Download PDF
Hamostaseologie 2023; 43(05): 348-359
DOI: 10.1055/a-2118-2932
Review Article

Intravital Imaging of Thrombosis Models in Mice

Klytaimnistra Kiouptsi
1   Center for Thrombosis and Hemostasis, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
2   German Center for Cardiovascular Research (DZHK), Partner Site Rhine-Main, Mainz, Germany
,
Martina Casari
1   Center for Thrombosis and Hemostasis, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
,
Jonathan Mandel
1   Center for Thrombosis and Hemostasis, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
,
Zhenling Gao
1   Center for Thrombosis and Hemostasis, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
,
Carsten Deppermann
1   Center for Thrombosis and Hemostasis, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
2   German Center for Cardiovascular Research (DZHK), Partner Site Rhine-Main, Mainz, Germany
› Author Affiliations
› Further Information
Also available at
   Permissions and Reprints

Abstract

Intravital microscopy is a powerful tool to study thrombosis in real time. The kinetics of thrombus formation and progression in vivo is studied after inflicting damage to the endothelium through mechanical, chemical, or laser injury. Mouse models of atherosclerosis are also used to induce thrombus formation. Vessels of different sizes and from different vascular beds such as carotid artery or vena cava, mesenteric or cremaster arterioles, can be targeted. Using fluorescent dyes, antibodies, or reporter mouse strains allows to visualize key cells and factors mediating the thrombotic processes. Here, we review the latest literature on using intravital microscopy to study thrombosis as well as thromboinflammation following transient middle cerebral artery occlusion, infection-induced immunothrombosis, and liver ischemia reperfusion.

Keywords

thrombosis - platelet - microscopy - intravital - mice


Publication History

Received: 02 May 2023

Accepted: 04 July 2023

Article published online:
19 October 2023

© 2023. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Massberg S, Gawaz M, Grüner S. et al. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med 2003; 197 (01) 41-49
    CrossrefPubMedSearch in Google Scholar
  • 2 Reinhardt C, von Brühl ML, Manukyan D. et al. Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J Clin Invest 2008; 118 (03) 1110-1122
    PubMedSearch in Google Scholar
  • 3 Savage B, Almus-Jacobs F, Ruggeri ZM. Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell 1998; 94 (05) 657-666
    CrossrefPubMedSearch in Google Scholar
  • 4 Jäckel S, Kiouptsi K, Lillich M. et al. Gut microbiota regulate hepatic von Willebrand factor synthesis and arterial thrombus formation via Toll-like receptor-2. Blood 2017; 130 (04) 542-553
    CrossrefPubMedSearch in Google Scholar
  • 5 Tseng MT, Dozier A, Haribabu B, Graham UM. Transendothelial migration of ferric ion in FeCl3 injured murine common carotid artery. Thromb Res 2006; 118 (02) 275-280
    CrossrefPubMedSearch in Google Scholar
  • 6 Eckly A, Hechler B, Freund M. et al. Mechanisms underlying FeCl3-induced arterial thrombosis. J Thromb Haemost 2011; 9 (04) 779-789
    CrossrefPubMedSearch in Google Scholar
  • 7 Woollard KJ, Sturgeon S, Chin-Dusting JP, Salem HH, Jackson SP. Erythrocyte hemolysis and hemoglobin oxidation promote ferric chloride-induced vascular injury. J Biol Chem 2009; 284 (19) 13110-13118
