Gene expression levels of matrix metalloproteinases in human atherosclerotic plaques and evaluation of radiolabeled inhibitors as imaging agents for plaque vulnerability

Nuclear Medicine and Biology

Volumn 41, Issue 7, 2014, Pages 562-569

  Müller, Adrienne ^a   Krämer, Stefanie D ^a   Meletta, Romana ^a   Beck, Katharina ^a   Selivanova, Svetlana V ^a   Rancic, Zoran ^b   Kaufmann, Philipp A ^b   Vos, Bernhard ^c   Meding, Jörg ^c   Stellfeld, Timo ^c   Heinrich, Tobias K ^c   Bauser, Marcus ^c   Hütter, Joachim ^c   Dinkelborg, Ludger M ^c   Schibli, Roger ^a   Ametamey, Simon M ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c Bayer HealthCare   (Germany)

Author keywords

Atherosclerosis; Autoradiography; Carotid artery plaque; Inflammation; Matrix metalloproteinases; Tissue inhibitor of metalloproteinase 3

Indexed keywords

2 [4 (4 FLUOROBENZAMIDO)PHENYLSULFONAMIDO] 3 (1H INDOL 3 YL)PROPANOIC ACID F 18; CD68 ANTIGEN; FLUORINE 18; GELATINASE A; GELATINASE A INHIBITOR F 18; GELATINASE B; GELATINASE B INHIBITOR; GELATINASE B INHIBITOR F 18; INTERSTITIAL COLLAGENASE; MACROPHAGE ELASTASE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE INHIBITOR; METHYL 4 [3 (FORMYLHYDROXYAMINO) 4 [4 (4 TRIFLUOROMETHOXYPHENOXY)PHENYLSULFONYL]BUTYL]BENZOATE H 3; NEUTROPHIL COLLAGENASE; STROMELYSIN 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TRACER; UNCLASSIFIED DRUG; BENZOIC ACID; CD68 ANTIGEN, HUMAN; DIFFERENTIATION ANTIGEN; LEUKOCYTE ANTIGEN; TRITIUM;

ADULT; AGED; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTORADIOGRAPHY; CAROTID ATHEROSCLEROSIS; CAROTID ATHEROSCLEROTIC PLAQUE RUPTURE; CAROTID ENDARTERECTOMY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE CLASSIFICATION; DISEASE CONTROL; DRUG TARGETING; ENZYME LOCALIZATION; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; ISOTOPE LABELING; MACROPHAGE; MALE; MOUSE; NON INVASIVE MEASUREMENT; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; WESTERN BLOTTING; ANIMAL; ARTERY; CHEMISTRY; DIAGNOSTIC USE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; MOLECULAR IMAGING; PLAQUE, ATHEROSCLEROTIC; PROCEDURES; PROTEIN TRANSPORT; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; ARTERIES; BENZOIC ACID; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOTOPE LABELING; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE INHIBITORS; MATRIX METALLOPROTEINASES; MICE; MIDDLE AGED; MOLECULAR IMAGING; PLAQUE, ATHEROSCLEROTIC; PROTEIN TRANSPORT; TISSUE INHIBITOR OF METALLOPROTEINASE-3; TRITIUM;

EID: 84904507299     PISSN: 09698051     EISSN: 18729614     Source Type: Journal    
DOI: 10.1016/j.nucmedbio.2014.04.085     Document Type: Article

References (48)

