Sensors-integrated organ-on-a-chip for biomedical applications
)
Download citation
687
Views
87
Downloads
5
Crossref
5
WoS
5
Scopus
0
CSCD
As a promising new micro-physiological system, organ-on-a-chip has been widely utilized for in vitro pharmaceutical study and tissues engineering based on the three-dimensional constructions of tissues/organs and delicate replication of in vivo-like microenvironment. To better observe the biological processes, a variety of sensors have been integrated to realize in-situ, real-time, and sensitive monitoring of critical signals for organs development and disease modeling. Herein, we discuss the recent research advances made with respect to sensors-integrated organ-on-a-chip in this overall review. Firstly, we briefly explore the underlying fabrication procedures of sensors within microfluidic platforms and several classifications of sensory principles. Then, emphasis is put on the highlighted applications of different types of organ-on-a-chip incorporated with various sensors. Last but not least, perspective on the remaining challenges and future development of sensors-integrated organ-on-a-chip are presented.
menu
Sensors-integrated organ-on-a-chip for biomedical applications
)
Abstract
As a promising new micro-physiological system, organ-on-a-chip has been widely utilized for in vitro pharmaceutical study and tissues engineering based on the three-dimensional constructions of tissues/organs and delicate replication of in vivo-like microenvironment. To better observe the biological processes, a variety of sensors have been integrated to realize in-situ, real-time, and sensitive monitoring of critical signals for organs development and disease modeling. Herein, we discuss the recent research advances made with respect to sensors-integrated organ-on-a-chip in this overall review. Firstly, we briefly explore the underlying fabrication procedures of sensors within microfluidic platforms and several classifications of sensory principles. Then, emphasis is put on the highlighted applications of different types of organ-on-a-chip incorporated with various sensors. Last but not least, perspective on the remaining challenges and future development of sensors-integrated organ-on-a-chip are presented.
References(164)
Ronaldson-Bouchard, K.; Vunjak-Novakovic, G. Organs-on-a-chip: A fast track for engineered human tissues in drug development. Cell Stem Cell 2018, 22, 310–324.
Young, A. T.; Rivera, K. R.; Erb, P. D.; Daniele, M. A. Monitoring of microphysiological systems: Integrating sensors and real-time data analysis toward autonomous decision-making. ACS Sens. 2019, 4, 1454–1464.
Kieninger, J.; Weltin, A.; Flamm, H.; Urban, G. A. Microsensor systems for cell metabolism—From 2D culture to organ-on-chip. Lab Chip 2018, 18, 1274–1291.
Park, S. E.; Georgescu, A.; Huh, D. Organoids-on-a-chip. Science 2019, 364, 960–965.
Manz, A.; Graber, N.; Widmer, H. M. Miniaturized total chemical analysis systems: A novel concept for chemical sensing. Sens. Actuators B:Chem. 1990, 1, 244–248.
van der Meer, A. D.; van den Berg, A. Organs-on-chips: Breaking the in vitro impasse. Integr. Biol. 2012, 4, 461–470.
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, e1142493.
Sutterby, E.; Thurgood, P.; Baratchi, S.; Khoshmanesh, K.; Pirogova, E. Microfluidic skin-on-a-chip models: Toward biomimetic artificial skin. Small 2020, 16, 2002515.
Marrero, D.; Pujol-Vila, F.; Vera, D.; Gabriel, G.; Illa, X.; Elizalde-Torrent, A.; Alvarez, M.; Villa, R. Gut-on-a-chip: Mimicking and monitoring the human intestine. Biosens. Bioelectron. 2021, 181, 113156.
Wang, X. D.; Wolfbeis, O. S.; Meier, R. J. Luminescent probes and sensors for temperature. Chem. Soc. Rev. 2013, 42, 7834–7869.
Herreros, P.; Tapia-González, S.; Sánchez-Olivares, L.; Laguna Heras, M. F.; Holgado, M. Alternative brain slice-on-a-chip for organotypic culture and effective fluorescence injection testing. Int. J. Mol. Sci. 2022, 23, 2549.
Fuchs, S.; Johansson, S.; Tjell, A. Ø.; Werr, G.; Mayr, T.; Tenje, M. In-line analysis of organ-on-chip systems with sensors: Integration, fabrication, challenges, and potential. ACS Biomater. Sci. Eng. 2021, 7, 2926–2948.
Zhang, B. Y.; Korolj, A.; Lai, B. F. L., Radisic, M. Advances in organ-on-a-chip engineering. Nat. Rev. Mater. 2018, 3, 257–278.
Santbergen, M. J. C.; van der Zande, M.; Bouwmeester, H.; Nielen, M. W. F. Online and in situ analysis of organs-on-a-chip. TrAC Trends Anal. Chem. 2019, 115, 138–146.
Kratz, S. R. A.; Höll, G.; Schuller, P.; Ertl, P.; Rothbauer, M. Latest trends in biosensing for microphysiological organs-on-a-chip and body-on-a-chip systems. Biosensors 2019, 9, 110.
Clarke, G. A.; Hartse, B. X.; Asli, A. E. N.; Taghavimehr, M.; Hashemi, N.; Shirsavar, M. A.; Montazami, R.; Alimoradi, N.; Nasirian, V.; Ouedraogo, L. J. et al. Advancement of sensor integrated organ-on-chip devices. Sensors 2021, 21, 1367.
Niculescu, A. G.; Chircov, C.; Bîrcă, A. C.; Grumezescu, A. M. Fabrication and applications of microfluidic devices: A review. Int. J. Mol. Sci. 2021, 22, 2011.
