Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
General Review Article

Advanced Microfluidic Vascularized Tissues as Platform for the Study of Human Diseases and Drug Development

Author(s): Behnam Noorani, Luca Cucullo*, Yeseul Ahn, Hossam Kadry, Aditya Bhalerao, Snehal Raut, Ehsan Nozohouri and Ekram Ahmed Chowdhury

Volume 21, Issue 3, 2023

Published on: 21 December, 2022

Page: [599 - 620] Pages: 22

DOI: 10.2174/1570159X20666220706112711

open access plus

Abstract

The vascular system plays a critical role in human physiology and diseases. It is a complex subject to study using in vitro models due to its dynamic and three-dimensional microenvironment. Microfluidic technology has recently become a popular technology in various biological fields for its advantages in mimicking complex microenvironments to an extent not achievable by more conventional platforms. Microfluidic technologies can reproduce different vascular system-related structures and functions that can be utilized for drug development and human diseases studies. Herein, we first review the relevant structural and functional vascular biology systems of various organ systems and then the fabrication methods to reproduce these vascular districts. We provide a thorough review of the latest achievement in vascular organ-on-chip modeling specific to lung, heart, and the brain microvasculature for drug screening and the study of human disorders.

Keywords: Cell lines, microfluidic, drug development, pharmacokinetic, permeability, tissue, alternative, endothelium.

« Previous Next »
Graphical Abstract

[1]
Munos, B. Lessons from 60 years of pharmaceutical innovation. Nat. Rev. Drug Discov., 2009, 8(12), 959-968.
[http://dx.doi.org/10.1038/nrd2961] [PMID: 19949401]
[2]
Hackam, D.G. Translating animal research into clinical benefit. BMJ, 2007, 334(7586), 163-164.
[http://dx.doi.org/10.1136/bmj.39104.362951.80] [PMID: 17255568]
[3]
Shanks, N.; Greek, R.; Greek, J. Are animal models predictive for humans? Philos. Ethics Humanit. Med., 2009, 4(1), 2.
[http://dx.doi.org/10.1186/1747-5341-4-2] [PMID: 19146696]
[4]
van der Worp, H.B.; Howells, D.W.; Sena, E.S.; Porritt, M.J.; Rewell, S.; O’Collins, V.; Macleod, M.R. Can animal models of disease reliably inform human studies? PLoS Med., 2010, 7(3), e1000245.
[http://dx.doi.org/10.1371/journal.pmed.1000245] [PMID: 20361020]
[5]
Bhalerao, A.; Sivandzade, F.; Archie, S.R.; Chowdhury, E.A.; Noorani, B.; Cucullo, L. In vitro modeling of the neurovascular unit: Advances in the field. Fluids Barriers CNS, 2020, 17(1), 22.
[http://dx.doi.org/10.1186/s12987-020-00183-7] [PMID: 32178700]
[6]
Naik, P.; Cucullo, L. In vitro blood-brain barrier models: Current and perspective technologies. J. Pharm. Sci., 2012, 101(4), 1337-1354.
[http://dx.doi.org/10.1002/jps.23022] [PMID: 22213383]
[7]
Meer, A.D.; Berg, A. Organs-on-chips: Breaking the in vitro impasse. Integr. Biol., 2012, 4(5), 461-470.
[http://dx.doi.org/10.1039/c2ib00176d] [PMID: 22388577]
[8]
Fatehullah, A.; Tan, S.H.; Barker, N. Organoids as an in vitro model of human development and disease. Nat. Cell Biol., 2016, 18(3), 246-254.
[http://dx.doi.org/10.1038/ncb3312] [PMID: 26911908]
[9]
Ryan, S.L.; Baird, A.M.; Vaz, G.; Urquhart, A.J. Senge; Richard, D.J.; O’Byrne, K.J.; Davies, A.M. Drug discovery approaches utilizing three-dimensional cell culture. Assay Drug Dev. Technol., 2016, 14(1), 19-28.
[http://dx.doi.org/10.1089/adt.2015.670] [PMID: 26866750]
[10]
Wu, J.; Chen, Q.; Liu, W.; He, Z.; Lin, J.M. Recent advances in microfluidic 3D cellular scaffolds for drug assays. Trends Analyt. Chem., 2017, 87, 19-31.
[http://dx.doi.org/10.1016/j.trac.2016.11.009]
[11]
van der Helm, M.W.; van der Meer, A.D.; Eijkel, J.C.T.; van den Berg, A.; Segerink, L.I. Microfluidic organ-on-chip technology for blood-brain barrier research. Tissue Barriers, 2016, 4(1), e1142493.
[http://dx.doi.org/10.1080/21688370.2016.1142493] [PMID: 27141422]
[12]
Nozohouri, S.; Noorani, B.; Al-Ahmad, A.; Abbruscato, T.J. Estimating brain permeability using in vitro blood-brain barrier models. Methods Mol. Biol., 2020, 2367, 47-72.
[http://dx.doi.org/10.1007/7651_2020_311] [PMID: 32789777]
[13]
Esch, E.W.; Bahinski, A.; Huh, D. Organs-on-chips at the frontiers of drug discovery. Nat. Rev. Drug Discov., 2015, 14(4), 248-260.
[http://dx.doi.org/10.1038/nrd4539] [PMID: 25792263]
[14]
Osaki, T.; Sivathanu, V.; Kamm, R.D. Vascularized microfluidic organ-chips for drug screening, disease models and tissue engineering. Curr. Opin. Biotechnol., 2018, 52, 116-123.
[http://dx.doi.org/10.1016/j.copbio.2018.03.011] [PMID: 29656237]
[15]
Lee, H.; Chung, M.; Jeon, N.L. Microvasculature: An essential component for organ-on-chip systems. MRS Bull., 2014, 39(1), 51-59.
[http://dx.doi.org/10.1557/mrs.2013.286]
[16]
Yu, F.; Selva Kumar, N.D.O.; Choudhury, D.; Foo, L.C.; Ng, S.H. Microfluidic platforms for modeling biological barriers in the circulatory system. Drug Discov. Today, 2018, 23(4), 815-829.
[http://dx.doi.org/10.1016/j.drudis.2018.01.036] [PMID: 29357288]
[17]
Xiong, B.; Ren, K.; Shu, Y.; Chen, Y.; Shen, B.; Wu, H. Recent developments in microfluidics for cell studies. Adv. Mater., 2014, 26(31), 5525-5532.
[http://dx.doi.org/10.1002/adma.201305348] [PMID: 24536032]
[18]
Smith, Q.; Gerecht, S. Going with the flow: Microfluidic platforms in vascular tissue engineering. Curr. Opin. Chem. Eng., 2014, 3, 42-50.
[http://dx.doi.org/10.1016/j.coche.2013.11.001] [PMID: 24644533]
[19]
Hasan, A.; Paul, A.; Vrana, N.E.; Zhao, X.; Memic, A.; Hwang, Y.S.; Dokmeci, M.R.; Khademhosseini, A. Microfluidic techniques for development of 3D vascularized tissue. Biomaterials, 2014, 35(26), 7308-7325.
[http://dx.doi.org/10.1016/j.biomaterials.2014.04.091] [PMID: 24906345]
[20]
Pugsley, M.K.; Tabrizchi, R. The vascular system. J. Pharmacol. Toxicol. Methods, 2000, 44(2), 333-340.
[http://dx.doi.org/10.1016/S1056-8719(00)00125-8] [PMID: 11325577]
[21]
Zheng, Y.; Chen, J.; López, J.A. Microvascular platforms for the study of platelet-vessel wall interactions. Thromb. Res., 2014, 133(4), 525-531.
