Monocytes and macrophages in abdominal aortic aneurysm

Nature Reviews Cardiology

Volumn 14, Issue 8, 2017, Pages 457-471

  Raffort, Juliette ^a,b,c,d   Lareyre, Fabien ^a,c,d   Clément, Marc ^a   Hassen Khodja, Réda ^c,d   Chinetti, Giulia ^c,d   Mallat, Ziad ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSERM   (France)

^c PASTEUR HOSPITAL   (France)

^d UNIVERSITY HOSPITAL OF NICE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; BIOLOGICAL MARKER; CATHEPSIN S; CD163 ANTIGEN; CD68 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CX3CR1; CHEMOKINE RECEPTOR CXCR3; CXCL1 CHEMOKINE; FLUORODEOXYGLUCOSE F 18; GELATINASE B; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; KRUPPEL LIKE FACTOR 5; KRUPPEL LIKE FACTOR 6; L SELECTIN; LYMPHOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN 6C; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; PEROXIREDOXIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RGS PROTEIN; STROMAL CELL DERIVED FACTOR 1; TISSUE INHIBITOR OF METALLOPROTEINASE; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE; UNCLASSIFIED DRUG;

ABDOMINAL AORTIC ANEURYSM; BLOOD VESSEL PERMEABILITY; CELL PROLIFERATION; CELL SUBPOPULATION; CYTOKINE PRODUCTION; DISEASE COURSE; DRUG TARGETING; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; INFLAMMATION; LEUKOCYTE MIGRATION; MACROPHAGE; MACROPHAGE MIGRATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MONOCYTE; MONOCYTOSIS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; TISSUE REPAIR; VASCULAR SMOOTH MUSCLE CELL; ARTERITIS; DRUG DEVELOPMENT; DRUG EFFECT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULAR REMODELING;

AORTIC ANEURYSM, ABDOMINAL; ARTERITIS; DRUG DISCOVERY; EXTRACELLULAR MATRIX; HUMANS; MACROPHAGES; MONOCYTES; VASCULAR REMODELING;

EID: 85017417601     PISSN: 17595002     EISSN: 17595010     Source Type: Journal    
DOI: 10.1038/nrcardio.2017.52     Document Type: Review

References (182)

1. Nordon, I. M., Hinchliffe, R. J., Loftus, I. M. & Thompson, M. M. Pathophysiology and epidemiology of abdominal aortic aneurysms. Nat. Rev. Cardiol. 8, 92-102 (2011).
2. Golledge, J., Muller, J., Daugherty, A. & Norman, P. Abdominal aortic aneurysm: pathogenesis and implications for management. Arterioscler. Thromb. Vasc. Biol. 26, 2605-2613 (2006).
3. Hong, H., Yang, Y., Liu, B. & Cai, W. Imaging of abdominal aortic aneurysm: the present and the future. Curr. Vasc. Pharmacol. 8, 808-819 (2010).
4. Trollope, A., Moxon, J. V., Moran, C. S. & Golledge, J. Animal models of abdominal aortic aneurysm and their role in furthering management of human disease. Cardiovasc. Pathol. 20, 114-123 (2011).
5. Dale, M. A., Ruhlman, M. K. & Baxter, B. T. Inflammatory cell phenotypes in AAAs: their role and potential as targets for therapy. Arterioscler. Thromb. Vasc. Biol. 35, 1746-1755 (2015).
6. Ziegler-Heitbrock, L. et al. Nomenclature of monocytes and dendritic cells in blood. Blood 116, e74-e80 (2010).
7. Idzkowska, E. et al. The role of different monocyte subsets in the pathogenesis of atherosclerosis and acute coronary syndromes. Scand. J. Immunol. 82, 163-173 (2015).
8. Yang, J., Zhang, L., Yu, C., Yang, X. F. & Wang, H. Monocyte and macrophage differentiation: circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomark. Res. 2, 1 (2014).
9. Wong, K. L. et al. Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood 118, e16-e31 (2011).
10. Randolph, G. J. The fate of monocytes in atherosclerosis. J. Thromb. Haemost. 7 (Suppl. 1), 28-30 (2009).
11. Auffray, C., Sieweke, M. H. & Geissmann, F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27, 669-692 (2009).
12. Dutta, P. & Nahrendorf, M. Regulation and consequences of monocytosis. Immunol. Rev. 262, 167-178 (2014).
13. Drechsler, M., Duchene, J. & Soehnlein, O. Chemokines control mobilization, recruitment, and fate of monocytes in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 35, 1050-1055 (2015).
14. Ghigliotti, G. et al. CD16+ monocyte subsets are increased in large abdominal aortic aneurysms and are differentially related with circulating and cell-associated biochemical and inflammatory biomarkers. Dis. Markers 34, 131-142 (2013).
