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PMID: 16536488 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Development of contrast agents targeted to macrophage scavenger receptors for MRI of vascular inflammation.

Bioconjugate chemistry ·Vol. 17 ·No. 2 ·2006-00-00 ·Pages 538-47

Gustafsson B, Youens S, Louie AY

Abstract

Atherosclerosis is a leading cause of death in the U.S. Because there is a potential to prevent coronary and arterial disease through early diagnosis, there is a need for methods to image arteries in the subclinical stage as well as clinical stage using various noninvasive techniques, including magnetic resonance imaging (MRI). We describe a development of a novel MRI contrast agent targeted to plaques that will allow imaging of lesion formation. The contrast agent is directed to macrophages, one of the earliest components of developing plaques. Macrophages are labeled through the macrophage scavenger receptor A, a macrophage specific cell surface protein, using an MRI contrast agent derived from scavenger receptor ligands. We have synthesized and characterized these contrast agents with a range of relaxivities. In vitro studies show that the targeted contrast agent accumulates in macrophages, and solution studies indicate that micromolar concentrations are sufficient to produce contrast in an MR image. Cell toxicity and initial biodistribution studies indicate low toxicity, no detectable retention in normal blood vessels, and rapid clearance from blood. The promising performance of this contrast agent targeted toward vascular inflammation opens doors to tracking of other inflammatory diseases such as tumor immunotherapy and transplant acceptance using MRI.

MeSH Terms
Animals Atherosclerosis/diagnosis,immunology,pathology Cattle Cell Line Chlorpromazine/metabolism Contrast Media/chemistry,metabolism Humans Macrophages/metabolism Magnetic Resonance Imaging/methods Rats Receptors, Scavenger/metabolism Serum Albumin, Bovine/chemistry,metabolism
Chemicals
Contrast Media Receptors, Scavenger Serum Albumin, Bovine Chlorpromazine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Gustafsson Björn
Department of Biomedical Engineering, University of California, Davis, California 95616, USA.
Youens Susan
Louie Angelique Y
References (80)
80 references, click to expand
  1. Characterization of signal properties in atherosclerotic plaque components by intravascular MRI.
    Arterioscler Thromb Vasc Biol. 2000 Jul;20(7):1824-30 PMID: 10894824
  2. Scavenger receptor classes A and B. Their roles in atherogenesis and the metabolism of modified LDL and HDL.
    Ann N Y Acad Sci. 2000 May;902:113-26; discussion 126-7 PMID: 10865831
  3. MR imaging for the noninvasive assessment of atherothrombotic plaques.
    Magn Reson Imaging Clin N Am. 2003 Feb;11(1):101-13 PMID: 12797513
  4. The role of scavenger receptors in the innate immune system.
    Microbes Infect. 2000 Mar;2(3):305-11 PMID: 10758407
  5. Effects of chlorpromazine with and without UV irradiation on gene expression of HepG2 cells.
    Mutat Res. 2005 Aug 4;575(1-2):47-60 PMID: 15924885
  6. Receptor mediated uptake of a radiolabeled contrast agent sensitive to beta-galactosidase activity.
    Nucl Med Biol. 2003 Apr;30(3):261-5 PMID: 12745017
  7. Binding characteristics of scavenger receptors on liver endothelial and Kupffer cells for modified low-density lipoproteins.
    Biochem J. 1994 Nov 15;304 ( Pt 1):69-73 PMID: 7998959
  8. Class A scavenger receptors, macrophages, and atherosclerosis.
    Curr Opin Lipidol. 2001 Oct;12(5):489-95 PMID: 11561167
  9. Uptake and fate of class B scavenger receptor ligands in HepG2 cells.
    Eur J Biochem. 1999 Apr;261(1):227-35 PMID: 10103054
  10. CD36 and atherosclerosis.
    Curr Opin Lipidol. 2000 Oct;11(5):483-91 PMID: 11048891
  11. Can receptors be imaged with MRI agents?
    Q J Nucl Med. 1997 Jun;41(2):155-62 PMID: 9203854
  12. Gd-DOTA, a potential MRI contrast agent. Current status of physicochemical knowledge.
    Invest Radiol. 1988 Sep;23 Suppl 1:S232-5 PMID: 3198351
  13. The binding of Yb(III) and Gd(III) to bovin serum albumin by a competitive spectrophotometry.
    J Inorg Biochem. 1993 Nov 15;52(3):157-63 PMID: 8254338
  14. CD36, a novel receptor for oxidized low-density lipoproteins, is highly expressed on lipid-laden macrophages in human atherosclerotic aorta.
