Cardiovascular Division, Brigham and Women s Hospital, Harvard Medical School
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1 Low Endothelial Shear Stress Upregulates Atherogenic and Inflammatory Genes Extremely Early in the Natural History of Coronary Artery Disease in Diabetic Hyperlipidemic Juvenile Swine Michail I. Papafaklis, Konstantinos C. Koskinas, Aaron B. Baker, Yiannis S. Chatzizisis, Ahmet U. Coskun, Joseph W. Franses, Saeko Takahashi, Elazer R. Edelman, Peter H. Stone, Charles L. Feldman Cardiovascular Division, Brigham and Women s Hospital, Harvard Medical School Harvard-MIT Division of Health Sciences, Massachusetts Institute of Technology
2 Disclosure Statement Conflicts of Interest Nothing to disclose
3 The Local Hemodynamic Environment is a Critical Factor in the Natural History of Atherosclerosis Although atherosclerosis is a systemic disease, its distribution is multifocal and heterogeneous Malek, et al. JAMA 1999;282: Local hemodynamic factors exhibit remarkable heterogeneity over short distances and are responsible for the heterogeneity in the spatial distribution of atherosclerotic lesions Understanding the molecular mechanisms related to initiation of atherosclerosis and the individual natural history of early lesions in vivo will allow for identification of areas at highest risk and selective preemptive therapy to reduce adverse cardiac events Papafaklis MI, et al. Curr Opin Cardiol 2010;25:627-38
4 Endothelial Shear Stress (ESS) Exerts a Multifactorial Influence on the Arterial Wall In vitro studies demonstrated that ESS determines regional cell phenotypes promoting atherosclerosis susceptibility or atherosclerosis protection García-Cardeña G, et al. Ann N Y Acad Sci 2001;947:1-6 Davies PF. Nat Clin Pract Cardiovasc Med 2009; 6:16-26 The presence of disturbed flow (low/oscillatory ESS) tips the balance of gene expression towards atherosclerosis susceptibility Hajra L, et al. Proc Natl Acad Sci USA 2000;97: In vitro experiments (cell cultures) are limited by the artificial application of flow conditions without accounting for the complex nature of the arterial environment Available in vivo studies primarily in mouse aortas are limited by the large differences in ESS levels compared to humans Suo J, et al. Arterioscler Thromb Vasc Biol 2007;27: The in vivo effect of local ESS on the cellular mechanisms responsible for coronary atherosclerosis initiation and early lesion formation has not been studied
5 Study Objectives To investigate the in vivo role of local ESS early in the natural history of coronary atherosclerosis, and assess the molecular mechanisms that link low ESS with the formation of early lesions, utilizing a pig model of human-like atherosclerosis To test the hypothesis that low ESS in vivo Upregulates pro-inflammatory and pro-atherogenic signaling pathways Augments the expression of leukocyte adhesion molecules and chemokines Promotes the uptake and catabolism of oxidized LDL reinforcing a pro-inflammatory vicious cycle
6 Methods: Study Protocol 4 Male Yorkshire Swine (Age: 3 months old) 11 coronary arteries Week 0 Week 4 Baseline Week 8 Follow-up Induction of Diabetes (IV streptozotocin) Initiation of High-fat Diet In Vivo Vascular Profiling Coronary Angiography, IVUS & Computational Fluid Dynamics Sacrifice Molecular Biology Analyses & Histopathology
7 Methods: Vascular Profiling for Serial, In Vivo Measurement of Local ESS and Wall Morphology Coronary Angiography Intravascular Ultrasound Coronary Blood Flow Acquisition of Image Data 3D Reconstruction of Lumen and EEM Generation of Grid for Computational Fluid Dynamics Determination of Velocity Vectors and Shear Stress Numerical Computation Stone PH, et al. Circulation 2003;108:
8 Circumference Circumference Methods: Identification of Arterial Segments in the Harvested Coronary Arteries Low Low High Baseline ESS Follow-up ESS 0 o 180 o 360 o 0 o 180 o Side branch Side branches [Pa] 3-mm segments of interest were identified: Baseline Low ESS ( 1.2 Pa; n=21) Baseline Higher ESS (>1.2 Pa; n=24) 360 o Side branch Side branches Axial Length [mm] Side branches were identified on the arteries harvested at follow-up The exact location of each segment of interest was identified on the preserved coronary arteries
