Dual-modality activity-based probes as molecular imaging agents for vascular inflammation

Journal of Nuclear Medicine

Volumn 57, Issue 10, 2016, Pages 1583-1590

  Withana, Nimali P ^a   Saito, Toshinobu ^a   Ma, Xiaowei ^b   Garland, Megan ^a   Liu, Changhao ^b   Kosuge, Hisanori ^a   Amsallem, Myriam ^a   Verdoes, Martijn ^a   Ofori, Leslie O ^a   Fischbein, Michael ^a   Arakawa, Mamoru ^a   Cheng, Zhen ^b   McConnell, Michael V ^a   Bogyo, Matthew ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Activity based probes; Animal imaging; Atherosclerosis; Cathepsins; Inflammation; Macrophages; Optical; PET; PET CT; Vascular

Indexed keywords

BMV 101; BMV 101 CU 64; BMV 109; CATHEPSIN; CATHEPSIN B; CATHEPSIN L; CATHEPSIN S; CATHEPSIN X; CD68 ANTIGEN; COPPER 64; CYSTEINE; ELASTIN; TRACER; UNCLASSIFIED DRUG; MOLECULAR PROBE;

ADVENTITIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; CAROTID ATHEROSCLEROSIS; CELL INFILTRATION; COMPUTED TOMOGRAPHY SCANNER; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CONTROLLED STUDY; EX VIVO STUDY; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; MACROPHAGE ACTIVATION; MOLECULAR IMAGING; MOLECULAR PROBE; MOUSE; NEOINTIMA; NON INVASIVE PROCEDURE; NONHUMAN; PET SCANNER; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; VASCULITIS; ANIMAL; CAROTID ARTERY; DIAGNOSTIC IMAGING; MACROPHAGE; METABOLISM; POSITRON EMISSION TOMOGRAPHY; PROCEDURES;

ANIMALS; ATHEROSCLEROSIS; CAROTID ARTERIES; CATHEPSINS; HUMANS; MACROPHAGES; MICE; MOLECULAR IMAGING; MOLECULAR PROBES; POSITRON-EMISSION TOMOGRAPHY;

EID: 84991384034     PISSN: 01615505     EISSN: 2159662X     Source Type: Journal    
DOI: 10.2967/jnumed.115.171553     Document Type: Article

References (38)

1. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
2. Libby P, Hansson GK. Inflammation and immunity in diseases of the arterial tree: players and layers. Circ Res. 2015;116:307-311.
3. Davies MJ, Thomas AC. Plaque fissuring: the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. Br Heart J. 1985;53:363-373.
4. Jickling GC, Chaturvedi S. Carotid plaque inflammation in stroke assessed by PET: a burning issue? Neurology. 2014;82:1672-1673.
5. Bentzon JF, Otsuka F, Virmani R, Falk E. Mechanisms of plaque formation and rupture. Circ Res. 2014;114:1852-1866.
6. Usman A, Ribatti D, Sadat U, Gillard JH. From lipid retention to immunemediate inflammation and associated angiogenesis in the pathogenesis of atherosclerosis. J Atheroscler Thromb. 2015;22:739-749.
7. Chistiakov DA, Bobryshev YV, Nikiforov NG, Elizova NV, Sobenin IA, Orekhov AN. Macrophage phenotypic plasticity in atherosclerosis: the associated features and the peculiarities of the expression of inflammatory genes. Int J Cardiol. 2015;184:436-445.
8. Ley K, Miller YI, Hedrick CC. Monocyte and macrophage dynamics during atherogenesis. Arterioscler Thromb Vasc Biol. 2011;31:1506-1516.
9. Galis ZS, Sukhova GK, Lark MW, 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.
10. Sukhova GK, Shi GP, Simon DI, Chapman HA, Libby P. Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest. 1998;102:576-583.
11. Vinegoni C, Botnaru I, Aikawa E, et al. Indocyanine green enables near-infrared fluorescence imaging of lipid-rich, inflamed atherosclerotic plaques. Sci Transl Med. 2011;3:84ra45.
12. Garland M, Yim JJ, Bogyo M. A bright future for precision medicine: advances in fluorescent chemical probe design and their clinical application. Cell Chem Biol. 2016;23:122-136.
13. Quillard T, Libby P. Molecular imaging of atherosclerosis for improving diagnostic and therapeutic development. Circ Res. 2012;111:231-244.
14. Rudd JH, Hyafil F, Fayad ZA. Inflammation imaging in atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29:1009-1016.
15. Alie N, Eldib M, Fayad ZA, Mani V. Inflammation, atherosclerosis, and coronary artery disease: PET/CT for the evaluation of atherosclerosis and inflammation. Clin Med Insights Cardiol. 2015;8:13-21.
16. Dweck MR, Chow MW, Joshi NV, et al. Coronary arterial18 F-sodium fluoride uptake: a novel marker of plaque biology. J Am Coll Cardiol. 2012;59:1539-1548.
17. 18F-FDG uptake in arterial atheroma on PET/CT? Implications for imaging the vulnerable plaque. Atherosclerosis. 2010;211:136-140.
18. 18Fluorodeoxyglucose positron emission tomography imaging of atherosclerotic plaque inflammation is highly reproducible: implications for atherosclerosis therapy trials. J Am Coll Cardiol. 2007;50:892-896.
19. Jezovnik MK, Zidar N, Lezaic L, Gersak B, Poredos P. Identification of inflamed atherosclerotic lesions in vivo using PET-CT. Inflammation. 2014;37:426-434.
20. 18F]-fluorodeoxyglucose positron emission tomography. Circulation. 2002;105:2708-2711.
21. Sadat U, Jaffer FA, van Zandvoort MA, Nicholls SJ, Ribatti D, Gillard JH. Inflammation and neovascularization intertwined in atherosclerosis: imaging of structural and molecular imaging targets. Circulation. 2014;130:786-794.
22. Kitagawa T, Kosuge H, Uchida M, et al. RGD-conjugated human ferritin nanoparticles for imaging vascular inflammation and angiogenesis in experimental carotid and aortic disease. Mol Imaging Biol. 2012;14:315-324.
23. 3 expression in human carotid atherosclerosis. JACC Cardiovasc Imaging. 2014;7:178-187.
24. 3 integrin: potential role in human atherosclerosis. Am J Pathol. 2004;165:247-258.
25. 3 integrin expression in normal and atherosclerotic artery. Circ Res. 1995;77:1129-1135.
26. Lutgens SP, Cleutjens KB, Daemen MJ, Heeneman S. Cathepsin cysteine proteases in cardiovascular disease. FASEB J. 2007;21:3029-3041.
27. -/- mice. J Cardiovasc Pharmacol. 2010;56:98-105.
28. Figueiredo JL, Aikawa M, Zheng C, et al. Selective cathepsin S inhibition attenuates atherosclerosis in apolipoprotein E-deficient mice with chronic renal disease. Am J Pathol. 2015;185:1156-1166.
29. Blum G, Weimer RM, Edgington LE, Adams W, Bogyo M. Comparative assessment of substrates and activity based probes as tools for non-invasive optical imaging of cysteine protease activity. PLoS One. 2009;4:e6374.
30. Ofori LO, Withana NP, Prestwood TR, et al. Design of protease activated optical contrast agents that exploit a latent lysosomotropic effect for use in fluorescence-guided surgery. ACS Chem Biol. 2015;10:1977-1988.
31. Sanman LE, Bogyo M. Activity-based profiling of proteases. Annu Rev Biochem. 2014;83:249-273.
32. Terashima M, Uchida M, Kosuge H, et al. Human ferritin cages for imaging vascular macrophages. Biomaterials. 2011;32:1430-1437.
33. Blum G, Mullins SR, Keren K, et al. Dynamic imaging of protease activity with fluorescently quenched activity-based probes. Nat Chem Biol. 2005;1:203-209.
34. Withana NP, Garland M, Verdoes M, Ofori LO, Segal E, Bogyo M. Labeling of active proteases in fresh-frozen tissues by topical application of quenched activity-based probes. Nat Protoc. 2016;11:184-191.
35. Withana NP, Ma X, McGuire HM, et al. Non-invasive imaging of idiopathic pulmonary fibrosis using cathepsin protease probes. Sci Rep. 2016;6:19755.
36. Verdoes M, Oresic Bender K, Segal E, et al. Improved quenched fluorescent probe for imaging of cysteine cathepsin activity. J Am Chem Soc. 2013;135:14726-14730.
37. Cutter JL, Cohen NT, Wang J, et al. Topical application of activity-based probes for visualization of brain tumor tissue. PLoS One. 2012;7:e33060.
38. Segal E, Prestwood TR, van der Linden WA, et al. Detection of intestinal cancer by local, topical application of a quenched fluorescence probe for cysteine cathepsins. Chem Biol. 2015;22:148-158.