Glycosaminoglycans as Novel Targets for in vivo Contrast-Enhanced Magnetic Resonance Imaging of Atherosclerosis
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Abstract
Atherosclerosis is an important promoter of cardiovascular disease potentiating myocardial infarction or stroke. Current demand in biomedical imaging necessitates noninvasive characterization of arterial changes responsible for transition of stable plaque into rupture-prone vulnerable plaque. in vivo contrast enhanced magnetic resonance (MR) imaging (MRI) allows quantitative and functional monitoring of pathomorphological changes through signal differences induced by the contrast agent uptake in the diseased vessel wall, therefore it is the ideal modality toward this goal. However, studies have so far focused on the cellular targets of persisting inflammation, leaving extracellular matrix (ECM) far behind. In this review, we portray ECM remodeling during atherosclerotic plaque progression by summarizing the state of the-art in MRI and current imaging targets. Finally, we aim to discuss glycosaminoglycans (GAGs) and their functional interactions, which might offer potential toward development of novel imaging probes for in vivo contrast-enhanced MRI of atherosclerosis.
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Ross R. Atherosclerosis — An Inflammatory Disease. N Engl J Med. 1999; 340: 115–126. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9887164
Benjamin EJ, Muntner P, Alonso A, Bittencourt MS, Callaway CW, et al. Heart disease and stroke statistics-2019 update: a report From the American Heart Association. Circulation. 2019; 139 :526–528. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30700139
Nichols M, Townsend N, Scarborough P, Rayner M. Cardiovascular disease in Europe 2014: epidemiological update. Eur Heart J. 2014; 35: 2950–2959. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25139896
Heidenreich PA, Trogdon JG, Khavjou OA, Butler J, Dracup K, et al. Forecasting the Future of Cardiovascular Disease in the United States: A Policy Statement From the American Heart Association. Circulation. 2011; 123: 933–944. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21262990
Nojiri S, Daida H. Atherosclerotic Cardiovascular Risk in Japan. Jpn Clin Med [Internet]. 2017; 8. PubMed: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5480958/
Pozo E, Agudo-Quilez P, Rojas-González A, Alvarado T, Olivera MJ, et al. Noninvasive diagnosis of vulnerable coronary plaque. World J Cardiol. 2016; 8: 520–533. PubMed: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5039354/
Tarkin JM, Dweck MR, Evans NR, Takx RA, Brown AJ, et al. Imaging atherosclerosis. Circ Res. 2016; 118: 750–769. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26892971
Skinner MP, Yuan C, Mitsumori L, Hayes CE, M.p.s EWR, Nelson JA, et al. Serial magnetic resonance imaging of experimental atherosclerosis detects lesion fine structure, progression and complications in vivo. Nat Med. 1995; 1: 69–73. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/7584956
Toussaint J-F, LaMuraglia GM, Southern JF, Fuster V, Kantor HL. Magnetic Resonance Images Lipid, Fibrous, Calcified, Hemorrhagic, and Thrombotic Components of Human Atherosclerosis in vivo. Circulation. 1996; 94: 932–8.
Botnar RM, Stuber M, Kissinger KV, Kim WY, Spuentrup E, et al. Noninvasive Coronary Vessel Wall and Plaque Imaging With Magnetic Resonance Imaging. Circulation. 2000; 102: 2582–2587. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11085960
Fayad ZA, Fuster V. Clinical Imaging of the High-Risk or Vulnerable Atherosclerotic Plaque. Circ Res. 2001; 89: 305–316. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11509446
Tang TY, Muller KH, Graves MJ, Li ZY, Walsh SR, et al. Iron Oxide Particles for Atheroma Imaging. Arterioscler Thromb Vasc Biol. 2009; 29:1001–1008. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19229073
Falk E, Shah PK, Fuster V. Coronary Plaque Disruption. Circulation. 1995; 92: 657–671. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/7634481
Virmani R, Kolodgie FD, Burke AP, Finn AV, Gold HK, N T, et al. Atherosclerotic Plaque Progression and Vulnerability to Rupture.
