Differences in DBA/1J and DBA/2J reveal lipid QTL genes

Journal of Lipid Research

Volumn 49, Issue 11, 2008, Pages 2402-2413

  Stylianou, Ioannis M ^a,c   Langley, Sarah R ^a   Walsh, Kenneth ^a   Chen, Yuan ^a   Revenu, Céline ^b   Paigen, Beverly ^a  

^a JACKSON LABORATORY   (United States)

^b CNRS   (France)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Body weight; Cyp27a1; Ihh; Quantitative trait loci; Triglycerides; Tshr; Villin

Indexed keywords

CHOLESTANETRIOL 26 MONOOXYGENASE; HIGH DENSITY LIPOPROTEIN; SONIC HEDGEHOG PROTEIN; THYROTROPIN RECEPTOR; THYROXINE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; VILLIN; VILLIN 1;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CHROMOSOME 1; CHROMOSOME 10; CHROMOSOME 11; CHROMOSOME 12; CHROMOSOME 13; CHROMOSOME 14; CHROMOSOME 16; CHROMOSOME 19; CHROMOSOME 2; CHROMOSOME 3; CHROMOSOME 4; CHROMOSOME 8; CHROMOSOME 9; CHROMOSOME MAP; CONTROLLED STUDY; DBA 1 MOUSE; DBA 2 MOUSE; FEMALE; GENE IDENTIFICATION; GENETIC CROSS; GENETIC VARIABILITY; LIPOPROTEIN BLOOD LEVEL; MALE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROGENY; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; SINGLE NUCLEOTIDE POLYMORPHISM; STRAIN DIFFERENCE; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; BAGG ALBINO MOUSE; BLOOD; C3H MOUSE; C57BL MOUSE; CHROMOSOME; COMPARATIVE STUDY; CROSS BREEDING; DBA MOUSE; GENETICS; METABOLISM; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; NEW ZEALAND BLACK MOUSE; SPECIES DIFFERENCE;

ANIMALS; CHROMOSOME MAPPING; CHROMOSOMES, MAMMALIAN; CROSSES, GENETIC; FEMALE; LIPOPROTEINS, HDL; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, INBRED MRL LPR; MICE, INBRED NZB; QUANTITATIVE TRAIT LOCI; SPECIES SPECIFICITY; TRIGLYCERIDES;

EID: 58149467316     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800244-JLR200     Document Type: Article

References (63)