Shan, C.; Zhang, C. J.; Liang, J.; Yang, Q.; Bian, H.; Yong, J. L.; Hou, X.; Chen, F. Femtosecond laser hybrid fabrication of a 3D microfluidic chip for PCR application. Opt. Express 2020, 28, 25716–25722.
Khoshmanesh, K.; Tang, S. Y.; Zhu, J. Y.; Schaefer, S.; Mitchell, A.; Kalantar-Zadeh, K.; Dickey, M. D. Liquid metal enabled microfluidics. Lab Chip 2017, 17, 974–993.
Gao, M.; Gui, L. Development of a fast thermal response microfluidic system using liquid metal. J. Micromechan. Microeng. 2016, 26, 075005.
Ma, Z. C.; Zhang, Y. L.; Han, B.; Liu, X. Q.; Zhang, H. Z.; Chen, Q. D.; Sun, H. B. Femtosecond laser direct writing of plasmonic Ag/Pd alloy nanostructures enables flexible integration of robust SERS substrates. Adv. Mater. Technol. 2017, 2, 1600270.
Fu, L. M.; Ju, W. J.; Yang, R. J.; Wang, Y. N. Rapid prototyping of glass-based microfluidic chips utilizing two-pass defocused CO2 laser beam method. Microfluid. Nanofluid. 2013, 14, 479–487.
Chen, L. X.; Luo, G. A.; Liu, K. H.; Ma, J. P.; Yao, B.; Yan, Y. C.; Wang, Y. M. Bonding of glass-based microfluidic chips at low- or room-temperature in routine laboratory. Sens. Actuators B:Chem. 2006, 119, 335–344.
Tahirbegi, I. B.; Ehgartner, J.; Sulzer, P.; Zieger, S.; Kasjanow, A.; Paradiso, M.; Strobl, M.; Bouwes, D.; Mayr, T. Fast pesticide detection inside microfluidic device with integrated optical pH, oxygen sensors and algal fluorescence. Biosens. Bioelectron. 2017, 88, 188–195.
Ma, X. Q.; Li, R.; Jin, Z. M.; Fan, Y. Q.; Zhou, X. C.; Zhang, Y. J. Injection molding and characterization of PMMA-based microfluidic devices. Microsyst. Technol. 2020, 26, 1317–1324.
Hamad, E. M.; Bilatto, S. E. R.; Adly, N. Y.; Correa, D. S.; Wolfrum, B.; Schöning, M. J.; Offenhäusser, A.; Yakushenko, A. Inkjet printing of UV-curable adhesive and dielectric inks for microfluidic devices. Lab Chip 2016, 16, 70–74.
Shen, C.; Li, Y. J.; Wang, Y.; Meng, Q. Non-swelling hydrogel-based microfluidic chips. Lab Chip 2019, 19, 3962–3973.
Krutkramelis, K.; Xia, B.; Oakey, J. Monodisperse polyethylene glycol diacrylate hydrogel microsphere formation by oxygen-controlled photopolymerization in a microfluidic device. Lab Chip 2016, 16, 1457–1465.
Bhusal, A.; Dogan, E.; Nguyen, H. A.; Labutina, O.; Nieto, D.; Khademhosseini, A.; Miri, A. K. Multi-material digital light processing bioprinting of hydrogel-based microfluidic chips. Biofabrication 2022, 14, 014103.
Han, J. L.; Qi, A. J.; Zhou, J. R.; Wang, G.; Li, B. W.; Chen, L. X. Simple way to fabricate novel paper-based valves using plastic comb binding spines. ACS Sens. 2018, 3, 1789–1794.
Li, X.; Qin, Z.; Fu, H.; Li, T.; Peng, R.; Li, Z. J.; Rini, J. M.; Liu, X. Y. Enhancing the performance of paper-based electrochemical impedance spectroscopy nanobiosensors: An experimental approach. Biosens. Bioelectron. 2021, 177, 112672.
Dou, M. W.; Sanjay, S. T.; Benhabib, M.; Xu, F.; Li, X. J. Low-cost bioanalysis on paper-based and its hybrid microfluidic platforms. Talanta 2015, 145, 43–54.
Qi, J.; Li, B. W.; Wang, X. Y.; Fu, L. W.; Luo, L. Q.; Chen, L. X. Rotational paper-based microfluidic-chip device for multiplexed and simultaneous fluorescence detection of phenolic pollutants based on a molecular-imprinting technique. Anal. Chem. 2018, 90, 11827–11834.
Liu, P.; Li, B. W.; Fu, L. W.; Huang, Y.; Man, M. S.; Qi, J.; Sun, X. Y.; Kang, Q.; Shen, D. Z.; Chen, L. X. Hybrid three dimensionally printed paper-based microfluidic platform for investigating a cell’s apoptosis and intracellular cross-talk. ACS Sens. 2020, 5, 464–473.
Yin, P. J.; Zhao, L.; Chen, Z. Z.; Jiao, Z. Q.; Shi, H. Y.; Hu, B.; Yuan, S. F.; Tian, J. Simulation and practice of particle inertial focusing in 3D-printed serpentine microfluidic chips via commercial 3D-printers. Soft Matter 2020, 16, 3096–3105.
Kotz, F.; Mader, M.; Dellen, N.; Risch, P.; Kick, A.; Helmer, D.; Rapp, B. E. Fused deposition modeling of microfluidic chips in polymethylmethacrylate. Micromachines 2020, 11, 873.
