Fine-mapping a locus for glucose tolerance using heterogeneous stock rats

Physiological Genomics

Volumn 41, Issue 1, 2010, Pages 102-108

  Solberg Woods, Leah C ^a   Holl, Katie ^a   Tschannen, Michael ^a   Valdar, William ^b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Mapping; Mixed model analysis; Quantitative trait loci; Type 2 diabetes

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BOOTSTRAPPING; CHROMOSOME 1; GENE MAPPING; GENOTYPE; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; HAPLOTYPE; MALE; MICROSATELLITE MARKER; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; RAT; REGULATORY MECHANISM;

ANIMALS; AREA UNDER CURVE; CROSSES, GENETIC; FEMALE; GENETIC MARKERS; GLUCOSE TOLERANCE TEST; INJECTIONS, INTRAPERITONEAL; MALE; PHENOTYPE; PHYSICAL CHROMOSOME MAPPING; QUANTITATIVE TRAIT LOCI; RATS;

ANIMALIA; RATTUS;

EID: 77949706465     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00178.2009     Document Type: Article

References (49)

1. Caballero A, Toro MA. Interrelations between effective population size and other pedigree tools for the management of conserved populations. Genet Res 75: 331-343, 2000.
2. Cho YM, Park KS, Lee HK. Genetic factors related to mitochondrial function and risk of diabetes mellitus. Diabetes Res Clin Pract 77, Suppl 1: S172-S177, 2007.
3. Chung WK, Zheng M, Chua M, Kershaw E, Power-Kehoe L, Tsuji M, Wu-Peng XS, Williams J, Chua SC Jr, Leibel RL. Genetic modifiers of Leprfa associated with variability in insulin production and susceptibility to NIDDM. Genomics 41: 332-344, 1997.
4. Churchill GA, Doerge RW. Naive application of permutation testing leads to inflated type I error rates. Genetics 178: 609-610, 2008.
5. Collins SC, Wallis RH, Wilder SP, Wallace KJ, Argoud K, Kaisaki PJ, Bihoreau MT, Gauguier D. Mapping diabetes QTL in an intercross derived from a congenic strain of the Brown Norway and Goto-Kakizaki rats. Mamm Genome 17: 538-547, 2006.
6. Duggirala R, Blangero J, Almasy L, Dyer TD, Williams KL, Leach RJ, O'Connell P, Stern MP. Linkage of type 2 diabetes mellitus and of age at onset to a genetic location on chromosome 10q in Mexican Americans. Am J Hum Genet 64: 1127-1140, 1999.
7. Fakhrai-Rad H, Nikoshkov A, Kamel A, Fernstrom M, Zierath JR, Norgren S, Luthman H, Galli J. Insulin-degrading enzyme identified as a candidate diabetes susceptibility gene in GK rats. Hum Mol Genet 9: 2149-2158, 2000.
8. Florez JC, Burtt N, de Bakker PI, Almgren P, Tuomi T, Holmkvist J, Gaudet D, Hudson TJ, Schaffner SF, Daly MJ, Hirschhorn JN, Groop L, Altshuler D. Haplotype structure and genotype-phenotype correlations of the sulfonylurea receptor and the islet ATP-sensitive potassium channel gene region. Diabetes 53: 1360-1368, 2004.
9. Fullerton JM, Willis-Owen SA, Yalcin B, Shifman S, Copley RR, Miller SR, Bhomra A, Davidson S, Oliver PL, Mott R, Flint J. Human-mouse quantitative trait locus concordance and the dissection of a human neuroticism locus. Biol Psychiatry 63: 874-883, 2008.
10. Galli J, Fakhrai-Rad H, Kamel A, Marcus C, Norgren S, Luthman H. Pathophysiological and genetic characterization of the major diabetes locus in GK rats. Diabetes 48: 2463-2470, 1999.
11. Galli J, Li LS, Glaser A, Ostenson CG, Jiao H, Fakhrai-Rad H, Jacob HJ, Lander ES, Luthman H. Genetic analysis of non-insulin dependent diabetes mellitus in the GK rat. Nat Genet 12: 31-37, 1996.
