Primary Human Lung Alveolus-on-a-chip Model of Intravascular Thrombosis for Assessment of Therapeutics

Clinical Pharmacology and Therapeutics

Volumn 103, Issue 2, 2018, Pages 332-340

  Jain, A ^a,b,c,g   Barrile, R ^a,h   van der Meer, A D ^a,i   Mammoto, A ^b   Mammoto, T ^b   De Ceunynck, K ^c   Aisiku, O ^c   Otieno, M A ^d   Louden, C S ^d   Hamilton, G A ^e   Flaumenhaft, R ^c   Ingber, D E ^a,b,f  

^a HARVARD UNIVERSITY   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

^e Emulate Inc   (United States)

^f HARVARD UNIVERSITY   (United States)

^g Texas A M University   (United States)

^h CEDARS SINAI MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICOAGULANT AGENT; LIPOPOLYSACCHARIDE; PROTEINASE ACTIVATED RECEPTOR 1; FIBRINOLYTIC AGENT;

ARTICLE; HUMAN; HUMAN TISSUE; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM; LUNG ENDOTHELIUM; METHODOLOGY; MICROFLUIDIC ANALYSIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PULMONARY VASCULAR DISEASE; QUANTITATIVE ANALYSIS; THROMBOSIS; TISSUE ENGINEERING; CELL CULTURE; COCULTURE; DEVICES; DRUG DEVELOPMENT; DRUG EFFECT; ENDOTHELIUM CELL; EPITHELIUM CELL; EVIDENCE BASED MEDICINE; LAB ON A CHIP; LUNG ALVEOLUS; LUNG GAS EXCHANGE; METABOLISM; MICROVASCULATURE; PATHOLOGY; PATIENT SAFETY; PROCEDURES; RISK ASSESSMENT; SIGNAL TRANSDUCTION; TRANSLATIONAL RESEARCH; VASCULARIZATION;

BLOOD-AIR BARRIER; CELLS, CULTURED; COCULTURE TECHNIQUES; DRUG DEVELOPMENT; DRUG DISCOVERY; ENDOTHELIAL CELLS; EPITHELIAL CELLS; EVIDENCE-BASED MEDICINE; FIBRINOLYTIC AGENTS; HUMANS; LAB-ON-A-CHIP DEVICES; MICROFLUIDIC ANALYTICAL TECHNIQUES; MICROVESSELS; PATIENT SAFETY; PULMONARY ALVEOLI; RISK ASSESSMENT; SIGNAL TRANSDUCTION; THROMBOSIS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 85023770580     PISSN: 00099236     EISSN: 15326535     Source Type: Journal    
DOI: 10.1002/cpt.742     Document Type: Article

References (50)

