BBS proteins interact genetically with the IFT pathway to influence SHH-related phenotypes

Human Molecular Genetics

Volumn 21, Issue 9, 2012, Pages 1945-1953

  Zhang, Qihong ^a   Seo, Seongjin ^a   Bugge, Kevin ^a   Stone, Edwin M ^a   Sheffield, Val C ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARDET BIEDL SYNDROME 1 PROTEIN; BARDET BIEDL SYNDROME 2 PROTEIN; BARDET BIEDL SYNDROME 4 PROTEIN; BARDET BIEDL SYNDROME 5 PROTEIN; BARDET BIEDL SYNDROME 7 PROTEIN; BARDET BIEDL SYNDROME 8 PROTEIN; BARDET BIEDL SYNDROME 9 PROTEIN; PROTEIN; PROTEIN PATCHED 1; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BARDET BIEDL SYNDROME; CLEFT PALATE; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; EUKARYOTIC FLAGELLUM; EXENCEPHALY; FLAGELLUM; GENE INTERACTION; HEART EDEMA; HUMAN; INTRACELLULAR SIGNALING; INTRACELLULAR TRANSPORT; LIMB DEVELOPMENT; LIMB MALFORMATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; BARDET-BIEDL SYNDROME; CELLS, CULTURED; CILIA; FEMALE; HEDGEHOG PROTEINS; HUMANS; MALE; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MUTANT PROTEINS; PHENOTYPE; PREGNANCY; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA; MUS;

EID: 84859219770     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds004     Document Type: Article

References (57)

1. Badano, J.L., Ansley, S.J., Leitch, C.C., Lewis, R.A., Lupski, J.R. and Katsanis, N. (2003) Identification of a novel Bardet-Biedl syndrome protein, BBS7, that shares structural features with BBS1 and BBS2. Am. J. Hum. Genet., 72, 650-658.
2. Chiang, A.P., Beck, J.S., Yen, H.J., Tayeh, M.K., Scheetz, T.E., Swiderski, R.E., Nishimura, D.Y., Braun, T.A., Kim, K.Y., Huang, J. et al. (2006) Homozygosity mapping with SNP arrays identifies TRIM32, an E3 ubiquitin ligase, as a Bardet-Biedl syndrome gene (BBS11). Proc. Natl Acad. Sci. USA, 103, 6287-6292.
3. Chiang, A.P., Nishimura, D., Searby, C., Elbedour, K., Carmi, R., Ferguson, A.L., Secrist, J., Braun, T., Casavant, T., Stone, E.M. et al. (2004) Comparative genomic analysis identifies an ADP-ribosylation factor-like gene as the cause of Bardet-Biedl syndrome (BBS3). Am. J. Hum. Genet., 75, 475-484.
4. Fan, Y., Esmail, M.A., Ansley, S.J., Blacque, O.E., Boroevich, K., Ross, A.J., Moore, S.J., Badano, J.L., May-Simera, H., Compton, D.S. et al. (2004) Mutations in a member of the Ras superfamily of small GTP-binding proteins causes Bardet-Biedl syndrome. Nat. Genet., 36, 989-993.
5. Leitch, C.C., Zaghloul, N.A., Davis, E.E., Stoetzel, C., Diaz-Font, A., Rix, S., Alfadhel, M., Lewis, R.A., Eyaid, W., Banin, E. et al. (2008) Hypomorphic mutations in syndromic encephalocele genes are associated with Bardet-Biedl syndrome. Nat. Genet., 40, 443-448.
6. Li, J.B., Gerdes, J.M., Haycraft, C.J., Fan, Y., Teslovich, T.M., May-Simera, H., Li, H., Blacque, O.E., Li, L., Leitch, C.C. et al. (2004) Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell, 117, 541-552.
7. Mykytyn, K., Braun, T., Carmi, R., Haider, N.B., Searby, C.C., Shastri, M., Beck, G., Wright, A.F., Iannaccone, A., Elbedour, K. et al. (2001) Identification of the gene that, when mutated, causes the human obesity syndrome BBS4. Nat. Genet., 28, 188-191.
8. Mykytyn, K., Nishimura, D.Y., Searby, C.C., Shastri, M., Yen, H.J., Beck, J.S., Braun, T., Streb, L.M., Cornier, A.S., Cox, G.F. et al. (2002) Identification of the gene (BBS1) most commonly involved in Bardet-Biedl syndrome, a complex human obesity syndrome. Nat. Genet., 31, 435-438.
