Specific Targeting of Atherosclerotic Plaques in ApoE−/− Mice Using a New Camelid sdAb Binding the Vulnerable Plaque Marker LOX-1

Molecular Imaging and Biology

Volumn 16, Issue 5, 2014, Pages 690-698

  De Vos, Jens ^a,b   Mathijs, Iris ^a   Xavier, Catarina ^a   Massa, Sam ^a,b   Wernery, Ulrich ^c   Bouwens, Luc ^a   Lahoutte, Tony ^a,d   Muyldermans, Serge ^a,b   Devoogdt, Nick ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c CENTRAL VETERINARY RESEARCH LABORATORY   (United Arab Emirates)

^d UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

Author keywords

Atherosclerosis; Camelid single domain antibody fragment (sdAb); Lectin like oxidized low density lipoprotein receptor (LOX 1); Molecular imaging; Nanobody

Indexed keywords

EID: 84897123834     PISSN: 15361632     EISSN: 18602002     Source Type: Journal    
DOI: 10.1007/s11307-014-0731-6     Document Type: Article

References (39)

1. Langer HF, Haubner R, Pichler BJ, Gawaz M (2008) Radionuclide imaging: a molecular key to the atherosclerotic plaque. J Am Coll Cardiol 52:1–12
2. Joshi NV, Vesey AT, Williams MC et al (2013) F-fluoride positron emission tomography for identification of ruptured and high-risk coronary atherosclerotic plaques: a prospective clinical trial. Lancet 383:705–713
3. Matter CM, Stuber M, Nahrendorf M (2009) Imaging of the unstable plaque: how far have we got? Eur Heart J 30:2566–2574
4. Sinusas AJ, Thomas JD, Mills G (2011) The future of molecular imaging. JACC Cardiovasc Imaging 4:799–806
5. Fleg JL, Stone GW, Fayad ZA et al (2012) Detection of high-risk atherosclerotic plaque: report of the NHLBI Working Group on current status and future directions. JACC Cardiovasc Imaging 5:941–955
6. Sawamura T, Kume N, Aoyama T et al (1997) An endothelial receptor for oxidized low-density lipoprotein. Nature 386:73–77
7. Kataoka H, Kume N, Miyamoto S et al (1999) Expression of lectin like oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation 99:3110–3117
8. Li DY, Chen HJ, Staples ED et al (2002) Oxidized low-density lipoprotein receptor LOX-1 and apoptosis in human atherosclerotic lesions. J Cardiovasc Pharmacol Ther 7:147–153
9. Saito A, Fujimura M, Inoue T et al (2010) Relationship between lectin-like oxidized low-density lipoprotein receptor 1 expression and preoperative echogenic findings of vulnerable carotid plaque. Acta Neurochir (Wien) 152:589–595
10. Ishino S, Mukai T, Kume N et al (2007) Lectin-like oxidized LDL receptor-1 (LOX-1) expression is associated with atherosclerotic plaque instability—analysis in hypercholesterolemic rabbits. Atherosclerosis 195:48–56
11. Chen J, Li D, Schaefer R, Mehta JL (2006) Cross-talk between dyslipidemia and renin-angiotensin system and the role of LOX-1 and MAPK in atherogenesis studies with the combined use of rosuvastatin and candesartan. Atherosclerosis 184:295–301
12. Mehta JL, Sanada N, Hu CP et al (2007) Deletion of LOX-1 reduces atherogenesis in LDLR knockout mice fed high cholesterol diet. Circ Res 100:1634–1642
13. White SJ, Sala-Newby GB, Newby AC (2011) Overexpression of scavenger receptor LOX-1 in endothelial cells promotes atherogenesis in the ApoE(−/−) mouse model. Cardiovasc Pathol 20:369–373
14. Li D, Patel AR, Klibanov AL et al (2010) Molecular imaging of atherosclerotic plaques targeted to oxidized LDL receptor LOX-1 by SPECT/CT and magnetic resonance. Circ Cardiovasc Imaging 3:464–472
15. Ishino S, Mukai T, Kuge Y et al (2008) Targeting of lectin like oxidized low-density lipoprotein receptor 1 (LOX-1) with 99mTc-labeled anti-LOX-1 antibody: potential agent for imaging of vulnerable plaque. J Nucl Med 49:1677–1685
16. Wen S, Liu DF, Cui Y et al (2013) In vivo MRI detection of carotid atherosclerotic lesions and kidney inflammation in ApoE-deficient mice by using LOX-1 targeted iron nanoparticles. Nanomedicine