    CrossrefPubMedSearch in Google Scholar
  • 8 Bender M, Hagedorn I, Nieswandt B. Genetic and antibody-induced glycoprotein VI deficiency equally protects mice from mechanically and FeCl(3) -induced thrombosis. J Thromb Haemost 2011; 9 (07) 1423-1426
    CrossrefPubMedSearch in Google Scholar
  • 9 Konstantinides S, Ware J, Marchese P, Almus-Jacobs F, Loskutoff DJ, Ruggeri ZM. Distinct antithrombotic consequences of platelet glycoprotein Ibalpha and VI deficiency in a mouse model of arterial thrombosis. J Thromb Haemost 2006; 4 (09) 2014-2021
    CrossrefPubMedSearch in Google Scholar
  • 10 Kuijpers MJ, Gilio K, Reitsma S. et al. Complementary roles of platelets and coagulation in thrombus formation on plaques acutely ruptured by targeted ultrasound treatment: a novel intravital model. J Thromb Haemost 2009; 7 (01) 152-161
    CrossrefPubMedSearch in Google Scholar
  • 11 Kuijpers MJ, Heemskerk JW. Intravital imaging of thrombus formation in small and large mouse arteries: experimentally induced vascular damage and plaque rupture in vivo. Methods Mol Biol 2012; 788: 3-19
    CrossrefPubMedSearch in Google Scholar
  • 12 Koizumi J, Yoshida Y, Nakazawa T, Ooneda G. Experimental studies of ischemic brain edema. I. A new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area. Jpn Stroke J 1986; 8: 1-8
    CrossrefPubMedSearch in Google Scholar
  • 13 Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989; 20 (01) 84-91
    CrossrefPubMedSearch in Google Scholar
  • 14 Braeuninger S, Kleinschnitz C, Nieswandt B, Stoll G. Focal cerebral ischemia. Methods Mol Biol 2012; 788: 29-42
    CrossrefPubMedSearch in Google Scholar
  • 15 Canazza A, Minati L, Boffano C, Parati E, Binks S. Experimental models of brain ischemia: a review of techniques, magnetic resonance imaging, and investigational cell-based therapies. Front Neurol 2014; 5: 19
    CrossrefPubMedSearch in Google Scholar
  • 16 Howells DW, Porritt MJ, Rewell SS. et al. Different strokes for different folks: the rich diversity of animal models of focal cerebral ischemia. J Cereb Blood Flow Metab 2010; 30 (08) 1412-1431
    CrossrefPubMedSearch in Google Scholar
  • 17 Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 1986; 17 (03) 472-476
    CrossrefPubMedSearch in Google Scholar
  • 18 Moran PM, Higgins LS, Cordell B, Moser PC. Age-related learning deficits in transgenic mice expressing the 751-amino acid isoform of human beta-amyloid precursor protein. Proc Natl Acad Sci U S A 1995; 92 (12) 5341-5345
    CrossrefPubMedSearch in Google Scholar
  • 19 Mizuma A, You JS, Yenari MA. Targeting reperfusion injury in the age of mechanical thrombectomy. Stroke 2018; 49 (07) 1796-1802
    CrossrefPubMedSearch in Google Scholar
  • 20 Stoll G, Nieswandt B. Thrombo-inflammation in acute ischaemic stroke - implications for treatment. Nat Rev Neurol 2019; 15 (08) 473-481
    CrossrefPubMedSearch in Google Scholar
  • 21 Nieswandt B, Kleinschnitz C, Stoll G. Ischaemic stroke: a thrombo-inflammatory disease?. J Physiol 2011; 589 (17) 4115-4123
    CrossrefPubMedSearch in Google Scholar