1. Assmann, G., H. Schulte, and A. von Eckardstein. 1996. Hypertriglyceridemia and elevated lipoprotein(a) are risk factors for major coronary events in middle-aged men. Am. J. Cardiol. 77: 1179-1184.
2. Fruchart, J. C., and P. Duriez. 2002. HDL and triglyceride as therapeutic targets. Curr. Opin. Lipidol. 13: 605-616.
3. Gordon, D. J., J. L. Probstfield, R. J. Garrison, J. D. Neaton, W. P. Castelli, J. D. Knoke, D. R. Jacobs, Jr., S. Bangdiwala, and H. A. Tyroler. 1989. High-density lipoprotein cholesterol and cardiovascular disease. Four prospective American studies. Circulation. 79: 8-15.
4. Nissen, S. E., T. Tsunoda, E. M. Tuzcu, P. Schoenhagen, C. J. Cooper, M. Yasin, G. M. Eaton, M. A. Lauer, W. S. Sheldon, C. L. Grines, et al. 2003. Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: a randomized controlled trial. J. Am. Med. Assoc. 290: 2292-2300.
5. Wilson, P. W., K. M. Anderson, T. Harris, W. B. Kannel, and W. P. Castelli. 1994. Determinants of change in total cholesterol and HDL-C with age: the Framingham Study. J. Gerontol. 49: M252-M257.
6. Badimon, J. J., L. Badimon, and V. Fuster. 1990. Regression of atherosclerotic lesions by high density lipoprotein plasma fraction in the cholesterol-fed rabbit. J. Clin. Invest. 85: 1234-1241.
7. Okamoto, H., F. Yonemori, K. Wakitani, T. Minowa, K. Maeda, and H. Shinkai. 2000. A cholesteryl ester transfer protein inhibitor attenuates atherosclerosis in rabbits. Nature. 406: 203-207.
8. Plump, A. S., C. J. Scott, and J. L. Breslow. 1994. Human apolipoprotein A-I gene expression increases high density lipoprotein and suppresses atherosclerosis in the apolipoprotein E-deficient mouse. Proc. Natl. Acad. Sci. USA. 91: 9607-9611.
9. Rittershaus, C. W., D. P. Miller, L. J. Thomas, M. D. Picard, C. M. Honan, C. D. Emmett, C. L. Pettey, H. Adari, R. A. Hammond, D. T. Beattie, et al. 2000. Vaccine-induced antibodies inhibit CETP activity in vivo and reduce aortic lesions in a rabbit model of atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 20: 2106-2112.
10. Rubin, E. M., R. M. Krauss, E. A. Spangler, J. G. Verstuyft, and S. M. Clift. 1991. Inhibition of early atherogenesis in transgenic mice by human apolipoprotein AI. Nature. 353: 265-267.
11. Sugano, M., N. Makino, S. Sawada, S. Otsuka, M. Watanabe, H. Okamoto, M. Kamada, and A. Mizushima. 1998. Effect of antisense oligonucleotides against cholesteryl ester transfer protein on the development of atherosclerosis in cholesterol-fed rabbits. J. Biol. Chem. 273: 5033-5036.
12. DiPetrillo, K., X. Wang, I. M. Stylianou, and B. Paigen. 2005. Bioinformatics toolbox for narrowing rodent quantitative trait loci. Trends Genet. 21: 683-692.
13. Hillebrandt, S., H. E. Wasmuth, R. Weiskirchen, C. Hellerbrand, H. Keppeler, A. Werth, R. Schirin-Sokhan, G. Wilkens, A. Geier, J. Lorenzen, et al. 2005. Complement factor 5 is a quantitative trait gene that modifies liver fibrogenesis in mice and humans. Nat. Genet. 37: 835-843.
14. Korstanje, R., and B. Paigen. 2002. From QTL to gene: the harvest begins. Nat. Genet. 31: 235-236.
15. Wang, X., M. Ria, P. M. Kelmenson, P. Eriksson, D. C. Higgins, A. Samnegard, C. Petros, J. Rollins, A. M. Bennet, B. Wiman, et al. 2005. Positional identification of TNFSF4, encoding OX40 ligand, as a gene that influences atherosclerosis susceptibility. Nat. Genet. 37: 365-372.
16. Churchill, G. A., D. C. Airey, H. Allayee, J. M. Angel, A. D. Attie, J. Beatty, W. D. Beavis, J. K. Belknap, B. Bennett, W. Berrettini, et al. 2004. The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nat. Genet. 36: 1133-1137.
