Reversal of hyperlipidemia with a genetic switch favorably affects the content and inflammatory state of macrophages in atherosclerotic plaques

Circulation

Volumn 123, Issue 9, 2011, Pages 989-998

  Feig, Jonathan E ^a   Parathath, Sajesh ^a   Rong, James X ^a,d   Mick, Stephanie L ^a   Vengrenyuk, Yuliya ^a   Grauer, Lisa ^a   Young, Stephen G ^b   Fisher, Edward A ^a,c,e  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d GLAXOSMITHKLINE   (United States)

^e Smilow 8 ^*  (United States)

Author keywords

atherosclerosis; lipoproteins; macrophage; murine model

Indexed keywords

CD68 ANTIGEN; CHOLESTEROL; CLODRONIC ACID; COLLAGEN; LIPID; PIOGLITAZONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROGENIC DIET; ATHEROSCLEROTIC PLAQUE; CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; GENE EXPRESSION; GENETIC MARKER; HYPERLIPIDEMIA; LIPID BLOOD LEVEL; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CARRIER PROTEINS; CELL MOVEMENT; DISEASE MODELS, ANIMAL; GENE TARGETING; GENE THERAPY; GENES, SWITCH; HYPERCHOLESTEROLEMIA; INFLAMMATION; MACROPHAGES; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSOMES; MONOCYTES; PLAQUE, ATHEROSCLEROTIC;

EID: 79952736069     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.110.984146     Document Type: Article

References (41)

