Macrophage phenotypes and their modulation in atherosclerosis

Circulation Journal

Volumn 78, Issue 8, 2014, Pages 1775-1781

  De Paoli, Federica ^a   Staels, Bart ^a   Chinetti Gbaguidi, Giulia ^a  

^a UNIV LILLE   (France)

Author keywords

Atherosclerosis; Macrophage phenotypes; Modulators

Indexed keywords

HIGH DENSITY LIPOPROTEIN; MICRORNA; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; THIOREDOXIN; TRANSCRIPTION FACTOR; TXN PROTEIN, HUMAN;

ANIMAL; ATHEROSCLEROSIS; CLASSIFICATION; HUMAN; IMMUNOLOGY; MACROPHAGE; PATHOLOGY; TH1 CELL; TH2 CELL;

ANIMALS; ATHEROSCLEROSIS; HUMANS; LIPOPROTEINS, HDL; MACROPHAGES; MICRORNAS; TH1 CELLS; TH2 CELLS; THIOREDOXINS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 84905028309     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-14-0621     Document Type: Review

References (83)

1. Ross R. Atherosclerosis: An inflammatory disease. N Engl J Med 1999; 340: 115-126.
2. Porcheray F, Viaud S, Rimaniol AC, Leone C, Samah B, Dereuddre- Bosquet N, et al. Macrophage activation switching: An asset for the resolution of inflammation. Clin Exp Immunol 2005; 142: 481-489.
3. Mantovani A, Garlanda C, Locati M. Macrophage diversity and polarization in atherosclerosis: A question of balance. Arterioscler Thromb Vasc Biol 2009; 29: 1419-1423.
4. Gordon S, Martinez FO. Alternative activation of macrophages: Mechanism and functions. Immunity 2010; 32: 593-604.
5. Stein M, Keshav S, Harris N, Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: A marker of alternative immunologic macrophage activation. J Exp Med 1992; 176: 287-292.
6. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004; 25: 677-686.
7. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci 2008; 13: 453-461.
8. Zizzo G, Hilliard BA, Monestier M, Cohen PL. Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J Immunol 2012; 189: 3508-3520.
9. Pinhal-Enfield G, Ramanathan M, Hasko G, Vogel SN, Salzman AL, Boons GJ, et al. An angiogenic switch in macrophages involving synergy between Toll-like receptors 2, 4, 7, and 9 and adenosine A(2A) receptors. Am J Pathol 2003; 163: 711-721.
10. Ferrante CJ, Pinhal-Enfield G, Elson G, Cronstein BN, Hasko G, Outram S, et al. The adenosine-dependent angiogenic switch of macrophages to an M2-like phenotype is independent of interleukin- 4 receptor alpha (IL-4Ralpha) signaling. Inflammation 2013; 36: 921-931.
11. Verreck FA, de Boer T, Langenberg DM, Hoeve MA, Kramer M, Vaisberg E, et al. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci USA 2004; 101: 4560-4565.
12. Waldo SW, Li Y, Buono C, Zhao B, Billings EM, Chang J, et al. Heterogeneity of human macrophages in culture and in atherosclerotic plaques. Am J Pathol 2008; 172: 1112-1126.
13. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: New molecules and patterns of gene expression. J Immunol 2006; 177: 7303-7311.
14. Gleissner CA, Shaked I, Little KM, Ley K. CXC chemokine ligand 4 induces a unique transcriptome in monocyte-derived macrophages. J Immunol 2010; 184: 4810-4818.
15. Adamson S, Leitinger N. Phenotypic modulation of macrophages in response to plaque lipids. Curr Opin Lipidol 2011; 22: 335-342.
16. Bouhlel MA, Derudas B, Rigamonti E, Dievart R, Brozek J, Haulon S, et al. PPARg activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab 2007; 6: 137-143.
17. Chinetti-Gbaguidi G, Baron M, Bouhlel MA, Vanhoutte J, Copin C, Sebti Y, et al. Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARγ and LXRα pathways. Circ Res 2011; 108: 985-995.
18. Boyle JJ, Harrington HA, Piper E, Elderfield K, Stark J, Landis RC, et al. Coronary intraplaque hemorrhage evokes a novel atheroprotective macrophage phenotype. Am J Pathol 2009; 174: 1097-1108.
19. Boyle JJ, Johns M, Kampfer T, Nguyen AT, Game L, Schaer DJ, et al. Activating transcription factor 1 directs Mhem atheroprotective macrophages through coordinated iron handling and foam cell protection. Circ Res 2012; 110: 20-33.