Song, K. N.; Li, G. Q.; Zu, X. Y.; Du, Z.; Liu, L. Y.; Hu, Z. G. The fabrication and application mechanism of microfluidic systems for high throughput biomedical screening: A review. Micromachines 2020, 11, 297.
Rothbauer, M.; Zirath, H.; Ertl, P. Recent advances in microfluidic technologies for cell-to-cell interaction studies. Lab Chip 2018, 18, 249–270.
Puryear III, J. R.; Yoon, J. K.; Kim, Y. Advanced fabrication techniques of microengineered physiological systems. Micromachines 2020, 11, 730.
Thakare, K.; Jerpseth, L.; Pei, Z. J.; Elwany, A.; Quek, F.; Qin, H. M. Bioprinting of organ-on-chip systems: A literature review from a manufacturing perspective. J. Manuf. Mater. Process. 2021, 5, 91.
Mi, S. L.; Du, Z. C.; Xu, Y. Y.; Sun, W. The crossing and integration between microfluidic technology and 3D printing for organ-on-chips. J. Mater. Chem. B 2018, 6, 6191–6206.
Kristensen, A.; Yang, J. K. W.; Bozhevolnyi, S. I.; Link, S.; Nordlander, P.; Halas, N. J.; Mortensen, N. A. Plasmonic colour generation. Nat. Rev. Mater. 2016, 2, 16088.
Garcia, R.; Knoll, A. W.; Riedo, E. Advanced scanning probe lithography. Nat. Nanotechnol. 2014, 9, 577–587.
Kooy, N.; Mohamed, K.; Pin, L. T.; Guan, O. S. A review of roll-to-roll nanoimprint lithography. Nanoscale Res. Lett. 2014, 9, 320.
Gan, Z. S.; Cao, Y. Y.; Evans, R. A.; Gu, M. Three-dimensional deep sub-diffraction optical beam lithography with 9 nm feature size. Nat. Commun. 2013, 4, 2061.
Ji, X. Y.; Ge, L. L.; Liu, C.; Tang, Z. M.; Xiao, Y. F.; Chen, W.; Lei, Z. Y.; Gao, W.; Blake, S.; De, D. B. et al. Capturing functional two-dimensional nanosheets from sandwich-structure vermiculite for cancer theranostics. Nat. Commun. 2021, 12, 1124.
Jawaid, A.; Hassan, A.; Neher, G.; Nepal, D.; Pachter, R.; Kennedy, W. J.; Ramakrishnan, S.; Vaia, R. A. Halogen etch of Ti3AlC2 MAX phase for MXene fabrication. ACS Nano 2021, 15, 2771–2777.
Pei, J. J.; Gai, X.; Yang, J.; Wang, X. B.; Yu, Z. F.; Choi, D. Y.; Luther-Davies, B.; Lu, Y. R. Producing air-stable monolayers of phosphorene and their defect engineering. Nat. Commun. 2016, 7, 10450.
Wang, Y. Y.; Zhang, Y. Q.; Liu, Z. J.; Xie, C.; Feng, S.; Liu, D. D.; Shao, M. F.; Wang, S. Y. Layered double hydroxide nanosheets with multiple vacancies obtained by dry exfoliation as highly efficient oxygen evolution electrocatalysts. Angew. Chem., Int. Ed. 2017, 56, 5867–5871.
Schwab, A.; Levato, R.; D'Este, M.; Piluso, S.; Eglin, D.; Malda, J. Printability and shape fidelity of bioinks in 3D bioprinting. Chem. Rev. 2020, 120, 11028–11055.
Kasani, S.; Curtin, K.; Wu, N. Q. A review of 2D and 3D plasmonic nanostructure array patterns: Fabrication, light management and sensing applications. Nanophotonics 2019, 8, 2065–2089.
Kümmel, F.; ten Hagen, B.; Wittkowski, R.; Buttinoni, I.; Eichhorn, R.; Volpe, G.; Löwen, H.; Bechinger, C. Circular motion of asymmetric self-propelling particles. Phys. Rev. Lett. 2013, 110, 198302.
Wehner, M.; Truby, R. L.; Fitzgerald, D. J.; Mosadegh, B.; Whitesides, G. M.; Lewis, J. A.; Wood, R. J. An integrated design and fabrication strategy for entirely soft, autonomous robots. Nature 2016, 536, 451–455.
Bhattacharjee, N.; Urrios, A.; Kang, S.; Folch, A. The upcoming 3D-printing revolution in microfluidics. Lab Chip 2016, 16, 1720–1742.
Lin, M. H.; Wang, J. J.; Zhou, G. B.; Wang, J. B.; Wu, N.; Lu, J. X.; Gao, J. M.; Chen, X. Q.; Shi, J. Y.; Zuo, X. L. et al. Programmable engineering of a biosensing interface with tetrahedral DNA nanostructures for ultrasensitive DNA detection. Angew. Chem., Int. Ed. 2015, 54, 2151–2155.
Peroz, C.; Dhuey, S.; Cornet, M.; Vogler, M.; Olynick, D.; Cabrini, S. Single digit nanofabrication by step-and-repeat nanoimprint lithography. Nanotechnology 2012, 23, 015305.
Rolland, J. P.; Hagberg, E. C.; Denison, G. M.; Carter, K. R.; De Simone, J. M. High-resolution soft lithography: Enabling materials for nanotechnologies. Angew. Chem., Int. Ed. 2004, 43, 5796–5799.
Zhou, W. M.; Min, G. Q.; Zhang, J.; Liu, Y. B.; Wang, J. H.; Zhang, Y. P.; Sun, F. Nanoimprint lithography: A processing technique for nanofabrication advancement. Nano-Micro Letters 2011, 3, 135–140.
