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Neuronal Cilia and Obesity

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Abstract

Obesity is an emerging public health concern that has numerous secondary health consequences, including heart disease, high blood pressure, diabetes mellitus, osteoarthritis, and overall reduced quality of life. Historically, obesity has been viewed as increased body fat caused by overconsumption of food, combined with the sedentary lifestyle of modern society. Simply put, energy input exceeds energy output, creating an excess in fat mass. This viewpoint largely focuses on environmental and social factors in the obesity epidemic. However, it fails to take into account a growing body of evidence from several monogenetic human obesity disorders and mutant mouse and rat obesity models that indicate a profound role for genetic factors. Although most of these monogenetic human conditions are rare, it is clear that the study of their molecular and cellular etiology will offer insights into the mechanisms that regulate appetite and satiety. The objectives of this review are to discuss how mutations in genes required for the formation or function of the cilium result in obesity in human and mouse models and how the cilium may function to regulate appetite and satiation responses.

Authors Nicolas F. Berbari and Raymond C. Pasek contributed equally to this work.

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References

  • Abu-Safieh L, Al-Anazi S, Al-Abdi L, Hashem M, Alkuraya H, Alamr M, Sirelkhatim MO, Al-Hassnan Z, Alkuraya B, Mohamed JY, Al-Salem A, Alrashed M, Faqeih E, Softah A, Al-Hashem A, Wali S, Rahbeeni Z, Alsayed M, Khan AO, Al-Gazali L, Taschner PE, Al-Hazzaa S, Alkuraya FS (2012) In search of triallelism in Bardet-Biedl syndrome. Eur J Hum Genet 20:420–427

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Bolado G, Paul FA, Blaess S (2012) Sonic hedgehog lineage in the mouse hypothalamus: from progenitor domains to hypothalamic regions. Neural Dev 7:4

    Article  PubMed  Google Scholar 

  • Ansley SJ, Badano JL, Blacque OE, Hill J, Hoskins BE, Leitch CC, Kim JC, Ross AJ, Eichers ER, Teslovich TM, Mah AK, Johnsen RC, Cavender JC, Lewis RA, Leroux MR, Beales PL, Katsanis N (2003) Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425:628–633

    Article  PubMed  CAS  Google Scholar 

  • Aponte G, Leung P, Gross D, Yamada T (1984) Effects of somatostatin on food intake in rats. Life Sci 35:741–746

    Article  PubMed  CAS  Google Scholar 

  • Arsov T, Silva DG, O’Bryan MK, Sainsbury A, Lee NJ, Kennedy C, Manji SS, Nelms K, Liu C, Vinuesa CG, de Kretser DM, Goodnow CC, Petrovsky N (2006) Fat aussie – a new Alstrom syndrome mouse showing a critical role for ALMS1 in obesity, diabetes, and spermatogenesis. Mol Endocrinol 20:1610–1622

    Article  PubMed  CAS  Google Scholar 

  • Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, Ahringer J, Ruvkun G (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421:268–272

    Article  PubMed  CAS  Google Scholar 

  • Badano JL, Ansley SJ, Leitch CC, Lewis RA, Lupski JR, 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

    Article  PubMed  CAS  Google Scholar 

  • Bardet G (1920) Sur un syndrome d’obesite’ congenitale avec polydactylie et retinite pigmentaire (contribution a l’etude des formes cliniques de l’obesite hypophysaire). University of Paris, Paris

    Google Scholar 

  • Beales PL, Warner AM, Hitman GA, Thakker R, Flinter FA (1997) Bardet-Biedl syndrome: a molecular and phenotypic study of 18 families. J Med Genet 34:92–98

    Article  PubMed  CAS  Google Scholar 

  • Beales PL, Elcioglu N, Woolf AS, Parker D, Flinter FA (1999) New criteria for improved diagnosis of Bardet-Biedl syndrome: results of a population survey. J Med Genet 36:437–446

    PubMed  CAS  Google Scholar 

  • Belgacem YH, Borodinsky LN (2011) Sonic hedgehog signaling is decoded by calcium spike activity in the developing spinal cord. Proc Natl Acad Sci USA 108:4482–4487

    Article  PubMed  CAS  Google Scholar 

  • Bell PD, Fitzgibbon W, Sas K, Stenbit AE, Amria M, Houston A, Reichert R, Gilley S, Siegal GP, Bissler J, Bilgen M, Chou PC, Guay-Woodford L, Yoder B, Haycraft CJ, Siroky B (2011) Loss of primary cilia upregulates renal hypertrophic signaling and promotes cystogenesis. J Am Soc Nephrol 22:839–848

    Article  PubMed  Google Scholar 

  • 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 USA 105:4242–4246

    Article  PubMed  CAS  Google Scholar 

  • Berbari NF, O’Connor AK, Haycraft CJ, Yoder BK (2009) The primary cilium as a complex signaling center. Curr Biol 19:R526–R535

    Article  PubMed  CAS  Google Scholar 

  • Bezard E, Baufreton J, Owens G, Crossman AR, Dudek H, Taupignon A, Brotchie JM (2003) Sonic hedgehog is a neuromodulator in the adult subthalamic nucleus. FASEB J 17:2337–2338

    PubMed  CAS  Google Scholar 

  • Biedl A (1922) Geschwisterpaar mit adipose-genitaler Dystrophie. Dtsch Med Wochenschr 48:1630

    Google Scholar 

  • Bishop GA, Berbari NF, Lewis J, Mykytyn K (2007) Type III adenylyl cyclase localizes to primary cilia throughout the adult mouse brain. J Comp Neurol 505:562–571