20. Finn AV, Nakano M, Polavarapu R, Karmali V, Saeed O, Zhao X, et al. Hemoglobin directs macrophage differentiation and prevents foam cell formation in human atherosclerotic plaques. J Am Coll Cardiol 2012; 59: 166-177.
21. Bories G, Colin S, Vanhoutte J, Derudas B, Copin C, Fanchon M, et al. Liver X receptor (LXR) activation stimulates iron export in human alternative macrophages. Circ Res 2013; 113: 1196-1205.
22. Erbel C, Tyka M, Helmes CM, Akhavanpoor M, Rupp G, Domschke G, et al. CXCL4-induced plaque macrophages can be specifically identified by co-expression of MMP7+S100A8+ in vitro and in vivo. Innate Immun 2014 March 24, doi:10.1177/1753425914526461.
23. Gleissner CA, Shaked I, Erbel C, Bockler D, Katus HA, Ley K. CXCL4 downregulates the atheroprotective hemoglobin receptor CD163 in human macrophages. Circ Res 2010; 106: 203-211.
24. Kadl A, Meher AK, Sharma PR, Lee MY, Doran AC, Johnstone SR, et al. Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ Res 2010; 107: 737-746.
25. Khallou-Laschet J, Varthaman A, Fornasa G, Compain C, Gaston AT, Clement M, et al. Macrophage plasticity in experimental atherosclerosis. PLoS One 2010; 5: e8852, doi:10.1371/journal.pone. 0008852.
26. Brocheriou I, Maouche S, Durand H, Braunersreuther V, Le Naour G, Gratchev A, et al. Antagonistic regulation of macrophage phenotype by M-CSF and GM-CSF: Implication in atherosclerosis. Atherosclerosis 2010; 214: 316-324.
27. Stoger JL, Gijbels MJ, van der Velden S, Manca M, van der Loos CM, Biessen EA, et al. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis 2012; 225: 461-468.
28. Cho KY, Miyoshi H, Kuroda S, Yasuda H, Kamiyama K, Nakagawara J, et al. The phenotype of infiltrating macrophages influences arteriosclerotic plaque vulnerability in the carotid artery. J Stroke Cerebrovasc Dis 2013; 22: 910-918.
29. Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell 2009; 136: 215-233.
30. Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 2005; 436: 740-744.
31. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 2006; 20: 515-524.
32. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 2010; 10: 111-122.
33. Raitoharju E, Lyytikainen LP, Levula M, Oksala N, Mennander A, Tarkka M, et al. miR-21, miR-210, miR-34a, and miR-146a/b are up-regulated in human atherosclerotic plaques in the Tampere Vascular Study. Atherosclerosis 2011; 219: 211-217.
34. Bidzhekov K, Gan L, Denecke B, Rostalsky A, Hristov M, Koeppel TA, et al. microRNA expression signatures and parallels between monocyte subsets and atherosclerotic plaque in humans. Thromb Haemost 2012; 107: 619-625.
35. Nazari-Jahantigh M, Wei Y, Noels H, Akhtar S, Zhou Z, Koenen RR, et al. MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J Clin Invest 2012; 122: 4190-4202.
36. O'Connell RM, Chaudhuri AA, Rao DS, Baltimore D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA 2009; 106: 7113-7118.
37. Donners MM, Wolfs IM, Stoger LJ, Van der Vorst EP, Pottgens CC, Heymans S, et al. Hematopoietic miR155 deficiency enhances atherosclerosis and decreases plaque stability in hyperlipidemic mice. PLoS One 2012; 7: e35877, doi:10.1371/journal.pone.0035877.
38. Cai X, Yin Y, Li N, Zhu D, Zhang J, Zhang CY, et al. Re-polarization of tumor-associated macrophages to pro-inflammatory M1 macrophages by microRNA-155. J Mol Cell Biol 2012; 4: 341-343.
39. Liu G, Friggeri A, Yang Y, Park YJ, Tsuruta Y, Abraham E. miR- 147, a microRNA that is induced upon Toll-like receptor stimulation, regulates murine macrophage inflammatory responses. Proc Natl Acad Sci USA 2009; 106: 15819-15824.
40. Sheedy FJ, Palsson-McDermott E, Hennessy EJ, Martin C, O'Leary JJ, Ruan Q, et al. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR- 21. Nat Immunol 2010; 11: 141-147.
41. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 2006; 103: 12481-12486.
42. Androulidaki A, Iliopoulos D, Arranz A, Doxaki C, Schworer S, Zacharioudaki V, et al. The kinase Akt1 controls macrophage response to lipopolysaccharide by regulating microRNAs. Immunity 2009; 31: 220-231.