Li, J. H.; Wu, C. T.; Chu, P. K.; Gelinsky, M. 3D printing of hydrogels:Rational design strategies and emerging biomedical applications. Mate. Sci. Eng: R: Rep. 2020, 140, 100543.
Zhou, L. Y.; Fu, J. Z.; He, Y. A review of 3D printing technologies for soft polymer materials. Adv. Funct. Mater. 2020, 30, 2000187.
Li, J. H.; Pumera, M. 3D printing of functional microrobots. Chem Soc Rev. 2021, 50, 2794–2838.
Quan, H. Y.; Zhang, T.; Xu, H.; Luo, S.; Nie, J.; Zhu, X. Q. Photo-curing 3D printing technique and its challenges. Bioact. Mater. 2020, 5, 110–115.
Wu, H.; Fahy, W. P.; Kim, S.; Kim, H.; Zhao, N.; Pilato, L.; Kafi, A.; Bateman, S.; Koo, J. H. Recent developments in polymers/polymer nanocomposites for additive manufacturing. Prog. Mater. Sci. 2020, 111, 100638.
Zakeri, S.; Vippola, M.; Levänen, E. A comprehensive review of the photopolymerization of ceramic resins used in stereolithography. Addit. Manuf. 2020, 35, 101177.
Lim, K. S.; Galarraga, J. H.; Cui, X. L.; Lindberg, G. C. J.; Burdick, J. A.; Woodfield, T. B. F. Fundamentals and applications of photo-cross-linking in bioprinting. Chem. Rev. 2020, 120, 10662–10694.
Zhu, W.; Ma, X. Y.; Gou, M. L.; Mei, D. Q.; Zhang, K.; Chen, S. C. 3D printing of functional biomaterials for tissue engineering. Curr Opin Biotechnol. 2016, 40, 103–112.
Ozbolat, I. T.; Hospodiuk, M. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials 2016, 76, 321–343.
Li, X. D.; Liu, B. X.; Pei, B.; Chen, J. W.; Zhou, D. Z.; Peng, J. Y.; Zhang, X. Z.; Jia, W.; Xu, T. Inkjet bioprinting of biomaterials. Chem. Rev. 2020, 120, 10793–10833.
Yamada, K.; Henares, T. G.; Suzuki, K.; Citterio, D. Paper-based inkjet-printed microfluidic analytical devices. Angew. Chem., Int. Ed. 2015, 54, 5294–5310.
Cummins, G.; Desmulliez, M. P. Y. Inkjet printing of conductive materials: A review. Circuit World 2012, 38, 193–213.
Guimarães, C. F.; Ahmed, R.; Marques, A. P.; Reis, R. L.; Demirci, U. Engineering hydrogel-based biomedical photonics: Design, fabrication, and applications. Adv. Mater. 2021, 33, 2006582.
Arrigoni, C.; Lopa, S.; Candrian, C.; Moretti, M. Organs-on-a-chip as model systems for multifactorial musculoskeletal diseases. Curr. Opin. Biotechnol. 2020, 63, 79–88.
Jin, Z. H.; Liu, Y. L.; Fan, W. T.; Huang, W. H. Integrating flexible electrochemical sensor into microfluidic chip for simulating and monitoring vascular mechanotransduction. Small 2020, 16, 1903204.
Zhao, Y. M.; Wang, E. Y.; Davenport, L. H.; Liao, Y.; Yeager, K.; Vunjak-Novakovic, G.; Radisic, M.; Zhang, B. Y. A multimaterial microphysiological platform enabled by rapid casting of elastic microwires. Adv. Healthc. Mater. 2019, 8, 1801187.
Lind, J. U.; Busbee, T. A.; Valentine, A. D.; Pasqualini, F. S.; Yuan, H. Y.; Yadid, M.; Park, S. J.; Kotikian, A.; Nesmith, A. P.; Campbell, P. H. et al. Instrumented cardiac microphysiological devices via multimaterial three-dimensional printing. Nat. Mater. 2017, 16, 303–308.
Liu, H. J.; MacQueen, L. A.; Usprech, J. F.; Maleki, H.; Sider, K. L.; Doyle, M. G.; Sun, Y.; Simmons, C. A. Microdevice arrays with strain sensors for 3D mechanical stimulation and monitoring of engineered tissues. Biomaterials 2018, 172, 30–40.
Chen, Y. F.; Chan, H. N.; Michael, S. A.; Shen, Y. S.; Chen, Y.; Tian, Q.; Huang, L.; Wu, H. K. A microfluidic circulatory system integrated with capillary-assisted pressure sensors. Lab Chip 2017, 17, 653–662.
Manjakkal, L.; Szwagierczak, D.; Dahiya, R. Metal oxides based electrochemical pH sensors: Current progress and future perspectives. Prog. Mater. Sci. 2020, 109, 100635.
Lee, C. S.; Kim, S. K.; Kim, M. Ion-sensitive field-effect transistor for biological sensing. Sensors 2009, 9, 7111–7131.
Gkoupidenis, P.; Schaefer, N.; Garlan, B.; Malliaras, G. G. Neuromorphic functions in PEDOT: PSS organic electrochemical transistors. Adv. Mater. 2015, 27, 7176–7180.
Curto, V. F.; Marchiori, B.; Hama, A.; Pappa, A. M.; Ferro, M. P.; Braendlein, M.; Rivnay, J.; Fiocchi, M.; Malliaras, G. G.; Ramuz, M. et al. Organic transistor platform with integrated microfluidics for in-line multi-parametric in vitro cell monitoring. Microsyst. Nanoeng. 2017, 3, 17028.