  • 22 Kleinschnitz C, Pozgajova M, Pham M, Bendszus M, Nieswandt B, Stoll G. Targeting platelets in acute experimental stroke: impact of glycoprotein Ib, VI, and IIb/IIIa blockade on infarct size, functional outcome, and intracranial bleeding. Circulation 2007; 115 (17) 2323-2330
    CrossrefPubMedSearch in Google Scholar
  • 23 Deppermann C, Cherpokova D, Nurden P. et al. Gray platelet syndrome and defective thrombo-inflammation in Nbeal2-deficient mice. J Clin Invest 2013; 123 (08) 3331-3342
    CrossrefPubMedSearch in Google Scholar
  • 24 Stegner D, Deppermann C, Kraft P. et al. Munc13-4-mediated secretion is essential for infarct progression but not intracranial hemostasis in acute stroke. J Thromb Haemost 2013; 11 (07) 1430-1433
    CrossrefPubMedSearch in Google Scholar
  • 25 Dong X, Gao J, Zhang CY, Hayworth C, Frank M, Wang Z. Neutrophil membrane-derived nanovesicles alleviate inflammation to protect mouse brain injury from ischemic stroke. ACS Nano 2019; 13 (02) 1272-1283
    PubMedSearch in Google Scholar
  • 26 Mostany R, Portera-Cailliau C. A craniotomy surgery procedure for chronic brain imaging. J Vis Exp 2008; (12) 680
    PubMedSearch in Google Scholar
  • 27 Desilles JP, Loyau S, Syvannarath V. et al. Alteplase reduces downstream microvascular thrombosis and improves the benefit of large artery recanalization in stroke. Stroke 2015; 46 (11) 3241-3248
    CrossrefPubMedSearch in Google Scholar
  • 28 Göb V, Voll MG, Zimmermann L. et al. Infarct growth precedes cerebral thrombosis following experimental stroke in mice. Sci Rep 2021; 11 (01) 22887
    CrossrefPubMedSearch in Google Scholar
  • 29 Ishikawa M, Vowinkel T, Stokes KY. et al. CD40/CD40 ligand signaling in mouse cerebral microvasculature after focal ischemia/reperfusion. Circulation 2005; 111 (13) 1690-1696
    CrossrefPubMedSearch in Google Scholar
  • 30 Bonnard T, Hagemeyer CE. Ferric chloride-induced thrombosis mouse model on carotid artery and mesentery vessel. J Vis Exp 2015; (100) e52838
    PubMedSearch in Google Scholar
  • 31 Zhang Y, Ye J, Hu L. et al. Increased platelet activation and thrombosis in transgenic mice expressing constitutively active P2Y12. J Thromb Haemost 2012; 10 (10) 2149-2157
    CrossrefPubMedSearch in Google Scholar
  • 32 Munnix IC, Strehl A, Kuijpers MJ. et al. The glycoprotein VI-phospholipase Cgamma2 signaling pathway controls thrombus formation induced by collagen and tissue factor in vitro and in vivo. Arterioscler Thromb Vasc Biol 2005; 25 (12) 2673-2678
    CrossrefPubMedSearch in Google Scholar
  • 33 Rybaltowski M, Suzuki Y, Mogami H. et al. In vivo imaging analysis of the interaction between unusually large von Willebrand factor multimers and platelets on the surface of vascular wall. Pflugers Arch 2011; 461 (06) 623-633
    CrossrefPubMedSearch in Google Scholar
  • 34 Leung FW, Su KC, Pique JM, Thiefin G, Passaro Jr E, Guth PH. Superior mesenteric artery is more important than inferior mesenteric artery in maintaining colonic mucosal perfusion and integrity in rats. Dig Dis Sci 1992; 37 (09) 1329-1335
    CrossrefPubMedSearch in Google Scholar
  • 35 Collard CD, Gelman S. Pathophysiology, clinical manifestations, and prevention of ischemia-reperfusion injury. Anesthesiology 2001; 94 (06) 1133-1138
    CrossrefPubMedSearch in Google Scholar
  • 36 Abela CB, Homer-Vanniasinkham S. Clinical implications of ischaemia-reperfusion injury. Pathophysiology 2003; 9 (04) 229-240
