In vivo fluorescence imaging of atherosclerotic plaques with activatable cell-penetrating peptides targeting thrombin activity

Integrative Biology (United Kingdom)

Volumn 4, Issue 6, 2012, Pages 595-605

  Olson, Emilia S ^a   Whitney, Michael A ^a   Friedman, Beth ^a   Aguilera, Todd A ^a   Crisp, Jessica L ^a   Baik, Fred M ^b   Jiang, Tao ^a   Baird, Stephen M ^a   Tsimikas, Sotirios ^c   Tsien, Roger Y ^a   Nguyen, Quyen T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGATROBAN; CELL PENETRATING PEPTIDE; HIRUDIN; LEPIRUDIN; PROTEINASE ACTIVATED RECEPTOR 1; THROMBIN; ANTITHROMBIN; FLUORESCENT DYE; HIRUDIN DERIVATIVE; PIPECOLIC ACID DERIVATIVE; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROTIC PLAQUE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FLUORESCENCE IMAGING; HUMAN; HUMAN TISSUE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; AMINO ACID SEQUENCE; ANIMAL; AORTA; C57BL MOUSE; CYTOCHEMISTRY; DRUG ANTAGONISM; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; METABOLISM; MOUSE MUTANT; PATHOLOGY; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; ANTITHROMBINS; AORTA; CELL-PENETRATING PEPTIDES; FLUORESCENT DYES; HIRUDINS; HISTOCYTOCHEMISTRY; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; PIPECOLIC ACIDS; PLAQUE, ATHEROSCLEROTIC; RECEPTOR, PAR-1; RECOMBINANT PROTEINS; THROMBIN;

EID: 84874417298     PISSN: 17579694     EISSN: 17579708     Source Type: Journal    
DOI: 10.1039/c2ib00161f     Document Type: Article

References (52)

1. V. L. Roger A. S. Go D. M. Lloyd-Jones E. J. Benjamin J. D. Berry W. B. Borden D. M. Bravata S. Dai E. S. Ford C. S. Fox H. J. Fullerton C. Gillespie S. M. Hailpern J. A. Heit V. J. Howard B. M. Kissela S. J. Kittner D. T. Lackland J. H. Lichtman L. D. Lisabeth D. M. Makuc G. M. Marcus A. Marelli D. B. Matchar C. S. Moy D. Mozaffarian M. E. Mussolino G. Nichol N. P. Paynter E. Z. Soliman P. D. Sorlie N. Sotoodehnia T. N. Turan S. S. Virani N. D. Wong D. Woo M. B. Turner Executive summary: Heart disease and stroke statistics-2012 update: A report from the American heart association Circulation 2012 125 188 197
2. H. C. Stary A. B. Chandler R. E. Dinsmore V. Fuster S. Glagov W. Insull, Jr. M. E. Rosenfeld C. J. Schwartz W. D. Wagner R. W. Wissler A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the committee on vascular lesions of the council on arteriosclerosis, American heart association Circulation 1995 92 1355 1374
3. M. E. Gaunt L. Brown T. Hartshorne P. R. Bell A. R. Naylor Unstable carotid plaques: Preoperative identification and association with intraoperative embolisation detected by transcranial doppler Eur. J. Vasc. Endovasc. Surg. 1996 11 78 82
4. A. Cohen C. Tzourio B. Bertrand C. Chauvel M. G. Bousser P. Amarenco Aortic plaque morphology and vascular events: A follow-up study in patients with ischemic stroke. Faps investigators. French study of aortic plaques in stroke Circulation 1997 96 3838 3841
5. M. Wintermark S. S. Jawadi J. H. Rapp T. Tihan E. Tong D. V. Glidden S. Abedin S. Schaeffer G. Acevedo-Bolton B. Boudignon B. Orwoll X. Pan D. Saloner High-resolution ct imaging of carotid artery atherosclerotic plaques AJNR Am. J. Neuroradiol. 2008 29 875 882
6. H. R. Underhill T. S. Hatsukami Z. A. Fayad V. Fuster C. Yuan Mri of carotid atherosclerosis: Clinical implications and future directions Nat. Rev. Cardiol. 2010 7 165 173
