Genomic structure of nucleotide diversity among Lyon rat models of metabolic syndrome

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Ma, Man Chun J ^a   Atanur, Santosh S ^b   Aitman, Timothy J ^b   Kwitek, Anne E ^a  

^a UNIVERSITY OF IOWA   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Evolution; Genetic mapping; Genome sequence; Metabolic syndrome; Nucleotide diversity; Rat genetic model

Indexed keywords

NUCLEOTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTIFICIAL SELECTION; CONTROLLED STUDY; GENE IDENTIFICATION; GENETIC VARIABILITY; GENOME ANALYSIS; HAPLOTYPE; METABOLIC SYNDROME X; NONHUMAN; PHENOTYPIC VARIATION; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; RAT; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; STRAIN DIFFERENCE; STRUCTURE ANALYSIS;

ANIMALS; CHROMOSOME MAPPING; DISEASE MODELS, ANIMAL; GENOME-WIDE ASSOCIATION STUDY; GENOMICS; HAPLOTYPES; MALE; METABOLIC SYNDROME X; PHENOTYPE; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; RATS; REPRODUCIBILITY OF RESULTS;

EID: 84899098966     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-197     Document Type: Article

References (67)

1. Alberti KGMM, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart J-C, James WPT, Loria CM, Smith SC. Harmonizing the Metabolic Syndrome. Circulation 2009, 120:1640-1645. 10.1161/CIRCULATIONAHA.109.192644, 19805654.
2. Ervin RB. Prevalence of metabolic syndrome among adults 20 years of age and over, by sex, age, race and ethnicity, and body mass index: United States, 2003-2006. Natl Health Stat Report 2009, 2009:1-7.
3. Dupont J, Dupont JC, Froment A, Milon H, Vincent M. Selection of three strains of rats with spontaneously different levels of blood pressure. Biomedicine 1973, 19:36-41.
4. Sassolas A, Vincent M, Benzoni D, Sassard J. Plasma Lipids in Genetically Hypertensive Rats of the Lyon Strain. J Cardiovasc Pharmacol 1981, 3:1008-1014. 10.1097/00005344-198109000-00011, 6168846.
5. Su DF, Cerutti C, Barres C, Vincent M, Sassard J. Blood pressure and baroreflex sensitivity in conscious hypertensive rats of Lyon strain. Am J Physiol 1986, 251:H1111-1117.
6. Vincent M, Boussairi EH, Cartier R, Lo M, Sassolas A, Cerutti C, Barres C, Gustin MP, Cuisinaud G, Samani NJ, Lathrop GM, Sassard J. High blood pressure and metabolic disorders are associated in the Lyon hypertensive rat. J Hypertens 1993, 11:1179-1185.
7. Vincent M, Cartier R, Privat P, Benzoni D, Samani NJ, Sassard J. Major cardiovascular risk factors in Lyon hypertensive rats. A correlation analysis in a segregating population. J Hypertens 1996, 14:469-474.
8. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. Prevalence of overweight and obesity in the United States, 1999-2004. Jama 2006, 295:1549-1555. 10.1001/jama.295.13.1549, 16595758.
9. Thom T, Haase N, Rosamond W, Howard VJ, Rumsfeld J, Manolio T, Zheng ZJ, Flegal K, O'Donnell C, Kittner S, Lloyd-Jones D, Goff DC, Hong Y, Adams R, Friday G, Furie K, Gorelick P, Kissela B, Marler J, Meigs J, Roger V, Sidney S, Sorlie P, Steinberger J, Wasserthiel-Smoller S, Wilson M, Wolf P. Heart disease and stroke statistics-2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2006, 113:e85-151. 10.1161/CIRCULATIONAHA.105.171600, 16407573.
10. Bilusic M, Bataillard A, Tschannen MR, Gao L, Barreto NE, Vincent M, Wang T, Jacob HJ, Sassard J, Kwitek AE. Mapping the genetic determinants of hypertension, metabolic diseases, and related phenotypes in the lyon hypertensive rat. Hypertension 2004, 44:695-701. 10.1161/01.HYP.0000144542.57306.5e, 15452030.
11. Thomas MA, Chen C-F, Jensen-Seaman MI, Tonellato PJ, Twigger SN. Phylogenetics of rat inbred strains. Mamm Genome 2003, 14:61-64. 10.1007/s00335-002-2204-5, 12532268.
