EXC 1003:  Cells in Motion - CiM: Imaging to Understand Cellular Behaviour in Organisms

Final Report Abstract

Dynamic cellular behaviour determines development, tissue homeostasis and regeneration. Over the past decade, live imaging strategies have revolutionised our perception of cellular behaviour and emphasised their dynamic nature, a topic to which the ‘Cells in Motion – CiM’ Cluster of Excellence has contributed significantly at national and international levels. Based on its broad interdisciplinary expertise CiM has overcome several existing limitations in optical and medical imaging and has deciphered crucial aspects of cellular behaviour in organisms by analysing systems of increasing complexity. Central to the CiM concept has been the use and development of novel imaging strategies to optimise temporal-spatial resolution and specificity. Our vision remains to promote an interfaculty environment boosting basic biomedical sciences and clinical translation and their interaction using imaging as a common strategy to understand cellular behaviour, regardless of whether this is in cells or tissues, in disease models or in patients. To foster knowledge transfer and scientific creativity we have overcome traditional barriers between faculties by establishing seven new interdisciplinary and two new clinical translational professorships, and a unique Cells in Motion Interfaculty Centre (CiMIC), housed in a new building, the Multiscale Imaging Centre (MIC), supported by WWU funding. Integral to our concept has been a new interfaculty educational structure (Careers in Motion Centre) that promotes gender equality and diversity, and includes a novel Master in ‘Experimental Medicine’ allowing medical students to enter into a structured PhD programme. This will continue to promote high quality clinical research and translation of basic science to the clinic. CiM has successfully and uniquely merged excellence at WWU in cell biology and molecular imaging and integrated interdisciplinary networks between the medical, natural sciences and mathematics faculties as well as the Max Planck Institute for Molecular Biomedicine (MPI), documented in several coordinated national and European programmes. The cluster has been a prime example of a new interactive and long-term sustainable structure linking the participating faculties in research and education. CiM has, thereby, changed the research landscape at WWU and has created a unique academic environment that strongly enhances the national and international visibility of WWU in the field of natural sciences and medicine. It will continue to promote excellence in biomedical research in Germany by the establishment of new Collaborative Research Centres and research networks, supported by CiMIC, and exploiting cutting-edge imaging techniques to address fundamental questions in cell biology and their application to diagnostics and therapy.

Link to the final report

https://doi.org/10.2314/KXP:170112324X

Publications

• Bacteria tracking by in vivo magnetic resonance imaging. BMC Biol. 2013; 11: 63
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• Blocking endocytosis enhances short-term synaptic depression under conditions of normal availability of vesicles. Neuron. 2013; 80: 343-349
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• cAMP-induced secretion of endothelial von Willebrand factor is regulated by a phosphorylation/dephosphorylation switch in annexin A2. Blood. 2013; 122: 1042-1051
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• Endothelial TWIK-related potassium channel-1 (TREK1) regulates immune-cell trafficking into the CNS. Nat Med. 2013; 19: 1161-1165
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• FIM, a novel FTIR-based imaging method for high throughput locomotion analysis. PLoS One. 2013; 8: e53963
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• Alarmin S100A8/S100A9 as a biomarker for molecular imaging of local inflammatory activity. Nat Commun. 2014; 5: 4593
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• Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature. 2014; 507: 323-328
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• Ena/VASP Proteins Cooperate with the WAVE Complex to Regulate the Actin Cytoskeleton. Dev Cell. 2014; 30: 569-584
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• Endothelial Notch activity promotes angiogenesis and osteogenesis in bone. Nature. 2014; 507: 376-380
  Ramasamy SK, Kusumbe AP, Wang L, Adams RH
  
