Integrated genomic approaches to identification of candidate genes underlying metabolic and cardiovascular phenotypes in the spontaneously hypertensive rat

Physiological Genomics

Volumn 43, Issue 21, 2011, Pages 1207-1218

  Morrissey, Catherine ^a   Grieve, Ian C ^a   Heinig, Matthias ^b   Atanur, Santosh ^a   Petretto, Enrico ^a,c   Pravenec, Michal ^d   Hubner, Norbert ^b   Aitman, Timothy J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c MRC CLINICAL SCIENCES CENTRE   (United Kingdom)

^d INSTITUTE OF PHYSIOLOGY   (Czech Republic)

Author keywords

Expression quantitative trait locus; Quantitative trait transcript; Sequence variation; Spontaneously hypertensive rat

Indexed keywords

GLUCOSE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; GENE LOCUS; GENE SEQUENCE; GENETIC SUSCEPTIBILITY; GENOMICS; GLUCOSE BLOOD LEVEL; HYPERTENSION; MALE; METABOLIC SYNDROME X; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE TRAIT LOCUS; RAT; RAT STRAIN; SINGLE NUCLEOTIDE POLYMORPHISM; SPONTANEOUSLY HYPERTENSIVE RAT; SYSTOLIC BLOOD PRESSURE;

5' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BINDING SITES; CARDIOVASCULAR DISEASES; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; GENOMICS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; POLYMERASE CHAIN REACTION; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; RATS; RATS, INBRED SHR; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; TRANSCRIPTION FACTORS;

RATTUS; RODENTIA;

EID: 80855140431     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00210.2010     Document Type: Article

References (72)