15. Rubio-Navarro, A. et al. Hemoglobin induces monocyte recruitment and CD163-macrophage polarization in abdominal aortic aneurysm. Int. J. Cardiol. 201, 66-78 (2015).
16. Lamblin, N. et al. Profile of macrophages in human abdominal aortic aneurysms: a transcriptomic, proteomic, and antibody protein array study. J. Proteome Res. 9, 3720-3729 (2010).
17. Moran, C. S. et al. Everolimus limits aortic aneurysm in the apolipoprotein E-deficient mouse by downregulating C-C chemokine receptor 2 positive monocytes. Arterioscler. Thromb. Vasc. Biol. 33, 814-821 (2013).
18. Tsou, C. L. et al. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J. Clin. Invest. 117, 902-909 (2007).
19. Mellak, S. et al. Angiotensin II mobilizes spleen monocytes to promote the development of abdominal aortic aneurysm in Apoe-mice. Arterioscler. Thromb. Vasc. Biol. 35, 378-388 (2015).
20. Yu, H. et al. Angiopoietin-2 attenuates angiotensin II-induced aortic aneurysm and atherosclerosis in apolipoprotein E-deficient mice. Sci. Rep. 6, 35190 (2016).
21. Owens, A. P. III et al. MyD88 deficiency attenuates angiotensin II-induced abdominal aortic aneurysm formation independent of signaling through Toll-like receptors 2 and 4. Arterioscler. Thromb. Vasc. Biol. 31, 2813-2819 (2011).
22. Hanna, R. N. et al. The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C- monocytes. Nat. Immunol. 12, 778-785 (2011).
23. Cui, M. et al. Orphan nuclear receptor Nur77 inhibits angiotensin II-induced vascular remodeling via downregulation of beta-catenin. Hypertension 67, 153-162 (2016).
24. Hanna, R. N. et al. NR4A1 (Nur77) deletion polarizes macrophages toward an inflammatory phenotype and increases atherosclerosis. Circ. Res. 110, 416-427 (2012).
25. Hamers, A. A. et al. Bone marrow-specific deficiency of nuclear receptor Nur77 enhances atherosclerosis. Circ. Res. 110, 428-438 (2012).
26. Thomas, G. D. et al. Deleting an Nr4a1 super-enhancer subdomain ablates Ly6Clow monocytes while preserving macrophage gene function. Immunity 45, 975-987 (2016).
27. Satoh, T. et al. Identification of an atypical monocyte and committed progenitor involved in fibrosis. Nature 541, 96-101 (2017).
28. Murray, P. J. et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41, 14-20 (2014).
29. Tabas, I. & Bornfeldt, K. E. Macrophage phenotype and function in different stages of atherosclerosis. Circ. Res. 118, 653-667 (2016).
30. Chinetti-Gbaguidi, G., Colin, S. & Staels, B. Macrophage subsets in atherosclerosis. Nat. Rev. Cardiol. 12, 10-17 (2015).
31. Menezes, S. et al. The heterogeneity of Ly6Chi monocytes controls their differentiation into iNOS+ macrophages or monocyte-derived dendritic cells. Immunity 45, 1205-1218 (2016).
32. Martinez, F. O. & Gordon, S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 6, 13 (2014).
33. Tieu, B. C. et al. An adventitial IL-6/MCP1 amplification loop accelerates macrophage-mediated vascular inflammation leading to aortic dissection in mice. J. Clin. Invest. 119, 3637-3651 (2009).
34. Wang, Y. et al. TGF-beta activity protects against inflammatory aortic aneurysm progression and complications in angiotensin II-infused mice. J. Clin. Invest. 120, 422-432 (2010).
35. Daugherty, A., Manning, M. W. & Cassis, L. A. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J. Clin. Invest. 105, 1605-1612 (2000).
36. Turner, G. H. et al. Assessment of macrophage infiltration in a murine model of abdominal aortic aneurysm. J. Magn. Reson. Imaging 30, 455-460 (2009).
37. Pyo, R. et al. Targeted gene disruption of matrix metalloproteinase-9 (gelatinase B) suppresses development of experimental abdominal aortic aneurysms. J. Clin. Invest. 105, 1641-1649 (2000).
38. Wang, Y. X. et al. Angiotensin II increases urokinase-type plasminogen activator expression and induces aneurysm in the abdominal aorta of apolipoprotein E-deficient mice. Am. J. Pathol. 159, 1455-1464 (2001).
39. Saraff, K., Babamusta, F., Cassis, L. A. & Daugherty, A. Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 23, 1621-1626 (2003).
40. Dutertre, C. A. et al. Deciphering the stromal and hematopoietic cell network of the adventitia from non-aneurysmal and aneurysmal human aorta. PLoS ONE 9, e89983 (2014).