    Arterioscler Thromb Vasc Biol. 1999 May;19(5):1333-9 PMID: 10323787
  15. The humoral immune response to macrocyclic chelating agent DOTA depends on the carrier molecule.
    J Nucl Med. 2001 Nov;42(11):1697-703 PMID: 11696642
  16. Kinetics of low-density lipoprotein receptor activity in Hep-G2 cells: derivation and validation of a Briggs-Haldane-based kinetic model for evaluating receptor-mediated endocytotic processes in which receptors recycle.
    Biochem J. 1997 May 1;323 ( Pt 3):649-59 PMID: 9169597
  17. Macrophage proliferation in atherosclerosis.
    Curr Opin Lipidol. 2000 Oct;11(5):503-9 PMID: 11048893
  18. Reversible binding of Pi by beef heart mitochondrial adenosine triphosphatase.
    J Biol Chem. 1977 May 10;252(9):2891-9 PMID: 16006
  19. The Gd(3+) complex of a fatty acid analogue of DOTP binds to multiple albumin sites with variable water relaxivities.
    Inorg Chem. 2001 Dec 17;40(26):6580-7 PMID: 11735466
  20. Role of the maleyl-albumin receptor in activation of murine peritoneal macrophages in vitro.
    J Immunol. 1989 Feb 1;142(3):855-62 PMID: 2536414
  21. MR imaging characterization of microvessels in experimental breast tumors by using a particulate contrast agent with histopathologic correlation.
    Radiology. 2001 Feb;218(2):562-9 PMID: 11161179
  22. Enzyme-Activated Gd(3+) Magnetic Resonance Imaging Contrast Agents with a Prominent Receptor-Induced Magnetization Enhancement We thank Dr. Shrikumar Nair for helpful discussions.
    Angew Chem Int Ed Engl. 2001 Aug 3;40(15):2903-2906 PMID: 11500904
  23. Receptor-mediated endocytosis: concepts emerging from the LDL receptor system.
    Annu Rev Cell Biol. 1985;1:1-39 PMID: 2881559
  24. Regional ligand domain is involved in scavenger receptor-mediated recognition of maleyl-albumin by rat sinusoidal liver cells.
    J Mol Recognit. 1989 Sep;2(2):56-62 PMID: 2636897
  25. Biochemical effects of chlorpromazine on mouse neuroblastoma cells.
    Vet Hum Toxicol. 1999 Oct;41(5):273-8 PMID: 10509425
  26. Molecular magnetic resonance imaging with targeted contrast agents.
    J Cell Biochem. 2003 Oct 15;90(3):518-24 PMID: 14523986
  27. Magnetic resonance characterization of tumor microvessels in experimental breast tumors using a slow clearance blood pool contrast agent (carboxymethyldextran-A2-Gd-DOTA) with histopathological correlation.
    Eur Radiol. 2005 Nov;15(11):2268-75 PMID: 16012822
  28. Carotid artery atherosclerotic plaque: clinical and morphological-immunohistochemical correlation.
    Med Sci Monit. 2004 Nov;10(11):CR606-14 PMID: 15507852
  29. Binding characteristics of reduced hepatic receptors for acetylated low-density lipoprotein and maleylated bovine serum albumin.
    Biochem J. 1990 Feb 1;265(3):689-98 PMID: 2154967
  30. Radiometal labeling of immunoproteins: covalent linkage of 2-(4-isothiocyanatobenzyl)diethylenetriaminepentaacetic acid ligands to immunoglobulin.
    Bioconjug Chem. 1990 Jan-Feb;1(1):59-65 PMID: 2095205
  31. O-phthalaldehyde: fluorogenic detection of primary amines in the picomole range. Comparison with fluorescamine and ninhydrin.
    Proc Natl Acad Sci U S A. 1975 Feb;72(2):619-22 PMID: 1054843
  32. Tissue relaxation enhancement after intravenous administration of (ITCB-DTPA)-gadolinum conjugated albumin, an intravascular magnetic resonance imaging contrast agent.
    Invest Radiol. 1991 Jul;26(7):674-80 PMID: 1885276
  33. Modulation of immunogenicity and antigenicity of proteins by maleylation to target scavenger receptors on macrophages.
    J Immunol. 1995 Jan 1;154(1):1-8 PMID: 7527810
  34. Albumin labeled with Gd-DTPA as an intravascular, blood pool-enhancing agent for MR imaging: biodistribution and imaging studies.
    Radiology. 1987 Jan;162(1 Pt 1):205-10 PMID: 3786763
  35. Albumin labeled with Gd-DTPA. An intravascular contrast-enhancing agent for magnetic resonance blood pool imaging: preparation and characterization.
