Olfactory receptor genes cooperate with protocadherin genes in human extreme obesity

Genes and Nutrition

Volumn 10, Issue 4, 2015, Pages

  Mariman, Edwin C M ^a   Szklarczyk, Radek ^a   Bouwman, Freek G ^a   Aller, Erik E J G ^a   van Baak, Marleen A ^a   Wang, Ping ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Extreme obesity; Genetic predisposition; Olfactory system; Protocadherins

Indexed keywords

ADULT; ARTICLE; CHROMOSOME 1Q; CHROMOSOME 5Q; CLINICAL ARTICLE; CONTROLLED STUDY; EXOME; EXTREME OBESITY; FEMALE; GENE; GENE CLUSTER; GENE FREQUENCY; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC PREDISPOSITION; GENETIC VARIABILITY; HUMAN; MALE; MISSENSE MUTATION; OBESITY; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PROTOCADHERIN GENE; RECEPTOR GENE;

EID: 84929501500     PISSN: 15558932     EISSN: 18653499     Source Type: Journal    
DOI: 10.1007/s12263-015-0465-3     Document Type: Article

References (38)

1. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7(4):248–249. doi:10.1038/nmeth0410-248
2. Baughman JM, Nilsson R, Gohil VM, Arlow DH, Gauhar Z, Mootha VK (2009) A computational screen for regulators of oxidative phosphorylation implicates SLIRP in mitochondrial RNA homeostasis. PLoS Genet 5(8):e1000590. doi:10.1371/journal.pgen.1000590
3. Berndt SI, Gustafsson S, Magi R, Ganna A, Wheeler E, Feitosa MF, Justice AE, Monda KL, Croteau-Chonka DC, Day FR, Esko T, Fall T, Ferreira T, Gentilini D, Jackson AU, Luan J, Randall JC, Vedantam S, Willer CJ, Winkler TW, Wood AR, Workalemahu T, Hu YJ, Lee SH, Liang L, Lin DY, Min JL, Neale BM, Thorleifsson G, Yang J, Albrecht E, Amin N, Bragg-Gresham JL, Cadby G, den Heijer M, Eklund N, Fischer K, Goel A, Hottenga JJ, Huffman JE, Jarick I, Johansson A, Johnson T, Kanoni S, Kleber ME, Konig IR, Kristiansson K, Kutalik Z, Lamina C, Lecoeur C, Li G, Mangino M, McArdle WL, Medina-Gomez C, Muller-Nurasyid M, Ngwa JS, Nolte IM, Paternoster L, Pechlivanis S, Perola M, Peters MJ, Preuss M, Rose LM, Shi J, Shungin D, Smith AV, Strawbridge RJ, Surakka I, Teumer A, Trip MD, Tyrer J, Van Vliet-Ostaptchouk JV, Vandenput L, Waite LL, Zhao JH, Absher D, Asselbergs FW, Atalay M, Attwood AP, Balmforth AJ, Basart H, Beilby J, Bonnycastle LL, Brambilla P, Bruinenberg M, Campbell H, Chasman DI, Chines PS, Collins FS, Connell JM, Cookson WO, de Faire U, de Vegt F, Dei M, Dimitriou M, Edkins S, Estrada K, Evans DM, Farrall M, Ferrario MM, Ferrieres J, Franke L, Frau F, Gejman PV, Grallert H, Gronberg H, Gudnason V, Hall AS, Hall P, Hartikainen AL, Hayward C, Heard-Costa NL, Heath AC, Hebebrand J, Homuth G, Hu FB, Hunt SE, Hypponen E, Iribarren C, Jacobs KB, Jansson JO, Jula A, Kahonen M, Kathiresan S, Kee F, Khaw KT, Kivimaki M, Koenig W, Kraja AT, Kumari M, Kuulasmaa K, Kuusisto J, Laitinen JH, Lakka TA, Langenberg C, Launer LJ, Lind L, Lindstrom J, Liu J, Liuzzi A, Lokki ML, Lorentzon