Hyperactive neuroendocrine secretion causes size, feeding, and metabolic defects of C. elegans bardet-biedl syndrome mutants

PLoS Biology

Volumn 9, Issue 12, 2011, Pages

  Lee, Brian H ^a   Liu, Jason ^a   Wong, Daisy ^a   Srinivasan, Supriya ^b   Ashrafi, Kaveh ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARDET BIEDL SYNDROME PROTEIN; BIOGENIC AMINE; CAENORHABDITIS ELEGANS PROTEIN; COMPLEMENTARY DNA; LYMPHOID ENHANCER FACTOR 1; NEUROPEPTIDE; RAB PROTEIN; RAB27A PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; FLP 1 PROTEIN, C ELEGANS; FLP-1 PROTEIN, C ELEGANS; IDA 1 PROTEIN, C ELEGANS; IDA-1 PROTEIN, C ELEGANS; INSULIN; MEMBRANE PROTEIN; PROTEIN TYROSINE PHOSPHATASE; SEROTONIN;

ARTICLE; BARDET BIEDL SYNDROME; BODY SIZE; CAENORHABDITIS ELEGANS; CELL VACUOLE; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; EUKARYOTIC FLAGELLUM; EXOCYTOSIS; FEEDING DISORDER; INSULIN RELEASE; METABOLIC DISORDER; NEUROENDOCRINE DISEASE; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; FEEDING BEHAVIOR; GENETICS; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; SECRETION;

ANIMALIA; CAENORHABDITIS ELEGANS;

ANIMALS; BARDET-BIEDL SYNDROME; BODY SIZE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE; CILIA; FEEDING BEHAVIOR; INSULIN; MEMBRANE GLYCOPROTEINS; MICE; NEUROPEPTIDES; PROTEIN TYROSINE PHOSPHATASES; SEROTONIN;

EID: 84855179325     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001219     Document Type: Article

References (54)

