Subscribe to RSS
Please copy the URL and add it into your RSS Feed Reader.
https://www.thieme-connect.de/rss/thieme/en/10.1055-s-00035024.xml
Thromb Haemost 2011; 105(05): 802-810
DOI: 10.1160/TH10-11-0735
DOI: 10.1160/TH10-11-0735
Theme Issue Article
Intravital imaging of phagocyte recruitment
Further Information
Publication History
Received:
16 November 2010
Accepted after major revision:
02 March 2011
Publication Date:
28 November 2017 (online)
Summary
Extravasation of neutrophils and monocytes is a hallmark event in acute and chronic inflammation. Owing to recent improvements in optical imaging techniques, the classical leukocyte extravasation cascade has been refined with intermediate steps being added. Further studies have shown tissue specific leukocyte recruitment patterns, thus allowing for more selective targeting. Here we focus on recent advances in intravital imaging of leukocyte recruitment by means of optical imaging techniques and emphasise the translation thereof into tissue-specific recruitment to the lungs, the liver and large arteries.
-
References
- 1 Soehnlein O, Lindbom L. Phagocyte partnership during the onset and resolution of inflammation. Nat Rev Immunol 2010; 10: 427-439.
- 2 Ley K, Laudanna C, Cybulsky MI. et al. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7: 678-689.
- 3 Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994; 76: 301-314.
- 4 Schenkel AR, Mamdouh Z, Muller WA. Locomotion of monocytes on endothelium is a critical step during extravasation. Nat Immunol 2004; 5: 393-400.
- 5 Phillipson M, Heit B, Colarusso P. et al. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J Exp Med 2006; 203: 2569-2575.
- 6 Grommes JM, Soehnlein OMP. Contribution of neutrophils to acute lung injury. Mol Med 2010; 17: 298-307.
- 7 Lee WY, Kubes P. Leukocyte adhesion in the liver: distinct adhesion paradigm from other organs. J Hepatol 2008; 48: 504-512.
- 8 McDonald B, McAvoy EF, Lam F. et al. Interaction of CD44 and hyaluronan is the dominant mechanism for neutrophil sequestration in inflamed liver sinusoids. J Exp Med 2008; 205: 915-927.
- 9 Drechsler M, Megens RT, van Zandvoort M. et al. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation 2010; 122: 1837-1845.
- 10 Voisin MB, Woodfin A, Nourshargh S. Monocytes and neutrophils exhibit both distinct and common mechanisms in penetrating the vascular basement membrane in vivo. Arterioscler Thromb Vasc Biol 2009; 29: 1193-1199.
- 11 Koenen RR, von Hundelshausen P, Nesmelova IV. et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med 2009; 15: 97-103.
- 12 von Hundelshausen P, Koenen RR, Sack M. et al. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005; 105: 924-930.
- 13 Soehnlein O, Zernecke A, Eriksson EE. et al. Neutrophil secretion products pave the way for inflammatory monocytes. Blood 2008; 112: 1461-1471.
- 14 Soehnlein O, Xie X, Ulbrich H. et al. Neutrophil-derived heparin-binding protein (HBP/CAP37) deposited on endothelium enhances monocyte arrest under flow conditions. J Immunol 2005; 174: 6399-6405.
- 15 Hidalgo A, Chang J, Jang JE. et al. Heterotypic interactions enabled by polarized neutrophil microdomains mediate thromboinflammatory injury. Nat Med 2009; 15: 384-391.
- 16 Nourshargh S, Hordijk PL, Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol 2010; 11: 366-378.
- 17 Okada T. Two-photon microscopy analysis of leukocyte trafficking and motility. Semin Immunopathol 2010; 32: 215-225.
- 18 Weissleder R, Pittet MJ. Imaging in the era of molecular oncology. Nature 2008; 452: 580-589.
- 19 Bullen A. Microscopic imaging techniques for drug discovery. Nat Rev Drug Discov 2008; 7: 54-67.
- 20 Khurana M, Moriyama EH, Mariampillai A. et al. Intravital high-resolution optical imaging of individual vessel response to photodynamic treatment. J Biomed Opt 2008; 13: 040502.
