Effects of high fat feeding and diabetes on regression of atherosclerosis induced by low-density lipoprotein receptor gene therapy in LDL receptor-deficient mice

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Willecke, Florian ^a   Yuan, Chujun ^a   Oka, Kazuhiro ^b   Chan, Lawrence ^b   Hu, Yunying ^a   Barnhart, Shelley ^c   Bornfeldt, Karin E ^c   Goldberg, Ira J ^a   Fisher, Edward A ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD68 ANTIGEN; LOW DENSITY LIPOPROTEIN RECEPTOR; CHOLESTEROL INTAKE; COLLAGEN; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA SINUS; ARTICLE; ATHEROSCLEROSIS; BRACHIOCEPHALIC TRUNK; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; FAST PROTEIN LIQUID CHROMATOGRAPHY; HYPERGLYCEMIA; INSULIN RESISTANCE; LASER CAPTURE MICRODISSECTION; LIPID ANALYSIS; LIPID DIET; LIQUID CHROMATOGRAPHY; MALE; METABOLIC SYNDROME X; MORPHOMETRICS; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN CONTENT; QUANTITATIVE ANALYSIS; ADENOVIRIDAE; ADMINISTRATION AND DOSAGE; ANIMAL; AORTA; C57BL MOUSE; CHEMICALLY INDUCED; CHOLESTEROL INTAKE; COMPLICATION; DEFICIENCY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION; GENE THERAPY; GENE VECTOR; GENETICS; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; PATHOLOGY; PLAQUE, ATHEROSCLEROTIC; PROCEDURES;

ADENOVIRIDAE; MUS;

ADENOVIRIDAE; ANIMALS; AORTA; ATHEROSCLEROSIS; CHOLESTEROL, DIETARY; COLLAGEN; DIABETES MELLITUS, EXPERIMENTAL; DIET, HIGH-FAT; GENE EXPRESSION; GENETIC THERAPY; GENETIC VECTORS; HYPERGLYCEMIA; INSULIN RESISTANCE; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLAQUE, ATHEROSCLEROTIC; RECEPTORS, LDL; STREPTOZOCIN;

EID: 84934947529     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128996     Document Type: Article

References (51)

1. Nicholls SJ, Ballantyne CM, Barter PJ, Chapman MJ, Erbel RM, Libby P, et al. Effect of two intensive statin regimens on progression of coronary disease. N Engl J Med. 2011; 365(22):2078-87. doi: 10. 1056/NEJMoa1110874 PMID: 22085316.
2. Nozue T, Yamamoto S, Tohyama S, Fukui K, Umezawa S, Onishi Y, et al. Impact of diabetes mellitus on coronary atherosclerosis and plaque composition under statin therapy - subanalysis of the TRUTH study. Circulation journal: official journal of the Japanese Circulation Society. 2012; 76(9):2188-96. Epub 2012/07/13. PMID: 22785608.
3. Nagareddy PR, Murphy AJ, Stirzaker RA, Hu Y, Yu S, Miller RG, et al. Hyperglycemia promotes myelopoiesis and impairs the resolution of atherosclerosis. Cell metabolism. 2013; 17(5):695-708. Epub 2013/05/15. doi: 10.1016/j.cmet.2013.04.001 PMID: 23663738; PubMed Central PMCID: PMCPMC3992275.
4. Grundy SM. Obesity, metabolic syndrome, and cardiovascular disease. J Clin Endocrinol Metab. 2004; 89(6):2595-600. doi: 10.1210/jc.2004-0372 PMID: 15181029.
5. Reis ED, Li J, Fayad ZA, Rong JX, Hansoty D, Aguinaldo JG, et al. Dramatic remodeling of advanced atherosclerotic plaques of the apolipoprotein E-deficient mouse in a novel transplantation model. J Vasc Surg. 2001; 34(3):541-7. doi: 10.1067/mva.2001.115963 PMID: 11533609.
