BBS4 and BBS5 show functional redundancy in the BBSome to regulate the degradative sorting of ciliary sensory receptors

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Xu, Qingwen ^c   Zhang, Yuxia ^a,c   Wei, Qing ^a,c   Huang, Yan ^c   Li, Yan ^a,c   Ling, Kun ^c   Hu, Jinghua ^a,b,c  

^a MAYO CLINIC   (United States)

^b Mayo Translational PKD Center   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BBS4 PROTEIN, HUMAN; BBS5 PROTEIN, HUMAN; CAENORHABDITIS ELEGANS PROTEIN; PROTEIN; SMALL INTERFERING RNA;

ANIMAL; ANTAGONISTS AND INHIBITORS; BARDET BIEDL SYNDROME; CAENORHABDITIS ELEGANS; CELL LINE; DOWN REGULATION; EUKARYOTIC FLAGELLUM; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MISSENSE MUTATION; PATHOLOGY; RNA INTERFERENCE; SENSORY NERVE CELL; UBIQUITINATION;

ANIMALS; BARDET-BIEDL SYNDROME; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE; CILIA; DOWN-REGULATION; HEK293 CELLS; HUMANS; MUTATION, MISSENSE; PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SENSORY RECEPTOR CELLS; UBIQUITINATION;

EID: 84936108939     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11855     Document Type: Article

References (54)