- 21 Meissner S, Knels L, Schnabel C. et al. Three-dimensional Fourier domain optical coherence tomography in vivo imaging of alveolar tissue in the intact thorax using the parietal pleura as a window. J Biomed Opt 2010; 15: 016030.
- 22 Sethuraman S, Amirian JH, Litovsky SH. et al. Ex vivo Characterization of Atherosclerosis using Intravascular Photoacoustic Imaging. Opt Express 2007; 15: 16657-16666.
- 23 Wang HW, Langohr IM, Sturek M. et al. Imaging and quantitative analysis of atherosclerotic lesions by CARS-based multimodal nonlinear optical microscopy. Arterioscler Thromb Vasc Biol 2009; 29: 1342-1348.
- 24 Minsky M. Memoir on Inventing the Confocal Scanning Microscope. Scanning 1988; 10: 128-138.
- 25 Brakenhoff GJ, van der Voort HT, van Spronsen EA. et al. Three-dimensional chromatin distribution in neuroblastoma nuclei shown by confocal scanning laser microscopy. Nature 1985; 317: 748-749.
- 26 Nakano A. Spinning-disk confocal microscopy -- a cutting-edge tool for imaging of membrane traffic. Cell Struct Funct 2002; 27: 349-355.
- 27 Masters BR, So PT. Antecedents of two-photon excitation laser scanning microscopy. Microsc Res Tech 2004; 63: 3-11.
- 28 Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science 1990; 248: 73-76.
- 29 Chalfie M, Tu Y, Euskirchen G. et al. Green fluorescent protein as a marker for gene expression. Science 1994; 263: 802-805.
- 30 Konig K, Ehlers A, Riemann I. et al. Clinical two-photon microendoscopy. Microsc Res Tech 2007; 70: 398-402.
- 31 Goetz M, Thomas S, Heimann A. et al. Dynamic in vivo imaging of microvasculature and perfusion by miniaturized confocal laser microscopy. Eur Surg Res 2008; 41: 290-297.
- 32 von Burstin J, Eser S, Seidler B. et al. Highly sensitive detection of early-stage pancreatic cancer by multimodal near-infrared molecular imaging in living mice. Int J Cancer 2008; 123: 2138-2147.
- 33 Laemmel E, Genet M, Le Goualher G. et al. Fibered confocal fluorescence microscopy (Cell-viZio) facilitates extended imaging in the field of microcirculation. A comparison with intravital microscopy. J Vasc Res 2004; 41: 400-411.
- 34 Li X, Yu W. Deep Tissue Microscopic Imaging of the Kidney with a Gradient-Index Lens System. Opt Commun 2008; 281: 1833-1840.
- 35 Tacke F, Alvarez D, Kaplan TJ. et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 2007; 117: 185-194.
- 36 Chiang EY, Hidalgo A, Chang J. et al. Imaging receptor microdomains on leukocyte subsets in live mice. Nat Methods 2007; 4: 219-222.
- 37 Daley JM, Thomay AA, Connolly MD. et al. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 2008; 83: 64-70.
- 38 Kunkel EJ, Chomas JE, Ley K. Role of primary and secondary capture for leukocyte accumulation in vivo. Circ Res 1998; 82: 30-38.
- 39 Eriksson EE. No detectable endothelial- or leukocyte-derived L-selectin ligand activity on the endothelium in inflamed cremaster muscle venules. J Leukoc Biol 2008; 84: 93-103.
- 40 Jayagopal A, Russ PK, Haselton FR. Surface engineering of quantum dots for in vivo vascular imaging. Bioconjug Chem 2007; 18: 1424-1433.
- 41 Ulbrich H, Eriksson EE, Lindbom L. Leukocyte and endothelial cell adhesion molecules as targets for therapeutic interventions in inflammatory disease. Trends Pharmacol Sci 2003; 24: 640-647.
- 42 Friedl P, Weigelin B. Interstitial leukocyte migration and immune function. Nat Immunol 2008; 9: 960-969.
- 43 Khandoga AG, Khandoga A, Reichel CA. et al. In vivo imaging and quantitative analysis of leukocyte directional migration and polarization in inflamed tissue. PLoS One 2009; 4: e4693.
