Angiotensin II mobilizes spleen monocytes to promote the development of abdominal aortic aneurysm in Apoe-/- mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 2, 2015, Pages 378-388

  Mellak, Safa ^a   Ait Oufella, Hafid ^a,b   Esposito, Bruno ^a   Loyer, Xavier ^a   Poirier, Maxime ^a   Tedder, Thomas F ^c   Tedgui, Alain ^a   Mallat, Ziad ^a,d   Potteaux, Stéphane ^a  

^a PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

aneurysm; B lymphocytes; metabolism; monocytes; splenectomy

Indexed keywords

ANGIOTENSIN II; LYMPHOCYTE ANTIGEN; APOLIPOPROTEIN E; DNA BINDING PROTEIN; LY ANTIGEN; LY6 PROTEIN, MOUSE; RAG2 PROTEIN, MOUSE;

ABDOMINAL AORTA; ABDOMINAL AORTA ANEURYSM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BLOOD PRESSURE; BONE MARROW TRANSPLANTATION; CELL MOTILITY; CONTROLLED STUDY; DISEASE PREDISPOSITION; FLOW CYTOMETRY; HYPERCHOLESTEROLEMIA; MACROPHAGE; MALE; MONITORING; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; SPLENECTOMY; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; CHEMICALLY INDUCED; COMPLICATION; DEFICIENCY; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SPLEEN; TIME;

ANGIOTENSIN II; ANIMALS; ANTIGENS, LY; AORTIC ANEURYSM, ABDOMINAL; APOLIPOPROTEINS E; B-LYMPHOCYTES; BONE MARROW TRANSPLANTATION; CELL MOVEMENT; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; HYPERCHOLESTEROLEMIA; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; SPLEEN; SPLENECTOMY; TIME FACTORS;

EID: 84922056299     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304389     Document Type: Article

References (56)