Hansson GK. Inflammation, Atherosclerosis, and Coronary Artery Disease. N Engl J Med. 2005; 352: 1685–1695. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15843671
Libby P, DiCarli M, Weissleder R. The Vascular Biology of Atherosclerosis and Imaging Targets. J Nucl Med. 2010; 51(Supplement 1): 335-375. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20395349
Rudd JHF, Hyafil F, Fayad ZA. Inflammation Imaging in Atherosclerosis. Arterioscler Thromb Vasc Biol. 2009; 29: 1009–1016.
Reimann C, Brangsch J, Colletini F, Walter T, Hamm B, Botnar RM, et al. Molecular imaging of the extracellular matrix in the context of atherosclerosis. Adv Drug Deliv Rev. 2017; 113:49–60. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27639968
Virmani R, Burke AP, Farb A, Kolodgie FD. Pathology of the Vulnerable Plaque. J Am Coll Cardiol. 2006; 47(8 Supplement): C13–18. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16631505
Järveläinen H, Sainio A, Koulu M, Wight TN, Penttinen R. Extracellular Matrix Molecules: Potential Targets in Pharmacotherapy. Pharmacol Rev. 2009; 61:198–223. PubMed: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2830117/s
Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol. 2005; 23: 47–55. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15637621
Grobner T. Gadolinium – a specific trigger for the development of nephrogenic fibrosing dermopathy and nephrogenic systemic fibrosis? Nephrol Dial Transplant. 2006; 21: 1104–1108. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16431890
George S j., Webb S m., Abraham J l., Cramer S p. Synchrotron X-ray analyses demonstrate phosphate-bound gadolinium in skin in nephrogenic systemic fibrosis. Br J Dermatol. 2010; 163: 1077–1081. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20560953
Laurent S, Vander Elst L, Henoumont C, Muller RN. How to measure the transmetallation of a gadolinium complex. Contrast Media Mol Imaging. 2010; 5: 305–308. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20803503
Taupitz M, Stolzenburg N, Ebert M, Schnorr J, Hauptmann R, Kratz H, et al. Gadolinium-containing magnetic resonance contrast media: investigation on the possible transchelation of Gd 3+ to the glycosaminoglycan heparin: GdCM, Glycosaminoglycans and Transchelation. Contrast Media Mol Imaging. 2013; 8:108–116. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23281283
Narula J, Virmani R, Iskandrian AE. Strategic targeting of atherosclerotic lesions. J Nucl Cardiol. 1999; 6: 81–90. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10070844
Chatzizisis YS, Coskun AU, Jonas M, Edelman ER, Feldman CL, et al. Role of Endothelial Shear Stress in the Natural History of Coronary Atherosclerosis and Vascular Remodeling: Molecular, Cellular, and Vascular Behavior. J Am Coll Cardiol. 2007; 49: 2379–2393. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17599600
Gimbrone MA, Topper JN, Nagel T, Anderson KR, Garcia-Cardeña G. Endothelial Dysfunction, Hemodynamic Forces, and Atherogenesisa. Ann N Y Acad Sci. 2000; 902: 230–240. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10865843
Navab M, Ananthramaiah GM, Reddy ST, Van Lenten BJ, Ansell BJ, et al. The Pathogenesis of Atherosclerosis-The oxidation hypothesis of atherogenesis: the role of oxidized phospholipids and HDL. J Lipid Res. 2004; 45: 993–1007. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15060092
Blankenberg S, Barbaux S, Tiret L. Adhesion molecules and atherosclerosis. Atherosclerosis. 2003; 170: 191–203. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/14612198
Winter PM, Morawski AM, Caruthers SD, Fuhrhop RW, Zhang H, et al. Molecular Imaging of Angiogenesis in Early-Stage Atherosclerosis With αvβ3-Integrin–Targeted Nanoparticles. Circulation. 2003; 108: 2270–2274. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/14557370
Galkina E, Ley K. Vascular Adhesion Molecules in Atherosclerosis. Arterioscler Thromb Vasc Biol. 2007; 27: 2292–2301. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17673705