1. Reis ED, Li J, Fayad ZA, Rong JX, Hansoty D, Aguinaldo JG, Fallon JT, Fisher EA. Dramatic remodeling of advanced atherosclerotic plaques of the apolipoprotein E-deficient mouse in a novel transplantation model. J Vasc Surg. 2001;34:541-547. (Pubitemid 33661190)
2. Trogan E, Fayad ZA, Itskovich VV, Aguinaldo JG, Mani V, Fallon JT, Chereshnev I, Fisher EA. Serial studies of mouse atherosclerosis by in vivo magnetic resonance imaging detect lesion regression after correction of dyslipidemia. Arterioscler Thromb Vasc Biol. 2004;24:1714-1719. (Pubitemid 39180900)
3. Llodra J, Angeli V, Liu J, Trogan E, Fisher EA, Randolph GJ. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc Natl Acad Sci USA. 2004;101:11779-11784. (Pubitemid 39095371)
4. Trogan E, Feig JE, Dogan S, Rothblat GH, Angeli V, Tacke F, Randolph GJ, Fisher EA. Gene expression changes in foam cells and the role of chemokine receptor ccr7 during atherosclerosis regression in apoEdeficient mice. Proc Natl Acad Sci USA. 2006;103:3781-3786. (Pubitemid 43376632)
5. Forster R, Schubel A, Breitfeld D, Kremmer E, Renner-Muller I, Wolf E, Lipp M. Ccr7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell. 1999; 99:23-33. (Pubitemid 29468627)
6. Lieu HD, Withycombe SK, Walker Q, Rong JX, Walzem RL, Wong JS, Hamilton RL, Fisher EA, Young SG. Eliminating atherogenesis in mice by switching off hepatic lipoprotein secretion. Circulation. 2003;107: 1315-1321. (Pubitemid 36314417)
7. Wetterau JR, Aggerbeck LP, Bouma ME, Eisenberg C, Munck A, Hermier M, Schmitz J, Gay G, Rader DJ, Gregg RE. Absence of microsomal triglyceride transfer protein in individuals with abetalipoproteinemia. Science. 1992;258:999-1001.
8. Gordon S. Alternative activation of macrophages. Nat Rev Immunol. 2003;3:23-35. (Pubitemid 37328697)
9. Dormandy JA, Charbonnel B, Eckland DJ, Erdmann E, Massi-Benedetti M, Moules IK, Skene AM, Tan MH, Lefebvre PJ, Murray GD, Standl E, Wilcox RG, Wilhelmsen L, Betteridge J, Birkeland K, Golay A, Heine RJ, Koranyi L, Laakso M, Mokan M, Norkus A, Pirags V, Podar T, Scheen A, Scherbaum W, Schernthaner G, Schmitz O, Skrha J, Smith U, Taton J. Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROACTIVE Study (Prospective Pioglitazone Clinical Trial in Macrovascular Events): a randomised controlled trial. Lancet. 2005;366:1279-1289. (Pubitemid 41416583)
10. Tacke F, Ginhoux F, Jakubzick C, Van Rooijen N, Merad M, Randolph GJ. Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. J Exp Med. 2006;203:583-597.
11. Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, Van Rooijen N, Lira SA, Habenicht AJ, Randolph GJ. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest. 2007;117:185-194. (Pubitemid 46048465)
12. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoEdeficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb. 1994;14:133-140.
13. Trogan E, Fisher EA. Laser capture microdissection for analysis of macrophage gene expression from atherosclerotic lesions. Methods Mol Biol. 2005;293:221-231.
14. Schneider F, Sukhova GK, Aikawa M, Canner J, Gerdes N, Tang SM, Shi GP, Apte SS, Libby P. Matrix-metalloproteinase-14 deficiency in bonemarrow- derived cells promotes collagen accumulation in mouse atherosclerotic plaques. Circulation. 2008;117:931-939. (Pubitemid 351272591)
15. Li AC, Binder CJ, Gutierrez A, Brown KK, Plotkin CR, Pattison JW, Valledor AF, Davis RA, Willson TM, Witztum JL, Palinski W, Glass CK. Differential inhibition of macrophage foam-cell formation and atherosclerosis in mice by PPARalpha, beta/delta, and gamma. J Clin Invest. 2004;114:1564-1576. (Pubitemid 40385547)
16. Rong JX, Shapiro M, Trogan E, Fisher EA. Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading. Proc Natl Acad Sci USA. 2003;100:13531-13536. (Pubitemid 37444776)
17. Bouhlel MA, Derudas B, Rigamonti E, Dievart R, Brozek J, Haulon S, Zawadzki C, Jude B, Torpier G, Marx N, Staels B, Chinetti-Gbaguidi G. PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab. 2007;6:137-143. (Pubitemid 47189091)
18. Gregoire C, Cognet C, Chasson L, Coupet CA, Dalod M, Reboldi A, Marvel J, Sallusto F, Vivier E, Walzer T. Intrasplenic trafficking of natural killer cells is redirected by chemokines upon inflammation. Eur J Immunol. 2008;38:2076-2084.
19. Boring L, Gosling J, Cleary M, Charo IF. Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature. 1998;394:894-897.
20. Lesnik P, Haskell CA, Charo IF. Decreased atherosclerosis in CX3CR1-/- mice reveals a role for fractalkine in atherogenesis. J Clin Invest. 2003;111:333-340.
21. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ. LY-6CHI monocytes dominate hypercholesterolemiaassociated monocytosis and give rise to macrophages in atheromata. J Clin Invest. 2007;117:195-205. (Pubitemid 46048466)
22. Tacke F, Randolph GJ. Migratory fate and differentiation of blood monocyte subsets. Immunobiology. 2006;211:609-618.
23. Finn AV, Nakano M, Narula J, Kolodgie FD, Virmani R. Concept of vulnerable/unstable plaque. Arterioscler Thromb Vasc Biol. 2010;30: 1282-1292.
24. Williams KJ, Feig JE, Fisher EA. Rapid regression of atherosclerosis: insights from the clinical and experimental literature. Nat Clin Pract Cardiovasc Med. 2008;5:91-102. (Pubitemid 351168064)
25. Mantovani A, Sica A, Locati M. Macrophage polarization comes of age. Immunity. 2005;23:344-346. (Pubitemid 41443435)
26. Vaughan DE. PAI-1 and atherothrombosis. J Thromb Haemost. 2005;3: 1879-1883. (Pubitemid 41716575)
27. Kato K, Satoh H, Endo Y, Yamada D, Midorikawa S, Sato W, Mizuno K, Fujita T, Tsukamoto K, Watanabe T. Thiazolidinediones down-regulate plasminogen activator inhibitor type 1 expression in human vascular endothelial cells: a possible role for PPARgamma in endothelial function. Biochem Biophys Res Commun. 1999;258:431-435. (Pubitemid 29287068)
28. Chereshnev I, Trogan E, Omerhodzic S, Itskovich V, Aguinaldo JG, Fayad ZA, Fisher EA, Reis ED. Mouse model of heterotopic aortic arch transplantation. J Surg Res. 2003;111:171-176. (Pubitemid 36808906)
29. Damas JK, Smith C, Oie E, Fevang B, Halvorsen B, Waehre T, Boullier A, Breland U, Yndestad A, Ovchinnikova O, Robertson AK, Sandberg WJ, Kjekshus J, Tasken K, Froland SS, Gullestad L, Hansson GK, Quehenberger O, Aukrust P. Enhanced expression of the homeostatic chemokines ccl19 and ccl21 in clinical and experimental atherosclerosis: possible pathogenic role in plaque destabilization. Arterioscler Thromb Vasc Biol. 2007;27:614-620.
30. Khallou-Laschet J, Varthaman A, Fornasa G, Compain C, Gaston AT, Clement M, Dussiot M, Levillain O, Graff-Dubois S, Nicoletti A, Caligiuri G. Macrophage plasticity in experimental atherosclerosis. PLoS One. 2010;5:e8852.
31. Nathan CF, Murray HW, Wiebe ME, Rubin BY. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med. 1983;158:670-689. (Pubitemid 13051337)
32. Goerdt S, Politz O, Schledzewski K, Birk R, Gratchev A, Guillot P, Hakiy N, Klemke CD, Dippel E, Kodelja V, Orfanos CE. Alternative versus classical activation of macrophages. Pathobiology. 1999;67:222-226. (Pubitemid 30135909)
33. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol. 2000;164:6166-6173. (Pubitemid 30408793)
34. Zhu X, Lee JY, Timmins JM, Brown JM, Boudyguina E, Mulya A, Gebre AK, Willingham MC, Hiltbold EM, Mishra N, Maeda N, Parks JS. Increased cellular free cholesterol in macrophage-specific abca1 knock-out mice enhances pro-inflammatory response of macrophages. J Biol Chem. 2008;283:22930-22941.
35. Yvan-Charvet L, Welch C, Pagler TA, Ranalletta M, Lamkanfi M, Han S, Ishibashi M, Li R, Wang N, Tall AR. Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation. 2008;118:1837-1847.
36. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, Red Eagle A, Vats D, Brombacher F, Ferrante AW, Chawla A. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature. 2007;447:1116-1120. (Pubitemid 47014427)
37. Thorp E, Kuriakose G, Shah YM, Gonzalez FJ, Tabas I. Pioglitazone increases macrophage apoptosis and plaque necrosis in advanced atherosclerotic lesions of nondiabetic low-density lipoprotein receptor-null mice. Circulation. 2007;116:2182-2190. (Pubitemid 350060356)
38. Durante W, Johnson FK, Johnson RA. Arginase: a critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol. 2007;34:906-911. (Pubitemid 47083958)
39. Kastelein JJ, Wedel MK, Baker BF, Su J, Bradley JD, Yu RZ, Chuang E, Graham MJ, Crooke RM. Potent reduction of apolipoprotein B and low-density lipoprotein cholesterol by short-term administration of an antisense inhibitor of apolipoprotein B. Circulation. 2006;114: 1729-1735. (Pubitemid 44607121)
40. Samaha FF, McKenney J, Bloedon LT, Sasiela WJ, Rader DJ. Inhibition of microsomal triglyceride transfer protein alone or with ezetimibe in patients with moderate hypercholesterolemia. Nat Clin Pract Cardiovasc Med. 2008;5:497-505.
41. LaRosa JC, Grundy SM, Waters DD, Shear C, Barter P, Fruchart JC, Gotto AM, Greten H, Kastelein JJ, Shepherd J, Wenger NK. Intensive lipid lowering with atorvastatin in patients with stable coronary disease. N Engl J Med. 2005;352:1425-1435. (Pubitemid 40471450)