9 Methods Molecular Biology & Histopathologic Analyses GENE EXPRESSION mrna was isolated from the intima and media of cryosections of the arterial segments Real Time RT-PCR for mrna expression of: Transcription Factors: NFκB1, KLF-2 Leukocyte Adhesion Molecules: ICAM-1, VCAM-1 Chemokines and Molecules Related to the Inflammatory Pathway: MCP-1, HMOX-1 Oxidized LDL Uptake and Catabolism: OxLDL receptor (LOX-1), Lp-PLA 2 HISTOPATHOLOGY MCP-1 Immunofluorescence for chemokine protein expression CD45 Immunostaining/Immunofluorescence for inflammatory cells
10 Results: Endothelial Shear Stress Regulates Critical Signaling Pathways Nuclear Factor kappa B1 LOW ESS Krüppel-like Factor-2 Induces Inflammatory Processes Downregulates Atheroprotection ATHEROGENESIS Atherogenesis Atheroprotection
11 Results: Low ESS Upregulates the Expression of Intercellular Adhesion Molecule-1 Upregulation of ICAM-1 leads to increased adhesion of inflammatory cells on the endothelial surface VCAM-1: vascular cell adhesion molecule-1
12 Results: Dose-Response Relationship Between ESS Magnitude and MCP-1 Gene Expression Expression of Monocyte Chemoattractant Protein-1 leads to increased monocyte penetration into the intima MCP-1 mrna= Ln(ESS) r =0.63 p<0.01 MCP-1
13 Results: Augmented MCP-1 Protein Expression in Regions Exposed to Low ESS MCP-1 Low ESS Lumen Higher ESS Lumen CD45 Lumen Media Intima MCP-1 Intima Media Lumen Intima Intima merge Lumen Media CD45 Media Lumen Media Intima Co-localization of MCP-1 expression with dense inflammatory infiltration Media Intima merge Minimal MCP-1 expression and reduced inflammatory infiltration
14 Results: Low ESS is Associated with Early Upregulation of LOX-1 and Lp-PLA 2 Lectin-like Oxidized LDL receptor-1 LOX-1 OxLDL binding, internalization and degradation in ECs Promotes EC activation Lp-PLA 2 Cleaves the oxidized PC to lysopc & oxidized free fatty acids Lipoprotein associated Phospholipase A 2 LysoPC: Lyso-PhosphatidylCholine
15 Results: Increased Expression of Heme Oxygenase-1 in Coronary Segments with Low ESS Inflammatory Signaling Related Pathway HMOX-1 is expressed in the lesion as a compensatory mechanism Oxidative Stress HMOX-1
16 Results: Low ESS Regions Exhibit Early Increase in Inflammatory Cell Infiltration CD45 Low ESS CD45 Higher ESS M M M M CD45 CD45 M: media intima-media border (internal elastic lamina)
17 Summary The Effect of Low ESS on Endothelial Cell Processes Drives the Focal Development of Inflammation and Leads to Early Atherosclerotic Lesions Low ESS Up-regulation of pro-inflammatory pathways Down-regulation of atheroprotective pathways Endothelial Cell Activation Increased OxLDL Uptake Increased Leukocyte Adhesion Augmented Leukocyte Penetration Increased OxLDL Catabolism Inflammation Early Lesion Formation
18 Conclusions Coronary regions of low ESS exhibit endothelial activation and inflammatory infiltration extremely early in the natural history of coronary artery disease Low ESS increased the expression of multiple atherogenic molecules within only 8 weeks following diabetes/hypercholesterolemia induction in juvenile swine Augmented expression of leukocyte adhesion molecules and increased leukocyte penetration into the intima co-localizing with dense inflammatory infiltration Increased oxidized LDL uptake and catabolism to pro-inflammatory compounds (i.e., LysoPC and oxidized fatty acids), all of which reinforce endothelial cell activation and the inflammatory response In vivo assessment of local ESS may identify early arterial regions prone to lesion formation and is suitable for surveillance of atherogenesis opportunities for preemptive treatments (local drug delivery?) to reduce the atherosclerotic burden and prevent adverse cardiac events
19 Acknowledgements Brigham and Women s Hospital Harvard Medical School Vascular Profiling Lab Peter H. Stone, MD Charles L. Feldman, ScD Konstantinos C. Koskinas, MD, MSc Yiannis S. Chatzizisis, MD, PhD Saeko Takahashi, MD Antonios A. Antoniadis, MD, PhD Libby Lab Peter Libby, MD Galina K. Sukhova, PhD Harvard-MIT Division of Health Sciences & Technology Edelman Lab Elazer R. Edelman, MD, PhD Aaron B. Baker, PhD Michael Jonas, MD Northeastern University Mechanical and Industrial Engineering Ahmet U. Coskun, PhD University of Washington Charles Maynard, PhD Funding Sources George D. Behrakis Research Fellowship Hellenic Heart Foundation Hellenic Harvard Foundation Boston Scientific Inc. Novartis Pharmaceuticals Inc.
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