Kelly KA, Allport JR, Tsourkas A, Shinde-Patil VR, Josephson L, et al. Detection of Vascular Adhesion Molecule-1 Expression Using a Novel Multimodal Nanoparticle. Circ Res. 2005; 96: 327–336. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15653572
Nahrendorf M, Jaffer FA, Kelly KA, Sosnovik DE, Aikawa E, et al. Noninvasive Vascular Cell Adhesion Molecule-1 Imaging Identifies Inflammatory Activation of Cells in Atherosclerosis. Circulation. 2006; 114: 1504–1511. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17000904
Briley-Saebo KC, Shaw PX, Mulder WJM, Choi S-H, Vucic E, et al. Targeted Molecular Probes for Imaging Atherosclerotic Lesions With Magnetic Resonance Using Antibodies That Recognize Oxidation-Specific Epitopes. Circulation. 2008; 117: 3206–3215. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18541740
McAteer MA, Schneider JE, Ali ZA, Warrick 1 Nicholas, Bursill CA, et al. Magnetic Resonance Imaging of Endothelial Adhesion Molecules in Mouse Atherosclerosis Using Dual-Targeted Microparticles of Iron Oxide. Arterioscler Thromb Vasc Biol. 2008 Jan;28(1):77–83. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17962629
Kwon HM, Sangiorgi G, Ritman EL, McKenna C, Holmes DR, et al. Enhanced coronary vasa vasorum neovascularization in experimental hypercholesterolemia. J Clin Invest. 1998; 101: 1551–1556. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9541483
Libby P. Inflammation in atherosclerosis. Nature. 2002; 420: 868–874.
Amirbekian V, Lipinski MJ, Briley-Saebo KC, Amirbekian S, Aguinaldo JGS, et al. Detecting and assessing macrophages in vivo to evaluate atherosclerosis noninvasively using molecular MRI. Proc Natl Acad Sci. 2007; 104: 961–966. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17215360
Ruehm SG, Corot C, Vogt P, Kolb S, Debatin JF. Magnetic Resonance Imaging of Atherosclerotic Plaque With Ultrasmall Superparamagnetic Particles of Iron Oxide in Hyperlipidemic Rabbits. Circulation. 2001; 103: 415–422. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11157694
Schmitz SA, Taupitz M, Wagner S, Wolf K-J, Beyersdorff D, et al. Magnetic resonance imaging of atherosclerotic plaques using superparamagnetic iron oxide particles. J Magn Reson Imaging. 2001; 14: 355–361. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11599058
Kooi ME, Cappendijk VC, Cleutjens KBJM, Kessels AGH, Kitslaar PJEHM, et al. Accumulation of Ultrasmall Superparamagnetic Particles of Iron Oxide in Human Atherosclerotic Plaques Can Be Detected by in vivo Magnetic Resonance Imaging. Circulation. 2003; 107: 2453–2458. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12719280
Chen J, Tung CH, Mahmood U, Ntziachristos V, Gyurko R, et al. in vivo Imaging of Proteolytic Activity in Atherosclerosis. Circulation. 2002; 105: 2766–2771. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12057992
Deguchi J, Aikawa M, Tung C-H, Aikawa E, Kim D-E, et al. Inflammation in Atherosclerosis: Visualizing Matrix Metalloproteinase Action in Macrophages in vivo. Circulation. 2006 Jul 4;114(1):55–62. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16801460
Shipley JM, Wesselschmidt RL, Kobayashi DK, Ley TJ, Shapiro SD. Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice. Proc Natl Acad Sci. 1996; 93: 3942–3946. PubMed: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC39464/
Hyafil F, Vucic E, Cornily J-C, Sharma R, Amirbekian V, et al. Monitoring of arterial wall remodelling in atherosclerotic rabbits with a magnetic resonance imaging contrast agent binding to matrix metalloproteinases. Eur Heart J. 2011; 32: 1561–1571. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21118852
Helske S, Syväranta S, Lindstedt KA, Lappalainen J, Öörni K, et al. Increased Expression of Elastolytic Cathepsins S, K, and V and Their Inhibitor Cystatin C in Stenotic Aortic Valves. Arterioscler Thromb Vasc Biol. 2006; 26: 1791–1798. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16728655
Majmudar MD, Nahrendorf M. Cardiovascular Molecular Imaging: The Road Ahead. J Nucl Med. 2012; 53: 673–676. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22492729
Lairez O, Fayad ZA. Imaging of atherosclerosis: Can molecular imaging do more? Arch Cardiovasc Dis. 2013; 106: 551–553.