43. Chaudhuri AA, So AY, Sinha N, Gibson WS, Taganov KD, O'Connell RM, et al. MicroRNA-125b potentiates macrophage activation. J Immunol 2011; 187: 5062-5068.
44. Gallardo-Soler A, Gomez-Nieto C, Campo ML, Marathe C, Tontonoz P, Castrillo A, et al. Arginase I induction by modified lipoproteins in macrophages: A peroxisome proliferator-activated receptor-gamma/ delta-mediated effect that links lipid metabolism and immunity. Mol Endocrinol 2008; 22: 1394-1402.
45. Bouhlel MA, Brozek J, Derudas B, Zawadzki C, Jude B, Staels B, et al. Unlike PPARgamma, PPARalpha or PPARbeta/delta activation does not promote human monocyte differentiation toward alternative macrophages. Biochem Biophys Res Commun 2009; 386: 459-462.
46. Kang K, Reilly SM, Karabacak V, Gangl MR, Fitzgerald K, Hatano B, et al. Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity. Cell Metab 2008; 7: 485-495.
47. Odegaard JI, Ricardo-Gonzalez RR, Red Eagle A, Vats D, Morel CR, Goforth MH, et al. Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab 2008; 7: 496-507.
48. Prieur X, Mok CY, Velagapudi VR, Nunez V, Fuentes L, Montaner D, et al. Differential lipid partitioning between adipocytes and tissue macrophages modulates macrophage lipotoxicity and M2/M1 polarization in obese mice. Diabetes 2011; 60: 797-809.
49. Stienstra R, Duval C, Keshtkar S, van der Laak J, Kersten S, Muller M. Peroxisome proliferator-activated receptor gamma activation promotes infiltration of alternatively activated macrophages into adipose tissue. J Biol Chem 2008; 283: 22620-22627.
50. Liao X, Sharma N, Kapadia F, Zhou G, Lu Y, Hong H, et al. Kruppellike factor 4 regulates macrophage polarization. J Clin Invest 2011; 121: 2736-2749.
51. Date D, Das R, Narla G, Simon DI, Jain MK, Mahabeleshwar GH. Kruppel-like transcription factor 6 regulates inflammatory macrophage polarization. J Biol Chem 2014; 289: 10318-10329.
52. Pourcet B, Feig JE, Vengrenyuk Y, Hobbs AJ, Kepka-Lenhart D, Garabedian MJ, et al. LXRalpha regulates macrophage arginase 1 through PU.1 and interferon regulatory factor 8. Circ Res 2011; 109: 492-501.
53. Ma H, Zhong W, Jiang Y, Fontaine C, Li S, Fu J, et al. Increased atherosclerotic lesions in LDL receptor deficient mice with hematopoietic nuclear receptor Rev-erbα knock- down. J Am Heart Assoc 2013; 2: e000235, doi:10.1161/JAHA.113.000235.
54. Hanna RN, Carlin LM, Hubbeling HG, Nackiewicz D, Green AM, Punt JA, et al. The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C- monocytes. Nat Immunol 2011; 12: 778-785.
55. Hamers AA, Vos M, Rassam F, Marinkovic G, Kurakula K, van Gorp PJ, et al. Bone marrow-specific deficiency of nuclear receptor Nur77 enhances atherosclerosis. Circ Res 2012; 110: 428-438.
56. Hanna RN, Shaked I, Hubbeling HG, Punt JA, Wu R, Herrley E, et al. NR4A1 (Nur77) deletion polarizes macrophages toward an inflammatory phenotype and increases atherosclerosis. Circ Res 2012; 110: 416-427.
57. Chao LC, Soto E, Hong C, Ito A, Pei L, Chawla A, et al. Bone marrow NR4A expression is not a dominant factor in the development of atherosclerosis or macrophage polarization in mice. J Lipid Res 2013; 54: 806-815.
58. Murphy E. Estrogen signaling and cardiovascular disease. Circ Res; 109: 687-696.
59. Ribas V, Drew BG, Le JA, Soleymani T, Daraei P, Sitz D, et al. Myeloid-specific estrogen receptor alpha deficiency impairs metabolic homeostasis and accelerates atherosclerotic lesion development. Proc Natl Acad Sci USA 2011; 108: 16457-16462.
60. Rader DJ. Molecular regulation of HDL metabolism and function: Implications for novel therapies. J Clin Invest 2006; 116: 3090-3100.
61. Cockerill GW, Rye KA, Gamble JR, Vadas MA, Barter PJ. Highdensity lipoproteins inhibit cytokine-induced expression of endothelial cell adhesion molecules. Arterioscler Thromb Vasc Biol 1995; 15: 1987-1994.
62. 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. Proc Natl Acad Sci USA 2011; 108: 7166-7171.
63. Sanson M, Distel E, Fisher EA. HDL induces the expression of the M2 macrophage markers arginase 1 and Fizz-1 in a STAT6-dependent process. PLoS One 2013; 8: e74676, doi:10.1371/journal.pone. 0074676.