1. Aitman TJ, Critser JK, Cuppen E, Dominiczak A, Fernandez-Suarez XM, Flint J, Gauguier D, Geurts AM, Gould M, Harris PC, Holmdahl R, Hubner N, Izsvak Z, Jacob HJ, Kuramoto T, Kwitek AE, Marrone A, Mashimo T, Moreno C, Mullins J, Mullins L, Olsson T, Pravenec M, Riley L, Saar K, Serikawa T, Shull JD, Szpirer C, Twigger SN, Voigt B, Worley K. Progress and prospects in rat genetics: a community view. Nat Genet 40: 516-522, 2008.
2. Aitman TJ, Glazier AM, Wallace CA, Cooper LD, Norsworthy PJ, Wahid FN, Al-Majali KM, Trembling PM, Mann CJ, Shoulders CC, Graf D, St Lezin E, Kurtz TW, Kren V, Pravenec M, Ibrahimi A, Abumrad NA, Stanton LW, Scott J. Identification of Cd36 (Fat) as an insulin-resistance gene causing defective fatty acid and glucose metabolism in hypertensive rats. Nat Genet 21: 76-83, 1999.
3. Aitman TJ, Gotoda T, Evans AL, Imrie H, Heath KE, Trembling PM, Truman H, Wallace CA, Rahman A, Dore C, Flint J, Kren V, Zidek V, Kurtz TW, Pravenec M, Scott J. Quantitative trait loci for cellular defects in glucose and fatty acid metabolism in hypertensive rats. Nat Genet 16: 197-201, 1997.
4. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr. Harmonizingthe metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120: 1640-1645, 2009.
5. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402, 1997.
6. Asleh R, Marsh S, Shilkrut M, Binah O, Guetta J, Lejbkowicz F, Enav B, Shehadeh N, Kanter Y, Lache O, Cohen O, Levy NS, Levy AP. Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ Res 92: 1193-1200, 2003.
7. 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 20: 791-803, 2010.
8. Bachli EB, Schaer DJ, Walter RB, Fehr J, Schoedon G. Functional expression of the CD163 scavenger receptor on acute myeloid leukemia cells of monocytic lineage. J Leukoc Biol 79: 312-318, 2006.
9. Bailey DW. Recombinant-inbred strains. An aid to finding identity, linkage, and function of histocompatibility and other genes. Transplantation 11: 325-327, 1971.
10. Bate KL, Jerums G. 3: Preventing complications of diabetes. Med J Aust 179: 498-503, 2003.
11. Bielavska E, Kren V, Musilova A, Zidek V, Pravenec M. Genome scanning of the HXB/BXH sets of recombinant inbred strains of the rat for quantitative trait loci associated with conditioned taste aversion. Behav Genet 32: 51-56, 2002.
12. Binda D, Nicod L, Viollon-Abadie C, Rodriguez S, Berthelot A, Coassolo P, Richert L. Strain difference (WKY, SPRD) in the hepatic antioxidant status in rat and effect of hypertension (SHR, DOCA). Ex vivo and in vitro data. Mol Cell Biochem 218: 139-146, 2001.
13. Boretti FS, Buehler PW, D'Agnillo F, Kluge K, Glaus T, Butt OI, Jia Y, Goede J, Pereira CP, Maggiorini M, Schoedon G, Alayash AI, Schaer DJ. Sequestration of extracellular hemoglobin within a haptoglobin complex decreases its hypertensive and oxidative effects in dogs and guinea pigs. J Clin Invest 119: 2271-2280, 2009.
14. Bottger A, van Lith HA, Kren V, Krenova D, Bila V, Vorlicek J, Zidek V, Musilova A, Zdobinska M, Wang JM, van Zutphen BF, Kurtz TW, Pravenec M. Quantitative trait loci influencing cholesterol and phospholipid phenotypes map to chromosomes that contain genes regulating blood pressure in the spontaneously hypertensive rat. J Clin Invest 98: 856-862, 1996.
15. Buehler PW, Abraham B, Vallelian F, Linnemayr C, Pereira CP, Cipollo JF, Jia Y, Mikolajczyk M, Boretti FS, Schoedon G, Alayash AI, Schaer DJ. Haptoglobin preserves the CD163 hemoglobin scavenger pathway by shielding hemoglobin from peroxidative modification. Blood 113: 2578-2586, 2009.
16. Burczynski ME, Lin HK, Penning TM. Isoform-specific induction of a human aldo-keto reductase by polycyclic aromatic hydrocarbons (PAHs), electrophiles, and oxidative stress: implications for the alternative pathway of PAH activation catalyzed by human dihydrodiol dehydrogenase. Cancer Res 59: 607-614, 1999.