12. Gauguier D, Froguel P, Parent V, Bernard C, Bihoreau MT, Portha B, James MR, Penicaud L, Lathrop M, Ktorza A. Chromosomal mapping of genetic loci associated with non-insulin dependent diabetes in the GK rat. Nat Genet 12: 38-43, 1996.
13. Ghazalpour A, Doss S, Kang H, Farber C, Wen PZ, Brozell A, Castellanos R, Eskin E, Smith DJ, Drake TA, Lusis AJ. High-resolution mapping of gene expression using association in an outbred mouse stock. PLoS Genet 4: e1000149, 2008.
14. Ghosh S, Watanabe RM, Valle TT, Hauser ER, Magnuson VL, Langefeld CD, Ally DS, Mohlke KL, Silander K, Kohtamaki K, Chines P, Balow J Jr, Birznieks G, Chang J, Eldridge W, Erdos MR, Karanjawala ZE, Knapp JI, Kudelko K, Martin C, Morales-Mena A, Musick A, Musick T, Pfahl C, Porter R, Rayman JB. The Finland-United States investigation of non-insulin-dependent diabetes mellitus genetics (FUSION) study. I. An autosomal genome scan for genes that predispose to type 2 diabetes. Am J Hum Genet 67: 1174-1185, 2000.
15. Granhall C, Park HB, Fakhrai-Rad H, Luthman H. High-resolution quantitative trait locus analysis reveals multiple diabetes susceptibility loci mapped to intervals<800 kb in the species-conserved Niddm1i of the GK rat. Genetics 174: 1565-1572, 2006.
16. Hansen C, Spuhler K. Development of the National Institutes of Health genetically heterogeneous rat stock. Alcohol Clin Exp Res 8: 477-479, 1984.
17. Ikeda H, Shino A, Matsuo T, Iwatsuka H, Suzuoki Z. A new genetically obese-hyperglycemic rat (Wistar fatty). Diabetes 30: 1045-1050, 1981.
18. Johannesson M, Lopez-Aumatell R, Stridh P, Diez M, Tuncel J, Blazquez G, Martinez-Membrives E, Canete T, Vicens-Costa E, Graham D, Copley RR, Hernandez-Pliego P, Beyeen AD, Ockinger J, Fernandez-Santamaria C, Gulko PS, Brenner M, Tobena A, Guitart-Masip M, Gimenez-Llort L, Dominiczak A, Holmdahl R, Gauguier D, Olsson T, Mott R, Valdar W, Redei EE, Fernandez-Teruel A, Flint J. A resource for the simultaneous high-resolution mapping of multiple quantitative trait loci in rats: the NIH heterogeneous stock. Genome Res 19: 150-158, 2009.
19. Jun G, Song Y, Stein CM, Iyengar SK. An autosome-wide search using longitudinal data for loci linked to type 2 diabetes progression. BMC Genet 4, Suppl 1: S8, 2003.
20. Kanemoto N, Hishigaki H, Miyakita A, Oga K, Okuno S, Tsuji A, Takagi T, Takahashi E, Nakamura Y, Watanabe TK. Genetic dissection of "OLETF", a rat model for non-insulin-dependent diabetes mellitus. Mamm Genome 9: 419-425, 1998.
21. Katayama S, Inaba M, Maruno Y, Morita T, Awata T, Oka Y. Glucose intolerance in spontaneously hypertensive and Wistar-Kyoto rats: enhanced gene expression and synthesis of skeletal muscle glucose transporter 4. Hypertens Res 20: 279-286, 1997.
22. Kennedy BW, Quinton M, van Arendonk JA. Estimation of effects of single genes on quantitative traits. J Anim Sci 70: 2000-2012, 1992.
23. Kimura M, Crow JF. On maximum avoidance of inbreeding. Genet Res 4: 399, 1963.
24. Lacraz G, Giroix MH, Kassis N, Coulaud J, Galinier A, Noll C, Cornut M, Schmidlin F, Paul JL, Janel N, Irminger JC, Kergoat M, Portha B, Donath MY, Ehses JA, Homo-Delarche F. Islet endothelial activation and oxidative stress gene expression is reduced by IL-1Ra treatment in the type 2 diabetic GK rat. PLoS One 4: e6963, 2009.
25. Lango H, Palmer CN, Morris AD, Zeggini E, Hattersley AT, Mc-Carthy MI, Frayling TM, Weedon MN. Assessing the combined impact of 18 common genetic variants of modest effect sizes on type 2 diabetes risk. Diabetes 57: 3129-3135, 2008.
