High-resolution imaging of intravascular atherogenic inflammation in live mice

Circulation Research

Volumn 114, Issue 5, 2014, Pages 770-779

  Chèvre, Raphael ^a   González Granado, Jose María ^a   Megens, Remco T A ^b,c,d   Sreeramkumar, Vinatha ^a   Silvestre Roig, Carlos ^a   Molina Sánchez, Pedro ^a   Weber, Christian ^b,c,d   Soehnlein, Oliver ^b,c,e   Hidalgo, Andrés ^a   Andrés, Vicente ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^d MAASTRICHT UNIVERSITY   (Netherlands)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Atherosclerosis; blood platelets; carotid arteries; neutrophils

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CAROTID ARTERY; CAROTID ARTERY BIFURCATION; COMMON CAROTID ARTERY; CONTROLLED STUDY; DISEASE COURSE; FLUORESCENCE; IN VIVO STUDY; LASER MICROSCOPY; LEUKOCYTE; LEUKOCYTE ROLLING; LIPID DIET; MALE; MICROCIRCULATION; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; T LYMPHOCYTE; THROMBOCYTE; THROMBOCYTE ACTIVATION; TWO PHOTON LASER SCANNING MICROSCOPY;

ATHEROSCLEROSIS; BLOOD PLATELETS; CAROTID ARTERIES; NEUTROPHILS;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BLOOD PLATELETS; CAROTID ARTERY DISEASES; CAROTID ARTERY, COMMON; FEMALE; GREEN FLUORESCENT PROTEINS; LEUKOCYTE ROLLING; LEUKOCYTES; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; MYELOID CELLS; NEUTROPHILS; REGIONAL BLOOD FLOW; VASCULITIS;

EID: 84896774884     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.114.302590     Document Type: Article

References (40)