Carlier S, Kakadiaris IA, Dib N, Vavuranakis M, O’Malley SM, et al. Vasa vasorum imaging: A new window to the clinical detection of vulnerable atherosclerotic plaques. Curr Atheroscler Rep. 2005; 7: 164–169. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15727733
Vakonakis I, Campbell ID. Extracellular matrix: from atomic resolution to ultrastructure. Curr Opin Cell Biol. 2007; 19: 578–583. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17942296
Aumailley M, Gayraud B. Structure and biological activity of the extracellular matrix. J Mol Med. 1998; 76: 253–265. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9535559
Katsuda S, Kaji T. Atherosclerosis and Extracellular Matrix. J Atheroscler Thromb. 2003; 10: 267–274. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/14718743
Wight TN, Lara S, Riessen R, Le Baron R, Isner J. Selective deposits of versican in the extracellular matrix of restenotic lesions from human peripheral arteries. Am J Pathol. 1997; 151: 963-973. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9327730
Wight TN, Merrilees MJ. Proteoglycans in Atherosclerosis and Restenosis: Key Roles for Versican. Circ Res. 2004; 94: 1158–1167. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15142969
Matter CM, Schuler PK, Alessi P, Meier P, Ricci R, Zhang D, et al. Molecular Imaging of Atherosclerotic Plaques Using a Human Antibody Against the Extra-Domain B of Fibronectin. Circ Res. 2004; 95: 1225–1233.
Ye F, Jeong E-K, Jia Z, Yang T, Parker D, et al. A Peptide Targeted Contrast Agent Specific to Fibrin-Fibronectin Complexes for Cancer Molecular Imaging with MRI. Bioconjug Chem. 2008; 19: 2300–2303. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19053180
Mayne R. Collagenous proteins of blood vessels. Arterioscler Thromb Vasc Biol. 1986; 6: 585–593.
Brodsky B, Persikov AV. Molecular Structure of the Collagen Triple Helix. Adv Protein Chem. 2005; 70: 301–339. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15837519
Caravan P, Das B, Dumas S, Epstein FH, Helm PA, et al. Collagen-Targeted MRI Contrast Agent for Molecular Imaging of Fibrosis. Angew Chem. 2007; 119: 8319–8321. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17893943
Helm PA, Caravan P, French BA, Jacques V, Shen L, Xu Y, et al. Postinfarction myocardial scarring in mice: molecular MR imaging with use of a collagen-targeting contrast agent. Radiology. 2008; 247: 788–796. PubMed: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5410958/
Jimi S, Sakata N, Matunaga A, Takebayashi S. Low density lipoproteins bind more to type I and III collagens by negative charge-dependent mechanisms than to type IV and V collagens. Atherosclerosis. 1994; 107: 109–116. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/7945553
Khalil MF. Molecular Interactions Leading to Lipoprotein Retention and the Initiation of Atherosclerosis. Arterioscler Thromb Vasc Biol. 2004; 24: 2211–2218. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15472124
Adiguzel E, Ahmad PJ, Franco C, Bendeck MP. Collagens in the progression and complications of atherosclerosis. Vasc Med. 2009; 14: 73–89. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19144782
