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PMID: 19960040 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Macrophage death and defective inflammation resolution in atherosclerosis.

Nature reviews. Immunology ·Vol. 10 ·No. 1 ·2010-01-00 ·Pages 36-46

Tabas I

Abstract

A key event in atherosclerosis is a maladaptive inflammatory response to subendothelial lipoproteins. A crucial aspect of this response is a failure to resolve inflammation, which normally involves the suppression of inflammatory cell influx, effective clearance of apoptotic cells and promotion of inflammatory cell egress. Defects in these processes promote the progression of atherosclerotic lesions into dangerous plaques, which can trigger atherothrombotic vascular disease, the leading cause of death in industrialized societies. In this Review I provide an overview of these concepts, with a focus on macrophage death and defective apoptotic cell clearance, and discuss new therapeutic strategies designed to boost inflammation resolution in atherosclerosis.

MeSH Terms
Animals Apoptosis/immunology Atherosclerosis/immunology,pathology,therapy Humans Inflammation/immunology,pathology,therapy Macrophage Activation/immunology Macrophages/immunology,pathology Phagocytosis/immunology
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Tabas Ira
Department of Medicine, Physiology and Cellular Biophysics, Columbia University, New York, New York 10032, USA. iat1@columbia.edu
References (130)
130 references, click to expand
  1. Rapid regression of atherosclerosis: insights from the clinical and experimental literature.
    Nat Clin Pract Cardiovasc Med. 2008 Feb;5(2):91-102 PMID: 18223541
  2. Gene-specific control of inflammation by TLR-induced chromatin modifications.
    Nature. 2007 Jun 21;447(7147):972-8 PMID: 17538624
  3. Inflammatory resolution: new opportunities for drug discovery.
    Nat Rev Drug Discov. 2004 May;3(5):401-16 PMID: 15136788
  4. Resolution of inflammation: state of the art, definitions and terms.
    FASEB J. 2007 Feb;21(2):325-32 PMID: 17267386
  5. LXR signaling couples sterol metabolism to proliferation in the acquired immune response.
    Cell. 2008 Jul 11;134(1):97-111 PMID: 18614014
  6. Resolution of inflammation-unraveling mechanistic links between periodontitis and cardiovascular disease.
    J Dent. 2009 Aug;37(8):S582-3 PMID: 19501948
  7. Reduced macrophage apoptosis is associated with accelerated atherosclerosis in low-density lipoprotein receptor-null mice.
    Arterioscler Thromb Vasc Biol. 2005 Jan;25(1):174-9 PMID: 15499039
  8. Apoptosis of vascular smooth muscle cells in atherosclerosis.
    Atherosclerosis. 1998 May;138(1):3-9 PMID: 9678766
  9. FTY720, a synthetic sphingosine 1 phosphate analogue, inhibits development of atherosclerosis in low-density lipoprotein receptor-deficient mice.
    Circulation. 2007 Jan 30;115(4):501-8 PMID: 17242282
  10. Overexpression of interleukin-10 by activated T lymphocytes inhibits atherosclerosis in LDL receptor-deficient Mice by altering lymphocyte and macrophage phenotypes.
    Circ Res. 2002 May 31;90(10):1064-71 PMID: 12039795
  11. Lactadherin deficiency leads to apoptotic cell accumulation and accelerated atherosclerosis in mice.
    Circulation. 2007 Apr 24;115(16):2168-77 PMID: 17420351
  12. Monocyte accumulation in mouse atherogenesis is progressive and proportional to extent of disease.
    Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10340-10345 PMID: 16801531
  13. Niemann-Pick C heterozygosity confers resistance to lesional necrosis and macrophage apoptosis in murine atherosclerosis.
    Proc Natl Acad Sci U S A. 2003 Sep 2;100(18):10423-8 PMID: 12923293
  14. The sphingosine-1-phosphate analogue FTY720 reduces atherosclerosis in apolipoprotein E-deficient mice.
    Arterioscler Thromb Vasc Biol. 2007 Mar;27(3):607-13 PMID: 17158351
  15. Interleukin-10: new perspectives on an old cytokine.
    Immunol Rev. 2008 Dec;226:205-18 PMID: 19161426
  16. Transforming growth factor-beta mediates balance between inflammation and fibrosis during plaque progression.
    Arterioscler Thromb Vasc Biol. 2002 Jun 1;22(6):975-82 PMID: 12067907
  17. Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis.