41. Rao, J. et al. Distinct macrophage phenotype and collagen organization within the intraluminal thrombus of abdominal aortic aneurysm. J. Vasc. Surg. 62, 585-593 (2015).
42. Boytard, L. et al. Role of proinflammatory CD68+ mannose receptor- macrophages in peroxiredoxin-1 expression and in abdominal aortic aneurysms in humans. Arterioscler. Thromb. Vasc. Biol. 33, 431-438 (2013).
43. Qin, Z. et al. Angiotensin II-induced TLR4 mediated abdominal aortic aneurysm in apolipoprotein E knockout mice is dependent on STAT3. J. Mol. Cell. Cardiol. 87, 160-170 (2015).
44. Dale, M. A. et al. Elastin-derived peptides promote abdominal aortic aneurysm formation by modulating M1/M2 macrophage polarization. J. Immunol. 196, 4536-4543 (2016).
45. Rateri, D. L. et al. Prolonged infusion of angiotensin II in apoE-mice promotes macrophage recruitment with continued expansion of abdominal aortic aneurysm. Am. J. Pathol. 179, 1542-1548 (2011).
46. Moore, J. P. et al. M2 macrophage accumulation in the aortic wall during angiotensin II infusion in mice is associated with fibrosis, elastin loss, and elevated blood pressure. Am. J. Physiol. Heart Circ. Physiol. 309, H906-H917 (2015).
47. Torocsik, D. et al. Factor XIII-A is involved in the regulation of gene expression in alternatively activated human macrophages. Thromb. Haemost. 104, 709-717 (2010).
48. Bakker, E. N. et al. Flow-dependent remodeling of small arteries in mice deficient for tissue-type transglutaminase: possible compensation by macrophage-derived factor XIII. Circ. Res. 99, 86-92 (2006).
49. Zhou, J. et al. CXCR3-dependent accumulation and activation of perivascular macrophages is necessary for homeostatic arterial remodeling to hemodynamic stresses. J. Exp. Med. 207, 1951-1966 (2010).
50. Zizzo, G., Hilliard, B. A., Monestier, M. & Cohen, P. L. Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J. Immunol. 189, 3508-3520 (2012).
51. Haskard, D. O., Boyle, J. J., Evans, P. C., Mason, J. C. & Randi, A. M. Cytoprotective signaling and gene expression in endothelial cells and macrophages-lessons for atherosclerosis. Microcirculation 20, 203-216 (2013).
52. Finn, A. V. et al. Hemoglobin directs macrophage differentiation and prevents foam cell formation in human atherosclerotic plaques. J. Am. Coll. Cardiol. 59, 166-177 (2012).
53. Boyle, J. J. et al. Activating transcription factor 1 directs Mhem atheroprotective macrophages through coordinated iron handling and foam cell protection. Circ. Res. 110, 20-33 (2012).
54. Perdiguero, E. G. & Geissmann, F. The development and maintenance of resident macrophages. Nat. Immunol. 17, 2-8 (2016).
55. Ginhoux, F. & Guilliams, M. Tissue-resident macrophage ontogeny and homeostasis. Immunity 44, 439-449 (2016).
56. Epelman, S. et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40, 91-104 (2014).
57. Ensan, S. et al. Self-renewing resident arterial macrophages arise from embryonic CX3CR1+ precursors and circulating monocytes immediately after birth. Nat. Immunol. 17, 159-168 (2016).
58. Lhotak, S. et al. Characterization of proliferating lesion-resident cells during all stages of atherosclerotic growth. J. Am. Heart Assoc. 5, e003945 (2016).
59. Lavine, K. J. et al. Distinct macrophage lineages contribute to disparate patterns of cardiac recovery and remodeling in the neonatal and adult heart. Proc. Natl Acad. Sci. USA 111, 16029-16034 (2014).
60. Woollard, K. J. & Geissmann, F. Monocytes in atherosclerosis: subsets and functions. Nat. Rev. Cardiol. 7, 77-86 (2010).
61. Michineau, S. et al. Chemokine (C-X-C motif) receptor 4 blockade by AMD3100 inhibits experimental abdominal aortic aneurysm expansion through anti-inflammatory effects. Arterioscler. Thromb. Vasc. Biol. 34, 1747-1755 (2014).
62. Nahrendorf, M. et al. Detection of macrophages in aortic aneurysms by nanoparticle positron emission tomography-computed tomography. Arterioscler. Thromb. Vasc. Biol. 31, 750-757 (2011).
63. Zhang, P. et al. Smad4 deficiency in smooth muscle cells initiates the formation of aortic aneurysm. Circ. Res. 118, 388-399 (2016).
64. Tan, C. K. et al. SMAD3 deficiency promotes inflammatory aortic aneurysms in angiotensin II-infused mice via activation of iNOS. J. Am. Heart Assoc. 2, e000269 (2013).