Chen W, Cormode DP, Vengrenyuk Y, Herranz B, Feig JE, et al. Collagen-Specific Peptide Conjugated HDL Nanoparticles as MRI Contrast Agent to Evaluate Compositional Changes in Atherosclerotic Plaque Regression. JACC Cardiovasc Imaging. 2013; 6: 373–384. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23433925
Spuentrup E, Ruhl KM, Botnar RM, Wiethoff AJ, Buhl A, et al. Molecular Magnetic Resonance Imaging of Myocardial Perfusion With EP-3600, a Collagen-Specific Contrast Agent: Initial Feasibility Study in a Swine Model. Circulation. 2009; 119: 1768–1775. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19307474
Li DY, Brooke B, Davis EC, Mecham RP, Sorensen LK, et al. Elastin is an essential determinant of arterial morphogenesis. Nature. 1998; 393: 276–280. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9607766
Karnik SK, Brooke BS, Bayes-Genis A, Sorensen L, Wythe JD, et al. A critical role for elastin signaling in vascular morphogenesis and disease. Development. 2003; 130: 411–423. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12466207
Kwon GP, Schroeder JL, Amar MJ, Remaley AT, Balaban RS. Contribution of Macromolecular Structure to the Retention of Low-Density Lipoprotein at Arterial Branch Points. Circulation. 2008; 117: 2919–2927. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18506002
Robert L, Robert AM, Jacotot B. Elastin–elastase–atherosclerosis revisited. Atherosclerosis. 1998; 140: 281–295. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9862271
Krettek A, Sukhova GK, Libby P. Elastogenesis in Human Arterial Disease: A Role for Macrophages in Disordered Elastin Synthesis. Arterioscler Thromb Vasc Biol. 2003; 23: 582–587. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12615674
Choudhury Robin P, Valentin F, Badimon Juan J, Fisher Edward A, Fayad Zahi A. MRI and Characterization of Atherosclerotic Plaque. Arterioscler Thromb Vasc Biol. 2002; 22: 1065–1074. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12117718
Makowski MR, Wiethoff AJ, Blume U, Cuello F, Warley A, et al. Assessment of atherosclerotic plaque burden with an elastin-specific magnetic resonance contrast agent. Nat Med. 2011; 17: 383–388. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21336283
Fuster V, Stein B, Ambrose JA, Badimon L, Badimon JJ, et al. Atherosclerotic plaque rupture and thrombosis. Evolving concepts. Circulation. 1990; 82(3 Suppl): II47-1159. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/2203564
La Corte ALC, Philippou H, Ariëns RAS. Role of Fibrin Structure in Thrombosis and Vascular Disease. Adv Protein Chem Struct Biol. 2011; 83: 75–127. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21570666
Tavora F, Cresswell N, Li L, Ripple M, Burke A. Immunolocalisation of fibrin in coronary atherosclerosis: implications for necrotic core development. Pathology (Phila). 2010; 42: 15‑22. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20025475
Botnar RM, Perez AS, Witte S, Wiethoff AJ, Laredo J, et al. in vivo Molecular Imaging of Acute and Subacute Thrombosis Using a Fibrin-Binding Magnetic Resonance Imaging Contrast Agent. Circulation. 2004; 109: 2023–2029. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15066940
Makowski MR, Forbes SC, Blume U, Warley A, Jansen CHP, et al. in vivo assessment of intraplaque and endothelial fibrin in ApoE−/− mice by molecular MRI. Atherosclerosis. 2012; 222: 43–49.