1. Freestone T, Turner RJ, Coady A, Higman DJ, Greenhalgh RM, Powell JT. Inflammation and matrix metalloproteinases in the enlarging abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol. 1995;15:1145-1151.
2. Nordon IM, Hinchliffe RJ, Loftus IM, Thompson MM. Pathophysiology and epidemiology of abdominal aortic aneurysms. Nat Rev Cardiol. 2011;8:92-102. doi: 10.1038/nrcardio.2010.180.
3. Golledge J, Muller J, Daugherty A, Norman P. Abdominal aortic aneurysm: pathogenesis and implications for management. Arterioscler Thromb Vasc Biol. 2006;26:2605-2613. doi: 10.1161/01. ATV.0000245819.32762.cb.
4. Hellenthal FA, Buurman WA, Wodzig WK, Schurink GW. Biomarkers of abdominal aortic aneurysm progression. Part 2: inflammation. Nat Rev Cardiol. 2009;6:543-552. doi: 10.1038/nrcardio.2009.102.
5. del Porto F, Proietta M, Tritapepe L, Miraldi F, Koverech A, Cardelli P, Tabacco F, de Santis V, Vecchione A, Mitterhofer AP, Nofroni I, Amodeo R, Trappolini M, Aliberti G. Inflammation and immune response in acute aortic dissection. Ann Med. 2010;42:622-629. doi: 10.3109/07853890.2010.518156.
6. Longo GM, Xiong W, Greiner TC, Zhao Y, Fiotti N, Baxter BT. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest. 2002;110:625-632. doi: 10.1172/JCI15334.
7. Pyo R, Lee JK, Shipley JM, Curci JA, Mao D, Ziporin SJ, Ennis TL, Shapiro SD, Senior RM, Thompson RW. Targeted gene disruption of matrix metalloproteinase-9 (gelatinase B) suppresses development of experimental abdominal aortic aneurysms. J Clin Invest. 2000;105:1641-1649. doi: 10.1172/JCI8931.
8. Tieu BC, Lee C, Sun H, Lejeune W, Recinos A III, Ju X, Spratt H, Guo DC, Milewicz D, Tilton RG, Brasier AR. An adventitial IL-6/MCP1 amplification loop accelerates macrophage-mediated vascular inflammation leading to aortic dissection in mice. J Clin Invest. 2009;119:3637-3651. doi: 10.1172/JCI38308.
9. Ishibashi M, Egashira K, Zhao Q, Hiasa K, Ohtani K, Ihara Y, Charo IF, Kura S, Tsuzuki T, Takeshita A, Sunagawa K. 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. 2004;24:e174-e178. doi: 10.1161/01.ATV.0000143384.69170.2d.
10. de Waard V, Bot I, de Jager SC, Talib S, Egashira K, de Vries MR, Quax PH, Biessen EA, van Berkel TJ. Systemic MCP1/CCR2 blockade and leukocyte specific MCP1/CCR2 inhibition affect aortic aneurysm formation differently. Atherosclerosis. 2010;211:84-89. doi: 10.1016/j. atherosclerosis.2010.01.042.
11. Moran CS, Jose RJ, Moxon JV, Roomberg A, Norman PE, Rush C, Körner H, Golledge J. Everolimus limits aortic aneurysm in the apolipoprotein E-deficient mouse by downregulating C-C chemokine receptor 2 positive monocytes. Arterioscler Thromb Vasc Biol. 2013;33:814-821. doi: 10.1161/ATVBAHA.112.301006.
12. Wang Y, Ait-Oufella H, Herbin O, Bonnin P, Ramkhelawon B, Taleb S, Huang J, Offenstadt G, Combadière C, Rénia L, Johnson JL, Tharaux PL, Tedgui A, Mallat Z. TGF-beta activity protects against inflammatory aortic aneurysm progression and complications in angiotensin II-infused mice. J Clin Invest. 2010;120:422-432. doi: 10.1172/JCI38136.
13. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 2003;19:71-82.
14. Ingersoll MA, Spanbroek R, Lottaz C, Gautier EL, Frankenberger M, Hoffmann R, Lang R, Haniffa M, Collin M, Tacke F, Habenicht AJ, Ziegler-Heitbrock L, Randolph GJ. Comparison of gene expression profiles between human and mouse monocyte subsets. Blood. 2010;115:e10-e19. doi: 10.1182/blood-2009-07-235028.
15. Grainger JR, Wohlfert EA, Fuss IJ, Bouladoux N, Askenase MH, Legrand F, Koo LY, Brenchley JM, Fraser ID, Belkaid Y. Inflammatory monocytes regulate pathologic responses to commensals during acute gastrointestinal infection. Nat Med. 2013;19:713-721. doi: 10.1038/nm.3189.
16. Peranzoni E, Zilio S, Marigo I, Dolcetti L, Zanovello P, Mandruzzato S, Bronte V. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol. 2010;22:238-244. doi: 10.1016/j. coi.2010.01.021.