[http://dx.doi.org/10.1016/j.thromres.2013.12.039] [PMID: 24438943]
[22]
Takehara, H.; Sakaguchi, K.; Sekine, H.; Okano, T.; Shimizu, T. Microfluidic vascular-bed devices for vascularized 3D tissue engineering: Tissue engineering on a chip. Biomed. Microdevices, 2020, 22(1), 9.
[http://dx.doi.org/10.1007/s10544-019-0461-2] [PMID: 31863202]
[23]
van Duinen, V.; Trietsch, S.J.; Joore, J.; Vulto, P.; Hankemeier, T. Microfluidic 3D cell culture: From tools to tissue models. Curr. Opin. Biotechnol., 2015, 35, 118-126.
[http://dx.doi.org/10.1016/j.copbio.2015.05.002] [PMID: 26094109]
[24]
Li, X.J.; Valadez, A.V.; Zuo, P.; Nie, Z. Microfluidic 3D cell culture: Potential application for tissue-based bioassays. Bioanalysis, 2012, 4(12), 1509-1525.
[http://dx.doi.org/10.4155/bio.12.133] [PMID: 22793034]
[25]
Adams, R.H.; Alitalo, K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol., 2007, 8(6), 464-478.
[http://dx.doi.org/10.1038/nrm2183] [PMID: 17522591]
[26]
Lafleur, M.A.; Handsley, M.M.; Edwards, D.R. Metalloproteinases and their inhibitors in angiogenesis. Expert Rev. Mol. Med., 2003, 5(23), 1-39.
[http://dx.doi.org/10.1017/S1462399403006628] [PMID: 14585170]
[27]
McGuigan, A.P.; Sefton, M.V. The influence of biomaterials on endothelial cell thrombogenicity. Biomaterials, 2007, 28(16), 2547-2571.
[http://dx.doi.org/10.1016/j.biomaterials.2007.01.039] [PMID: 17316788]
[28]
Ratcliffe, A. Tissue engineering of vascular grafts. Matrix Biol., 2000, 19(4), 353-357.
[http://dx.doi.org/10.1016/S0945-053X(00)00080-9] [PMID: 10963996]
[29]
Rayner, S.G.; Zheng, Y. Engineered microvessels for the study of human disease. J. Biomech. Eng., 2016, 138(11), 110801.
[http://dx.doi.org/10.1115/1.4034428] [PMID: 27537085]
[30]
Feihl, F.; Liaudet, L.; Waeber, B.; Levy, B.I. Hypertension. Hypertension, 2006, 48(6), 1012-1017.
[http://dx.doi.org/10.1161/01.HYP.0000249510.20326.72] [PMID: 17060505]
[31]
van Dijk, C.G.M.; Nieuweboer, F.E.; Pei, J.Y.; Xu, Y.J.; Burgisser, P.; van Mulligen, E.; el Azzouzi, H.; Duncker, D.J.; Verhaar, M.C.; Cheng, C. The complex mural cell: Pericyte function in health and disease. Int. J. Cardiol., 2015, 190, 75-89.
[http://dx.doi.org/10.1016/j.ijcard.2015.03.258] [PMID: 25918055]
[32]
Kaihara, S.; Borenstein, J.; Koka, R.; Lalan, S.; Ochoa, E.R.; Ravens, M.; Pien, H.; Cunningham, B.; Vacanti, J.P. Silicon micromachining to tissue engineer branched vascular channels for liver fabrication. Tissue Eng., 2000, 6(2), 105-117.
[http://dx.doi.org/10.1089/107632700320739] [PMID: 10941206]
[33]
Borenstein, J.T.; Terai, H.; King, K.R.; Weinberg, E.J.; Kaazempur-Mofrad, M.R.; Vacanti, J.P. Microfabrication technology for vascularized tissue engineering. Biomed. Microdevices, 2002, 4(3), 167-175.
[http://dx.doi.org/10.1023/A:1016040212127]
[34]
López, J.A.; Zheng, Y. Synthetic microvessels. J. Thromb. Haemost., 2013, 11(Suppl. 1), 67-74.
[http://dx.doi.org/10.1111/jth.12245] [PMID: 23809111]
[35]
Chrobak, K.M.; Potter, D.R.; Tien, J. Formation of perfused, functional microvascular tubes in vitro. Microvasc. Res., 2006, 71(3), 185-196.
[http://dx.doi.org/10.1016/j.mvr.2006.02.005] [PMID: 16600313]
[36]
Nichol, J.W.; Koshy, S.T.; Bae, H.; Hwang, C.M.; Yamanlar, S.; Khademhosseini, A. Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials, 2010, 31(21), 5536-5544.
[http://dx.doi.org/10.1016/j.biomaterials.2010.03.064] [PMID: 20417964]
[37]
Yoshida, H.; Matsusaki, M.; Akashi, M. Multilayered blood capillary analogs in biodegradable hydrogels for in vitro drug permeability assays. Adv. Funct. Mater., 2013, 23(14), 1736-1742.
[http://dx.doi.org/10.1002/adfm.201201905]
[38]
Zheng, Y.; Chen, J.; Craven, M.; Choi, N.W.; Totorica, S.; Diaz-Santana, A.; Kermani, P.; Hempstead, B.; Fischbach-Teschl, C.; López, J.A.; Stroock, A.D. In vitro microvessels for the study of angiogenesis and thrombosis. Proc. Natl. Acad. Sci. USA, 2012, 109(24), 9342-9347.
[http://dx.doi.org/10.1073/pnas.1201240109] [PMID: 22645376]
[39]
Bischel, L.L.; Young, E.W.K.; Mader, B.R.; Beebe, D.J. Tubeless microfluidic angiogenesis assay with three-dimensional endothelial-lined microvessels. Biomaterials, 2013, 34(5), 1471-1477.
[http://dx.doi.org/10.1016/j.biomaterials.2012.11.005] [PMID: 23191982]
[40]
He, J.; Chen, R.; Lu, Y.; Zhan, L.; Liu, Y.; Li, D.; Jin, Z. Fabrication of circular microfluidic network in enzymatically-crosslinked gelatin hydrogel. Mater. Sci. Eng. C, 2016, 59, 53-60.
[http://dx.doi.org/10.1016/j.msec.2015.09.104] [PMID: 26652348]
[41]
Zhang, B.; Montgomery, M.; Chamberlain, M.D.; Ogawa, S.; Korolj, A.; Pahnke, A.; Wells, L.A.; Massé, S.; Kim, J.; Reis, L.; Momen, A.; Nunes, S.S.; Wheeler, A.R.; Nanthakumar, K.; Keller, G.; Sefton, M.V.; Radisic, M. Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis. Nat. Mater., 2016, 15(6), 669-678.
[http://dx.doi.org/10.1038/nmat4570] [PMID: 26950595]
[42]
Golden, A.P.; Tien, J. Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip, 2007, 7(6), 720-725.
[http://dx.doi.org/10.1039/b618409j] [PMID: 17538713]
[43]
Miller, J.S.; Stevens, K.R.; Yang, M.T.; Baker, B.M.; Nguyen, D.H.T.; Cohen, D.M.; Toro, E.; Chen, A.A.; Galie, P.A.; Yu, X.; Chaturvedi, R.; Bhatia, S.N.; Chen, C.S. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater., 2012, 11(9), 768-774.
[http://dx.doi.org/10.1038/nmat3357] [PMID: 22751181]
[44]
Kinstlinger, I.S.; Miller, J.S. 3D-printed fluidic networks as vasculature for engineered tissue. Lab Chip, 2016, 16(11), 2025-2043.
[http://dx.doi.org/10.1039/C6LC00193A] [PMID: 27173478]
[45]
Colosi, C.; Shin, S.R.; Manoharan, V.; Massa, S.; Costantini, M.; Barbetta, A.; Dokmeci, M.R.; Dentini, M.; Khademhosseini, A. Microfluidic bioprinting of heterogeneous 3D tissue constructs using low-viscosity bioink. Adv. Mater., 2016, 28(4), 677-684.
