Developing human tissue engineered arterial constructs to simulate human in vivo thrombus formation

References

• Neubauer K, Zieger B. Endothelial cells and coagulation. Cell Tissue Res. 2022;387:391–7. doi: 10.1007/s00441-021-03471-2.
   PubMed Web of Science ®Google Scholar
• Watson SP. Platelet activation by extracellular matrix proteins in haemostasis and thrombosis. Curr Pharm Des. 2009;15:1358–1372. doi: 10.2174/138161209787846702.
   PubMed Web of Science ®Google Scholar
• Wang L, Miller C, Swarthout RF, Rao M, Mackman N, Taubman MB. Vascular smooth muscle–derived tissue factor is critical for arterial thrombosis after ferric chloride–induced injury. Blood. 2009;113(3):705–713. doi: 10.1182/blood-2007-05-090944.
   PubMed Web of Science ®Google Scholar
• Nesbitt WS, Westein E, Tovar-Lopez FJ. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med. 2009;15:665–673. doi: 10.1038/nm.1955.
   PubMed Web of Science ®Google Scholar
• Westein E, van der Meer AD, Kuijpers MJ, Frimat JP, van den Berg A, Heemskerk JW. Atherosclerotic geometries exacerbate pathological thrombus formation poststenosis in a von Willebrand factor-dependent manner. Proc Natl Acad Sci USA. 2013;110:1357–1362. doi: 10.1073/pnas.1209905110.
   PubMed Web of Science ®Google Scholar
• Westrick RJ, Winn ME, Eitzman DT. Murine models of vascular thrombosis (Eitzman series). Arterioscler Thromb Vasc Biol. 2007;27:2079–2093. doi: 10.1161/ATVBAHA.107.142810.
   PubMed Web of Science ®Google Scholar
• Denis CV, Dubois C, Brass LF, Heemskerk JWM, Lenting PJ. Towards standardization of in vivo thrombosis studies in mice. J Thromb Haemost. 2011;9:1641–1644. doi: 10.1111/j.1538-7836.2011.04350.x.
   PubMed Web of Science ®Google Scholar
• Perlman RL. Mouse models of human disease: an evolutionary perspective. Evol Med Public Heal. 2016;2016:170–176. doi: 10.1093/emph/eow014.
   PubMed Web of Science ®Google Scholar
• Ware J. Dysfunctional platelet membrane receptors: from humans to mice. Thromb Haemost. 2004;92:478–485. doi: 10.1160/TH04-05-0308.
   PubMed Web of Science ®Google Scholar
• Siller-Matula JM, Plasenzotti R, Spiel A, Quehenberger P, Jilma B. Interspecies differences in coagulation profile. Thromb Haemost. 2008;100:397–404. doi: 10.1160/TH08-02-0103.
   PubMed Web of Science ®Google Scholar
• Cooley BC. Murine arterial thrombus induction mechanism influences subsequent thrombodynamics. Thromb Res Elsevier Ltd. 2015;135:939–943. doi: 10.1016/j.thromres.2015.02.016.
   PubMed Web of Science ®Google Scholar
• Hechler B, Nonne C, Eckly A, Magnenat S, Rinckel J-Y, Denis CV, Freund M, Cazenave J-P, Lanza F, Gachet C. Arterial thrombosis: relevance of a model with two levels of severity assessed by histologic, ultrastructural and functional characterization. J Thromb Haemost. 2010;8:173–184. doi: 10.1111/j.1538-7836.2009.03666.x.
   PubMed Web of Science ®Google Scholar
• Whinna HC. Overview of murine thrombosis models. Thromb Res. 2008;122(S1):S64–69. doi: 10.1016/S0049-3848(08)70022-7.
   PubMedGoogle Scholar
• Sashindranath M, Sturgeon SA, French S, Craenmehr DDD, Selan C, Freddi S, Johnson C, Cody SH, Nesbitt WS, Hamilton JR, et al. The mode of anesthesia influences outcome in mouse models of arterial thrombosis. Res Pract Thromb Haemost. 2019;3:197–206. doi:10.1002/rth2.12184.