17. Wade, C. M., and M. J. Daly. 2005. Genetic variation in laboratory mice. Nat. Genet. 37: 1175-1180.
18. Svenson, K. L., R. Von Smith, P. A. Magnani, H. R. Suetin, B. Paigen, J. K. Naggert, R. Li, G. A. Churchill, and L. L. Peters. 2007. Multiple trait measurements in 43 inbred mouse strains capture the phenotypic diversity characteristic of human populations. J. Appl. Physiol. 102: 2369-2378.
19. Beamer, W. J., E. M. Eicher, L. J. Maltais, and J. L. Southard. 1981. Inherited primary hypothyroidism in mice. Science. 212: 61-63.
20. Gu, W. X., G. G. Du, P. Kopp, A. Rentoumis, C. Albanese, L. D. Kohn, L. D. Madison, and J. L. Jameson. 1995. The thyrotropin (TSH) receptor transmembrane domain mutation (Pro556-Leu) in the hypothyroid hyt/hyt mouse results in plasma membrane targeting but defective TSH binding. Endocrinology. 136: 3146-3153.
21. Ferrary, E., M. Cohen-Tannoudji, G. Pehau-Arnaudet, A. Lapillonne, R. Athman, T. Ruiz, L. Boulouha, F. El Marjou, A. Doye, J. J. Fontaine, et al. 1999. In vivo, villin is required for Ca(2+)-dependent F-actin disruption in intestinal brush borders. J. Cell Biol. 146: 819-830.
22. Nishina, P. M., J. Verstuyft, and B. Paigen. 1990. Synthetic low and high fat diets for the study of atherosclerosis in the mouse. J. Lipid Res. 31: 859-869.
23. Petkov, P. M., Y. Ding, M. A. Cassell, W. Zhang, G. Wagner, E. E. Sargent, S. Asquith, V. Crew, K. A. Johnson, P. Robinson, et al. 2004. An efficient SNP system for mouse genome scanning and elucidating strain relationships. Genome Res. 14: 1806-1811.
24. Stylianou, I. M., S.W. Tsaih, K. DiPetrillo, N. Ishimori, R. Li, B. Paigen, and G. Churchill. 2006. Complex genetic architecture revealed by analysis of high-density lipoprotein cholesterol in chromosome substitution strains and F2 crosses. Genetics. 174: 999-1007.
25. Jensen-Seaman, M. I., T. S. Furey, B. A. Payseur, Y. Lu, K. M. Roskin, C. F. Chen, M. A. Thomas, D. Haussler, and H. J. Jacob. 2004. Comparative recombination rates in the rat, mouse, and human genomes. Genome Res. 14: 528-538.
26. Churchill, G. A., and R. W. Doerge. 1994. Empirical threshold values for quantitative trait mapping. Genetics. 138: 963-971.
27. Wang, X., and B. Paigen. 2005. Genome-wide search for new genes controlling plasma lipid concentrations in mice and humans. Curr. Opin. Lipidol. 16: 127-137.
28. Rowen, L., J. Young, B. Birditt, A. Kaur, A. Madan, D. L. Philipps, S. Qin, P. Minx, R. K. Wilson, L. Hood, et al. 2002. Analysis of the human neurexin genes: alternative splicing and the generation of protein diversity. Genomics. 79: 587-597.
29. Cooper, D. S. 2001. Clinical practice. Subclinical hypothyroidism. N. Engl. J. Med. 345: 260-265.
30. Knudsen, N., P. Laurberg, L. B. Rasmussen, I. Bulow, H. Perrild, L. Ovesen, and T. Jorgensen. 2005. Small differences in thyroid function may be important for body mass index and the occurrence of obesity in the population. J. Clin. Endocrinol. Metab. 90: 4019-4024.
31. Toft, A. D. 2001. Clinical practice. Subclinical hyperthyroidism. N. Engl. J. Med. 345: 512-516.
32. Bell, A., A. Gagnon, L. Grunder, S. J. Parikh, T. J. Smith, and A. Sorisky. 2000. Functional TSH receptor in human abdominal preadipocytes and orbital fibroblasts. Am. J. Physiol. Cell Physiol. 279: C335-C340.
33. Stein, S. A., E. L. Oates, C. R. Hall, R. M. Grumbles, L. M. Fernandez, N. A. Taylor, D. Puett, and S. Jin. 1994. Identification of a point mutation in the thyrotropin receptor of the hyt/hyt hypothyroid mouse. Mol. Endocrinol. 8: 129-138