12. Saar K, Beck A, Bihoreau MT, Birney E, Brocklebank D, Chen Y, Cuppen E, Demonchy S, Dopazo J, Flicek P, Foglio M, Fujiyama A, Gut IG, Gauguier D, Guigo R, Guryev V, Heinig M, Hummel O, Jahn N, Klages S, Kren V, Kube M, Kuhl H, Kuramoto T, Kuroki Y, Lechner D, Lee YA, Lopez-Bigas N, Lathrop GM, Mashimo T, et al. SNP and haplotype mapping for genetic analysis in the rat. Nat Genet 2008, 40:560-566. 10.1038/ng.124, 18443594.
13. Atanur SS, Diaz AG, Maratou K, Sarkis A, Rotival M, Game L, Tschannen MR, Kaisaki PJ, Otto GW, Ma MC, Keane TM, Hummel O, Saar K, Chen W, Guryev V, Gopalakrishnan K, Garrett MR, Joe B, Citterio L, Bianchi G, McBride M, Dominiczak A, Adams DJ, Serikawa T, Flicek P, Cuppen E, Hubner N, Petretto E, Gauguier D, Kwitek A, et al. Genome Sequencing Reveals Loci under Artificial Selection that Underlie Disease Phenotypes in the Laboratory Rat. Cell 2013, 154:691-703. 10.1016/j.cell.2013.06.040, 3732391, 23890820.
14. Gilibert S, Kwitek AE, Hubner N, Tschannen M, Jacob HJ, Sassard J, Bataillard A. Effects of chromosome 17 on features of the metabolic syndrome in the Lyon hypertensive rat. Physiol Genomics 2008, 33:212-217. 10.1152/physiolgenomics.00262.2007, 18285521.
15. Gilibert S, Bataillard A, Nussberger J, Sassard J, Kwitek AE. Implication of chromosome 13 on hypertension and associated disorders in Lyon hypertensive rats. J Hypertens 2009, 27:1186-1193. 10.1097/HJH.0b013e328329e4c0, 2915542, 19462495.
16. Albrechtsen A, Nielsen FC, Nielsen R. Ascertainment biases in SNP chips affect measures of population divergence. Mol Biol Evol 2010, 27:2534-2547. 10.1093/molbev/msq148, 3107607, 20558595.
17. Nielsen R, Signorovitch J. Correcting for ascertainment biases when analyzing SNP data: applications to the estimation of linkage disequilibrium. Theor Popul Biol 2003, 63:245-255. 10.1016/S0040-5809(03)00005-4, 12689795.
18. Gibbs RA, Weinstock GM, Metzker ML, Muzny DM, Sodergren EJ, Scherer S, Scott G, Steffen D, Worley KC, Burch PE, Okwuonu G, Hines S, Lewis L, DeRamo C, Delgado O, Dugan-Rocha S, Miner G, Morgan M, Hawes A, Gill R, Celera, Holt RA, Adams MD, Amanatides PG, Baden-Tillson H, Barnstead M, Chin S, Evans CA, Ferriera S, Fosler C. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 2004, 428:493-521.
19. Atanur SS, Birol I, Guryev V, Hirst M, Hummel O, Morrissey C, Behmoaras J, Fernandez-Suarez XM, Johnson MD, McLaren WM, Patone G, Petretto E, Plessy C, Rockland KS, Rockland C, Saar K, Zhao Y, Carninci P, Flicek P, Kurtz T, Cuppen E, Pravenec M, Hubner N, Jones SJ, Birney E, Aitman TJ. The genome sequence of the spontaneously hypertensive rat: Analysis and functional significance. Genome Res 2010, 20:791-803. 10.1101/gr.103499.109, 2877576, 20430781.
20. Laulederkind SJ, Hayman GT, Wang SJ, Smith JR, Lowry TF, Nigam R, Petri V, de Pons J, Dwinell MR, Shimoyama M, Munzenmaier DH, Worthey EA, Jacob HJ. The Rat Genome Database 2013-data, tools and users. Brief Bioinform 2013, 14:520-526. 10.1093/bib/bbt007, 3713714, 23434633.
21. Kin T, Ono Y. Idiographica: a general-purpose web application to build idiograms on-demand for human, mouse and rat. Bioinformatics (Oxford, England) 2007, 23:2945-2946.
22. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, Cunningham F. Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor. Bioinformatics (Oxford, England) 2010, 26:2069-2070.
23. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. A method and server for predicting damaging missense mutations. Nature methods 2010, 7:248-249. 10.1038/nmeth0410-248, 2855889, 20354512.
