Dual-contrast molecular imaging allows noninvasive characterization of myocardial ischemia/reperfusion injury after coronary vessel occlusion in mice by magnetic resonance imaging

Circulation

Volumn 130, Issue 8, 2014, Pages 676-687

  Von Elverfeldt, Dominik ^a   Maier, Alexander ^b   Duerschmied, Daniel ^b   Braig, Moritz ^a   Witsch, Thilo ^b   Wang, Xiaowei ^c   Mauler, Maximilian ^b,d   Neudorfer, Irene ^b   Menza, Marius ^a   Idzko, Marco ^a   Zirlik, Andreas ^b   Heidt, Timo ^b,e   Bronsert, Peter ^a   Bode, Christoph ^b   Peter, Karlheinz ^c   Von Zur Muhlen, Constantin ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY HEART CENTER FREIBURG BAD KROZINGEN   (Germany)

^c BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^d UNIVERSITY OF FREIBURG   (Germany)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

blood platelets; magnetic resonance imaging; reperfusion; thrombosis

Indexed keywords

CONTRAST MEDIUM; FIBRINOGEN RECEPTOR; GADOBENATE DIMEGLUMINE; LIGAND; MICROPARTICLE OF IRON OXIDE; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; UNCLASSIFIED DRUG; FERRIC ION; FERRIC OXIDE; GADOLINIUM; MONOCLONAL ANTIBODY; P2RY12 PROTEIN, MOUSE; PURINERGIC P2Y12 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BLOOD VESSEL OCCLUSION; CONTRAST ENHANCEMENT; CONTROLLED STUDY; CORONARY ARTERY LIGATION; CORONARY BLOOD VESSEL; DRUG UPTAKE; HEART MUSCLE ISCHEMIA; HEART MUSCLE NECROSIS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LEFT ANTERIOR DESCENDING CORONARY ARTERY; LIGAND INDUCED BINDING SITE; MOLECULAR IMAGING; MOUSE; NEUTROPHIL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; REPERFUSION INJURY; RETROSPECTIVE STUDY; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; ANIMAL; C57BL MOUSE; CARDIAC IMAGING; CORONARY ARTERY OCCLUSION; CORONARY ARTERY THROMBOSIS; DIAGNOSTIC USE; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM; NECROSIS; PATHOLOGY; PROCEDURES;

ANIMALS; ANTIBODIES, MONOCLONAL; BLOOD PLATELETS; CARDIAC IMAGING TECHNIQUES; CONTRAST MEDIA; CORONARY OCCLUSION; CORONARY THROMBOSIS; DISEASE MODELS, ANIMAL; FERRIC COMPOUNDS; GADOLINIUM; MAGNETIC RESONANCE IMAGING; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR IMAGING; MYOCARDIAL REPERFUSION INJURY; NECROSIS; NEUTROPHILS; PLATELET ACTIVATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; RECEPTORS, PURINERGIC P2Y12;

EID: 85027939977     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.008157     Document Type: Article

References (47)

1. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007;357:1121-1135.
2. Köhler D, Straub A, Weissmüller T, Faigle M, Bender S, Lehmann R, Wendel HP, Kurz J, Walter U, Zacharowski K, Rosenberger P. Phosphorylation of vasodilator-stimulated phosphoprotein prevents platelet-neutrophil complex formation and dampens myocardial ischemiareperfusion injury. Circulation. 2011;123:2579-2590.
3. Prasad A, Stone GW, Holmes DR, Gersh B. Reperfusion injury, microvascular dysfunction, and cardioprotection: the "dark side" of reperfusion. Circulation. 2009;120:2105-2112.
4. Wallentin L, Becker RC, Budaj A, Cannon CP, Emanuelsson H, Held C, Horrow J, Husted S, James S, Katus H, Mahaffey KW, Scirica BM, Skene A, Steg PG, Storey RF, Harrington RA, Freij A, Thorsén M; PLATO Investigators. Ticagrelor versus clopidogrel in patients with acute coronary syndromes. N Engl J Med. 2009;361:1045-1057.
5. Montalescot G, Wiviott SD, Braunwald E, Murphy SA, Gibson CM, McCabe CH, Antman EM; TRITON-TIMI 38 Investigators. Prasugrel compared with clopidogrel in patients undergoing percutaneous coronary intervention for ST-elevation myocardial infarction (TRITON-TIMI 38): double-blind, randomised controlled trial. Lancet. 2009;373:723-731.
6. Liu Y, Gao XM, Fang L, Jennings NL, Su Y, Q X, Samson AL, Kiriazis H, Wang XF, Shan L, Sturgeon SA, Medcalf RL, Jackson SP, Dart AM, Du XJ. Novel role of platelets in mediating inflammatory responses and ventricular rupture or remodeling following myocardial infarction. Arterioscler Thromb Vasc Biol. 2011;31:834-841.
7. Bekkers SC, Yazdani SK, Virmani R, Waltenberger J. Microvascular obstruction: underlying pathophysiology and clinical diagnosis. J Am Coll Cardiol. 2010;55:1649-1660.
8. Jaffe R, Dick A, Strauss BH. Prevention and treatment of microvascular obstruction-related myocardial injury and coronary no-reflow following percutaneous coronary intervention: a systematic approach. JACC Cardiovasc Interv. 2010;3:695-704.
9. Kim RJ, Wu E, Rafael A, Chen EL, Parker MA, Simonetti O, Klocke FJ, Bonow RO, Judd RM. The use of contrast-enhanced magnetic resonance imaging to identify reversible myocardial dysfunction. N Engl J Med. 2000;343:1445-1453.
10. Wong TC, Piehler KM, Zareba KM, Lin K, Phrampus A, Patel A, Moon JC, Ugander M, Valeti U, Holtz JE, Fu B, Chang CC, Mathier M, Kellman P, Butler J, Gheorghiade M, Schelbert EB. Myocardial damage detected by late gadolinium enhancement cardiovascular magnetic resonance is associated with subsequent hospitalization for heart failure. J Am Heart Assoc. 2013;2:e000416.
11. Lima JA. Myocardial viability assessment by contrast-enhanced magnetic resonance imaging. J Am Coll Cardiol. 2003;42:902-904.
12. Isbell DC, Kramer CM. Magnetic resonance for the assessment of myocardial viability. Curr Opin Cardiol. 2006;21:469-472.
13. Thomson LE, Kim RJ, Judd RM. Magnetic resonance imaging for the assessment of myocardial viability. J Magn Reson Imaging. 2004;19:771-788.
14. McAteer MA, Akhtar AM, von Zur Muhlen C, Choudhury RP. An approach to molecular imaging of atherosclerosis, thrombosis, and vascular inflammation using microparticles of iron oxide. Atherosclerosis. 2010;209:18-27.
15. Schwarz M, Röttgen P, Takada Y, Le Gall F, Knackmuss S, Bassler N, Büttner C, Little M, Bode C, Peter K. Single-chain antibodies for the conformation-specific blockade of activated platelet integrin alphaIIbbeta3 designed by subtractive selection from naive human phage libraries. FASEB J. 2004;18:1704-1706.
16. von zur Muhlen C, von Elverfeldt D, Moeller JA, Choudhury RP, Paul D, Hagemeyer CE, Olschewski M, Becker A, Neudorfer I, Bassler N, Schwarz M, Bode C, Peter K. Magnetic resonance imaging contrast agent targeted toward activated platelets allows in vivo detection of thrombosis and monitoring of thrombolysis. Circulation. 2008;118:258-267.