   PubMed Web of Science ®Google Scholar
• Day SM, Reeve JL, Myers DD, Fay WP. Murine thrombosis models. Thromb Haemost. 2004;92:486–494. doi: 10.1055/s-0037-1613739.
   PubMed Web of Science ®Google Scholar
• Fay W, Eitzman D, Shapiro A, Madison E, Ginsburg D. Platelets inhibit fibrinolysis in vitro by both plasminogen activator inhibitor-1-dependent and -independent mechanisms. Blood. 1999;83:351–356. doi: 10.1182/blood.V83.2.351.351.
   Google Scholar
• Konstantinides S, Schäfer K, Thinnes T, Loskutoff DJ. Plasminogen activator inhibitor-1 and its cofactor vitronectin stabilize arterial thrombi after vascular injury in Mice. Circulation. 2001;103:576–583. doi: 10.1161/01.CIR.103.4.576.
   PubMed Web of Science ®Google Scholar
• Vyas MV, Gros R, Hackam DG. Translation of cardiovascular animal models to human randomized trials. Am J Cardiol. 2020;137:141. doi: 10.1016/j.amjcard.2020.10.027.
   PubMed Web of Science ®Google Scholar
• Rajeeva Pandian NK, Walther BK, Suresh R, Cooke JP, Jain A. Microengineered human vein-chip recreates venous valve architecture and its contribution to thrombosis. Small. 2020;16:e2003401. doi: 10.1002/smll.202003401.
   PubMed Web of Science ®Google Scholar
• Mangin PH, Gardiner EE, Nesbitt WS, Kerrigan SW, Korin N, Lam WA, Panteleev MA. Subcommittee on Biorheology. In vitro flow based systems to study platelet function and thrombus formation: recommendations for standardization: communication from the SSC on Biorheology of the ISTH. J Thromb Haemost. 2020;18:748–752. doi: 10.1111/jth.14717.
   PubMed Web of Science ®Google Scholar
• Pandian NKR, Mannino RG, Lam WA, Jain A. Thrombosis-on-a-chip: prospective impact of microphysiological models of vascular thrombosis. Curr Opin Biomed Eng. 2018;5:29–34. doi: 10.1016/j.cobme.2017.12.001.
   PubMedGoogle Scholar
• Neeves KB, Onasoga AA, Hansen RR, Lilly JJ, Venckunaite D, Sumner MB, Irish AT, Brodsky G, Manco-Johnson MJ, Di Paola JA. Sources of variability in platelet accumulation on type 1 fibrillar collagen in microfluidic flow assays. PLoS One. 2013;8:e54680. doi: 10.1371/journal.pone.0054680.
   PubMed Web of Science ®Google Scholar
• Chen VM, Hogg PJ. Encryption and decryption of tissue factor. J Thromb Haemost. 2013;11 Suppl 1:277–284. doi: 10.1111/jth.12228.
   PubMedGoogle Scholar
• Govindarajan V, Zhu S, Li R, Lu Y, Diamond SL, Reifman J, Mitrophanov AY. Impact of tissue factor localization on blood clot structure and resistance under Venous Shear. Biophys J. 2018;114:978–991. doi: 10.1016/j.bpj.2017.12.034.
   PubMed Web of Science ®Google Scholar
• Mannino RG, Qiu Y, Lam WA. Endothelial cell culture in microfluidic devices for investigating microvascular processes. Biomicrofluidics. 2018;12:042203. doi: 10.1063/1.5024901.
   PubMed Web of Science ®Google Scholar
• Coenen DM, Mastenbroek TG, Cosemans JMEM. Platelet interaction with activated endothelium: mechanistic insights from microfluidics. Blood. 2017;130:2819–2828. doi: 10.1182/blood-2017-04-780825.