[http://dx.doi.org/10.1002/adma.201503310] [PMID: 26606883]
[46]
Jia, W.; Gungor-Ozkerim, P.S.; Zhang, Y.S.; Yue, K.; Zhu, K.; Liu, W.; Pi, Q.; Byambaa, B.; Dokmeci, M.R.; Shin, S.R.; Khademhosseini, A. Direct 3D bioprinting of perfusable vascular constructs using a blend bioink. Biomaterials, 2016, 106, 58-68.
[http://dx.doi.org/10.1016/j.biomaterials.2016.07.038] [PMID: 27552316]
[47]
Zhang, Y.S.; Arneri, A.; Bersini, S.; Shin, S.R.; Zhu, K.; Goli-Malekabadi, Z.; Aleman, J.; Colosi, C.; Busignani, F.; Dell’Erba, V.; Bishop, C.; Shupe, T.; Demarchi, D.; Moretti, M.; Rasponi, M.; Dokmeci, M.R.; Atala, A.; Khademhosseini, A. Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomaterials, 2016, 110, 45-59.
[http://dx.doi.org/10.1016/j.biomaterials.2016.09.003] [PMID: 27710832]
[48]
Nikkhah, M.; Edalat, F.; Manoucheri, S.; Khademhosseini, A. Engineering microscale topographies to control the cell–substrate interface. Biomaterials, 2012, 33(21), 5230-5246.
[http://dx.doi.org/10.1016/j.biomaterials.2012.03.079] [PMID: 22521491]
[49]
Folkman, J.; Haudenschild, C.C.; Zetter, B.R. Long-term culture of capillary endothelial cells. Proc. Natl. Acad. Sci. USA, 1979, 76(10), 5217-5221.
[http://dx.doi.org/10.1073/pnas.76.10.5217] [PMID: 291937]
[50]
Takei, T.; Sakai, S.; Yoshida, M. In vitro formation of vascular-like networks using hydrogels. J. Biosci. Bioeng., 2016, 122(5), 519-527.
[http://dx.doi.org/10.1016/j.jbiosc.2016.03.023] [PMID: 27117917]
[51]
Nicodemus, G.D.; Bryant, S.J. Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng. Part B Rev., 2008, 14(2), 149-165.
[http://dx.doi.org/10.1089/ten.teb.2007.0332] [PMID: 18498217]
[52]
Raghavan, S.; Nelson, C.M.; Baranski, J.D.; Lim, E.; Chen, C.S. Geometrically controlled endothelial tubulogenesis in micropatterned gels. Tissue Eng. Part A, 2010, 16(7), 2255-2263.
[http://dx.doi.org/10.1089/ten.tea.2009.0584] [PMID: 20180698]
[53]
Nikkhah, M.; Eshak, N.; Zorlutuna, P.; Annabi, N.; Castello, M.; Kim, K.; Dolatshahi-Pirouz, A.; Edalat, F.; Bae, H.; Yang, Y.; Khademhosseini, A. Directed endothelial cell morphogenesis in micropatterned gelatin methacrylate hydrogels. Biomaterials, 2012, 33(35), 9009-9018.
[http://dx.doi.org/10.1016/j.biomaterials.2012.08.068] [PMID: 23018132]
[54]
Hu, C.; Chen, Y.; Tan, M.J.A.; Ren, K.; Wu, H. Microfluidic technologies for vasculature biomimicry. Analyst (Lond.), 2019, 144(15), 4461-4471.
[http://dx.doi.org/10.1039/C9AN00421A] [PMID: 31162494]
[55]
Yeon, J.H.; Ryu, H.R.; Chung, M.; Hu, Q.P.; Jeon, N.L. In vitro formation and characterization of a perfusable three-dimensional tubular capillary network in microfluidic devices. Lab Chip, 2012, 12(16), 2815-2822.
[http://dx.doi.org/10.1039/c2lc40131b] [PMID: 22767334]
[56]
Kim, S.; Lee, H.; Chung, M.; Jeon, N.L. Engineering of functional, perfusable 3D microvascular networks on a chip. Lab Chip, 2013, 13(8), 1489-1500.
[http://dx.doi.org/10.1039/c3lc41320a] [PMID: 23440068]
[57]
Nillesen, S.T.M.; Geutjes, P.J.; Wismans, R.; Schalkwijk, J.; Daamen, W.F.; van Kuppevelt, T.H. Increased angiogenesis and blood vessel maturation in acellular collagen–heparin scaffolds containing both FGF2 and VEGF. Biomaterials, 2007, 28(6), 1123-1131.
[http://dx.doi.org/10.1016/j.biomaterials.2006.10.029] [PMID: 17113636]
[58]
Jeon, J.S.; Bersini, S.; Whisler, J.A.; Chen, M.B.; Dubini, G.; Charest, J.L.; Moretti, M.; Kamm, R.D. Generation of 3D functional microvascular networks with human mesenchymal stem cells in microfluidic systems. Integr. Biol., 2014, 6(5), 555-563.
[http://dx.doi.org/10.1039/C3IB40267C] [PMID: 24676392]
[59]
Jeon, J.S.; Bersini, S.; Gilardi, M.; Dubini, G.; Charest, J.L.; Moretti, M.; Kamm, R.D. Human 3D vascularized organotypic microfluidic assays to study breast cancer cell extravasation. Proc. Natl. Acad. Sci. USA, 2015, 112(1), 214-219.
[http://dx.doi.org/10.1073/pnas.1417115112] [PMID: 25524628]
[60]
Chen, M.B.; Whisler, J.A.; Fröse, J.; Yu, C.; Shin, Y.; Kamm, R.D. On-chip human microvasculature assay for visualization and quantification of tumor cell extravasation dynamics. Nat. Protoc., 2017, 12(5), 865-880.
[http://dx.doi.org/10.1038/nprot.2017.018] [PMID: 28358393]
[61]
Osaki, T.; Sivathanu, V.; Kamm, R.D. Engineered 3D vascular and neuronal networks in a microfluidic platform. Sci. Rep., 2018, 8(1), 5168.
[http://dx.doi.org/10.1038/s41598-018-23512-1] [PMID: 29581463]
[62]
Kim, J.; Chung, M.; Kim, S.; Jo, D.H.; Kim, J.H.; Jeon, N.L. Engineering of a biomimetic pericyte-covered 3D microvascular network. PLoS One, 2015, 10(7), e0133880.
[http://dx.doi.org/10.1371/journal.pone.0133880] [PMID: 26204526]
[63]
Zepp, J.A.; Morrisey, E.E. Cellular crosstalk in the development and regeneration of the respiratory system. Nat. Rev. Mol. Cell Biol., 2019, 20(9), 551-566.
[http://dx.doi.org/10.1038/s41580-019-0141-3] [PMID: 31217577]
[64]
Gump, A.; Haughney, L.; Fredberg, J. Relaxation of activated airway smooth muscle: Relative potency of isoproterenol vs. tidal stretch. J. Appl. Physiol. (1985), 2001, 90(6), 2306-10.
[http://dx.doi.org/10.1152/jappl.2001.90.6.2306] [PMID: 11356796]
[65]
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, 2010, 328(5986), 1662-1668.
[http://dx.doi.org/10.1126/science.1188302] [PMID: 20576885]
[66]
Thodeti, C.K.; Matthews, B.; Ravi, A.; Mammoto, A.; Ghosh, K.; Bracha, A.L.; Ingber, D.E. TRPV4 channels mediate cyclic strain-induced endothelial cell reorientation through integrin-to-integrin signaling. Circ. Res., 2009, 104(9), 1123-1130.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.192930] [PMID: 19359599]
[67]
Pampaloni, F.; Reynaud, E.G.; Stelzer, E.H.K. The third dimension bridges the gap between cell culture and live tissue. Nat. Rev. Mol. Cell Biol., 2007, 8(10), 839-845.