1. Singla, V. & Reiter, J. F. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science (New York, N.Y) 313, 629-633 (2006).
2. Goetz, S. C. & Anderson, K. V. The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11, 331-344, doi: 10.1038/nrg2774 (2010).
3. Badano, J. L., Mitsuma, N., Beales, P. L. & Katsanis, N. The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 7, 125-148 (2006).
4. Adams, M., Smith, U. M., Logan, C. V. & Johnson, C. A. Recent advances in the molecular pathology, cell biology and genetics of ciliopathies. J Med Genet 45, 257-267 (2008).
5. Hildebrandt, F. & Zhou, W. Nephronophthisis-associated ciliopathies. J Am Soc Nephrol 18, 1855-1871, doi: 10.1681/ASN.2006121344 (2007).
6. Hu, J., Wittekind, S. G. & Barr, M. M. STAM and Hrs down-regulate ciliary TRP receptors. Mol Biol Cell 18, 3277-3289, doi: 10.1091/mbc.E07-03-0239 (2007).
7. Hu, J., Bae, Y. K., Knobel, K. M. & Barr, M. M. Casein kinase II and calcineurin modulate TRPP function and ciliary localization. Mol Biol Cell 17, 2200-2211, doi: 10.1091/mbc.E05-10-0935 (2006).
8. Sattar, S. & Gleeson, J. G. The ciliopathies in neuronal development: a clinical approach to investigation of Joubert syndrome and Joubert syndrome-related disorders. Dev Med Child Neurol 53, 793-798, doi: 10.1111/j.1469-8749.2011.04021.x (2011).
9. Scheidecker, S. et al. Exome sequencing of Bardet-Biedl syndrome patient identifies a null mutation in the BBSome subunit BBIP1 (BBS18). J Med Genet 51, 132-136, doi: 10.1136/jmedgenet-2013-101785 (2014).
10. Loktev, A. V. et al. A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev Cell 15, 854-865, doi: 10.1016/j.devcel.2008.11.001 (2008).
11. Nachury, M. V. et al. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129, 1201-1213, doi: 10.1016/j.cell.2007.03.053 (2007).
12. Jin, H. et al. The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 141, 1208-1219, doi: 10.1016/j.cell.2010.05.015 (2010).
13. Seo, S. et al. A novel protein LZTFL1 regulates ciliary trafficking of the BBSome and Smoothened. PLoS genetics 7, e1002358, doi: 10.1371/journal.pgen.1002358 (2011).
14. Lechtreck, K. F. et al. Cycling of the signaling protein phospholipase D through cilia requires the BBSome only for the export phase. J Cell Biol 201, 249-261, doi: 10.1083/jcb.201207139 (2013).
15. Lechtreck, K. F. et al. The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J Cell Biol 187, 1117-1132, doi: 10.1083/jcb.200909183 (2009).
16. Yen, H. J. et al. Bardet-Biedl syndrome genes are important in retrograde intracellular trafficking and Kupffer's vesicle cilia function. Hum Mol Genetics 15, 667-677, doi: 10.1093/hmg/ddi468 (2006).
17. Berbari, N. F., Lewis, J. S., Bishop, G. A., Askwith, C. C. & Mykytyn, K. Bardet-Biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia. Proc Natl Acad Sci USA 105, 4242-4246 (2008).
18. Su, X. et al. Bardet-Biedl syndrome proteins 1 and 3 regulate the ciliary trafficking of polycystic kidney disease 1 protein. Hum Mol Genet, doi: 10.1093/hmg/ddu267 (2014).
19. Domire, J. S. et al. Dopamine receptor 1 localizes to neuronal cilia in a dynamic process that requires the Bardet-Biedl syndrome proteins. Cell and Mol Life Sci : CMLS 68, 2951-2960, doi: 10.1007/s00018-010-0603-4 (2011).
20. Zhang, Q. et al. BBS7 is required for BBSome formation and its absence in mice results in Bardet-Biedl syndrome phenotypes and selective abnormalities in membrane protein trafficking. J Cell Sci 126, 2372-2380, doi: 10.1242/jcs.111740 (2013).
21. Zhang, Q., Seo, S., Bugge, K., Stone, E. M. & Sheffield, V. C. BBS proteins interact genetically with the IFT pathway to influence SHH-related phenotypes. Hum Mol Genet 21, 1945-1953, doi: 10.1093/hmg/dds004 (2012).
22. Zhang, Q. et al. Bardet-Biedl syndrome 3 (Bbs3) knockout mouse model reveals common BBS-associated phenotypes and Bbs3 unique phenotypes. Proc Natl Acad Sci USA a 108, 20678-20683, doi: 10.1073/pnas.1113220108 (2011).
23. Eguether, T. et al. IFT27 links the BBSome to IFT for maintenance of the ciliary signaling compartment. Dev Cell 31, 279-290, doi: 10.1016/j.devcel.2014.09.011 (2014).
24. Liew, G. M. et al. The intraflagellar transport protein IFT27 promotes BBSome exit from cilia through the GTPase ARL6/BBS3. Dev Cell 31, 265-278, doi: 10.1016/j.devcel.2014.09.004 (2014).
25. Wei, Q. et al. The BBSome controls IFT assembly and turnaround in cilia. Nat Cell Biol 14, 950-957, doi: 10.1038/ncb2560 (2012).