M, Madden PA, Magnusson PK, Manunta P, Marek D, Marz W, Mateo Leach I, McKnight B, Medland SE, Mihailov E, Milani L, Montgomery GW, Mooser V, Muhleisen TW, Munroe PB, Musk AW, Narisu N, Navis G, Nicholson G, Nohr EA, Ong KK, Oostra BA, Palmer CN, Palotie A, Peden JF, Pedersen N, Peters A, Polasek O, Pouta A, Pramstaller PP, Prokopenko I, Putter C, Radhakrishnan A, Raitakari O, Rendon A, Rivadeneira F, Rudan I, Saaristo TE, Sambrook JG, Sanders AR, Sanna S, Saramies J, Schipf S, Schreiber S, Schunkert H, Shin SY, Signorini S, Sinisalo J, Skrobek B, Soranzo N, Stancakova A, Stark K, Stephens JC, Stirrups K, Stolk RP, Stumvoll M, Swift AJ, Theodoraki EV, Thorand B, Tregouet DA, Tremoli E, Van der Klauw MM, van Meurs JB, Vermeulen SH, Viikari J, Virtamo J, Vitart V, Waeber G, Wang Z, Widen E, Wild SH, Willemsen G, Winkelmann BR, Witteman JC, Wolffenbuttel BH, Wong A, Wright AF, Zillikens MC, Amouyel P, Boehm BO, Boerwinkle E, Boomsma DI, Caulfield MJ, Chanock SJ, Cupples LA, Cusi D, Dedoussis GV, Erdmann J, Eriksson JG, Franks PW, Froguel P, Gieger C, Gyllensten U, Hamsten A, Harris TB, Hengstenberg C, Hicks AA, Hingorani A, Hinney A, Hofman A, Hovingh KG, Hveem K, Illig T, Jarvelin MR, Jockel KH, Keinanen-Kiukaanniemi SM, Kiemeney LA, Kuh D, Laakso M, Lehtimaki T, Levinson DF, Martin NG, Metspalu A, Morris AD, Nieminen MS, Njolstad I, Ohlsson C, Oldehinkel AJ, Ouwehand WH, Palmer LJ, Penninx B, Power C, Province MA, Psaty BM, Qi L, Rauramaa R, Ridker PM, Ripatti S, Salomaa V, Samani NJ, Snieder H, Sorensen TI, Spector TD, Stefansson K, Tonjes A, Tuomilehto J, Uitterlinden AG, Uusitupa M, van der Harst P, Vollenweider P, Wallaschofski H, Wareham NJ, Watkins H, Wichmann HE, Wilson JF, Abecasis GR, Assimes TL, Barroso I, Boehnke M, Borecki IB, Deloukas P, Fox CS, Frayling T, Groop LC, Haritunian T, Heid IM, Hunter D, Kaplan RC, Karpe F, Moffatt MF, Mohlke KL, O’Connell JR, Pawitan Y, Schadt EE, Schlessinger D, Steinthorsdottir V, Strachan DP, Thorsteinsdottir U, van Duijn CM, Visscher PM, Di Blasio AM, Hirschhorn JN, Lindgren CM, Morris AP, Meyre D, Scherag A, McCarthy MI, Speliotes EK, North KE, Loos RJ, Ingelsson E (2013) Genome-wide meta-analysis identifies 11 new loci for anthropometric traits and provides insights into genetic architecture. Nat Genet 45(5):501–512. doi:10.1038/ng.2606
4. Blundell JE, Finlayson G (2004) Is susceptibility to weight gain characterized by homeostatic or hedonic risk factors for overconsumption? Physiol Behav 82(1):21–25. doi:10.1016/j.physbeh.2004.04.021
5. Choquette AC, Bouchard L, Drapeau V, Lemieux S, Tremblay A, Bouchard C, Vohl MC, Perusse L (2012) Association between olfactory receptor genes, eating behavior traits and adiposity: results from the Quebec Family Study. Physiol Behav 105(3):772–776. doi:10.1016/j.physbeh.2011.10.015
6. Cleland TA (2014) Construction of odor representations by olfactory bulb microcircuits. Prog Brain Res 208:177–203. doi:10.1016/b978-0-444-63350-7.00007-3