[http://dx.doi.org/10.1038/nrm2236] [PMID: 17684528]
[68]
Stucki, A.O.; Stucki, J.D.; Hall, S.R.R.; Felder, M.; Mermoud, Y.; Schmid, R.A.; Geiser, T.; Guenat, O.T. A lung-on-a-chip array with an integrated bio-inspired respiration mechanism. Lab Chip, 2015, 15(5), 1302-1310.
[http://dx.doi.org/10.1039/C4LC01252F] [PMID: 25521475]
[69]
Blume, C.; Reale, R.; Held, M.; Millar, T.M.; Collins, J.E.; Davies, D.E.; Morgan, H.; Swindle, E.J. Temporal monitoring of differentiated human airway epithelial cells using microfluidics. PLoS One, 2015, 10(10), e0139872.
[http://dx.doi.org/10.1371/journal.pone.0139872] [PMID: 26436734]
[70]
Benam, K.H.; Villenave, R.; Lucchesi, C.; Varone, A.; Hubeau, C.; Lee, H.H.; Alves, S.E.; Salmon, M.; Ferrante, T.C.; Weaver, J.C.; Bahinski, A.; Hamilton, G.A.; Ingber, D.E. Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro. Nat. Methods, 2016, 13(2), 151-157.
[http://dx.doi.org/10.1038/nmeth.3697] [PMID: 26689262]
[71]
Zamprogno, P.; Wüthrich, S.; Achenbach, S.; Thoma, G.; Stucki, J.D.; Hobi, N.; Schneider-Daum, N.; Lehr, C.M.; Huwer, H.; Geiser, T.; Schmid, R.A.; Guenat, O.T. Second-generation lung-on-a-chip with an array of stretchable alveoli made with a biological membrane. Commun. Biol., 2021, 4(1), 168.
[http://dx.doi.org/10.1038/s42003-021-01695-0] [PMID: 33547387]
[72]
Xu, Z.; Gao, Y.; Hao, Y.; Li, E.; Wang, Y.; Zhang, J.; Wang, W.; Gao, Z.; Wang, Q. Application of a microfluidic chip-based 3D co-culture to test drug sensitivity for individualized treatment of lung cancer. Biomaterials, 2013, 34(16), 4109-4117.
[http://dx.doi.org/10.1016/j.biomaterials.2013.02.045] [PMID: 23473962]
[73]
Hassell, B.A.; Goyal, G.; Lee, E.; Sontheimer-Phelps, A.; Levy, O.; Chen, C.S.; Ingber, D.E. Human organ chip models recapitulate orthotopic lung cancer growth, therapeutic responses, and tumor dormancy in vitro. Cell Rep., 2017, 21(2), 508-516.
[http://dx.doi.org/10.1016/j.celrep.2017.09.043] [PMID: 29020635]
[74]
Zhang, M.; Xu, C.; Jiang, L.; Qin, J. A 3D human lung-on-a-chip model for nanotoxicity testing. Toxicol. Res. (Camb.), 2018, 7(6), 1048-1060.
[http://dx.doi.org/10.1039/C8TX00156A] [PMID: 30510678]
[75]
Jastrzebska, E.; Tomecka, E.; Jesion, I. Heart-on-a-chip based on stem cell biology. Biosens. Bioelectron., 2016, 75, 67-81.
[http://dx.doi.org/10.1016/j.bios.2015.08.012] [PMID: 26298640]
[76]
Trepat, X.; Deng, L.; An, S.S.; Navajas, D.; Tschumperlin, D.J.; Gerthoffer, W.T.; Butler, J.P.; Fredberg, J.J. Universal physical responses to stretch in the living cell. Nature, 2007, 447(7144), 592-595.
[http://dx.doi.org/10.1038/nature05824] [PMID: 17538621]
[77]
Salameh, A.; Wustmann, A.; Karl, S.; Blanke, K.; Apel, D.; Rojas-Gomez, D.; Franke, H.; Mohr, F.W.; Janousek, J.; Dhein, S. Cyclic mechanical stretch induces cardiomyocyte orientation and polarization of the gap junction protein connexin43. Circ. Res., 2010, 106(10), 1592-1602.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.214429] [PMID: 20378856]
[78]
Zhuang, J.; Yamada, K.A.; Saffitz, J.E.; Kléber, A.G. Pulsatile stretch remodels cell-to-cell communication in cultured myocytes. Circ. Res., 2000, 87(4), 316-322.
[http://dx.doi.org/10.1161/01.RES.87.4.316] [PMID: 10948066]
[79]
Mathur, A.; Loskill, P.; Shao, K.; Huebsch, N.; Hong, S.; Marcus, S.G.; Marks, N.; Mandegar, M.; Conklin, B.R.; Lee, L.P.; Healy, K.E. Human iPSC-based cardiac microphysiological system for drug screening applications. Sci. Rep., 2015, 5(1), 8883.
[http://dx.doi.org/10.1038/srep08883] [PMID: 25748532]
[80]
Agarwal, A.; Goss, J.A.; Cho, A.; McCain, M.L.; Parker, K.K. Microfluidic heart on a chip for higher throughput pharmacological studies. Lab Chip, 2013, 13(18), 3599-3608.
[http://dx.doi.org/10.1039/c3lc50350j] [PMID: 23807141]
[81]
Thavandiran, N.; Dubois, N.; Mikryukov, A.; Massé, S.; Beca, B.; Simmons, C.A.; Deshpande, V.S.; McGarry, J.P.; Chen, C.S.; Nanthakumar, K.; Keller, G.M.; Radisic, M.; Zandstra, P.W. Design and formulation of functional pluripotent stem cell-derived cardiac microtissues. Proc. Natl. Acad. Sci. USA, 2013, 110(49), E4698-E4707.
[http://dx.doi.org/10.1073/pnas.1311120110] [PMID: 24255110]
[82]
Chiu, L.L.Y.; Montgomery, M.; Liang, Y.; Liu, H.; Radisic, M. Perfusable branching microvessel bed for vascularization of engineered tissues. Proc. Natl. Acad. Sci. USA, 2012, 109(50), E3414-E3423.
[http://dx.doi.org/10.1073/pnas.1210580109] [PMID: 23184971]
[83]
Marsano, A.; Conficconi, C.; Lemme, M.; Occhetta, P.; Gaudiello, E.; Votta, E.; Cerino, G.; Redaelli, A.; Rasponi, M. Beating heart on a chip: A novel microfluidic platform to generate functional 3D cardiac microtissues. Lab Chip, 2016, 16(3), 599-610.
[http://dx.doi.org/10.1039/C5LC01356A] [PMID: 26758922]
[84]
Turnbull, I.C.; Karakikes, I.; Serrao, G.W.; Backeris, P.; Lee, J.J.; Xie, C.; Senyei, G.; Gordon, R.E.; Li, R.A.; Akar, F.G.; Hajjar, R.J.; Hulot, J.S.; Costa, K.D. Advancing functional engineered cardiac tissues toward a preclinical model of human myocardium. FASEB J., 2014, 28(2), 644-654.
[http://dx.doi.org/10.1096/fj.13-228007] [PMID: 24174427]
[85]
Schaaf, S.; Shibamiya, A.; Mewe, M.; Eder, A.; Stöhr, A.; Hirt, M.N.; Rau, T.; Zimmermann, W.H.; Conradi, L.; Eschenhagen, T.; Hansen, A. Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. PLoS One, 2011, 6(10), e26397.
