Abstract
Drug efficacy and toxicity are key factors of drug development. Conventional 2D cell models or animal models have their limitations for the efficacy or toxicity assessment in preclinical assays, which induce the failure of candidate drugs or withdrawal of approved drugs. Human organs-on-chips (OOCs) emerged to present human-specific properties based on their 3D bioinspired structures and functions in the recent decade. In this review, the basic definition and superiority of OOCs will be introduced. Moreover, a specific OOC, heart-on-achip (HOC) will be focused. We introduce HOC modeling in the sensor-free and sensor-based way and illustrate the advantages of sensor-based HOC in detail by taking examples of recent studies. We provide a new perspective on the integration of HOC technology and biosensing to develop a new sensor-based HOC platform.
Keywords: Human organs-on-chips, sensor-free/sensor-based heart-on-a-chip, biomaterial, intracellular/extracellular recording, synchronized electromechanical integration recording, 2D cell models.
[1]
Paul SM, Mytelka DS, Dunwiddie CT, et al. How to improve R&D productivity: the pharmaceutical industry’s grand challenge. Nat Rev Drug Discov 2010; 9(3): 203-14.
[2]
Scannell JW, Blanckley A, Boldon H, Warrington B. Diagnosing the decline in pharmaceutical R&D efficiency. Nat Rev Drug Discov 2012; 11(3): 191-200.
[3]
Kantarjian HM, Fojo T, Mathisen M, Zwelling LA. Cancer drugs in the United States: Justum Pretium--the just price. J Clin Oncol 2013; 31(28): 3600-4.
[4]
Breslin S, O’Driscoll L. Three-dimensional cell culture: the missing link in drug discovery. Drug Discov Today 2013; 18(5-6): 240-9.
[5]
Choi SM, Kim Y, Shim JS, et al. Efficient drug screening and gene correction for treating liver disease using patient-specific stem cells. Hepatology 2013; 57(6): 2458-68.
[6]
Kola I, Landis J. Can the pharmaceutical industry reduce attrition rates? Nat Rev Drug Discov 2004; 3(8): 711-5.
[7]
Caponigro G, Sellers WR. Advances in the preclinical testing of cancer therapeutic hypotheses. Nat Rev Drug Discov 2011; 10(3): 179-87.
[8]
Bowes J, Brown AJ, Hamon J, et al. Reducing safety-related drug attrition: the use of in vitro pharmacological profiling. Nat Rev Drug Discov 2012; 11(12): 909-22.
[9]
Woodcock J, Woosley R. The FDA critical path initiative and its influence on new drug development. Annu Rev Med 2008; 59: 1-12.
[10]
Mohs RC, Greig NH. Drug discovery and development: Role of basic biological research. Alzheimers Dement (N Y) 2017; 3(4): 651-7.
[11]
Bowes J, Brown AJ, Hamon J, et al. Reducing safety-related drug attrition: the use of in vitro pharmacological profiling. Nat Rev Drug Discov 2012; 11(12): 909-22.
[12]
Ouzounis CA. The emergence of bioinformatics: historical perspective, quick overview and future trends 2009.
[13]
Whitesides GM, Ostuni E, Takayama S, Jiang X, Ingber DE. Soft lithography in biology and biochemistry. Annu Rev Biomed Eng 2001; 3: 335-73.
[14]
Beebe DJ, Mensing GA, Walker GM. Physics and applications of microfluidics in biology. Annu Rev Biomed Eng 2002; 4: 261-86.
[15]
Shamir ER, Ewald AJ. Three-dimensional organotypic culture: experimental models of mammalian biology and disease. Nat Rev Mol Cell Biol 2014; 15(10): 647-64.
[16]
Huh D, Hamilton GA, Ingber DE. From 3D cell culture to organs-on-chips. Trends Cell Biol 2011; 21(12): 745-54.