• Fusing VE-Cadherin to alpha-Catenin Impairs Fetal Liver Hematopoiesis and Lymph but Not Blood Vessel Formation. Mol Cell Biol. 2014; 34: 1634-1648
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• Large Scale RNAi Reveals the Requirement of Nuclear Envelope Breakdown for Nuclear Import of Human Papillomaviruses. PLoS Pathog. 2014; 10: e1004162
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• Leukocyte extravasation and vascular permeability are each controlled in vivo by different tyrosine residues of VE-cadherin. Nat Immunol. 2014; 15: 223-230
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• Serial F-18-FDG PET/CT distinguishes inflamed from stable plaque phenotypes in shear-stress induced murine atherosclerosis. Atherosclerosis. 2014; 234: 276-282
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• The Drosophila FHOD1-like formin Knittrig acts through Rok to promote stress fiber formation and directed macrophage migration during the cellular immune response. Development. 2014; 141: 1366-1380
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• Total variation regularization in measurement and image space for PET reconstruction. Inverse Probl. 2014; 30: 105003
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• Ultraviolet B light attenuates the systemic immune response in central nervous system autoimmunity. Ann Neurol. 2014; 75: 739-758
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• Viral suppressors of the RIG-I-mediated interferon response are pre-packaged in influenza virions. Nat Commun. 2014; 5: 5645
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• VLA-4 blockade promotes differential routes into human CNS involving PSGL-1 rolling of T cells and MCAM- adhesion of TH17 cells. J Exp Med. 2014; 211: 1833-1846
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• A Bio-Inspired, Catalytic E --> Z Isomerization of Activated Olefins. J Am Chem Soc. 2015; 137: 11254-11257
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• A Dynamic Unfolded Protein Response Contributes to the Control of Cortical Neurogenesis. Developmental Cell. 2015; 35: 553-567
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• Blocking neutrophil diapedesis prevents hemorrhage during thrombocytopenia. J Exp Med. 2015; 212: 1255-1266
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• CD8+ T cell-mediated neuronal dysfunction and degeneration in limbic encephalitis. Front Neurol. 2015; 6: 163
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• Differential phospholipase C-dependent modulation of TASK and TREK two-pore domain K+ channels in rat thalamocortical relay neurons. J Physiol. 2015; 593: 127-144
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• Focal MMP-2 and MMP-9 Activity at the Blood-Brain Barrier Promotes Chemokine-Induced Leukocyte Migration. Cell Rep. 2015; 10: 1040-1054
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• Influence of cell shape, inhomogeneities and diffusion barriers in cell polarization models. Phys Biol. 2015; 12: 066014
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• Interfering with VE-PTP stabilizes endothelial junctions in vivo via Tie-2 in the absence of VE-cadherin. J Exp Med. 2015; 212: 2267-2287
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• JAM-A regulates cortical dynein localization through Cdc42 to control planar spindle orientation during mitosis. Nat Commun. 2015; 6: 8128
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• Multimodal imaging reveals temporal and spatial microglia and matrix metalloproteinase activity after experimental stroke. J Cereb Blood Flow Metab.2015; 35: 1711-1721
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• Optimization of Codon Translation Rates via tRNA Modifications Maintains Proteome Integrity. Cell. 2015; 161: 1606-1618
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• Puzzle Approach to Pose Tracking of a Rigid Object in a Multi Camera System. Lect Notes Comput Sc. 2015; 9256: 337-349
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• The motorized RhoGAP myosin IXb (Myo9b) in leukocytes regulates experimental autoimmune encephalomyelitis induction and recovery. J Neuroimmunol. 2015; 282: 25-32
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• The Triple-Repeat Protein Anakonda Controls Epithelial Tricellular Junction Formation in Drosophila. Dev Cell. 2015; 33: 535-548
  Byri S, Misra T, Syed ZA, Bätz T, Shah J, Boril L, Glashauser J, Aegerter-Wilmsen T, Matzat T, Moussian B, Uv A, Luschnig S
  
• A novel family of fluorescent hypoxia sensors reveal strong heterogeneity in tumor hypoxia at the cellular level. Embo J. 2016; 35: 102-113
  Erapaneedi R, Belousov VV, Schäfers M, Kiefer F
  