[http://dx.doi.org/10.1371/journal.pone.0026397] [PMID: 22028871]
[86]
Jonsson, M.K.B.; Wang, Q.D.; Becker, B. Impedance-based detection of beating rhythm and proarrhythmic effects of compounds on stem cell-derived cardiomyocytes. Assay Drug Dev. Technol., 2011, 9(6), 589-599.
[http://dx.doi.org/10.1089/adt.2011.0396] [PMID: 22085047]
[87]
MacQueen, L.A.; Sheehy, S.P.; Chantre, C.O.; Zimmerman, J.F.; Pasqualini, F.S.; Liu, X.; Goss, J.A.; Campbell, P.H.; Gonzalez, G.M.; Park, S.J.; Capulli, A.K.; Ferrier, J.P.; Kosar, T.F.; Mahadevan, L.; Pu, W.T.; Parker, K.K. A tissue-engineered scale model of the heart ventricle. Nat. Biomed. Eng., 2018, 2(12), 930-941.
[http://dx.doi.org/10.1038/s41551-018-0271-5] [PMID: 31015723]
[88]
Grosberg, A.; Alford, P.W.; McCain, M.L.; Parker, K.K. Ensembles of engineered cardiac tissues for physiological and pharmacological study: Heart on a chip. Lab Chip, 2011, 11(24), 4165-4173.
[http://dx.doi.org/10.1039/c1lc20557a] [PMID: 22072288]
[89]
Ellis, B.W.; Acun, A.; Can, U.I.; Zorlutuna, P. Human iPSC-derived myocardium-on-chip with capillary-like flow for personalized medicine. Biomicrofluidics, 2017, 11(2), 024105.
[http://dx.doi.org/10.1063/1.4978468] [PMID: 28396709]
[90]
Veldhuizen, J.; Cutts, J.; Brafman, D.A.; Migrino, R.Q.; Nikkhah, M. Engineering anisotropic human stem cell-derived three-dimensional cardiac tissue on-a-chip. Biomaterials, 2020, 256, 120195.
[http://dx.doi.org/10.1016/j.biomaterials.2020.120195] [PMID: 32623207]
[91]
Mastikhina, O.; Moon, B.U.; Williams, K.; Hatkar, R.; Gustafson, D.; Mourad, O.; Sun, X.; Koo, M.; Lam, A.Y.L.; Sun, Y.; Fish, J.E.; Young, E.W.K.; Nunes, S.S. Human cardiac fibrosis-on-a-chip model recapitulates disease hallmarks and can serve as a platform for drug testing. Biomaterials, 2020, 233, 119741.
[http://dx.doi.org/10.1016/j.biomaterials.2019.119741] [PMID: 31927251]
[92]
Kadry, H.; Noorani, B.; Cucullo, L. A blood–brain barrier overview on structure, function, impairment, and biomarkers of integrity. Fluids Barriers CNS, 2020, 17(1), 69.
[http://dx.doi.org/10.1186/s12987-020-00230-3] [PMID: 33208141]
[93]
Wang, X.; Xu, B.; Xiang, M.; Yang, X.; Liu, Y.; Liu, X.; Shen, Y. Advances on fluid shear stress regulating blood-brain barrier. Microvasc. Res., 2020, 128, 103930.
[http://dx.doi.org/10.1016/j.mvr.2019.103930] [PMID: 31639383]
[94]
Vatine, G.D.; Barrile, R.; Workman, M.J.; Sances, S.; Barriga, B.K.; Rahnama, M.; Barthakur, S.; Kasendra, M.; Lucchesi, C.; Kerns, J.; Wen, N.; Spivia, W.R.; Chen, Z.; Van Eyk, J.; Svendsen, C.N. Human iPSC-derived blood-brain barrier chips enable disease modeling and personalized medicine applications. Cell Stem Cell, 2019, 24(6), 995-1005.e6.
[http://dx.doi.org/10.1016/j.stem.2019.05.011] [PMID: 31173718]
[95]
DeStefano, J.G.; Xu, Z.S.; Williams, A.J.; Yimam, N.; Searson, P.C. Effect of shear stress on iPSC-derived human brain microvascular endothelial cells (dhBMECs). Fluids Barriers CNS, 2017, 14(1), 20.
[http://dx.doi.org/10.1186/s12987-017-0068-z] [PMID: 28774343]
[96]
Cucullo, L.; Hossain, M.; Puvenna, V.; Marchi, N.; Janigro, D. The role of shear stress in blood-brain barrier endothelial physiology. BMC Neurosci., 2011, 12(1), 40.
[http://dx.doi.org/10.1186/1471-2202-12-40] [PMID: 21569296]
[97]
Campisi, M.; Shin, Y.; Osaki, T.; Hajal, C.; Chiono, V.; Kamm, R.D. 3D self-organized microvascular model of the human blood-brain barrier with endothelial cells, pericytes and astrocytes. Biomaterials, 2018, 180, 117-129.
[http://dx.doi.org/10.1016/j.biomaterials.2018.07.014] [PMID: 30032046]
[98]
DeStefano, J.G.; Jamieson, J.J.; Linville, R.M.; Searson, P.C. Benchmarking in vitro tissue-engineered blood–brain barrier models. Fluids Barriers CNS, 2018, 15(1), 32.
[http://dx.doi.org/10.1186/s12987-018-0117-2] [PMID: 30514389]
[99]
Linville, R.M.; DeStefano, J.G.; Sklar, M.B.; Chu, C.; Walczak, P.; Searson, P.C. Modeling hyperosmotic blood–brain barrier opening within human tissue-engineered in vitro brain microvessels. J. Cereb. Blood Flow Metab., 2020, 40(7), 1517-1532.
[http://dx.doi.org/10.1177/0271678X19867980] [PMID: 31394959]
[100]
Linville, R.M.; DeStefano, J.G.; Sklar, M.B.; Xu, Z.; Farrell, A.M.; Bogorad, M.I.; Chu, C.; Walczak, P.; Cheng, L.; Mahairaki, V.; Whartenby, K.A.; Calabresi, P.A.; Searson, P.C. Human iPSC-derived blood-brain barrier microvessels: Validation of barrier function and endothelial cell behavior. Biomaterials, 2019, 190-191, 24-37.
[http://dx.doi.org/10.1016/j.biomaterials.2018.10.023] [PMID: 30391800]
[101]
Jamieson, J.J.; Linville, R.M.; Ding, Y.Y.; Gerecht, S.; Searson, P.C. Role of iPSC-derived pericytes on barrier function of iPSC-derived brain microvascular endothelial cells in 2D and 3D. Fluids Barriers CNS, 2019, 16(1), 15.
[http://dx.doi.org/10.1186/s12987-019-0136-7] [PMID: 31167667]
[102]
Cho, H.; Seo, J.H.; Wong, K.H.K.; Terasaki, Y.; Park, J.; Bong, K.; Arai, K.; Lo, E.H.; Irimia, D. Three-dimensional blood-brain barrier model for in vitro studies of neurovascular pathology. Sci. Rep., 2015, 5(1), 15222.
[http://dx.doi.org/10.1038/srep15222] [PMID: 26503597]
[103]
Kim, J.A.; Kim, H.N.; Im, S.K.; Chung, S.; Kang, J.Y.; Choi, N. Collagen-based brain microvasculature model in vitro using three-dimensional printed template. Biomicrofluidics, 2015, 9(2), 024115.
[http://dx.doi.org/10.1063/1.4917508] [PMID: 25945141]
[104]
Phan, D.T.T.; Bender, R.H.F.; Andrejecsk, J.W.; Sobrino, A.; Hachey, S.J.; George, S.C.; Hughes, C.C.W. Blood–brain barrier-on-a-chip: Microphysiological systems that capture the complexity of the blood–central nervous system interface. Exp. Biol. Med. (Maywood), 2017, 242(17), 1669-1678.