[17]
Lee JS, Romero R, Han YM, et al. Placenta-on-a-chip: A novel platform to study the biology of the human placenta. J Matern Fetal Neonatal Med 2016; 29(7): 1046-54.
[18]
Esch EW, Bahinski A, Huh D. Organs-on-chips at the frontiers of drug discovery. Nat Rev Drug Discov 2015; 14(4): 248-60.
[19]
Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a chip. Science 2010; 328(5986): 1662-8.
[20]
Inamdar NK, Borenstein JT. Microfluidic cell culture models for tissue engineering. Curr Opin Biotechnol 2011; 22(5): 681-9.
[21]
Huh D, Leslie DC, Matthews BD, et al. Thorneloe KS, McAlexander MA, Ingber DE. A human disease model of drug toxicity–induced pulmonary edema in a lung-on-a-chip microdevice. Science translational medicine 2012; 4: 159ra147.
[22]
Khetani SR, Bhatia SN. Microscale culture of human liver cells for drug development. Nat Biotechnol 2008; 26(1): 120-6.
[23]
Agarwal A, Goss JA, Cho A, McCain ML, Parker KK. Microfluidic heart on a chip for higher throughput pharmacological studies. Lab Chip 2013; 13(18): 3599-608.
[24]
Egert U, Meyer T. Heart on a chip—extracellular multielectrode recordings from cardiac myocytes in vitro. In: ed.^eds., Practical Methods in Cardiovascular Research. Springer, 2005; pp. 432-453.
[25]
Grosberg A, Alford PW, McCain ML, Parker KK. Ensembles of engineered cardiac tissues for physiological and pharmacological study: heart on a chip. Lab Chip 2011; 11(24): 4165-73.
[26]
Jastrzebska E, Tomecka E, Jesion I. Heart-on-a-chip based on stem cell biology. Biosens Bioelectron 2016; 75: 67-81.
[27]
Marsano A, Conficconi C, Lemme M, et al. Beating heart on a chip: A novel microfluidic platform to generate functional 3D cardiac microtissues. Lab Chip 2016; 16(3): 599-610.
[28]
Wang G, McCain ML, Yang L, et al. Modeling the mitochondrial cardiomyopathy of Barth syndrome with iPSC and heart-on-chip technologies. Nat Med 2014; 20: 616.
[29]
Wang G, McCain ML, Yang L, et al. Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat Med 2014; 20(6): 616-23.
[30]
Zhang X, Wang T, Wang P, Hu N. High-throughput assessment of drug cardiac safety using a high-speed impedance detection technology-based Heart-on-a-chip. Micromachines (Basel) 2016; 7(7): 122.
[31]
Zhang YS, Aleman J, Arneri A, et al. From cardiac tissue engineering to heart-on-a-chip: beating challenges. Biomed Mater 2015; 10(3): 034006.
[32]
Zhang YS, Arneri A, Bersini S, et al. Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomaterials 2016; 110: 45-59.
[33]
Dauth S, Maoz BM, Sheehy SP, et al. Neurons derived from different brain regions are inherently different in vitro: A novel multiregional brain-on-a-chip. J Neurophysiol 2017; 117(3): 1320-41.
[34]
Griep LM, Wolbers F, de Wagenaar B, et al. BBB on chip: microfluidic platform to mechanically and biochemically modulate blood-brain barrier function. Biomed Microdevices 2013; 15(1): 145-50.
[35]
Kilic O, Pamies D, Lavell E, et al. Brain-on-a-chip model enables analysis of human neuronal differentiation and chemotaxis. Lab Chip 2016; 16(21): 4152-62.
[36]
Pamies D, Hartung T, Hogberg HT. Biological and medical applications of a brain-on-a-chip. Exp Biol Med (Maywood) 2014; 239(9): 1096-107.
[37]
Park J, Lee BK, Jeong GS, Hyun JK, Lee CJ, 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): 141-50.
[39]
Benam KH, Villenave R, Lucchesi C, et al. Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro. Nat Methods 2016; 13(2): 151-7.