17. von Elverfeldt D, von zur Muhlen C, Wiens K, Neudorfer I, Zirlik A, Meissner M, Tilly P, Charles AL, Bode C, Peter K, Fabre JE. In vivo detection of activated platelets allows characterizing rupture of atherosclerotic plaques with molecular magnetic resonance imaging in mice. PLoS One. 2012;7:e45008.
18. Duerschmied D, Meißner M, Peter K, Neudorfer I, Roming F, Zirlik A, Bode C, von Elverfeldt D, von Zur Muhlen C. Molecular magnetic resonance imaging allows the detection of activated platelets in a new mouse model of coronary artery thrombosis. Invest Radiol. 2011;46:618-623.
19. Schwarz M, Katagiri Y, Kotani M, Bassler N, Loeffler C, Bode C, Peter K. Reversibility versus persistence of GPIIb/IIIa blocker-induced conformational change of GPIIb/IIIa (alphaIIbbeta3, CD41/CD61). J Pharmacol Exp Ther. 2004;308:1002-1011.
20. Stoll P, Bassler N, Hagemeyer CE, Eisenhardt SU, Chen YC, Schmidt R, Schwarz M, Ahrens I, Katagiri Y, Pannen B, Bode C, Peter K. Targeting ligand-induced binding sites on GPIIb/IIIa via single-chain antibody allows effective anticoagulation without bleeding time prolongation. Arterioscler Thromb Vasc Biol. 2007;27:1206-1212.
21. Schwarz M, Meade G, Stoll P, Ylanne J, Bassler N, Chen YC, Hagemeyer CE, Ahrens I, Moran N, Kenny D, Fitzgerald D, Bode C, Peter K. Conformationspecific blockade of the integrin GPIIb/IIIa: a novel antiplatelet strategy that selectively targets activated platelets. Circ Res. 2006;99:25-33.
22. von Zur Muhlen C, Sibson NR, Peter K, Campbell SJ, Wilainam P, Grau GE, Bode C, Choudhury RP, Anthony DC. A contrast agent recognizing activated platelets reveals murine cerebral malaria pathology undetectable by conventional MRI. J Clin Invest. 2008;118:1198-1207.
23. von zur Muhlen C, von Elverfeldt D, Moeller JA, Choudhury RP, Paul D, Hagemeyer CE, Olschewski M, Becker A, Neudorfer I, Bassler N, Schwarz M, Bode C, Peter K. Magnetic resonance imaging contrast agent targeted toward activated platelets allows in vivo detection of thrombosis and monitoring of thrombolysis. Circulation. 2008;118:258-267.
24. von zur Muhlen C, Peter K, Ali ZA, Schneider JE, McAteer MA, Neubauer S, Channon KM, Bode C, Choudhury RP. Visualization of activated platelets by targeted magnetic resonance imaging utilizing conformation-specific antibodies against glycoprotein IIb/IIIa. J Vasc Res. 2009;46:6-14.
25. Wang X, Hagemeyer CE, Hohmann JD, Leitner E, Armstrong PC, Jia F, Olschewski M, Needles A, Peter K, Ahrens I. Novel single-chain antibody-targeted microbubbles for molecular ultrasound imaging of thrombosis: validation of a unique noninvasive method for rapid and sensitive detection of thrombi and monitoring of success or failure of thrombolysis in mice. Circulation. 2012;125:3117-3126.
26. Ben Addi A, Cammarata D, Conley PB, Boeynaems JM, Robaye B. Role of the P2Y12 receptor in the modulation of murine dendritic cell function by ADP. J Immunol. 2010;185:5900-5906.
27. Andre P, Delaney SM, La Rocca T, Vincent D, DeGuzman F, Jurek M, Koller B, Phillips DR, Conley PB. P2Y12 regulates platelet adhesion/activation, thrombus growth, and thrombus stability in injured arteries. J Clin Invest. 2003;112:398-406.
28. Majmudar MD, Nahrendorf M. Cardiovascular molecular imaging: the road ahead. J Nucl Med. 2012;53:673-676.
29. Shah BN, Khattar RS, Senior R. The hibernating myocardium: current concepts, diagnostic dilemmas, and clinical challenges in the post-STICH era. Eur Heart J. 2013;34:1323-1336.
30. Dagres N, Hindricks G. Risk stratification after myocardial infarction: is left ventricular ejection fraction enough to prevent sudden cardiac death? Eur Heart J. 2013;34:1964-1971.
31. Ordovas KG, Higgins CB. Delayed contrast enhancement on MR images of myocardium: past, present, future. Radiology. 2011;261:358-374.