65. Babamusta, F. et al. Angiotensin II infusion induces site-specific intra-laminar hemorrhage in macrophage colony-stimulating factor-deficient mice. Atherosclerosis 186, 282-290 (2006).
66. Combadiere, C. et al. Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6Chi and Ly6Clo monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation 117, 1649-1657 (2008).
67. Ishibashi, M. et al. Bone marrow-derived monocyte chemoattractant protein-1 receptor CCR2 is critical in angiotensin II-induced acceleration of atherosclerosis and aneurysm formation in hypercholesterolemic mice. Arterioscler. Thromb. Vasc. Biol. 24, e174-e178 (2004).
68. Tieu, B. C. et al. Aortic adventitial fibroblasts participate in angiotensin-induced vascular wall inflammation and remodeling. J. Vasc. Res. 48, 261-272 (2011).
69. Moehle, C. W. et al. Bone marrow-derived MCP1 required for experimental aortic aneurysm formation and smooth muscle phenotypic modulation. J. Thorac. Cardiovasc. Surg. 142, 1567-1574 (2011).
70. Iida, Y. et al. Peptide inhibitor of CXCL4-CCL5 heterodimer formation, MKEY, inhibits experimental aortic aneurysm initiation and progression. Arterioscler. Thromb. Vasc. Biol. 33, 718-726 (2013).
71. MacTaggart, J. N., Xiong, W., Knispel, R. & Baxter, B. T. Deletion of CCR2 but not CCR5 or CXCR3 inhibits aortic aneurysm formation. Surgery 142, 284-288 (2007).
72. Kehrl, J. H. Heterotrimeric G protein signaling: roles in immune function and fine-tuning by RGS proteins. Immunity 8, 1-10 (1998).
73. Patel, J. et al. RGS1 regulates myeloid cell accumulation in atherosclerosis and aortic aneurysm rupture through altered chemokine signalling. Nat. Commun. 6, 6614 (2015).
74. Ley, K. The role of selectins in inflammation and disease. Trends Mol. Med. 9, 263-268 (2003).
75. Hannawa, K. K. et al. L-selectin-mediated neutrophil recruitment in experimental rodent aneurysm formation. Circulation 112, 241-247 (2005).
76. Soehnlein, O., Lindbom, L. & Weber, C. Mechanisms underlying neutrophil-mediated monocyte recruitment. Blood 114, 4613-4623 (2009).
77. Norman, P. E. & Curci, J. A. Understanding the effects of tobacco smoke on the pathogenesis of aortic aneurysm. Arterioscler. Thromb. Vasc. Biol. 33, 1473-1477 (2013).
78. Harrison, D. G. et al. Inflammation, immunity, and hypertension. Hypertension 57, 132-140 (2011).
79. Hance, K. A., Tataria, M., Ziporin, S. J., Lee, J. K. & Thompson, R. W. Monocyte chemotactic activity in human abdominal aortic aneurysms: role of elastin degradation peptides and the 67-kD cell surface elastin receptor. J. Vasc. Surg. 35, 254-261 (2002).
80. Bruemmer, D. et al. Angiotensin II-accelerated atherosclerosis and aneurysm formation is attenuated in osteopontin-deficient mice. J. Clin. Invest. 112, 1318-1331 (2003).
81. Liu, Z. et al. Thrombospondin-1 (TSP1) contributes to the development of vascular inflammation by regulating monocytic cell motility in mouse models of abdominal aortic aneurysm. Circ. Res. 117, 129-141 (2015).
82. Gong, Y., Hart, E., Shchurin, A. & Hoover-Plow, J. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J. Clin. Invest. 118, 3012-3024 (2008).
83. Sho, E. et al. Hemodynamic forces regulate mural macrophage infiltration in experimental aortic aneurysms. Exp. Mol. Pathol. 76, 108-116 (2004).
84. Golledge, J., Clancy, P., Jamrozik, K. & Norman, P. E. Obesity, adipokines, and abdominal aortic aneurysm: Health in Men study. Circulation 116, 2275-2279 (2007).
85. Thanassoulis, G. et al. Periaortic adipose tissue and aortic dimensions in the Framingham Heart Study. J. Am. Heart Assoc. 1, e000885 (2012).
86. Police, S. B., Thatcher, S. E., Charnigo, R., Daugherty, A. & Cassis, L. A. Obesity promotes inflammation in periaortic adipose tissue and angiotensin II-induced abdominal aortic aneurysm formation. Arterioscler. Thromb. Vasc. Biol. 29, 1458-1464 (2009).
87. Blomkalns, A. L. et al. CD14 directs adventitial macrophage precursor recruitment: role in early abdominal aortic aneurysm formation. J. Am. Heart Assoc. 2, e000065 (2013).