24. Ugarte A, Eguibar JR, Cortes Mdel C, Leon-Chavez BA, Melo AI. Comparative analysis of maternal care in the high-yawning (HY) and low-yawning (LY) sublines from Sprague-Dawley rats. Dev Psychobiol 2011, 53:105-117. 10.1002/dev.20497, 20886537.
25. Yen YC, Mauch CP, Dahlhoff M, Micale V, Bunck M, Sartori SB, Singewald N, Landgraf R, Wotjak CT. Increased levels of conditioned fear and avoidance behavior coincide with changes in phosphorylation of the protein kinase B (AKT) within the amygdala in a mouse model of extremes in trait anxiety. Neurobiol Learn Mem 2012, 98:56-65. 10.1016/j.nlm.2012.04.009, 22579802.
26. Bell R, Herring SM, Gokul N, Monita M, Grove ML, Boerwinkle E, Doris PA. High-resolution identity by descent mapping uncovers the genetic basis for blood pressure differences between spontaneously hypertensive rat lines. Circ Cardiovasc Genet 2011, 4:223-231. 10.1161/CIRCGENETICS.110.958934, 3116070, 21406686.
27. Wade CM, Kulbokas EJ, Kirby AW, Zody MC, Mullikin JC, Lander ES, Lindblad-Toh K, Daly MJ. The mosaic structure of variation in the laboratory mouse genome. Nature 2002, 420:574-578. 10.1038/nature01252, 12466852.
28. Adams DJ, Dermitzakis ET, Cox T, Smith J, Davies R, Banerjee R, Bonfield J, Mullikin JC, Chung YJ, Rogers J, Bradley A. Complex haplotypes, copy number polymorphisms and coding variation in two recently divergent mouse strains. Nat Genet 2005, 37:532-536. 10.1038/ng1551, 15852006.
29. Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol 1975, 7:256-276. 10.1016/0040-5809(75)90020-9, 1145509.
30. Reuveni E, Birney E, Gross CT. The consequence of natural selection on genetic variation in the mouse. Genomics 2010, 95:196-202. 10.1016/j.ygeno.2010.02.004, 20171270.
31. Wang L, Hao L, Li X, Hu S, Ge S, Yu J. SNP deserts of Asian cultivated rice: genomic regions under domestication. J Evol Biol 2009, 22:751-761. 10.1111/j.1420-9101.2009.01698.x, 19243488.
32. Subbaiyan GK, Waters DL, Katiyar SK, Sadananda AR, Vaddadi S, Henry RJ. Genome-wide DNA polymorphisms in elite indica rice inbreds discovered by whole-genome sequencing. Plant Biotechnol J 2012, 10:623-634. 10.1111/j.1467-7652.2011.00676.x, 22222031.
33. Axelsson E, Ratnakumar A, Arendt ML, Maqbool K, Webster MT, Perloski M, Liberg O, Arnemo JM, Hedhammar A, Lindblad-Toh K. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 2013, 495:360-364. 10.1038/nature11837, 23354050.
34. Kwitek-Black AE, Jacob HJ. The use of designer rats in the genetic dissection of hypertension. Curr Hypertens Rep 2001, 3:12-18. 10.1007/s11906-001-0072-0, 11177702.
35. Corona G, Rastrelli G, Boddi V, Monami M, Melani C, Balzi D, Sforza A, Forti G, Mannucci E, Maggi M. Prolactin levels independently predict major cardiovascular events in patients with erectile dysfunction. Int J Androl 2011, 34:217-224. 10.1111/j.1365-2605.2010.01076.x, 20522124.
36. Balbach L, Wallaschofski H, Volzke H, Nauck M, Dorr M, Haring R. Serum prolactin concentrations as risk factor of metabolic syndrome or type 2 diabetes?. BMC Endocr Disord 2013, 13:12. 10.1186/1472-6823-13-12, 3614874, 23517652.
37. Finlay C, Argoud K, Wilder SP, Ouali F, Ktorza A, Kaisaki PJ, Gauguier D. Chromosomal mapping of pancreatic islet morphological features and regulatory hormones in the spontaneously diabetic (Type 2) Goto-Kakizaki rat. Mammalian genome : official journal of the International Mammalian Genome Society 2010, 21:499-508. 10.1007/s00335-010-9285-3, 2974204, 20878524.