    Circ Res. 2008 Feb 1;102(2):209-17 PMID: 17991882
  18. Synthetic LXR ligand inhibits the development of atherosclerosis in mice.
    Proc Natl Acad Sci U S A. 2002 May 28;99(11):7604-9 PMID: 12032330
  19. Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR.
    Immunity. 2009 Aug 21;31(2):245-58 PMID: 19646905
  20. Emigration of monocyte-derived cells to lymph nodes during resolution of inflammation and its failure in atherosclerosis.
    Curr Opin Lipidol. 2008 Oct;19(5):462-8 PMID: 18769227
  21. Apoptosis and related proteins in different stages of human atherosclerotic plaques.
    Circulation. 1998 Jun 16;97(23):2307-15 PMID: 9639374
  22. Regulation of dendritic cells and macrophages by an anti-apoptotic cell natural antibody that suppresses TLR responses and inhibits inflammatory arthritis.
    J Immunol. 2009 Jul 15;183(2):1346-59 PMID: 19564341
  23. Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor (op) and apolipoprotein E.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8264-8 PMID: 7667279
  24. Macrophage EP4 deficiency increases apoptosis and suppresses early atherosclerosis.
    Cell Metab. 2008 Dec;8(6):492-501 PMID: 19041765
  25. Milk fat globule epidermal growth factor-factor VIII is down-regulated in sepsis via the lipopolysaccharide-CD14 pathway.
    J Immunol. 2009 Jan 1;182(1):581-7 PMID: 19109191
  26. Apoptotic cell removal.
    Curr Biol. 2001 Oct 2;11(19):R795-805 PMID: 11591341
  27. The arginase II gene is an anti-inflammatory target of liver X receptor in macrophages.
    J Biol Chem. 2006 Oct 27;281(43):32197-206 PMID: 16943198
  28. Anti-inflammatory cytokine profile in acute coronary syndromes: behavior of interleukin-10 in association with serum metalloproteinases and proinflammatory cytokines.
    Int J Cardiol. 2003 Dec;92(2-3):169-75 PMID: 14659849
  29. Liver X receptor-dependent repression of matrix metalloproteinase-9 expression in macrophages.
    J Biol Chem. 2003 Mar 21;278(12):10443-9 PMID: 12531895
  30. Macrophage suppression following phagocytosis of apoptotic neutrophils is mediated by the S100A9 calcium-binding protein.
    Immunobiology. 2010 May;215(5):341-7 PMID: 19656587
  31. Increased CD36 protein as a response to defective insulin signaling in macrophages.
    J Clin Invest. 2004 Mar;113(5):764-73 PMID: 14991075
  32. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum.
    Genes Dev. 1998 Apr 1;12(7):982-95 PMID: 9531536
  33. Atherosclerosis: evidence for impairment of resolution of vascular inflammation governed by specific lipid mediators.
    FASEB J. 2008 Oct;22(10):3595-606 PMID: 18559988
  34. Apoptosis and efferocytosis in mouse models of atherosclerosis.
    Curr Drug Targets. 2007 Dec;8(12):1288-96 PMID: 18220705
  35. Vulnerable plaque: the pathology of unstable coronary lesions.
    J Interv Cardiol. 2002 Dec;15(6):439-46 PMID: 12476646
  36. Interleukin-10 deficiency increases atherosclerosis, thrombosis, and low-density lipoproteins in apolipoprotein E knockout mice.
    Mol Med. 2003 Jan-Feb;9(1-2):10-7 PMID: 12765335
  37. TGF-beta and TNF-alpha: antagonistic cytokines controlling type I collagen gene expression.
    Cell Signal. 2004 Aug;16(8):873-80 PMID: 15157666
  38. Leukocyte transglutaminase 2 expression limits atherosclerotic lesion size.
    Arterioscler Thromb Vasc Biol. 2006 Mar;26(3):563-9 PMID: 16410462
  39. Downregulated CD36 and oxLDL uptake and stimulated ABCA1/G1 and cholesterol efflux as anti-atherosclerotic mechanisms of interleukin-10.