88. Wang, K. C. et al. Membrane-bound thrombomodulin regulates macrophage inflammation in abdominal aortic aneurysm. Arterioscler. Thromb. Vasc. Biol. 35, 2412-2422 (2015).
89. Samadzadeh, K. M. et al. Monocyte activity is linked with abdominal aortic aneurysm diameter. J. Surg. Res. 190, 328-334 (2014).
90. Murray, P. J. & Wynn, T. A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723-737 (2011).
91. Longo, G. M. et al. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J. Clin. Invest. 110, 625-632 (2002).
92. Longo, G. M. et al. MMP-12 has a role in abdominal aortic aneurysms in mice. Surgery 137, 457-462 (2005).
93. Qin, Y. et al. Deficiency of cathepsin S attenuates angiotensin II-induced abdominal aortic aneurysm formation in apolipoprotein E-deficient mice. Cardiovasc. Res. 96, 401-410 (2012).
94. Eskandari, M. K. et al. Enhanced abdominal aortic aneurysm in TIMP-1-deficient mice. J. Surg. Res. 123, 289-293 (2005).
95. Curci, J. A., Liao, S., Huffman, M. D., Shapiro, S. D. & Thompson, R. W. Expression and localization of macrophage elastase (matrix metalloproteinase-12) in abdominal aortic aneurysms. J. Clin. Invest. 102, 1900-1910 (1998).
96. Liu, J. et al. Cathepsin L expression and regulation in human abdominal aortic aneurysm, atherosclerosis, and vascular cells. Atherosclerosis 184, 302-311 (2006).
97. Takei, Y., Tanaka, T., Kent, K. C. & Yamanouchi, D. Osteoclastogenic differentiation of macrophages in the development of abdominal aortic aneurysms. Arterioscler. Thromb. Vasc. Biol. 36, 1962-1971 (2016).
98. Findeisen, H. M. et al. Telomerase deficiency in bone marrow-derived cells attenuates angiotensin II-induced abdominal aortic aneurysm formation. Arterioscler. Thromb. Vasc. Biol. 31, 253-260 (2011).
99. Ma, D. et al. Inhibition of KLF5-Myo9b-RhoA pathway-mediated podosome formation in macrophages ameliorates abdominal aortic aneurysm. Circ. Res. 120, 799-815 (2017).
100. Shimizu, K., Mitchell, R. N. & Libby, P. Inflammation and cellular immune responses in abdominal aortic aneurysms. Arterioscler. Thromb. Vasc. Biol. 26, 987-994 (2006).
101. Mallat, Z. Macrophages. Arterioscler. Thromb. Vasc. Biol. 34, 2509-2519 (2014).
102. Arango Duque, G. & Descoteaux, A. Macrophage cytokines: involvement in immunity and infectious diseases. Front. Immunol. 5, 491 (2014).
103. Mosser, D. M. & Edwards, J. P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8, 958-969 (2008).
104. Anzai, A. et al. Adventitial CXCL1/G-CSF expression in response to acute aortic dissection triggers local neutrophil recruitment and activation leading to aortic rupture. Circ. Res. 116, 612-623 (2015).
105. Usui, F. et al. Inflammasome activation by mitochondrial oxidative stress in macrophages leads to the development of angiotensin II-induced aortic aneurysm. Arterioscler. Thromb. Vasc. Biol. 35, 127-136 (2015).
106. Johnston, W. F. et al. Genetic and pharmacologic disruption of interleukin-1beta signaling inhibits experimental aortic aneurysm formation. Arterioscler. Thromb. Vasc. Biol. 33, 294-304 (2013).
107. Xiong, W. et al. Blocking TNF-alpha attenuates aneurysm formation in a murine model. J. Immunol. 183, 2741-2746 (2009).
108. Ju, X. et al. Interleukin-6-signal transducer and activator of transcription-3 signaling mediates aortic dissections induced by angiotensin II via the T-helper lymphocyte 17-interleukin 17 axis in C57BL/6 mice. Arterioscler. Thromb. Vasc. Biol. 33, 1612-1621 (2013).
109. Ait-Oufella, H. et al. Natural regulatory T cells limit angiotensin II-induced aneurysm formation and rupture in mice. Arterioscler. Thromb. Vasc. Biol. 33, 2374-2379 (2013).
110. Vucevic, D. et al. Inverse production of IL-6 and IL-10 by abdominal aortic aneurysm explant tissues in culture. Cardiovasc. Pathol. 21, 482-489 (2012).
111. Date, D. et al. Kruppel-like transcription factor 6 regulates inflammatory macrophage polarization. J. Biol. Chem. 289, 10318-10329 (2014).
112. Son, B. K. et al. Granulocyte macrophage colony-stimulating factor is required for aortic dissection/intramural haematoma. Nat. Commun. 6, 6994 (2015).