1. Glas, G.J., Van Der Sluijs, K.F., Schultz, M.J., Hofstra, J.J., Van Der Poll, T. & Levi, M. Bronchoalveolar hemostasis in lung injury and acute respiratory distress syndrome. J. Thromb. Haemost. 11, 17–25 (2013).
2. Wygrecka, M., Jablonska, E., Guenther, A., Preissner, K.T. & Markart, P. Current view on alveolar coagulation and fibrinolysis in acute inflammatory and chronic interstitial lung diseases. Thromb. Haemost. 99, 494–501 (2008).
3. Bozza, F.A., Shah, A.M., Weyrich, A.S. & Zimmerman, G.A. Amicus or adversary: platelets in lung biology, acute injury, and inflammation. Am. J. Respir. Cell Mol. Biol. 40, 123–134 (2009).
4. Finigan, J.H. The coagulation system and pulmonary endothelial function in acute lung injury. Microvasc. Res. 77, 35–38 (2009).
5. Cuttica, M.J. & Machado, R. Pulmonary artery thrombosis: another piece to the acute chest syndrome puzzle. Am. J. Respir. Crit. Care Med. 184, 990–991 (2011).
6. Herve, P. et al. Pathobiology of pulmonary hypertension. The role of platelets and thrombosis. Clin. Chest Med. 22, 451–458 (2001).
7. Toshner, M. & Pepke-Zaba, J. Chronic thromboembolic pulmonary hypertension: time for research in pathophysiology to catch up with developments in treatment. F1000Prime Rep. 6, 38 (2014).
8. Matute-Bello, G., Frevert, C.W. & Martin, T.R. Animal models of acute lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L379–L399 (2008).
9. Vivero, M. & Padera, R.F. Histopathology of lung disease in the connective tissue diseases. Rheum. Dis. Clin. North Am. 41, 197–211 (2015).
10. Johnson, S.R., Granton, J.T. & Mehta, S. Thrombotic arteriopathy and anticoagulation in pulmonary hypertension. Chest 130, 545–552 (2006).
11. Benam, K.H. et al. Engineered in vitro disease models. Annu. Rev. Pathol. 10, 195–262 (2015).
12. Bhatia, S.N. & Ingber, D.E. Microfluidic organs-on-chips. Nat. Biotechnol. 32, 760–772 (2014).
13. Jackson, S.P. The growing complexity of platelet aggregation. Blood 109, 5087–5095 (2007).
14. Sagripanti, A. & Carpi, A. Antithrombotic and prothrombotic activities of the vascular endothelium. Biomed. Pharmacother. 54, 107–111 (2000).
15. Wolberg, A.S., Aleman, M.M., Leiderman, K. & Machlus, K.R. Procoagulant activity in hemostasis and thrombosis: Virchow's triad revisited. Anesth. Analg. 114, 275–285 (2012).
16. Andrews, D.A. & Low, P.S. Role of red blood cells in thrombosis. Curr. Opin. Hematol. 6, 76–82 (1999).
17. Weyrich, A.S. & Zimmerman, G.A. Platelets in lung biology. Annu. Rev. Physiol. 75, 569–591 (2013).
18. Casa, L.D., Deaton, D.H. & Ku, D.N. Role of high shear rate in thrombosis. J. Vasc. Surg. 61, 1068–1080 (2015).
19. Ingber, D.E. Reverse engineering human pathophysiology with organs-on-chips. Cell 164, 1105–1109 (2016).
20. Huh, D., Matthews, B.D., Mammoto, A., Montoya-Zavala, M., Hsin, H.Y. & Ingber, D.E. Reconstituting organ-level lung functions on a chip. Science 328, 1662–1668 (2010).
21. Huh, D. et al. A human disease model of drug toxicity-induced pulmonary edema in a lung-on-a-chip microdevice. Sci. Transl. Med. 4, 159ra147 (2012).
22. Lieber, M., Smith, B., Szakal, A., Nelson-Rees, W. & Todaro, G. A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int. J. Cancer 17, 62–70 (1976).
23. Benam, K.H. et al. Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro. Nat. Methods 13, 151–157 (2016).
24. Colace, T., Falls, E., Zheng, X.L. & Diamond, S.L. Analysis of morphology of platelet aggregates formed on collagen under laminar blood flow. Ann. Biomed. Eng. 39, 922–929 (2011).
25. Neeves, K.B. et al. Sources of variability in platelet accumulation on type 1 fibrillar collagen in microfluidic flow assays. PLoS One 8, e54680 (2013).
26. Cosemans, J.M., Angelillo-Scherrer, A., Mattheij, N.J. & Heemskerk, J.W. The effects of arterial flow on platelet activation, thrombus growth, and stabilization. Cardiovasc. Res. 99, 342–352 (2013).
27. Pircher, J. et al. Prothrombotic effects of tumor necrosis factor alpha in vivo are amplified by the absence of TNF-alpha receptor subtype 1 and require TNF-alpha receptor subtype 2. Arthritis Res. Ther. 14, R225 (2012).