    Cardiovasc Res. 2006 Feb 1;69(2):527-35 PMID: 16336952
  40. Vascular smooth muscle cell-derived, Gla-containing growth-potentiating factor for Ca(2+)-mobilizing growth factors.
    J Biol Chem. 1995 Mar 17;270(11):5702-5 PMID: 7890695
  41. Calcium/calmodulin-dependent protein kinase II links ER stress with Fas and mitochondrial apoptosis pathways.
    J Clin Invest. 2009 Oct;119(10):2925-41 PMID: 19741297
  42. Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions.
    Cell Metab. 2006 Apr;3(4):257-66 PMID: 16581003
  43. A role for the apoptosis inhibitory factor AIM/Spalpha/Api6 in atherosclerosis development.
    Cell Metab. 2005 Mar;1(3):201-13 PMID: 16054063
  44. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation.
    Nat Rev Immunol. 2009 Jan;9(1):62-70 PMID: 19104500
  45. Macrophage diversity and polarization in atherosclerosis: a question of balance.
    Arterioscler Thromb Vasc Biol. 2009 Oct;29(10):1419-23 PMID: 19696407
  46. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency.
    Arterioscler Thromb Vasc Biol. 2005 Nov;25(11):2255-64 PMID: 16141399
  47. Novel pharmacological strategies for driving inflammatory cell apoptosis and enhancing the resolution of inflammation.
    Trends Pharmacol Sci. 2008 May;29(5):250-7 PMID: 18407359
  48. Cholesterol-induced apoptotic macrophages elicit an inflammatory response in phagocytes, which is partially attenuated by the Mer receptor.
    J Biol Chem. 2006 Mar 10;281(10):6707-17 PMID: 16380374
  49. Histochemical detection and differentiation of free and esterified cholesterol in swine atherosclerosis using filipin.
    Exp Mol Pathol. 1984 Jun;40(3):288-94 PMID: 6202548
  50. Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/- and Ldlr-/- mice lacking CHOP.
    Cell Metab. 2009 May;9(5):474-81 PMID: 19416717
  51. Macrophage p53 controls macrophage death in atherosclerotic lesions of apolipoprotein E deficient mice.
    Atherosclerosis. 2009 Dec;207(2):399-404 PMID: 19608184
  52. Leukocyte-derived interleukin 10 is required for protection against atherosclerosis in low-density lipoprotein receptor knockout mice.
    Arterioscler Thromb Vasc Biol. 2004 Aug;24(8):1474-8 PMID: 15178562
  53. Defective mer receptor tyrosine kinase signaling in bone marrow cells promotes apoptotic cell accumulation and accelerates atherosclerosis.
    Arterioscler Thromb Vasc Biol. 2008 Aug;28(8):1429-31 PMID: 18467644
  54. Interleukin-10 blocks atherosclerotic events in vitro and in vivo.
    Arterioscler Thromb Vasc Biol. 1999 Dec;19(12):2847-53 PMID: 10591660
  55. Macrophage phagocytosis of apoptotic neutrophils is critically regulated by the opposing actions of pro-inflammatory and anti-inflammatory agents: key role for TNF-alpha.
    FASEB J. 2009 Mar;23(3):844-54 PMID: 18971259
  56. Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis.
    Arterioscler Thromb Vasc Biol. 2005 Jun;25(6):1256-61 PMID: 15831805
  57. Combinatorial pattern recognition receptor signaling alters the balance of life and death in macrophages.
    Proc Natl Acad Sci U S A. 2006 Dec 26;103(52):19794-9 PMID: 17167049
  58. Alternative activation of macrophages: an immunologic functional perspective.
    Annu Rev Immunol. 2009;27:451-83 PMID: 19105661
  59. Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions.
    J Exp Med. 2009 Jan 16;206(1):15-23 PMID: 19103881
  60. Obesity, metabolic syndrome, and cardiovascular disease.
    J Clin Endocrinol Metab. 2004 Jun;89(6):2595-600 PMID: 15181029
  61. Atherosclerosis. the road ahead.
    Cell. 2001 Feb 23;104(4):503-16 PMID: 11239408
  62. Shattuck lecture--cardiovascular medicine at the turn of the millennium: triumphs, concerns, and opportunities.
    N Engl J Med. 1997 Nov 6;337(19):1360-9 PMID: 9358131
  63. Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome.