[http://dx.doi.org/10.1177/1535370217694100] [PMID: 28195514]
[105]
Wang, Y.I.; Abaci, H.E.; Shuler, M.L. Microfluidic blood–brain barrier model provides in vivo like barrier properties for drug permeability screening. Biotechnol. Bioeng., 2017, 114(1), 184-194.
[http://dx.doi.org/10.1002/bit.26045] [PMID: 27399645]
[106]
Noorani, B.; Bhalerao, A.; Raut, S.; Nozohouri, E.; Bickel, U.; Cucullo, L. A quasi-physiological microfluidic blood-brain barrier model for brain permeability studies. Pharmaceutics, 2021, 13(9), 1474.
[http://dx.doi.org/10.3390/pharmaceutics13091474] [PMID: 34575550]
[107]
Park, T.E.; Mustafaoglu, N.; Herland, A.; Hasselkus, R.; Mannix, R.; Fitz, G.E.A.; Prantil-Baun, R.; Watters, A.; Henry, O.; Benz, M.; Sanchez, H.; McCrea, H.J.; Goumnerova, L.C.; Song, H.W.; Palecek, S.P.; Shusta, E.; Ingber, D.E. Hypoxia-enhanced blood-brain barrier chip recapitulates human barrier function and shuttling of drugs and antibodies. Nat. Commun., 2019, 10(1), 2621.
[http://dx.doi.org/10.1038/s41467-019-10588-0] [PMID: 31197168]
[108]
Park, J.; Lee, B.K.; Jeong, G.S.; Hyun, J.K.; Lee, C.J.; Lee, S.H. Three-dimensional brain-on-a-chip with an interstitial level of flow and its application as an in vitro model of Alzheimer’s disease. Lab Chip, 2015, 15(1), 141-150.
[http://dx.doi.org/10.1039/C4LC00962B] [PMID: 25317977]
[109]
Park, J.; Wetzel, I.; Marriott, I.; Dréau, D.; D’Avanzo, C.; Kim, D.Y.; Tanzi, R.E.; Cho, H. A 3D human triculture system modeling neurodegeneration and neuroinflammation in Alzheimer’s disease. Nat. Neurosci., 2018, 21(7), 941-951.
[http://dx.doi.org/10.1038/s41593-018-0175-4] [PMID: 29950669]
[110]
Bolognin, S.; Fossépré, M.; Qing, X.; Jarazo, J.; Ščančar, J.; Moreno, E.L.; Nickels, S.L.; Wasner, K.; Ouzren, N.; Walter, J.; Grünewald, A.; Glaab, E.; Salamanca, L.; Fleming, R.M.T.; Antony, P.M.A.; Schwamborn, J.C. 3D cultures of Parkinson’s disease-specific dopaminergic neurons for high content phenotyping and drug testing. Adv. Sci. (Weinh.), 2019, 6(1), 1800927.
[http://dx.doi.org/10.1002/advs.201800927] [PMID: 30643711]
[111]
Lapointe, S.; Perry, A.; Butowski, N.A. Primary brain tumours in adults. Lancet, 2018, 392(10145), 432-446.
[http://dx.doi.org/10.1016/S0140-6736(18)30990-5] [PMID: 30060998]
[112]
Fan, Y.; Nguyen, D.T.; Akay, Y.; Xu, F.; Akay, M. Engineering a brain cancer chip for high-throughput drug screening. Sci. Rep., 2016, 6(1), 25062.
[http://dx.doi.org/10.1038/srep25062] [PMID: 27151082]
[113]
Liu, W.; Sun, P.; Yang, L.; Wang, J.; Li, L.; Wang, J. Assay of glioma cell responses to an anticancer drug in a cell-based microfluidic device. Microfluid. Nanofluidics, 2010, 9(4-5), 717-725.
[http://dx.doi.org/10.1007/s10404-010-0584-5]
[114]
Kong, J.; Luo, Y.; Jin, D.; An, F.; Zhang, W.; Liu, L.; Li, J.; Fang, S.; Li, X.; Yang, X.; Lin, B.; Liu, T. A novel microfluidic model can mimic organ-specific metastasis of circulating tumor cells. Oncotarget, 2016, 7(48), 78421-78432.
[http://dx.doi.org/10.18632/oncotarget.9382] [PMID: 27191997]
[115]
Xu, Z.; Li, E.; Guo, Z.; Yu, R.; Hao, H.; Xu, Y.; Sun, Z.; Li, X.; Lyu, J.; Wang, Q. Design and construction of a multi-organ microfluidic chip mimicking the in vivo microenvironment of lung cancer metastasis. ACS Appl. Mater. Interfaces, 2016, 8(39), 25840-25847.
[http://dx.doi.org/10.1021/acsami.6b08746] [PMID: 27606718]
[116]
Terrell-Hall, T.B.; Ammer, A.G.; Griffith, J.I.G.; Lockman, P.R. Permeability across a novel microfluidic blood-tumor barrier model. Fluids Barriers CNS, 2017, 14(1), 3.
[http://dx.doi.org/10.1186/s12987-017-0050-9] [PMID: 28114946]
[117]
Xu, H.; Li, Z.; Yu, Y.; Sizdahkhani, S.; Ho, W.S.; Yin, F.; Wang, L.; Zhu, G.; Zhang, M.; Jiang, L.; Zhuang, Z.; Qin, J. A dynamic in vivo-like organotypic blood-brain barrier model to probe metastatic brain tumors. Sci. Rep., 2016, 6(1), 36670.
[http://dx.doi.org/10.1038/srep36670] [PMID: 27830712]
[118]
Liu, W.; Song, J.; Du, X.; Zhou, Y.; Li, Y.; Li, R.; Lyu, L.; He, Y.; Hao, J.; Ben, J.; Wang, W.; Shi, H.; Wang, Q. AKR1B10 (Aldo-keto reductase family 1 B10) promotes brain metastasis of lung cancer cells in a multi-organ microfluidic chip model. Acta Biomater., 2019, 91, 195-208.
[http://dx.doi.org/10.1016/j.actbio.2019.04.053] [PMID: 31034948]
[119]
Feng, S.; Cen, J.; Huang, Y.; Shen, H.; Yao, L.; Wang, Y.; Chen, Z. Matrix metalloproteinase-2 and -9 secreted by leukemic cells increase the permeability of blood-brain barrier by disrupting tight junction proteins. PLoS One, 2011, 6(8), e20599.
[http://dx.doi.org/10.1371/journal.pone.0020599] [PMID: 21857898]
[120]
Brown, T.D.; Nowak, M.; Bayles, A.V.; Prabhakarpandian, B.; Karande, P.; Lahann, J.; Helgeson, M.E.; Mitragotricorresponding, S. A microfluidic model of human brain (μHuB) for assessment of blood brain barrier. Bioeng. Transl. Med., 2019, 4(2), e10126.
[http://dx.doi.org/10.1002/btm2.10126] [PMID: 31249876]
[121]
Schwartz, M.P.; Hou, Z.; Propson, N.E.; Zhang, J.; Engstrom, C.J.; Costa, V.S.; Jiang, P.; Nguyen, B.K.; Bolin, J.M.; Daly, W.; Wang, Y.; Stewart, R.; Page, C.D.; Murphy, W.L.; Thomson, J.A. Human pluripotent stem cell-derived neural constructs for predicting neural toxicity. Proc. Natl. Acad. Sci. USA, 2015, 112(40), 12516-12521.
[http://dx.doi.org/10.1073/pnas.1516645112] [PMID: 26392547]
[122]
Cakir, B.; Xiang, Y.; Tanaka, Y.; Kural, M.H.; Parent, M.; Kang, Y.J.; Chapeton, K.; Patterson, B.; Yuan, Y.; He, C.S.; Raredon, M.S.B.; Dengelegi, J.; Kim, K.Y.; Sun, P.; Zhong, M.; Lee, S.; Patra, P.; Hyder, F.; Niklason, L.E.; Lee, S.H.; Yoon, Y.S.; Park, I.H. Engineering of human brain organoids with a functional vascular-like system. Nat. Methods, 2019, 16(11), 1169-1175.