34. Repa, J. J., E. G. Lund, J. D. Horton, E. Leitersdorf, D. W. Russell, J. M. Dietschy, and S. D. Turley. 2000. Disruption of the sterol 27-hydroxylase gene in mice results in hepatomegaly and hypertri-glyceridemia. Reversal by cholic acid feeding. J. Biol. Chem. 275: 39685-39692.
35. Buhman, K. K., L. C. Wang, Y. Tang, E. A. Swietlicki, S. Kennedy, Y. Xie, Z. Y. Liu, L. C. Burkly, M. S. Levin, D. C. Rubin, et al. 2004. Inhibition of Hedgehog signaling protects adult mice from diet-induced weight gain. J. Nutr. 134: 2979-2984.
36. Wang, X., and B. Paigen. 2005. Genetics of variation in HDL cholesterol in humans and mice. Circ. Res. 96: 27-42.
37. Boberg, J., P. A. Dahlberg, B. Vessby, and H. Lithell. 1984. Serum lipoprotein and apolipoprotein concentrations in patients with hyperthyroidism and the effect of treatment with carbimazole. Acta Med. Scand. 215: 453-459.
38. Canaris, G. J., N. R. Manowitz, G. Mayor, and E. C. Ridgway. 2000. The Colorado thyroid disease prevalence study. Arch. Intern. Med. 160: 526-534.
39. Kanaya, A. M., F. Harris, S. Volpato, E. J. Perez-Stable, T. Harris, and D. C. Bauer. 2002. Association between thyroid dysfunction and total cholesterol level in an older biracial population: the health, aging and body composition study. Arch. Intern. Med. 162: 773-779.
40. Vierhapper, H., A. Nardi, P. Grosser, W. Raber, and A. Gessl. 2000. Low-density lipoprotein cholesterol in subclinical hypothyroidism. Thyroid. 10: 981-984.
41. Danese, M. D., P. W. Ladenson, C. L. Meinert, and N. R. Powe. 2000. Clinical review 115: effect of thyroxine therapy on serum lipoproteins in patients with mild thyroid failure: a quantitative review of the literature. J. Clin. Endocrinol. Metab. 85: 2993-3001.
42. Kong, W. M., M. H. Sheikh, P. J. Lumb, R. P. Naoumova, D. B. Freedman, M. Crook, C. J. Dore, and N. Finer. 2002. A 6-month randomized trial of thyroxine treatment in women with mild subclinical hypothyroidism. Am. J. Med. 112: 348-354.
43. Meier, C., J. J. Staub, C. B. Roth, M. Guglielmetti, M. Kunz, A. R. Miserez, J. Drewe, P. Huber, R. Herzog, and B. Muller. 2001. TSH-controlled L-thyroxine therapy reduces cholesterol levels and clinical symptoms in subclinical hypothyroidism: a double blind, placebo-controlled trial (Basel Thyroid Study). J. Clin. Endocrinol. Metab. 86: 4860-4866.
44. Tzotzas, T., G. E. Krassas, T. Konstantinidis, and M. Bougoulia. 2000. Changes in lipoprotein(a) levels in overt and subclinical hypothyroidism before and during treatment. Thyroid. 10: 803-808.
45. Berkenstam, A., J. Kristensen, K. Mellstrom, B. Carlsson, J. Malm, S. Rehnmark, N. Garg, C. M. Andersson, M. Rudling, F. Sjoberg, et al. 2008. The thyroid hormone mimetic compound KB2115 lowers plasma LDL cholesterol and stimulates bile acid synthesis without cardiac effects in humans. Proc. Natl. Acad. Sci. USA. 105: 663-667.
46. Friederich, E., E. Pringault, M. Arpin, and D. Louvard. 1990. From the structure to the function of villin, an actin-binding protein of the brush border. Bioessays. 12: 403-408.
47. Valdar, W., L. C. Solberg, D. Gauguier, S. Burnett, P. Klenerman, W. O. Cookson, M. S. Taylor, J. N. Rawlins, R. Mott, and J. Flint. 2006. Genome-wide genetic association of complex traits in heterogeneous stock mice. Nat. Genet. 38: 879-887.
48. Williams, R. W., K. W. Broman, J. M. Cheverud, G. A. Churchill, R. W. Hitzemann, K. W. Hunter, J. D. Mountz, P. Pomp, R. H. Reeves, L. C. Schalkwyk, et al. 2002. A collaborative cross for high-precision complex trait analysis. 1st Workshop Report of the Complex Trait Consortium, Memphis, TN.