    CrossrefPubMedSearch in Google Scholar
  • 37 Parks DA, Granger DN. Contributions of ischemia and reperfusion to mucosal lesion formation. Am J Physiol 1986; 250 (6, Pt 1): G749-G753
    PubMedSearch in Google Scholar
  • 38 Cicalese L, Iyengar A, Subbotin V. et al. Protection afforded by pyruvate during acute rejection of small-bowel allografts is mediated by inhibition of oxygen-free radicals and cytolytic activity (perforin and granzyme-B mRNA expression) in activated leukocytes. Transplant Proc 1997; 29 (1-2): 704
    CrossrefPubMedSearch in Google Scholar
  • 39 Thorburn T, Aali M, Lehmann C. Immune response to systemic inflammation in the intestinal microcirculation. Front Biosci 2018; 23 (04) 782-795
    PubMedSearch in Google Scholar
  • 40 Bayer F, Ascher S, Kiouptsi K, Kittner JM, Stauber RH, Reinhardt C. Colonization with altered Schaedler flora impacts leukocyte adhesion in mesenteric ischemia-reperfusion injury. Microorganisms 2021; 9 (08) 1601
    CrossrefPubMedSearch in Google Scholar
  • 41 Ascher S, Wilms E, Pontarollo G. et al. Gut microbiota restricts NETosis in acute mesenteric ischemia-reperfusion injury. Arterioscler Thromb Vasc Biol 2020; 40 (09) 2279-2292
    CrossrefPubMedSearch in Google Scholar
  • 42 Grover SP, Bendapudi PK, Yang M. et al. Injury measurements improve interpretation of thrombus formation data in the cremaster arteriole laser-induced injury model of thrombosis. J Thromb Haemost 2020; 18 (11) 3078-3085
    CrossrefPubMedSearch in Google Scholar
  • 43 Falati S, Gross P, Merrill-Skoloff G, Furie BC, Furie B. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat Med 2002; 8 (10) 1175-1181
    CrossrefPubMedSearch in Google Scholar
  • 44 Chou J, Mackman N, Merrill-Skoloff G, Pedersen B, Furie BC, Furie B. Hematopoietic cell-derived microparticle tissue factor contributes to fibrin formation during thrombus propagation. Blood 2004; 104 (10) 3190-3197
    CrossrefPubMedSearch in Google Scholar
  • 45 Duan X, Perveen R, Dandamudi A. et al. Pharmacologic targeting of Cdc42 GTPase by a small molecule Cdc42 activity-specific inhibitor prevents platelet activation and thrombosis. Sci Rep 2021; 11 (01) 13170
    CrossrefPubMedSearch in Google Scholar
  • 46 Dubois C, Panicot-Dubois L, Gainor JF, Furie BC, Furie B. Thrombin-initiated platelet activation in vivo is vWF independent during thrombus formation in a laser injury model. J Clin Invest 2007; 117 (04) 953-960
    CrossrefPubMedSearch in Google Scholar
  • 47 Atkinson BT, Jasuja R, Chen VM, Nandivada P, Furie B, Furie BC. Laser-induced endothelial cell activation supports fibrin formation. Blood 2010; 116 (22) 4675-4683
    CrossrefPubMedSearch in Google Scholar
  • 48 Neyman M, Gewirtz J, Poncz M. Analysis of the spatial and temporal characteristics of platelet-delivered factor VIII-based clots. Blood 2008; 112 (04) 1101-1108
    CrossrefPubMedSearch in Google Scholar
  • 49 Mangin P, Yap CL, Nonne C. et al. Thrombin overcomes the thrombosis defect associated with platelet GPVI/FcRgamma deficiency. Blood 2006; 107 (11) 4346-4353
    CrossrefPubMedSearch in Google Scholar
  • 50 Mitrophanov AY, Merrill-Skoloff G, Grover SP. et al. Injury length and arteriole constriction shape clot growth and blood-flow acceleration in a mouse model of thrombosis. Arterioscler Thromb Vasc Biol 2020; 40 (09) 2114-2126