113. Tazume, H. et al. Macrophage-derived angiopoietin-like protein 2 accelerates development of abdominal aortic aneurysm. Arterioscler. Thromb. Vasc. Biol. 32, 1400-1409 (2012).
114. Hwang, J. S. et al. PPARdelta reduces abdominal aortic aneurysm formation in angiotensin II-infused apolipoprotein E-deficient mice by regulating extracellular matrix homeostasis and inflammatory responses. Int. J. Cardiol. 174, 43-50 (2014).
115. Oller, J. et al. Nitric oxide mediates aortic disease in mice deficient in the metalloprotease Adamts1 and in a mouse model of Marfan syndrome. Nat. Med. 23, 200-212 (2017).
116. Zhang, J. et al. Inducible nitric oxide synthase is present in human abdominal aortic aneurysm and promotes oxidative vascular injury. J. Vasc. Surg. 38, 360-367 (2003).
117. Lee, J. K., Borhani, M., Ennis, T. L., Upchurch, G. R. Jr & Thompson, R. W. Experimental abdominal aortic aneurysms in mice lacking expression of inducible nitric oxide synthase. Arterioscler. Thromb. Vasc. Biol. 21, 1393-1401 (2001).
118. Johanning, J. M., Franklin, D. P., Han, D. C., Carey, D. J. & Elmore, J. R. Inhibition of inducible nitric oxide synthase limits nitric oxide production and experimental aneurysm expansion. J. Vasc. Surg. 33, 579-586 (2001).
119. Armstrong, P. J., Franklin, D. P., Carey, D. J. & Elmore, J. R. Suppression of experimental aortic aneurysms: comparison of inducible nitric oxide synthase and cyclooxygenase inhibitors. Ann. Vasc. Surg. 19, 248-257 (2005).
120. Kossmann, S. et al. Inflammatory monocytes determine endothelial nitric-oxide synthase uncoupling and nitro-oxidative stress induced by angiotensin II. J. Biol. Chem. 289, 27540-27550 (2014).
121. Rifkind, J. M., Mohanty, J. G. & Nagababu, E. The pathophysiology of extracellular hemoglobin associated with enhanced oxidative reactions. Front. Physiol. 5, 500 (2014).
122. Keaney, J. F. Jr. Oxidative stress and the vascular wall: NADPH oxidases take center stage. Circulation 112, 2585-2588 (2005).
123. Thomas, M. et al. Deletion of p47phox attenuates angiotensin II-induced abdominal aortic aneurysm formation in apolipoprotein E-deficient mice. Circulation 114, 404-413 (2006).
124. Kigawa, Y. et al. NADPH oxidase deficiency exacerbates angiotensin II-induced abdominal aortic aneurysms in mice. Arterioscler. Thromb. Vasc. Biol. 34, 2413-2420 (2014).
125. Sharma, A. K. et al. Mesenchymal stem cells attenuate NADPH oxidase-dependent high mobility group box 1 production and inhibit abdominal aortic aneurysms. Arterioscler. Thromb. Vasc. Biol. 36, 908-918 (2016).
126. Henson, P. M., Bratton, D. L. & Fadok, V. A. Apoptotic cell removal. Curr. Biol. 11, R795-R805 (2001).
127. Kojima, Y. et al. Cyclin-dependent kinase inhibitor 2B regulates efferocytosis and atherosclerosis. J. Clin. Invest. 124, 1083-1097 (2014).
128. Kojima, Y. et al. CD47-blocking antibodies restore phagocytosis and prevent atherosclerosis. Nature 536, 86-90 (2016).
129. Wan, E. et al. Enhanced efferocytosis of apoptotic cardiomyocytes through myeloid-epithelial-reproductive tyrosine kinase links acute inflammation resolution to cardiac repair after infarction. Circ. Res. 113, 1004-1012 (2013).
130. Howangyin, K. Y. et al. Myeloid-epithelial-reproductive receptor tyrosine kinase and milk fat globule epidermal growth factor 8 coordinately improve remodeling after myocardial infarction via local delivery of vascular endothelial growth factor. Circulation 133, 826-839 (2016).
131. He, H. et al. Perivascular macrophages limit permeability. Arterioscler. Thromb. Vasc. Biol. 36, 2203-2212 (2016).
132. Machnik, A. et al. Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-C-dependent buffering mechanism. Nat. Med. 15, 545-552 (2009).
133. Mallat, Z., Tedgui, A. & Henrion, D. Role of microvascular tone and extracellular matrix contraction in the regulation of interstitial fluid: implications for aortic dissection. Arterioscler. Thromb. Vasc. Biol. 36, 1742-1747 (2016).
134. Golestani, R. & Sadeghi, M. M. Emergence of molecular imaging of aortic aneurysm: implications for risk stratification and management. J. Nucl. Cardiol. 21, 251-267 (2014).
