Deep congenic analysis identifies many strong, context-dependent QTLs, one of which, Slc35b4, regulates obesity and glucose homeostasis

Genome Research

Volumn 21, Issue 7, 2011, Pages 1065-1073

  Yazbek, Soha N ^a,b   Buchner, David A ^a,c   Geisinger, Jonathan M ^a   Burrage, Lindsay C ^a,d   Spiezio, Sabrina H ^a,e   Zentner, Gabriel E ^a   Hsieh, Chang Wen ^a   Scacheri, Peter C ^a   Croniger, Colleen M ^a,c   Nadeau, Joseph H ^a,e  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^e INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHROMOSOME 6; CHROMOSOME SUBSTITUTION; CONTROLLED STUDY; DIET; GENETIC ANALYSIS; GENETIC IDENTIFICATION; GENETIC RECOMBINATION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GLUCONEOGENESIS; GLUCOSE HOMEOSTASIS; HUMAN; HUMAN CELL; INSULIN RESISTANCE; METABOLIC DISORDER; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS MAPPING;

ANIMALS; BODY WEIGHT; CHROMOSOME MAPPING; CHROMOSOMES, MAMMALIAN; DIABETES MELLITUS, TYPE 2; DIET; GENE EXPRESSION REGULATION; GLUCONEOGENESIS; GLUCOSE; HEP G2 CELLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOMEOSTASIS; HUMANS; INSULIN RESISTANCE; MALE; MICE; MICE, CONGENIC; MODELS, ANIMAL; NUCLEOTIDE TRANSPORT PROTEINS; OBESITY; PHENOTYPE; QUANTITATIVE TRAIT LOCI; SEQUENCE ANALYSIS, DNA;

MUS;

EID: 79959888771     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.120741.111     Document Type: Article

References (59)