[http://dx.doi.org/10.1038/s41592-019-0586-5] [PMID: 31591580]
[123]
Song, L.; Yuan, X.; Jones, Z.; Griffin, K.; Zhou, Y.; Ma, T.; Li, Y. Assembly of human stem cell-derived cortical spheroids and vascular spheroids to model 3-D brain-like tissues. Sci. Rep., 2019, 9(1), 5977.
[http://dx.doi.org/10.1038/s41598-019-42439-9] [PMID: 30979929]
[124]
Pham, M.T.; Pollock, K.M.; Rose, M.D.; Cary, W.A.; Stewart, H.R.; Zhou, P.; Nolta, J.A.; Waldau, B. Generation of human vascularized brain organoids. Neuroreport, 2018, 29(7), 588-593.
[http://dx.doi.org/10.1097/WNR.0000000000001014] [PMID: 29570159]
[125]
Bergmann, S.; Lawler, S.E.; Qu, Y.; Fadzen, C.M.; Wolfe, J.M.; Regan, M.S.; Pentelute, B.L.; Agar, N.Y.R.; Cho, C.F. Blood–brain-barrier organoids for investigating the permeability of CNS therapeutics. Nat. Protoc., 2018, 13(12), 2827-2843.
[http://dx.doi.org/10.1038/s41596-018-0066-x] [PMID: 30382243]
[126]
Cho, A.N.; Jin, Y.; An, Y.; Kim, J.; Choi, Y.S.; Lee, J.S.; Kim, J.; Choi, W.Y.; Koo, D.J.; Yu, W.; Chang, G.E.; Kim, D.Y.; Jo, S.H.; Kim, J.; Kim, S.Y.; Kim, Y.G.; Kim, J.Y.; Choi, N.; Cheong, E.; Kim, Y.J.; Je, H.S.; Kang, H.C.; Cho, S.W. Microfluidic device with brain extracellular matrix promotes structural and functional maturation of human brain organoids. Nat. Commun., 2021, 12(1), 4730.
[http://dx.doi.org/10.1038/s41467-021-24775-5] [PMID: 34354063]
[127]
Salmon, I.; Grebenyuk, S.; Abdel, F.A.R.; Rustandi, G.; Pilkington, T.; Verfaillie, C.; Ranga, A. Engineering neurovascular organoids with 3D printed microfluidic chips. Lab Chip, 2022, 22(8), 1615-1629.
[http://dx.doi.org/10.1039/D1LC00535A] [PMID: 35333271]
[128]
Qian, X.; Nguyen, H.N.; Song, M.M.; Hadiono, C.; Ogden, S.C.; Hammack, C.; Yao, B.; Hamersky, G.R.; Jacob, F.; Zhong, C.; Yoon, K.; Jeang, W.; Lin, L.; Li, Y.; Thakor, J.; Berg, D.A.; Zhang, C.; Kang, E.; Chickering, M.; Nauen, D.; Ho, C.Y.; Wen, Z.; Christian, K.M.; Shi, P.Y.; Maher, B.J.; Wu, H.; Jin, P.; Tang, H.; Song, H.; Ming, G. Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell, 2016, 165(5), 1238-1254.
[http://dx.doi.org/10.1016/j.cell.2016.04.032] [PMID: 27118425]
[129]
Shahabipour, F.; Satta, S.; Mahmoodi, M.; Sun, A.; de Barros, N.R.; Li, S.; Hsiai, T.K.; Ashammakhi, N. Engineering organ-on-a-chip systems to model viral infections. Biofabrication, 2022.
[http://dx.doi.org/10.1088/1758-5090/ac6538] [PMID: 35390777]
[130]
Sun, A.M.; Hoffman, T.; Luu, B.Q.; Ashammakhi, N.; Li, S. Application of lung microphysiological systems to COVID-19 modeling and drug discovery: A review. Biodes. Manuf., 2021, 4(4), 757-775.
[http://dx.doi.org/10.1007/s42242-021-00136-5] [PMID: 34178414]
[131]
Buzhdygan, T.P.; DeOre, B.J.; Baldwin-Leclair, A.; Bullock, T.A.; McGary, H.M.; Khan, J.A.; Razmpour, R.; Hale, J.F.; Galie, P.A.; Potula, R.; Andrews, A.M.; Ramirez, S.H. The SARS-CoV-2 spike protein alters barrier function in 2D static and 3D microfluidic in-vitro models of the human blood–brain barrier. Neurobiol. Dis., 2020, 146, 105131.
[http://dx.doi.org/10.1016/j.nbd.2020.105131] [PMID: 33053430]
[132]
Pellegrini, L.; Albecka, A.; Mallery, D.L.; Kellner, M.J.; Paul, D.; Carter, A.P.; James, L.C.; Lancaster, M.A. SARS-CoV-2 infects the brain choroid plexus and disrupts the blood-CSF barrier in human brain organoids. Cell Stem Cell, 2020, 27(6), 951-961.e5.
[http://dx.doi.org/10.1016/j.stem.2020.10.001] [PMID: 33113348]
[133]
Ramani, A.; Müller, L.; Ostermann, P.N.; Gabriel, E.; Abida-Islam, P.; Müller-Schiffmann, A.; Mariappan, A.; Goureau, O.; Gruell, H.; Walker, A.; Andrée, M.; Hauka, S.; Houwaart, T.; Dilthey, A.; Wohlgemuth, K.; Omran, H.; Klein, F.; Wieczorek, D.; Adams, O.; Timm, J.; Korth, C.; Schaal, H.; Gopalakrishnan, J. SARS CoV 2 targets neurons of 3D human brain organoids. EMBO J., 2020, 39(20), e106230.
[http://dx.doi.org/10.15252/embj.2020106230] [PMID: 32876341]
[134]
Aird, W.C. Endothelium and haemostasis. Hamostaseologie, 2015, 35(1), 11-16.
[http://dx.doi.org/10.5482/HAMO-14-11-0075] [PMID: 25666572]
[135]
Flammer, A.J.; Anderson, T.; Celermajer, D.S.; Creager, M.A.; Deanfield, J.; Ganz, P.; Hamburg, N.M.; Lüscher, T.F.; Shechter, M.; Taddei, S.; Vita, J.A.; Lerman, A. The assessment of endothelial function: From research into clinical practice. Circulation, 2012, 126(6), 753-767.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.112.093245] [PMID: 22869857]
[136]
Davignon, J.; Ganz, P. Role of endothelial dysfunction in atherosclerosis. Circulation, 2004, 109(23)(Suppl. 1), III27-III32.
[PMID: 15198963]
[137]
Budhiraja, R.; Tuder, R.M.; Hassoun, P.M. Endothelial dysfunction in pulmonary hypertension. Circulation, 2004, 109(2), 159-165.
[http://dx.doi.org/10.1161/01.CIR.0000102381.57477.50] [PMID: 14734504]
[138]
Kim, S.K.; Moon, W.K.; Park, J.Y.; Jung, H. Inflammatory mimetic microfluidic chip by immobilization of cell adhesion molecules for T cell adhesion. Analyst (Lond.), 2012, 137(17), 4062-4068.
[http://dx.doi.org/10.1039/c2an35424a] [PMID: 22822477]
[139]
Colace, T.V.; Jobson, J.; Diamond, S.L. Relipidated tissue factor linked to collagen surfaces potentiates platelet adhesion and fibrin formation in a microfluidic model of vessel injury. Bioconjug. Chem., 2011, 22(10), 2104-2109.