• Age-dependent modulation of vascular niches for haematopoietic stem cells. Nature. 2016; 532: 380-384
  Kusumbe AP, Ramasamy SK, Itkin T, Mäe MA, Langen UH, Betsholtz C, Lapidot T, Adams RH
  
• Cannabinoid Receptor 2 Modulates Susceptibility to Experimental Cerebral Malaria through a CCL17-dependent Mechanism. J Biol Chem. 2016; 291: 19517-19531
  Alferink J, Specht S, Arends H, Schumak B, Schmidt K, Ruland C, Lundt R, Kemter A, Dlugos A, Kuepper JM, Poppensieker K, Findeiss M, Albayram O, Otte D-M, Marazzi J, Gertsch J, Forster I, Maier W, Scheu S, Hoerauf A, Zimmer A
  
• Combinatorial effects of doxorubicin and retargeted tissue factor by intratumoral entrapment of doxorubicin and proapoptotic increase of tumor vascular infarction. Oncotarget. 2016; 7: 82458-82472
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• Directed transport of neutrophil-derived extracellular vesicles enables platelet-mediated innate immune response. Nat Commun. 2016; 7: 13464
  Rossaint J, Kühne K, Skupski J, Van Aken H, Looney MR, Hidalgo A, Zarbock A
  
• Equilibrium physics breakdown reveals the active nature of red blood cell flickering. Nat Phys. 2016; 12: 513-519
  Turlier H, Fedosov DA, Audoly B, Auth T, Gov NS, Sykes C, Joanny J-F, Gompper G, Betz T
  
• FGF23 signaling impairs neutrophil recruitment and host defense during CKD. J Clin Invest. 2016; 126: 962-974
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• Fluorinated matrix metalloproteinases inhibitors-Phosphonate based potential probes for positron emission tomography. Bioorg Med Chem. 2016; 24: 902-909
  Beutel B, Daniliuc CG, Riemann B, Schäfers M, Haufe G
  
• Gemcitabine Mechanism of Action Confounds Early Assessment of Treatment Response by 3'-Deoxy-3'-[18F]Fluorothymidine in Preclinical Models of Lung Cancer. Cancer Res. 2016; 76: 7096-7105
  Schelhaas S, Held A, Wachsmuth L, Hermann S, Honess DJ, Heinzmann K, Smith D-M, Griffiths JR, Faber C, Jacobs AH
  
• Imaging by Elemental and Molecular Mass Spectrometry Reveals the Uptake of an Arsenolipid in the Brain of Drosophila melanogaster. Anal Chem. 2016; 88: 5258-5263
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• Imaging matrix metalloproteinase activity in multiple sclerosis as a specific marker of leukocyte penetration of the blood-brain barrier. Sci Transl Med. 2016; 8: 364ra152
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• Impaired NK-mediated regulation of T-cell activity in multiple sclerosis is reconstituted by IL-2 receptor modulation. Proc Natl Acad Sci USA. 2016; 113: E2973-82
  Gross CC, Schulte-Mecklenbeck A, Runzi A, Kuhlmann T, Posevitz-Fejfar A, Schwab N, Schneider-Hohendorf T, Herich S, Held K, Konjevic M, Hartwig M, Dornmair K, Hohlfeld R, Ziemssen T, Klotz L, Meuth SG, Wiendl H
  
• Labeling and Selective Inactivation of Gram-Positive Bacteria Employing Bimodal Photoprobes with Dual Readouts. Chemistry. 2016; 22: 5243-5252
  Galstyan A, Block D, Niemann S, Grüner MC, Abbruzzetti S, Oneto M, Daniliuc CG, Hermann S, Viappiani C, Schäfers M, Löffler B, Strassert CA, Faust A
  
• Melanocortin-1 receptor activation is neuroprotective in mouse models of neuroinflammatory disease. Sci Transl Med. 2016; 8: 362ra146
  Mykicki N, Herrmann AM, Schwab N, Deenen R, Sparwasser T, Limmer A, Wachsmuth L, Klotz L, Köhrer K, Faber C, Wiendl H, Luger TA, Meuth SG, Loser K
  