1. Altshuler D, Daly MJ, Lander ES. 2008. Genetic mapping in human disease. Science 322: 881-888.
2. Arya R, Blangero J, Williams K, Almasy L, Dyer TD, Leach RJ, O'Connell P, Stern MP, Duggirala R. 2002. Factors of insulin resistance syndrome-related phenotypes are linked to genetic locations on chromosomes 6 and 7 in nondiabetic Mexican-Americans. Diabetes 51: 841-847. (Pubitemid 34760198)
3. Ashikov A, Routier F, Fuhlrott J, Helmus Y, Wild M, Gerardy-Schahn R, Bakker H. 2005. The human solute carrier gene SLC35B4 encodes a bifunctional nucleotide sugar transporter with specificity for UDP-xylose and UDP-N-acetylglucosamine. J Biol Chem 280: 27230-27235. (Pubitemid 41040762)
4. Ayala JE, Bracy DP, McGuinness OP, Wasserman DH. 2006. Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 55: 390-397. (Pubitemid 43343268)
5. Aylor DL, Valdar W, Foulds-Mathes W, Buus RJ, Verdugo RA, Baric RS, Ferris MT, Frelinger JA, Heise M, Frieman MB, et al. 2011. Genetic analysis of complext traits in the emerging collaborative cross. Genome Res (in press). doi: 10.1101/gr.111310.110.
6. Brown KM, MacGregor S, Montgomery GW, Craig DW, Zhao ZZ, Iyadurai KK, Henders A, Homer N, Campbel, MJ, Stark M, et al. 2008. Common sequence variants on 20q11.22 confer melanoma susceptibility. Nat Genet 40: 838-840. (Pubitemid 351913651)
7. Brunetti-Pierri N, Berg JS, Scaglia F, Belmont J, Bacino CA, Sahoo T, Lalani SR, Graham B, Lee B, Shinawi M, et al. 2008. Recurrent reciprocal 1q21.1 deletions and duplications associated with microcephaly or macrocephaly and developmental and behavioral abnormalities. Nat Genet 40: 1466-1471.
8. Buchner DA, Burrage LC, Hill AE, Yazbek SN, O'Brien WE, Croniger CM, Nadeau JH. 2008. Resistance to diet-induced obesity in mice with a single substituted chromosome. Physiol Genomics 35: 116-122.
9. Buchner DA, Yazbek SN, Solinas P, Burrage LC, Morgan MG, Hoppel CL, Nadeau JH. 2010. Increased mitochondrial oxidative phosphorylation in the liver is associated with obesity and insulin resistance. Obesity (Silver Spring) 19: 917-924.
10. Burrage L, Baskin-Hill A, Sinasac D, Singer J, Croniger C, Kirby A, Kulbokas E, Daly M, Lander E, Broman K, et al. 2010. Genetic resistance to diet-induced obesity in chromosome substitution strains of mice. Mamm Genome 21: 115-129.
11. Cecil JE, Tavendale R, Watt P, Hetherington MM, Palmer CNA. 2008. An obesity-associated FTO gene variant and increased energy intake in children. N Engl J Med 359: 2558-2566.
12. Cunningham F, Rios D, Griffiths M, Smith J, Ning Z, Cox T, Flicek P, Marin-Garcin P, Herrero J, Rogers J, et al. 2006. Transcript SNP View: a genomewide catalog of mouse coding variation. Nat Genet 38: 853. (Pubitemid 44141641)
13. Di Bernardo MC, Crowther-Swanepoel D, Broderick P, Webb E, Sellick G, Wild R, Sullivan K, Vijayakrishnan J, Wang Y, Pittman AM, et al. 2008. A genome-wide association study identifies six susceptibility loci for chronic lymphocytic leukemia. Nat Genet 40: 1204-1210.
14. Ehrenreich IM, Torabi N, Jia Y, Kent J, Martis S, Shapiro JA, Gresham D, Caudy AA, Kruglyak L. 2010. Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464: 1039-1042.
15. Emison ES, McCallion AS, Kashuk CS, Bush RT, Grice E, Lin S, Portnoy ME, Cutler DJ, Green ED, Chakravarti A. 2005. A common sex-dependent mutation in a RET enhancer underlies Hirschsprung disease risk. Nature 434: 857-863. (Pubitemid 40558992)
16. Erkko H, Xia B, Nikkila J, Schleutker J, Syrjakoski K, Mannermaa A, Kallioniemi A, Pylkas K, Karppinen SM, Rapakko K, et al. 2007. A recurrent mutation in PALB2 in Finnish cancer families. Nature 446: 316-319. (Pubitemid 46426155)
17. Feitosa MF, Borecki IB, Rich SS, Arnett DK, Sholinsky P, Myers RH, Leppert M, Province MA. 2002. Quantitative-trait loci influencing body-mass index reside on chromosomes 7 and 13: the National Heart, Lung, and Blood Institute Family Heart Study. Am J Hum Genet 70: 72-82. (Pubitemid 34031699)
18. Flint J, Mackay TF. 2009. Genetic architecture of quantitative traits in mice, flies, and humans. Genome Res 19: 723-733.