9. Nishimura, D.Y., Searby, C.C., Carmi, R., Elbedour, K., Van Maldergem, L., Fulton, A.B., Lam, B.L., Powell, B.R., Swiderski, R.E., Bugge, K.E. et al. (2001) Positional cloning of a novel gene on chromosome 16q causing Bardet-Biedl syndrome (BBS2). Hum. Mol. Genet., 10, 865-874.
10. Nishimura, D.Y., Swiderski, R.E., Searby, C.C., Berg, E.M., Ferguson, A.L., Hennekam, R., Merin, S., Weleber, R.G., Biesecker, L.G., Stone, E.M. et al. (2005) Comparative genomics and gene expression analysis identifies BBS9, a new Bardet-Biedl syndrome gene. Am. J. Hum. Genet., 77, 1021-1033.
11. Stoetzel, C., Laurier, V., Davis, E.E., Muller, J., Rix, S., Badano, J.L., Leitch, C.C., Salem, N., Chouery, E., Corbani, S. et al. (2006) BBS10 encodes a vertebrate-specific chaperonin-like protein and is a major BBS locus. Nat. Genet., 38, 521-524.
12. Stoetzel, C., Muller, J., Laurier, V., Davis, E.E., Zaghloul, N.A., Vicaire, S., Jacquelin, C., Plewniak, F., Leitch, C.C., Sarda, P. et al. (2007) Identification of a novel BBS gene (BBS12) highlights the major role of a vertebrate-specific branch of chaperonin-related proteins in Bardet-Biedl syndrome. Am. J. Hum. Genet., 80, 1-11.
13. Kim, S.K., Shindo, A., Park, T.J., Oh, E.C., Ghosh, S., Gray, R.S., Lewis, R.A., Johnson, C.A., Attie-Bittach, T., Katsanis, N. et al. (2010) Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science, 329, 1337-1340.
14. Nachury, M.V., Loktev, A.V., Zhang, Q., Westlake, C.J., Peranen, J., Merdes, A., Slusarski, D.C., Scheller, R.H., Bazan, J.F., Sheffield, V.C. et al. (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell, 129, 1201-1213.
15. Berbari, N.F., Johnson, A.D., Lewis, J.S., Askwith, C.C. and Mykytyn, K. (2008) Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors. Mol. Biol. Cell, 19, 1540-1547.
16. Berbari, N.F., Lewis, J.S., Bishop, G.A., Askwith, C.C. and Mykytyn, K. (2008) 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.
17. Davis, R.E., Swiderski, R.E., Rahmouni, K., Nishimura, D.Y., Mullins, R.F., Agassandian, K., Philp, A.R., Searby, C.C., Andrews, M.P., Thompson, S. et al. (2007) A knockin mouse model of the Bardet-Biedl syndrome 1 M390R mutation has cilia defects, ventriculomegaly, retinopathy, and obesity. Proc. Natl Acad. Sci. USA, 104, 19422-19427.
18. Fath, M.A., Mullins, R.F., Searby, C., Nishimura, D.Y., Wei, J., Rahmouni, K., Davis, R.E., Tayeh, M.K., Andrews, M., Yang, B. et al. (2005) Mkks-null mice have a phenotype resembling Bardet-Biedl syndrome. Hum. Mol. Genet., 14, 1109-1118.
19. Mykytyn, K., Mullins, R.F., Andrews, M., Chiang, A.P., Swiderski, R.E., Yang, B., Braun, T., Casavant, T., Stone, E.M. and Sheffield, V.C. (2004) Bardet-Biedl syndrome type 4 (BBS4)-null mice implicate Bbs4 in flagella formation but not global cilia assembly. Proc. Natl Acad. Sci. USA, 101, 8664-8669.
20. Nishimura, D.Y., Fath, M., Mullins, R.F., Searby, C., Andrews, M., Davis, R., Andorf, J.L., Mykytyn, K., Swiderski, R.E., Yang, B. et al. (2004) Bbs2-null mice have neurosensory deficits, a defect in social dominance, and retinopathy associated with mislocalization of rhodopsin. Proc. Natl Acad. Sci. USA, 101, 16588-16593.
21. Bai, C.B., Stephen, D. and Joyner, A.L. (2004) All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev. Cell, 6, 103-115.
22. Corbit, K.C., Shyer, A.E., Dowdle, W.E., Gaulden, J., Singla, V., Chen, M.H., Chuang, P.T. and Reiter, J.F. (2008) Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat. Cell Biol., 10, 70-76.
23. Haycraft, C.J., Banizs, B., Aydin-Son, Y., Zhang, Q., Michaud, E.J. and Yoder, B.K. (2005) Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet., 1, e53.
24. Huangfu, D., Liu, A., Rakeman, A.S., Murcia, N.S., Niswander, L. and Anderson, K.V. (2003) Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature, 426, 83-87.