Bavli, D.; Prill, S.; Ezra, E.; Levy, G.; Cohen, M.; Vinken, M.; Vanfleteren, J.; Jaeger, M.; Nahmias, Y. Real-time monitoring of metabolic function in liver-on-chip microdevices tracks the dynamics of mitochondrial dysfunction. Proc. Natl. Acad. Sci. USA 2016, 113, E2231–E2240.
Steinegger, A.; Wolfbeis, O. S.; Borisov, S. M. Optical sensing and imaging of pH values: Spectroscopies, materials, and applications. Chem. Rev. 2020, 120, 12357–12489.
Arandian, A.; Bagheri, Z.; Ehtesabi, H.; Nobar, S. N.; Aminoroaya, N.; Samimi, A.; Latifi, H. Optical imaging approaches to monitor static and dynamic cell-on-chip platforms: A tutorial review. Small 2019, 15, 1900737.
Grate, J. W.; Egorov, O. B.; O'Hara, M. J.; Devol, T. A. Radionuclide sensors for environmental monitoring: From flow injection solid-phase absorptiometry to equilibration-based preconcentrating minicolumn sensors with radiometric detection. Chem. Rev. 2008, 108, 543–562.
Shaegh, S. A. M.; De Ferrari, F.; Zhang, Y. S.; Nabavinia, M.; Mohammad, N. B.; Ryan, J.; Pourmand, A.; Laukaitis, E.; Sadeghian, R. B.; Nadhman, A. et al. A microfluidic optical platform for real-time monitoring of pH and oxygen in microfluidic bioreactors and organ-on-chip devices. Biomicrofluidics 2016, 10, 044111.
Armstrong, E.; O'Dwyer, C. Artificial opal photonic crystals and inverse opal structures—Fundamentals and applications from optics to energy storage. J. Mater. Chem. C 2015, 3, 6109–6143.
Shang, Y. X.; Chen, Z. Y.; Fu, F. F.; Sun, L. Y.; Shao, C. M.; Jin, W.; Liu, H.; Zhao, Y. J. Cardiomyocyte-driven structural color actuation in anisotropic inverse opals. ACS Nano 2019, 13, 796–802.
Hu, Z. C.; Deibert, B. J.; Li, J. Luminescent metal-organic frameworks for chemical sensing and explosive detection. Chem. Soc. Rev. 2014, 43, 5815–5840.
Perottoni, S.; Neto, N. G. B.; Di Nitto, C.; Dmitriev, R. I.; Raimondi, M. T.; Monaghan, M. G. Intracellular label-free detection of mesenchymal stem cell metabolism within a perivascular niche-on-a-chip. Lab Chip 2021, 21, 1395–1408.
Yang, Q. Z.; Xiao, Z. F.; Lv, X. M.; Zhang, T. T.; Liu, H. Fabrication and biomedical applications of heart-on-a-chip. Int. J. Bioprint. 2021, 7, 54–70.
Wan, H.; Gu, C. L.; Gan, Y.; Wei, X. W.; Zhu, K.; Hu, N.; Wang, P. Sensor-free and sensor-based heart-on-a-chip platform: A review of design and applications. Curr. Pharm. Des. 2018, 24, 5375–5385.
Cho, K. W.; Lee, W. H.; Kim, B. S.; Kim, D. H. Sensors in heart-on-a-chip: A review on recent progress. Talanta 2020, 219, 121269.
Beussman, K. M.; Rodriguez, M. L.; Leonard, A.; Taparia, N.; Thompson, C. R.; Sniadecki, N. J. Micropost arrays for measuring stem cell-derived cardiomyocyte contractility. Methods 2016, 94, 43–50.
Fu, F. F.; Shang, L. R.; Chen, Z. Y.; Yu, Y. R.; Zhao, Y. J. Bioinspired living structural color hydrogels. Sci. Robot. 2018, 3, eaar8580.
Wang, L.; Dou, W. K.; Malhi, M.; Zhu, M.; Liu, H. J.; Plakhotnik, J.; Xu, Z. S.; Zhao, Q. L.; Chen, J.; Chen, S. Y. et al. Microdevice platform for continuous measurement of contractility, beating rate, and beating rhythm of human-induced pluripotent stem cell-cardiomyocytes inside a controlled incubator environment. ACS Appl. Mater. Interfaces 2018, 10, 21173–21183.
Qian, F.; Huang, C.; Lin, Y. D.; Ivanovskaya, A. N.; O’Hara, T. J.; Booth, R. H.; Creek, C. J.; Enright, H. A.; Soscia, D. A.; Belle, A. M. et al. Simultaneous electrical recording of cardiac electrophysiology and contraction on chip. Lab Chip 2017, 17, 1732–1739.
Huebsch, N.; Charrez, B.; Neiman, G.; Siemons, B.; Boggess, S. C.; Wall, S.; Charwat, V.; Jæger, K. H.; Cleres, D.; Telle, Å. et al. Metabolically driven maturation of human-induced-pluripotent-stem-cell-derived cardiac microtissues on microfluidic chips. Nat. Biomed. Eng. 2022, 6, 372–388.
Xie, C.; Lin, Z. L.; Hanson, L.; Cui, Y.; Cui, B. X. Intracellular recording of action potentials by nanopillar electroporation. Nat. Nanotechnol. 2012, 7, 185–190.