6. Chereshnev I, Trogan E, Omerhodzic S, Itskovich V, Aguinaldo JG, Fayad ZA, et al. Mouse model of heterotopic aortic arch transplantation. J Surg Res. 2003; 111(2):171-6. PMID: 12850459.
7. Lieu HD, Withycombe SK, Walker Q, Rong JX, Walzem RL, Wong JS, et al. Eliminating atherogenesis in mice by switching off hepatic lipoprotein secretion. Circulation. 2003; 107(9):1315-21. Epub 2003/03/12. PMID: 12628954.
8. Parathath S, Grauer L, Huang LS, Sanson M, Distel E, Goldberg IJ, et al. Diabetes adversely affects macrophages during atherosclerotic plaque regression in mice. Diabetes. 2011; 60(6):1759-69. doi: 10.2337/db10-0778 PMID: 21562077; PubMed Central PMCID: PMC3114401.
9. Van Craeyveld E, Gordts SC, Nefyodova E, Jacobs F, De Geest B. Regression and stabilization of advanced murine atherosclerotic lesions: a comparison of LDL lowering and HDL raising gene transfer strategies. Journal of molecular medicine (Berlin, Germany). 2011; 89(6):555-67. Epub 2011/01/21. doi: 10.1007/s00109-011-0722-x PMID: 21249329; PubMed Central PMCID: PMCPMC3098380.
10. Harris JD, Schepelmann S, Athanasopoulos T, Graham IR, Stannard AK, Mohri Z, et al. Inhibition of atherosclerosis in apolipoprotein-E-deficient mice following muscle transduction with adeno-associated virus vectors encoding human apolipoprotein-E. Gene therapy. 2002; 9(1):21-9. Epub 2002/02/19. doi: 10.1038/sj.gt.3301615 PMID: 11850719.
11. Tangirala RK, Tsukamoto K, Chun SH, Usher D, Pure E, Rader DJ. Regression of atherosclerosis induced by liver-directed gene transfer of apolipoprotein A-I in mice. Circulation. 1999; 100(17):1816-22. Epub 1999/10/27. PMID: 10534470.
12. Kawashiri M-a, Zhang Y, Usher D, Reilly M, Puré E, Rader DJ. Effects of coexpression of the LDL receptor and apoE on cholesterol metabolism and atherosclerosis in LDL receptor-deficient mice. Journal of Lipid Research. 2001; 42(6):943-50. PMID: 11369802
13. Potteaux S, Gautier EL, Hutchison SB, van Rooijen N, Rader DJ, Thomas MJ, et al. Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe-/- mice during disease regression. J Clin Invest. 2011; 121(5):2025-36. Epub 2011/04/21. doi: 10.1172/jci43802 PMID: 21505265; PubMed Central PMCID: PMCPMC3083793.
14. Li R, Chao H, Ko KW, Cormier S, Dieker C, Nour EA, et al. Gene Therapy Targeting LDL Cholesterol but not HDL Cholesterol Induces Regression of Advanced Atherosclerosis in a Mouse Model of Familial Hypercholesterolemia. J Genet Syndr Gene Ther. 2011; 2:106. Epub 2012/10/30. PMID: 23106034; PubMed Central PMCID: PMCPMC3480198.
15. Nomura S, Merched A, Nour E, Dieker C, Oka K, Chan L. Low-density lipoprotein receptor gene therapy using helper-dependent adenovirus produces long-term protection against atherosclerosis in a mouse model of familial hypercholesterolemia. Gene therapy. 2004; 11(20):1540-8. doi: 10.1038/sj.gt.3302310 PMID: 15269711.
16. Morral N, O'Neal W, Rice K, Leland M, Kaplan J, Piedra PA, et al. Administration of helper-dependent adenoviral vectors and sequential delivery of different vector serotype for long-term liver-directed gene transfer in baboons. Proceedings of the National Academy of Sciences of the United States of America. 1999; 96(22):12816-21. PMID: 10536005; PubMed Central PMCID: PMC23112.