    Article  PubMed  Google Scholar 

  • Blacque OE, Reardon MJ, Li C, McCarthy J, Mahjoub MR, Ansley SJ, Badano JL, Mah AK, Beales PL, Davidson WS, Johnsen RC, Audeh M, Plasterk RH, Baillie DL, Katsanis N, Quarmby LM, Wicks SR, Leroux MR (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

    Article  PubMed  CAS  Google Scholar 

  • Boehlke C, Kotsis F, Patel V, Braeg S, Voelker H, Bredt S, Beyer T, Janusch H, Hamann C, Godel M, Muller K, Herbst M, Hornung M, Doerken M, Kottgen M, Nitschke R, Igarashi P, Walz G, Kuehn EW (2010) Primary cilia regulate mTORC1 activity and cell size through Lkb1. Nat Cell Biol 12:1115–1122

    Article  PubMed  CAS  Google Scholar 

  • Borowsky B, Durkin MM, Ogozalek K, Marzabadi MR, DeLeon J, Lagu B, Heurich R, Lichtblau H, Shaposhnik Z, Daniewska I, Blackburn TP, Branchek TA, Gerald C, Vaysse PJ, Forray C (2002) Antidepressant, anxiolytic and anorectic effects of a melanin-concentrating hormone-1 receptor antagonist. Nat Med 8:825–830

    PubMed  CAS  Google Scholar 

  • Brailov I, Bancila M, Brisorgueil MJ, Miquel MC, Hamon M, Verge D (2000) Localization of 5-HT(6) receptors at the plasma membrane of neuronal cilia in the rat brain. Brain Res 872:271–275

    Article  PubMed  CAS  Google Scholar 

  • Breunig JJ, Sarkisian MR, Arellano JI, Morozov YM, Ayoub AE, Sojitra S, Wang B, Flavell RA, Rakic P, Town T (2008) Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc Natl Acad Sci USA 105:13127–13132

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Hu C, Hsu CK, Zhang Q, Bi C, Asnicar M, Hsiung HM, Fox N, Slieker LJ, Yang DD, Heiman ML, Shi Y (2002) Targeted disruption of the melanin-concentrating hormone receptor-1 results in hyperphagia and resistance to diet-induced obesity. Endocrinology 143:2469–2477

    Article  PubMed  CAS  Google Scholar 

  • Chen J, Smaoui N, Hammer MB, Jiao X, Riazuddin SA, Harper S, Katsanis N, Riazuddin S, Chaabouni H, Berson EL, Hejtmancik JF (2011) Molecular analysis of Bardet-Biedl syndrome families: report of 21 novel mutations in 10 genes. Invest Ophthalmol Vis Sci 52:5317–5324

    Article  PubMed  CAS  Google Scholar 

  • Chiang AP, Nishimura D, Searby C, Elbedour K, Carmi R, Ferguson AL, Secrist J, Braun T, Casavant T, Stone EM, Sheffield VC (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

    Article  PubMed  CAS  Google Scholar 

  • Chiang AP, Beck JS, Yen HJ, Tayeh MK, Scheetz TE, Swiderski RE, Nishimura DY, Braun TA, Kim KY, Huang J, Elbedour K, Carmi R, Slusarski DC, Casavant TL, Stone EM, Sheffield VC (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

    Article  PubMed  CAS  Google Scholar 

  • Chizhikov VV, Davenport J, Zhang Q, Shih EK, Cabello OA, Fuchs JL, Yoder BK, Millen KJ (2007) Cilia proteins control cerebellar morphogenesis by promoting expansion of the granule progenitor pool. J Neurosci 27:9780–9789

    Article  PubMed  CAS  Google Scholar 

  • Coleman DL, Eicher EM (1990) Fat (fat) and tubby (tub): two autosomal recessive mutations causing obesity syndromes in the mouse. J Hered 81:424–427

    PubMed  CAS  Google Scholar 

  • Collin GB, Marshall JD, Ikeda A, So WV, Russell-Eggitt I, Maffei P, Beck S, Boerkoel CF, Sicolo N, Martin M, Nishina PM, Naggert JK (2002) Mutations in ALMS1 cause obesity, type 2 diabetes and neurosensory degeneration in Alstrom syndrome. Nat Genet 31:74–78

    PubMed  CAS  Google Scholar 

  • Collin GB, Cyr E, Bronson R, Marshall JD, Gifford EJ, Hicks W, Murray SA, Zheng QY, Smith RS, Nishina PM, Naggert JK (2005) Alms1-disrupted mice recapitulate human Alstrom syndrome. Hum Mol Genet 14:2323–2333

    Article  PubMed  CAS  Google Scholar 

  • Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL et al (1996) Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 334:292–295

    Article  PubMed  CAS  Google Scholar 

  • Cota D, Proulx K, Smith KA, Kozma SC, Thomas G, Woods SC, Seeley RJ (2006) Hypothalamic mTOR signaling regulates food intake. Science 312:927–930

    Article  PubMed  CAS  Google Scholar 

  • Craige B, Tsao CC, Diener DR, Hou Y, Lechtreck KF, Rosenbaum JL, Witman GB (2010) CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 190:927–940

    Article  PubMed  CAS  Google Scholar 

  • Croft JB, Morrell D, Chase CL, Swift M (1995) Obesity in heterozygous carriers of the gene for the Bardet-Biedl syndrome. Am J Med Genet 55:12–15