    Circulation. 2007 Sep 11;116(11):1226-33 PMID: 17709641
  64. Impaired clearance of apoptotic cells promotes synergy between atherogenesis and autoimmune disease.
    J Exp Med. 2004 Apr 19;199(8):1121-31 PMID: 15096538
  65. Improved outcome after acute coronary syndromes with an intensive versus standard lipid-lowering regimen: results from the Pravastatin or Atorvastatin Evaluation and Infection Therapy-Thrombolysis in Myocardial Infarction 22 (PROVE IT-TIMI 22) trial.
    Am J Med. 2005 Dec;118 Suppl 12A:28-35 PMID: 16356805
  66. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications.
    Circulation. 2007 Oct 16;116(16):1832-44 PMID: 17938300
  67. Extracellular Nampt promotes macrophage survival via a nonenzymatic interleukin-6/STAT3 signaling mechanism.
    J Biol Chem. 2008 Dec 12;283(50):34833-43 PMID: 18945671
  68. Macrophage liver X receptor is required for antiatherogenic activity of LXR agonists.
    Arterioscler Thromb Vasc Biol. 2005 Jan;25(1):135-42 PMID: 15539622
  69. Signal transducer and activator of transcription-1 is critical for apoptosis in macrophages subjected to endoplasmic reticulum stress in vitro and in advanced atherosclerotic lesions in vivo.
    Circulation. 2008 Feb 19;117(7):940-51 PMID: 18227389
  70. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice.
    Nat Med. 2009 Aug;15(8):940-5 PMID: 19633655
  71. Oxidized low-density lipoproteins trigger endoplasmic reticulum stress in vascular cells: prevention by oxygen-regulated protein 150 expression.
    Circ Res. 2009 Feb 13;104(3):328-36 PMID: 19106412
  72. Modulation of phagocytosis of apoptotic neutrophils by supernatant from dexamethasone-treated macrophages and annexin-derived peptide Ac(2-26).
    J Immunol. 2005 Mar 15;174(6):3727-33 PMID: 15749912
  73. Migration to apoptotic "find-me" signals is mediated via the phagocyte receptor G2A.
    J Biol Chem. 2008 Feb 29;283(9):5296-305 PMID: 18089568
  74. Putting on the brakes: cyclic AMP as a multipronged controller of macrophage function.
    Sci Signal. 2009 Jun 16;2(75):pe37 PMID: 19531801
  75. Coordination of inflammation and metabolism by PPAR and LXR nuclear receptors.
    Curr Opin Genet Dev. 2008 Oct;18(5):461-7 PMID: 18782619
  76. Atherosclerosis.
    Nature. 2000 Sep 14;407(6801):233-41 PMID: 11001066
  77. Cytokines in the generation and maturation of dendritic cells: recent advances.
    Eur Cytokine Netw. 2002 Apr-Jun;13(2):186-99 PMID: 12101074
  78. PPAR-gamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation.
    Nat Med. 2001 Jan;7(1):48-52 PMID: 11135615
  79. The GAIT system: a gatekeeper of inflammatory gene expression.
    Trends Biochem Sci. 2009 Jul;34(7):324-31 PMID: 19535251
  80. Regression of atherosclerosis: role of nitric oxide and apoptosis.
    Circulation. 1999 Mar 9;99(9):1236-41 PMID: 10069793
  81. Mechanisms and consequences of macrophage apoptosis in atherosclerosis.
    J Lipid Res. 2009 Apr;50 Suppl:S382-7 PMID: 18953058
  82. Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of apoe-/- mice.
    Arterioscler Thromb Vasc Biol. 2008 Aug;28(8):1421-8 PMID: 18451332
  83. Phagocytosis in atherosclerosis: Molecular mechanisms and implications for plaque progression and stability.
    Cardiovasc Res. 2007 Feb 1;73(3):470-80 PMID: 17084825
  84. Cues for apoptotic cell engulfment: eat-me, don't eat-me and come-get-me signals.
    Trends Cell Biol. 2003 Dec;13(12):648-56 PMID: 14624843
  85. TGF-beta: the perpetrator of immune suppression by regulatory T cells and suicidal T cells.
    J Leukoc Biol. 2004 Jul;76(1):15-24 PMID: 14966194
  86. Highly purified omega-3 polyunsaturated fatty acids are effective as adjunct therapy for secondary prevention of myocardial infarction.