    CrossrefPubMedSearch in Google Scholar
  • 51 Stolla M, Stefanini L, Roden RC. et al. The kinetics of αIIbβ3 activation determines the size and stability of thrombi in mice: implications for antiplatelet therapy. Blood 2011; 117 (03) 1005-1013
    CrossrefPubMedSearch in Google Scholar
  • 52 Gromotowicz-Poplawska A, Flaumenhaft R, Gholami SK. et al. Enhanced thrombotic responses are associated with Striatin deficiency and aldosterone. J Am Heart Assoc 2021; 10 (22) e022975
    CrossrefPubMedSearch in Google Scholar
  • 53 Revollo L, Merrill-Skoloff G, De Ceunynck K. et al. The secreted tyrosine kinase VLK is essential for normal platelet activation and thrombus formation. Blood 2022; 139 (01) 104-117
    CrossrefPubMedSearch in Google Scholar
  • 54 Lutsey PL, Zakai NA. Epidemiology and prevention of venous thromboembolism. Nat Rev Cardiol 2023; 20 (04) 248-262
    Search in Google Scholar
  • 55 López JA, Chen J. Pathophysiology of venous thrombosis. Thromb Res 2009; 123 (Suppl. 04) S30-S34
    CrossrefPubMedSearch in Google Scholar
  • 56 Wang X, Smith PL, Hsu MY, Ogletree ML, Schumacher WA. Murine model of ferric chloride-induced vena cava thrombosis: evidence for effect of potato carboxypeptidase inhibitor. J Thromb Haemost 2006; 4 (02) 403-410
    CrossrefPubMedSearch in Google Scholar
  • 57 Witsch T, Mauler M, Herr N. et al. A novel hollow and perforated flexible wire allows the safe and effective local application of thrombolytic therapy in a mouse model of deep vein thrombosis. J Thromb Thrombolysis 2014; 37 (04) 450-454
    CrossrefPubMedSearch in Google Scholar
  • 58 Esmon CT. Basic mechanisms and pathogenesis of venous thrombosis. Blood Rev 2009; 23 (05) 225-229
    CrossrefPubMedSearch in Google Scholar
  • 59 Payne H, Brill A. Stenosis of the inferior vena cava: a murine model of deep vein thrombosis. J Vis Exp 2017; (130) 56697
    PubMedSearch in Google Scholar
  • 60 Wrobleski SK, Farris DM, Diaz JA, Myers Jr DD, Wakefield TW. Mouse complete stasis model of inferior vena cava thrombosis. J Vis Exp 2011; (52) 2738
    PubMedSearch in Google Scholar
  • 61 Wakefield TW, Strieter RM, Wilke CA. et al. Venous thrombosis-associated inflammation and attenuation with neutralizing antibodies to cytokines and adhesion molecules. Arterioscler Thromb Vasc Biol 1995; 15 (02) 258-268
    CrossrefPubMedSearch in Google Scholar
  • 62 von Brühl ML, Stark K, Steinhart A. et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012; 209 (04) 819-835
    CrossrefPubMedSearch in Google Scholar
  • 63 Mwiza JMN, Lee RH, Paul DS. et al. Both G protein-coupled and immunoreceptor tyrosine-based activation motif receptors mediate venous thrombosis in mice. Blood 2022; 139 (21) 3194-3203
    CrossrefPubMedSearch in Google Scholar
  • 64 Schönfelder T, Jäckel S, Wenzel P. Mouse models of deep vein thrombosis. Gefasschirurgie 2017; 22 (Suppl. 01) 28-33
    CrossrefPubMedSearch in Google Scholar
  • 65 Diaz JA, Obi AT, Myers Jr DD. et al. Critical review of mouse models of venous thrombosis. Arterioscler Thromb Vasc Biol 2012; 32 (03) 556-562
    CrossrefPubMedSearch in Google Scholar
  • 66 Brandt M, Schönfelder T, Schwenk M. et al. Deep vein thrombus formation induced by flow reduction in mice is determined by venous side branches. Clin Hemorheol Microcirc 2014; 56 (02) 145-152