7. Consortium GotN (2014) Whole-genome sequence variation, population structure and demographic history of the Dutch population. Nat Genet 46(8):818–825. doi:10.1038/ng.3021
8. Eriksson N, Macpherson JM, Tung JY, Hon LS, Naughton B, Saxonov S, Avey L, Wojcicki A, Pe’er I, Mountain J (2010) Web-based, participant-driven studies yield novel genetic associations for common traits. PLoS Genet 6(6):e1000993. doi:10.1371/journal.pgen.1000993
9. Farooqi IS, O’Rahilly S (2007) Genetic factors in human obesity. Obes Rev 8(Suppl 1):37–40. doi:10.1111/j.1467-789X.2007.00315.x
10. Gu X, Karp PH, Brody SL, Pierce RA, Welsh MJ, Holtzman MJ, Ben-Shahar Y (2014) Chemosensory functions for pulmonary neuroendocrine cells. Am J Respir Cell Mol Biol 50(3):637–646. doi:10.1165/rcmb.2013-0199OC
11. Hasegawa S, Hirabayashi T, Kondo T, Inoue K, Esumi S, Okayama A, Hamada S, Yagi T (2012) Constitutively expressed Protocadherin-alpha regulates the coalescence and elimination of homotypic olfactory axons through its cytoplasmic region. Front Mol Neurosci 5:97. doi:10.3389/fnmol.2012.00097
12. Hasin-Brumshtein Y, Lancet D, Olender T (2009) Human olfaction: from genomic variation to phenotypic diversity. Trends Genet TIG 25(4):178–184. doi:10.1016/j.tig.2009.02.002
13. Hirano K, Kaneko R, Izawa T, Kawaguchi M, Kitsukawa T, Yagi T (2012) Single-neuron diversity generated by Protocadherin-beta cluster in mouse central and peripheral nervous systems. Front Mol Neurosci 5:90. doi:10.3389/fnmol.2012.00090
14. Jaeger SR, McRae JF, Bava CM, Beresford MK, Hunter D, Jia Y, Chheang SL, Jin D, Peng M, Gamble JC, Atkinson KR, Axten LG, Paisley AG, Tooman L, Pineau B, Rouse SA, Newcomb RD (2013) A Mendelian trait for olfactory sensitivity affects odor experience and food selection. Curr Biol CB 23(16):1601–1605. doi:10.1016/j.cub.2013.07.030
15. Jarick I, Vogel CI, Scherag S, Schafer H, Hebebrand J, Hinney A, Scherag A (2011) Novel common copy number variation for early onset extreme obesity on chromosome 11q11 identified by a genome-wide analysis. Hum Mol Genet 20(4):840–852. doi:10.1093/hmg/ddq518
16. Keller A, Zhuang H, Chi Q, Vosshall LB, Matsunami H (2007) Genetic variation in a human odorant receptor alters odour perception. Nature 449(7161):468–472. doi:10.1038/nature06162
17. Ledderose J, Dieter S, Schwarz MK (2013) Maturation of postnatally generated olfactory bulb granule cells depends on functional gamma-protocadherin expression. Sci Rep 3:1514. doi:10.1038/srep01514
18. Li Y, Serwanski DR, Miralles CP, Fiondella CG, Loturco JJ, Rubio ME, De Blas AL (2010) Synaptic and nonsynaptic localization of protocadherin-gammaC5 in the rat brain. J Comp Neurol 518(17):3439–3463. doi:10.1002/cne.22390
19. Loos RJF (2012) Genetic determinants of common obesity and their value in prediction. Best Pract Res Clin Endocrinol Metab 26(2):211–226. doi:10.1016/j.beem.2011.11.003