26. Lin JM, Ortsater H, Fakhrai-Rad H, Galli J, Luthman H, Bergsten P. Phenotyping of individual pancreatic islets locates genetic defects in stimulus secretion coupling to Niddm1i within the major diabetes locus in GK rats. Diabetes 50: 2737-2743, 2001.
27. Lindgren CM, Mahtani MM, Widen E, McCarthy MI, Daly MJ, Kirby A, Reeve MP, Kruglyak L, Parker A, Meyer J, Almgren P, Lehto M, Kanninen T, Tuomi T, Groop LC, Lander ES. Genomewide search for type 2 diabetes mellitus susceptibility loci in Finnish families: the Botnia study. Am J Hum Genet 70: 509-516, 2002.
28. Meigs JB, Panhuysen CI, Myers RH, Wilson PW, Cupples LA. A genome-wide scan for loci linked to plasma levels of glucose and HbA(1c) in a community-based sample of Caucasian pedigrees: The Framingham Offspring Study. Diabetes 51: 833-840, 2002.
29. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273, 2003.
30. Moreno C, Kennedy K, Andrae JW, Jacob HJ. Genome-wide scanning with SSLPs in the rat. Methods Mol Med 108: 131-138, 2005.
31. Mott R, Talbot CJ, Turri MG, Collins AC, Flint J. A method for fine mapping quantitative trait loci in outbred animal stocks. Proc Natl Acad Sci USA 97: 12649-12654, 2000.
32. Nobrega MA, Woods LC, Fleming S, Jacob HJ. Distinct genetic regulation of progression of diabetes and renal disease in the Goto-Kakizaki rat. Physiol Genomics 39: 38-46, 2009.
33. Rieseberg LH, Widmer A, Arntz AM, Burke JM. The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Philos Trans R Soc Lond B Biol Sci 358: 1141-1147, 2003.
34. Saxena R, Voight BF, Lyssenko V, Burtt NP, de Bakker PI, Chen H, Roix JJ, Kathiresan S, Hirschhorn JN, Daly MJ, Hughes TE, Groop L, Altshuler D, Almgren P, Florez JC, Meyer J, Ardlie K, Bengtsson Bostrom K, Isomaa B, Lettre G, Lindblad U, Lyon HN, Melander O, Newton-Cheh C, Nilsson P, Orho-Melander M, Rastam L, Speliotes EK, Taskinen MR, Tuomi T, Guiducci C, Berglund A, Carlson J, Gianniny L, Hackett R, Hall L, Holmkvist J, Laurila E, Sjogren M, Sterner M, Surti A, Svensson M, Tewhey R, Blumenstiel B, Parkin M, Defelice M, Barry R, Brodeur W, Camarata J, Chia N, Fava M, Gibbons J, Handsaker B, Healy C, Nguyen K, Gates C, Sougnez C, Gage D, Nizzari M, Gabriel SB, Chirn GW, Ma Q, Parikh H, Richardson D, Ricke D, Purcell S. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316: 1331-1336, 2007.
35. Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, Erdos MR, Stringham HM, Chines PS, Jackson AU, Prokunina-Olsson L, Ding CJ, Swift AJ, Narisu N, Hu T, Pruim R, Xiao R, Li XY, Conneely KN, Riebow NL, Sprau AG, Tong M, White PP, Hetrick KN, Barnhart MW, Bark CW, Goldstein JL, Watkins L, Xiang F, Saramies J, Buchanan TA, Watanabe RM, Valle TT, Kinnunen L, Abecasis GR, Pugh EW, Doheny KF, Bergman RN, Tuomilehto J, Collins FS, Boehnke M. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 316: 1341-1345, 2007.
36. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, Serre D, Boutin P, Vincent D, Belisle A, Hadjadj S, Balkau B, Heude B, Charpentier G, Hudson TJ, Montpetit A, Pshezhetsky AV, Prentki M, Posner BI, Balding DJ, Meyre D, Polychronakos C, Froguel P. A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445: 881-885, 2007.
37. Solberg Woods LC, Ahmadiyeh N, Baum A, Shimomura K, Li Q, Steiner DF, Turek FW, Takahashi JS, Churchill GA, Redei EE. Identification of genetic loci involved in diabetes using a rat model of depression. Mamm Genome 20: 486-497, 2009.