26. Ou, G., Blacque, O. E., Snow, J. J., Leroux, M. R. & Scholey, J. M. Functional coordination of intraflagellar transport motors. Nature 436, 583-587, doi: 10.1038/nature03818 (2005).
27. Blacque, O. E. et al. Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. Genes Dev 18, 1630-1642, doi: 10.1101/gad.1194004 (2004).
28. Hedgecock, E. M., Culotti, J. G., Thomson, J. N. & Perkins, L. A. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev Biol 111, 158-170 (1985).
29. 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).
30. Ou, G. et al. Sensory ciliogenesis in Caenorhabditis elegans: assignment of IFT components into distinct modules based on transport and phenotypic profiles. Mol Biol Cell 18, 1554-1569, doi: 10.1091/mbc.E06-09-0805 (2007).
31. Torres, V. E., Bankir, L. & Grantham, J. J. A case for water in the treatment of polycystic kidney disease. Cli J Am Soc Nephrol 4, 1140-1150, doi:10.2215/CJN.00790209 (2009).
32. Barr, M. M. & Sternberg, P. W. A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401, 386-389, doi: 10.1038/43913 (1999).
33. Braunreiter, K., Hamlin, S. & Lyman-Gingerich, J. Identification and characterization of a novel allele of Caenorhabditis elegans bbs-7. PloS one 9, e113737, doi: 10.1371/journal.pone.0113737 (2014).
34. Tobin, D. et al. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35, 307-318 (2002).
35. Sengupta, P., Chou, J. H. & Bargmann, C. I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84, 899-909 (1996).
36. Zhang, Q., Yu, D., Seo, S., Stone, E. M. & Sheffield, V. C. 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, doi: 10.1074/jbc.M112.341487 (2012).
37. Wei, Q. et al. Transition fibre protein FBF1 is required for the ciliary entry of assembled intraflagellar transport complexes. Nat Comm 4, 2750, doi: 10.1038/ncomms3750 (2013).
38. Stenson, P. D. et al. The Human Gene Mutation Database: building a comprehensive mutation repository for clinical and molecular genetics, diagnostic testing and personalized genomic medicine. Hum Genet 133, 1-9, doi: 10.1007/s00439-013-1358-4 (2014).
39. Katsanis, N. et al. BBS4 is a minor contributor to Bardet-Biedl syndrome and may also participate in triallelic inheritance. Am J Hum Genet 71, 22-29, doi:10.1086/341031 (2002).
40. Wang, H. et al. Exome capture sequencing identifies a novel mutation in BBS4. Mol Vis 17, 3529-3540 (2011).
41. Qin, H. et al. Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane. Curr Biol 15, 1695-1699, doi: 10.1016/j.cub.2005.08.047 (2005).
42. Burbea, M., Dreier, L., Dittman, J. S., Grunwald, M. E. & Kaplan, J. M. Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans. Neuron 35, 107-120 (2002).
43. Thrower, J. S., Hoffman, L., Rechsteiner, M. & Pickart, C. M. Recognition of the polyubiquitin proteolytic signal. Embo J 19, 94-102 (2000).
44. Li, J. et al. Differential regulation of amyloid-beta endocytic trafficking and lysosomal degradation by apolipoprotein E isoforms. J Biol Chem 287, 44593-44601, doi: 10.1074/jbc.M112.420224 (2012).
45. Liu, Y. P. et al. Ciliopathy proteins regulate paracrine signaling by modulating proteasomal degradation of mediators. J Cli Inv 124, 2059-2070, doi:10.1172/JCI71898 (2014).
46. Scholey, J. M. & Anderson, K. V. Intraflagellar transport and cilium-based signaling. Cell 125, 439-442 (2006).
47. Marshall, W. F. & Nonaka, S. Cilia: Tuning in to the Cell's Antenna. Curr Biol 16, R604-614 (2006).
48. Katzmann, D. J., Odorizzi, G. & Emr, S. D. Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 3, 893-905 (2002).
49. Kaplan, O. I. et al. Endocytosis genes facilitate protein and membrane transport in C. elegans sensory cilia. Curr Biol 22, 451-460, doi: 10.1016/j.cub.2012.01.060 (2012).
50. Leitch, C. C., Lodh, S., Prieto-Echague, V., Badano, J. L. & Zaghloul, N. A. Basal body proteins regulate Notch signaling through endosomal trafficking. J Cell Sci 127, 2407-2419, doi: 10.1242/jcs.130344 (2014).
51. Sibilia, M. et al. The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 75, 770-787, doi: 10.1111/j.1432-0436.2007.00238.x (2007).
52. Platt, F. M., Boland, B. & van der Spoel, A. C. The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J Cell Biol 199, 723-734, doi: 10.1083/jcb.201208152 (2012).
53. Boustany, R. M. Lysosomal storage diseases-the horizon expands. Nat Rev Neurol 9, 583-598, doi: 10.1038/nrneurol.2013.163 (2013).
54. Xu, Q. et al. PIPKIgamma targets to the centrosome and restrains centriole duplication. J Cell Sci 127, 1293-1305, doi: 10.1242/jcs.141465 (2014).