20. Lunde K, Egelandsdal B, Skuterud E, Mainland JD, Lea T, Hersleth M, Matsunami H (2012) Genetic variation of an odorant receptor OR7D4 and sensory perception of cooked meat containing androstenone. PLoS ONE 7(5):e35259. doi:10.1371/journal.pone.0035259
21. MacArthur DG, Manolio TA, Dimmock DP, Rehm HL, Shendure J, Abecasis GR, Adams DR, Altman RB, Antonarakis SE, Ashley EA, Barrett JC, Biesecker LG, Conrad DF, Cooper GM, Cox NJ, Daly MJ, Gerstein MB, Goldstein DB, Hirschhorn JN, Leal SM, Pennacchio LA, Stamatoyannopoulos JA, Sunyaev SR, Valle D, Voight BF, Winckler W, Gunter C (2014) Guidelines for investigating causality of sequence variants in human disease. Nature 508(7497):469–476. doi:10.1038/nature13127
22. Mainland JD, Keller A, Li YR, Zhou T, Trimmer C, Snyder LL, Moberly AH, Adipietro KA, Liu WL, Zhuang H, Zhan S, Lee SS, Lin A, Matsunami H (2014) The missense of smell: functional variability in the human odorant receptor repertoire. Nat Neurosci 17(1):114–120. doi:10.1038/nn.3598
23. Malnic B, Godfrey PA, Buck LB (2004) The human olfactory receptor gene family. Proc Natl Acad Sci USA 101(8):2584–2589
24. Mariman EC, Bouwman FG, Aller EE, van Baak MA, Wang P (2014) High frequency of rare variants with a moderate-to-high predicted biological effect in protocadherin genes of extremely obese. Genes Nutr 9(3):399. doi:10.1007/s12263-014-0399-1
25. Ng PC, Henikoff S (2003) SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res 31(13):3812–3814
26. Palouzier-Paulignan B, Lacroix MC, Aime P, Baly C, Caillol M, Congar P, Julliard AK, Tucker K, Fadool DA (2012) Olfaction under metabolic influences. Chem Senses 37(9):769–797. doi:10.1093/chemse/bjs059
27. Primeaux SD, Braymer HD, Bray GA (2013) High fat diet differentially regulates the expression of olfactory receptors in the duodenum of obesity-prone and obesity-resistant rats. Dig Dis Sci 58(1):72–76. doi:10.1007/s10620-012-2421-z
28. Reed DR, Knaapila A (2010) Genetics of taste and smell: poisons and pleasures. Prog Mol Biol Transl Sci 94:213–240. doi:10.1016/b978-0-12-375003-7.00008-x
29. Reumers J, Schymkowitz J, Ferkinghoff-Borg J, Stricher F, Serrano L, Rousseau F (2005) SNPeffect: a database mapping molecular phenotypic effects of human non-synonymous coding SNPs. Nucleic acids research 33(Database issue):D527–D532. doi:10.1093/nar/gki086
30. Richardson BE, Vander Woude EA, Sudan R, Thompson JS, Leopold DA (2004) Altered olfactory acuity in the morbidly obese. Obes Surg 14(7):967–969. doi:10.1381/0960892041719617
31. Richardson BE, Vanderwoude EA, Sudan R, Leopold DA, Thompson JS (2012) Gastric bypass does not influence olfactory function in obese patients. Obes Surg 22(2):283–286. doi:10.1007/s11695-011-0487-x
32. Shepherd GM (2006) Smell images and the flavour system in the human brain. Nature 444(7117):316–321. doi:10.1038/nature05405