38. Steinthorsdottir V, Thorleifsson G, Reynisdottir I, Benediktsson R, Jonsdottir T, Walters GB, Styrkarsdottir U, Gretarsdottir S, Emilsson V, Ghosh S, Baker A, Snorradottir S, Bjarnason H, Ng MC, Hansen T, Bagger Y, Wilensky RL, Reilly MP, Adeyemo A, Chen Y, Zhou J, Gudnason V, Chen G, Huang H, Lashley K, Doumatey A, So WY, Ma RC, Andersen G, Borch-Johnsen K, Jorgensen T, van Vliet-Ostaptchouk JV, Hofker MH, Wijmenga C, Christiansen C, Rader DJ, Rotimi C, Gurney M, Chan JC, Pedersen O, Sigurdsson G, Gulcher JR, Thorsteinsdottir U, Kong A, Stefansson K. A variant in CDKAL1 influences insulin response and risk of type 2 diabetes. Nat Genet 39: 770-775, 2007.
39. Talbot CJ, Radcliffe RA, Fullerton J, Hitzemann R, Wehner JM, Flint J. Fine scale mapping of a genetic locus for conditioned fear. Mamm Genome 14: 223-230, 2003.
40. Valdar W, Holmes CC, Mott R, Flint J. Mapping in structured populations by resample model averaging. Genetics 182: 1263-1277, 2009.
41. Valdar W, Solberg LC, Gauguier D, Burnett S, Klenerman P, Cookson WO, Taylor MS, Rawlins JN, Mott R, Flint J. Genome-wide genetic association of complex traits in heterogeneous stock mice. Nat Genet 38: 879-887, 2006.
42. Vionnet N, Hani EH, Lesage S, Philippi A, Hager J, Varret M, Stoffel M, Tanizawa Y, Chiu KC, Glaser B, Permutt MA, Passa P, Demenais F, Froguel P. Genetics of NIDDM in France: studies with 19 candidate genes in affected sib pairs. Diabetes 46: 1062-1068, 1997.
43. Visscher PM, Thompson R, Haley CS. Confidence intervals in QTL mapping by bootstrapping. Genetics 143: 1013-1020, 1996.
44. Wallis RH, Collins SC, Kaisaki PJ, Argoud K, Wilder SP, Wallace KJ, Ria M, Ktorza A, Rorsman P, Bihoreau MT, Gauguier D. Pathophysiological, genetic and gene expression features of a novel rodent model of the cardio-metabolic syndrome. PLoS ONE 3: e2962, 2008.
45. Wallis RH, Wang K, Marandi L, Hsieh E, Ning T, Chao GY, Sarmiento J, Paterson AD, Poussier P. Type 1 diabetes in the BB rat: a polygenic disease. Diabetes 58: 1007-1017, 2009.
46. Wei S, Wei K, Moralejo DH, Ogino T, Koike G, Jacob HJ, Sugiura K, Sasaki Y, Yamada T, Matsumoto K. Mapping and characterization of quantitative trait loci for non-insulin-dependent diabetes mellitus with an improved genetic map in the Otsuka Long-Evans Tokushima fatty rat. Mamm Genome 10: 249-258, 1999.
47. Wiltshire S, Hattersley AT, Hitman GA, Walker M, Levy JC, Sampson M, O'Rahilly S, Frayling TM, Bell JI, Lathrop GM, Bennett A, Dhillon R, Fletcher C, Groves CJ, Jones E, Prestwich P, Simecek N, Rao PV, Wishart M, Bottazzo GF, Foxon R, Howell S, Smedley D, Cardon LR, Menzel S, McCarthy MI. A genomewide scan for loci predisposing to type 2 diabetes in a UK population (the Diabetes UK Warren 2 Repository): analysis of 573 pedigrees provides independent replication of a susceptibility locus on chromosome 1q. Am J Hum Genet 69: 553-569, 2001.
48. Yalcin B, Flint J, Mott R. Using progenitor strain information to identify quantitative trait nucleotides in outbred mice. Genetics 2005.
49. Zeggini E, Weedon MN, Lindgren CM, Frayling TM, Elliott KS, Lango H, Timpson NJ, Perry JR, Rayner NW, Freathy RM, Barrett JC, Shields B, Morris AP, Ellard S, Groves CJ, Harries LW, Marchini JL, Owen KR, Knight B, Cardon LR, Walker M, Hitman GA, Morris AD, Doney AS, McCarthy MI, Hattersley AT. Replication of genomewide association signals in UK samples reveals risk loci for type 2 diabetes. Science 316: 1336-1341, 2007.