• Modifying the 5'-Cap for Click Reactions of Eukaryotic mRNA and To Tune Translation Efficiency in Living Cells. Angew Chem Int Ed Engl. 2016; 55: 10899-10903
  Holstein JM, Anhäuser L, Rentmeister A
  
• Protection from septic peritonitis by rapid neutrophil recruitment through omental high endothelial venules. Nat Commun. 2016; 7: 10828
  Buscher K, Wang H, Zhang X, Striewski P, Wirth B, Saggu G, Lütke-Enking S, Mayadas TN, Ley K, Sorokin L, Song J
  
• Repulsive cues combined with physical barriers and cell-cell adhesion determine progenitor cell positioning during organogenesis. Nat Commun. 2016; 7: 11288
  Paksa A, Bandemer J, Hoeckendorf B, Razin N, Tarbashevich K, Minina S, Meyen D, Biundo A, Leidel SA, Peyrieras N, Gov NS, Keller PJ, Raz E
  
• Repulsive Epithelial Cues Direct Glial Migration along the Nerve. Dev Cell. 2016; 39: 696-707
  Sasse S, Klämbt C
  
• Staccato/Unc-13-4 controls secretory lysosome-mediated lumen fusion during epithelial tube anastomosis. Nat Cell Biol. 2016; 18: 727-739
  Caviglia S, Brankatschk M, Fischer EJ, Eaton S, Luschnig S
  
• A central region in the minor capsid protein of papillomaviruses facilitates viral genome tethering and membrane penetration for mitotic nuclear entry. PLoS Pathog. 2017; 13: e1006308
  Aydin I, Villalonga-Planells R, Greune L, Bronnimann MP, Calton CM, Becker M, Lai K-Y, Campos SK, Schmidt MA, Schelhaas M
  
• A Novel Mouse Model of Staphylococcus aureus Vascular Graft Infection: Noninvasive Imaging of Biofilm Development in Vivo. Am J Pathol. 2017; 187: 268-279
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• An Evolutionarily Conserved Role for Polydom/Svep1 During Lymphatic Vessel Formation. Circ Res. 2017; 120: 1263-1275
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• An FIM-Based Long-Term In-Vial Monitoring System for Drosophila Larvae. IEEE Trans Biomed Eng. 2017; 64: 1862-1874
  Berh D, Risse B, Michels T, Otto N, Jiang X, Klämbt C
  