1. Rosamond W., Flegal K., Friday G., Furie K., Go A., Greenlund K., et al. Heart disease and stroke statistics-2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2007, 115:e69-e171.
2. Liapis C.D., Bell P.R., Mikhailidis D., Sivenius J., Nicolaides A. Fernandes e Fernandes J, et al. ESVS guidelines. Invasive treatment for carotid stenosis: indications, techniques. Eur J Vasc Endovasc Surg 2009, 37:1-19.
3. Hansson G.K. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005, 352:1685-1695.
4. Libby P. Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol 2012, 32:2045-2051.
5. Khokha R., Murthy A., Weiss A. Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat Rev Immunol 2013, 13:649-665.
6. Higashikata T., Yamagishi M., Higashi T., Nagata I., Iihara K., Miyamoto S., et al. Altered expression balance of matrix metalloproteinases and their inhibitors in human carotid plaque disruption: results of quantitative tissue analysis using real-time RT-PCR method. Atherosclerosis 2006, 185:165-172.
7. Müller A., Mu L., Meletta R., Beck K., Rancic Z., Drandarov K., et al. Towards non-invasive imaging of vulnerable atherosclerotic plaques by targeting co-stimulatory molecules. Int J Cardiol 2014, 10.1016/j.ijcard.2014.04.071.
8. 18F]-fluorodeoxyglucose positron emission tomography. Circulation 2002, 105:2708-2711.
9. Davies J.R., Rudd J.H., Fryer T.D., Graves M.J., Clark J.C., Kirkpatrick P.J., et al. Identification of culprit lesions after transient ischemic attack by combined 18F fluorodeoxyglucose positron-emission tomography and high-resolution magnetic resonance imaging. Stroke 2005, 36:2642-2647.
10. Tahara N., Mukherjee J., de Haas H.J., Petrov A.D., Tawakol A., Haider N., et al. 2-deoxy-2-[F]fluoro-d-mannose positron emission tomography imaging in atherosclerosis. Nat Med 2014, 10.1038/nm.3437.
11. Ayala-Lopez W., Xia W., Varghese B., Low P.S. Imaging of atherosclerosis in apoliprotein e knockout mice: targeting of a folate-conjugated radiopharmaceutical to activated macrophages. J Nucl Med 2010, 51:768-774.
12. Winkel L.C., Groen H.C., van Thiel B.S., Müller C., van der Steen A.F., Wentzel J.J., et al. Folate receptor-targeted single-photon emission computed tomography/computed tomography to detect activated macrophages in atherosclerosis: Can It distinguish vulnerable from stable atherosclerotic plaques?. Mol Imaging 2013, 12:1-5.
13. 18F-folate radiotracer. Mol Imaging 2014, 13:1-11.
14. Fujimoto S., Hartung D., Ohshima S., Edwards D.S., Zhou J., Yalamanchili P., et al. Molecular imaging of matrix metalloproteinase in atherosclerotic lesions: resolution with dietary modification and statin therapy. J Am Coll Cardiol 2008, 52:1847-1857.
15. Hermann S., Starsichova A., Waschkau B., Kuhlmann M., Wenning C., Schober O., et al. Non-FDG imaging of atherosclerosis: will imaging of MMPs assess plaque vulnerability?. J Nucl Cardiol 2012, 19:609-617.
16. Sadeghi M.M., Glover D.K., Lanza G.M., Fayad Z.A., Johnson L.L. Imaging atherosclerosis and vulnerable plaque. J Nucl Med 2010, 51(Suppl 1):51S-65S.
17. Schäfers M., Schober O., Hermann S. Matrix-metalloproteinases as imaging targets for inflammatory activity in atherosclerotic plaques. J Nucl Med 2010, 51:663-666.
18. Newby A.C. Do metalloproteinases destabilize vulnerable atherosclerotic plaques?. Curr Opin Lipidol 2006, 17:556-561.
19. Galis Z.S., Sukhova G.K., Lark M.W., Libby P. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest 1994, 94:2493-2503.
20. Pepper M.S. Extracellular proteolysis and angiogenesis. Thromb Haemost 2001, 86:346-355.
21. Visse R., Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003, 92:827-839.
22. Malemud C.J. Matrix metalloproteinases (MMPs) in health and disease: an overview. Front Biosci 2006, 11:1696-1701.
23. Sluijter J.P., Pulskens W.P., Schoneveld A.H., Velema E., Strijder C.F., Moll F., et al. Matrix metalloproteinase 2 is associated with stable and matrix metalloproteinases 8 and 9 with vulnerable carotid atherosclerotic lesions: a study in human endarterectomy specimen pointing to a role for different extracellular matrix metalloproteinase inducer glycosylation forms. Stroke 2006, 37:235-239.
24. Hobeika M.J., Thompson R.W., Muhs B.E., Brooks P.C., Gagne P.J. Matrix metalloproteinases in peripheral vascular disease. J Vasc Surg 2007, 45:849-857.
25. Hugenberg V., Breyholz H.J., Riemann B., Hermann S., Schober O., Schäfers M., et al. A new class of highly potent matrix metalloproteinase inhibitors based on triazole-substituted hydroxamates: (radio)synthesis and in vitro and first in vivo evaluation. J Med Chem 2012, 55:4714-4727.