    Herz. 2006 Dec;31 Suppl 3:49-59 PMID: 17575805
  87. Inflammation in atherosclerosis.
    Nature. 2002 Dec 19-26;420(6917):868-74 PMID: 12490960
  88. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity.
    Circulation. 1999 Jan 26;99(3):348-53 PMID: 9918520
  89. Aromatic lipoxin A4 and lipoxin B4 analogues display potent biological activities.
    J Med Chem. 2007 Nov 29;50(24):5894-902 PMID: 17960922
  90. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation.
    J Clin Invest. 2002 Jan;109(1):41-50 PMID: 11781349
  91. Complement C1q reduces early atherosclerosis in low-density lipoprotein receptor-deficient mice.
    Am J Pathol. 2007 Jan;170(1):416-26 PMID: 17200212
  92. The unfolded protein response is an important regulator of inflammatory genes in endothelial cells.
    Arterioscler Thromb Vasc Biol. 2006 Nov;26(11):2490-6 PMID: 16931790
  93. Molecular imaging and therapy of atherosclerosis with targeted nanoparticles.
    J Magn Reson Imaging. 2007 Apr;25(4):667-80 PMID: 17347992
  94. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance.
    Nature. 2007 Jun 28;447(7148):1116-20 PMID: 17515919
  95. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages.
    J Immunol. 2000 Feb 15;164(4):1663-7 PMID: 10657608
  96. THE DISTRIBUTION OF LIPIDS AND ENZYMES IN THE AORTIC WALL IN DIETARY RABBIT ATHEROMA AND HUMAN ATHEROSCLEROSIS.
    J Pathol Bacteriol. 1963 Oct;86:421-30 PMID: 14068950
  97. Rimonabant, a selective cannabinoid CB1 receptor antagonist, inhibits atherosclerosis in LDL receptor-deficient mice.
    Arterioscler Thromb Vasc Biol. 2009 Jan;29(1):12-8 PMID: 18845788
  98. Recognition and phagocytosis of cells undergoing apoptosis.
    Br Med Bull. 1997;53(3):491-508 PMID: 9374033
  99. Chronic inflammation: a failure of resolution?
    Int J Exp Pathol. 2007 Apr;88(2):85-94 PMID: 17408451
  100. Serum levels of interleukin-10 are inversely related to future events in patients with acute myocardial infarction.
    J Thromb Haemost. 2004 Feb;2(2):350-2 PMID: 14996010
  101. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte.
    Cell. 2005 Oct 21;123(2):321-34 PMID: 16239148
  102. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques.
    Proc Natl Acad Sci U S A. 2004 Aug 10;101(32):11779-84 PMID: 15280540
  103. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators.
    Nat Rev Immunol. 2008 May;8(5):349-61 PMID: 18437155
  104. The pro- and anti-inflammatory markers in patients with acute myocardial infarction and chronic stable angina.
    Int J Mol Med. 2004 Aug;14(2):317-22 PMID: 15254785
  105. Mitochondrial calcium signalling and cell death: approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis.
    Cell Calcium. 2006 Nov-Dec;40(5-6):553-60 PMID: 17074387
  106. CaMKII inhibition protects against necrosis and apoptosis in irreversible ischemia-reperfusion injury.
    Cardiovasc Res. 2007 Mar 1;73(4):689-98 PMID: 17217936
  107. Negative regulation of toll-like receptor-mediated immune responses.
    Nat Rev Immunol. 2005 Jun;5(6):446-58 PMID: 15928677
  108. Morphologic findings of coronary atherosclerotic plaques in diabetics: a postmortem study.
    Arterioscler Thromb Vasc Biol. 2004 Jul;24(7):1266-71 PMID: 15142859
  109. Loss of SR-A and CD36 activity reduces atherosclerotic lesion complexity without abrogating foam cell formation in hyperlipidemic mice.
    Arterioscler Thromb Vasc Biol. 2009 Jan;29(1):19-26 PMID: 18948635
  110. Macrophages and atherosclerotic plaque stability.
    Curr Opin Lipidol. 1996 Oct;7(5):330-5 PMID: 8937525
  111. Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor.
    J Cell Biol. 2005 Oct 10;171(1):61-73 PMID: 16203857
  112. Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase.