49. Purcell-Huynh, D. A., A. Weinreb, L. W. Castellani, M. Mehrabian, M. H. Doolittle, and A. J. Lusis. 1995. Genetic factors in lipoprotein metabolism. Analysis of a genetic cross between inbred mouse strains NZB/ BINJ and SM/J using a complete linkage map approach. J. Clin. Invest. 96: 1845-1858.
50. Srivastava, A. K., S. Mohan, G. L. Masinde, H. Yu, and D. J. Baylink. 2006. Identification of quantitative trait loci that regulate obesity and serum lipid levels in MRL/MpJ x SJL/J inbred mice. J. Lipid Res. 47: 123-133.
51. Reifsnyder, P. C., G. Churchill, and E. H. Leiter. 2000. Maternal environment and genotype interact to establish diabesity in mice. Genome Res. 10: 1568-1578.
52. Su, Z., Y. Li, J. C. James, M. McDuffie, A. H. Matsumoto, G. A. Helm, J. L. Weber, A. J. Lusis, and W. Shi. 2006. Quantitative trait locus analysis of atherosclerosis in an intercross between C57BL/6 and C3H mice carrying the mutant apolipoprotein E gene. Genetics. 172: 1799-1807.
53. Suto, J., Y. Takahashi, and K. Sekikawa. 2004. Quantitative trait locus analysis of plasma cholesterol and triglyceride levels in C57BL/6J x RR F2 mice. Biochem. Genet. 42: 347-363.
54. Colinayo, V. V., J. H. Qiao, X. Wang, K. L. Krass, E. Schadt, A. J. Lusis, and T. A. Drake. 2003. Genetic loci for diet-induced atherosclerotic lesions and plasma lipids in mice. Mamm. Genome. 14: 464-471.
55. Seidelmann, S. B., C. De Luca, R. L. Leibel, J. L. Breslow, A. R. Tall, and C. L. Welch. 2005. Quantitative trait locus mapping of genetic modifiers of metabolic syndrome and atherosclerosis in low-density lipoprotein receptor-deficient mice: identification of a locus for metabolic syndrome and increased atherosclerosis on chromosome 4. Arterioscler. Thromb. Vasc. Biol. 25: 204-210.
56. Ishimori, N., R. Li, P. M. Kelmenson, R. Korstanje, K. A. Walsh, G. A. Churchill, K. Forsman-Semb, and B. Paigen. 2004. Quantitative trait loci that determine plasma lipids and obesity in C57BL/6J and 129S1/SvImJ inbred mice. J. Lipid Res. 45: 1624-1632.
57. Shike, T., S. Hirose, M. Kobayashi, K. Funabiki, T. Shirai, and Y. Tomino. 2001. Susceptibility and negative epistatic loci contributing to type 2 diabetes and related phenotypes in a KK/Ta mouse model. Diabetes. 50: 1943-1948.
58. Gu, L., M. W. Johnson, and A. J. Lusis. 1999. Quantitative trait locus analysis of plasma lipoprotein levels in an autoimmune mouse model: interactions between lipoprotein metabolism, autoimmune disease, and atherogenesis. Arterioscler. Thromb. Vasc. Biol. 19: 442-453.
59. Su, Z., S. W. Tsaih, J. Szatkiewicz, Y. Shen, and B. Paigen. 2008. Candidate genes for plasma triglyceride, free fatty acid, and glucose revealed from an intercross between inbred mouse strains NZB/B1NJ x NZW/ LacJ. J. Lipid Res. 49: 1500-1510.
60. Suto, J., and K. Sekikawa. 2003. Quantitative trait locus analysis of plasma cholesterol and triglyceride levels in KK x RR F2 mice. Biochem. Genet. 41: 325-341.
61. Suto, J., S. Matsuura, H. Yamanaka, and K. Sekikawa. 1999. Quantitative trait loci that regulate plasma lipid concentration in hereditary obese KK and KK-Ay mice. Biochim. Biophys. Acta. 1453: 385-395.
62. Cheverud, J. M., T. H. Ehrich, T. Hrbek, J. P. Kenney, L. S. Pletscher, and C. F. Semenkovich. 2004. Quantitative trait loci for obesity- and diabetes-related traits and their dietary responses to high-fat feeding in LGXSM recombinant inbred mouse strains. Diabetes. 53: 3328-3336.
63. Wergedal, J. E., C. L. Ackert-Bicknell, W. G. Beamer, S. Mohan, D. J. Baylink, and A. K. Srivastava. 2007. Mapping genetic loci that regulate lipid levels in a NZB/B1NJxRF/J intercross and a combined intercross involving NZB/B1NJ, RF/J, MRL/MpJ, and SJL/J mouse strains. J. Lipid Res. 48: 1724-1734.