Flacke S, Fischer S, Scott MJ, Fuhrhop RJ, Allen JS, et al. Novel MRI Contrast Agent for Molecular Imaging of Fibrin: Implications for Detecting Vulnerable Plaques. Circulation. 2001; 104: 1280–1285. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11551880
Sirol M, Aguinaldo JGS, Graham PB, Weisskoff R, Lauffer R, et al. Fibrin-targeted contrast agent for improvement of in vivo acute thrombus detection with magnetic resonance imaging. Atherosclerosis. 2005; 182: 79–85. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16115477
Jackson RL, Busch SJ, Cardin AD. Glycosaminoglucans : molecular properties, protein interactions, and role in physiological processes. Physiol Rev. 1991; 71: 481–539. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/2006221
Salisbury BG, Wagner WD. Isolation and preliminary characterization of proteoglycans dissociatively extracted from human aorta. J Biol Chem. 1981; 256: 8050–8057. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/7263639
Berenson GS, Radhakrishnamurthy B, Srinivasan SR, Vijayagopal P, Dalferes ER. Proteoglycans and Potential Mechanisms Related to Atherosclerosisa. Ann N Y Acad Sci. 1985; 454: 69–78. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/3865616
Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J. 2006; 20: 9–22. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16394262
Lindahl U, Hook M. Glycosaminoglycans and their binding to biological macromolecules. Annu Rev Biochem. 1978; 47: 385–417. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/354500
Turnbull J, Powell A, Guimond S. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol. 2001; 11: 75–82. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11166215
Nugent MA. Heparin sequencing brings structure to the function of complex oligosaccharides. Proc Natl Acad Sci. 2000; 97: 10301–10303. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10984527
Evanko SP, Raines EW, Ross R, Gold LI, Wight TN. Proteoglycan distribution in lesions of atherosclerosis depends on lesion severity, structural characteristics, and the proximity of platelet-derived growth factor and transforming growth factor-beta. Am J Pathol. 1998; 152: 533–546. PubMed: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1857967/
Stevens RL, Colombo M, Gonzales JJ, Hollander W, Schmid K. The glycosaminoglycans of the human artery and their changes in atherosclerosis. J Clin Invest. 1976; 58: 470–481. PubMed: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC333202/
Ballinger ML, Nigro J, Frontanilla KV, Dart AM, Little PJ. Regulation of glycosaminoglycan structure and atherogenesis. Cell Mol Life Sci CMLS. 2004; 61: 1296–1306. pubMed: https://www.ncbi.nlm.nih.gov/pubmed/15170508
Kolodgie FD, Burke AP, Farb A, Weber DK, Kutys R, et al. Differential Accumulation of Proteoglycans and Hyaluronan in Culprit Lesions: Insights Into Plaque Erosion. Arterioscler Thromb Vasc Biol. 2002; 22: 1642–1648. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12377743
O'Brien KD, Olin KL, Alpers CE, Chiu W, Ferguson M, et al. Comparison of Apolipoprotein and Proteoglycan Deposits in Human Coronary Atherosclerotic Plaques: Colocalization of Biglycan With Apolipoproteins. Circulation. 1998; 98: 519–527. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9714108
Merrilees MJ, Beaumont B, Scott LJ. Comparison of deposits of versican, biglycan and decorin in saphenous vein and internal thoracic, radial and coronary arteries: correlation to patency. Coron Artery Dis. 2001; 12:7–16. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11211169
Radhakrishnamurthy B, Srinivasan SR, Vijayagopal P, Berenson GS. Arterial wall proteoglycans‑biological properties related to pathogenesis of atherosclerosis. Eur Heart J. 1990; 11: 148‑157. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/2226523
Reitsma S, Slaaf DW, Vink H, van Zandvoort MAMJ, oude Egbrink MGA. The endothelial glycocalyx: composition, functions, and visualization. Pflüg Arch - Eur J Physiol. 2007; 454: 345–59. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17256154
Tarbell JM, Cancel LM. The glycocalyx and its significance in human medicine. J Intern Med. 2016; 280:97–113. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26749537
Selleck SB. Proteoglycans and pattern formation: sugar biochemistry meets developmental genetics. Trends Genet. 2000; 16: 206–212. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10782114
Hileman RE, Fromm JR, Weiler JM, Linhardt RJ. Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays. 1998; 20: 156–167. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9631661
Wight TN. The extracellular matrix and atherosclerosis. Curr Opin Lipidol. 1995; 6: 326.