28. Jain, A. et al. Assessment of whole blood thrombosis in a microfluidic device lined by fixed human endothelium. Biomed. Microdevices 18, 73 (2016).
29. Furie, B. & Furie, B.C. Mechanisms of thrombus formation. N. Engl. J. Med. 359, 938–949 (2008).
30. Cooley, B.C. In vivo fluorescence imaging of large-vessel thrombosis in mice. Arterioscler. Thromb. Vasc. Biol. 31, 1351–1356 (2011).
31. Stalker, T.J. et al. A systems approach to hemostasis: 3. Thrombus consolidation regulates intrathrombus solute transport and local thrombin activity. Blood 124, 1824–1831 (2014).
32. Falati, S., Gross, P., Merrill-Skoloff, G., Furie, B.C. & Furie, B. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat. Med. 8, 1175–1181 (2002).
33. Westein, E., de Witt, S., Lamers, M., Cosemans, J.M. & Heemskerk, J.W. Monitoring in vitro thrombus formation with novel microfluidic devices. Platelets 23, 501–509 (2012).
34. Hansen, R.R., Wufsus, A.R., Barton, S.T., Onasoga, A.A., Johnson-Paben, R.M. & Neeves, K.B. High content evaluation of shear dependent platelet function in a microfluidic flow assay. Ann. Biomed. Eng. 41, 250–262 (2013).
35. Jain, A., Graveline, A., Waterhouse, A., Vernet, A., Flaumenhaft, R. & Ingber, D.E. A shear gradient-activated microfluidic device for automated monitoring of whole blood haemostasis and platelet function. Nat. Commun. 7, 10176 (2016).
36. Welsh, J.D. et al. A systems approach to hemostasis: 1. The interdependence of thrombus architecture and agonist movements in the gaps between platelets. Blood 124, 1808–1815 (2014).
37. Proudfoot, A.G., McAuley, D.F., Griffiths, M.J. & Hind, M. Human models of acute lung injury. Dis. Model. Mech. 4, 145–153 (2011).
38. Liu, F., Li, W., Pauluhn, J., Trübel, H. & Wang, C. Lipopolysaccharide-induced acute lung injury in rats: comparative assessment of intratracheal instillation and aerosol inhalation. Toxicology 304, 158–166 (2013).
39. Wung, B.S., Ni, C.W. & Wang, D.L. ICAM-1 induction by TNFalpha and IL-6 is mediated by distinct pathways via Rac in endothelial cells. J. Biomed. Sci. 12, 91–101 (2005).
40. Hawiger, J., Veach, R.A. & Zienkiewicz, J. New paradigms in sepsis: from prevention to protection of failing microcirculation. J. Thromb. Haemost. 13, 1743–1756 (2015).
41. De Ceunynck, K.E.P. et al. A chemical APC mimetic protects endothelium from thromboinflammatory injury. Presented at the 58th American Society of Hematology Annual Meeting & Exposition, San Diego, CA, 3–6 December 2016. Abstract 3835.
42. Aisiku, O. et al. Parmodulins inhibit thrombus formation without inducing endothelial injury caused by vorapaxar. Blood 125, 1976–1985 (2015).
43. Conti, G. et al. Evaluation of lung inflammation induced by intratracheal administration of LPS in mice: comparison between MRI and histology. MAGMA 23, 93–101 (2010).
44. Wootton, D.M. & Ku, D.N. Fluid mechanics of vascular systems, diseases, and thrombosis. Annu. Rev. Biomed. Eng. 1, 299–329 (1999).
45. Fogelson, A.L. & Neeves, K.B. Fluid mechanics of blood clot formation. Annu. Rev. Fluid Mech. 47, 377–403 (2015).
46. Flamm, M.H. & Diamond, S.L. Multiscale systems biology and physics of thrombosis under flow. Ann. Biomed. Eng. 40, 2355–2364 (2012).
47. Zheng, Y. et al. In vitro microvessels for the study of angiogenesis and thrombosis. Proc. Natl. Acad. Sci. USA 109, 9342–9347 (2012).
48. Zhang, B., Peticone, C., Murthy, S.K. & Radisic, M. A standalone perfusion platform for drug testing and target validation in micro-vessel networks. Biomicrofluidics 7, 44125 (2013).
49. Tsai, M. et al. In vitro modeling of the microvascular occlusion and thrombosis that occur in hematologic diseases using microfluidic technology. J. Clin. Invest. 122, 408–418 (2012).
50. Li, X., Xu, S., He, P. & Liu, Y. In vitro recapitulation of functional microvessels for the study of endothelial shear response, nitric oxide and [Ca2+]i. PLoS One 10, e0126797 (2015).