135. Jalalzadeh, H. et al. Inflammation as a predictor of abdominal aortic aneurysm growth and rupture: a systematic review of imaging biomarkers. Eur. J. Vasc. Endovasc. Surg. 52, 333-342 (2016).
136. Huang, Y. et al. High structural stress and presence of intraluminal thrombus predict abdominal aortic aneurysm 18F-FDG uptake: insights from biomechanics. Circ. Cardiovasc. Imaging 9, e004656 (2016).
137. Richards, J. M. et al. Abdominal aortic aneurysm growth predicted by uptake of ultrasmall superparamagnetic particles of iron oxide: a pilot study. Circ. Cardiovasc. Imaging 4, 274-281 (2011).
138. McBride, O. M. et al. Positron emission tomography and magnetic resonance imaging of cellular inflammation in patients with abdominal aortic aneurysms. Eur. J. Vasc. Endovasc. Surg. 51, 518-526 (2016).
139. Rinne, P. et al. Comparison of somatostatin receptor 2-targeting PET tracers in the detection of mouse atherosclerotic plaques. Mol. Imaging Biol. 18, 99-108 (2016).
140. Li, X. et al. 68Ga-DOTATATE PET/CT for the detection of inflammation of large arteries: correlation with18F-FDG, calcium burden and risk factors. EJNMMI Res. 2, 52 (2012).
141. Pedersen, S. F. et al. 64Cu-DOTATATE PET/MRI for detection of activated macrophages in carotid atherosclerotic plaques: studies in patients undergoing endarterectomy. Arterioscler. Thromb. Vasc. Biol. 35, 1696-1703 (2015).
142. Keliher, E. J. et al. Polyglucose nanoparticles with renal elimination and macrophage avidity facilitate PET imaging in ischaemic heart disease. Nat. Commun. 8, 14064 (2017).
143. de Waard, V. et al. Systemic MCP1/CCR2 blockade and leukocyte specific MCP1/CCR2 inhibition affect aortic aneurysm formation differently. Atherosclerosis 211, 84-89 (2010).
144. Leuschner, F. et al. Therapeutic siRNA silencing in inflammatory monocytes in mice. Nat. Biotechnol. 29, 1005-1010 (2011).
145. Leuschner, F. et al. Silencing of CCR2 in myocarditis. Eur. Heart J. 36, 1478-1488 (2015).
146. US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT01736813 (2017).
147. US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT02134717 (2016)
148. Bonvin, P., Power, C. A. & Proudfoot, A. E. Evasins: therapeutic potential of a new family of chemokine-binding proteins from ticks. Front. Immunol. 7, 208 (2016).
149. Hennigan, S. & Kavanaugh, A. Interleukin-6 inhibitors in the treatment of rheumatoid arthritis. Ther. Clin. Risk Manag. 4, 767-775 (2008).
150. Harrison, S. C. et al. Interleukin-6 receptor pathways in abdominal aortic aneurysm. Eur. Heart J. 34, 3707-3716 (2013).
151. Interleukin-6 Receptor Mendelian Randomisation Analysis (IL6R MR) Consortium et al. The interleukin-6 receptor as a target for prevention of coronary heart disease: a Mendelian randomisation analysis. Lancet 379, 1214-1224 (2012).
152. IL6R Genetics Consortium Emerging Risk Factors Collaboration et al. Interleukin-6 receptor pathways in coronary heart disease: a collaborative meta-analysis of 82 studies. Lancet 379, 1205-1213 (2012).
153. US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT02007252 (2016).
154. Interleukin 1 Genetics Consortium. Cardiometabolic effects of genetic upregulation of the interleukin 1 receptor antagonist: a Mendelian randomisation analysis. Lancet Diabetes Endocrinol. 3, 243-253 (2015).
155. Tsuruda, T. et al. Inhibition of development of abdominal aortic aneurysm by glycolysis restriction. Arterioscler. Thromb. Vasc. Biol. 32, 1410-1417 (2012).
156. Pope, N. H. et al. D-series resolvins inhibit murine abdominal aortic aneurysm formation and increase M2 macrophage polarization. FASEB J. 30, 4192-4201 (2016).
157. Yodoi, K. et al. Foxp3+ regulatory T cells play a protective role in angiotensin II-induced aortic aneurysm formation in mice. Hypertension 65, 889-895 (2015).
158. Zhou, Y. et al. Regulatory T cells in human and angiotensin II-induced mouse abdominal aortic aneurysms. Cardiovasc. Res. 107, 98-107 (2015).
159. Meng, X. et al. Regulatory T cells prevent angiotensin II-induced abdominal aortic aneurysm in apolipoprotein E knockout mice. Hypertension 64, 875-882 (2014).