Scott JE. Structure and function in extracellular matrices depend on interactions between anionic glycosaminoglycans. Elsevier; 2001; 49: 284-289. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11428163
Srinivasan SR, Xu J-H, Vijayagopal P, Radhakrishnamurthy B, Berenson GS. Low-density lipoprotein binding affinity of arterial chondroitin sulfate proteoglycan modulates cholesteryl ester accumulation in macrophages. Atherosclerosis. 1994; 109: 97.
Hurt-Camejo E, Olsson U, Wiklund O, Bondjers G, Camejo G. Cellular Consequences of the Association of ApoB Lipoproteins With Proteoglycans. Arterioscler Thromb Vasc Biol. 1997; 17: 1011–1017. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9194748
Camejo G, Olofsson SO, Lopez F, Carlsson P, Bondjers G. Identification of Apo B-100 segments mediating the interaction of low density lipoproteins with arterial proteoglycans. Arterioscler Thromb Vasc Biol. 1988; 8: 368–377. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/3395272
Skålén K, Gustafsson M, Rydberg EK, Hultén LM, Wiklund O, et al. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature. 2002; 417: 750–754. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12066187
Borén J, Olin K, Lee I, Chait A, Wight TN, et al. Identification of the principal proteoglycan-binding site in LDL. A single-point mutation in apo-B100 severely affects proteoglycan interaction without affecting LDL receptor binding. J Clin Invest. 1998; 101: 2658–2664. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9637699
Imberty A, Lortat-Jacob H, Pérez S. Structural view of glycosaminoglycan–protein interactions. Carbohydr Res. 2007; 342: 430–439. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17229412
Busch C, Dawes J, Pepper DS, Wasteson A. Binding of platelet factor 4 to cultured human umbilical vein endothelial cells. Thromb Res. 1980; 19: 129–137. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/7444850
Stuckey JA, Charles RSt, Edwards BFP. A model of the platelet factor 4 complex with heparin. Proteins Struct Funct Bioinforma. 1992 ; 14: 277–287.
Perollet C, Han ZC, Savona C, Caen JP, Bikfalvi A. Platelet Factor 4 Modulates Fibroblast Growth Factor 2 (FGF-2) Activity and Inhibits FGF-2 Dimerization. Blood. 1998; 91: 3289–3299. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9558385
Petersen F, Brandt E, Lindahl U, Spillmann D. Characterization of a Neutrophil Cell Surface Glycosaminoglycan That Mediates Binding of Platelet Factor 4. J Biol Chem. 1999; 274: 12376–12382. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10212210
Jin L, Abrahams JP, Skinner R, Petitou M, Pike RN, Carrell RW. The anticoagulant activation of antithrombin by heparin. Proc Natl Acad Sci. 1997; 94: 14683–14688. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9405673
Li W, Johnson DJD, Esmon CT, Huntington JA. Structure of the antithrombin–thrombin–heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat Struct Mol Biol. 2004; 11: 857–862. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15311269
Raman R, Venkataraman G, Ernst S, Sasisekharan V, Sasisekharan R. Structural specificity of heparin binding in the fibroblast growth factor family of proteins. Proc Natl Acad Sci. 2003; 100:2357–2362. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12604799
Guerrini M, Agulles T, Bisio A, Hricovini M, Lay L, et al. Minimal Heparin/Heparan Sulfate Sequences for Binding to Fibroblast Growth Factor-1. Biochem Biophys Res Commun. 2002; 292: 222–230. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11890696
Capila I, Linhardt RJ. Heparin–Protein Interactions. Angew Chem Int Ed. 2002; 41: 390–412. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12491369
Desai UR, Petitou M, Björk I, Olson ST. Mechanism of Heparin Activation of Antithrombin Role of Individual Residues of the Pentasaccharide Activating Sequence in the Recognition of Native and Activated States of Antithrombin. J Biol Chem. 1998; 273: 7478–87. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/9516447