   PubMed Web of Science ®Google Scholar
• Costa PF, Albers HJ, Linssen JEA, Middelkamp HHT, van der Hout L, Passier R, van den Berg A, Malda J, van der Meer AD. Mimicking arterial thrombosis in a 3D-printed microfluidic in vitro vascular model based on computed tomography angiography data. Lab Chip. 2017;17:2785–2792. doi: 10.1039/C7LC00202E.
   PubMed Web of Science ®Google Scholar
• Tsai M, Kita A, Leach J, Rounsevell R, Huang JN, Moake J, Ware RE, Fletcher DA, Lam WA. In vitro modeling of the microvascular occlusion and thrombosis that occur in hematologic diseases using microfluidic technology. J Clin Invest. 2012;122:408–418. doi: 10.1172/JCI58753.
   PubMed Web of Science ®Google Scholar
• Mannino RG, Myers DR, Ahn B, Wang Y, Rollins M, Gole H, Lin AS, Guldberg RE, Giddens DP, Timmins LH, et al. Do-it-yourself in vitro vasculature that recapitulates in vivo geometries for investigating endothelial-blood cell interactions. Sci Rep. 2015;5:12401. doi:10.1038/srep12401.
   PubMed Web of Science ®Google Scholar
• Dupuy A, Hagimola L, Mgaieth NSA, Houlahan CB, Preketes-Tardiani RE, Coleman PR, Passam FH. Thromboinflammation model-on-A-chip by whole blood microfluidics on fixed human Endothelium. Diagnostics (Basel). 2021;11:203. doi: 10.3390/diagnostics11020203.
   PubMedGoogle Scholar
• Lundkvist A, Lilleodden E, Siekhaus W, Kinney J, Pruitt L, Balooch M. Viscoelastic properties of healthy human artery measured in saline solution by AFM-based indentation technique. MRS Online Proc Lib. 1996;436:353–358. doi: 10.1557/PROC-436-353.
   Google Scholar
• Mahmoud M, Cancel L, Tarbell JM. Matrix stiffness affects Glycocalyx expression in cultured Endothelial cells. Front Cell Dev Biol. 2021;9:731666. doi: 10.3389/fcell.2021.731666.
   PubMed Web of Science ®Google Scholar
• Huynh J, Nishimura N, Rana K, Peloquin JM, Califano JP, Montague CR, King MR, Schaffer CB, Reinhart-King CA. Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci Transl Med. 2011;3:112ra122. doi: 10.1126/scitranslmed.3002761.
   PubMed Web of Science ®Google Scholar
• Qiu Y, Brown AC, Myers DR, Sakurai Y, Mannino RG, Tran R, Ahn B, Hardy ET, Kee MF, Kumar S, et al. Platelet mechanosensing of substrate stiffness during clot formation mediates adhesion, spreading, and activation. Proc Natl Acad Sci USA. 2014;111:14430–14435. doi: 10.1073/pnas.1322917111.
   PubMed Web of Science ®Google Scholar
• Kee MF, Myers DR, Sakurai Y, Lam WA, Qiu Y. Platelet mechanosensing of collagen matrices. PLoS One. 2015;10:e0126624. doi: 10.1371/journal.pone.0126624.
   PubMed Web of Science ®Google Scholar
• Berry J, Peaudecerf FJ, Masters NA, Neeves KB, Goldstein RE, Harper MT. An “occlusive thrombosis-on-a-chip” microfluidic device for investigating the effect of anti-thrombotic drugs. Lab Chip. 2021;21:4104–4117. doi: 10.1039/D1LC00347J.
   PubMed Web of Science ®Google Scholar
• Devillard CD, Marquette CA. Vascular tissue engineering: challenges and requirements for an ideal large scale blood vessel. Front Bioeng Biotechnol. 2021;9:721843. doi: 10.3389/fbioe.2021.721843.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Chen J, Craven M, Choi NW, Totorica S, Diaz-Santana A, Kermani P, Hempstead B, Fischbach-Teschl C, López JA, et al. In vitro microvessels for the study of angiogenesis and thrombosis. Proc Natl Acad Sci USA. 2012;109:9342–9347. doi: 10.1073/pnas.1201240109.