    Article  PubMed  CAS  Google Scholar 

  • Davenport JR, Watts AJ, Roper VC, Croyle MJ, van Groen T, Wyss JM, Nagy TR, Kesterson RA, Yoder BK (2007) Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr Biol 17:1586–1594

    Article  PubMed  CAS  Google Scholar 

  • Davis RE, Swiderski RE, Rahmouni K, Nishimura DY, Mullins RF, Agassandian K, Philp AR, Searby CC, Andrews MP, Thompson S, Berry CJ, Thedens DR, Yang B, Weiss RM, Cassell MD, Stone EM, Sheffield VC (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

    Article  PubMed  CAS  Google Scholar 

  • Dazert E, Hall MN (2011) mTOR signaling in disease. Curr Opin Cell Biol 23:744–755

    Article  PubMed  CAS  Google Scholar 

  • Deffert C, Niel F, Mochel F, Barrey C, Romana C, Souied E, Stoetzel C, Goossens M, Dollfus H, Verloes A, Girodon E, Gerard-Blanluet M (2007) Recurrent insertional polydactyly and situs inversus in a Bardet-Biedl syndrome family. Am J Med Genet A 143:208–213

    PubMed  Google Scholar 

  • Domire JS, Green JA, Lee KG, Johnson AD, Askwith CC, Mykytyn K (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

    Article  PubMed  CAS  Google Scholar 

  • Eichers ER, Abd-El-Barr MM, Paylor R, Lewis RA, Bi W, Lin X, Meehan TP, Stockton DW, Wu SM, Lindsay E, Justice MJ, Beales PL, Katsanis N, Lupski JR (2006) Phenotypic characterization of Bbs4 null mice reveals age-dependent penetrance and variable expressivity. Hum Genet 120:211–226

    Article  PubMed  CAS  Google Scholar 

  • Fath MA, Mullins RF, Searby C, Nishimura DY, Wei J, Rahmouni K, Davis RE, Tayeh MK, Andrews M, Yang B, Sigmund CD, Stone EM, Sheffield VC (2005) Mkks-null mice have a phenotype resembling Bardet-Biedl syndrome. Hum Mol Genet 14:1109–1118

    Article  PubMed  CAS  Google Scholar 

  • Feuillan PP, Ng D, Han JC, Sapp JC, Wetsch K, Spaulding E, Zheng YC, Caruso RC, Brooks BP, Johnston JJ, Yanovski JA, Biesecker LG (2011) Patients with Bardet-Biedl syndrome have hyperleptinemia suggestive of leptin resistance. J Clin Endocrinol Metab 96:E528–E535

    Article  PubMed  CAS  Google Scholar 

  • Gao XB, van den Pol AN (2001) Melanin concentrating hormone depresses synaptic activity of glutamate and GABA neurons from rat lateral hypothalamus. J Physiol 533:237–252

    Article  PubMed  CAS  Google Scholar 

  • Gao XB, van den Pol AN (2002) Melanin-concentrating hormone depresses L-, N-, and P/Q-type voltage-dependent calcium channels in rat lateral hypothalamic neurons. J Physiol 542:273–286

    Article  PubMed  CAS  Google Scholar 

  • Ghadami M, Tomita HA, Najafi MT, Damavandi E, Farahvash MS, Yamada K, Majidzadeh AK, Niikawa N (2000) Bardet-Biedl syndrome type 3 in an Iranian family: clinical study and confirmation of disease localization. Am J Med Genet 94:433–437

    Article  PubMed  CAS  Google Scholar 

  • Girard D, Petrovsky N (2011) Alstrom syndrome: insights into the pathogenesis of metabolic disorders. Nat Rev Endocrinol 7:77–88

    Article  PubMed  CAS  Google Scholar 

  • Goetz SC, Anderson KV (2010) The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11:331–344

    Article  PubMed  CAS  Google Scholar 

  • Gomori A, Ishihara A, Ito M, Mashiko S, Matsushita H, Yumoto M, Ito M, Tanaka T, Tokita S, Moriya M, Iwaasa H, Kanatani A (2003) Chronic intracerebroventricular infusion of MCH causes obesity in mice. Melanin-concentrating hormone. Am j Physiol Endocrinol Metab 284:E583–E588

    PubMed  CAS  Google Scholar 

  • Grace C, Beales P, Summerbell C, Jebb SA, Wright A, Parker D, Kopelman P (2003) Energy metabolism in Bardet-Biedl syndrome. Int J Obes Relat Metab Disord 27:1319–1324

    Article  PubMed  CAS  Google Scholar 

  • Hamon M, Doucet E, Lefevre K, Miquel MC, Lanfumey L, Insausti R, Frechilla D, Del Rio J, Verge D (1999) Antibodies and antisense oligonucleotide for probing the distribution and putative functions of central 5-HT6 receptors. Neuropsychopharmacology 21:68S–76S

    PubMed  CAS  Google Scholar 

  • Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S, Alvarez-Buylla A (2008) Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11:277–284

    Article  PubMed  CAS  Google Scholar 

  • Han YG, Kim HJ, Dlugosz AA, Ellison DW, Gilbertson RJ, Alvarez-Buylla A (2009) Dual and opposing roles of primary cilia in medulloblastoma development. Nat Med 15:1062–1065

    Article  PubMed  CAS  Google Scholar 

  • Handel M, Schulz S, Stanarius A, Schreff M, Erdtmann-Vourliotis M, Schmidt H, Wolf G, Hollt V (1999) Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89:909–926