[http://dx.doi.org/10.1021/bc200326v] [PMID: 21902184]
[140]
Shen, F.; Kastrup, C.J.; Liu, Y.; Ismagilov, R.F. Threshold response of initiation of blood coagulation by tissue factor in patterned microfluidic capillaries is controlled by shear rate. Arterioscler. Thromb. Vasc. Biol., 2008, 28(11), 2035-2041.
[http://dx.doi.org/10.1161/ATVBAHA.108.173930] [PMID: 18703776]
[141]
Wagner, D.D.; Frenette, P.S. The vessel wall and its interactions. Blood, 2008, 111(11), 5271-5281.
[http://dx.doi.org/10.1182/blood-2008-01-078204] [PMID: 18502843]
[142]
Kim, E.; Schueller, O.; Sweetnam, P.M. Targeting the leukocyte activation cascade: Getting to the site of inflammation using microfabricated assays. Lab Chip, 2012, 12(12), 2255-2264.
[http://dx.doi.org/10.1039/c2lc21078a] [PMID: 22437145]
[143]
Han, S.; Yan, J.J.; Shin, Y.; Jeon, J.J.; Won, J.; Eun Jeong, H.; Kamm, R.D.; Kim, Y.J.; Chung, S. A versatile assay for monitoring in vivo-like transendothelial migration of neutrophils. Lab Chip, 2012, 12(20), 3861-3865.
[http://dx.doi.org/10.1039/c2lc40445a] [PMID: 22903230]
[144]
Molteni, R.; Bianchi, E.; Patete, P.; Fabbri, M.; Baroni, G.; Dubini, G.; Pardi, R. A novel device to concurrently assess leukocyte extravasation and interstitial migration within a defined 3D environment. Lab Chip, 2015, 15(1), 195-207.
[http://dx.doi.org/10.1039/C4LC00741G] [PMID: 25337693]
[145]
Jain, N.G.; Wong, E.A.; Aranyosi, A.J.; Boneschansker, L.; Markmann, J.F.; Briscoe, D.M.; Irimia, D. Microfluidic mazes to characterize T-cell exploration patterns following activation in vitro. Integr. Biol., 2015, 7(11), 1423-1431.
[http://dx.doi.org/10.1039/C5IB00146C] [PMID: 26325525]
[146]
Hamza, B.; Irimia, D. Whole blood human neutrophil trafficking in a microfluidic model of infection and inflammation. Lab Chip, 2015, 15(12), 2625-2633.
[http://dx.doi.org/10.1039/C5LC00245A] [PMID: 25987163]
[147]
Preira, P.; Forel, J.M.; Robert, P.; Nègre, P.; Biarnes-Pelicot, M.; Xeridat, F.; Bongrand, P.; Papazian, L.; Theodoly, O. The leukocyte-stiffening property of plasma in early acute respiratory distress syndrome (ARDS) revealed by a microfluidic single-cell study: the role of cytokines and protection with antibodies. Crit. Care, 2015, 20(1), 8.
[http://dx.doi.org/10.1186/s13054-015-1157-5] [PMID: 26757701]
[148]
Kotz, K.T.; Xiao, W.; Miller-Graziano, C.; Qian, W.J.; Russom, A.; Warner, E.A.; Moldawer, L.L.; De, A.; Bankey, P.E.; Petritis, B.O.; Camp, D.G., II; Rosenbach, A.E.; Goverman, J.; Fagan, S.P.; Brownstein, B.H.; Irimia, D.; Xu, W.; Wilhelmy, J.; Mindrinos, M.N.; Smith, R.D.; Davis, R.W.; Tompkins, R.G.; Toner, M. Clinical microfluidics for neutrophil genomics and proteomics. Nat. Med., 2010, 16(9), 1042-1047.
[http://dx.doi.org/10.1038/nm.2205] [PMID: 20802500]
[149]
Levi, M.; Keller, T.T.; van Gorp, E.; ten Cate, H. Infection and inflammation and the coagulation system. Cardiovasc. Res., 2003, 60(1), 26-39.
[http://dx.doi.org/10.1016/S0008-6363(02)00857-X] [PMID: 14522404]
[150]
Ruggeri, Z.M. Platelet adhesion under flow. Microcirculation, 2009, 16(1), 58-83.
[http://dx.doi.org/10.1080/10739680802651477] [PMID: 19191170]
[151]
Westein, E.; van der Meer, A.D.; Kuijpers, M.J.E.; Frimat, J.P.; van den Berg, A.; Heemskerk, J.W.M. Atherosclerotic geometries exacerbate pathological thrombus formation poststenosis in a von Willebrand factor-dependent manner. Proc. Natl. Acad. Sci. USA, 2013, 110(4), 1357-1362.
[http://dx.doi.org/10.1073/pnas.1209905110] [PMID: 23288905]
[152]
Jain, A.; Barrile, R.; van der Meer, A.D.; Mammoto, A.; Mammoto, T.; Ceunynck, K.; Aisiku, O.; Otieno, M.A.; Louden, C.S.; Hamilton, G.A.; Flaumenhaft, R.; Ingber, D.E. Primary human lung alveolus on a chip model of intravascular thrombosis for assessment of therapeutics. Clin. Pharmacol. Ther., 2018, 103(2), 332-340.
[http://dx.doi.org/10.1002/cpt.742] [PMID: 28516446]
[153]
Katt, M.E.; Placone, A.L.; Wong, A.D.; Xu, Z.S.; Searson, P.C. In vitro tumor models: Advantages, disadvantages, variables, and selecting the right platform. Front. Bioeng. Biotechnol., 2016, 4, 12.
[http://dx.doi.org/10.3389/fbioe.2016.00012] [PMID: 26904541]
[154]
Shang, M.; Soon, R.H.; Lim, C.T.; Khoo, B.L.; Han, J. Microfluidic modelling of the tumor microenvironment for anti-cancer drug development. Lab Chip, 2019, 19(3), 369-386.
[http://dx.doi.org/10.1039/C8LC00970H] [PMID: 30644496]
[155]
Buchanan, C.F.; Verbridge, S.S.; Vlachos, P.P.; Rylander, M.N. Flow shear stress regulates endothelial barrier function and expression of angiogenic factors in a 3D microfluidic tumor vascular model. Cell Adhes. Migr., 2014, 8(5), 517-524.
[http://dx.doi.org/10.4161/19336918.2014.970001] [PMID: 25482628]
[156]
Calabrese, E.J.; Mattson, M.P. How does hormesis impact biology, toxicology, and medicine? NPJ Aging Mech. Dis., 2017, 3(1), 13.
[http://dx.doi.org/10.1038/s41514-017-0013-z] [PMID: 28944077]
[157]
Calabrese, E.J.; Iavicoli, I.; Calabrese, V. Hormesis: Why it is important to biogerontologists. Biogerontology, 2012, 13(3), 215-235.
[http://dx.doi.org/10.1007/s10522-012-9374-7] [PMID: 22270337]
[158]
Calabrese, V.; Cornelius, C.; Dinkova-Kostova, A.T.; Calabrese, E.J. Vitagenes, cellular stress response, and acetylcarnitine: Relevance to hormesis. Biofactors, 2009, 35(2), 146-160.
[http://dx.doi.org/10.1002/biof.22] [PMID: 19449442]
[159]
Calabrese, E.J.; Mattson, M.P.; Calabrese, V. Resveratrol commonly displays hormesis: Occurrence and biomedical significance. Hum. Exp. Toxicol., 2010, 29(12), 980-1015.
[http://dx.doi.org/10.1177/0960327110383625] [PMID: 21115559]

Rights & Permissions Print Cite
Article Metrics
53
2
World Autism Awareness Day
© 2024 Bentham Science Publishers | Privacy Policy