25. Rohatgi, R., Milenkovic, L., Corcoran, R.B. and Scott, M.P. (2009) Hedgehog signal transduction by Smoothened: pharmacologic evidence for a 2-step activation process. Proc. Natl Acad. Sci. USA, 106, 3196-3201.
26. Rohatgi, R., Milenkovic, L. and Scott, M.P. (2007) Patched1 regulates hedgehog signaling at the primary cilium. Science, 317, 372-376.
27. Tran, P.V., Haycraft, C.J., Besschetnova, T.Y., Turbe-Doan, A., Stottmann, R.W., Herron, B.J., Chesebro, A.L., Qiu, H., Scherz, P.J., Shah, J.V. et al. (2008) THM1 negatively modulates mouse sonic hedgehog signal transduction and affects retrograde intraflagellar transport in cilia. Nat. Genet., 40, 403-410.
28. Gerdes, J.M., Liu, Y., Zaghloul, N.A., Leitch, C.C., Lawson, S.S., Kato, M., Beachy, P.A., Beales, P.L., DeMartino, G.N., Fisher, S. et al. (2007) Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat. Genet., 39, 1350-1360.
29. Marion, V., Stoetzel, C., Schlicht, D., Messaddeq, N., Koch, M., Flori, E., Danse, J.M., Mandel, J.L. and Dollfus, H. (2009) Transient ciliogenesis involving Bardet-Biedl syndrome proteins is a fundamental characteristic of adipogenic differentiation. Proc. Natl Acad. Sci. USA, 106, 1820-1825.
30. Ross, A.J., May-Simera, H., Eichers, E.R., Kai, M., Hill, J., Jagger, D.J., Leitch, C.C., Chapple, J.P., Munro, P.M., Fisher, S. et al. (2005) Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet., 37, 1135-1140.
31. Wiens, C.J., Tong, Y., Esmail, M.A., Oh, E., Gerdes, J.M., Wang, J., Tempel, W., Rattner, J.B., Katsanis, N., Park, H.W. et al. (2010) Bardet-Biedl syndrome-associated small GTPase ARL6 (BBS3) functions at or near the ciliary gate and modulates Wnt signaling. J. Biol. Chem., 285, 16218-16230.
32. Villavicencio, E.H., Walterhouse, D.O. and Iannaccone, P.M. (2000) The sonic hedgehog-patched-gli pathway in human development and disease. Am. J. Hum. Genet., 67, 1047-1054.
33. Lechtreck, K.F., Johnson, E.C., Sakai, T., Cochran, D., Ballif, B.A., Rush, J., Pazour, G.J., Ikebe, M. and Witman, G.B. (2009) The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J. Cell Biol., 187, 1117-1132.
34. Yen, H.J., Tayeh, M.K., Mullins, R.F., Stone, E.M., Sheffield, V.C. and Slusarski, D.C. (2006) Bardet-Biedl syndrome genes are important in retrograde intracellular trafficking and Kupffer's vesicle cilia function. Hum. Mol. Genet., 15, 667-677.
35. Varjosalo, M., Li, S.P. and Taipale, J. (2006) Divergence of hedgehog signal transduction mechanism between Drosophila and mammals. Dev. Cell, 10, 177-186.
36. Zhao, Y., Tong, C. and Jiang, J. (2007) Hedgehog regulates smoothened activity by inducing a conformational switch. Nature, 450, 252-258.
37. Pazour, G.J., San Agustin, J.T., Follit, J.A., Rosenbaum, J.L. and Witman, G.B. (2002) Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Curr. Biol., 12, R378-R380.
38. Zhang, Q., Murcia, N.S., Chittenden, L.R., Richards, W.G., Michaud, E.J., Woychik, R.P. and Yoder, B.K. (2003) Loss of the Tg737 protein results in skeletal patterning defects. Dev. Dyn., 227, 78-90.
39. Cano, D.A., Murcia, N.S., Pazour, G.J. and Hebrok, M. (2004) Orpk mouse model of polycystic kidney disease reveals essential role of primary cilia in pancreatic tissue organization. Development, 131, 3457-3467.
40. Moyer, J.H., Lee-Tischler, M.J., Kwon, H.Y., Schrick, J.J., Avner, E.D., Sweeney, W.E., Godfrey, V.L., Cacheiro, N.L., Wilkinson, J.E. and Woychik, R.P. (1994) Candidate gene associated with a mutation causing recessive polycystic kidney disease in mice. Science, 264, 1329-1333.