38. Eberlein A, Kalbe C, Goldammer T, Brunner RM, Kuehn C, Weikard R. Annotation of novel transcripts putatively relevant for bovine fat metabolism. Mol Biol Rep 2011, 38:2975-2986. 10.1007/s11033-010-9962-z, 20127178.
39. Casas E, Shackelford SD, Keele JW, Koohmaraie M, Smith TP, Stone RT. Detection of quantitative trait loci for growth and carcass composition in cattle. J Anim Sci 2003, 81:2976-2983.
40. De Camilli P, Thomas A, Cofiell R, Folli F, Lichte B, Piccolo G, Meinck HM, Austoni M, Fassetta G, Bottazzo G, Bates D, Cartlidge N, Solimena M, Kilimann MW, et al. The synaptic vesicle-associated protein amphiphysin is the 128-kD autoantigen of Stiff-Man syndrome with breast cancer. J Exp Med 1993, 178:2219-2223. 10.1084/jem.178.6.2219, 2191289, 8245793.
41. Fox CS, Heard-Costa N, Cupples LA, Dupuis J, Vasan RS, Atwood LD. Genome-wide association to body mass index and waist circumference: the Framingham Heart Study 100K project. BMC Med Genet 2007, 8(Suppl 1):S18. 10.1186/1471-2350-8-S1-S18, 1995618, 17903300.
42. Totsukawa G, Kaneko Y, Uchiyama K, Toh H, Tamura K, Kondo H. VCIP135 deubiquitinase and its binding protein, WAC, in p97ATPase-mediated membrane fusion. Embo J 2011, 30:3581-3593. 10.1038/emboj.2011.260, 3181489, 21811234.
43. Onichtchouk D, Chen YG, Dosch R, Gawantka V, Delius H, Massague J, Niehrs C. Silencing of TGF-beta signalling by the pseudoreceptor BAMBI. Nature 1999, 401:480-485. 10.1038/46794, 10519551.
44. Chen J, Bush JO, Ovitt CE, Lan Y, Jiang R. The TGF-beta pseudoreceptor gene Bambi is dispensable for mouse embryonic development and postnatal survival. Genesis 2007, 45:482-486. 10.1002/dvg.20320, 2376806, 17661381.
45. Guillot N, Kollins D, Badimon JJ, Schlondorff D, Hutter R. Accelerated reendothelialization, increased neovascularization and erythrocyte extravasation after arterial injury in BAMBI-/- mice. PloS one 2013, 8:e58550. 10.1371/journal.pone.0058550, 3585719, 23469285.
46. Kamura T, Sato S, Iwai K, Czyzyk-Krzeska M, Conaway RC, Conaway JW. Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc Natl Acad Sci USA 2000, 97:10430-10435. 10.1073/pnas.190332597, 27041, 10973499.
47. Jiang C, Qu A, Matsubara T, Chanturiya T, Jou W, Gavrilova O, Shah YM, Gonzalez FJ. Disruption of hypoxia-inducible factor 1 in adipocytes improves insulin sensitivity and decreases adiposity in high-fat diet-fed mice. Diabetes 2011, 60:2484-2495. 10.2337/db11-0174, 3178277, 21873554.
48. Boyden LM, Choi M, Choate KA, Nelson-Williams CJ, Farhi A, Toka HR, Tikhonova IR, Bjornson R, Mane SM, Colussi G, Lebel M, Gordon RD, Semmekrot BA, Poujol A, Valimaki MJ, De Ferrari ME, Sanjad SA, Gutkin M, Karet FE, Tucci JR, Stockigt JR, Keppler-Noreuil KM, Porter CC, Anand SK, Whiteford ML, Davis ID, Dewar SB, Bettinelli A, Fadrowski JJ, Belsha CW, et al. Mutations in kelch-like 3 and cullin 3 cause hypertension and electrolyte abnormalities. Nature 2012, 482:98-102. 10.1038/nature10814, 3278668, 22266938.
49. Favre D, Le Gouill E, Fahmi D, Verdumo C, Chinetti-Gbaguidi G, Staels B, Caiazzo R, Pattou F, Le KA, Tappy L, Regazzi R, Giusti V, Vollenweider P, Waeber G, Abderrahmani A. Impaired expression of the inducible cAMP early repressor accounts for sustained adipose CREB activity in obesity. Diabetes 2011, 60:3169-3174. 10.2337/db10-1743, 3219947, 21998402.
50. Muller FU, Lewin G, Matus M, Neumann J, Riemann B, Wistuba J, Schutz G, Schmitz W. Impaired cardiac contraction and relaxation and decreased expression of sarcoplasmic Ca2+-ATPase in mice lacking the CREM gene. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 2003, 17:103-105.
