The Centriolar Satellite Protein AZI1 Interacts with BBS4 and Regulates Ciliary Trafficking of the BBSome

PLoS Genetics

Volumn 10, Issue 2, 2014, Pages

  Chamling, Xitiz ^a   Seo, Seongjin ^a   Searby, Charles C ^a,b   Kim, GunHee ^a   Slusarski, Diane C ^c   Sheffield, Val C ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZACYTIDINE INDUCED 1 PROTEIN; BARDET BIEDL SYNDROME 3 PROTEIN; BARDET BIEDL SYNDROME 4 PROTEIN; BARDET BIEDL SYNDROME 5 PROTEIN; BBSOME; CELL PROTEIN; TETRATRICOPEPTIDE REPEAT PROTEIN; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ARL6 PROTEIN, ZEBRAFISH; AZI1 PROTEIN, ZEBRAFISH; BBS4 PROTEIN, HUMAN; BBS4 PROTEIN, ZEBRAFISH; CELL CYCLE PROTEIN; CEP131 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE PROTEIN; PROTEIN; SMALL INTERFERING RNA; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AZI1 GENE; BARDET BIEDL SYNDROME; BBS4 GENE; CELL MIGRATION; CELL TRANSPORT; CELLULAR DISTRIBUTION; CILIARY TRAFFICKING; CONTROLLED STUDY; CORRELATIONAL STUDY; EMBRYO; EUKARYOTIC FLAGELLUM; GENE; GENE OVEREXPRESSION; GENE SILENCING; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; PROTEIN TRANSPORT; ZEBRA FISH; ANIMAL; CENTRIOLE; CENTROSOME; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MUTATION; PATHOLOGY;

ADP-RIBOSYLATION FACTORS; ANIMALS; BARDET-BIEDL SYNDROME; CELL CYCLE PROTEINS; CENTRIOLES; CENTROSOME; CILIA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICROTUBULE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; PROTEIN TRANSPORT; PROTEINS; RNA, SMALL INTERFERING; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84901742708     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004083     Document Type: Article

References (39)