7. C. Vinegoni I. Botnaru E. Aikawa M. A. Calfon Y. Iwamoto E. J. Folco V. Ntziachristos R. Weissleder P. Libby F. A. Jaffer Indocyanine green enables near-infrared fluorescence imaging of lipid-rich, inflamed atherosclerotic plaques Sci. Transl. Med. 2011 3 84ra45
8. N. Haider D. Hartung S. Fujimoto A. Petrov F. D. Kolodgie R. Virmani S. Ohshima H. Liu J. Zhou A. Fujimoto A. Tahara L. Hofstra N. Narula C. Reutelingsperger J. Narula Dual molecular imaging for targeting metalloproteinase activity and apoptosis in atherosclerosis: Molecular imaging facilitates understanding of pathogenesis J. Nucl. Cardiol. 2009 16 753 762
9. F. A. Jaffer D. E. Kim L. Quinti C. H. Tung E. Aikawa A. N. Pande R. H. Kohler G. P. Shi P. Libby R. Weissleder Optical visualization of cathepsin k activity in atherosclerosis with a novel, protease-activatable fluorescence sensor Circulation 2007 115 2292 2298
10. Z. Li L. Li H. R. Zielke L. Cheng R. Xiao M. T. Crow W. G. Stetler-Stevenson J. Froehlich E. G. Lakatta Increased expression of 72-kd type iv collagenase (mmp-2) in human aortic atherosclerotic lesions Am. J. Pathol. 1996 148 121 128
11. J. I. Borissoff S. Heeneman E. Kilinc P. Kassak R. Van Oerle K. Winckers J. W. Govers-Riemslag K. Hamulyak T. M. Hackeng M. J. Daemen H. ten Cate H. M. Spronk Early atherosclerosis exhibits an enhanced procoagulant state Circulation 2010 122 821 830
12. J. I. Borissoff H. M. Spronk S. Heeneman H. ten Cate Is thrombin a key player in the 'coagulation-atherogenesis' maze? Cardiovasc. Res. 2009 82 392 403
13. M. T. Garcia-Lopez M. Gutierrez-Rodriguez R. Herranz Thrombin-activated receptors: Promising targets for cancer therapy? Curr. Med. Chem. 2010 17 109 128
14. E. Aikawa M. Nahrendorf J. L. Figueiredo F. K. Swirski T. Shtatland R. H. Kohler F. A. Jaffer M. Aikawa R. Weissleder Osteogenesis associates with inflammation in early-stage atherosclerosis evaluated by molecular imaging in vivo Circulation 2007 116 2841 2850
15. A. J. Leger L. Covic A. Kuliopulos Protease-activated receptors in cardiovascular diseases Circulation 2006 114 1070 1077
16. A. Gupta M. D. Williams W. L. Macias B. A. Molitoris B. W. Grinnell Activated protein c and acute kidney injury: Selective targeting of par-1 Curr. Drug Targets 2009 10 1212 1226
17. G. Mannaioni A. G. Orr C. E. Hamill H. Yuan K. H. Pedone K. L. McCoy R. Palmini Berlinguer C. E. Junge C. J. Lee M. Yepes J. R. Hepler S. F. Traynelis Plasmin potentiates synaptic n-methyl-d-aspartate receptor function in hippocampal neurons through activation of protease-activated receptor-1 J. Biol. Chem. 2008 283 20600 20611
18. A. Kuliopulos L. Covic S. K. Seeley P. J. Sheridan J. Helin C. E. Costello Plasmin desensitization of the par1 thrombin receptor: Kinetics, sites of truncation, and implications for thrombolytic therapy Biochemistry 1999 38 4572 4585
19. S. L. Jacques M. LeMasurier P. J. Sheridan S. K. Seeley A. Kuliopulos Substrate-assisted catalysis of the par1 thrombin receptor. Enhancement of macromolecular association and cleavage J. Biol. Chem. 2000 275 40671 40678
20. M. A. Parry T. Myles J. Tschopp S. R. Stone Cleavage of the thrombin receptor: Identification of potential activators and inactivators Biochem. J. 1996 320 Pt 1 335 341
21. H. J. Breyholz S. Wagner A. Faust B. Riemann C. Holtke S. Hermann O. Schober M. Schafers K. Kopka Radiofluorinated pyrimidine-2,4,6-triones as molecular probes for noninvasive mmp-targeted imaging ChemMedChem 2010 5 777 789
22. A. Faust B. Waschkau J. Waldeck C. Holtke H. J. Breyholz S. Wagner K. Kopka W. Heindel M. Schafers C. Bremer Synthesis and evaluation of a novel fluorescent photoprobe for imaging matrix metalloproteinases Bioconjugate Chem. 2008 19 1001 1008