19. Fox CS, Heard-Costa N, Cupples LA, Dupuis J, Vasan RS, Atwood LD. 2007. Genome-wide association to body mass index and waist circumference: the Framingham Heart Study 100K project. BMC Med Genet 8 (Suppl 1) : S18. doi: 10.1186/1471-2350-8-S1-S18.
20. Gerken T, Girard CA, Tung Y-CL, Webby CJ, Saudek V, Hewitson KS, Yeo GSH, McDonough MA, Cunliffe S, McNeill LA, et al. 2007. The obesity-associated FTO gene encodes a 2-oxoglutarate-dependent nucleic acid demethylase. Science 318: 1469-1472. (Pubitemid 350208961)
21. Gibson G. 2009. Decanalization and the origin of complex disease. Nat Rev Genet 10: 134-140.
22. Goldstein DB. 2009. Common genetic variation and human traits. N Engl J Med 360: 1696-1698.
23. Halseth AE, Bracy DP, Wasserman DH. 1999. Overexpression of hexokinase II increases insulinand exercise-stimulated muscle glucose uptake in vivo. Am J Physiol 276: E70-E77. (Pubitemid 29065595)
24. Hill-Baskin AE, Markiewski MM, Buchner DA, Shao H, DeSantis D, Hsiao G, Subramaniam S, Berger NA, Croniger C, Lambris JD, et al. 2009. Diet-induced hepatocellular carcinoma in genetically predisposed mice. Hum Mol Genet 18: 2975-2988.
25. Inoue M, Chiang SH, Chang L, Chen XW, Saltiel AR. 2006. Compartmentalization of the exocyst complex in lipid rafts controls Glut4 vesicle tethering. Mol Biol Cell 17: 2303-2311. (Pubitemid 44011745)
26. Kruglyak L. 2008. The road to genome-wide association studies. Nat Rev Genet 9: 314-318. (Pubitemid 351399831)
27. Laramie JM, Wilk JB, Williamson SL, Nagle MW, Latourelle JC, Tobin JE, Province MA, Borecki IB, Myers RH. 2008. Polymorphisms near EXOC4 and LRGUK on chromosome 7q32 are associated with type 2 diabetes and fasting glucose: the NHLBI Family Heart Study. BMC Med Genet 9: 46.
28. Love DC, Hanover JA. 2005. The hexosamine signaling pathway: deciphering the "O-GlcNAc code". Sci STKE 2005: re13. doi: 10.1126/stke. 3122005re13.
29. Lyons PD, Peck GR, Kettenbach AN, Gerber SA, Roudaia L, Lienhard GE. 2009. Insulin stimulates the phosphorylation of the exocyst protein Sec8 in adipocytes. Biosci Rep 29: 229-235.
30. Mackay TFC, Stone EA, Ayroles JF. 2009. The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10: 565-577.
31. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, et al. 2009. Finding the missing heritability of complex diseases. Nature 461: 747-753.
32. Matin A, Collin GB, Asada Y, Varnum D, Nadeau JH. 1999. Susceptibility to testicular germ-cell tumours in a 129.MOLF-Chr 19 chromosome substitution strain. Nat Genet 23: 237-240. (Pubitemid 29455401)
33. McClellan J, King M-C. 2010. Genetic heterogeneity in human disease. Cell 141: 210-217.
34. Meijers-Heijboer H, van den Ouweland A, Klijn J, Wasielewski M, de Snoo A, Oldenburg R, Hollestelle A, Houben M, Crepin E, van Veghel-Plandsoen M, et al. 2002. Low-penetrance susceptibility to breast cancer due to CHEK2(*)1100delC in noncarriers of BRCA1 or BRCA2 mutations. Nat Genet 31: 55-59.
35. Millward CA, Burrage LC, Shao H, Sinasac DS, Kawasoe JH, Hill-Baskin AE, Ernest SR, Gornicka A, Hsieh CW, Pisano S, et al. 2009. Genetic factors for resistance to diet-induced obesity and associated metabolic traits on mouse chromosome 17. Mamm Genome 20: 71-82.
36. Mott R, Flint J. 2008. Prospects for complex trait analysis in the mouse. Mamm Genome 19: 306-308.
37. Nadeau JH. 2009. Transgenerational genetic effects on phenotypic variation and disease risk. Hum Mol Genet 18: R202-R210.
38. Nadeau JH, Singer JB, Matin A, Lander ES. 2000. Analysing complex genetic traits with chromosome substitution strains. Nat Genet 24: 221-225. (Pubitemid 30132188)
39. Papaemmanuil E, Hosking FJ, Vijayakrishnan J, Price A, Olver B, Sheridan E, Kinsey SE, Lightfoot T, Roman E, Irving JA, et al. 2009. Loci on 7p12.2, 10q21.2 and 14q11.2 are associated with risk of childhood acute lymphoblastic leukemia. Nat Genet 41: 1006-1010.
40. Phillips PC. 2008. Epistasis: the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9: 855-867.
41. Plank J, Blaha J, Cordingley J, Wilinska ME, Chassin LJ, Morgan C, Squire S, Haluzik M, Kremen J, Svacina S, et al. 2006. Multicentric, randomized, controlled trial to evaluate blood glucose control by the model predictive control algorithm versus routine glucose management protocols in intensive care unit patients: Response to Ligtenberg et al. Diabetes Care 29: 1987-1988. (Pubitemid 44156675)