26. Schrigten D., Breyholz H.J., Wagner S., Hermann S., Schober O., Schäfers M., et al. A new generation of radiofluorinated pyrimidine-2,4,6-triones as MMP-targeted radiotracers for positron emission tomography. J Med Chem 2012, 55:223-232.
27. Selivanova S.V., Stellfeld T., Heinrich T.K., Müller A., Krämer S.D., Schubiger P.A., et al. Design, synthesis, and initial evaluation of a high affinity positron emission tomography probe for imaging matrix metalloproteinases 2 and 9. J Med Chem 2013, 56:4912-4920.
28. Wagner S., Faust A., Breyholz H.J., Schober O., Schäfers M., Kopka K. The MMP inhibitor (R)-2-(N-benzyl-4-(2-[18F]fluoroethoxy)phenylsulphonamido)-N-hydroxy-3-methylbuta namide: Improved precursor synthesis and fully automated radiosynthesis. Appl Radiat Isot 2011, 69:862-868.
29. Benjamin M.M., Khalil R.A. Matrix metalloproteinase inhibitors as investigative tools in the pathogenesis and management of vascular disease. EXS 2012, 103:209-279.
30. Scherer R.L., McIntyre J.O., Matrisian L.M. Imaging matrix metalloproteinases in cancer. Cancer Metastasis Rev 2008, 27:679-690.
31. Wada C.K., Holms J.H., Curtin M.L., Dai Y., Florjancic A.S., Garland R.B., et al. Phenoxyphenyl sulfone N-formylhydroxylamines (retrohydroxamates) as potent, selective, orally bioavailable matrix metalloproteinase inhibitors. J Med Chem 2002, 45:219-232.
32. Nett P.C., Zund G., Pretre R., Niederhouser U., Vogt P.R., Turina M. A 20-year follow-up of internal carotid artery endarterectomy with bifurcation advancement. Thorac Cardiovasc Surg 2000, 48:279-284.
33. -δδCt Method. Methods 2001, 25:402-408.
34. Stary H.C., Chandler A.B., Dinsmore R.E., Fuster V., Glagov S., Insull W., et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. Circulation 1995, 92:1355-1374.
35. Müller A., Mu L., Meletta R., Beck K., Rancic Z., Drandarov K., et al. Towards non-invasive imaging of vulnerable atherosclerotic plaques by targeting co-stimulatory molecules. Int J Cardiol 2014, [accepted for publication]. 10.1016/j.ijcard.2014.04.071.
36. Sternlicht M.D., Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001, 17:463-516.
37. Gonzalez-Avila G., Iturria C., Vadillo F., Teran L., Selman M., Perez-Tamayo R. 72-kD (MMP-2) and 92-kD (MMP-9) type IV collagenase production and activity in different histologic types of lung cancer cells. Pathobiology 1998, 66:5-16.
38. Sands M.F. Localization of matrix metalloproteinase (MMP)-9 in lung tissue of a murine model of allergic asthma. Immunol Invest 2012, 41:87-96.
39. Lee D.-H., Kang K. Purification and characterization of human 92-kDa type IV collagenase (gelatinase B). Exp Mol Med 1996, 28:161-165.
40. Sukhova G.K., Schonbeck U., Rabkin E., Schoen F.J., Poole A.R., Billinghurst R.C., et al. Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques. Circulation 1999, 99:2503-2509.
41. Molloy K.J., Thompson M.M., Jones J.L., Schwalbe E.C., Bell P.R., Naylor A.R., et al. Unstable carotid plaques exhibit raised matrix metalloproteinase-8 activity. Circulation 2004, 110:337-343.
42. Laxton R.C., Hu Y., Duchene J., Zhang F., Zhang Z., Leung K.Y., et al. A role of matrix metalloproteinase-8 in atherosclerosis. Circ Res 2009, 105:921-929.
43. Luttun A., Lutgens E., Manderveld A., Maris K., Collen D., Carmeliet P., et al. Loss of matrix metalloproteinase-9 or matrix metalloproteinase-12 protects apolipoprotein E-deficient mice against atherosclerotic media destruction but differentially affects plaque growth. Circulation 2004, 109:1408-1414.
44. Schneider F., Sukhova G.K., Aikawa M., Canner J., Gerdes N., Tang S.M., et al. Matrix-metalloproteinase-14 deficiency in bone-marrow-derived cells promotes collagen accumulation in mouse atherosclerotic plaques. Circulation 2008, 117:931-939.
45. Vihinen P., Ala-aho R., Kahari V.M. Matrix metalloproteinases as therapeutic targets in cancer. Curr Cancer Drug Targets 2005, 5:203-220.
46. Newby A.C. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev 2005, 85:1-31.
47. Fedak P.W., Altamentova S.M., Weisel R.D., Nili N., Ohno N., Verma S., et al. Matrix remodeling in experimental and human heart failure: a possible regulatory role for TIMP-3. Am J Physiol Heart Circ Physiol 2003, 284:H626-H634.
48. Wang J., Medina C., Radomski M.W., Gilmer J.F. N-substituted homopiperazine barbiturates as gelatinase inhibitors. Bioorg Med Chem 2011, 19:4985-4999.