[41]
Huh D, Fujioka H, Tung Y-C, et al. Acoustically detectable cellular-level lung injury induced by fluid mechanical stresses in microfluidic airway systems. Proc Natl Acad Sci USA 2007; 104(48): 18886-91.
[42]
Konar D, Devarasetty M, Yildiz DV, Atala A, Murphy SV. Lung-On-A-Chip Technologies for Disease Modeling and Drug Development: Supplementary Issue: Image and Video Acquisition and Processing for Clinical Applications. Biomedical engineering and computational biology 2016; S34252.
[43]
Long C, Finch C, Esch M, Anderson W, Shuler M, Hickman J. Design optimization of liquid-phase flow patterns for microfabricated lung on a chip. Ann Biomed Eng 2012; 40(6): 1255-67.
[44]
Punde TH, Wu W-H, Lien P-C, et al. A biologically inspired lung-on-a-chip device for the study of protein-induced lung inflammation. Integr Biol 2015; 7(2): 162-9.
[45]
Stucki AO, Stucki JD, Hall SR, et al. A lung-on-a-chip array with an integrated bio-inspired respiration mechanism. Lab Chip 2015; 15(5): 1302-10.
[46]
Kim HJ, Huh D, Hamilton G, Ingber DE. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 2012; 12(12): 2165-74.
[47]
Kim HJ, Ingber DE. Gut-on-a-Chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr Biol 2013; 5(9): 1130-40.
[48]
Kim HJ, Lee J, Choi J-H, Bahinski A, Ingber DE. Co-culture of Living Microbiome with Microengineered Human Intestinal Villi in a Gut-on-a-Chip Microfluidic Device. J Vis Exp 2016; (114).
[49]
Kim HJ, Li H, Collins JJ, Ingber DE. Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip. Proc Natl Acad Sci USA 2016; 113(1): E7-E15.
[50]
Villenave R, Wales SQ, Hamkins-Indik T, et al. Human gut-on-a-chip supports polarized infection of coxsackie B1 virus in vitro. PLoS One 2017; 12(2): e0169412.
[51]
Bavli D, Prill S, Ezra E, et al. Real-time monitoring of metabolic function in liver-on-chip microdevices tracks the dynamics of mitochondrial dysfunction. Proc Natl Acad Sci USA 2016; 113(16): E2231-40.
[52]
Bhise NS, Manoharan V, Massa S, et al. A liver-on-a-chip platform with bioprinted hepatic spheroids. Biofabrication 2016; 8(1): 014101.
[53]
Esch MB, Ueno H, Applegate DR, Shuler ML. Modular, pumpless body-on-a-chip platform for the co-culture of GI tract epithelium and 3D primary liver tissue. Lab Chip 2016; 16(14): 2719-29.
[54]
Gori M, Simonelli MC, Giannitelli SM, Businaro L, Trombetta M, Rainer A. Investigating nonalcoholic fatty liver disease in a liver-on-a-chip microfluidic device. PLoS One 2016; 11(7): e0159729.
[55]
Ho C-T, Lin R-Z, Chang W-Y, Chang H-Y, Liu C-H. Rapid heterogeneous liver-cell on-chip patterning via the enhanced field-induced dielectrophoresis trap. Lab Chip 2006; 6(6): 724-34.
[56]
Ho C-T, Lin R-Z, Chen R-J, et al. Liver-cell patterning lab chip: mimicking the morphology of liver lobule tissue. Lab Chip 2013; 13(18): 3578-87.
[57]
Knowlton S, Tasoglu S. A bioprinted liver-on-a-chip for drug screening applications. Trends Biotechnol 2016; 34(9): 681-2.
[58]
Lee J, Kim SH, Kim Y-C, Choi I, Sung JH. Fabrication and characterization of microfluidic liver-on-a-chip using microsomal enzymes. Enzyme Microb Technol 2013; 53(3): 159-64.