17. Buresova M, Zidek V, Musilova A, Simakova M, Fucikova A, Bila V, Kren V, Kazdova L, Di Nicolantonio R, Pravenec M. Genetic relationship between placental and fetal weights and markers of the metabolic syndrome in rat recombinant inbred strains. Physiol Genomics 26: 226-231, 2006.
18. Charchar FJ, Kaiser M, Bingham AJ, Fotinatos N, Ahmady F, Tomaszewski M, Samani NJ. Whole genome survey of copy number variation in the spontaneously hypertensive rat: relationship to quantitative trait loci, gene expression, and blood pressure. Hypertension 55: 1231-1238, 2010.
19. Costa C, Catania S, De Pasquale R, Stancanelli R, Scribano GM, Melchini A. Exposure of human skin to benzo[a]pyrene: role of CYP1A1 and aryl hydrocarbon receptor in oxidative stress generation. Toxicology 271: 83-86, 2010.
20. de Wolf ID, Fielmich-Bouman XM, van Oost BA, Beynen AC, Kren V, Pravenec M, van Zutphen LF, van Lith HA. Genetic and correlation analysis of hepatic copper content in the rat. Biochem Biophys Res Commun 289: 1247-1251, 2001.
21. Dressler GR. The specification and maintenance of renal cell types by epigenetic factors. Organogenesis 5: 73-82, 2009.
22. 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, Glodek A, Gu Z, Jennings D, Kraft CL, Nguyen T, Pfannkoch CM, Sitter C, Sutton GG, Venter JC, Woodage T, Smith D, Lee HM, Gustafson E, Cahill P, Kana A, Doucette-Stamm L, Weinstock K, Fechtel K, Weiss RB, Dunn DM, Green ED, Blakesley RW, Bouffard GG, De Jong PJ, Osoegawa K, Zhu B, Marra M, Schein J, Bosdet I, Fjell C, Jones S, Krzywinski M, Mathewson C, Siddiqui A, Wye N, McPherson J, Zhao S, Fraser CM, Shetty J, Shatsman S, Geer K, Chen Y, Abramzon S, Nierman WC, Havlak PH, Chen R, Durbin KJ, Egan A, Ren Y, Song XZ, Li B, Liu Y, Qin X, Cawley S, Cooney AJ, D'Souza LM, Martin K, Wu JQ, Gonzalez- Garay ML, Jackson AR, Kalafus KJ, McLeod MP, Milosavljevic A, Virk D, Volkov A, Wheeler DA, Zhang Z, Bailey JA, Eichler EE, Tuzun E, Birney E, Mongin E, Ureta-Vidal A, Woodwark C, Zdobnov E, Bork P, Suyama M, Torrents D, Alexandersson M, Trask BJ, Young JM, Huang H, Wang H, Xing H, Daniels S, Gietzen D, Schmidt J, Stevens K, Vitt U, Wingrove J, Camara F, Mar Alba M, Abril JF, Guigo R, Smit A, Dubchak I, Rubin EM, Couronne O, Poliakov A, Hübner N, Ganten D, Goesele C, Hummel O, Kreitler T, Lee YA, Monti J, Schulz H, Zimdahl H, Himmelbauer H, Lehrach H, Jacob HJ, Bromberg S, Gullings-Handley J, Jensen-Seaman MI, Kwitek AE, Lazar J, Pasko D, Tonellato PJ, Twigger S, Ponting CP, Duarte JM, Rice S, Goodstadt L, Beatson SA, Emes RD, Winter EE, Webber C, Brandt P, Nyakatura G, Adetobi M, Chiaromonte F, Elnitski L, Eswara P, Hardison RC, Hou M, Kolbe D, Makova K, Miller W, Nekrutenko A, Riemer C, Schwartz S, Taylor J, Yang S, Zhang Y, Lindpaintner K, Andrews TD, Caccamo M, Clamp M, Clarke L, Curwen V, Durbin R, Eyras E, Searle SM, Cooper GM, Batzoglou S, Brudno M, Sidow A, Stone EA, Venter JC, Payseur BA, Bourque G, López-Otín C, Puente XS, Chakrabarti K, Chatterji S, Dewey C, Pachter L, Bray N, Yap VB, Caspi A, Tesler G, Pevzner PA, Haussler D, Roskin KM, Baertsch R, Clawson H, Furey TS, Hinrichs AS, Karolchik D, Kent WJ, Rosenbloom KR, Trumbower H, Weirauch M, Cooper DN, Stenson PD, Ma B, Brent M, Arumugam M, Shteynberg D, Copley RR, Taylor MS, Riethman H, Mudunuri U, Peterson J, Guyer M, Felsenfeld A, Old S, Mockrin S, Collins F; Rat Genome Sequencing Project Consortium. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428: 493-521, 2004.
23. Grieve IC, Dickens NJ, Pravenec M, Kren V, Hubner N, Cook SA, Aitman TJ, Petretto E, Mangion J. Genome-wide co-expression analysis in multiple tissues. PLoS One 3: e4033, 2008.