17. Woollard KJ, Geissmann F. Monocytes in atherosclerosis: subsets and functions. Nat Rev Cardiol. 2010;7:77-86. doi: 10.1038/nrcardio.2009.228.
18. Boring L, Gosling J, Chensue SW, Kunkel SL, Farese RV Jr, Broxmeyer HE, Charo IF. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J Clin Invest. 1997;100:2552-2561. doi: 10.1172/JCI119798.
19. Serbina NV, Jia T, Hohl TM, Pamer EG. Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol. 2008;26:421-452. doi: 10.1146/annurev.immunol.26.021607.090326.
20. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, Sarnacki S, Cumano A, Lauvau G, Geissmann F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science. 2007;317:666-670. doi: 10.1126/science.1142883.
21. Shi C, Jia T, Mendez-Ferrer S, Hohl TM, Serbina NV, Lipuma L, Leiner I, Li MO, Frenette PS, Pamer EG. Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating toll-like receptor ligands. Immunity. 2011;34:590-601. doi: 10.1016/j. immuni.2011.02.016.
22. Landsman L, Varol C, Jung S. Distinct differentiation potential of blood monocyte subsets in the lung. J Immunol. 2007;178:2000-2007.
23. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007;204:3037-3047. doi: 10.1084/jem.20070885.
24. Shechter R, London A, Varol C, Raposo C, Cusimano M, Yovel G, Rolls A, Mack M, Pluchino S, Martino G, Jung S, Schwartz M. Infiltrating bloodderived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med. 2009;6:e1000113. doi: 10.1371/journal.pmed.1000113.
25. Hilgendorf I, Gerhardt LM, Tan TC, Winter C, Holderried TA, Chousterman BG, Iwamoto Y, Liao R, Zirlik A, Scherer-Crosbie M, Hedrick CC, Libby P, Nahrendorf M, Weissleder R, Swirski FK. Ly-6Chigh monocytes depend on Nr4a1 to balance both inflammatory and reparative phases in the infarcted myocardium. Circ Res. 2014;114:1611-1622. doi: 10.1161/ CIRCRESAHA.114.303204.
26. 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. doi: 10.1172/JCI28549.
27. Combadière C, Potteaux S, Rodero M, Simon T, Pezard A, Esposito B, Merval R, Proudfoot A, Tedgui A, Mallat Z. Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6C(hi) and Ly6C(lo) monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation. 2008;117:1649-1657. doi: 10.1161/ CIRCULATIONAHA.107.745091.
28. Soehnlein O, Drechsler M, Döring Y, et al. Distinct functions of chemokine receptor axes in the atherogenic mobilization and recruitment of classical monocytes. EMBO Mol Med. 2013;5:471-481. doi: 10.1002/ emmm.201201717.
29. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest. 2007;117:195-205. doi: 10.1172/JCI29950.
30. Potteaux S, Gautier EL, Hutchison SB, van Rooijen N, Rader DJ, Thomas MJ, Sorci-Thomas MG, Randolph GJ. Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe-/-mice during disease regression. J Clin Invest. 2011;121:2025-2036. doi: 10.1172/JCI43802.
31. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009;325:612-616. doi: 10.1126/science.1175202.
32. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000;105:1605-1612. doi: 10.1172/JCI7818.
33. Cassis LA, Gupte M, Thayer S, Zhang X, Charnigo R, Howatt DA, Rateri DL, Daugherty A. ANG II infusion promotes abdominal aortic aneurysms independent of increased blood pressure in hypercholesterolemic mice. Am J Physiol Heart Circ Physiol. 2009;296:H1660-H1665. doi: 10.1152/ ajpheart.00028.2009.
34. Sampson UK, Perati PR, Prins PA, Pham W, Liu Z, Harrell FE Jr, Linton MF, Gore JC, Kon V, Fazio S. Quantitative estimates of the variability of in vivo sonographic measurements of the mouse aorta for studies of abdominal aortic aneurysms and related arterial diseases. J Ultrasound Med. 2011;30:773-784.
35. Palframan RT, Jung S, Cheng G, Weninger W, Luo Y, Dorf M, Littman DR, Rollins BJ, Zweerink H, Rot A, von Andrian UH. Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J Exp Med. 2001;194:1361-1373.
36. Van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods. 1994;174:83-93.
37. Kragballe K, Nielsen JL, Sølling J, Ellegaard J. Monocyte cytotoxicity after splenectomy. Scand J Haematol. 1981;27:271-278.