1. Roger VL, Go AS, Lloyd-Jones DM, et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2011 update: A report from the American Heart Association. Circulation. 2011;123:e18-e209.
2. Binder CJ, Chang MK, Shaw PX, Miller YI, Hartvigsen K, Dewan A, Witztum JL. Innate and acquired immunity in atherogenesis. Nat Med. 2002;8:1218-1226.
3. Huo Y, Ley KF. Role of platelets in the development of atherosclerosis. Trends Cardiovasc Med. 2004;14:18-22.
4. Galkina E, Ley K. Leukocyte influx in atherosclerosis. Curr Drug Targets. 2007;8:1239-1248.
5. Weber C, Noels H. Atherosclerosis: Current pathogenesis and therapeutic options. Nat Med. 2011;17:1410-1422.
6. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature. 2011;473:317-325.
7. Dring Y, Drechsler M, Wantha S, Kemmerich K, Lievens D, Vijayan S, Gallo RL, Weber C, Soehnlein O. Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ Res. 2012;110:1052-1056.
8. Huo Y, Schober A, Forlow SB, Smith DF, Hyman MC, Jung S, Littman DR, Weber C, Ley K. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med. 2003;9:61-67.
9. Megens RT, Vijayan S, Lievens D, Dring Y, Van Zandvoort MA, Grommes J, Weber C, Soehnlein O. Presence of luminal neutrophil extracellular traps in atherosclerosis. Thromb Haemost. 2012;107:597-598.
10. Zernecke A, Bot I, Djalali-Talab Y, Shagdarsuren E, Bidzhekov K, Meiler S, Krohn R, Schober A, Sperandio M, Soehnlein O, Bornemann J, Tacke F, Biessen EA, Weber C. Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis. Circ Res. 2008;102:209-217.
11. Ramos CL, Huo Y, Jung U, Ghosh S, Manka DR, Sarembock IJ, Ley K. Direct demonstration of P-selectin-and VCAM-1-dependent mononuclear cell rolling in early atherosclerotic lesions of apolipoprotein E-deficient mice. Circ Res. 1999;84:1237-1244.
12. Koltsova EK, Garcia Z, Chodaczek G, Landau M, McArdle S, Scott SR, von Vietinghoff S, Galkina E, Miller YI, Acton ST, Ley K. Dynamic T cell-APC interactions sustain chronic inflammation in atherosclerosis. J Clin Invest. 2012;122:3114-3126.
13. Drechsler M, Megens RT, Van Zandvoort M, Weber C, Soehnlein O. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation. 2010;122:1837-1845.
14. Eriksson EE, Xie X, Werr J, Thoren P, Lindbom L. Direct viewing of atherosclerosis in vivo: Plaque invasion by leukocytes is initiated by the endothelial selectins. FASEB J. 2001;15:1149-1157.
15. Megens RT, Kemmerich K, Pyta J, Weber C, Soehnlein O. Intravital imaging of phagocyte recruitment. Thromb Haemost. 2011;105:802-810.
16. Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13:463-469.
17. Hidalgo A, Chang J, Jang JE, Peired AJ, Chiang EY, Frenette PS. Heterotypic interactions enabled by polarized neutrophil microdomains mediate thromboinflammatory injury. Nat Med. 2009;15:384-391.
18. Burnett SH, Kershen EJ, Zhang J, Zeng L, Straley SC, Kaplan AM, Cohen DA. Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene. J Leukoc Biol. 2004;75:612-623.
19. Rotzius P, Soehnlein O, Kenne E, Lindbom L, Nystrom K, Thams S, Eriksson EE. ApoE(-/-)/lysozyme M(EGFP/EGFP) mice as a versatile model to study monocyte and neutrophil trafficking in atherosclerosis. Atherosclerosis. 2009;202:111-118.
20. Chiang EY, Hidalgo A, Chang J, Frenette PS. Imaging receptor microdomains on leukocyte subsets in live mice. Nat Methods. 2007;4:219-222.
21. Parzy E, Miraux S, Franconi JM, Thiaudire E. In vivo quantification of blood velocity in mouse carotid and pulmonary arteries by ECG-triggered 3D time-resolved magnetic resonance angiography. NMR Biomed. 2009;22:532-537.
22. Eriksson EE. Intravital microscopy on atherosclerosis in apolipoprotein e-deficient mice establishes microvessels as major entry pathways for leukocytes to advanced lesions. Circulation. 2011;124:2129-2138.
23. Yipp BG, Kubes P. Antibodies against neutrophil LY6G do not inhibit leukocyte recruitment in mice in vivo. Blood. 2013;121:241-242.
24. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7:678-689.
25. Barreiro O, De La Fuente H, Mittelbrunn M, Snchez-Madrid F. Functional insights on the polarized redistribution of leukocyte integrins and their ligands during leukocyte migration and immune interactions. Immunol Rev. 2007;218:147-164.
26. Phillipson M, Heit B, Colarusso P, Liu L, Ballantyne CM, Kubes P. Intraluminal crawling of neutrophils to emigration sites: A molecularly distinct process from adhesion in the recruitment cascade. J Exp Med. 2006;203:2569-2575.
27. Lievens D, von Hundelshausen P. Platelets in atherosclerosis. Thromb Haemost. 2011;106:827-838.
28. Koenen RR, von Hundelshausen P, Nesmelova IV, Zernecke A, Liehn EA, Sarabi A, Kramp BK, Piccinini AM, Paludan SR, Kowalska MA, Kungl AJ, Hackeng TM, Mayo KH, Weber C. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med. 2009;15:97-103.
29. Bergmeier W, Schulte V, Brockhoff G, Bier U, Zirngibl H, Nieswandt B. Flow cytometric detection of activated mouse integrin alphaIIbbeta3 with a novel monoclonal antibody. Cytometry. 2002;48:80-86.
30. Megens RT, Reitsma S, Prinzen L, oude Egbrink MG, Engels W, Leenders PJ, Brunenberg EJ, Reesink KD, Janssen BJ, ter Haar Romeny BM, Slaaf DW, Van Zandvoort MA. In vivo high-resolution structural imaging of large arteries in small rodents using two-photon laser scanning microscopy. J Biomed Opt. 2010;15:011108.
31. 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.
32. Esplugues E, Huber S, Gagliani N, et al. Control of TH17 cells occurs in the small intestine. Nature. 2011;475:514-518.
33. Faust N, Varas F, Kelly LM, Heck S, Graf T. Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood. 2000;96:719-726.
34. Zhang J, Varas F, Stadtfeld M, Heck S, Faust N, Graf T. CD41-YFP mice allow in vivo labeling of megakaryocytic cells and reveal a subset of platelets hyperreactive to thrombin stimulation. Exp Hematol. 2007;35:490-499.
35. Yu W, Braz JC, Dutton AM, Prusakov P, Rekhter M. In vivo imaging of atherosclerotic plaques in apolipoprotein E deficient mice using nonlinear microscopy. J Biomed Opt. 2007;12:054008.
36. Janssen BJ, De Celle T, Debets JJ, Brouns AE, Callahan MF, Smith TL. Effects of anesthetics on systemic hemodynamics in mice. Am J Physiol Heart Circ Physiol. 2004;287:H1618-H1624.
37. 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.
38. Soehnlein O. Multiple roles for neutrophils in atherosclerosis. Circ Res. 2012;110:875-888.
39. Myers DD, Hawley AE, Farris DM, Wrobleski SK, Thanaporn P, Schaub RG, Wagner DD, Kumar A, Wakefield TW. P-selectin and leukocyte microparticles are associated with venous thrombogenesis. J Vasc Surg. 2003;38:1075-1089.
40. Falati S, Gross P, Merrill-Skoloff G, Furie BC, Furie B. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat Med. 2002;8:1175-1181.