33. Song H, Yao E, Lin C, Gacayan R, Chen MH, Chuang PT (2012) Functional characterization of pulmonary neuroendocrine cells in lung development, injury, and tumorigenesis. Proc Natl Acad Sci USA 109(43):17531–17536. doi:10.1073/pnas.1207238109
34. Sorensen LB, Moller P, Flint A, Martens M, Raben A (2003) Effect of sensory perception of foods on appetite and food intake: a review of studies on humans. Int J Obes Relat Metab Disord 27(10):1152–1166. doi:10.1038/sj.ijo.0802391
35. Speliotes EK, Willer CJ, Berndt SI, Monda KL, Thorleifsson G, Jackson AU, Lango Allen H, Lindgren CM, Luan J, Magi R, Randall JC, Vedantam S, Winkler TW, Qi L, Workalemahu T, Heid IM, Steinthorsdottir V, Stringham HM, Weedon MN, Wheeler E, Wood AR, Ferreira T, Weyant RJ, Segre AV, Estrada K, Liang L, Nemesh J, Park JH, Gustafsson S, Kilpelainen TO, Yang J, Bouatia-Naji N, Esko T, Feitosa MF, Kutalik Z, Mangino M, Raychaudhuri S, Scherag A, Smith AV, Welch R, Zhao JH, Aben KK, Absher DM, Amin N, Dixon AL, Fisher E, Glazer NL, Goddard ME, Heard-Costa NL, Hoesel V, Hottenga JJ, Johansson A, Johnson T, Ketkar S, Lamina C, Li S, Moffatt MF, Myers RH, Narisu N, Perry JR, Peters MJ, Preuss M, Ripatti S, Rivadeneira F, Sandholt C, Scott LJ, Timpson NJ, Tyrer JP, van Wingerden S, Watanabe RM, White CC, Wiklund F, Barlassina C, Chasman DI, Cooper MN, Jansson JO, Lawrence RW, Pellikka N, Prokopenko I, Shi J, Thiering E, Alavere H, Alibrandi MT, Almgren P, Arnold AM, Aspelund T, Atwood LD, Balkau B, Balmforth AJ, Bennett AJ, Ben-Shlomo Y, Bergman RN, Bergmann S, Biebermann H, Blakemore AI, Boes T, Bonnycastle LL, Bornstein SR, Brown MJ, Buchanan TA, Busonero F, Campbell H, Cappuccio FP, Cavalcanti-Proenca C, Chen YD, Chen CM, Chines PS, Clarke R, Coin L, Connell J, Day IN, den Heijer M, Duan J, Ebrahim S, Elliott P, Elosua R, Eiriksdottir G, Erdos MR, Eriksson JG, Facheris MF, Felix SB, Fischer-Posovszky P, Folsom AR, Friedrich N, Freimer NB, Fu M, Gaget S, Gejman PV, Geus EJ, Gieger C, Gjesing AP, Goel A, Goyette P, Grallert H, Grassler J, Greenawalt DM, Groves CJ, Gudnason V, Guiducci C, Hartikainen AL, Hassanali N, Hall AS, Havulinna AS, Hayward C, Heath AC, Hengstenberg C, Hicks AA, Hinney A, Hofman A, Homuth G, Hui J, Igl W, Iribarren C, Isomaa B, Jacobs KB, Jarick I, Jewell E, John U, Jorgensen T, Jousilahti P, Jula A, Kaakinen M, Kajantie E, Kaplan LM, Kathiresan S, Kettunen J, Kinnunen L, Knowles JW, Kolcic I, Konig IR, Koskinen S, Kovacs P, Kuusisto J, Kraft P, Kvaloy K, Laitinen J, Lantieri O, Lanzani C, Launer LJ, Lecoeur C, Lehtimaki T, Lettre G, Liu J, Lokki ML, Lorentzon M, Luben RN, Ludwig B, Magic Manunta P, Marek D, Marre M, Martin NG, McArdle WL, McCarthy A, McKnight B, Meitinger T, Melander O, Meyre D, Midthjell K, Montgomery GW, Morken MA, Morris AP, Mulic R, Ngwa JS, Nelis M, Neville MJ, Nyholt DR, O’Donnell CJ, O’Rahilly S, Ong KK, Oostra