38. Nahrendorf M, Keliher E, Marinelli B, Leuschner F, Robbins CS, Gerszten RE, Pittet MJ, Swirski FK, Weissleder R. Detection of macrophages in aortic aneurysms by nanoparticle positron emission tomography-computed tomography. Arterioscler Thromb Vasc Biol. 2011;31:750-757. doi: 10.1161/ATVBAHA.110.221499.
39. Zouggari Y, Ait-Oufella H, Bonnin P, et al. B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat Med. 2013;19:1273-1280. doi: 10.1038/nm.3284.
40. Bourgeois C, Stockinger B. CD25+CD4+ regulatory T cells and memory T cells prevent lymphopenia-induced proliferation of naive T cells in transient states of lymphopenia. J Immunol. 2006;177:4558-4566.
41. Uchida J, Lee Y, Hasegawa M, Liang Y, Bradney A, Oliver JA, Bowen K, Steeber DA, Haas KM, Poe JC, Tedder TF. Mouse CD20 expression and function. Int Immunol. 2004;16:119-129.
42. Ait-Oufella H, Herbin O, Bouaziz JD, Binder CJ, Uyttenhove C, Laurans L, Taleb S, Van Vré E, Esposito B, Vilar J, Sirvent J, Van Snick J, Tedgui A, Tedder TF, Mallat Z. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med. 2010;207:1579-1587. doi: 10.1084/ jem.20100155.
43. Gautier EL, Jakubzick C, Randolph GJ. Regulation of the migration and survival of monocyte subsets by chemokine receptors and its relevance to atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29:1412-1418. doi: 10.1161/ATVBAHA.108.180505.
44. Olivares R, Ducimetière P, Claude JR. Monocyte count: a risk factor for coronary heart disease? Am J Epidemiol. 1993;137:49-53.
45. Weber C, Zernecke A, Libby P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Immunol. 2008;8:802-815. doi: 10.1038/nri2415.
46. Nasir K, Guallar E, Navas-Acien A, Criqui MH, Lima JA. Relationship of monocyte count and peripheral arterial disease: results from the National Health and Nutrition Examination Survey 1999-2002. Arterioscler Thromb Vasc Biol. 2005;25:1966-1971. doi: 10.1161/01. ATV.0000175296.02550.e4.
47. Kintscher U, Wakino S, Kim S, Fleck E, Hsueh WA, Law RE. Angiotensin II induces migration and Pyk2/paxillin phosphorylation of human monocytes. Hypertension. 2001;37(2 Pt 2):587-593.
48. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. 2002;8:403-409. doi: 10.1038/nm0402-403.
49. Psaltis PJ, Harbuzariu A, Delacroix S, Witt TA, Holroyd EW, Spoon DB, Hoffman SJ, Pan S, Kleppe LS, Mueske CS, Gulati R, Sandhu GS, Simari RD. Identification of a monocyte-predisposed hierarchy of hematopoietic progenitor cells in the adventitia of postnatal murine aorta. Circulation. 2012;125:592-603. doi: 10.1161/CIRCULATIONAHA.111.059360.
50. Sunderkötter C, Nikolic T, Dillon MJ, Van Rooijen N, Stehling M, Drevets DA, Leenen PJ. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol. 2004;172:4410-4417.
51. Varol C, Landsman L, Fogg DK, Greenshtein L, Gildor B, Margalit R, Kalchenko V, Geissmann F, Jung S. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med. 2007;204:171-180. doi: 10.1084/jem.20061011.
52. 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. doi: 10.1084/jem.20052119.
53. Geissmann F, Auffray C, Palframan R, Wirrig C, Ciocca A, Campisi L, Narni-Mancinelli E, Lauvau G. Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol Cell Biol. 2008;86:398-408. doi: 10.1038/icb.2008.19.
54. Epelman S, Lavine KJ, Beaudin AE, et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity. 2014;40:91-104. doi: 10.1016/j.immuni.2013.11.019.
55. Chapman CM, Beilby JP, McQuillan BM, Thompson PL, Hung J. Monocyte count, but not C-reactive protein or interleukin-6, is an independent risk marker for subclinical carotid atherosclerosis. Stroke. 2004;35:1619-1624. doi: 10.1161/01.STR.0000130857.19423.ad.
56. Drevets DA, Dillon MJ, Schawang JS, Van Rooijen N, Ehrchen J, Sunderkötter C, Leenen PJ. The Ly-6Chigh monocyte subpopulation transports Listeria monocytogenes into the brain during systemic infection of mice. J Immunol. 2004;172:4418-4424.