    CrossrefPubMedSearch in Google Scholar
  • 67 Geddings J, Aleman MM, Wolberg A, von Brühl ML, Massberg S, Mackman N. Strengths and weaknesses of a new mouse model of thrombosis induced by inferior vena cava stenosis: communication from the SSC of the ISTH. J Thromb Haemost 2014; 12 (04) 571-573
    CrossrefPubMedSearch in Google Scholar
  • 68 Stark K, Massberg S. Interplay between inflammation and thrombosis in cardiovascular pathology. Nat Rev Cardiol 2021; 18 (09) 666-682
    CrossrefPubMedSearch in Google Scholar
  • 69 Beristain-Covarrubias N, Perez-Toledo M, Thomas MR, Henderson IR, Watson SP, Cunningham AF. Understanding infection-induced thrombosis: lessons learned from animal models. Front Immunol 2019; 10: 2569
    CrossrefPubMedSearch in Google Scholar
  • 70 Hitchcock JR, Cook CN, Bobat S. et al. Inflammation drives thrombosis after Salmonella infection via CLEC-2 on platelets. J Clin Invest 2015; 125 (12) 4429-4446
    CrossrefPubMedSearch in Google Scholar
  • 71 Beristain-Covarrubias N, Perez-Toledo M, Flores-Langarica A. et al. Salmonella-induced thrombi in mice develop asynchronously in the spleen and liver and are not effective bacterial traps. Blood 2019; 133 (06) 600-604
    CrossrefPubMedSearch in Google Scholar
  • 72 Levi M, Ten Cate H. Disseminated intravascular coagulation. N Engl J Med 1999; 341 (08) 586-592
    Search in Google Scholar
  • 73 van der Poll T, Opal SM. Host-pathogen interactions in sepsis. Lancet Infect Dis 2008; 8 (01) 32-43
    Search in Google Scholar
  • 74 van der Poll T, van de Veerdonk FL, Scicluna BP, Netea MG. The immunopathology of sepsis and potential therapeutic targets. Nat Rev Immunol 2017; 17 (07) 407-420
    CrossrefPubMedSearch in Google Scholar
  • 75 Berube BJ, Bubeck Wardenburg J. Staphylococcus aureus α-toxin: nearly a century of intrigue. Toxins (Basel) 2013; 5 (06) 1140-1166
    CrossrefPubMedSearch in Google Scholar
  • 76 Parimon T, Li Z, Bolz DD. et al. Staphylococcus aureus α-hemolysin promotes platelet-neutrophil aggregate formation. J Infect Dis 2013; 208 (05) 761-770
    CrossrefPubMedSearch in Google Scholar
  • 77 Surewaard BGJ, Thanabalasuriar A, Zeng Z. et al. α-Toxin induces platelet aggregation and liver injury during Staphylococcus aureus sepsis. Cell Host Microbe 2018; 24 (02) 271-284.e3
    CrossrefPubMedSearch in Google Scholar
  • 78 Surewaard BGJ, Kubes P. Measurement of bacterial capture and phagosome maturation of Kupffer cells by intravital microscopy. Methods 2017; 128: 12-19
    CrossrefPubMedSearch in Google Scholar
  • 79 Agopian VG, Harlander-Locke MP, Markovic D. et al. Evaluation of early allograft function using the liver graft assessment following transplantation risk score model. JAMA Surg 2018; 153 (05) 436-444
    CrossrefPubMedSearch in Google Scholar
  • 80 Eltzschig HK, Eckle T. Ischemia and reperfusion – from mechanism to translation. Nat Med 2011; 17 (11) 1391-1401
    CrossrefPubMedSearch in Google Scholar
  • 81 Zhai Y, Petrowsky H, Hong JC, Busuttil RW, Kupiec-Weglinski JW. Ischaemia-reperfusion injury in liver transplantation – from bench to bedside. Nat Rev Gastroenterol Hepatol 2013; 10 (02) 79-89
    CrossrefPubMedSearch in Google Scholar
  • 82 Selzner M, Selzner N, Jochum W, Graf R, Clavien P-A. Increased ischemic injury in old mouse liver: an ATP-dependent mechanism. Liver Transpl 2007; 13 (03) 382-390
