Bardet-Biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 11, 2008, Pages 4242-4246

  Berbari, Nicolas F ^a,b   Lewis, Jacqueline S ^a,b   Bishop, Georgia A ^a   Askwith, Candice C ^a   Mykytyn, Kirk ^a,b  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Melanin concentrating hormone receptor 1; Neuronal cilia; Obesity; Somatostatin receptor 3; Type III adenylyl cyclase

Indexed keywords

G PROTEIN COUPLED RECEPTOR; MELANIN CONCENTRATING HORMONE RECEPTOR 1; SOMATOSTATIN RECEPTOR 3; BARDET BIEDL SYNDROME 2 PROTEIN, MOUSE; BARDET-BIEDL SYNDROME 2 PROTEIN, MOUSE; BBS4 PROTEIN, MOUSE; MCH1R PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN; SOMATOSTATIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BARDET BIEDL SYNDROME; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CILIARY BODY; FEEDING BEHAVIOR; HYPERPHAGIA; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; ANIMAL; CELL CULTURE; EUKARYOTIC FLAGELLUM; GENETICS; METABOLISM; MOUSE MUTANT; MUTATION;

MUS;

ANIMALS; BARDET-BIEDL SYNDROME; CELLS, CULTURED; CILIA; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; PROTEINS; RECEPTORS, SOMATOSTATIN;

EID: 41949116864     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0711027105     Document Type: Article

References (43)

1. Wheatley DN, Wang AM, Strugnell GE (1996) Expression of primary cilia in mammalian cells. Cell Biol Int 20:73-81.
2. Pan J, Wang Q, Snell WJ (2005) Cilium-generated signaling and cilia-related disorders. Lab Invest 85:452-463.
3. Singla V, Reiter JF (2006) The primary cilium as the cell's antenna: Signaling at a sensory organelle. Science 313:629-633.
4. Marshall WF, Nonaka S (2006) Cilia: Tuning in to the cell's antenna. Curr Biol 16:R604-R614.
5. Eggenschwiler JT, Anderson KV (2007) Cilia and developmental signaling. Annu Rev Cell Dev Biol 23:345-373.
6. Praetorius HA, Spring KR (2001) Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 184:71-79.
7. Nauli SM, et al. (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33:129-137.
8. Hildebrandt F, Otto E (2005) Cilia and centrosomes: A unifying pathogenic concept for cystic kidney disease? Nat Rev Genet 6:928-940.
9. Davenport JR, Yoder BK (2005) An incredible decade for the primary cilium: A look at a once-forgotten organelle. Am J Physiol 289:F1159-F1169.
10. Fliegauf M, Benzing T, Omran H (2007) When cilia go bad: Cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8:880-893.
11. Tobin JL, Beales PL (2007) Bardet-Biedl syndrome: Beyond the cilium. Pediatr Nephrol 22:926-936.
12. Blacque OE, Leroux MR (2006) Bardet-Biedl syndrome: An emerging pathomechanism of intracellular transport. Cell Mol Life Sci 63:2145-2161.
13. Nachury MV, et al. (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129:1201-1213.
14. Dahl HA (1963) Fine structure of cilia in rat cerebral cortex. Z Zellforsch Mikrosk Anat 60:369-386.
15. Handel M, et al. (1999) Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89:909-926.
16. Hamon M, et al. (1999) Antibodies and antisense oligonucleotide for probing the distribution and putative functions of central 5-HT6 receptors. Neuropsychopharmacology 21:68S-76S.
17. Brailov I, et al. (2000) Localization of 5-HT(6) receptors at the plasma membrane of neuronal cilia in the rat brain. Brain Res 872:271-275.
18. Badano JL, Mitsuma N, Beales PL, Katsanis N (2006) The ciliopathies: An emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 7:125-148.
19. Bishop GA, Berbari NF, Lewis JS, Mykytyn K (2007) Type III adenylyl cyclase localizes to primary cilia throughout the adult mouse brain. J Comp Neurol 505:562-571.
20. Berbari NF, Bishop GA, Askwith CC, Lewis JS, Mykytyn K (2007) Hippocampal neurons possess primary cilia in culture. J Neurosci Res 85:1095-1100.
21. Pissios P, Bradley RL, Maratos-Flier E (2006) Expanding the scales: The multiple roles of MCH in regulating energy balance and other biological functions. Endocr Rev 27:606-620.
22. Marszalek JR, et al. (2000) Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102:175-187.
23. Dwyer ND, Adler CE, Crump JG, L'Etoile ND, Bargmann CI (2001) Polarized dendritic transport and the AP-1 mu1 clathrin adaptor UNC-101 localize odorant receptors to olfactory cilia. Neuron 31:277-287.
24. Qin H, et al. (2005) Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane. Curr Biol 15:1695-1699.
25. McEwen DP, et al. (2007) Hypomorphic CEP290/NPHP6 mutations result in anosmia caused by the selective loss of G proteins in cilia of olfactory sensory neurons. Proc Natl Acad Sci USA 104:15917-15922.
26. den Hollander AI, et al. (2006) Mutations in the CEP290 (NPHP6) gene are a frequent cause of Leber congenital amaurosis. Am J Hum Genet 79:556-561.
27. Nishimura DY, 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.
28. Abd-El-Barr MM, et al. (2007) Impaired photoreceptor protein transport and synaptic transmission in a mouse model of Bardet-Biedl syndrome. Vision Res 47:3394-3407.
29. Fath MA, et al. (2005) Mkks-null mice have a phenotype resembling Bardet-Biedl syndrome. Hum Mol Genet 14:1109-1118.
30. Ross AJ, et al. (2005) Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat Genet 37:1135-1140.
31. Kulaga HM, et al. (2004) Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat Genet 36:994-998.
32. Kim JC, 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.
33. Tan PL, et al. (2007) From the cover: Loss of Bardet-Biedl syndrome proteins causes defects in peripheral sensory innervation and function. Proc Natl Acad Sci USA 104:17524-17529.
34. Patel YC (1999) Somatostatin and its receptor family. Front Neuroendocrinol 20:157-198.
35. Weckbecker G, et al. (2003) Opportunities in somatostatin research: Biological, chemical and therapeutic aspects. Nat Rev Drug Discov 2:999-1017.
36. Qu D, et al. (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380:243-247.
37. Borowsky B, et al. (2002) Antidepressant, anxiolytic and anorectic effects of a melanin-concentrating hormone-1 receptor antagonist. Nat Med 8:825-830.
38. Ludwig DS, et al. (2001) Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J Clin Invest 107:379-386.
39. Shimada M, Tritos NA, Lowell BB, Flier JS, Maratos-Flier E (1998) Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature 396:670-674.
40. Chen Y, et al. (2002) Targeted disruption of the melanin-concentrating hormone receptor-1 results in hyperphagia and resistance to diet-induced obesity. Endocrinology 143:2469-2477.
41. Davenport JR, et al. (2007) Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr Biol 17:1586-1594.
42. Mykytyn K, et al. (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.
43. Berbari NF, Johnson AD, Lewis JS, Askwith CC, Mykytyn K (2008) Identification of Ciliary Localization Sequences within the Third Intracellular Loop of G Protein-Coupled Receptors. Mol Biol Cell, in press.