17. Kim IH, Jozkowicz A, Piedra PA, Oka K, Chan L. Lifetime correction of genetic deficiency in mice with a single injection of helper-dependent adenoviral vector. Proceedings of the National Academy of Sciences of the United States of America. 2001; 98(23):13282-7. doi: 10.1073/pnas.241506298 PMID: 11687662; PubMed Central PMCID: PMC60862.
18. Oka K, Chan L. Liver-directed gene therapy for dyslipidemia and diabetes. Curr Atheroscler Rep. 2004; 6(3):203-9. PMID: 15068745; PubMed Central PMCID: PMC1224746.
19. Oka K, Chan L. Construction and characterization of helper-dependent adenoviral vectors for sustained in vivo gene therapy. Methods Mol Med. 2005; 108:329-50. PMID: 16028693.
20. Teupser D, Persky AD, Breslow JL. Induction of atherosclerosis by low-fat, semisynthetic diets in LDL receptor-deficient C57BL/6J and FVB/NJ mice: comparison of lesions of the aortic root, brachiocephalic artery, and whole aorta (en face measurement). Arteriosclerosis, thrombosis, and vascular biology. 2003; 23(10):1907-13. Epub 2003/08/09. doi: 10.1161/01.atv.0000090126.34881.b1 PMID: 12907460.
21. Brosius F. Low-Dose Streptozotocin Induction Protocol (Mouse). Animal Models of Diabetic Complications Consortium. 2003;www.diacomp.org/shared/showFile.aspx?doctypeid=3&docid=19, accessed May 19, 2014 (http://www.diacomp.org/shared/showFile.aspx?doctypeid=3&docid=19).
22. Hsueh W, Abel ED, Breslow JL, Maeda N, Davis RC, Fisher EA, et al. Recipes for creating animal models of diabetic cardiovascular disease. Circ Res. 2007; 100(10):1415-27. Epub 2007/05/26. doi: 10.1161/01.RES.0000266449.37396.1f PMID: 17525381.
23. Kanter JE, Kramer F, Barnhart S, Averill MM, Vivekanandan-Giri A, Vickery T, et al. Diabetes promotes an inflammatory macrophage phenotype and atherosclerosis through acyl-CoA synthetase 1. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(12):E715-24. Epub 2012/02/07. doi: 10.1073/pnas.1111600109 PMID: 22308341; PubMed Central PMCID: PMCPMC3311324.
24. Renard CB, Kramer F, Johansson F, Lamharzi N, Tannock LR, Herrath MGv, et al. Diabetes and diabetes-associated lipid abnormalities have distinct effects on initiation and progression of atherosclerotic lesions. The Journal of Clinical Investigation. 2004; 114(5):659-68. doi: 10.1172/JCI17867 PMID: 15343384
25. Feig JE, Fisher EA. Laser capture microdissection for analysis of macrophage gene expression from atherosclerotic lesions. Methods in molecular biology (Clifton, NJ). 2013; 1027:123-35. Epub 2013/08/06. doi: 10.1007/978-1-60327-369-5-5 PMID: 23912984; PubMed Central PMCID: PMCPMC4278963.
26. Finn AV, Nakano M, Narula J, Kolodgie FD, Virmani R. Concept of vulnerable/unstable plaque. Arteriosclerosis, thrombosis, and vascular biology. 2010; 30(7):1282-92. Epub 2010/06/18. doi: 10.1161/atvbaha.108.179739 PMID: 20554950.
27. Trogan E, Feig JE, Dogan S, Rothblat GH, Angeli V, Tacke F, et al. Gene expression changes in foam cells and the role of chemokine receptor CCR7 during atherosclerosis regression in ApoE-deficient mice. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103(10):3781-6. doi: 10.1073/pnas.0511043103 PMID: 16537455; PubMed Central PMCID: PMC1450154.
28. Feig JE, Rong JX, Shamir R, Sanson M, Vengrenyuk Y, Liu J, et al. HDL promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108(17):7166-71. doi: 10.1073/pnas.1016086108 PMID: 21482781; PubMed Central PMCID: PMC3084076.