    Article  PubMed  CAS  Google Scholar 

  • Haycraft CJ, Zhang Q, Song B, Jackson WS, Detloff PJ, Serra R, Yoder BK (2007) Intraflagellar transport is essential for endochondral bone formation. Development 134:307–316

    Article  PubMed  CAS  Google Scholar 

  • Hearn T, Renforth GL, Spalluto C, Hanley NA, Piper K, Brickwood S, White C, Connolly V, Taylor JF, Russell-Eggitt I, Bonneau D, Walker M, Wilson DI (2002) Mutation of ALMS1, a large gene with a tandem repeat encoding 47 amino acids, causes Alstrom syndrome. Nat Genet 31:79–83

    PubMed  CAS  Google Scholar 

  • Hearn T, Spalluto C, Phillips VJ, Renforth GL, Copin N, Hanley NA, Wilson DI (2005) Subcellular localization of ALMS1 supports involvement of centrosome and basal body dysfunction in the pathogenesis of obesity, insulin resistance, and type 2 diabetes. Diabetes 54:1581–1587

    Article  PubMed  CAS  Google Scholar 

  • Hebebrand J, Volckmar AL, Knoll N, Hinney A (2010) Chipping away the ‘missing heritability’: GIANT steps forward in the molecular elucidation of obesity – but still lots to go. Obes Facts 3:294–303

    Article  PubMed  Google Scholar 

  • Jin H, White SR, Shida T, Schulz S, Aguiar M, Gygi SP, Bazan JF, Nachury MV (2010) The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 141:1208–1219

    Article  PubMed  CAS  Google Scholar 

  • Joy T, Cao H, Black G, Malik R, Charlton-Menys V, Hegele RA, Durrington PN (2007) Alstrom syndrome (OMIM 203800): a case report and literature review. Orphanet J Rare Dis 2:49

    Article  PubMed  Google Scholar 

  • Kaplan OI, Doroquez DB, Cevik S, Bowie RV, Clarke L, Sanders AA, Kida K, Rappoport JZ, Sengupta P, Blacque OE (2012) Endocytosis genes facilitate protein and membrane transport in C. elegans sensory cilia. Curr Biol 22:451–460

    Article  PubMed  CAS  Google Scholar 

  • Katsanis N, Ansley SJ, Badano JL, Eichers ER, Lewis RA, Hoskins BE, Scambler PJ, Davidson WS, Beales PL, Lupski JR (2001) Triallelic inheritance in Bardet-Biedl syndrome, a Mendelian recessive disorder. Science 293:2256–2259

    Article  PubMed  CAS  Google Scholar 

  • Kim SK, Shindo A, Park TJ, Oh EC, Ghosh S, Gray RS, Lewis RA, Johnson CA, Attie-Bittach T, Katsanis N, Wallingford JB (2010) Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 329:1337–1340

    Article  PubMed  CAS  Google Scholar 

  • Klein D, Ammann F (1969) The syndrome of Laurence-Moon-Bardet-Biedl and allied diseases in Switzerland. Clinical, genetic and epidemiological studies. J Neurol Sci 9:479–513

    Article  PubMed  CAS  Google Scholar 

  • Kleyn PW, Fan W, Kovats SG, Lee JJ, Pulido JC, Wu Y, Berkemeier LR, Misumi DJ, Holmgren L, Charlat O, Woolf EA, Tayber O, Brody T, Shu P, Hawkins F, Kennedy B, Baldini L, Ebeling C, Alperin GD, Deeds J, Lakey ND, Culpepper J, Chen H, Glucksmann-Kuis MA, Carlson GA, Duyk GM, Moore KJ (1996) Identification and characterization of the mouse obesity gene tubby: a member of a novel gene family. Cell 85:281–290

    Article  PubMed  CAS  Google Scholar 

  • Knorz VJ, Spalluto C, Lessard M, Purvis TL, Adigun FF, Collin GB, Hanley NA, Wilson DI, Hearn T (2010) Centriolar association of ALMS1 and likely centrosomal functions of the ALMS motif-containing proteins C10orf90 and KIAA1731. Mol Biol Cell 21:3617–3629

    Article  PubMed  CAS  Google Scholar 

  • Kokoeva MV, Yin H, Flier JS (2005) Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310:679–683

    Article  PubMed  CAS  Google Scholar 

  • Kudryashova E, Wu J, Havton LA, Spencer MJ (2009) Deficiency of the E3 ubiquitin ligase TRIM32 in mice leads to a myopathy with a neurogenic component. Hum Mol Genet 18:1353–1367

    Article  PubMed  CAS  Google Scholar 

  • Kudryashova E, Struyk A, Mokhonova E, Cannon SC, Spencer MJ (2011) The common missense mutation D489N in TRIM32 causing limb girdle muscular dystrophy 2H leads to loss of the mutated protein in knock-in mice resulting in a Trim32-null phenotype. Hum Mol Genet 20:3925–3932

    Article  PubMed  CAS  Google Scholar 

  • Kulaga HM, Leitch CC, Eichers ER, Badano JL, Lesemann A, Hoskins BE, Lupski JR, Beales PL, Reed RR, Katsanis N (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

    Article  PubMed  CAS  Google Scholar 

  • Lancaster MA, Gopal DJ, Kim J, Saleem SN, Silhavy JL, Louie CM, Thacker BE, Williams Y, Zaki MS, Gleeson JG (2011) Defective Wnt-dependent cerebellar midline fusion in a mouse model of Joubert syndrome. Nat Med 17:726–731