Kireev, D.; Seyock, S.; Lewen, J.; Maybeck, V.; Wolfrum, B.; Offenhäusser, A. Graphene multielectrode arrays as a versatile tool for extracellular measurements. Adv. Healthc. Mater. 2017, 6, 1601433.
Liu, S. F.; Xia, X. H.; Yao, Z. J.; Wu, J. B.; Zhang, L. Y.; Deng, S. J.; Zhou, C. G.; Shen, S. H.; Wang, X. L.; Tu, J. P. Straw-brick-like carbon fiber cloth/lithium composite electrode as an advanced lithium metal anode. Small Methods 2018, 2, 1800035.
Hai, A.; Shappir, J.; Spira, M. E. In-cell recordings by extracellular microelectrodes. Nat. Methods 2010, 7, 200–202.
Xu, D. X.; Fang, J. R.; Zhang, M. Y.; Xia, Q. J.; Li, H. B.; Hu, N. Porous polyethylene terephthalate nanotemplate electrodes for sensitive intracellular recording of action potentials. Nano Lett. 2022, 22, 2479–2489.
Abbott, J.; Ye, T. Y.; Qin, L.; Jorgolli, M.; Gertner, R. S.; Ham, D.; Park, H. CMOS nanoelectrode array for all-electrical intracellular electrophysiological imaging. Nat. Nanotechnol. 2017, 12, 460–466.
Dou, W. K.; Malhi, M.; Cui, T.; Wang, M. Y.; Wang, T. C.; Shan, G. Q.; Law, J.; Gong, Z. Y.; Plakhotnik, J.; Filleter, T. et al. A carbon-based biosensing platform for simultaneously measuring the contraction and electrophysiology of iPSC-cardiomyocyte monolayers. ACS Nano 2022, 16, 11278–11290.
Lee, S.; Sasaki, D.; Kim, D.; Mori, M.; Yokota, T.; Lee, H.; Park, S.; Fukuda, K.; Sekino, M.; Matsuura, K. et al. Ultrasoft electronics to monitor dynamically pulsing cardiomyocytes. Nat. Nanotechnol. 2019, 14, 156–160.
Ding, S.; Zhang, H. J.; Wang, X. M. Microfluidic-chip-integrated biosensors for lung disease models. Biosensors 2021, 11, 456.
Schilders, K. A. A.; Eenjes, E.; van Riet, S.; Poot, A. A.; Stamatialis, D.; Truckenmüller, R.; Hiemstra, P. S.; Rottier, R. J. Regeneration of the lung: Lung stem cells and the development of lung mimicking devices. Respir. Res. 2016, 17, 44.
Wang, Y. Q.; Wang, P.; Qin, J. H. Microfluidic organs-on-a-chip for modeling human infectious diseases. Acc. Chem. Res. 2021, 54, 3550–3562.
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, 1662–1668.
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. et al. Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro. Nat Methods 2016, 13, 151–157.
Zhu, Y. J.; Sun, L. Y.; Wang, Y.; Cai, L. J.; Zhang, Z. H.; Shang, Y. X.; Zhao, Y. J. A biomimetic human lung-on-a-chip with colorful display of microphysiological breath. Adv. Mater. 2022, 34, 2108972.
Henry, O. Y. F.; Villenave, R.; Cronce, M. J.; Leineweber, W. D.; Benz, M. A.; Ingber, D. E. Organs-on-chips with integrated electrodes for trans-epithelial electrical resistance (TEER) measurements of human epithelial barrier function. Lab Chip 2017, 17, 2264–2271.
Huang, D.; Liu, T. T.; Liao, J. L.; Maharjan, S.; Xie, X.; Pérez, M.; Anaya, I.; Wang, S. W.; Mayer, A. T.; Kang, Z. X. et al. Reversed-engineered human alveolar lung-on-a-chip model. Proc. Natl. Acad. Sci. USA 2021, 118, e2016146118.
Benam, K. H.; Novak, R.; Nawroth, J.; Hirano-Kobayashi, M.; Ferrante, T. C.; Choe, Y.; Prantil-Baun, R.; Weaver, J. C.; Bahinski, A.; Parker, K. K. et al. Matched-comparative modeling of normal and diseased human airway responses using a microengineered breathing lung chip. Cell Syst. 2016, 3, 456–466.e4.
Chen, P. Y.; Hsieh, M. J.; Liao, Y. H.; Lin, Y. C.; Hou, Y. T. Liver-on-a-chip platform to study anticancer effect of statin and its metabolites. Biochem. Eng. J. 2021, 165, 107831.
Banaeiyan, A. A.; Theobald, J.; Paukštyte, J.; Wölfl, S.; Adiels, C. B.; Goksör, M. Design and fabrication of a scalable liver-lobule-on-a-chip microphysiological platform. Biofabrication 2017, 9, 015014.
Deng, J.; Wei, W. B.; Chen, Z. Z.; Lin, B. C.; Zhao, W. J.; Luo, Y.; Zhang, X. L. Engineered liver-on-a-chip platform to mimic liver functions and its biomedical applications: A review. Micromachines 2019, 10, 676.
Kulkeaw, K.; Pengsart, W. Progress and challenges in the use of a liver-on-a-chip for hepatotropic infectious diseases. Micromachines 2021, 12, 842.
Shin, S. R.; Kilic, T.; Zhang, Y. S.; Avci, H.; Hu, N.; Kim, D.; Branco, C.; Aleman, J.; Massa, S.; Silvestri, A. et al. Label-free and regenerative electrochemical microfluidic biosensors for continual monitoring of cell secretomes. Adv. Sci. 2017, 4, 1600522.