Maimone MM, Tollefsen DM. Structure of a dermatan sulfate hexasaccharide that binds to heparin cofactor II with high affinity. J Biol Chem. 1990; 265: 18263–18271. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/2211700
Liaw PCY, Becker DL, Stafford AR, Fredenburgh JC, Weitz JI. Molecular Basis for the Susceptibility of Fibrin-bound Thrombin to Inactivation by Heparin Cofactor II in the Presence of Dermatan Sulfate but Not Heparin. J Biol Chem. 2001; 276: 20959–20965. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11294849
Uca YO, Hallmann D, Hesse B, Seim C, Stolzenburg N, Pietsch H, et al. Microdistribution of Magnetic Resonance Imaging Contrast Agents in Atherosclerotic Plaques Determined by LA-ICP-MS and SR‑µXRF Imaging. Invest Radiol. 2020 Mar 24 (Manuscript submitted for publication)
Collingwood JF, Adams F. Chemical imaging analysis of the brain with X-ray methods. Spectrochim Acta Part B At Spectrosc. 2017; 130: 101–18.
Hare D, Austin C, Doble P. Quantification strategies for elemental imaging of biological samples using laser ablation-inductively coupled plasma- mass spectrometry. Analyst. 2012; 137: 1527–1537. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22314636
Kubaski F, Osago H, Mason RW, Yamaguchi S, Kobayashi H, et al. Glycosaminoglycans detection methods: Applications of mass spectrometry. Mol Genet Metab. 2017; 120: 67–77. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27746032
Caravan P. Strategies for increasing the sensitivity of gadolinium based MRI contrast agents. Chem Soc Rev. 2006; 35: 512-523. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16729145
Ziegler A, Seelig J. Binding and Clustering of Glycosaminoglycans: A Common Property of Mono- and Multivalent Cell-Penetrating Compounds. Biophys J. 2008; 94: 2142–2149. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18065465
Parish CR. The role of heparan sulphate in inflammation. Nat Rev Immunol. 2006; 6: 633–643. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16917509
Li Q, Park PW, Wilson CL, Parks WC. Matrilysin Shedding of Syndecan-1 Regulates Chemokine Mobilization and Transepithelial Efflux of Neutrophils in Acute Lung Injury. Cell. 2002; 111: 635–646. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12464176
Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML, et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 1999; 68: 729–777. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10872465
Handel TM, Johnson Z, Crown SE, Lau EK, Proudfoot AE. Regulation of Protein Function by Glycosaminoglycans—as Exemplified by Chemokines. Annu Rev Biochem. 2005; 74: 385–410. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15952892
Fischer JW, Steitz SA, Johnson PY, Burke A, Kolodgie F, et al. Decorin Promotes Aortic Smooth Muscle Cell Calcification and Colocalizes to Calcified Regions in Human Atherosclerotic Lesions. Arterioscler Thromb Vasc Biol. 2004; 24: 2391–2396. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15472131
McDonald JA. Extracellular matrix assembly. Annu Rev Cell Biol. 1988;4(1):183–207.
Costa DS da, Reis RL, Pashkuleva I. Sulfation of Glycosaminoglycans and Its Implications in Human Health and Disorders. Annu Rev Biomed Eng. 2017; 19: 1–26. PubMed: https://www.ncbi.nlm.Fnih.gov/pubmed/28226217
Thacker BE, Xu D, Lawrence R, Esko JD. Heparan sulfate 3-O-sulfation: A rare modification in search of a function. Matrix Biol. 2014; 35: 60–72. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24361527
Busby TF, Argraves WS, Brew SA, Pechik I, Gilliland GL, et al. Heparin Binding by Fibronectin Module III-13 Involves Six Discontinuous Basic Residues Brought Together to Form a Cationic Cradle. J Biol Chem. 1995; 270: 18558–18562. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/7629186