B, Pare G, Parker AN, Perola M, Pichler I, Pietilainen KH, Platou CG, Polasek O, Pouta A, Rafelt S, Raitakari O, Rayner NW, Ridderstrale M, Rief W, Ruokonen A, Robertson NR, Rzehak P, Salomaa V, Sanders AR, Sandhu MS, Sanna S, Saramies J, Savolainen MJ, Scherag S, Schipf S, Schreiber S, Schunkert H, Silander K, Sinisalo J, Siscovick DS, Smit JH, Soranzo N, Sovio U, Stephens J, Surakka I, Swift AJ, Tammesoo ML, Tardif JC, Teder-Laving M, Teslovich TM, Thompson JR, Thomson B, Tonjes A, Tuomi T, van Meurs JB, van Ommen GJ, Vatin V, Viikari J, Visvikis-Siest S, Vitart V, Vogel CI, Voight BF, Waite LL, Wallaschofski H, Walters GB, Widen E, Wiegand S, Wild SH, Willemsen G, Witte DR, Witteman JC, Xu J, Zhang Q, Zgaga L, Ziegler A, Zitting P, Beilby JP, Farooqi IS, Hebebrand J, Huikuri HV, James AL, Kahonen M, Levinson DF, Macciardi F, Nieminen MS, Ohlsson C, Palmer LJ, Ridker PM, Stumvoll M, Beckmann JS, Boeing H, Boerwinkle E, Boomsma DI, Caulfield MJ, Chanock SJ, Collins FS, Cupples LA, Smith GD, Erdmann J, Froguel P, Gronberg H, Gyllensten U, Hall P, Hansen T, Harris TB, Hattersley AT, Hayes RB, Heinrich J, Hu FB, Hveem K, Illig T, Jarvelin MR, Kaprio J, Karpe F, Khaw KT, Kiemeney LA, Krude H, Laakso M, Lawlor DA, Metspalu A, Munroe PB, Ouwehand WH, Pedersen O, Penninx BW, Peters A, Pramstaller PP, Quertermous T, Reinehr T, Rissanen A, Rudan I, Samani NJ, Schwarz PE, Shuldiner AR, Spector TD, Tuomilehto J, Uda M, Uitterlinden A, Valle TT, Wabitsch M, Waeber G, Wareham NJ, Watkins H, Procardis C, Wilson JF, Wright AF, Zillikens MC, Chatterjee N, McCarroll SA, Purcell S, Schadt EE, Visscher PM, Assimes TL, Borecki IB, Deloukas P, Fox CS, Groop LC, Haritunians T, Hunter DJ, Kaplan RC, Mohlke KL, O’Connell JR, Peltonen L, Schlessinger D, Strachan DP, van Duijn CM, Wichmann HE, Frayling TM, Thorsteinsdottir U, Abecasis GR, Barroso I, Boehnke M, Stefansson K, North KE, McCarthy MI, Hirschhorn JN, Ingelsson E, Loos RJ (2010) Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nat Genet 42(11):937–948. doi:10.1038/ng.686
36. van Helden YG, Godschalk RW, Heil SG, Bunschoten A, Hessel S, Amengual J, Bonet ML, von Lintig J, van Schooten FJ, Keijer J (2010) Downregulation of Fzd6 and Cthrc1 and upregulation of olfactory receptors and protocadherins by dietary beta-carotene in lungs of Bcmo1-/-mice. Carcinogenesis 31(8):1329–1337. doi:10.1093/carcin/bgq083
37. Walley AJ, Blakemore AI, Froguel P (2006) Genetics of obesity and the prediction of risk for health. Human molecular genetics 15(Spec No 2):R124–R130. doi:10.1093/hmg/ddl215
38. Wheeler E, Huang N, Bochukova EG, Keogh JM, Lindsay S, Garg S, Henning E, Blackburn H, Loos RJ, Wareham NJ, O’Rahilly S, Hurles ME, Barroso I, Farooqi IS (2013) Genome-wide SNP and CNV analysis identifies common and low-frequency variants associated with severe early-onset obesity. Nat Genet 45(5):513–517. doi:10.1038/ng.2607