64. Colin S, Fanchon M, Belloy L, Bochem AE, Copin C, Derudas B, et al. HDL does not influence the polarization of human monocytes toward an alternative phenotype. Int J Cardiol 2014; 172: 179-184.
65. Yamawaki H, Haendeler J, Berk BC. Thioredoxin: A key regulator of cardiovascular homeostasis. Circ Res 2003; 93: 1029-1033.
66. Holmgren A, Lu J. Thioredoxin and thioredoxin reductase: Current research with special reference to human disease. Biochem Biophys Res Commun 2010; 396: 120-124.
67. El Hadri K, Mahmood DF, Couchie D, Jguirim-Souissi I, Genze F, Diderot V, et al. Thioredoxin-1 promotes anti-inflammatory macrophages of the M2 phenotype and antagonizes atherosclerosis. Arterioscler Thromb Vasc Biol 2012; 32: 1445-1452.
68. Mahmood DF, Abderrazak A, Couchie D, Lunov O, Diderot V, Syrovets T, et al. Truncated thioredoxin (Trx-80) promotes pro-inflammatory macrophages of the M1 phenotype and enhances atherosclerosis. J Cell Physiol 2013; 228: 1577-1583.
69. Vezina C, Kudelski A, Sehgal SN. Rapamycin (AY-22,989), a new antifungal antibiotic. I: Taxonomy of the producing streptomycete and isolation of the active principle. J Antibiot (Tokyo) 1975; 28: 721-726.
70. Terada N, Lucas JJ, Szepesi A, Franklin RA, Domenico J, Gelfand EW. Rapamycin blocks cell cycle progression of activated T cells prior to events characteristic of the middle to late G1 phase of the cycle. J Cell Physiol 1993; 154: 7-15.
71. Inoki K, Corradetti MN, Guan KL. Dysregulation of the TSC-mTOR pathway in human disease. Nat Genet 2005; 37: 19-24.
72. Mercalli A, Sordi V, Ponzoni M, Maffi P, De Taddeo F, Gatti G, et al. Rapamycin induces a caspase-independent cell death in human monocytes. Am J Transplant 2006; 6: 1331-1341.
73. Weichhart T, Costantino G, Poglitsch M, Rosner M, Zeyda M, Stuhlmeier KM, et al. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 2008; 29: 565-577.
74. Mercalli A, Calavita I, Dugnani E, Citro A, Cantarelli E, Nano R, et al. Rapamycin unbalances the polarization of human macrophages to M1. Immunology 2013; 140: 179-190.
75. Byles V, Covarrubias AJ, Ben-Sahra I, Lamming DW, Sabatini DM, Manning BD, et al. The TSC-mTOR pathway regulates macrophage polarization. Nat Commun 2013; 4: 2834.
76. Assaad-Khalil SH, Lachine N, Sidrak M, Amara F, Jacotot B, Fahmy MH. Immuno-metabolic factors in schistosomal hepatic fibrosis modulating atherogenesis. Ann Biol Clin (Paris) 1992; 50: 697-701.
77. Cudejko C, Wouters K, Fuentes L, Hannou SA, Paquet C, Bantubungi K, et al. p16INK4a deficiency promotes IL-4-induced polarization and inhibits proinflammatory signaling in macrophages. Blood 2011; 118: 2556-2566.
78. Wolfs IM, Stoger JL, Goossens P, Pottgens C, Gijbels MJ, Wijnands E, et al. Reprogramming macrophages to an anti-inflammatory phenotype by helminth antigens reduces murine atherosclerosis. Faseb J 2014; 28: 288-299.
79. Adams MJ, Hardenbergh PH, Constine LS, Lipshultz SE. Radiationassociated cardiovascular disease. Crit Rev Oncol Hematol 2003; 45: 55-75.
80. Darby SC, Cutter DJ, Boerma M, Constine LS, Fajardo LF, Kodama K, et al. Radiation-related heart disease: Current knowledge and future prospects. Int J Radiat Oncol Biol Phys 2010; 76: 656-665.
81. Hoving S, Heeneman S, Gijbels MJ, te Poele JA, Russell NS, Daemen MJ, et al. Single-dose and fractionated irradiation promote initiation and progression of atherosclerosis and induce an inflammatory plaque phenotype in ApoE(-/-) mice. Int J Radiat Oncol Biol Phys 2008; 71: 848-857.
82. Stewart FA, Heeneman S, Te Poele J, Kruse J, Russell NS, Gijbels M, et al. Ionizing radiation accelerates the development of atherosclerotic lesions in ApoE-/- mice and predisposes to an inflammatory plaque phenotype prone to hemorrhage. Am J Pathol 2006; 168: 649-658.
83. Gabriels K, Hoving S, Gijbels MJ, Pol JF, Te Poele JA, Biessen EA, et al. Irradiation of existing atherosclerotic lesions increased inflammation by favoring pro-inflammatory macrophages. Radiother Oncol 2014; 110: 455-460.