• Bleb Expansion in Migrating Cells Depends on Supply of Membrane from Cell Surface Invaginations. Dev Cell. 2017; 43: 577-587.e5
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• Cell-matrix signals specify bone endothelial cells during developmental osteogenesis. Nat Cell Biol. 2017; 19: 189-201
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• Changing POU dimerization preferences converts Oct6 into a pluripotency inducer. EMBO Rep. 2017; 18: 319-333
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• Combined PET Imaging of the Inflammatory Tumor Microenvironment Identifies Margins of Unique Radiotracer Uptake. Cancer Res. 2017; 77: 1831-1841
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• Dll4 and Notch signalling couples sprouting angiogenesis and artery formation. Nat Cell Biol. 2017; 19: 915-927
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• Endoglin controls blood vessel diameter through endothelial cell shape changes in response to haemodynamic cues. Nat Cell Biol. 2017; 19: 653-665
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• Endothelial basement membrane laminin 511 is essential for shear stress response. EMBO J. 2017; 36: 183-201
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• Endothelial Notch signalling limits angiogenesis via control of artery formation. Nat Cell Biol. 2017; 19: 928-940
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• FIM2c : A Multicolour, Multipurpose Imaging System to Manipulate and Analyse Animal Behaviour. IEEE Trans Biomed Eng. 2017; 64: 610-620
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• FIMTrack: An open source tracking and locomotion analysis software for small animals. PLoS Comput Biol. 2017; 13: e1005530
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• Generic wound signals initiate regeneration in missing-tissue contexts. Nat Commun. 2017; 8: 2282
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• Mutations in KEOPS-complex genes cause nephrotic syndrome with primary microcephaly. Nat Genet. 2017; 49: 1529-1538
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• PAR-1 promotes microtubule breakdown during dendrite pruning in Drosophila. EMBO J. 2017; 36: 1981-1991
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• Polarized actin and VE-cadherin dynamics regulate junctional remodelling and cell migration during sprouting angiogenesis. Nat Commun. 2017; 8 (1): 2210
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• Radiolabeled Selective Matrix Metalloproteinase 13 (MMP-13) Inhibitors: (Radio)Syntheses and in Vitro and First in Vivo Evaluation. J Med Chem. 2017; 60: 307-321
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• Reversible Stabilization of Vesicles: Redox-Responsive Polymer Nanocontainers for Intracellular Delivery. Angew Chem Int Ed Engl. 2017; 56: 9603-9607
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• S100-alarmin-induced innate immune programming protects newborn infants from sepsis. Nat Immunol. 2017; 18: 622-632
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• VGLUT1 functions as a glutamate/proton exchanger with chloride channel activity in hippocampal glutamatergic synapses. Nat Commun. 2017; 8: 2279
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• VIPAR, a quantitative approach to 3D histopathology applied to lymphatic malformations. JCI Insight. 2017; 2
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• Addressable Cholesterol Analogs for Live Imaging of Cellular Membranes. Cell Chem Biol. 2018; 25: 952-961.e12
  Rakers L, Grill D, Matos ALL, Wulff S, Wang D, Börgel J, Körsgen M, Arlinghaus HF, Galla H-J, Gerke V, Glorius F
  
• Autoinhibitory regulation of S100A8/S100A9 alarmin activity locally restricts sterile inflammation. J Clin Invest. 2018; 128: 1852-1866
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• CD99L2 deficiency inhibits leukocyte entry into the central nervous system and ameliorates neuroinflammation. J Leukoc Biol. 2018; 104: 787-797
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• Codon-specific translation reprogramming promotes resistance to targeted therapy. Nature. 2018; 558: 605-609
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• Collective Cell Migration in Embryogenesis Follows the Laws of Wetting. Biophys J. 2018; 114: 213-222
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• Distinct roles of VE‐cadherin for development and maintenance of specific lymph vessel beds. EMBO J. 2018: e98271
  Hägerling R, Hoppe E, Dierkes C, Stehling M, Makinen T, Butz S, Vestweber D, Kiefer F
  
• Enzymatic or In Vivo Installation of Propargyl Groups in Combination with Click Chemistry for the Enrichment and Detection of Methyltransferase Target Sites in RNA. Angew Chem Int Ed Engl. 2018; 57: 6342-6346
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• Harnessing the Maltodextrin Transport Mechanism for Targeted Bacterial Imaging: Structural Requirements for Improved in vivo Stability in Tracer Design. Chem Med Chem. 2018; 13: 241-250
  Axer A, Hermann S, Kehr G, Clases D, Karst U, Fischer-Riepe L, Roth J, Fobker M, Schäfers M, Gilmour R, Faust A
  
• Human T cells in silico: Modelling dynamic intracellular calcium and its influence on cellular electrophysiology. J Immunol Methods. 2018; 461: 78-84
  Eichinger P, Herrmann AM, Ruck T, Herty M, Gola L, Kovac S, Budde T, Meuth SG, Hundehege P
  
• Imaging, myeloid precursor immortalization, and genome editing for defining mechanisms of leukocyte recruitment in vivo. Theranostics. 2018; 8: 2407-2423
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• Lateral plasma membrane compartmentalization links protein function and turnover. Embo J. 2018; 37: e99473
  Busto JV, Elting A, Haase D, Spira F, Kuhlman J, Schäfer-Herte M, Wedlich-Söldner R
  
• Molecular imaging of MMP activity discriminates unstable from stable plaque phenotypes in shear-stress induced murine atherosclerosis. PLoS One. 2018; 13: e0204305
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