42. Previs SF, Ciraolo ST, Fernandez CA, Beylot M, Agarwal KC, Soloview MV, Brunengraber H. 1994. Use of [6,6-2H2]glucose and of low-enrichment [U-13C6]-glucose for sequential or simultaneous measurements of glucose turnover by gas chromatography-mass spectrometry. Anal Biochem 218: 192-196.
43. Rahman N, Seal S, Thompson D, Kelly P, Renwick A, Elliott A, Reid S, Spanova K, Barfoot R, Chagtai T, et al. 2007. PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene. Nat Genet 39: 165-167. (Pubitemid 46184346)
44. Renwick A, Thompson D, Seal S, Kelly P, Chagtai T, Ahmed M, North B, Jayatilake H, Barfoot R, Spanova K, et al. 2006. ATM mutations that cause ataxia-telangiectasia are breast cancer susceptibility alleles. Nat Genet 38: 873-875. (Pubitemid 44141653)
45. Saito T, Shibasaki T, Seino S. 2008. Involvement of Exoc3l, a protein structurally related to the exocyst subunit Sec6, in insulin secretion. Biomed Res 29: 85-91. (Pubitemid 351753467)
46. Saunders CL, Chiodini BD, Sham P, Lewis CM, Abkevich V, Adeyemo AA, de Andrade M, Arya R, Berenson GS, Blangero J, et al. 2007. Meta-analysis of genome-wide linkage studies in BMI and obesity. Obesity (Silver Spring) 15: 2263-2275.
47. Seal S, Thompson D, Renwick A, Elliott A, Kelly P, Barfoot R, Chagtai T, Jayatilake H, Ahmed M, Spanova K, et al. 2006. Truncating mutations in the Fanconi anemia J gene BRIP1 are low-penetrance breast cancer susceptibility alleles. Nat Genet 38: 1239-1241.
48. Shao H, Burrage LC, Sinasac DS, Hill AE, Ernest SR, O'Brien W, Courtland HW, Jepsen KJ, Kirby A, Kulbokas EJ, et al. 2008. Genetic architecture of complex traits: large phenotypic effects and pervasive epistasis. Proc Natl Acad Sci 105: 19910-19914.
49. Shao H, Sinasac DS, Burrage LC, Hodges CA, Supelak PJ, Palmert MR, Moreno C, Cowley MA, Jacob HJ, Nadeau JH. 2010. Analyzing complex traits with congenic strains. Mamm Genome 21: 276-286.
50. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050. (Pubitemid 41126859)
51. Singer JB, Hill AE, Burrage LC, Olszens KR, Song J, Justice M, O'Brien WE, Conti DV, Witte JS, Lander ES, et al. 2004. Genetic dissection of complex traits with chromosome substitution strains ofmice. Science 304: 445-448. (Pubitemid 38495941)
52. Stolerman ES, Florez JC. 2009. Genomics of type 2 diabetes mellitus: implications for the clinician. Nat Rev Endocrinol 5: 429-436.
53. Tang W, Miller MB, Rich SS, North KE, Pankow JS, Borecki IB, Myers RH, Hopkins PN, Leppert M, Arnett DK. 2003. Linkage analysis of a composite factor for the multiple metabolic syndrome: the National Heart, Lung, and Blood Institute Family Heart Study. Diabetes 52: 2840-2847. (Pubitemid 37339715)
54. Teo CF, Wollaston-Hayden EE, Wells L. 2010. Hexosamine flux, the OGlcNAc modification, and the development of insulin resistance in adipocytes. Mol Cell Endocrinol 318: 44-53.
55. Tomlinson IPM, Webb E, Carvajal-Carmona L, Broderick P, Howarth K, Pittman AM, Spain S, Lubbe S, Walther A, Sullivan K, et al. 2008. A genome-wide association study identifies colorectal cancer susceptibility loci on chromosomes 10p14 and 8q23.3. Nat Genet 40:623-630. (Pubitemid 351601204)
56. Wahlsten D, Metten P, Phillips TJ, Boehm SL II, Berkhart-Kasch S, Dorow J, Doerksen S, Downing C, Fogarty J, Rodd-Henricks K, et al. 2003. Different data from different labs: Lessons from studies of gene-environment interaction. J Neurobiol 54: 283-311. (Pubitemid 36050068)
57. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW 3rd, et al. 2009. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10: R130. doi: 10.1186/gb-2009-10-11-r130.
58. Yang X, Ongusaha PP, Miles PD, Havstad JC, Zhang F, So WV, Kudlow JE, Michell RH, Olefsky JM, Field SJ, et al. 2008. Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance. Nature 451: 964-969. (Pubitemid 351301737)
59. Youngren KK, Nadeau JH, Matin A. 2003. Testicular cancer susceptibility in the 129.MOLF-Chr19 mouse strain: additive effects, gene interactions and epigenetic modifications. Hum Mol Genet 12: 389-398. (Pubitemid 36285131)