- 44 Mempel TR, Moser C, Hutter J. et al. Visualization of leukocyte transendothelial and interstitial migration using reflected light oblique transillumination in intravital video microscopy. J Vasc Res 2003; 40: 435-441.
- 45 Fiebig E, Ley K, Arfors KE. Rapid leukocyte accumulation by “spontaneous” rolling and adhesion in the exteriorized rabbit mesentery. Int J Microcirc Clin Exp 1991; 10: 127-144.
- 46 Thorlacius H, Raud J, Rosengren-Beezley S. et al. Mast cell activation induces P-selectin-dependent leukocyte rolling and adhesion in postcapillary venules in vivo. Biochem Biophys Res Commun 1994; 203: 1043-1049.
- 47 Harris AG, Costa JJ, Delano FA. et al. Mechanisms of cell injury in rat mesentery and cremaster muscle. Am J Physiol 1998; 274: H1009-1015.
- 48 Vajkoczy P, Menger MD, Simpson E. et al. Angiogenesis and vascularization of murine pancreatic islet isografts. Transplantation 1995; 60: 123-127.
- 49 Vollmar B, Laschke MW, Rohan R. et al. In vivo imaging of physiological angio-genesis from immature to preovulatory ovarian follicles. Am J Pathol 2001; 159: 1661-1670.
- 50 Koehl GE, Gaumann A, Geissler EK. Intravital microscopy of tumor angiogenesis and regression in the dorsal skin fold chamber: mechanistic insights and preclinical testing of therapeutic strategies. Clin Exp Metastasis 2009; 26: 329-344.
- 51 Kenne E, Soehnlein O, Genove G. et al. Immune cell recruitment to inflammatory loci is impaired in mice deficient in basement membrane protein laminin alpha4. J Leukoc Biol 2010; 88: 523-528.
- 52 Rotzius P, Soehnlein O, Kenne E. et al. ApoE(-/-)/lysozyme M(EGFP/EGFP) mice as a versatile model to study monocyte and neutrophil trafficking in atherosclerosis. Atherosclerosis 2009; 202: 111-118.
- 53 Galkina E, Kadl A, Sanders J. et al. Lymphocyte recruitment into the aortic wall be-fore and during development of atherosclerosis is partially L-selectin dependent. J Exp Med 2006; 203: 1273-1282.
- 54 Reutershan J, Basit A, Galkina EV. et al. Sequential recruitment of neutrophils into lung and bronchoalveolar lavage fluid in LPS-induced acute lung injury. Am J Physiol Lung Cell Mol Physiol 2005; 289: L807-815.
- 55 Chtanova T, Schaeffer M, Han SJ. et al. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 2008; 29: 487-496.
- 56 Junt T, Moseman EA, Iannacone M. et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007; 450: 110-114.
- 57 Junt T, Schulze H, Chen Z. et al. Dynamic visualization of thrombopoiesis within bone marrow. Science 2007; 317: 1767-1770.
- 58 Massberg S, Schaerli P, Knezevic-Maramica I. et al. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 2007; 131: 994-1008.
- 59 Swirski FK, Nahrendorf M, Etzrodt M. et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009; 325: 612-616.
- 60 Cahalan MD, Parker I. Choreography of cell motility and interaction dynamics imaged by two-photon microscopy in lymphoid organs. Annu Rev Immunol 2008; 26: 585-626.
- 61 Lo Celso C, Wu JW, Lin CP. In vivo imaging of hematopoietic stem cells and their microenvironment. J Biophotonics 2009; 2: 619-631.
- 62 Doerschuk CM. Mechanisms of leukocyte sequestration in inflamed lungs. Microcirculation 2001; 8: 71-88.
- 63 Burns JA, Issekutz TB, Yagita H. et al. The alpha 4 beta 1 (very late antigen (VLA)-4, CD49d/CD29) and alpha 5 beta 1 (VLA-5, CD49e/CD29) integrins mediate beta 2 (CD11/CD18) integrin-independent neutrophil recruitment to endotoxin-induced lung inflammation. J Immunol 2001; 166: 4644-4649.
- 64 Mulligan MS, Paulson JC, De Frees S. et al. Protective effects of oligosaccharides in P-selectin-dependent lung injury. Nature 1993; 364: 149-151.