29. Wright JJ, Kim J, Buchanan J, Boudina S, Sena S, Bakirtzi K, et al. Mechanisms for increased myocardial fatty acid utilization following short-term high-fat feeding. Cardiovascular research. 2009; 82(2):351-60. Epub 2009/01/17. doi: 10.1093/cvr/cvp017 PMID: 19147655; PubMed Central PMCID: PMCPMC2675931.
30. Winzell MS, Ahrén B. The High-Fat Diet-Fed Mouse: A Model for Studying Mechanisms and Treatment of Impaired Glucose Tolerance and Type 2 Diabetes. Diabetes. 2004; 53(suppl 3):S215-S9. doi: 10.2337/diabetes.53.suppl-3.S215 PMID: 15561913
31. Park SY, Cho YR, Kim HJ, Higashimori T, Danton C, Lee MK, et al. Unraveling the temporal pattern of diet-induced insulin resistance in individual organs and cardiac dysfunction in C57BL/6 mice. Diabetes. 2005; 54(12):3530-40. Epub 2005/11/25. PMID: 16306372.
32. Kennedy A, Martinez K, Chuang C- C, LaPoint K, McIntosh M. Saturated Fatty Acid-Mediated Inflammation and Insulin Resistance in Adipose Tissue: Mechanisms of Action and Implications. The Journal of Nutrition. 2009; 139(1):1-4. doi: 10.3945/jn.108.098269 PMID: 19056664
33. Reynoso R, Salgado LM, Calderon V. High levels of palmitic acid lead to insulin resistance due to changes in the level of phosphorylation of the insulin receptor and insulin receptor substrate-1. Molecular and cellular biochemistry. 2003; 246(1-2):155-62. Epub 2003/07/05. PMID: 12841357.
34. Chavez JA, Summers SA. Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Archives of biochemistry and biophysics. 2003; 419(2):101-9. Epub 2003/11/01. PMID: 14592453.
35. Forouhi NG, Koulman A, Sharp SJ, Imamura F, Kröger J, Schulze MB, et al. Differences in the prospective association between individual plasma phospholipid saturated fatty acids and incident type 2 diabetes: the EPIC-InterAct case-cohort study. The Lancet Diabetes & Endocrinology. 2014; 2(10):810-8. doi: http://dx.doi.org/10.1016/S2213-8587(14)70146-9.
36. Feig JE, Parathath S, Rong JX, Mick SL, Vengrenyuk Y, Grauer L, et al. Reversal of hyperlipidemia with a genetic switch favorably affects the content and inflammatory state of macrophages in atherosclerotic plaques. Circulation. 2011; 123(9):989-98. doi: 10.1161/CIRCULATIONAHA.110.984146 PMID: 21339485; PubMed Central PMCID: PMC3131163.
37. Tholstrup T, Hjerpsted J, Raff M. Palm olein increases plasma cholesterol moderately compared with olive oil in healthy individuals. Am J Clin Nutr. 2011; 94(6):1426-32. Epub 2011/11/11. doi: 10.3945/ajcn.111.018846 PMID: 22071711.
38. Spady DK, Woollett LA, Dietschy JM. Regulation of plasma LDL-cholesterol levels by dietary cholesterol and fatty acids. Annual review of nutrition. 1993; 13:355-81. Epub 1993/01/01. doi: 10.1146/annurev.nu.13.070193.002035 PMID: 8369151.
39. Moore RE, Kawashiri MA, Kitajima K, Secreto A, Millar JS, Pratico D, et al. Apolipoprotein A-I deficiency results in markedly increased atherosclerosis in mice lacking the LDL receptor. Arteriosclerosis, thrombosis, and vascular biology. 2003; 23(10):1914-20. Epub 2003/08/23. doi: 10.1161/01.atv.0000092328.66882.f5 PMID: 12933536.
40. Vikramadithyan RK, Hu Y, Noh HL, Liang CP, Hallam K, Tall AR, et al. Human aldose reductase expression accelerates diabetic atherosclerosis in transgenic mice. J Clin Invest. 2005; 115(9):2434-43. Epub 2005/08/30. doi: 10.1172/jci24819 PMID: 16127462; PubMed Central PMCID: PMCPMC1190371.
