New molecular probes of vascular inflammation

Quarterly Journal of Nuclear Medicine and Molecular Imaging

Volumn 60, Issue 3, 2016, Pages 194-204

  Vrachimis, Alexis ^a,b   Honold, Lisa ^b   Faufaust, Andreas ^b   Hermann, Sven ^b   Schäfers, Michael ^a,b  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Atherosclerosis; Inflammation; Molecular imaging

Indexed keywords

C REACTIVE PROTEIN; FLUORODEOXYGLUCOSE F 18; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 3; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MANNOSE; MATRIX METALLOPROTEINASE; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; VASCULOTROPIN; MOLECULAR PROBE;

APOPTOSIS; ATHEROSCLEROSIS; BINDING AFFINITY; CALCIFICATION; CELL DEATH; CEREBROVASCULAR ACCIDENT; HEART INFARCTION; HUMAN; HYPOXIA; MOLECULAR IMAGING; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERIPHERAL VASCULAR DISEASE; PHOSPHORYLATION; POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION; REVIEW; RISK FACTOR; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; VASCULITIS; ANIMAL; BLOOD; CALCINOSIS; CARDIOLOGY; CHEMISTRY; DIAGNOSTIC IMAGING; DISEASE MODEL; INFLAMMATION; MOLECULAR PROBE; MOUSE; POSITRON EMISSION TOMOGRAPHY-COMPUTED TOMOGRAPHY; PROCEDURES; TRANSLATIONAL RESEARCH;

ANIMALS; APOPTOSIS; ATHEROSCLEROSIS; CALCINOSIS; CARDIOLOGY; DISEASE MODELS, ANIMAL; FLUORODEOXYGLUCOSE F18; HUMANS; HYPOXIA; INFLAMMATION; MICE; MOLECULAR PROBES; NEOVASCULARIZATION, PATHOLOGIC; POSITRON EMISSION TOMOGRAPHY COMPUTED TOMOGRAPHY; POSITRON-EMISSION TOMOGRAPHY; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84992499901     PISSN: 18244785     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (69)