Asif, A.; Park, S. H.; Soomro, A. M.; Khalid, M. A. U.; Salih, A. R. C.; Kang, B.; Ahmed, F.; Kim, K. H.; Choi, K. H. Microphysiological system with continuous analysis of albumin for hepatotoxicity modeling and drug screening. J. Ind. Eng. Chem. 2021, 98, 318–326.
Meissner, R.; Eker, B.; Kasi, H.; Bertsch, A.; Renaud, P. Distinguishing drug-induced minor morphological changes from major cellular damage via label-free impedimetric toxicity screening. Lab Chip 2011, 11, 2352–2361.
Moya, A.; Ortega-Ribera, M.; Guimerà, X.; Sowade, E.; Zea, M.; Illa, X.; Ramon, E.; Villa, R.; Gracia-Sancho, J.; Gabriel, G. Online oxygen monitoring using integrated inkjet-printed sensors in a liver-on-a-chip system. Lab Chip 2018, 18, 2023–2035.
Karimi, M.; Bahrami, S.; Mirshekari, H.; Basri, S. M. M.; Nik, A. B.; Aref, A. R.; Akbari, M.; Hamblin, M. R. Microfluidic systems for stem cell-based neural tissue engineering. Lab Chip 2016, 16, 2551–2571.
Wan, J. D.; Zhou, S. T.; Mea, H. J.; Guo, Y. J.; Ku, H.; Urbina, B. M. Emerging roles of microfluidics in brain research: From cerebral fluids manipulation to brain-on-a-chip and neuroelectronic devices engineering. Chem. Rev. 2022, 122, 7142–7181.
Bang, S.; Jeong, S.; Choi, N.; Kim, H. N. Brain-on-a-chip: A history of development and future perspective. Biomicrofluidics 2019, 13, 051301.
Brown, T. D.; Nowak, M.; Bayles, A. V.; Prabhakarpandian, B.; Karande, P.; Lahann, J.; Helgeson, M. E.; Mitragotri, S. A microfluidic model of human brain (μHuB) for assessment of blood brain barrier. Bioeng. Transl. Med. 2019, 4, e10126.
Wang, J. D.; Khafagy, E. S.; Khanafer, K.; Takayama, S.; Elsayed, M. E. H. Organization of endothelial cells, pericytes, and astrocytes into a 3D microfluidic in vitro model of the blood-brain barrier. Mol. Pharmaceutics 2016, 13, 895–906.
Wang, X. B.; Hou, Y.; Ai, X. P.; Sun, J. Y.; Xu, B. J.; Meng, X. L.; Zhang, Y.; Zhang, S. Y. Potential applications of microfluidics based blood brain barrier (BBB)-on-chips for in vitro drug development. Biomed. Pharmacother. 2020, 132, 110822.
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, 184–194.
Sticker, D.; Rothbauer, M.; Ehgartner, J.; Steininger, C.; Liske, O.; Liska, R.; Neuhaus, W.; Mayr, T.; Haraldsson, T.; Kutter, J. P. et al. Oxygen management at the microscale: A functional biochip material with long-lasting and tunable oxygen scavenging properties for cell culture applications. ACS Appl. Mater. Interfaces 2019, 11, 9730–9739.
Kafi, M. A.; Cho, H. Y.; Choi, J. W. Engineered peptide-based nanobiomaterials for electrochemical cell chip. Nano Converg. 2016, 3, 17.
Kafi, M. A.; Kim, T. H.; An, J. H.; Choi, J. W. Fabrication of cell chip for detection of cell cycle progression based on electrochemical method. Anal. Chem. 2011, 83, 2104–2111.
Andrzejewska, A.; Nowakowski, A.; Grygorowicz, T.; Dabrowska, S.; Orzel, J.; Walczak, P.; Lukomska, B.; Janowski, M. Single-cell, high-throughput analysis of cell docking to vessel wall. J. Cereb. Blood Flow Metab. 2019, 39, 2308–2320.
Zhang, S.; Wan, Z. P.; Kamm, R. D. Vascularized organoids on a chip: Strategies for engineering organoids with functional vasculature. Lab Chip 2021, 21, 473–488.
Booth, R.; Kim, H. Characterization of a microfluidic in vitro model of the blood-brain barrier (μBBB). Lab Chip 2012, 12, 1784–1792.
Skardal, A.; Shupe, T.; Atala, A. Organoid-on-a-chip and body-on-a-chip systems for drug screening and disease modeling. Drug Discov. Today 2016, 21, 1399–1411.
Kim, Y.; Lobatto, M. E.; Kawahara, T.; Chung, B. L.; Mieszawska, A. J.; Sanchez-Gaytan, B. L.; Fay, F.; Senders, M. L.; Calcagno, C.; Becraft, J. et al. Probing nanoparticle translocation across the permeable endothelium in experimental atherosclerosis. Proc. Natl. Acad. Sci. USA 2014, 111, 1078–1083.
Zheng, W. F.; Jiang, B.; Wang, D.; Zhang, W.; Wang, Z.; Jiang, X. Y. A microfluidic flow-stretch chip for investigating blood vessel biomechanics. Lab Chip 2012, 12, 3441–3450.
Mandrycky, C. J.; Howard, C. C.; Rayner, S. G.; Shin, Y. J.; Zheng, Y. Organ-on-a-chip systems for vascular biology. J. Mol. Cell. Cardiol. 2021, 159, 1–13.
Xie, R. X.; Zheng, W. C.; Guan, L. D.; Ai, Y. J.; Liang, Q. L. Engineering of hydrogel materials with perfusable microchannels for building vascularized tissues. Small 2020, 16, 1902838.