24. Heinig M, Petretto E, Wallace C, Bottolo L, Rotival M, Lu H, Li Y, Sarwar R, Langley SR, Bauerfeind A, Hummel O, Lee YA, Paskas S, Rintisch C, Saar K, Cooper J, Buchan R, Gray EE, Cyster JG, Cardiogenics Consortium, Erdmann J, Hengstenberg C, Maouche S, Ouwehand W, Rice CM, Samani NJ, Schunkert H, Goodall AH, Schulz H, Roider HG, Vingron M, Blankenberg S, Munzel T, Zeller T, Szymczak S, Ziegler A, Tiret L, Smyth DJ, Pravanec M, Aitman T, Cambien F, Clayton D, Todd JA, Hubner N, Cook SA. A trans-acting locus regulates an anti-viral expression network and type 1 diabetes risk. Nature 467: 460-464, 2010.
25. Hopps E, Noto D, Caimi G, Averna MR. A novel component of the metabolic syndrome: the oxidative stress. Nutr Metab Cardiovasc Dis 20: 72-77, 2010.
26. Hubner N, Wallace CA, Zimdahl H, Petretto E, Schulz H, Maciver F, Mueller M, Hummel O, Monti J, Zidek V, Musilova A, Kren V, Causton H, Game L, Born G, Schmidt S, Muller A, Cook SA, Kurtz TW, Whittaker J, Pravenec M, Aitman TJ. Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat Genet 37: 243-253, 2005.
27. Hvidberg V, Maniecki MB, Jacobsen C, Hojrup P, Moller HJ, Moestrup SK. Identification of the receptor scavenging hemopexin-heme complexes. Blood 106: 2572-2579, 2005.
28. Jirout ML, Friese RS, Mahapatra NR, Mahata M, Taupenot L, Mahata SK, Kren V, Zidek V, Fischer J, Maatz H, Ziegler MG, Pravenec M, Hubner N, Aitman TJ, Schork NJ, O'Connor DT. Genetic regulation of catecholamine synthesis, storage and secretion in the spontaneously hypertensive rat. Hum Mol Genet, 2010.
29. Johnson MD, He L, Herman D, Wakimoto H, Wallace CA, Zidek V, Mlejnek P, Musilova A, Simakova M, Vorlicek J, Kren V, Viklicky O, Qi NR, Wang J, Seidman CE, Seidman J, Kurtz TW, Aitman TJ, Pravenec M. Dissection of chromosome 18 blood pressure and saltsensitivity quantitative trait loci in the spontaneously hypertensive rat. Hypertension 54: 639-645, 2009.
30. Kitts DD, Yuan YV, Godin DV. Plasma and lipoprotein lipid composition and hepatic antioxidant status in spontaneously hypertensive (SHR) and normotensive (WKY) rats. Can J Physiol Pharmacol 76: 202-209, 1998.
31. Krueger K, Koch K, Juhling A, Tepel M, Scholze A. Low expression of thiosulfate sulfurtransferase (rhodanese) predicts mortality in hemodialysis patients. Clin Biochem 43: 95-101, 2010.
32. Kunes J, Kren V, Klir P, Zicha J, Pravenec M. Genetic determination of heart and kidney weights studied using a set of recombinant inbred strains: the relationship to blood pressure. J Hypertens 8: 1091-1095, 1990.
33. Lindoso RS, Verdoorn KS, Einicker-Lamas M. Renal recovery after injury: the role of Pax-2. Nephrol Dial Transplant 24: 2628-2633, 2009.
34. Lum PY, Chen Y, Zhu J, Lamb J, Melmed S, Wang S, Drake TA, Lusis AJ, Schadt EE. Elucidating the murine brain transcriptional network in a segregating mouse population to identify core functional modules for obesity and diabetes. J Neurochem 97, Suppl 1: 50-62, 2006.
35. MacDonald RJ, Swift GH, Quinto C, Swain W, Pictet RL, Nikovits W, Rutter WJ. Primary structure of two distinct rat pancreatic preproelastases determined by sequence analysis of the complete cloned messenger ribonucleic acid sequences. Biochemistry 21: 1453-1463, 1982.
36. Manke T, Heinig M, Vingron M. Quantifying the effect of sequence variation on regulatory interactions. Hum Mutat 31: 477-483, 2010.
37. Manke T, Roider HG, Vingron M. Statistical modeling of transcription factor binding affinities predicts regulatory interactions. PLoS Comput Biol 4: e1000039, 2008.
38. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre- Dirrie A, Reuter I, Chekmenev D, Krull M, Hornischer K, Voss N, Stegmaier P, Lewicki-Potapov B, Saxel H, Kel AE, Wingender E. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34: D108-D110, 2006.
39. Mueller M, Goel A, Thimma M, Dickens NJ, Aitman TJ, Mangion J. eQTL Explorer: integrated mining of combined genetic linkage and expression experiments. Bioinformatics 22: 509-511, 2006.
40. Oliviero S, Cortese R. The human haptoglobin gene promoter: interleukin- 6-responsive elements interact with a DNA-binding protein induced by interleukin-6. EMBO J 8: 1145-1151, 1989.
41. Oliviero S, Morrone G, Cortese R. The human haptoglobin gene: transcriptional regulation during development and acute phase induction. EMBO J 6: 1905-1912, 1987.
42. Passador-Gurgel G, Hsieh WP, Hunt P, Deighton N, Gibson G. Quantitative trait transcripts for nicotine resistance in Drosophila melanogaster. Nat Genet 39: 264-268, 2007.
43. Petretto E, Mangion J, Dickens NJ, Cook SA, Kumaran MK, Lu H, Fischer J, Maatz H, Kren V, Pravenec M, Hubner N, Aitman TJ. Heritability and tissue specificity of expression quantitative trait loci. PLoS Genet 2: e172, 2006.
44. Petretto E, Sarwar R, Grieve I, Lu H, Kumaran MK, Muckett PJ, Mangion J, Schroen B, Benson M, Punjabi PP, Prasad SK, Pennell DJ, Kiesewetter C, Tasheva ES, Corpuz LM, Webb MD, Conrad GW, Kurtz TW, Kren V, Fischer J, Hubner N, Pinto YM, Pravenec M, Aitman TJ, Cook SA. Integrated genomic approaches implicate osteoglycin (Ogn) in the regulation of left ventricular mass. Nat Genet 40: 546-552, 2008.
45. Pravenec M, Churchill PC, Churchill MC, Viklicky O, Kazdova L, Aitman TJ, Petretto E, Hubner N, Wallace CA, Zimdahl H, Zidek V, Landa V, Dunbar J, Bidani A, Griffin K, Qi N, Maxova M, Kren V, Mlejnek P, Wang J, Kurtz TW. Identification of renal Cd36 as a determinant of blood pressure and risk for hypertension. Nat Genet 40: 952-954, 2008.
46. Pravenec M, Gauguier D, Schott JJ, Buard J, Kren V, Bila V, Szpirer C, Szpirer J, Wang JM, Huang H. Mapping of quantitative trait loci for blood pressure and cardiac mass in the rat by genome scanning of recombinant inbred strains. J Clin Invest 96: 1973-1978, 1995.
47. Pravenec M, Klir P, Kren V, Zicha J, Kunes J. An analysis of spontaneous hypertension in spontaneously hypertensive rats by means of new recombinant inbred strains. J Hypertens 7: 217-221, 1989.
48. Pravenec M, Kunes J, Zicha J, Kren V, Klir P. Platelet aggregation in spontaneous hypertension: genetic determination and correlation analysis. J Hypertens 10: 1453-1456, 1992.
49. Pravenec M, Kurtz TW. Recent advances in genetics of the spontaneously hypertensive rat. Curr Hypertens Rep 12: 5-9, 2010.
50. Pravenec M, Zidek V, Musilova A, Kren V, Bila V, Di Nicolantonio R. Chromosomal mapping of a major quantitative trait locus regulating compensatory renal growth in the rat. J Am Soc Nephrol 11: 1261-1265, 2000.
51. Pravenec M, Zidek V, Musilova A, Simakova M, Kostka V, Mlejnek P, Kren V, Krenova D, Bila V, Mikova B, Jachymova M, Horky K, Kazdova L, St Lezin E, Kurtz TW. Genetic analysis of metabolic defects in the spontaneously hypertensive rat. Mamm Genome 13: 253-258, 2002.
52. Pravenec M, Zidek V, Simakova M, Kren V, Krenova D, Horky K, Jachymova M, Mikova B, Kazdova L, Aitman TJ, Churchill PC, Webb RC, Hingarh NH, Yang Y, Wang JM, Lezin EM, Kurtz TW. Genetics of Cd36 and the clustering of multiple cardiovascular risk factors in spontaneous hypertension. J Clin Invest 103: 1651-1657, 1999.
53. Pravenec M, Zidek V, Zdobinska M, Kren V, Krenova D, Bottger A, van Zutphen LF, Wang J, St Lezin E. Mapping genes controlling hematocrit in the spontaneously hypertensive rat. Mamm Genome 8: 387-389, 1997.
54. Roider HG, Kanhere A, Manke T, Vingron M. Predicting transcription factor affinities to DNA from a biophysical model. Bioinformatics 23: 134-141, 2007.