1. Anderson GF, Chu E. Expanding priorities-confronting chronic disease in countries with low income. NEngl J Med 2007;356:209-11.
2. Bucerius J, Hyafil F, Verberne HJ, Slart RH, Lindner O, Sciagra R, et al. Position paper of the Cardiovascular Committee of the European Association of Nuclear Medicine (EANM) on PET imaging of atherosclerosis. Eur J Nucl Med Mol Imaging 2016;43:780-92.
3. WHO. Cardiovascular diseases (CVDs). Fact sheet no. 317. Geneva: World Health Organization; [Internet] 2015. Available from: http://www.who.int/mediacentre/factsheets/fs317/en/ [cited 2016, Jun 13].
4. Glass CK, Witztum JL. Atherosclerosis. the road ahead. Cell 2001;104:503-16.
5. Skalen K, Gustafsson M, Rydberg EK, Hulten LM, Wiklund O, Innerarity TL, et al. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature 2002;417:750-4.
6. Libby P. Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol 2012;32:2045-51.
7. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 1999;340:115-26.
8. Dutta P, Courties G, Wei Y, Leuschner F, Gorbatov R, Robbins CS, et al. Myocardial infarction accelerates atherosclerosis. Nature 2012;487:325-9.
9. Tarkin JM, Joshi FR, Rudd JH. PET imaging of inflammation in atherosclerosis. Nat Rev Cardiol 2014;11:443-57.
10. 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(Suppl 3):13-21.
11. Quillard T, Libby P. Molecular imaging of atherosclerosis for improving diagnostic and therapeutic development. Circ Res 2012;111:231-44.
12. Rudd JH, Hyafil F, Fayad ZA. Inflammation imaging in atherosclerosis. Arterioscler Thromb Vasc Biol 2009;29:1009-16.
13. Tawakol A, Migrino RQ, Bashian GG, Bedri S, Vermylen D, Cury RC, et al. In vivo 18F-fluorodeoxyglucose positron emission tomography imaging provides a noninvasive measure of carotid plaque inflammation in patients. J Am Coll Cardiol 2006;48:1818-24.
14. Folco EJ, Sheikine Y, Rocha VZ, Christen T, Shvartz E, Sukhova GK, et al. Hypoxia but not inflammation augments glucose uptake in human macrophages: Implications for imaging atherosclerosis with 18fluorine-labeled 2-deoxy-D-glucose positron emission tomography. J Am Coll Cardiol 2011;58:603-14.
15. Pedersen SF, Graebe M, Hag AM, Hojgaard L, Sillesen H, Kjaer A. (18)F-FDG imaging of human atherosclerotic carotid plaques reflects gene expression of the key hypoxia marker HIF-1alpha. Am J Nucl Med Mol Imaging 2013;3:384-92.
16. Glaudemans AW, Bonanno E, Galli F, Zeebregts CJ, de Vries EF, Koole M, et al. In vivo and in vitro evidence that (9)(9)mTc-HYNIC-interleukin-2 is able to detect T lymphocytes in vulnerable atherosclerotic plaques of the carotid artery. Eur J Nucl Med Mol Imaging 2014;41:1710-9.
17. Liu Y, Pierce R, Luehmann HP, Sharp TL, Welch MJ. PET imaging of chemokine receptors in vascular injury-accelerated atherosclerosis. J Nucl Med 2013;54:1135-41.
18. Luehmann HP, Detering L, Fors BP, Pressly ED, Woodard PK, Randolph GJ, et al. PET/CT Imaging of Chemokine Receptors in Inflammatory Atherosclerosis Using Targeted Nanoparticles. J Nucl Med 2016 Jan 21 [Epub ahead of print].
19. Junker A, Kokornaczyk AK, Zweemer AJ, Frehland B, Schepmann D, Yamaguchi J, et al. Synthesis, binding affinity and structure-activity relationships of novel, selective and dual targeting CCR2 and CCR5 receptor antagonists. Org Biomol Chem 2015;13:2407-22.
20. Winkel LC, Groen HC, van Thiel BS, Muller C, van der Steen AF, Wentzel JJ, 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 2014;13:10.2310/7290.2013.00061.
21. Wenning C, Kloth C, Kuhlmann MT, Jacobs AH, Schober O, Hermann S, et al. Serial F-18-FDG PET/CT distinguishes inflamed from stable plaque phenotypes in shear-stress induced murine atherosclerosis. Atherosclerosis 2014;234:276-82.
22. Jager NA, Westra J, Golestani R, van Dam GM, Low PS, Tio RA, et al. Folate receptor-beta imaging using 99mTc-folate to explore distribution of polarized macrophage populations in human atherosclerotic plaque. J Nucl Med 2014;55:1945-51.
23. Tahara N, Mukherjee J, de Haas HJ, Petrov AD, Tawakol A, Haider N, et al. 2-deoxy-2-[18F]fluoro-D-mannose positron emission tomography imaging in atherosclerosis. Nat Med 2014;20:215-9.
24. Li D, Patel AR, Klibanov AL, Kramer CM, Ruiz M, Kang BY, et al. Molecular imaging of atherosclerotic plaques targeted to oxidized LDLreceptor LOX-1 by SPECT/CT and magnetic resonance. Circ Cardiovasc Imaging 2010;3:464-72.
25. Wen S, Liu DF, Cui Y, Harris SS, Chen YC, Li KC, et al. In vivo MRIdetection of carotid atherosclerotic lesions and kidney inflammation in ApoE-deficient mice by using LOX-1 targeted iron nanoparticles. Nanomedicine 2014;10:639-49.