    Article  PubMed  CAS  Google Scholar 

  • Laurier V, Stoetzel C, Muller J, Thibault C, Corbani S, Jalkh N, Salem N, Chouery E, Poch O, Licaire S, Danse JM, Amati-Bonneau P, Bonneau D, Megarbane A, Mandel JL, Dollfus H (2006) Pitfalls of homozygosity mapping: an extended consanguineous Bardet-Biedl syndrome family with two mutant genes (BBS2, BBS10), three mutations, but no triallelism. Eur J Hum Genet 14:1195–1203

    Article  PubMed  CAS  Google Scholar 

  • Lechtreck KF, Johnson EC, Sakai T, Cochran D, Ballif BA, Rush J, Pazour GJ, Ikebe M, Witman GB (2009) The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J Cell Biol 187:1117–1132

    Article  PubMed  CAS  Google Scholar 

  • Lee BH, Liu J, Wong D, Srinivasan S, Ashrafi K (2011) Hyperactive neuroendocrine secretion causes size, feeding, and metabolic defects of C. elegans Bardet-Biedl syndrome mutants. PLoS Biol 9:e1001219

    Article  PubMed  CAS  Google Scholar 

  • Lee DA, Bedont JL, Pak T, Wang H, Song J, Miranda-Angulo A, Takiar V, Charubhumi V, Balordi F, Takebayashi H, Aja S, Ford E, Fishell G, Blackshaw S (2012) Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat Neurosci 15(5):700–702

    Article  PubMed  CAS  Google Scholar 

  • Lehman JM, Michaud EJ, Schoeb TR, Aydin-Son Y, Miller M, Yoder BK (2008) The Oak Ridge Polycystic Kidney mouse: modeling ciliopathies of mice and men. Dev Dyn 237:1960–1971

    Article  PubMed  Google Scholar 

  • Leitch CC, Zaghloul NA, Davis EE, Stoetzel C, Diaz-Font A, Rix S, Alfadhel M, Lewis RA, Eyaid W, Banin E, Dollfus H, Beales PL, Badano JL, Katsanis N (2008) Hypomorphic mutations in syndromic encephalocele genes are associated with Bardet-Biedl syndrome. Nat Genet 40:443–448

    Article  PubMed  CAS  Google Scholar 

  • Lorda-Sanchez I, Ayuso C, Ibanez A (2000) Situs inversus and hirschsprung disease: two uncommon manifestations in Bardet-Biedl syndrome. Am J Med Genet 90:80–81

    Article  PubMed  CAS  Google Scholar 

  • Ludwig DS, Tritos NA, Mastaitis JW, Kulkarni R, Kokkotou E, Elmquist J, Lowell B, Flier JS, Maratos-Flier E (2001) Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J Clin Invest 107:379–386

    Article  PubMed  CAS  Google Scholar 

  • Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y, Fei H, Kim S, Lallone R, Ranganathan S et al (1995) Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1:1155–1161

    Article  PubMed  CAS  Google Scholar 

  • Maffei P, Boschetti M, Marshall JD, Paisey RB, Beck S, Resmini E, Collin GB, Naggert JK, Milan G, Vettor R, Minuto F, Sicolo N, Barreca A (2007) Characterization of the IGF system in 15 patients with Alstrom syndrome. Clin Endocrinol (Oxf) 66:269–275

    Article  CAS  Google Scholar 

  • Marley A, von Zastrow M (2010) DISC1 regulates primary cilia that display specific dopamine receptors. PLoS One 5:e10902

    Article  PubMed  CAS  Google Scholar 

  • Marshall JD, Hinman EG, Collin GB, Beck S, Cerqueira R, Maffei P, Milan G, Zhang W, Wilson DI, Hearn T, Tavares P, Vettor R, Veronese C, Martin M, So WV, Nishina PM, Naggert JK (2007) Spectrum of ALMS1 variants and evaluation of genotype-phenotype correlations in Alstrom syndrome. Hum Mutat 28:1114–1123

    Article  PubMed  CAS  Google Scholar 

  • Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR, Goldstein LS (1999) Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci USA 96:5043–5048

    Article  PubMed  CAS  Google Scholar 

  • Mistlberger RE (2009) Food-anticipatory circadian rhythms: concepts and methods. Eur J Neurosci 30:1718–1729

    Article  PubMed  Google Scholar 

  • Mok CA, Healey MP, Shekhar T, Leroux MR, Heon E, Zhen M (2011) Mutations in a guanylate cyclase GCY-35/GCY-36 modify Bardet-Biedl syndrome-associated phenotypes in Caenorhabditis elegans. PLoS Genet 7:e1002335

    Article  PubMed  CAS  Google Scholar 

  • Mountjoy KG (2010) Functions for pro-opiomelanocortin-derived peptides in obesity and diabetes. Biochem J 428:305–324

    Article  PubMed  CAS  Google Scholar 

  • Moyer JH, Lee-Tischler MJ, Kwon HY, Schrick JJ, Avner ED, Sweeney WE, Godfrey VL, Cacheiro NL, Wilkinson JE, Woychik RP (1994) Candidate gene associated with a mutation causing recessive polycystic kidney disease in mice. Science 264:1329–1333

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay A, Deplancke B, Walhout AJ, Tissenbaum HA (2005) C. elegans tubby regulates life span and fat storage by two independent mechanisms. Cell Metab 2:35–42

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay S, Wen X, Chih B, Nelson CD, Lane WS, Scales SJ, Jackson PK (2010) TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia. Genes Dev 24:2180–2193