55. Santiago JV. Overview of the complications of diabetes. Clin Chem 32: B48-B53, 1986.
56. Schadt EE, Lamb J, Yang X, Zhu J, Edwards S, Guhathakurta D, Sieberts SK, Monks S, Reitman M, Zhang C, Lum PY, Leonardson A, Thieringer R, Metzger JM, Yang L, Castle J, Zhu H, Kash SF, Drake TA, Sachs A, Lusis AJ. An integrative genomics approach to infer causal associations between gene expression and disease. Nat Genet 37: 710-7, 2005.
57. Schaer DJ, Schaer CA, Buehler PW, Boykins RA, Schoedon G, Alayash AI, Schaffner A. CD163 is the macrophage scavenger receptor for native and chemically modified hemoglobins in the absence of haptoglobin. Blood 107: 373-380, 2006.
58. Schrader M, Fahimi HD. Peroxisomes and oxidative stress. Biochim Biophys Acta 1763: 1755-1766, 2006.
59. Singh R, Lemire J, Mailloux RJ, Appanna VD. A novel strategy involved in [corrected] anti-oxidative defense: the conversion of NADH into NADPH by a metabolic network. PLoS One 3: e2682, 2008.
60. STAR Consortium, 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, Medina I, Mott R, Patone G, Perrier-Cornet JA, Platzer M, Pravenec M, Reinhardt R, Sakaki Y, Schilhabel M, Schulz H, Serikawa T, Shikhagaie M, Tatsumoto S, Taudien S, Toyoda A, Voigt B, Zelenika D, Zimdahl H, Hubner N. SNP and haplotype mapping for genetic analysis in the rat. Nat Genet 40: 560-566, 2008.
61. Stohs SJ. Oxidative stress induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Free Radic Biol Med 9: 79-90, 1990.
62. Tanito M, Nakamura H, Kwon YW, Teratani A, Masutani H, Shioji K, Kishimoto C, Ohira A, Horie R, Yodoi J. Enhanced oxidative stress and impaired thioredoxin expression in spontaneously hypertensive rats. Antioxid Redox Signal 6: 89-97, 2004.
63. Teye K, Quaye IK, Koda Y, Soejima M, Tsuneoka M, Pang H, Ekem I, Amoah AG, Adjei A, Kimura H. A-61C and C-101G Hp gene promoter polymorphisms are, respectively, associated with ahaptoglobinaemia and hypohaptoglobinaemia in Ghana. Clin Genet 64: 439-443, 2003.
64. Thomas RJ, Palumbo PJ, Melton LJ 3rd, Roger VL, Ransom J, O'Brien PC, Leibson CL. Trends in the mortality burden associated with diabetes mellitus: a population-based study in Rochester, Minn, 1970-1994. Arch Intern Med 163: 445-451, 2003.
65. Thongboonkerd V, Barati MT, McLeish KR, Benarafa C, Remold- O'Donnell E, Zheng S, Rovin BH, Pierce WM, Epstein PN, Klein JB. Alterations in the renal elastin-elastase system in type 1 diabetic nephropathy identified by proteomic analysis. J Am Soc Nephrol 15: 650-662, 2004.
66. Tolosano E, Altruda F. Hemopexin: structure, function, regulation. DNA Cell Biol 21: 297-306, 2002.
67. Torres M, Gomez-Pardo E, Dressler GR, Gruss P. Pax-2 controls multiple steps of urogenital development. Development 121: 4057-4065, 1995.
68. Twigger SN, Shimoyama M, Bromberg S, Kwitek AE, Jacob HJ. The Rat Genome Database, update 2007-easing the path from disease to data and back again. Nucleic Acids Res 35: D658-D662, 2007.
69. Wang J, Williams RW, Manly KF. WebQTL: web-based complex trait analysis. Neuroinformatics 1: 299-308, 2003.
70. Winkler BS, Solomon F. High activities of NADP+-dependent isocitrate dehydrogenase and malic enzyme in rabbit lens epithelial cells. Invest Ophthalmol Vis Sci 29: 821-823, 1988.
71. Yuan YV, Kitts DD, Godin DV. Heart and red blood cell antioxidant status and plasma lipid levels in the spontaneously hypertensive and normotensive Wistar-Kyoto rat. Can J Physiol Pharmacol 74: 290-297, 1996.
72. Zidek V, Pintir J, Musilova A, Bila V, Kren V, Pravenec M. Mapping of quantitative trait loci for seminal vesicle mass and litter size to rat chromosome 8. J Reprod Fertil 116: 329-333, 1999.