17. De Vos J, Devoogdt N, Lahoutte T, Muyldermans S (2013) Camelid single-domain antibody-fragment engineering for (pre)clinical in vivo molecular imaging applications: adjusting the bullet to its target. Expert Opin Biol Ther 13:1149–1160
18. Hamers-Casterman C, Atarhouch T, Muyldermans S et al (1993) Naturally occurring antibodies devoid of light chains. Nature 363:446–448
19. Arbabi Ghahroudi M, Desmyter A et al (1997) Selection and identification of single domain antibody fragments from camel heavy-chain antibodies. FEBS Lett 414:521–526
20. Devoogdt N, Xavier C, Hernot S et al (2012) Molecular imaging using nanobodies: a case study. Methods Mol Biol 911:559–567
21. Vaneycken I, D’Huyvetter M, Hernot S et al (2011) Immuno-imaging using nanobodies. Curr Opin Biotechnol 22:877–881
22. Xavier C, Vaneycken I, D'Huyvetter M et al (2013) Synthesis, preclinical validation, dosimetry, and toxicity of 68Ga-NOTA-Anti-HER2 nanobodies for iPET imaging of HER2 receptor expression in cancer. J Nucl Med 54:776–784
23. Gainkam LO, Huang L, Caveliers V et al (2008) Comparison of the biodistribution and tumor targeting of two 99mTc-labeled anti-EGFR nanobodies in mice, using pinhole SPECT/micro-CT. J Nucl Med 49:788–795
24. Oliveira S, van Dongen GA, Stigter-van Walsum M et al (2012) Rapid visualization of human tumor xenografts through optical imaging with a near-infrared fluorescent anti-epidermal growth factor receptor nanobody. Mol Imaging 11:33–46
25. Hernot S, Unnikrishnan S, Du Z et al (2012) Nanobody-coupled microbubbles as novel molecular tracer. J Control Release 158:346–353
26. 99mTc: a practical guide. Methods Mol Biol 911:485–490
27. Broisat A, Hernot S, Toczek J et al (2012) Nanobodies targeting mouse/human VCAM1 for the nuclear imaging of atherosclerotic lesions. Circ Res 110:927–937
28. Conrath KE, Lauwereys M, Galleni M et al (2001) Beta-lactamase inhibitors derived from single-domain antibody fragments elicited in the Camelidae. Antimicrob Agents Chemother 45:2807–2812
29. Vaneycken I, Govaert J, Vincke C et al (2010) In vitro analysis and in vivo tumor targeting of a humanized, grafted nanobody in mice using pinhole SPECT/micro-CT. J Nucl Med 51:1099–1106
30. Nakashima Y, Plump AS, Raines EW et al (1994) ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb 14:133–140
31. Vaneycken I, Devoogdt N, Van Gassen N et al (2011) Preclinical screening of anti-HER2 nanobodies for molecular imaging of breast cancer. FASEB J 25:2433–2446
32. Pirillo A, Norata GD, Catapano AL (2013) LOX-1, OxLDL, and atherosclerosis. Mediators Inflamm 2013:152786
33. Kuge Y, Kume N, Ishino S et al (2008) Prominent lectin-like oxidized low density lipoprotein (LDL) receptor-1 (LOX-1) expression in atherosclerotic lesions is associated with tissue factor expression and apoptosis in hypercholesterolemic rabbits. Biol Pharm Bull 31:1475–1482
34. Smith DD, Tan X, Raveendran VV et al (2012) Mast cell deficiency attenuates progression of atherosclerosis and hepatic steatosis in apolipoprotein E-null mice. Am J Physiol Heart Circ Physiol 302:H2612–H2621
35. Fisker Hag AM, Pedersen SF, Kjaer A (2008) Gene expression of LOX-1, VCAM-1, and ICAM-1 in pre-atherosclerotic mice. Biochem Biophys Res Commun 377:689–693
36. Meir KS, Leitersdorf E (2004) Atherosclerosis in the apolipoprotein-E-deficient mouse: a decade of progress. Arterioscler Thromb Vasc Biol 24:1006–1014
37. Movahedi K, Schoonooghe S, Laoui D et al (2012) Nanobody-based targeting of the macrophage mannose receptor for effective in vivo imaging of tumor-associated macrophages. Cancer Res 72:4165–4177
38. Tchouate Gainkam LO, Caveliers V, Devoogdt N et al (2011) Localization, mechanism and reduction of renal retention of technetium-99m labeled epidermal growth factor receptor-specific nanobody in mice. Contrast Media Mol Imaging 6:85–92
39. Vaneycken I, Xavier C, Blykers A et al (2011) Synthesis and first in vivo evaluation of 18F-anti-HER2-nanobodies: a new probe for PET imaging of HER2 expression in breast cancer. J Nucl Med 52:664–664