26. Rominger A, Saam T, Vogl E, Ubleis C, la Fougere C, Forster S, et al. In vivo imaging of macrophage activity in the coronary arteries using 68Ga-DOTATATEPET/CT: correlation with coronary calcium burden and risk factors. J Nucl Med 2010;51:193-7.
27. Li X, Samnick S, Lapa C, Israel I, Buck AK, Kreissl MC, et al. 68Ga-DOTATATE PET/CT for the detection of inflammation of large arteries: correlation with18F-FDG, calcium burden and risk factors. EJNMMIRes 2012;2:52, 219X-2-52.
28. US National Library of Medicine. ClinicalTrials.gov; 2013 [Internet]. Available from: http://clinicaltrials.gov/show/NCT02021188 [cited 2016, Jun 13].
29. Pedersen SF, Sandholt BV, Keller SH, Hansen AE, Clemmensen AE, Sillesen H, et al. 64Cu-DOTATATEPET/MRIfor Detection of Activated Macrophages in Carotid Atherosclerotic Plaques: Studies in Patients Undergoing Endarterectomy. Arterioscler Thromb Vasc Biol 2015;35:1696-703.
30. Malmberg C, Ripa RS, Johnbeck CB, Knigge U, Langer SW, Mortensen J, et al. 64Cu-DOTATATEfor Noninvasive Assessment of Atherosclerosis in Large Arteries and Its Correlation with Risk Factors: Head-to-Head Comparison with 68Ga-DOTATOCin 60 Patients. J Nucl Med 2015;56:1895-900.
31. Foss CA, Bedja D, Mease RC, Wang H, Kass DA, Chatterjee S, et al. Molecular imaging of inflammation in the ApoE -/- mouse model of atherosclerosis with IodoDPA. Biochem Biophys Res Commun 2015;461:70-5.
32. Pugliese F, Gaemperli O, Kinderlerer AR, Lamare F, Shalhoub J, Davies AH, et al. Imaging of vascular inflammation with [11C]-PK11195 and positron emission tomography/computed tomography angiography. J Am Coll Cardiol 2010;56:653-61.
33. Gaemperli O, Shalhoub J, Owen DR, Lamare F, Johansson S, Fouladi N, et al. Imaging intraplaque inflammation in carotid atherosclerosis with 11C-PK11195 positron emission tomography/computed tomography. Eur Heart J 2012;33:1902-10.
34. Tarkin JM, Joshi FR, Rajani NK, Rudd JH. PET imaging of atherosclerosis. Future Cardiol 2015;11:115-31.
35. Owen DR, Lindsay AC, Choudhury RP, Fayad ZA. Imaging of atherosclerosis. Annu Rev Med 2011;62:25-40.
36. Bucerius J, Schmaljohann J, Bohm I, Palmedo H, Guhlke S, Tiemann K, et al. Feasibility of 18F-fluoromethylcholine PET/CT for imaging of vessel wall alterations in humans-first results. Eur J Nucl Med Mol Imaging 2008;35:815-20.
37. Kato K, Schober O, Ikeda M, Schafers M, Ishigaki T, Kies P, et al. Evaluation and comparison of 11C-choline uptake and calcification in aortic and common carotid arterial walls with combined PET/CT. Eur J Nucl Med Mol Imaging 2009;36:1622-8.
38. US National Library of Medicine. ClinicalTrials.gov; 2013 [Internet]. Available from: http://clinicaltrials.gov/ct2/show/NCT01899014 [cited 2016, Jun 13].
39. Kircher MF, Grimm J, Swirski FK, Libby P, Gerszten RE, Allport JR, et al. Noninvasive in vivo imaging of monocyte trafficking to atherosclerotic lesions. Circulation 2008;117:388-95.
40. van der Valk FM, Kroon J, Potters WV, Thurlings RM, Bennink RJ, Verberne HJ, et al. In vivo imaging of enhanced leukocyte accumulation in atherosclerotic lesions in humans. J Am Coll Cardiol 2014;64:1019-29.
41. Schafers M, Schober O, Hermann S. Matrix-metalloproteinases as imaging targets for inflammatory activity in atherosclerotic plaques. J Nucl Med 2010;51:663-6.
42. Bremer C, Tung CH, Weissleder R. In vivo molecular target assessment of matrix metalloproteinase inhibition. Nat Med 2001;7:743-8.
43. Wagner S, Breyholz HJ, Faust A, Holtke C, Levkau B, Schober O, et al. Molecular imaging of matrix metalloproteinases in vivo using small molecule inhibitors for SPECT and PET. Curr Med Chem 2006;13:2819-38.
44. Faust A, Waschkau B, Waldeck J, Holtke C, Breyholz HJ, Wagner S, et al. Synthesis and evaluation of a novel hydroxamate based fluorescent photoprobe for imaging of matrix metalloproteinases. Bioconjug Chem 2009;20:904-12.
45. Hugenberg V, Riemann B, Hermann S, Schober O, Schafers M, Szardenings K, et al. Inverse 1, 2, 3-triazole-1-yl-ethyl substituted hydroxamates as highly potent matrix metalloproteinase inhibitors: (radio)synthesis, in vitro and first in vivo evaluation. J Med Chem 2013;56:6858-70.
46. Razavian M, Nie L, Challa A, Zhang J, Golestani R, Jung JJ, et al. Lipid lowering and imaging protease activation in atherosclerosis. J Nucl Cardiol 2014;21:319-28.
47. Fujimoto S, Hartung D, Ohshima S, Edwards DS, 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;52:1847-57.
48. Hartung D, Schafers M, Fujimoto S, Levkau B, Narula N, Kopka K, et al. Targeting of matrix metalloproteinase activation for noninvasive detection of vulnerable atherosclerotic lesions. Eur J Nucl Med Mol Imaging 2007;34 Suppl 1:S1-8.