    Article  PubMed  CAS  Google Scholar 

  • Murcia NS, Richards WG, Yoder BK, Mucenski ML, Dunlap JR, Woychik RP (2000) The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 127:2347–2355

    PubMed  CAS  Google Scholar 

  • Mykytyn K, Braun T, Carmi R, Haider NB, Searby CC, Shastri M, Beck G, Wright AF, Iannaccone A, Elbedour K, Riise R, Baldi A, Raas-Rothschild A, Gorman SW, Duhl DM, Jacobson SG, Casavant T, Stone EM, Sheffield VC (2001) Identification of the gene that, when mutated, causes the human obesity syndrome BBS4. Nat Genet 28:188–191

    Article  PubMed  CAS  Google Scholar 

  • Mykytyn K, Nishimura DY, Searby CC, Shastri M, Yen HJ, Beck JS, Braun T, Streb LM, Cornier AS, Cox GF, Fulton AB, Carmi R, Luleci G, Chandrasekharappa SC, Collins FS, Jacobson SG, Heckenlively JR, Weleber RG, Stone EM, Sheffield VC (2002) Identification of the gene (BBS1) most commonly involved in Bardet-Biedl syndrome, a complex human obesity syndrome. Nat Genet 31:435–438

    PubMed  CAS  Google Scholar 

  • Mykytyn K, Nishimura DY, Searby CC, Beck G, Bugge K, Haines HL, Cornier AS, Cox GF, Fulton AB, Carmi R, Iannaccone A, Jacobson SG, Weleber RG, Wright AF, Riise R, Hennekam RC, Luleci G, Berker-Karauzum S, Biesecker LG, Stone EM, Sheffield VC (2003) Evaluation of complex inheritance involving the most common Bardet-Biedl syndrome locus (BBS1). Am J Hum Genet 72:429–437

    Article  PubMed  CAS  Google Scholar 

  • Mykytyn K, Mullins RF, Andrews M, Chiang AP, Swiderski RE, Yang B, Braun T, Casavant T, Stone EM, Sheffield VC (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

    Article  PubMed  CAS  Google Scholar 

  • Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peranen J, Merdes A, Slusarski DC, Scheller RH, Bazan JF, Sheffield VC, Jackson PK (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129:1201–1213

    Article  PubMed  CAS  Google Scholar 

  • Nishimura DY, Searby CC, Carmi R, Elbedour K, Van Maldergem L, Fulton AB, Lam BL, Powell BR, Swiderski RE, Bugge KE, Haider NB, Kwitek-Black AE, Ying L, Duhl DM, Gorman SW, Heon E, Iannaccone A, Bonneau D, Biesecker LG, Jacobson SG, Stone EM, Sheffield VC (2001) Positional cloning of a novel gene on chromosome 16q causing Bardet-Biedl syndrome (BBS2). Hum Mol Genet 10:865–874

    Article  PubMed  CAS  Google Scholar 

  • Nishimura DY, Fath M, Mullins RF, Searby C, Andrews M, Davis R, Andorf JL, Mykytyn K, Swiderski RE, Yang B, Carmi R, Stone EM, Sheffield VC (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

    Article  PubMed  CAS  Google Scholar 

  • Nishimura DY, Swiderski RE, Searby CC, Berg EM, Ferguson AL, Hennekam R, Merin S, Weleber RG, Biesecker LG, Stone EM, Sheffield VC (2005) Comparative genomics and gene expression analysis identifies BBS9, a new Bardet-Biedl syndrome gene. Am J Hum Genet 77:1021–1033

    Article  PubMed  CAS  Google Scholar 

  • Nordman S, Abulaiti A, Hilding A, Langberg EC, Humphreys K, Ostenson CG, Efendic S, Gu HF (2008) Genetic variation of the adenylyl cyclase 3 (AC3) locus and its influence on type 2 diabetes and obesity susceptibility in Swedish men. Int J Obes (Lond) 32:407–412

    Article  CAS  Google Scholar 

  • Norman RX, Ko HW, Huang V, Eun CM, Abler LL, Zhang Z, Sun X, Eggenschwiler JT (2009) Tubby-like protein 3 (TULP3) regulates patterning in the mouse embryo through inhibition of Hedgehog signaling. Hum Mol Genet 18:1740–1754

    Article  PubMed  CAS  Google Scholar 

  • Ohlemiller KK, Hughes RM, Mosinger-Ogilvie J, Speck JD, Grosof DH, Silverman MS (1995) Cochlear and retinal degeneration in the tubby mouse. Neuroreport 6:845–849

    Article  PubMed  CAS  Google Scholar 

  • Pascual O, Traiffort E, Baker DP, Galdes A, Ruat M, Champagnat J (2005) Sonic hedgehog signalling in neurons of adult ventrolateral nucleus tractus solitarius. Eur J Neurosci 22:389–396

    Article  PubMed  Google Scholar 

  • Pedersen LB, Rosenbaum JL (2008) Chapter two intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85:23–61

    Article  PubMed  CAS  Google Scholar 

  • Pierce AA, Xu AW (2010) De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance. J Neurosci 30:723–730

    Article  PubMed  CAS  Google Scholar 

  • Plum L, Lin HV, Aizawa KS, Liu Y, Accili D (2012) InsR/FoxO1 signaling curtails hypothalamic POMC neuron number. PLoS One 7:e31487