Sung, J. H.; Esch, M. B; Prot, J. M.; Long, C. J.; Smith, A.; Hickman, J. J; Shuler, M. L. Microfabricated mammalian organ systems and their integration into models of whole animals and humans. Lab Chip 2013, 13, 1201–1212.
Voiculescu, I.; Li, F.; Liu, F.; Zhang, X. D.; Cancel, L. M.; Tarbell, J. M.; Khademhosseini, A. Study of long-term viability of endothelial cells for lab-on-a-chip devices. Sens. Actuators B:Chem. 2013, 182, 696–705.
Bein, A.; Shin, W.; Jalili-Firoozinezhad, S.; Park, M. H.; Sontheimer-Phelps, A.; Tovaglieri, A.; Chalkiadaki, A.; Kim, H. J.; Ingber, D. E. Microfluidic organ-on-a-chip models of human intestine. Cell. Mol. Gastroenterol. Hepatol. 2018, 5, 659–668.
Lee, K. K.; McCauley, H. A.; Broda, T. R.; Kofron, M. J.; Wells, J. M.; Hong, C. I. Human stomach-on-a-chip with luminal flow and peristaltic-like motility. Lab Chip 2018, 18, 3079–3085.
Jalili-Firoozinezhad, S.; Gazzaniga, F. S.; Calamari, E. L.; Camacho, D. M.; Fadel, C. W.; Bein, A.; Swenor, B.; Nestor, B.; Cronce, M. J.; Tovaglieri, A. et al. A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nat. Biomed. Eng. 2019, 3, 520–531.
Kashaninejad, N.; Shiddiky, M. J. A.; Nguyen, N. T. Advances in microfluidics-based assisted reproductive technology: From sperm sorter to reproductive system-on-a-chip. Adv. Biosys. 2018, 2, 1700197.
Chen, H. X.; Bian, F. K.; Sun, L. Y.; Zhang, D. G.; Shang, L. R.; Zhao, Y. J. Hierarchically molecular imprinted porous particles for biomimetic kidney cleaning. Adv. Mater. 2020, 32, 2005394.
Ortega, M. A.; Fernández-Garibay, X.; Castaño, A. G.; De Chiara, F.; Hernández-Albors, A.; Balaguer-Trias, J.; Ramón-Azcón, J. Muscle-on-a-chip with an on-site multiplexed biosensing system for in situ monitoring of secreted IL-6 and TNF-α. Lab Chip 2019, 19, 2568–2580.
Frey, O.; Misun, P. M.; Fluri, D. A.; Hengstler, J. G.; Hierlemann, A. Reconfigurable microfluidic hanging drop network for multi-tissue interaction and analysis. Nat. Commun. 2014, 5, 4250.
Lai, B. F. L.; Huyer, L. D.; Lu, R. X. Z.; Drecun, S.; Radisic, M.; Zhang, B. Y. InVADE: Integrated vasculature for assessing dynamic events. Adv. Funct. Mater. 2017, 27, 1703524.
Picollet-D'hahan, N.; Zuchowska, A.; Lemeunier, I.; Le Gac, S. Multiorgan-on-a-chip: A systemic approach to model and decipher inter-organ communication. Trends Biotechnol. 2021, 39, 788–810.
Jeon, S.; Kim, S.; Ha, S.; Lee, S.; Kim, E.; Kim, S. Y.; Park, S. H.; Jeon, J. H.; Kim, S. W.; Moon, C. et al. Magnetically actuated microrobots as a platform for stem cell transplantation. Sci. Robot. 2019, 4, eaav4317.
Lei, F.; Liang, M. H.; Liu, Y.; Huang, H. H.; Li, H. F.; Dong, H. Multi-compartment organ-on-a-chip based on electrospun nanofiber membrane as in vitro jaundice disease model. Adv. Fiber Mater. 2021, 3, 383–393.
Zhang, Y. S.; Aleman, J.; Shin, S. R.; Kilic, T.; Kim, D.; Shaegh, S. A. M.; Massa, S.; Riahi, R.; Chae, S.; Hu, N. et al. Multisensor-integrated organs-on-chips platform for automated and continual in situ monitoring of organoid behaviors. Proc. Natl. Acad. Sci. USA 2017, 114, E2293–E2302.
Oleaga, C.; Lavado, A.; Riu, A.; Rothemund, S.; Carmona-Moran, C. A.; Persaud, K.; Yurko, A.; Lear, J.; Narasimhan, N. S.; Long, C. J. et al. Long-term electrical and mechanical function monitoring of a human-on-a-chip system. Adv. Funct. Mater. 2019, 29, 1805792.
Skardal, A.; Murphy, S. V.; Devarasetty, M.; Mead, I.; Kang, H. W.; Seol, Y. J.; Zhang, Y. S.; Shin, S. R.; Zhao, L. et al. Multi-tissue interactions in an integrated three-tissue organ-on-a-chip platform. Sci. Rep. 2017, 7, 8837.
Publication history
Copyright
Acknowledgements
This work was supported by the National Key Research and Development Program of China (No. 2020YFA0908200), the National Natural Science Foundation of China (Nos. T2225003, 52073060, and 61927805), the Nanjing Medical Science and Technique Development Foundation (No. ZKX21019), the Guangdong Basic and Applied Basic Research Foundation (No. 2021B1515120054), and the Shenzhen Fundamental Research Program (Nos. JCYJ20190813152616459 and JCYJ20210324133214038).
FEEDBACK 
TOP