51. Lewin G, Matus M, Basu A, Frebel K, Rohsbach SP, Safronenko A, Seidl MD, Stumpel F, Buchwalow I, Konig S, Engelhardt S, Lohse MJ, Schmitz W, Muller FU. Critical role of transcription factor cyclic AMP response element modulator in beta1-adrenoceptor-mediated cardiac dysfunction. Circulation 2009, 119:79-88. 10.1161/CIRCULATIONAHA.108.786533, 19103994.
52. Bhoj EJ, Romeo S, Baroni MG, Bartov G, Schultz RA, Zinn AR. MODY-like diabetes associated with an apparently balanced translocation: possible involvement of MPP7 gene and cell polarity in the pathogenesis of diabetes. Mole Cytogenet 2009, 2:5.
53. Larson MG, Atwood LD, Benjamin EJ, Cupples LA, D'Agostino RB, Fox CS, Govindaraju DR, Guo CY, Heard-Costa NL, Hwang SJ, Murabito JM, Newton-Cheh C, O'Donnell CJ, Seshadri S, Vasan RS, Wang TJ, Wolf PA, Levy D. Framingham Heart Study 100K project: genome-wide associations for cardiovascular disease outcomes. BMC Med Genet 2007, 8(Suppl 1):S5. 10.1186/1471-2350-8-S1-S5, 1995607, 17903304.
54. Meigs JB, Manning AK, Fox CS, Florez JC, Liu C, Cupples LA, Dupuis J. Genome-wide association with diabetes-related traits in the Framingham Heart Study. BMC Med Genet 2007, 8(Suppl 1):S16. 10.1186/1471-2350-8-S1-S16, 1995610, 17903298.
55. Vasan RS, Larson MG, Aragam J, Wang TJ, Mitchell GF, Kathiresan S, Newton-Cheh C, Vita JA, Keyes MJ, O'Donnell CJ, Levy D, Benjamin EJ. Genome-wide association of echocardiographic dimensions, brachial artery endothelial function and treadmill exercise responses in the Framingham Heart Study. BMC Med Genet 2007, 8(Suppl 1):S2. 10.1186/1471-2350-8-S1-S2, 1995617, 17903301.
56. Ferrell F, Lanou A, Gray SD. Salt level in weaning diet affects saline preference and fluid intake in Dahl rats. Hypertension 1986, 8:1021-1026. 10.1161/01.HYP.8.11.1021, 3770865.
57. Nishikimi T, Mori Y, Kobayashi N, Tadokoro K, Wang X, Akimoto K, Yoshihara F, Kangawa K, Matsuoka H. Renoprotective effect of chronic adrenomedullin infusion in Dahl salt-sensitive rats. Hypertension 2002, 39:1077-1082. 10.1161/01.HYP.0000018910.74377.93, 12052845.
58. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England) 2009, 25:1754-1760.
59. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010, 20:1297-1303. 10.1101/gr.107524.110, 2928508, 20644199.
60. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011, 43:491-498. 10.1038/ng.806, 3083463, 21478889.
61. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics (Oxford, England) 2010, 26:841-842.
62. Wand MP, Jones MC. Kernel Smoothing 1995, Chapman & Hall/CRC, First.
63. R Development Core Team R: A Language and Environment for Statistical Computing 2011, Vienna, Austria: R Foundation for Statistical Computing, R Development Core Team.
64. Flicek P, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, Gordon L, Hendrix M, Hourlier T, Johnson N, Kahari AK, Keefe D, Keenan S, Kinsella R, Komorowska M, Koscielny G, Kulesha E, Larsson P, Longden I, McLaren W, Muffato M, Overduin B, Pignatelli M, Pritchard B, Riat HS, et al. Ensembl 2012. Nucleic Acids Res 2012, 40:D84-90. 10.1093/nar/gkr991, 3245178, 22086963.
65. Kinsella RJ, Kähäri A, Haider S, Zamora J, Proctor G, Spudich G, Almeida-King J, Staines D, Derwent P, Kerhornou A, Kersey P, Flicek P. Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database 2011, bar030. doi:10.1093/database/bar030.
66. The UniProt Consortium Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 2012, 40:D71-D75. 3245120, 22102590, The UniProt Consortium.
67. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 2012, 13:134. 10.1186/1471-2105-13-134, 3412702, 22708584.