    Article  PubMed  CAS  Google Scholar 

  • Pollock JD, Rowland N (1981) Peripherally administered serotonin decreases food intake in rats. Pharmacol Biochem Behav 15:179–183

    Article  PubMed  CAS  Google Scholar 

  • Qu D, Ludwig DS, Gammeltoft S, Piper M, Pelleymounter MA, Cullen MJ, Mathes WF, Przypek R, Kanarek R, Maratos-Flier E (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380:243–247

    Article  PubMed  CAS  Google Scholar 

  • Rahmouni K, Fath MA, Seo S, Thedens DR, Berry CJ, Weiss R, Nishimura DY, Sheffield VC (2008) Leptin resistance contributes to obesity and hypertension in mouse models of Bardet-Biedl syndrome. J Clin Invest 118:1458–1467

    Article  PubMed  CAS  Google Scholar 

  • Riise R, Andreasson S, Borgastrom MK, Wright AF, Tommerup N, Rosenberg T, Tornqvist K (1997) Intrafamilial variation of the phenotype in Bardet-Biedl syndrome. Br J Ophthalmol 81:378–385

    Article  PubMed  CAS  Google Scholar 

  • Salamone JD, Zigmond MJ, Stricker EM (1990) Characterization of the impaired feeding behavior in rats given haloperidol or dopamine-depleting brain lesions. Neuroscience 39:17–24

    Article  PubMed  CAS  Google Scholar 

  • Schaefer E, Zaloszyc A, Lauer J, Durand M, Stutzmann F, Perdomo-Trujillo Y, Redin C, Bennouna Greene V, Toutain A, Perrin L, Gerard M, Caillard S, Bei X, Lewis RA, Christmann D, Letsch J, Kribs M, Mutter C, Muller J, Stoetzel C, Fischbach M, Marion V, Katsanis N, Dollfus H (2011) Mutations in SDCCAG8/NPHP10 cause Bardet-Biedl syndrome and are associated with penetrant renal disease and absent polydactyly. Mol Syndromol 1:273–281

    Article  PubMed  CAS  Google Scholar 

  • Schulz S, Handel M, Schreff M, Schmidt H, Hollt V (2000) Localization of five somatostatin receptors in the rat central nervous system using subtype-specific antibodies. J Physiol Paris 94:259–264

    Article  PubMed  CAS  Google Scholar 

  • Seo S, Guo DF, Bugge K, Morgan DA, Rahmouni K, Sheffield VC (2009) Requirement of Bardet-Biedl syndrome proteins for leptin receptor signaling. Hum Mol Genet 18(7):1323–1331

    Article  PubMed  CAS  Google Scholar 

  • Seo S, Baye LM, Schulz NP, Beck JS, Zhang Q, Slusarski DC, Sheffield VC (2010) BBS6, BBS10, and BBS12 form a complex with CCT/TRiC family chaperonins and mediate BBSome assembly. Proc Natl Acad Sci USA 107:1488–1493

    Article  PubMed  CAS  Google Scholar 

  • Sharma N, Berbari NF, Yoder BK (2008) Ciliary dysfunction in developmental abnormalities and diseases. Curr Top Dev Biol 85:371–427

    Article  PubMed  CAS  Google Scholar 

  • Sharma N, Kosan ZA, Stallworth JE, Berbari NF, Yoder BK (2011) Soluble levels of cytosolic tubulin regulate ciliary length control. Mol Biol Cell 22:806–816

    Article  PubMed  CAS  Google Scholar 

  • Shillingford JM, Murcia NS, Larson CH, Low SH, Hedgepeth R, Brown N, Flask CA, Novick AC, Goldfarb DA, Kramer-Zucker A, Walz G, Piontek KB, Germino GG, Weimbs T (2006) The mTOR pathway is regulated by polycystin-1, and its inhibition reverses renal cystogenesis in polycystic kidney disease. Proc Natl Acad Sci USA 103:5466–5471

    Article  PubMed  CAS  Google Scholar 

  • Shillingford JM, Piontek KB, Germino GG, Weimbs T (2010) Rapamycin ameliorates PKD resulting from conditional inactivation of Pkd1. J Am Soc Nephrol 21:489–497

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Slavotinek AM, Stone EM, Mykytyn K, Heckenlively JR, Green JS, Heon E, Musarella MA, Parfrey PS, Sheffield VC, Biesecker LG (2000) Mutations in MKKS cause Bardet-Biedl syndrome. Nat Genet 26:15–16

    Article  PubMed  CAS  Google Scholar 

  • Smaoui N, Chaabouni M, Sergeev YV, Kallel H, Li S, Mahfoudh N, Maazoul F, Kammoun H, Gandoura N, Bouaziz A, Nouiri E, M’Rad R, Chaabouni H, Hejtmancik JF (2006) Screening of the eight BBS genes in Tunisian families: no evidence of triallelism. Invest Ophthalmol Vis Sci 47:3487–3495

    Article  PubMed  Google Scholar 

  • Stoetzel C, Laurier V, Davis EE, Muller J, Rix S, Badano JL, Leitch CC, Salem N, Chouery E, Corbani S, Jalk N, Vicaire S, Sarda P, Hamel C, Lacombe D, Holder M, Odent S, Holder S, Brooks AS, Elcioglu NH, Da Silva E, Rossillion B, Sigaudy S, de Ravel TJ, Alan Lewis R, Leheup B, Verloes A, Amati-Bonneau P, Megarbane A, Poch O, Bonneau D, Beales PL, Mandel JL, Katsanis N, Dollfus H (2006) BBS10 encodes a vertebrate-specific chaperonin-like protein and is a major BBS locus. Nat Genet 38(5):521–524