49. Zinnhardt B, Viel T, Wachsmuth L, Vrachimis A, Wagner S, Breyholz HJ, et al. Multimodal imaging reveals temporal and spatial microglia and matrix metalloproteinase activity after experimental stroke. J Cereb Blood Flow Metab 2015;35:1711-21.
50. Wagner S, Faust A, Breyholz HJ, Schober O, Schafers 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;69:862-8.
51. Kietselaer BL, Reutelingsperger CP, Heidendal GA, Daemen MJ, Mess WH, Hofstra L, et al. Noninvasive detection of plaque instability with use of radiolabeled annexin A5 in patients with carotid-artery atherosclerosis. NEngl J Med 2004;350:1472-3.
52. Hight MR, Cheung YY, Nickels ML, Dawson ES, Zhao P, Saleh S, et al. Apeptide-based positron emission tomography probe for in vivo detection of caspase activity in apoptotic cells. Clin Cancer Res 2014;20:2126-35.
53. De Saint-Hubert M, Bauwens M, Deckers N, Drummen M, Douma K, Granton P, et al. In vivo molecular imaging of apoptosis and necrosis in atherosclerotic plaques using microSPECT-CT and microPET-CT imaging. Mol Imaging Biol 2014;16:246-54.
54. Hyafil F, Tran-Dinh A, Burg S, Leygnac S, Louedec L, Milliner M, et al. Detection of Apoptotic Cells in a Rabbit Model with Atherosclerosis-Like Lesions Using the Positron Emission Tomography Radiotracer [18F]ML-10. Mol Imaging 2015;14:433-42.
55. Falk E, Nakano M, Bentzon JF, Finn AV, Virmani R. Update on acute coronary syndromes: the pathologists' view. Eur Heart J 2013;34:719-28.
56. Virmani R, Kolodgie FD, Burke AP, Finn AV, Gold HK, Tulenko TN, et al. Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol 2005;25:2054-61.
57. Su H, Gorodny N, Gomez LF, Gangadharmath UB, Mu F, Chen G, et al. Atherosclerotic plaque uptake of a novel integrin tracer (1)(8)F-Flotegatide in a mouse model of atherosclerosis. J Nucl Cardiol 2014;21:553-62.
58. Beer AJ, Pelisek J, Heider P, Saraste A, Reeps C, Metz S, et al. PET/CT imaging of integrin alphavbeta3 expression in human carotid atherosclerosis. JACCCardiovasc Imaging 2014;7:178-87.
59. Paeng JC, Lee YS, Lee JS, Jeong JM, Kim KB, Chung JK, et al. Feasibility and kinetic characteristics of (68)Ga-NOTA-RGDPET for in vivo atherosclerosis imaging. Ann Nucl Med 2013;27:847-54.
60. Razavian M, Marfatia R, Mongue-Din H, Tavakoli S, Sinusas AJ, Zhang J, et al. Integrin-targeted imaging of inflammation in vascular remodeling. Arterioscler Thromb Vasc Biol 2011;31:2820-6.
61. Golestani R, Zeebregts CJ, Terwisscha van Scheltinga AG, Lub-de Hooge MN, van Dam GM, Glaudemans AW, et al. Feasibility of vascular endothelial growth factor imaging in human atherosclerotic plaque using (89)Zr-bevacizumab positron emission tomography. Mol Imaging 2013;12:235-43.
62. Zhang J, Razavian M, Tavakoli S, Nie L, Tellides G, Backer JM, et al. Molecular imaging of vascular endothelial growth factor receptors in graft arteriosclerosis. Arterioscler Thromb Vasc Biol 2012;32:1849-55.
63. Yu H, Segers F, Sliedregt-Bol K, Bot I, Woltman AM, Boross P, et al. Identification of a novel CD40 ligand for targeted imaging of inflammatory plaques by phage display. FASEB J 2013;27:4136-46.
64. Mateo J, Izquierdo-Garcia D, Badimon JJ, Fayad ZA, Fuster V. Noninvasive assessment of hypoxia in rabbit advanced atherosclerosis using (1)(8)F-fluoromisonidazole positron emission tomographic imaging. Circ Cardiovasc Imaging 2014;7:312-20.
65. Vengrenyuk Y, Carlier S, Xanthos S, Cardoso L, Ganatos P, Virmani R, et al. Ahypothesis for vulnerable plaque rupture due to stress-induced debonding around cellular microcalcifications in thin fibrous caps. Proc Natl Acad Sci US A2006;103:14678-83.
66. Irkle A, Vesey AT, Lewis DY, Skepper JN, Bird JL, Dweck MR, et al. Identifying active vascular microcalcification by (18)F-sodium fluoride positron emission tomography. Nat Commun 2015;6:7495.
67. Derlin T, Richter U, Bannas P, Begemann P, Buchert R, Mester J, et al. Feasibility of 18F-sodium fluoride PET/CT for imaging of atherosclerotic plaque. J Nucl Med 2010;51:862-5.
68. Derlin T, Wisotzki C, Richter U, Apostolova I, Bannas P, Weber C, et al. In vivo imaging of mineral deposition in carotid plaque using 18F-sodium fluoride PET/CT: correlation with atherogenic risk factors. J Nucl Med 2011;52:362-8.
69. Joshi NV, Vesey AT, Williams MC, Shah AS, Calvert PA, Craighead FH, et al. 18F-fluoride positron emission tomography for identification of ruptured and high-risk coronary atherosclerotic plaques: a prospective clinical trial. Lancet 2014;383:705-13.