- 65 Mizgerd JP, Kubo H, Kutkoski GJ. et al. Neutrophil emigration in the skin, lungs, and peritoneum: different requirements for CD11/CD18 revealed by CD18-deficient mice. J Exp Med 1997; 186: 1357-1364.
- 66 Xu J, Gao XP, Ramchandran R. et al. Nonmuscle myosin light-chain kinase mediates neutrophil transmigration in sepsis-induced lung inflammation by activating beta2 integrins. Nat Immunol 2008; 9: 880-886.
- 67 Razavi HM, Wang le F, Weicker S. et al. Pulmonary neutrophil infiltration in murine sepsis: role of inducible nitric oxide synthase. Am J Respir Crit Care Med 2004; 170: 227-233.
- 68 Tabuchi A, Mertens M, Kuppe H. et al. Intravital microscopy of the murine pulmonary microcirculation. J Appl Physiol 2008; 104: 338-346.
- 69 Short AC, Montoya ML, Gebb SA. et al. Pulmonary capillary diameters and recruitment characteristics in subpleural and interior networks. J Appl Physiol 1996; 80: 1568-1573.
- 70 Looney MR, Thornton EE, Sen D. et al. Stabilized imaging of immune surveillance in the mouse lung. Nat Methods 2011; 8: 91-96.
- 71 Megens RT, Reitsma S, Prinzen L. et al. In vivo high-resolution structural imaging of large arteries in small rodents using two-photon laser scanning microscopy. J Biomed Opt 2010; 15: 011108.
- 72 McCuskey RS, Urbaschek R, McCuskey PA. et al. In vivo microscopic studies of the responses of the liver to endotoxin. Klin Wochenschr 1982; 60: 749-751.
- 73 Clemens M, Zhang J. Regulation of Sinusoidal Perfusion: In Vivo Methodology and Control by Endothelins. Seminars Liver Dis 1999; 19: 383-396.
- 74 Kloek JJ, Levi M, Heger M. et al. Cholestasis enhances liver ischemia/reperfusion-induced coagulation activation in rats. Hepatol Res 2010; 40: 204-215.
- 75 Laschke MW, Dold S, Jeppsson B. et al. Rho-kinase inhibitor attenuates cholestasis-induced CXC chemokine formation, leukocyte recruitment, and hepatocellular damage in the liver. J Surg Res 2010; 159: 666-673.
- 76 Khandoga A, Huettinger S, Khandoga AG. et al. Leukocyte transmigration in inflamed liver: A role for endothelial cell-selective adhesion molecule. J Hepatol 2009; 50: 755-765.
- 77 Caldwell CC, Martignoni A, Leonis MA. et al. Ron receptor tyrosine kinase-dependent hepatic neutrophil recruitment and survival benefit in a murine model of bacterial peritonitis. Crit Care Med 2008; 36: 1585-1593.
- 78 Kubes P, Kerfoot SM. Leukocyte recruitment in the microcirculation: the rolling paradigm revisited. News Physiol Sci 2001; 16: 76-80.
- 79 Thiberge S, Blazquez S, Baldacci P. et al. In vivo imaging of malaria parasites in the murine liver. Nat Protoc 2007; 2: 1811-1818.
- 80 Eriksson E, Boykin JV, Pittman RN. Method for in vivo microscopy of the cutaneous microcirculation of the hairless mouse ear. Microvasc Res 1980; 19: 374-379.
- 81 Kissenpfennig A, Henri S, Dubois B. et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 2005; 22: 643-654.
- 82 Auffray C, Fogg D, Garfa M. et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007; 317: 666-670.
- 83 Peters NC, Egen JG, Secundino N. et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 2008; 321: 970-974.
- 84 Soehnlein O, Weber C. Myeloid cells in atherosclerosis: initiators and decision shapers. Semin Immunopathol 2009; 31: 35-47.
- 85 Weber C, Zernecke A, Libby P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Immunol 2008; 8: 802-815.
- 86 Hansson GK, Libby P, Schonbeck U. et al. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ Res 2002; 91: 281-291.
- 87 Eriksson EE, Xie X, Werr J. et al. Direct viewing of atherosclerosis in vivo: plaque invasion by leukocytes is initiated by the endothelial selectins. Faseb J 2001; 15: 1149-1157.