23. T. A. Aguilera E. S. Olson M. M. Timmers T. Jiang R. Y. Tsien Systemic in vivo distribution of activatable cell penetrating peptides is superior to that of cell penetrating peptides Integr. Biol. 2009 1 371 381
24. T. Jiang E. S. Olson Q. T. Nguyen M. Roy P. A. Jennings R. Y. Tsien Tumor imaging by means of proteolytic activation of cell-penetrating peptides Proc. Natl. Acad. Sci. U. S. A. 2004 101 17867 17872
25. E. S. Olson T. A. Aguilera T. Jiang L. G. Ellies Q. T. Nguyen E. H. Wong L. A. Gross R. Y. Tsien In vivo characterization of activatable cell penetrating peptides for targeting protease activity in cancer Integr. Biol. 2009 1 382 393
26. E. S. Olson T. Jiang T. A. Aguilera Q. T. Nguyen L. G. Ellies M. Scadeng R. Y. Tsien Activatable cell penetrating peptides linked to nanoparticles as dual probes for in vivo fluorescence and mr imaging of proteases Proc. Natl. Acad. Sci. U. S. A. 2010 107 4311 4316
27. C. Bremer S. Bredow U. Mahmood R. Weissleder C. H. Tung Optical imaging of matrix metalloproteinase-2 activity in tumors: Feasibility study in a mouse model Radiology (Oak Brook, IL, U. S.) 2001 221 523 529
28. S. Ohshima S. Fujimoto A. Petrov H. Nakagami N. Haider J. Zhou N. Tahara M. K. Osako A. Fujimoto J. Zhu T. Murohara D. S. Edwards N. Narula N. D. Wong Y. Chandrashekhar R. Morishita J. Narula Effect of an antimicrobial agent on atherosclerotic plaques: Assessment of metalloproteinase activity by molecular imaging J. Am. Coll. Cardiol. 2010 55 1240 1249
29. F. A. Jaffer P. Libby R. Weissleder Molecular imaging of cardiovascular disease Circulation 2007 116 1052 1061
30. F. A. Jaffer C. H. Tung R. E. Gerszten R. Weissleder In vivo imaging of thrombin activity in experimental thrombi with thrombin-sensitive near-infrared molecular probe Arterioscler., Thromb., Vasc. Biol. 2002 22 1929 1935
31. C. H. Tung R. E. Gerszten F. A. Jaffer R. Weissleder A novel near-infrared fluorescence sensor for detection of thrombin activation in blood ChemBioChem 2002 3 207 211
32. G. Blum G. von Degenfeld M. J. Merchant H. M. Blau M. Bogyo Noninvasive optical imaging of cysteine protease activity using fluorescently quenched activity-based probes Nat. Chem. Biol. 2007 3 668 677
33. M. Whitney J. L. Crisp E. S. Olson T. A. Aguilera L. A. Gross L. G. Ellies R. Y. Tsien Parallel in vivo and in vitro selection using phage display identifies protease-dependent tumor-targeting peptides J. Biol. Chem. 2010 285 22532 22541
34. R. Coleman T. Hayek S. Keidar M. Aviram A mouse model for human atherosclerosis: Long-term histopathological study of lesion development in the aortic arch of apolipoprotein e-deficient (e0) mice Acta Histochem. 2006 108 415 424
35. B. J. Backes J. L. Harris F. Leonetti C. S. Craik J. A. Ellman Synthesis of positional-scanning libraries of fluorogenic peptide substrates to define the extended substrate specificity of plasmin and thrombin Nat. Biotechnol. 2000 18 187 193
36. A. Kuliopulos L. Covic S. K. Seeley P. J. Sheridan J. Helin C. E. Costello Plasmin desensitization of the par1 thrombin receptor: Kinetics, sites of truncation, and implications for thrombolytic therapy Biochemistry 1999 38 4572 4585
37. R. L. Reddick S. H. Zhang N. Maeda Atherosclerosis in mice lacking apo e. Evaluation of lesional development and progression Arterioscler. Thromb. 1994 14 141 147