[59]
Yoon No D, Lee KH, Lee J, Lee SH. 3D liver models on a microplatform: well-defined culture, engineering of liver tissue and liver-on-a-chip. Lab Chip 2015; 15(19): 3822-37.
[60]
Lee S-A, No Y, Kang E, Ju J, Kim DS, Lee SH. Spheroid-based three-dimensional liver-on-a-chip to investigate hepatocyte-hepatic stellate cell interactions and flow effects. Lab Chip 2013; 13(18): 3529-37.
[61]
Ha L, Jang K-J, Suh K-Y. Kidney on a Chip In: ed.^eds., Microfluidics for Medical Applications, 2014; pp. 19-39.
[62]
Jang K-J, Mehr AP, Hamilton GA, et al. Human kidney proximal tubule-on-a-chip for drug transport and nephrotoxicity assessment. Integr Biol 2013; 5(9): 1119-29.
[63]
Kim S. LesherPerez SC, Kim BC, et al. Pharmacokinetic profile that reduces nephrotoxicity of gentamicin in a perfused kidney-on-a-chip. Biofabrication 2016; 8(1): 015021.
[64]
Nieskens TT, Wilmer MJ. Kidney-on-a-chip technology for renal proximal tubule tissue reconstruction. Eur J Pharmacol 2016; 790: 46-56.
[65]
Sochol RD, Gupta NR, Bonventre JV. A role for 3D printing in kidney-on-a-chip platforms. Curr Transplant Rep 2016; 3(1): 82-92.
[66]
Wilmer MJ, Ng CP, Lanz HL, Vulto P, Suter-Dick L, Masereeuw R. Kidney-on-a-chip technology for drug-induced nephrotoxicity screening. Trends Biotechnol 2016; 34(2): 156-70.
[67]
Torisawa YS, Spina CS, Mammoto T, et al. Bone marrow-on-a-chip replicates hematopoietic niche physiology in vitro. Nat Methods 2014; 11(6): 663-9.
[68]
Yasotharan S, Pinto S, Sled JG, Bolz S-S, Günther A. Artery-on-a-chip platform for automated, multimodal assessment of cerebral blood vessel structure and function. Lab Chip 2015; 15(12): 2660-9.
[69]
Jain A, Graveline A, Waterhouse A, Vernet A, Flaumenhaft R, Ingber DE. A shear gradient-activated microfluidic device for automated monitoring of whole blood haemostasis and platelet function. Nat Commun 2016; 7: 10176.
[70]
Maschmeyer I, Lorenz AK, Schimek K, et al. A four-organ-chip for interconnected long-term co-culture of human intestine, liver, skin and kidney equivalents. Lab Chip 2015; 15(12): 2688-99.
[71]
Zhang YS, Aleman J, Shin SR, et al. Multisensor-integrated organs-on-chips platform for automated and continual in situ monitoring of organoid behaviors. Proceedings of the National Academy of Sciences 2017; 201612906.
[72]
Wikswo JP, Block FE III, Cliffel DE, et al. Engineering challenges for instrumenting and controlling integrated organ-on-chip systems. IEEE Trans Biomed Eng 2013; 60(3): 682-90.
[73]
Esch MB, King TL, Shuler ML. The role of body-on-a-chip devices in drug and toxicity studies. Annu Rev Biomed Eng 2011; 13: 55-72.
[74]
Esch MB, Mahler GJ, Stokol T, Shuler ML. Body-on-a-chip simulation with gastrointestinal tract and liver tissues suggests that ingested nanoparticles have the potential to cause liver injury. Lab Chip 2014; 14(16): 3081-92.
[75]
Williamson A, Singh S, Fernekorn U, Schober A. The future of the patient-specific Body-on-a-chip. Lab Chip 2013; 13(18): 3471-80.
[76]
Griffith LG, Swartz MA. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 2006; 7(3): 211-24.