1. Singla V, Reiter JF, (2006) The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313: 629-633.
2. Goetz SC, Anderson KV, (2010) The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11: 331-344.
3. Williams CL, Li C, Kida K, Inglis PN, Mohan S, et al. (2011) 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.
4. Badano JL, Katsanis N, (2006) Life without centrioles: cilia in the spotlight. Cell 125: 1228-1230.
5. Hildebrandt F, Zhou W, (2007) Nephronophthisis-associated ciliopathies. J Am Soc Nephrol 18: 1855-1871.
6. Zariwala MA, Knowles MR, Omran H, (2007) Genetic defects in ciliary structure and function. Annu Rev Physiol 69: 423-450.
7. Chih B, Liu P, Chinn Y, Chalouni C, Komuves LG, et al. (2012) A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nat Cell Biol 14: 61-72.
8. Craige B, Tsao CC, Diener DR, Hou Y, Lechtreck KF, et al. (2010) CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 190: 927-940.
9. Garcia-Gonzalo FR, Corbit KC, Sirerol-Piquer MS, Ramaswami G, Otto EA, et al. (2011) A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat Genet 43: 776-784.
10. Sang L, Miller JJ, Corbit KC, Giles RH, Brauer MJ, et al. (2011) Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 145: 513-528.
11. Pedersen LB, Rosenbaum JL, (2008) Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85: 23-61.
12. Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peranen J, et al. (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129: 1201-1213.
13. Loktev AV, Zhang Q, Beck JS, Searby CC, Scheetz TE, et al. (2008) A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev Cell 15: 854-865.
14. Domire JS, Green JA, Lee KG, Johnson AD, Askwith CC, et al. (2011) Dopamine receptor 1 localizes to neuronal cilia in a dynamic process that requires the Bardet-Biedl syndrome proteins. Cell Mol Life Sci 68: 2951-2960.
15. Berbari NF, Lewis JS, Bishop GA, Askwith CC, Mykytyn K, (2008) Bardet-Biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia. Proc Natl Acad Sci U S A 105: 4242-4246.
16. Kim JC, Badano JL, Sibold S, Esmail MA, Hill J, et al. (2004) The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat Genet 36: 462-470.
17. Seo S, Zhang Q, Bugge K, Breslow DK, Searby CC, et al. (2011) A novel protein LZTFL1 regulates ciliary trafficking of the BBSome and Smoothened. PLoS Genet 7: e1002358.
18. Chamling X, Seo S, Bugge K, Searby C, Guo DF, et al. (2013) Ectopic Expression of Human BBS4 Can Rescue Bardet-Biedl Syndrome Phenotypes in Bbs4 Null Mice. PLoS One 8: e59101.
19. Zhang Q, Yu D, Seo S, Stone EM, Sheffield VC, (2012) Intrinsic protein-protein interaction-mediated and chaperonin-assisted sequential assembly of stable bardet-biedl syndrome protein complex, the BBSome. J Biol Chem 287: 20625-20635.
20. Stowe TR, Wilkinson CJ, Iqbal A, Stearns T, (2012) The centriolar satellite proteins Cep72 and Cep290 interact and are required for recruitment of BBS proteins to the cilium. Mol Biol Cell 23: 3322-35.
21. Staples CJ, Myers KN, Beveridge RD, Patil AA, Lee AJ, et al. (2012) The centriolar satellite protein Cep131 is important for genome stability. J Cell Sci 125: 4770-4779.
22. Gabernet-Castello C, Dubois KN, Nimmo C, Field MC, (2011) Rab11 function in Trypanosoma brucei: identification of conserved and novel interaction partners. Eukaryot Cell 10: 1082-1094.
23. Akimov V, Rigbolt KT, Nielsen MM, Blagoev B, (2011) Characterization of ubiquitination dependent dynamics in growth factor receptor signaling by quantitative proteomics. Mol Biosyst 7: 3223-3233.
24. Jin H, White SR, Shida T, Schulz S, Aguiar M, et al. (2010) The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 141: 1208-1219.
25. Ge X, Frank CL, Calderon de Anda F, Tsai LH, (2010) Hook3 interacts with PCM1 to regulate pericentriolar material assembly and the timing of neurogenesis. Neuron 65: 191-203.
26. Lee JY, Stearns T, (2013) FOP is a centriolar satellite protein involved in ciliogenesis. PLoS One 8: e58589.
27. Wang G, Chen Q, Zhang X, Zhang B, Zhuo X, et al. (2013) PCM1 recruits Plk1 to the pericentriolar matrix to promote primary cilia disassembly before mitotic entry. J Cell Sci 126: 1355-1365.
28. Yen HJ, Tayeh MK, Mullins RF, Stone EM, Sheffield VC, et al. (2006) Bardet-Biedl syndrome genes are important in retrograde intracellular trafficking and Kupffer's vesicle cilia function. Hum Mol Genet 15: 667-677.
29. Tayeh MK, Yen HJ, Beck JS, Searby CC, Westfall TA, et al. (2008) Genetic interaction between Bardet-Biedl syndrome genes and implications for limb patterning. Hum Mol Genet 17: 1956-1967.
30. Seo S, Baye LM, Schulz NP, Beck JS, Zhang Q, et al. (2010) BBS6, BBS10, and BBS12 form a complex with CCT/TRiC family chaperonins and mediate BBSome assembly. Proc Natl Acad Sci U S A 107: 1488-1493.
31. Pretorius PR, Baye LM, Nishimura DY, Searby CC, Bugge K, et al. (2010) Identification and functional analysis of the vision-specific BBS3 (ARL6) long isoform. PLoS Genet 6: e1000884.
32. Wilkinson CJ, Carl M, Harris WA, (2009) Cep70 and Cep131 contribute to ciliogenesis in zebrafish embryos. BMC Cell Biol 10: 17.
33. Baye LM, Patrinostro X, Swaminathan S, Beck JS, Zhang Y, et al. (2011) The N-terminal region of centrosomal protein 290 (CEP290) restores vision in a zebrafish model of human blindness. Hum Mol Genet 20: 1467-1477.
34. Pretorius PR, Aldahmesh MA, Alkuraya FS, Sheffield VC, Slusarski DC, (2011) Functional analysis of BBS3 A89V that results in non-syndromic retinal degeneration. Hum Mol Genet 20: 1625-1632.
35. Easter SS Jr, Nicola GN, (1996) The development of vision in the zebrafish (Danio rerio). Dev Biol 180: 646-663.
36. Sanger WT (1998) Ctalogue of somatic mutations in cancer. In: Institue WTS, editor. Ctalogue of somatic mutations in cancer. Hinxton, UK: Wellcome Trust Sanger Institute.
37. Ma L, Jarman AP, (2011) Dilatory is a Drosophila protein related to AZI1 (CEP131) that is located at the ciliary base and required for cilium formation. J Cell Sci 124: 2622-2630.
38. Marion V, Stutzmann F, Gerard M, De Melo C, Schaefer E, et al. (2012) Exome sequencing identifies mutations in LZTFL1, a BBSome and smoothened trafficking regulator, in a family with Bardet-Biedl syndrome with situs inversus and insertional polydactyly. J Med Genet 49: 317-321.
39. Nachury MV, (2008) Tandem affinity purification of the BBSome, a critical regulator of Rab8 in ciliogenesis. Methods Enzymol 439: 501-513.