20048263.
52. Knödler A, Feng S, Zhang J, Zhang X, Das A, Peränen J, Guo W. Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc Natl Acad Sci 2010, 107:6346-6351. 10.1073/pnas.1002401107, 2851980, 20308558.
53. Kim J, Krishnaswami SR, Gleeson JG. CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum Mol Genet 2008, 17:3796-3805. 10.1093/hmg/ddn277, 2722899, 18772192.
54. Garcia-Gonzalo FR, Corbit KC, Sirerol-Piquer MS, Ramaswami G, Otto EA, Noriega TR, Seol AD, Robinson JF, Bennett CL, Josifova DJ, García-Verdugo JM, Katsanis N, Hildebrandt F, Reiter JF. A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat Genet 2011, 43:776-784. 10.1038/ng.891, 3145011, 21725307.
55. Nalefski EA, Falke JJ. The C2 domain calcium-binding motif: Structural and functional diversity. Protein Sci 1996, 5:2375-2390. 10.1002/pro.5560051201, 2143302, 8976547.
56. Bachmann-Gagescu R, Phelps IG, Stearns G, Link BA, Brockerhoff SE, Moens CB, Doherty D. The ciliopathy gene cc2d2a controls zebrafish photoreceptor outer segment development through a role in Rab8-dependent vesicle trafficking. Hum Mol Genet 2011, 20:4041-4055. 10.1093/hmg/ddr332, 3177654, 21816947.
57. Jin H, White SR, Shida T, Schulz S, Aguiar M, Gygi SP, Bazan JF, Nachury MV. The Conserved Bardet-Biedl Syndrome Proteins Assemble a Coat that Traffics Membrane Proteins to Cilia. Cell 2010, 141:1208-1219. 10.1016/j.cell.2010.05.015, 2898735, 20603001.
58. Lechtreck K-F, Johnson EC, Sakai T, Cochran D, Ballif BA, Rush J, Pazour GJ, Ikebe M, Witman GB. The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J Cell Biol 2009, 187:1117-1132. 10.1083/jcb.200909183, 2806276, 20038682.
59. Huang K, Diener DR, Rosenbaum JL. The ubiquitin conjugation system is involved in the disassembly of cilia and flagella. J Cell Biol 2009, 186:601-613. 10.1083/jcb.200903066, 2733750, 19704024.
60. Sang L, Miller Julie J, Corbit Kevin C, Giles Rachel H, Brauer Matthew J, Otto Edgar A, Baye Lisa M, Wen X, Scales Suzie J, Kwong M, Huntzicker EG, Sfakianos MK, Sandoval W, Bazan JF, Kulkarni P, Garcia-Gonzalo FR, Seol AD, O'Toole JF, Held S, Reutter HM, Lane WS, Rafiq MA, Noor A, Ansar M, Devi AR, Sheffield VC, Slusarski DC, Vincent JB, Doherty DA, Hildebrandt F. Mapping the NPHP-JBTS-MKS Protein Network Reveals Ciliopathy Disease Genes and Pathways. Cell 2011, 145:513-528. 10.1016/j.cell.2011.04.019, 3383065, 21565611.
61. Jiang S-T, Chiou Y-Y, Wang E, Chien Y-L, Ho H-H, Tsai F-J, Lin C-Y, Tsai S-P, Li H. Essential role of nephrocystin in photoreceptor intraflagellar transport in mouse. Hum Mol Genet 2009, 18:1566-1577. 10.1093/hmg/ddp068, 19208653.
62. Shiba D, Manning DK, Koga H, Beier DR, Yokoyama T. Inv acts as a molecular anchor for Nphp3 and Nek8 in the proximal segment of primary cilia. Cytoskeleton 2010, 67:112-119.
63. Li A, Saito M, Chuang J-Z, Tseng Y-Y, Dedesma C, Tomizawa K, Kaitsuka T, Sung C-H. Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorption, S-phase entry and fate of neural progenitors. Nat Cell Biol 2011, 13:402-411. 10.1038/ncb2218, 21394082.
64. Chuang J-Z, Yeh T-Y, Bollati F, Conde C, Canavosio F, Caceres A, Sung C-H. The Dynein Light Chain Tctex-1 Has a Dynein-Independent Role in Actin Remodeling during Neurite Outgrowth. Dev Cell 2005, 9:75-86. 10.1016/j.devcel.2005.04.003, 15992542.
65. Huang L, Szymanska K, Jensen VL, Janecke AR, Innes AM, Davis EE, Frosk P, Li C, Willer JR, Chodirker BN, Greenberg CR, McLeod DR, Bernier FP, Chudley AE, Müller T, Shboul M, Logan CV, Loucks CM, Beaulieu CL, Bowie RV, Bell SM, Adkins J, Zuniga FI, Ross KD, Wang J, Ban MR, Beck C, Nürnberg P, Douglas S, Craft CM, Akimenko M-A, 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, 89:713-730. 10.1016/j.ajhg.2011.11.005, 3234373, 22152675.
66. Khanna H, Davis EE, Murga-Zamalloa CA, Estrada-Cuzcano A, Lopez I, den Hollander AI, Zonneveld MN, Othman MI, Waseem N, Chakarova CF, Maubaret C, Diaz-Font A, MacDonald I, Muzny DM, Wheeler DA, Morgan M, Lewis LR, Logan CV, Tan PL, Beer MA, Inglehearn CF, Lewis RA, Jacobson SG, Bergmann C, Beales PL, Attié-Bitach T, Johnson CA, Otto EA, Bhattacharya SS, Hildebrandt F, et al. A common allele in RPGRIP1L is a modifier of retinal degeneration in ciliopathies. Nat Genet 2009, 41:739-745. 10.1038/ng.366, 2783476, 19430481.