[79]
Olson H, Betton G, Robinson D, et al. Concordance of the toxicity of pharmaceuticals in humans and in animals. Regul Toxicol Pharmacol 2000; 32(1): 56-67.
[80]
Mak IW, Evaniew N, Ghert M. Lost in translation: Animal models and clinical trials in cancer treatment. Am J Transl Res 2014; 6(2): 114-8.
[81]
Seok J, Warren HS, Cuenca AG, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA 2013; 110(9): 3507-12.
[82]
Henderson VC, Kimmelman J, Fergusson D, Grimshaw JM, Hackam DG. Threats to validity in the design and conduct of preclinical efficacy studies: A systematic review of guidelines for in vivo animal experiments. PLoS Med 2013; 10(7): e1001489.
[83]
Samatov TR, Senyavina NV, Galatenko VV, et al. Tumour-like druggable gene expression pattern of CaCo2 cells in microfluidic chip. Biochip J 2016; 10: 215-20.
[84]
Polini A, Prodanov L, Bhise NS, Manoharan V, Dokmeci MR, Khademhosseini A. Organs-on-a-chip: A new tool for drug discovery. Expert Opin Drug Discov 2014; 9(4): 335-52.
[85]
Jacot JG, McCulloch AD, Omens JH. Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys J 2008; 95(7): 3479-87.
[86]
Cheng W, Klauke N, Smith G, Cooper JM. Microfluidic cell arrays for metabolic monitoring of stimulated cardiomyocytes. Electrophoresis 2010; 31(8): 1405-13.
[87]
Kim K, Taylor R, Sim J, et al. Calibrated micropost arrays for biomechanical characterisation of cardiomyocytes. Micro & Nano Lett 2011; 6: 317-22.
[88]
Cheng W, Klauke N, Sedgwick H, Smith GL, Cooper JM. Metabolic monitoring of the electrically stimulated single heart cell within a microfluidic platform. Lab Chip 2006; 6(11): 1424-31.
[89]
Agarwal A, Farouz Y, Nesmith AP, Deravi LF, McCain ML, Parker KK. Micropatterning alginate substrates for in vitro cardiovascular muscle on a chip. Adv Funct Mater 2013; 23(30): 3738-46.
[90]
McCain ML, Agarwal A, Nesmith HW, Nesmith AP, Parker KK. Micromolded gelatin hydrogels for extended culture of engineered cardiac tissues. Biomaterials 2014; 35(21): 5462-71.
[91]
Reza B, Ali N, Mustafa M, Alireza A, Ali K. Cardiac responsiveness to beta-adrenergics in rats with lead-induced hypertension. Biol Med (Aligarh) 2009; 1: 75-81.
[92]
Juberg EN, Minneman KP, Abel PW. β 1- and β 2-adrenoceptor binding and functional response in right and left atria of rat heart. Naunyn Schmiedebergs Arch Pharmacol 1985; 330(3): 193-202.
[93]
Gulick T, Pieper SJ, Murphy MA, Lange LG, Schreiner GF. A new method for assessment of cultured cardiac myocyte contractility detects immune factor-mediated inhibition of beta-adrenergic responses. Circulation 1991; 84(1): 313-21.
[94]
Desai VG, Herman EH, Moland CL, et al. Development of doxorubicin-induced chronic cardiotoxicity in the B6C3F1 mouse model. Toxicol Appl Pharmacol 2013; 266(1): 109-21.
[95]
Alderton PM, Gross J, Green MD. Comparative study of doxorubicin, mitoxantrone, and epirubicin in combination with ICRF-187 (ADR-529) in a chronic cardiotoxicity animal model. Cancer Res 1992; 52(1): 194-201.
[96]
Herman EH, Rahman A, Ferrans VJ, Vick JA, Schein PS. Prevention of chronic doxorubicin cardiotoxicity in beagles by liposomal encapsulation. Cancer Res 1983; 43(11): 5427-32.