41. Zhang, Q., Davenport, J.R., Croyle, M.J., Haycraft, C.J. and Yoder, B.K. (2005) Disruption of IFT results in both exocrine and endocrine abnormalities in the pancreas of Tg737(orpk) mutant mice. Lab. Invest., 85, 45-64.
42. Loktev, A.V., Zhang, Q., Beck, J.S., Searby, C.C., Scheetz, T.E., Bazan, J.F., Slusarski, D.C., Sheffield, V.C., Jackson, P.K. and Nachury, M.V. (2008) A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev. Cell, 15, 854-865.
43. Corbit, K.C., Aanstad, P., Singla, V., Norman, A.R., Stainier, D.Y. and Reiter, J.F. (2005) Vertebrate Smoothened functions at the primary cilium. Nature, 437, 1018-1021.
44. Qin, J., Lin, Y., Norman, R.X., Ko, H.W. and Eggenschwiler, J.T. (2011) Intraflagellar transport protein 122 antagonizes Sonic Hedgehog signaling and controls ciliary localization of pathway components. Proc. Natl Acad. Sci. USA, 108, 1456-1461.
45. Huang, P. and Schier, A.F. (2009) Dampened hedgehog signaling but normal Wnt signaling in zebrafish without cilia. Development, 136, 3089-3098.
46. Ocbina, P.J., Tuson, M. and Anderson, K.V. (2009) Primary cilia are not required for normal canonical Wnt signaling in the mouse embryo. PLoS One, 4, 1-8.
47. Sugiyama, N., Tsukiyama, T., Yamaguchi, T.P. and Yokoyama, T. (2011) The canonical Wnt signaling pathway is not involved in renal cyst development in the kidneys of inv mutant mice. Kidney Int., 79, 957-965.
48. Lancaster, M.A., Gopal, D.J., Kim, J., Saleem, S.N., Silhavy, J.L., Louie, C.M., Thacker, B.E., Williams, Y., Zaki, M.S. and Gleeson, J.G. (2011) Defective Wnt-dependent cerebellar midline fusion in a mouse model of Joubert syndrome. Nat. Med., 17, 726-731.
49. Lancaster, M.A., Louie, C.M., Silhavy, J.L., Sintasath, L., Decambre, M., Nigam, S.K., Willert, K. and Gleeson, J.G. (2009) Impaired Wnt-beta-catenin signaling disrupts adult renal homeostasis and leads to cystic kidney ciliopathy. Nat. Med., 15, 1046-1054.
50. McDermott, K.M., Liu, B.Y., Tlsty, T.D. and Pazour, G.J. (2010) Primary cilia regulate branching morphogenesis during mammary gland development. Curr. Biol., 20, 731-737.
51. Simons, M., Gloy, J., Ganner, A., Bullerkotte, A., Bashkurov, M., Kronig, C., Schermer, B., Benzing, T., Cabello, O.A., Jenny, A. et al. (2005) Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch betweenWnt signaling pathways. Nat. Genet., 37, 537-543.
52. Ocbina, P.J., Eggenschwiler, J.T., Moskowitz, I. and Anderson, K.V. (2011) Complex interactions between genes controlling trafficking in primary cilia. Nat. Genet., 43, 547-553.
53. Blacque, O.E., Reardon, M.J., Li, C., McCarthy, J., Mahjoub, M.R., Ansley, S.J., Badano, J.L., Mah, A.K., Beales, P.L., Davidson, W.S. et al. (2004) Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. Genes Dev., 18, 1630-1642.
54. Chen, M.H., Wilson, C.W., Li, Y.J., Law, K.K., Lu, C.S., Gacayan, R., Zhang, X., Hui, C.C. and Chuang, P.T. (2009) Cilium-independent regulation of Gli protein function by Sufu in hedgehog signaling is evolutionarily conserved. Genes Dev., 23, 1910-1928.
55. Humke, E.W., Dorn, K.V., Milenkovic, L., Scott, M.P. and Rohatgi, R. (2010) The output of hedgehog signaling is controlled by the dynamic association between suppressor of fused and the Gli proteins. Genes Dev., 24, 670-682.
56. Tukachinsky, H., Lopez, L.V. and Salic, A. (2010) A mechanism for vertebrate hedgehog signaling: recruitment to cilia and dissociation of SuFu-Gli protein complexes. J. Cell Biol., 191, 415-428.
57. Lum, L., Zhang, C., Oh, S., Mann, R.K., von Kessler, D.P., Taipale, J., Weis-Garcia, F., Gong, R., Wang, B. and Beachy, P.A. (2003) Hedgehog signal transduction via smoothened association with a cytoplasmic complex scaffolded by the atypical kinesin, Costal-2. Mol. Cell, 12, 1261-1274