1. Beales P. L, Elcioglu N, Woolf A. S, Parker D, Flinter F. A, (1999) New criteria for improved diagnosis of Bardet-Biedl syndrome: results of a population survey. J Med Genet 36: 437-446.
2. Baker K, Beales P. L, (2009) Making sense of cilia in disease: the human ciliopathies. American Journal of Medical Genetics Part C, Seminars in Medical Genetics 151C: 281-295.
3. Zaghloul N. A, Katsanis N, (2009) Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy. J Clin Invest 119: 428-437.
4. Nachury M. V, Loktev A. V, Zhang Q, Westlake C. J, Peränen J, et al. (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129: 1201-1213.
5. Jin H, White S. R, Shida T, Schulz S, Aguiar M, et al. The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 141: 1208-1219.
6. Berbari N. F, Lewis J. S, Bishop G. A, Askwith C. C, 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.
7. Lechtreck K-F, Johnson E. C, Sakai T, Cochran D, Ballif B. A, et al. (2009) The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J Cell Biol 187: 1117-1132.
8. Ansley S. J, Badano J. L, Blacque O. E, Hill J, Hoskins B. E, et al. (2003) Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425: 628-633.
9. Tan P. L, Barr T, Inglis P. N, Mitsuma N, Huang S. M, et al. (2007) Loss of Bardet Biedl syndrome proteins causes defects in peripheral sensory innervation and function. Proc Natl Acad Sci U S A 104: 17524-17529.
10. Seo S, Guo D-F, Bugge K, Morgan D. A, Rahmouni K, et al. (2009) Requirement of Bardet-Biedl syndrome proteins for leptin receptor signaling. Hum Mol Genet 18: 1323-1331.
11. Rahmouni K, Fath M. A, Seo S, Thedens D. R, Berry C. J, et al. (2008) Leptin resistance contributes to obesity and hypertension in mouse models of Bardet-Biedl syndrome. J Clin Invest 118: 1458-1467.
12. Davenport J. R, Watts A. J, Roper V. C, Croyle M. J, van Groen T, et al. (2007) Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr Biol 17: 1586-1594.
13. Nishimura D. Y, Fath M, Mullins R. F, Searby C, Andrews M, 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 U S A 101: 16588-16593.
14. Eichers E. R, Abd-El-Barr M. M, Paylor R, Lewis R. A, Bi W, et al. (2006) Phenotypic characterization of Bbs4 null mice reveals age-dependent penetrance and variable expressivity. Hum Genet 120: 211-226.
15. Bargmann C. I, (2006) Chemosensation in C. elegans. WormBook pp. 1-29.
16. Greer E. R, Pérez C. L, Van Gilst M. R, Lee B. H, Ashrafi K, (2008) Neural and molecular dissection of a C. elegans sensory circuit that regulates fat and feeding. Cell Metab 8: 118-131.
17. Srinivasan S, Sadegh L, Elle I. C, Christensen A. G. L, Faergeman N. J, et al. (2008) Serotonin regulates C. elegans fat and feeding through independent molecular mechanisms. Cell Metab 7: 533-544.
18. Blacque O. E, Reardon M. J, Li C, McCarthy J, Mahjoub M. R, 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.
19. Ou G, Blacque O. E, Snow J. J, Leroux M. R, Scholey J. M, (2005) Functional coordination of intraflagellar transport motors. Nature 436: 583-587.
20. Pierce S. B, Costa M, Wisotzkey R, Devadhar S, Homburger S. A, et al. (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev 15: 672-686.
21. Lee B. H, Ashrafi K, (2008) A TRPV channel modulates C. elegans neurosecretion, larval starvation survival, and adult lifespan. PLoS Genet 4: e1000213 doi:10.1371/journal.pgen.1000213.
22. Kao G, Nordenson C, Still M, Rönnlund A, Tuck S, et al. (2007) ASNA-1 positively regulates insulin secretion in C. elegans and mammalian cells. Cell 128: 577-587.
23. Sieburth D, Madison J. M, Kaplan J. M, (2007) PKC-1 regulates secretion of neuropeptides. Nat Neurosci 10: 49-57.
24. Perkins L. A, Hedgecock E. M, Thomson J. N, Culotti J. G, (1986) Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117: 456-487.
25. Hu P. J, (2007) Dauer. WormBook pp. 1-19.
26. Gracheva E. O, Burdina A. O, Touroutine D, Berthelot-Grosjean M, Parekh H, et al. (2007) Tomosyn negatively regulates both synaptic transmitter and neuropeptide release at the C. elegans neuromuscular junction. J Physiol (Lond) 585: 705-709.
27. Vowels J. J, Thomas J. H, (1992) Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130: 105-123.
28. Rogers C, Reale V, Kim K, Chatwin H, Li C, et al. (2003) Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat Neurosci 6: 1178-1185.