[97]
McCain ML, Sheehy SP, Grosberg A, Goss JA, Parker KK. Recapitulating maladaptive, multiscale remodeling of failing myocardium on a chip. Proc Natl Acad Sci USA 2013; 110(24): 9770-5.
[98]
Bouten CV, Dankers PY, Driessen-Mol A, Pedron S, Brizard AM, Baaijens FP. Substrates for cardiovascular tissue engineering. Adv Drug Deliv Rev 2011; 63(4-5): 221-41.
[99]
Miyagawa S, Roth M, Saito A, Sawa Y, Kostin S. Tissue-engineered cardiac constructs for cardiac repair. Ann Thorac Surg 2011; 91(1): 320-9.
[100]
Annabi N, Tsang K, Mithieux SM, et al. Highly elastic micropatterned hydrogel for engineering functional cardiac tissue. Adv Funct Mater 2013; 23(39): 4950-9.
[101]
Radisic M, Park H, Gerecht S, Cannizzaro C, Langer R, Vunjak-Novakovic G. Biomimetic approach to cardiac tissue engineering. Philos Trans R Soc Lond B Biol Sci 2007; 362(1484): 1357-68.
[102]
Radisic M, Park H, Shing H, et al. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci USA 2004; 101(52): 18129-34.
[103]
Engelmayr GC Jr, Cheng M, Bettinger CJ, Borenstein JT, Langer R, Freed LE. Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat Mater 2008; 7(12): 1003-10.
[104]
Kujala VJ, Pasqualini FS, Goss JA, Nawroth JC, Parker KK. Laminar ventricular myocardium on a microelectrode array-based chip. J Mater Chem B Mater Biol Med 2016; 4: 3534-43.
[105]
Fleischer S, Shapira A, Feiner R, Dvir T. Modular assembly of thick multifunctional cardiac patches. Proceedings of the National Academy of Sciences 2017; 201615728.
[106]
You J-O, Rafat M, Ye GJ, Auguste DT. Nanoengineering the heart: conductive scaffolds enhance connexin 43 expression. Nano Lett 2011; 11(9): 3643-8.
[107]
Dvir T, Timko BP, Brigham MD, et al. Nanowired three-dimensional cardiac patches. Nat Nanotechnol 2011; 6(11): 720-5.
[108]
Silva GA, Czeisler C, Niece KL, et al. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 2004; 303(5662): 1352-5.
[109]
Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005; 23(1): 47-55.
[110]
Shin SR, Jung SM, Zalabany M, et al. Carbon-nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators. ACS Nano 2013; 7(3): 2369-80.
[111]
Shin SR, Shin C, Memic A, et al. Aligned carbon nanotube-based flexible gel substrates for engineering bio-hybrid tissue actuators. Adv Funct Mater 2015; 25(28): 4486-95.
[112]
Shin SR, Aghaei-Ghareh-Bolagh B, Gao X, et al. Layer-by-layer assembly of 3D tissue constructs with functionalized graphene. Adv Funct Mater 2014; 24(39): 6136-44.
[113]
Itzhaki I, Maizels L, Huber I, et al. Modelling the long QT syndrome with induced pluripotent stem cells. Nature 2011; 471(7337): 225-9.
[114]
Matsa E, Rajamohan D, Dick E, et al. Drug evaluation in cardiomyocytes derived from human induced pluripotent stem cells carrying a long QT syndrome type 2 mutation. Eur Heart J 2011; 32(8): 952-62.
[115]
Lan F, Lee AS, Liang P, et al. Abnormal calcium handling properties underlie familial hypertrophic cardiomyopathy pathology in patient-specific induced pluripotent stem cells. Cell Stem Cell 2013; 12(1): 101-13.
[116]
Sun N, Yazawa M, Liu J, et al. Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy Science translational medicine, 2012; 4: 130ra47-130ra47.