- 88 Massberg S, Gawaz M, Gruner S. et al. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med 2003; 197: 41-49.
- 89 Lievens D, Zernecke A, Seijkens T. et al. Platelet CD40L mediates thrombotic and inflammatory processes in atherosclerosis. Blood 2010; 116: 4317-4327.
- 90 Lutgens E, Lievens D, Beckers L. et al. Deficient CD40-TRAF6 signaling in leukocytes prevents atherosclerosis by skewing the immune response toward an anti-inflammatory profile. J Exp Med 2010; 207: 391-404.
- 91 Kuijpers MJ, Gilio K, Reitsma S. et al. Complementary roles of platelets and coagulation in thrombus formation on plaques acutely ruptured by targeted ultra-sound treatment: a novel intravital model. J Thromb Haemost 2009; 7: 152-161.
- 92 van Zandvoort M, Engels W, Douma K. et al. Two-photon microscopy for imaging of the (atherosclerotic) vascular wall: a proof of concept study. J Vasc Res 2004; 41: 54-63.
- 93 Maffia P, Zinselmeyer BH, Ialenti A. et al. Images in cardiovascular medicine. Multiphoton microscopy for 3-dimensional imaging of lymphocyte recruitment into apolipoprotein-E-deficient mouse carotid artery. Circulation 2007; 115: e326-328.
- 94 Megens RT, Oude Egbrink MG, Cleutjens JP. et al. Imaging collagen in intact viable healthy and atherosclerotic arteries using fluorescently labeled CNA35 and two-photon laser scanning microscopy. Mol Imaging 2007; 6: 247-260.
- 95 Megens RT, oude Egbrink MG, Merkx M. et al. Two-photon microscopy on vital carotid arteries: imaging the relationship between collagen and inflammatory cells in atherosclerotic plaques. J Biomed Opt 2008; 13: 044022.
- 96 Megens RT, Reitsma S, Schiffers PH. et al. Two-photon microscopy of vital murine elastic and muscular arteries. Combined structural and functional imaging with subcellular resolution. J Vasc Res 2007; 44: 87-98.
- 97 Yu W, Braz JC, Dutton AM. et al. In vivo imaging of atherosclerotic plaques in apolipoprotein E deficient mice using nonlinear microscopy. J Biomed Opt 2007; 12: 054008.
- 98 Fan GY, Fujisaki H, Miyawaki A. et al. Video-rate scanning two-photon excitation fluorescence microscopy and ratio imaging with cameleons. Biophys J 1999; 76: 2412-2420.
- 99 Niesner RA, Andresen V, Gunzer M. Intravital two-photon microscopy: focus on speed and time resolved imaging modalities. Immunol Rev 2008; 221: 7-25.
- 100 Stoletov K, Fang L, Choi SH. et al. Vascular lipid accumulation, lipo-protein oxidation, and macrophage lipid uptake in hypercholesterolemic zebrafish. Circ Res 2009; 104: 952-960.
- 101 Holtta-Vuori M, Salo VT, Nyberg L. et al. Zebrafish: gaining popularity in lipid research. Biochem J 2010; 429: 235-242.
- 102 Miller YI, Choi SH, Fang L. et al. Toll-like receptor-4 and lipo-protein accumulation in macrophages. Trends Cardiovasc Med 2009; 19: 227-232.
- 103 Sasmono RT, Oceandy D, Pollard JW. et al. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 2003; 101: 1155-1163.
- 104 Jung S, Aliberti J, Graemmel P. et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 2000; 20: 4106-4114.
- 105 Faust N, Varas F, Kelly LM. et al. Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 2000; 96: 719-726.
- 106 Boes M, Cerny J, Massol R. et al. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 2002; 418: 983-988.
- 107 Motoike T, Loughna S, Perens E. et al. Universal GFP reporter for the study of vascular development. Genesis 2000; 28: 75-81.
- 108 Lindquist RL, Shakhar G, Dudziak D. et al. Visualizing dendritic cell networks in vivo. Nat Immunol 2004; 5: 1243-1250.
- 109 Passegue E, Wagner EF, Weissman IL. JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell 2004; 119: 431-443.