41. Goldberg IJ, Hu Y, Noh HL, Wei J, Huggins LA, Rackmill MG, et al. Decreased lipoprotein clearance is responsible for increased cholesterol in LDL receptor knockout mice with streptozotocin-induced diabetes. Diabetes. 2008; 57(6):1674-82. Epub 2008/03/19. doi: 10.2337/db08-0083 PMID: 18346984.
42. Gaudreault N, Kumar N, Olivas VR, Eberle D, Stephens K, Raffai RL. Hyperglycemia impairs atherosclerosis regression in mice. Am J Pathol. 2013; 183(6):1981-92. Epub 2013/10/12. doi: 10.1016/j.ajpath.2013.08.019 PMID: 24113453.
43. Johansson F, Kramer F, Barnhart S, Kanter JE, Vaisar T, Merrill RD, et al. Type 1 diabetes promotes disruption of advanced atherosclerotic lesions in LDL receptor-deficient mice. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(6):2082-7. Epub 2008/02/07. doi: 10.1073/pnas.0709958105 PMID: 18252823; PubMed Central PMCID: PMCPMC2538884.
44. Moore KJ, Sheedy FJ, Fisher EA. Macrophages in atherosclerosis: a dynamic balance. Nature reviews Immunology. 2013; 13(10):709-21. Epub 2013/09/03. doi: 10.1038/nri3520 PMID: 23995626.
45. Geissmann F, Gordon S, Hume DA, Mowat AM, Randolph GJ. Unravelling mononuclear phagocyte heterogeneity. Nature reviews Immunology. 2010; 10(6):453-60. Epub 2010/05/15. doi: 10.1038/nri2784 PMID: 20467425; PubMed Central PMCID: PMCPMC3032581.
46. Bouhlel MA, Derudas B, Rigamonti E, Dievart R, Brozek J, Haulon S, et al. PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell metabolism. 2007; 6(2):137-43. Epub 2007/08/08. doi: 10.1016/j.cmet.2007.06.010 PMID: 17681149.
47. Khallou-Laschet J, Varthaman A, Fornasa G, Compain C, Gaston AT, Clement M, et al. Macrophage plasticity in experimental atherosclerosis. PLoS One. 2010; 5(1):e8852. Epub 2010/01/30. doi: 10.1371/journal.pone.0008852 PMID: 20111605; PubMed Central PMCID: PMCPMC2810335.
48. Deonarine K, Panelli MC, Stashower ME, Jin P, Smith K, Slade HB, et al. Gene expression profiling of cutaneous wound healing. J Transl Med. 2007; 5:11. Epub 2007/02/23. doi: 10.1186/1479-5876-5-11 PMID: 17313672; PubMed Central PMCID: PMCPMC1804259.
49. Feig JE, Shang Y, Rotllan N, Vengrenyuk Y, Wu C, Shamir R, et al. Statins promote the regression of atherosclerosis via activation of the CCR7-dependent emigration pathway in macrophages. PLoS One. 2011; 6(12):e28534. Epub 2011/12/14. doi: 10.1371/journal.pone.0028534 PMID: 22163030; PubMed Central PMCID: PMCPMC3232231.
50. Rong X, Albert CJ, Hong C, Duerr MA, Chamberlain BT, Tarling EJ, et al. LXRs regulate ER stress and inflammation through dynamic modulation of membrane phospholipid composition. Cell metabolism. 2013; 18(5):685-97. Epub 2013/11/12. doi: 10.1016/j.cmet.2013.10.002 PMID: 24206663; PubMed Central PMCID: PMCPMC3889491.
51. Calkin AC, Tontonoz P. Liver x receptor signaling pathways and atherosclerosis. Arteriosclerosis, thrombosis, and vascular biology. 2010; 30(8):1513-8. Epub 2010/07/16. doi: 10.1161/atvbaha.109.191197 PMID: 20631351; PubMed Central PMCID: PMCPMC2919217.