    CrossrefPubMedSearch in Google Scholar
  • 83 Guan L-Y, Fu PY, Li PD. et al. Mechanisms of hepatic ischemia-reperfusion injury and protective effects of nitric oxide. World J Gastrointest Surg 2014; 6 (07) 122-128
    CrossrefPubMedSearch in Google Scholar
  • 84 Brenner C, Galluzzi L, Kepp O, Kroemer G. Decoding cell death signals in liver inflammation. J Hepatol 2013; 59 (03) 583-594
    CrossrefPubMedSearch in Google Scholar
  • 85 Nakamura K, Kageyama S, Ke B. et al. Sirtuin 1 attenuates inflammation and hepatocellular damage in liver transplant ischemia/Reperfusion: from mouse to human. Liver Transpl 2017; 23 (10) 1282-1293
    CrossrefPubMedSearch in Google Scholar
  • 86 Zhang XJ, Cheng X, Yan ZZ. et al. An ALOX12-12-HETE-GPR31 signaling axis is a key mediator of hepatic ischemia-reperfusion injury. Nat Med 2018; 24 (01) 73-83
    CrossrefPubMedSearch in Google Scholar
  • 87 Li P, He K, Li J, Liu Z, Gong J. The role of Kupffer cells in hepatic diseases. Mol Immunol 2017; 85: 222-229
    CrossrefPubMedSearch in Google Scholar
  • 88 Zhang J, Xu P, Song P. et al. CCL2-CCR2 signaling promotes hepatic ischemia/reperfusion injury. J Surg Res 2016; 202 (02) 352-362
    CrossrefPubMedSearch in Google Scholar
  • 89 Yang X, Liang L, Zong C. et al. Kupffer cells-dependent inflammation in the injured liver increases recruitment of mesenchymal stem cells in aging mice. Oncotarget 2016; 7 (02) 1084-1095
    CrossrefPubMedSearch in Google Scholar
  • 90 Lai X, Gong J, Wang W. et al. Acetyl-3-aminoethyl salicylate ameliorates hepatic ischemia/reperfusion injury and liver graft survival through a high-mobility group box 1/toll-like receptor 4-dependent mechanism. Liver Transpl 2019; 25 (08) 1220-1232
    CrossrefPubMedSearch in Google Scholar
  • 91 de Oliveira THC, Marques PE, Poosti F. et al. Intravital microscopic evaluation of the effects of a CXCR2 antagonist in a model of liver ischemia reperfusion injury in mice. Front Immunol 2018; 8: 1917
    CrossrefPubMedSearch in Google Scholar
  • 92 Faust N, Varas F, Kelly LM, Heck S, Graf T. Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 2000; 96 (02) 719-726
    CrossrefPubMedSearch in Google Scholar
  • 93 Marques PE, Oliveira AG, Chang L, Paula-Neto HA, Menezes GB. Understanding liver immunology using intravital microscopy. J Hepatol 2015; 63 (03) 733-742
    CrossrefPubMedSearch in Google Scholar
  • 94 Cywes R, Packham MA, Tietze L. et al. Role of platelets in hepatic allograft preservation injury in the rat. Hepatology 1993; 18 (03) 635-647
    CrossrefPubMedSearch in Google Scholar
  • 95 Cywes R, Mullen JB, Stratis MA. et al. Prediction of the outcome of transplantation in man by platelet adherence in donor liver allografts. Evidence of the importance of prepreservation injury. Transplantation 1993; 56 (02) 316-323
    CrossrefPubMedSearch in Google Scholar
  • 96 Yadav SS, Howell DN, Steeber DA, Harland RC, Tedder TF, Clavien P-A. P-Selectin mediates reperfusion injury through neutrophil and platelet sequestration in the warm ischemic mouse liver. Hepatology 1999; 29 (05) 1494-1502
    CrossrefPubMedSearch in Google Scholar
  • 97 Khandoga A, Biberthaler P, Messmer K, Krombach F. Platelet-endothelial cell interactions during hepatic ischemia-reperfusion in vivo: a systematic analysis. Microvasc Res 2003; 65 (02) 71-77