   PubMed Web of Science ®Google Scholar
• Poventud-Fuentes I, Kwon KW, Seo J, Tomaiuolo M, Stalker TJ, Brass LF, Huh D. A human vascular injury-on-a-chip model of Hemostasis. Small. 2021;17:e2004889. doi: 10.1002/smll.202004889.
   PubMed Web of Science ®Google Scholar
• Menon NV, Tay HM, Wee SN, Li KHH, Hou HW. Micro-engineered perfusable 3D vasculatures for cardiovascular diseases. Lab Chip. 2017;17:2960–2968. doi: 10.1039/C7LC00607A.
   PubMed Web of Science ®Google Scholar
• Hasan A, Paul A, Memic A, Khademhosseini A. A multilayered microfluidic blood vessel-like structure. Biomed Microdevices. 2015;17:88. doi: 10.1007/s10544-015-9993-2.
   PubMed Web of Science ®Google Scholar
• Njoroge W, Hernández ACH, Musa FI, Butler R, Harper AGS, Yang Y. The combination of tissue-engineered blood vessel constructs and parallel flow chamber provides a potential alternative to in vivo drug testing models. Pharmaceutics. 2021;13:340. doi: 10.3390/pharmaceutics13030340.
   PubMed Web of Science ®Google Scholar
• Avendano A, Chang JJ, Cortes-Medina MG, Seibel AJ, Admasu BR, Boutelle CM, Bushman AR, Garg AA, DeShetler CM, Cole SL, et al. Integrated biophysical characterization of Fibrillar Collagen-based hydrogels. ACS Biomater Sci Eng. 2020;6:1408–1417. doi: 10.1021/acsbiomaterials.9b01873.
   PubMed Web of Science ®Google Scholar
• Sarrigiannidis SO, Rey JM, Dobre O, González-García C, Dalby MJ, Salmeron-Sanchez M. A tough act to follow: collagen hydrogel modifications to improve mechanical and growth factor loading capabilities. Mater Today Bio. 2021;10:100098. doi: 10.1016/j.mtbio.2021.100098.
   PubMedGoogle Scholar
• Rickel AP, Deng X, Engebretson D, Hong Z. Electrospun nanofiber scaffold for vascular tissue engineering. Mater Sci Eng C Mater Biol Appl. 2021 Oct;129:112373. doi:10.1016/j.msec.2021.112373.
   PubMed Web of Science ®Google Scholar
• Musa FI, Harper AG, Yang Y. A real-time monitoring system to assess the platelet aggregatory capacity of components of a tissue-engineered blood vessel wall. Tissue Eng Part C Methods. 2016;22:691–699. doi: 10.1089/ten.tec.2015.0582.
   PubMed Web of Science ®Google Scholar
• Chen EP, Toksoy Z, Davis BA, Geibel JP. 3D Bioprinting of vascularized tissues for in vitro and in vivo applications. Front Bioeng Biotechnol. 2021;9:664188. doi: 10.3389/fbioe.2021.664188.
   PubMed Web of Science ®Google Scholar
• Cochrane A, Albers HJ, Passier R, Mummery CL, van den Berg A, Orlova VV, van der Meer AD. Advanced in vitro models of vascular biology: human induced pluripotent stem cells and organ-on-chip technology. Adv Drug Deliv Rev. 2019;140:68–77. doi: 10.1016/j.addr.2018.06.007.
   PubMed Web of Science ®Google Scholar
• Mallone A, Gericke C, Hosseini V, Chahbi K, Haenseler W, Emmert MY, von Eckardstein A, Walther JH, View Vogel V, Weber B, et al. Human induced pluripotent stem cell-derived vessels as dynamic atherosclerosis model on a chip. Biorxiv. doi:10.1101/2020.11.27.401034.