[117]
Navarrete EG, Liang P, Lan F, et al. Screening drug-induced arrhythmia [corrected] using human induced pluripotent stem cell-derived cardiomyocytes and low-impedance microelectrode arrays. Circulation 2013; 128(11)(Suppl. 1): S3-S13.
[118]
Natarajan A, Stancescu M, Dhir V, et al. Patterned cardiomyocytes on microelectrode arrays as a functional, high information content drug screening platform. Biomaterials 2011; 32(18): 4267-74.
[119]
Xiao L, Hu Z, Zhang W, Wu C, Yu H, Wang P. Evaluation of doxorubicin toxicity on cardiomyocytes using a dual functional extracellular biochip. Biosens Bioelectron 2010; 26(4): 1493-9.
[120]
Xiao L, Liu Q, Hu Z, Zhang W, Yu H, Wang P. A multi-scale electrode array (MSEA) to study excitation–contraction coupling of cardiomyocytes for high-throughput bioassays. Sens Actuators B Chem 2011; 152: 107-14.
[121]
Lin ZC, Xie C, Osakada Y, Cui Y, Cui B. Iridium oxide nanotube electrodes for sensitive and prolonged intracellular measurement of action potentials. Nat Commun 2014; 5: 3206.
[122]
Fendyur A, Spira ME. Toward on-chip, in-cell recordings from cultured cardiomyocytes by arrays of gold mushroom-shaped microelectrodes. Front Neuroeng 2012; 5: 21.
[123]
Hai A, Shappir J, Spira ME. In-cell recordings by extracellular microelectrodes. Nat Methods 2010; 7(3): 200-2.
[124]
Xie C, Lin Z, Hanson L, Cui Y, Cui B. Intracellular recording of action potentials by nanopillar electroporation. Nat Nanotechnol 2012; 7(3): 185-90.
[125]
Lee K-Y, Kim I, Kim S-E, et al. Vertical nanowire probes for intracellular signaling of living cells. Nanoscale Res Lett 2014; 9(1): 56.
[126]
Abbott J, Ye T, Qin L, et al. CMOS nanoelectrode array for all-electrical intracellular electrophysiological imaging. Nat Nanotechnol 2017; 12(5): 460-6.
[127]
Abbott J, Ye T, Ham D, Park H. Optimizing Nanoelectrode Arrays for Scalable Intracellular Electrophysiology. Acc Chem Res 2018; 51(3): 600-8.
[128]
Santoro F, Dasgupta S, Schnitker J, et al. Interfacing electrogenic cells with 3D nanoelectrodes: position, shape, and size matter. ACS Nano 2014; 8(7): 6713-23.
[129]
Dipalo M, Amin H, Lovato L, et al. Intracellular and Extracellular Recording of Spontaneous Action Potentials in Mammalian Neurons and Cardiac Cells with 3D Plasmonic Nanoelectrodes. Nano Lett 2017; 17(6): 3932-9.
[131]
Tian B, Cohen-Karni T, Qing Q, Duan X, Xie P, Lieber CM. Three-dimensional, flexible nanoscale field-effect transistors as localized bioprobes. Science 2010; 329(5993): 830-4.
[132]
Wightman RM. Detection technologies. Probing cellular chemistry in biological systems with microelectrodes. Science 2006; 311(5767): 1570-4.
[133]
Ewing AG, Strein TG, Lau YY. Analytical chemistry in microenvironments: single nerve cells. Acc Chem Res 1992; 25: 440-7.
[134]
Ieong M, Doris B, Kedzierski J, Rim K, Yang M. Silicon device scaling to the sub-10-nm regime. Science 2004; 306(5704): 2057-60.
[135]
Ferrari M. Cancer nanotechnology: opportunities and challenges. Nat Rev Cancer 2005; 5(3): 161-71.
[136]
Ingebrandt S, Yeung C-K, Krause M, Offenhäusser A. Cardiomyocyte-transistor-hybrids for sensor application. Biosens Bioelectron 2001; 16(7-8): 565-70.