32. Kwong RY, Chan AK, Brown KA, Chan CW, Reynolds HG, Tsang S, Davis RB. Impact of unrecognized myocardial scar detected by cardiac magnetic resonance imaging on event-free survival in patients presenting with signs or symptoms of coronary artery disease. Circulation. 2006;113:2733-2743.
33. Iles L, Pfluger H, Lefkovits L, Butler MJ, Kistler PM, Kaye DM, Taylor AJ. Myocardial fibrosis predicts appropriate device therapy in patients with implantable cardioverter-defibrillators for primary prevention of sudden cardiac death. J Am Coll Cardiol. 2011;57:821-828.
34. Leuschner F, Nahrendorf M. Molecular imaging of coronary atherosclerosis and myocardial infarction: considerations for the bench and perspectives for the clinic. Circ Res. 2011;108:593-606.
35. Lee WW, Marinelli B, van der Laan AM, Sena BF, Gorbatov R, Leuschner F, Dutta P, Iwamoto Y, Ueno T, Begieneman MP, Niessen HW, Piek JJ, Vinegoni C, Pittet MJ, Swirski FK, Tawakol A, Di Carli M, Weissleder R, Nahrendorf M. PET/MRI of inflammation in myocardial infarction. J Am Coll Cardiol. 2012;59:153-163.
36. Seligmann C, Prechtl G, Kusus-Seligmann M, Daniel WG. A myocardial ischemia- and reperfusion-induced injury is mediated by reactive oxygen species released from blood platelets. Platelets. 2013;24:37-43.
37. Barrabés JA, Inserte J, Mirabet M, Quiroga A, Hernando V, Figueras J, Garcia-Dorado D. Antagonism of P2Y12 or GPIIb/IIIa receptors reduces platelet-mediated myocardial injury after ischaemia and reperfusion in isolated rat hearts. Thromb Haemost. 2010;104:128-135.
38. Ito H. No reflow phenomenon in coronary heart disease. J Cardiol. 2001;37(suppl 1):39-42.
39. Langer H, Gawaz M. The role of platelets for the pathophysiology of acute coronary syndromes [in German]. Hamostaseologie. 2006;26:114-118.
40. Cura FA, L'Allier PL, Kapadia SR, Houghtaling PL, Dipaola LM, Ellis SG, Topol EJ, Brener SJ; GUSTO IIb and RAPPORT Investigators. Predictors and prognosis of suboptimal coronary blood flow after primary coronary angioplasty in patients with acute myocardial infarction. Am J Cardiol. 2001;88:124-128.
41. Lund GK, Stork A, Saeed M, Bansmann MP, Gerken JH, Müller V, Mester J, Higgins CB, Adam G, Meinertz T. Acute myocardial infarction: evaluation with first-pass enhancement and delayed enhancement MR imaging compared with 201Tl SPECT imaging. Radiology. 2004;232:49-57.
42. Antman EM, Giugliano RP, Gibson CM, McCabe CH, Coussement P, Kleiman NS, Vahanian A, Adgey AA, Menown I, Rupprecht HJ, Van der Wieken R, Ducas J, Scherer J, Anderson K, Van de Werf F, Braunwald E. Abciximab facilitates the rate and extent of thrombolysis: results of the Thrombolysis in Myocardial Infarction (TIMI) 14 trial: the TIMI 14 Investigators. Circulation. 1999;99:2720-2732.
43. Wagenhaus B, Pohlmann A, Dieringer MA, Els A, Waiczies H, Waiczies S, Schulz-Menger J, Niendorf T. Functional and morphological cardiac magnetic resonance imaging of mice using a cryogenic quadrature radiofrequency coil. PLoS One. 2012;7:e42383.
44. Perman WH, Bhattacharya P, Leupold J, Lin AP, Harris KC, Norton VA, Hövener JB, Ross BD. Fast volumetric spatial-spectral MR imaging of hyperpolarized 13C-labeled compounds using multiple echo 3D bSSFP. Magn Reson Imaging. 2010;28:459-465.
45. Viale A, Aime S. Current concepts on hyperpolarized molecules in MRI. Curr Opin Chem Biol. 2010;14:90-96.
46. Hagemeyer CE, von Zur Muhlen C, von Elverfeldt D, Peter K. Singlechain antibodies as diagnostic tools and therapeutic agents. Thromb Haemost. 2009;101:1012-1019.
47. von Zur Muhlen C, von Elverfeldt D, Choudhury RP, Ender J, Ahrens I, Schwarz M, Hennig J, Bode C, Peter K. Functionalized magnetic resonance contrast agent selectively binds to glycoprotein IIb/IIIa on activated human platelets under flow conditions and is detectable at clinically relevant field strengths. Mol Imaging. 2008;7:59-67.