38. H. C. Stary A. B. Chandler S. Glagov J. R. Guyton W. Insull, Jr. M. E. Rosenfeld S. A. Schaffer C. J. Schwartz W. D. Wagner R. W. Wissler A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the committee on vascular lesions of the council on arteriosclerosis, American heart association Circulation 1994 89 2462 2478
39. G. W. Stone A. Maehara A. J. Lansky B. de Bruyne E. Cristea G. S. Mintz R. Mehran J. McPherson N. Farhat S. P. Marso H. Parise B. Templin R. White Z. Zhang P. W. Serruys A prospective natural-history study of coronary atherosclerosis N. Engl. J. Med. 2011 364 226 235
40. S. Ishibashi J. L. Goldstein M. S. Brown J. Herz D. K. Burns Massive xanthomatosis and atherosclerosis in cholesterol-fed low density lipoprotein receptor-negative mice J. Clin. Invest. 1994 93 1885 1893
41. W. Palinski R. K. Tangirala E. Miller S. G. Young J. L. Witztum Increased autoantibody titers against epitopes of oxidized ldl in ldl receptor-deficient mice with increased atherosclerosis Arterioscler., Thromb., Vasc. Biol. 1995 15 1569 1576
42. J. O. Deguchi M. Aikawa C. H. Tung E. Aikawa D. E. Kim V. Ntziachristos R. Weissleder P. Libby Inflammation in atherosclerosis: Visualizing matrix metalloproteinase action in macrophages in vivo Circulation 2006 114 55 62
43. S. Ohshima A. Petrov S. Fujimoto J. Zhou M. Azure D. S. Edwards T. Murohara N. Narula S. Tsimikas J. Narula Molecular imaging of matrix metalloproteinase expression in atherosclerotic plaques of mice deficient in apolipoprotein e or low-density-lipoprotein receptor J. Nucl. Med. 2009 50 612 617
44. F. L. Silver A. Mackey W. M. Clark W. Brooks C. H. Timaran D. Chiu L. B. Goldstein J. F. Meschia R. D. Ferguson W. S. Moore G. Howard T. G. Brott Safety of stenting and endarterectomy by symptomatic status in the carotid revascularization endarterectomy versus stenting trial (crest) Stroke 2011 42 675 680
45. G. M. van Dam G. Themelis L. M. Crane N. J. Harlaar R. G. Pleijhuis W. Kelder A. Sarantopoulos J. S. de Jong H. J. Arts A. G. van der Zee J. Bart P. S. Low V. Ntziachristos Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-alpha targeting: First in-human results Nat. Med. (N. Y.) 2011 17 1315 1319
46. D. Razansky N. Deliolanis C. Vinegoni V. Ntziachristos Deep tissue optical and optoacoustic molecular imaging technologies for small animal research and drug discovery Curr. Pharm. Biotechnol. 2012 13 504 22
47. S. Butenas C. van't Veer K. G. Mann "Normal" thrombin generation Blood 1999 94 2169 2178
48. S. A. Cederholm-Williams Concentration of plasminogen and antiplasmin in plasma and serum J. Clin. Pathol. 1981 34 979 981
49. Q. T. Nguyen E. S. Olson T. A. Aguilera T. Jiang M. Scadeng L. G. Ellies R. Y. Tsien Surgery with molecular fluorescence imaging using activatable cell-penetrating peptides decreases residual cancer and improves survival Proc. Natl. Acad. Sci. U. S. A. 2010 107 4317 4322
50. A. A. Stoop F. Lupu H. Pannekoek Colocalization of thrombin, pai-1, and vitronectin in the atherosclerotic vessel wall: A potential regulatory mechanism of thrombin activity by pai-1/vitronectin complexes Arterioscler., Thromb., Vasc. Biol. 2000 20 1143 1149
51. R. K. Tangirala E. M. Rubin W. Palinski Quantitation of atherosclerosis in murine models: Correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in ldl receptor-deficient and apolipoprotein e-deficient mice J. Lipid Res. 1995 36 2320 2328
52. H. Yoo J. W. Kim M. Shishkov E. Namati T. Morse R. Shubochkin J. R. McCarthy V. Ntziachristos B. E. Bouma F. A. Jaffer G. J. Tearney Nat. Med 2011 17 1680 4