    CrossrefPubMedSearch in Google Scholar
  • 98 Tedder TF, Steeber DA, Chen A, Engel P. The selectins: vascular adhesion molecules. FASEB J 1995; 9 (10) 866-873
    CrossrefPubMedSearch in Google Scholar
  • 99 Khandoga A, Biberthaler P, Enders G. et al. P-selectin mediates platelet-endothelial cell interactions and reperfusion injury in the mouse liver in vivo. Shock 2002; 18 (06) 529-535
    CrossrefPubMedSearch in Google Scholar
  • 100 Mende K, Reifart J, Rosentreter D. et al. Targeting platelet migration in the postischemic liver by blocking protease-activated receptor 4. Transplantation 2014; 97 (02) 154-160
    CrossrefPubMedSearch in Google Scholar
  • 101 Khandoga A, Biberthaler P, Enders G. et al. Platelet adhesion mediated by fibrinogen-intercellular adhesion molecule-1 binding induces tissue injury in the postischemic liver in vivo. Transplantation 2002; 74 (05) 681-688
    CrossrefPubMedSearch in Google Scholar
  • 102 Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 2003; 284 (01) G15-G26
    CrossrefPubMedSearch in Google Scholar
  • 103 Gow AJ, Thom SR, Ischiropoulos H. Nitric oxide and peroxynitrite-mediated pulmonary cell death. Am J Physiol 1998; 274 (01) L112-L118
    PubMedSearch in Google Scholar
  • 104 Selzner N, Rudiger H, Graf R, Clavien PA. Protective strategies against ischemic injury of the liver. Gastroenterology 2003; 125 (03) 917-936
    CrossrefPubMedSearch in Google Scholar
  • 105 Vodovotz Y, Kim PK, Bagci EZ. et al. Inflammatory modulation of hepatocyte apoptosis by nitric oxide: in vivo, in vitro, and in silico studies. Curr Mol Med 2004; 4 (07) 753-762
    CrossrefPubMedSearch in Google Scholar
  • 106 Lesurtel M, Graf R, Aleil B. et al. Platelet-derived serotonin mediates liver regeneration. Science 2006; 312 (5770) 104-107
    CrossrefPubMedSearch in Google Scholar
  • 107 Nocito A, Georgiev P, Dahm F. et al. Platelets and platelet-derived serotonin promote tissue repair after normothermic hepatic ischemia in mice. Hepatology 2007; 45 (02) 369-376
    CrossrefPubMedSearch in Google Scholar
  • 108 Zhang H, Goswami J, Varley P. et al. Hepatic surgical stress promotes systemic immunothrombosis that results in distant organ injury. Front Immunol 2020; 11: 987
    CrossrefPubMedSearch in Google Scholar
  • 109 Panteleev MA, Korin N, Reesink KD. et al. Wall shear rates in human and mouse arteries: standardization of hemodynamics for in vitro blood flow assays: communication from the ISTH SSC subcommittee on biorheology. J Thromb Haemost 2021; 19 (02) 588-595
    CrossrefPubMedSearch in Google Scholar
  • 110 Allan-Rahill NH, Lamont MRE, Chilian WM, Nishimura N, Small DM. Intravital microscopy of the beating murine heart to understand cardiac leukocyte dynamics. Front Immunol 2020; 11: 92
    CrossrefPubMedSearch in Google Scholar
  • 111 Kalia N. A historical review of experimental imaging of the beating heart coronary microcirculation in vivo. J Anat 2023; 242 (01) 3-16
    CrossrefPubMedSearch in Google Scholar
  • 112 Mahmoud O, El-Sakka M, Janssen BGH. Two-step machine learning method for the rapid analysis of microvascular flow in intravital video microscopy. Sci Rep 2021; 11 (01) 10047
    CrossrefPubMedSearch in Google Scholar