29. Gerdes J. M, Liu Y, Zaghloul N. A, Leitch C. C, Lawson S. S, et al. (2007) Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat Genet 39: 1350-1360.
30. Ann K, Kowalchyk J. A, Loyet K. M, Martin T. F, (1997) Novel Ca2+-binding protein (CAPS) related to UNC-31 required for Ca2+-activated exocytosis. J Biol Chem 272: 19637-19640.
31. Mukhopadhyay S, Lu Y, Shaham S, Sengupta P, (2008) Sensory signaling-dependent remodeling of olfactory cilia architecture in C. elegans. Dev Cell 14: 762-774.
32. Mahoney T. R, Liu Q, Itoh T, Luo S, Hadwiger G, et al. (2006) Regulation of synaptic transmission by RAB-3 and RAB-27 in Caenorhabditis elegans. Mol Biol Cell 17: 2617-2625.
33. Ch'ng Q, Sieburth D, Kaplan J. M, (2008) Profiling synaptic proteins identifies regulators of insulin secretion and lifespan. PLoS Genet 4: e1000283 doi:10.1371/journal.pgen.1000283.
34. Zahn T. R, Angleson J. K, MacMorris M. A, Domke E, Hutton J. F, et al. (2004) Dense core vesicle dynamics in Caenorhabditis elegans neurons and the role of kinesin UNC-104. Traffic 5: 544-559.
35. Williams C. L, Li C, Kida K, Inglis P. N, Mohan S, et al. 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.
36. Starich T. A, Herman R. K, Kari C. K, Yeh W. H, Schackwitz W. S, et al. (1995) Mutations affecting the chemosensory neurons of Caenorhabditis elegans. Genetics 139: 171-188.
37. Chen N, Mah A, Blacque O. E, Chu J, Phgora K, et al. (2006) Identification of ciliary and ciliopathy genes in Caenorhabditis elegans through comparative genomics. Genome Biol 7: R126.
38. Mak H. Y, Nelson L. S, Basson M, Johnson C. D, Ruvkun G, (2006) Polygenic control of Caenorhabditis elegans fat storage. Nat Genet 38: 363-368.
39. Moussaif M, Sze J. Y, (2009) Intraflagellar transport/Hedgehog-related signaling components couple sensory cilium morphology and serotonin biosynthesis in Caenorhabditis elegans. J Neurosci 29: 4065-4075.
40. Mykytyn K, Mullins R. F, Andrews M, Chiang A. P, Swiderski R. E, 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 U S A 101: 8664-8669.
41. Fujiwara M, Sengupta P, McIntire S. L, (2002) Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36: 1091-1102.
42. Davis L, Barbera M, McDonnell A, McIntyre K, Sternglanz R, et al. (2001) The Saccharomyces cerevisiae MUM2 gene interacts with the DNA replication machinery and is required for meiotic levels of double strand breaks. Genetics 157: 1179-1189.
43. Mullaney B. C, Blind R. D, Lemieux G. A, Perez C. L, Elle I. C, et al. Regulation of C. elegans fat uptake and storage by Acyl-CoA synthase-3 is dependent on NR5A family nuclear hormone receptor nhr-25. Cell Metab 12: 398-410.
44. Lemieux G. A, Liu J, Mayer N, Bainton R. J, Ashrafi K, et al. A whole-organism screen identifies new regulators of fat storage. Nat Chem Biol 7: 206-213.
45. Jones K. T, Greer E. R, Pearce D, Ashrafi K, (2009) Rictor/TORC2 regulates Caenorhabditis elegans fat storage, body size, and development through sgk-1. PLoS Biol 7: e60 doi:10.1371/journal.pbio.1000060.
46. Avery L, (1993) The genetics of feeding in Caenorhabditis elegans. Genetics 133: 897-917.
47. Avery L, Horvitz H. R, (1990) Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J Exp Zool 253: 263-270.
48. Sze J. Y, Victor M, Loer C, Shi Y, Ruvkun G, (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560-564.
49. Feuillan P. P, Ng D, Han J. C, Sapp J. C, Wetsch K, et al. Patients with bardet-biedl syndrome have hyperleptinemia suggestive of leptin resistance. J Clin Endocrinol Metab 96: E528-E535.
50. Yen H-J, Tayeh M. K, Mullins R. F, Stone E. M, Sheffield V. C, 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.
51. Torayama I, Ishihara T, Katsura I, (2007) Caenorhabditis elegans integrates the signals of butanone and food to enhance chemotaxis to butanone. J Neurosci 27: 741-750.
52. Finetti F, Paccani S. R, Riparbelli M. G, Giacomello E, Perinetti G, et al. (2009) Intraflagellar transport is required for polarized recycling of the TCR/CD3 complex to the immune synapse. Nat Cell Biol 11: 1332-1339.
53. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
54. Van Gilst M. R, Hadjivassiliou H, Yamamoto K. R, (2005) A Caenorhabditis elegans nutrient response system partially dependent on nuclear receptor NHR-49. Proc Natl Acad Sci U S A 102: 13496-13501.