    Invest Radiol. 1987 Aug;22(8):665-71 PMID: 3667174
  36. In vivo molecular imaging of acute and subacute thrombosis using a fibrin-binding magnetic resonance imaging contrast agent.
    Circulation. 2004 Apr 27;109(16):2023-9 PMID: 15066940
  37. Comparison of cell uptake, biodistribution and tumor retention of folate-coated and PEG-coated gadolinium nanoparticles in tumor-bearing mice.
    J Control Release. 2004 Mar 24;95(3):613-26 PMID: 15023471
  38. Manganese toxicity upon overexposure.
    NMR Biomed. 2004 Dec;17(8):544-53 PMID: 15617053
  39. Is the class A macrophage scavenger receptor (SR-A) multifunctional? - The mouse's tale.
    J Clin Invest. 2001 Sep;108(5):649-54 PMID: 11544267
  40. Clinical and angiographic factors associated with asymptomatic restenosis after percutaneous coronary intervention.
    Circulation. 2001 Nov 6;104(19):2289-94 PMID: 11696467
  41. Scavenger receptors for oxidized and glycated proteins.
    Amino Acids. 2003 Dec;25(3-4):283-92 PMID: 14661091
  42. Development of a lipoprotein based molecular imaging MR contrast agent for the noninvasive detection of early atherosclerotic disease.
    Int J Cardiovasc Imaging. 2004 Dec;20(6):561-7 PMID: 15856643
  43. Overexpression of vascular endothelial growth factor 165 drives peritumor interstitial convection and induces lymphatic drain: magnetic resonance imaging, confocal microscopy, and histological tracking of triple-labeled albumin.
    Cancer Res. 2002 Nov 15;62(22):6731-9 PMID: 12438274
  44. Toxicity and carcinogenicity studies of chlorpromazine hydrochloride and p-cresidine in the p53 heterozygous mouse model.
    Toxicol Pathol. 2002 Nov-Dec;30(6):696-704 PMID: 12512871
  45. Atherosclerotic plaque caps are locally weakened when macrophages density is increased.
    Atherosclerosis. 1991 Mar;87(1):87-90 PMID: 1872926
  46. Angiogenesis and the atherosclerotic carotid plaque: an association between symptomatology and plaque morphology.
    J Vasc Surg. 1999 Aug;30(2):261-8 PMID: 10436445
  47. Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits.
    Circulation. 2001 Jan 23;103(3):415-22 PMID: 11157694
  48. Involvement of lysine residues of goat serum albumin in high-affinity binding of bilirubin.
    Biochim Biophys Acta. 1994 Apr 13;1205(2):171-7 PMID: 8155694
  49. Macrophage scavenger receptor class A: A multifunctional receptor in atherosclerosis.
    Arterioscler Thromb Vasc Biol. 2000 Feb;20(2):290-7 PMID: 10669623
  50. Cellular and physiological roles of SR-BI, a lipoprotein receptor which mediates selective lipid uptake.
    Biochim Biophys Acta. 2000 Dec 15;1529(1-3):276-86 PMID: 11111095
  51. Biochemistry and cell biology of mammalian scavenger receptors.
    Atherosclerosis. 2005 Sep;182(1):1-15 PMID: 15904923
  52. Differentiation of binding sites on reconstituted hepatic scavenger receptors using oxidized low-density lipoprotein.
    Biochem J. 1992 Feb 1;281 ( Pt 3):745-51 PMID: 1536652
  53. The processing of ligands by the class A scavenger receptor is dependent on signal information located in the cytoplasmic domain.
    J Biol Chem. 1999 Dec 17;274(51):36808-16 PMID: 10593991
  54. AUR Memorial Award 1991. Immunogenicity of gadolinium-based contrast agents for magnetic resonance imaging. Induction and characterization of antibodies in animals.
    Invest Radiol. 1991 Dec;26(12):1035-40 PMID: 1722486
  55. [14] Maleylation of amino groups.
    Methods Enzymol. 1972;25:191-9 PMID: 23014401
  56. A model for MRI contrast enhancement using T1 agents.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8443-8 PMID: 9671697
  57. Vascular endothelial growth factor enhances atherosclerotic plaque progression.
    Nat Med. 2001 Apr;7(4):425-9 PMID: 11283668
  58. Compartmentalization of a gadolinium complex in the apoferritin cavity: a route to obtain high relaxivity contrast agents for magnetic resonance imaging.
    Angew Chem Int Ed Engl. 2002 Mar 15;41(6):1017-9 PMID: 12491298
  59. Comparison of different types of blood pool agents (P792, MS325, USPIO) in a rabbit MR angiography-like protocol.
    Invest Radiol. 2003 Jun;38(6):311-9 PMID: 12908698
  60. Cohort movement of different ligands and receptors in the intracellular endocytic pathway of alveolar macrophages.
    J Biol Chem. 1989 May 15;264(14):8164-70 PMID: 2470742
  61. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing.