160. Alvarez, M. M. et al. Delivery strategies to control inflammatory response: modulating M1-M2 polarization in tissue engineering applications. J. Control. Release 240, 349-363 (2016).
161. Fulop, T. et al. From inflamm-aging to immune-paralysis: a slippery slope during aging for immune-adaptation. Biogerontology 17, 147-157 (2016).
162. Campesi, I., Marino, M., Montella, A., Pais, S. & Franconi, F. Sex differences in estrogen receptor alpha and beta levels and activation status in LPS-stimulated human macrophages. J. Cell. Physiol. 232, 340-345 (2017).
163. Bhatia, A., Sekhon, H. K. & Kaur, G. Sex hormones and immune dimorphism. ScientificWorldJournal 2014, 159150 (2014).
164. Qiu, F. et al. Impacts of cigarette smoking on immune responsiveness: up and down or upside down? Oncotarget 8, 268-284 (2017).
165. Wright, M. D. & Binger, K. J. Macrophage heterogeneity and renin-angiotensin system disorders. Pflugers Arch. 469, 445-454 (2017).
166. Sarov-Blat, L. et al. Predominance of a proinflammatory phenotype in monocyte-derived macrophages from subjects with low plasma HDL-cholesterol. Arterioscler. Thromb. Vasc. Biol. 27, 1115-1122 (2007).
167. Senemaud, J. et al. Translational relevance and recent advances of animal models of abdominal aortic aneurysm. Arterioscler. Thromb. Vasc. Biol. 37, 401-410 (2017).
168. Jacomelli, J., Summers, L., Stevenson, A., Lees, T. & Earnshaw, J. J. Impact of the first 5 years of a national abdominal aortic aneurysm screening programme. Br. J. Surg. 103, 1125-1131 (2016).
169. Moll, F. L. et al. Management of abdominal aortic aneurysms clinical practice guidelines of the European society for vascular surgery. Eur. J. Vasc. Endovasc. Surg. 41 (Suppl. 1), S1-S58 (2011).
170. Brady, A. R. et al. Abdominal aortic aneurysm expansion: risk factors and time intervals for surveillance. Circulation 110, 16-21 (2004).
171. Sweeting, M. J., Thompson, S. G., Brown, L. C., Powell, J. T. & RESCAN collaborators. Meta-analysis of individual patient data to examine factors affecting growth and rupture of small abdominal aortic aneurysms. Br. J. Surg. 99, 655-665 (2012).
172. Helgadottir, A. et al. The same sequence variant on 9p21 associates with myocardial infarction, abdominal aortic aneurysm and intracranial aneurysm. Nat. Genet. 40, 217-224 (2008).
173. Gretarsdottir, S. et al. Genome-wide association study identifies a sequence variant within the DAB2IP gene conferring susceptibility to abdominal aortic aneurysm. Nat. Genet. 42, 692-697 (2010).
174. Bown, M. J. et al. Abdominal aortic aneurysm is associated with a variant in low-density lipoprotein receptor-related protein 1. Am. J. Hum. Genet. 89, 619-627 (2011).
175. Jones, G. T. et al. Meta-analysis of genome-wide association studies for abdominal aortic aneurysm identifies four new disease-specific risk loci. Circ. Res. 120, 341-353 (2017).
176. Patel, R., Sweeting, M. J., Powell, J. T., Greenhalgh, R. M. & EVAR trial investigators. Endovascular versus open repair of abdominal aortic aneurysm in 15-years'' follow-up of the UK endovascular aneurysm repair trial 1 (EVAR trial 1): a randomised controlled trial. Lancet 388, 2366-2374 (2016).
177. Azuma, J., Asagami, T., Dalman, R. & Tsao, P. S. Creation of murine experimental abdominal aortic aneurysms with elastase. J. Vis. Exp. http://dx.doi.org/10.3791/1280 (2009).
178. Wang, Y., Krishna, S. & Golledge, J. The calcium chloride-induced rodent model of abdominal aortic aneurysm. Atherosclerosis 226, 29-39 (2013).
179. Kurihara, T. et al. Neutrophil-derived matrix metalloproteinase 9 triggers acute aortic dissection. Circulation 126, 3070-3080 (2012).
180. Liu, S. et al. Mineralocorticoid receptor agonists induce mouse aortic aneurysm formation and rupture in the presence of high salt. Arterioscler. Thromb. Vasc. Biol. 33, 1568-1579 (2013).
181. Daugherty, A. & Cassis, L. Angiotensin II and abdominal aortic aneurysms. Curr. Hypertens. Rep. 6, 442-446 (2004).
182. Trachet, B. et al. Ascending aortic aneurysm in angiotensin II-infused mice: formation, progression, and the role of focal dissections. Arterioscler. Thromb. Vasc. Biol. 36, 673-681 (2016).