   Google Scholar
• Cai Q, Liao W, Xue F, Wang X, Zhou W, Li Y, Zeng W. Selection of different endothelialization modes and different seed cells for tissue-engineered vascular graft. Bioact Mater. 2021;6:2557–2568. doi: 10.1016/j.bioactmat.2020.12.021.
   PubMed Web of Science ®Google Scholar
• Mathur T, Singh KA, Pandian NKR, Tsai SH, Hein TW, Gaharwar AK, Flanagan JM, Jain A. Organ-on-chips made of blood: endothelial progenitor cells from blood reconstitute vascular thromboinflammation in vessel-chips. Lab Chip. 2019 Jul 23;19:2500–2511. doi:10.1039/C9LC00469F.
   PubMed Web of Science ®Google Scholar
• Greiner AM, Sales A, Chen H, Biela SA, Kaufmann D, Kemkemer R. Nano-and microstructured materials for in vitro studies of the physiology of vascular cells. Beilstein J Nanotechnol. 2016;7:1620–1641. doi: 10.3762/bjnano.7.155.
   PubMed Web of Science ®Google Scholar
• Selden C, Fuller B. Role of bioreactor technology in tissue engineering for clinical use and therapeutic target design. Bioengineering. 2018;5:32. doi: 10.3390/bioengineering5020032.
   PubMedGoogle Scholar
• Mertsching H, Hansmann J. Bioreactor technology in cardiovascular tissue engineering. In: Kasper C, van Griensven M, Pörtner R, editors. Bioreactor systems for tissue engineering. Advances in biochemical engineering/biotechnology. Vol. 112. Berlin, Heidelberg: Springer; 2019.
   Google Scholar
• Beamish JA, He P, Kottke-Marchant K, Marchant RE. Molecular regulation of contractile smooth muscle cell phenotype: implications for vascular tissue engineering. Tissue Eng Part B Rev. 2010;16:467–491. doi: 10.1089/ten.teb.2009.0630.
   PubMed Web of Science ®Google Scholar
• Bachmann BJ, Bernardi L, Loosli C, Marschewski J, Perrini M, Ehrbar M, Ermanni P, Poulikakos D, Ferrari A, Mazza E. A novel bioreactor system for the assessment of Endothelialization on deformable surfaces. Sci Rep. 2016;6:38861. doi: 10.1038/srep38861.
   PubMed Web of Science ®Google Scholar
• Davies JE, Lopresto D, Apta BHR, Lin Z, Ma W, Harper MT. Using Yoda-1 to mimic laminar flow in vitro: a tool to simplify drug testing. Biochem Pharmacol. 2019;168:473–480. doi: 10.1016/j.bcp.2019.08.013.
   PubMed Web of Science ®Google Scholar
• Pound P, Ram R. Are researchers moving away from animal models as a result of poor clinical translation in the field of stroke? An analysis of opinion papers. BMJ Open Sci. 2020;4:e100041. doi: 10.1136/bmjos-2019-100041.
   PubMedGoogle Scholar
• Stalker TJ, Traxler EA, Wu J, Wannemacher KM, Cermignano SL, Voronov R, Diamond SL, Brass LF. Hierarchical organization in the hemostatic response and its relationship to the platelet-signaling network. Blood. 2013;121:1875–1885. doi: 10.1182/blood-2012-09-457739.
   PubMed Web of Science ®Google Scholar
• Chen J, Zhang X, Millican R, Lynd T, Gangasani M, Malhotra S, Sherwood J, Hwang PT, Cho Y, Brott BC, et al. Recent progress in in vitro models for Atherosclerosis studies. Front Cardiovasc Med. 2022;8:790529. doi: 10.3389/fcvm.2021.790529.
   PubMed Web of Science ®Google Scholar