    Nature. 1999 Jul 22;400(6742):378-82 PMID: 10432118
  113. Induction of transglutaminase 2 by a liver X receptor/retinoic acid receptor alpha pathway increases the clearance of apoptotic cells by human macrophages.
    Circ Res. 2009 Aug 14;105(4):393-401 PMID: 19628791
  114. Reciprocal regulation of inflammation and lipid metabolism by liver X receptors.
    Nat Med. 2003 Feb;9(2):213-9 PMID: 12524534
  115. In vivo downregulation of T helper cell 1 immune responses reduces atherogenesis in apolipoprotein E-knockout mice.
    Circulation. 2001 Jul 10;104(2):197-202 PMID: 11447086
  116. Dyslipidemia associated with atherosclerotic disease systemically alters dendritic cell mobilization.
    Immunity. 2004 Oct;21(4):561-74 PMID: 15485633
  117. New phosphatidylserine receptors: clearance of apoptotic cells and more.
    Dev Cell. 2007 Dec;13(6):759-60 PMID: 18061557
  118. Cannabinoids, endocannabinoids, and related analogs in inflammation.
    AAPS J. 2009 Mar;11(1):109-19 PMID: 19199042
  119. Ligand activation of LXR beta reverses atherosclerosis and cellular cholesterol overload in mice lacking LXR alpha and apoE.
    J Clin Invest. 2007 Aug;117(8):2337-46 PMID: 17657314
  120. The prevalence and incidence of coronary heart disease is significantly increased in periodontitis: a meta-analysis.
    Am Heart J. 2007 Nov;154(5):830-7 PMID: 17967586
  121. TGF-[beta]1 limits plaque growth, stabilizes plaque structure, and prevents aortic dilation in apolipoprotein E-null mice.
    Arterioscler Thromb Vasc Biol. 2009 Sep;29(9):1251-7 PMID: 19325140
  122. Differential inhibition of macrophage foam-cell formation and atherosclerosis in mice by PPARalpha, beta/delta, and gamma.
    J Clin Invest. 2004 Dec;114(11):1564-76 PMID: 15578089
  123. Effects of EPA on coronary artery disease in hypercholesterolemic patients with multiple risk factors: sub-analysis of primary prevention cases from the Japan EPA Lipid Intervention Study (JELIS).
    Atherosclerosis. 2008 Sep;200(1):135-40 PMID: 18667204
  124. Macrophage deficiency of p38alpha MAPK promotes apoptosis and plaque necrosis in advanced atherosclerotic lesions in mice.
    J Clin Invest. 2009 Apr;119(4):886-98 PMID: 19287091
  125. Inhibition of transforming growth factor-beta signaling accelerates atherosclerosis and induces an unstable plaque phenotype in mice.
    Circ Res. 2001 Nov 9;89(10):930-4 PMID: 11701621
  126. Animal models of spontaneous plaque rupture: the holy grail of experimental atherosclerosis research.
    Curr Atheroscler Rep. 2002 May;4(3):238-42 PMID: 11931722
  127. A soluble form of the Mer receptor tyrosine kinase inhibits macrophage clearance of apoptotic cells and platelet aggregation.
    Blood. 2007 Feb 1;109(3):1026-33 PMID: 17047157
  128. Emerging role of Toll-like receptors in atherosclerosis.
    J Lipid Res. 2009 Apr;50 Suppl:S340-5 PMID: 18980945
  129. Apoptosis and plaque destabilization in atherosclerosis: the role of macrophage apoptosis induced by cholesterol.
    Cell Death Differ. 2004 Jul;11 Suppl 1:S12-6 PMID: 15143347
  130. Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis.
    J Cell Biol. 2009 Sep 21;186(6):783-92 PMID: 19752026
Article Info
Journal
Nature reviews. Immunology
Abbr.
Nat Rev Immunol
ISSN
1474-1741
Published
2010-01-00
Epub
2009-00-04
Pages
36-46
Language
English
Region
England
NLM ID
101124169
PMCID
PMC2854623
Subset
IM
Grants
NHLBI NIH HHS · HL75662 · United States
NHLBI NIH HHS · P01 HL054591 · United States
NHLBI NIH HHS · R01 HL075662 · United States
NHLBI NIH HHS · HL54591 · United States
NHLBI NIH HHS · P01 HL054591-140004 · United States
NHLBI NIH HHS · R01 HL075662-07 · United States
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