[137]
Ingebrandt S, Yeung CK, Staab W, Zetterer T, Offenhäusser A. Backside contacted field effect transistor array for extracellular signal recording. Biosens Bioelectron 2003; 18(4): 429-35.
[138]
Yeung C-K, Ingebrandt S, Krause M, Offenhäusser A, Knoll W. Validation of the use of field effect transistors for extracellular signal recording in pharmacological bioassays. J Pharmacol Toxicol Methods 2001; 45(3): 207-14.
[139]
Patolsky F, Timko BP, Yu G, et al. Detection, stimulation, and inhibition of neuronal signals with high-density nanowire transistor arrays. Science 2006; 313(5790): 1100-4.
[140]
Cohen-Karni T, Timko BP, Weiss LE, Lieber CM. Flexible electrical recording from cells using nanowire transistor arrays. Proc Natl Acad Sci USA 2009; 106(18): 7309-13.
[141]
Cohen-Karni T, Qing Q, Li Q, Fang Y, Lieber CM. Graphene and nanowire transistors for cellular interfaces and electrical recording. Nano Lett 2010; 10(3): 1098-102.
[142]
Pui TS, Agarwal A, Ye F, Balasubramanian N, Chen P. CMOS-Compatible nanowire sensor arrays for detection of cellular bioelectricity. Small 2009; 5(2): 208-12.
[143]
Cohen-Karni T, Casanova D, Cahoon JF, Qing Q, Bell DC, Lieber CM. Synthetically encoded ultrashort-channel nanowire transistors for fast, pointlike cellular signal detection. Nano Lett 2012; 12(5): 2639-44.
[144]
Qing Q, Jiang Z, Xu L, Gao R, Mai L, Lieber CM. Free-standing kinked nanowire transistor probes for targeted intracellular recording in three dimensions. Nat Nanotechnol 2014; 9(2): 142-7.
[145]
Duan X, Gao R, Xie P, et al. Intracellular recordings of action potentials by an extracellular nanoscale field-effect transistor. Nat Nanotechnol 2011; 7(3): 174-9.
[146]
Sakmann B, Neher E. Patch clamp techniques for studying ionic channels in excitable membranes. Annu Rev Physiol 1984; 46: 455-72.
[147]
Luong JH, Habibi-Rezaei M, Meghrous J, Xiao C, Male KB, Kamen A. Monitoring motility, spreading, and mortality of adherent insect cells using an impedance sensor. Anal Chem 2001; 73(8): 1844-8.
[148]
Opp D, Wafula B, Lim J, Huang E, Lo J-C, Lo C-M. Use of electric cell-substrate impedance sensing to assess in vitro cytotoxicity. Biosens Bioelectron 2009; 24(8): 2625-9.
[149]
Xiao C, Lachance B, Sunahara G, Luong JH. Assessment of cytotoxicity using electric cell-substrate impedance sensing: concentration and time response function approach. Anal Chem 2002; 74(22): 5748-53.
[150]
Kammermann M, Denelavas A, Imbach A, et al. Impedance measurement: A new method to detect ligand-biased receptor signaling. Biochem Biophys Res Commun 2011; 412(3): 419-24.
[151]
Smout MJ, Laha T, Mulvenna J, et al. A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells. PLoS Pathog 2009; 5(10): e1000611.
[152]
Wang T, Hu N, Cao J, Wu J, Su K, Wang P. A cardiomyocyte-based biosensor for antiarrhythmic drug evaluation by simultaneously monitoring cell growth and beating. Biosens Bioelectron 2013; 49: 9-13.
[153]
Hu N, Wang T, Wang Q, et al. High-performance beating pattern function of human induced pluripotent stem cell-derived cardiomyocyte-based biosensors for hERG inhibition recognition. Biosens Bioelectron 2015; 67: 146-53.
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