    Cancer Res. 1987 Feb 15;47(4):936-42 PMID: 3802100
  62. Molecular, cellular and functional imaging of atherothrombosis.
    Nat Rev Drug Discov. 2004 Nov;3(11):913-25 PMID: 15520814
  63. Cellular delivery of MRI contrast agents.
    Chem Biol. 2004 Mar;11(3):301-7 PMID: 15123259
  64. Dynamic MRI enhanced with albumin-(Gd-DTPA)30 or ultrasmall superparamagnetic iron oxide particles (NC100150 injection) for the measurement of microvessel permeability in experimental breast tumors.
    Acad Radiol. 2002 May;9 Suppl 1:S112-4 PMID: 12019843
  65. Activated clearance of a biotinylated macromolecular MRI contrast agent from the blood pool using an avidin chase.
    Bioconjug Chem. 2003 Sep-Oct;14(5):1044-7 PMID: 13129410
  66. The pathogenesis of atherosclerosis: a perspective for the 1990s.
    Nature. 1993 Apr 29;362(6423):801-9 PMID: 8479518
  67. Insights into the use of paramagnetic Gd(III) complexes in MR-molecular imaging investigations.
    J Magn Reson Imaging. 2002 Oct;16(4):394-406 PMID: 12353255
  68. Murine macrophage scavenger receptor: in vivo expression and function as receptor for macrophage adhesion in lymphoid and non-lymphoid organs.
    Eur J Immunol. 1995 Feb;25(2):466-73 PMID: 7875210
  69. Fluorescence reaction for amino acids.
    Anal Chem. 1971 Jun;43(7):880-2 PMID: 5576608
  70. Chlorpromazine for schizophrenia: a Cochrane systematic review of 50 years of randomised controlled trials.
    BMC Med. 2005;3:15 PMID: 16229742
  71. Iron-oxide-enhanced magnetic resonance imaging of atherosclerotic plaques: postmortem analysis of accuracy, inter-observer agreement, and pitfalls.
    Invest Radiol. 2002 Jul;37(7):405-11 PMID: 12068163
  72. MRI monitoring of Avastin antiangiogenesis therapy using B22956/1, a new blood pool contrast agent, in an experimental model of human cancer.
    J Magn Reson Imaging. 2004 Nov;20(5):865-73 PMID: 15503324
  73. Molecular magnetic resonance imaging of coronary thrombosis and pulmonary emboli with a novel fibrin-targeted contrast agent.
    Circulation. 2005 Mar 22;111(11):1377-82 PMID: 15738354
  74. Human myeloperoxidase: a potential target for molecular MR imaging in atherosclerosis.
    Magn Reson Med. 2004 Nov;52(5):1021-8 PMID: 15508166
  75. Targeting dendrimer-chelates to tumors and tumor cells expressing the high-affinity folate receptor.
    Invest Radiol. 1997 Dec;32(12):748-54 PMID: 9406015
  76. Heterogeneity in the angiogenic response of a BT474 human breast cancer to a novel vascular endothelial growth factor-receptor tyrosine kinase inhibitor: assessment by voxel analysis of dynamic contrast-enhanced MRI.
    J Magn Reson Imaging. 2005 Oct;22(4):511-9 PMID: 16161072
  77. Gadolinium(III) Chelates as MRI Contrast Agents: Structure, Dynamics, and Applications.
    Chem Rev. 1999 Sep 8;99(9):2293-352 PMID: 11749483
  78. Atherosclerosis imaging using MR imaging: current and emerging applications.
    Magn Reson Imaging Clin N Am. 2005 Feb;13(1):171-80, vii PMID: 15760763
  79. Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP).
    Annu Rev Biochem. 1994;63:601-37 PMID: 7979249
  80. Accumulation of manganese in the brain of mice after intravenous injection of manganese-based contrast agents.
    Chem Res Toxicol. 1997 Apr;10(4):360-3 PMID: 9114970
Article Info
Journal
Bioconjugate chemistry
Abbr.
Bioconjug Chem
ISSN
1043-1802
Published
2006-00-00
Pages
538-47
Language
English
Region
United States
NLM ID
9010319
PMCID
PMC2556229
Subset
IM
Grants
NIBIB NIH HHS · R01 EB000993 · United States
NIBIB NIH HHS · R01 EB000993-01A1 · United States
NIBIB NIH HHS · R01 EB000993-02 · United States
NIBIB NIH HHS · R01 EB000993-03 · United States
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