    Article  PubMed  CAS  Google Scholar 

  • Stoetzel C, Muller J, Laurier V, Davis EE, Zaghloul NA, Vicaire S, Jacquelin C, Plewniak F, Leitch CC, Sarda P, Hamel C, de Ravel TJ, Lewis RA, Friederich E, Thibault C, Danse JM, Verloes A, Bonneau D, Katsanis N, Poch O, Mandel JL, Dollfus H (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

    Article  PubMed  CAS  Google Scholar 

  • Stubdal H, Lynch CA, Moriarty A, Fang Q, Chickering T, Deeds JD, Fairchild-Huntress V, Charlat O, Dunmore JH, Kleyn P, Huszar D, Kapeller R (2000) Targeted deletion of the tub mouse obesity gene reveals that tubby is a loss-of-function mutation. Mol Cell Biol 20:878–882

    Article  PubMed  CAS  Google Scholar 

  • Szabo NE, Zhao T, Cankaya M, Theil T, Zhou X, Alvarez-Bolado G (2009) Role of neuroepithelial Sonic hedgehog in hypothalamic patterning. J Neurosci 29:6989–7002

    Article  PubMed  CAS  Google Scholar 

  • Tadenev AL, Kulaga HM, May-Simera HL, Kelley MW, Katsanis N, Reed RR (2011) Loss of Bardet-Biedl syndrome protein-8 (BBS8) perturbs olfactory function, protein localization, and axon targeting. Proc Natl Acad Sci USA 108:10320–10325

    Article  PubMed  CAS  Google Scholar 

  • Tan PL, Barr T, Inglis PN, Mitsuma N, Huang SM, Garcia-Gonzalez MA, Bradley BA, Coforio S, Albrecht PJ, Watnick T, Germino GG, Beales PL, Caterina MJ, Leroux MR, Rice FL, Katsanis N (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

    Article  PubMed  CAS  Google Scholar 

  • Traiffort E, Charytoniuk DA, Faure H, Ruat M (1998) Regional distribution of Sonic Hedgehog, patched, and smoothened mRNA in the adult rat brain. J Neurochem 70:1327–1330

    Article  PubMed  CAS  Google Scholar 

  • Traiffort E, Charytoniuk D, Watroba L, Faure H, Sales N, Ruat M (1999) Discrete localizations of hedgehog signalling components in the developing and adult rat nervous system. Eur J Neurosci 11:3199–3214

    Article  PubMed  CAS  Google Scholar 

  • Traiffort E, Angot E, Ruat M (2010) Sonic Hedgehog signaling in the mammalian brain. J Neurochem 113:576–590

    Article  PubMed  CAS  Google Scholar 

  • Vijayan E, McCann SM (1977) Suppression of feeding and drinking activity in rats following intraventricular injection of thyrotropin releasing hormone (TRH). Endocrinology 100:1727–1730

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Li V, Chan GC, Phan T, Nudelman AS, Xia Z, Storm DR (2009) Adult type 3 adenylyl cyclase-deficient mice are obese. PLoS One 4:e6979

    Article  PubMed  CAS  Google Scholar 

  • Weatherbee SD, Niswander LA, Anderson KV (2009) A mouse model for Meckel syndrome reveals Mks1 is required for ciliogenesis and Hedgehog signaling. Hum Mol Genet 18:4565–4575

    Article  PubMed  CAS  Google Scholar 

  • Wong ST, Trinh K, Hacker B, Chan GC, Lowe G, Gaggar A, Xia Z, Gold GH, Storm DR (2000) Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27:487–497

    Article  PubMed  CAS  Google Scholar 

  • Xu AW, Kaelin CB, Morton GJ, Ogimoto K, Stanhope K, Graham J, Baskin DG, Havel P, Schwartz MW, Barsh GS (2005a) Effects of hypothalamic neurodegeneration on energy balance. PLoS Biol 3:e415

    Article  PubMed  CAS  Google Scholar 

  • Xu AW, Kaelin CB, Takeda K, Akira S, Schwartz MW, Barsh GS (2005b) PI3K integrates the action of insulin and leptin on hypothalamic neurons. J Clin Invest 115:951–958

    PubMed  CAS  Google Scholar 

  • Xu Y, Tamamaki N, Noda T, Kimura K, Itokazu Y, Matsumoto N, Dezawa M, Ide C (2005c) Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp Neurol 192:251–264

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Nishimura D, Seo S, Vogel T, Morgan DA, Searby C, Bugge K, Stone EM, Rahmouni K, Sheffield VC (2011) Bardet-Biedl syndrome 3 (Bbs3) knockout mouse model reveals common BBS-associated phenotypes and Bbs3 unique phenotypes. Proc Natl Acad Sci USA 108:20678-20683

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Romero MI, Ghosh P, Ye Z, Charnay P, Rushing EJ, Marth JD, Parada LF (2001) Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 15:859–876

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Yoder lab members for suggestions and critical review of the chapter. This work was supported in part by NIH RO1 DK075996 to BKY. NFB was supported by NRSA F32 DK088404, RCP was supported by T32 GM008111 to (Dr. Yoder).

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Correspondence to Bradley K. Yoder Ph.D. .

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Berbari, N.F., Pasek, R.C., Yoder, B.K. (2013). Neuronal Cilia and Obesity. In: Tucker, K., Caspary, T. (eds) Cilia and Nervous System Development and Function. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5808-7_6

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