Engineering challenges for instrumenting and controlling integrated organ-on-chip systems

IEEE Transactions on Biomedical Engineering

Volumn 60, Issue 3, 2013, Pages 682-690

  Wikswo, John P ^a   Block III, Frank E ^b   Cliffel, David E ^a   Goodwin, Cody R ^a   Marasco, Christina C ^b   Markov, Dmitry A ^c   McLean, David L ^a   McLean, John A ^a   McKenzie, Jennifer R ^a   Reiserer, Ronald S ^a   Samson, Philip C ^a   Schaffer, David K ^a   Seale, Kevin T ^b   Sherrod, Stacy D ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Artificial biological organs; Biological systems; Biotechnology; Systems biology

Indexed keywords

DRUG DEVELOPMENT PIPELINE; ENGINEERING CHALLENGES; FUNCTIONAL ACTIVITIES; FUNCTIONAL PROTOTYPES; INTEGRATED ELECTRONICS; ION MOBILITY-MASS SPECTROMETRY; PHYSIOLOGICAL RESPONSE; SYSTEMS BIOLOGY;

BIOINFORMATICS; BIOLOGICAL SYSTEMS; BIOTECHNOLOGY; CHEMICAL ANALYSIS; CONTROL; LEARNING ALGORITHMS; MICROFABRICATION; PHYSIOLOGY;

CELL ENGINEERING;

ALGORITHM; BIOENGINEERING; BIOINFORMATICS; BIOREACTOR; BIOSENSOR; CELL DENSITY; ELECTROCHEMICAL ANALYSIS; HUMAN; INFORMATION SYSTEM; MACHINE LEARNING; MASS SPECTROMETRY; MICROSCOPY; MICROTECHNOLOGY; NONHUMAN; ORGAN ON CHIP SYSTEM; REVIEW; SYSTEMS BIOLOGY; TISSUE ENGINEERING; ARTIFICIAL ORGAN; BIOLOGICAL MODEL; BIOMEDICAL ENGINEERING; DEVICES; LAB ON A CHIP; PROCEDURES;

ARTIFICIAL ORGANS; BIOMEDICAL ENGINEERING; HUMANS; LAB-ON-A-CHIP DEVICES; MODELS, BIOLOGICAL; SYSTEMS BIOLOGY;

EID: 84882268761     PISSN: 00189294     EISSN: 15582531     Source Type: Journal    
DOI: 10.1109/TBME.2013.2244891     Document Type: Review

References (80)

1. I. Kola, "The state of innovation in drug development," Clin. Pharmacol. Ther., vol. 83, no. 2, pp. 227-230, 2008.
2. D. Huh, Y. S. Torisawa, G. A. Hamilton, H. J. Kim, and D. E. Ingber, "Microengineered physiological biomimicry: Organs-on-chips," Lab Chip, vol. 12, no. 12, pp. 2156-2164, 2012.
3. C. Moraes, G. Mehta, S. C. Lesher-Perez, and S. Takayama, "Organs-on-a-Chip: A focus on compartmentalized microdevices," Ann. Biomed. Eng., vol. 40, no. 6, pp. 1211-1227, 2012.
4. A. D. van der Meer and A. van den Berg, "Organs-on-chips: Breaking the in vitro impasse," Integr. Biol., vol. 4, pp. 461-470, 2012.
5. M. B. Esch, T. L. King, and M. L. Shuler, "The role of body-on-a-chip devices in drug and toxicity studies," Annu. Rev. Biomed. Engr., vol. 13, pp. 55-72, 2011.
6. J. H. Sung, C. Kam, and M. L. Shuler, "A microfluidic device for a pharmacokinetic-pharmacodynamic (PK-PD) model on a chip," LabChip, vol. 10, no. 4, pp. 446-455, 2010.
7. S. Huang and J. Wikswo, "Dimensions of systems biology," in Reviews of Physiology, Biochemistry and Pharmacology, 157th ed. S. G. Amara, E. Bamberg, T. Gudermann, S. C. Hebert, R. Jahn, W. J. Lederer, R. Lill, A. Miyajima, and S. Offermanns, Eds., Berlin, Heidelberg: Springer, 2007, pp. 81-104.
8. (2010, Feb. 24). Advancing Regulatory Science through Novel Research and Science-Based Technologies (U01), RFA No. RFA-RM-10-006, NIH [Online]. Available: http://grants.nih.gov/grants/guide/rfa-files/RFA-RM-10-006.html
9. (2011, Sep. 11). Microphysiological Systems, Solicitation no. DARPA-BAA-11-73 [Online]. https://www.fbo.gov/index?s=opportunity&mode= form&id=956b160c42aaa386cf5762f12c21be9f&tab=core&-cview=0
10. (2011, Nov. 11). Integrated Microphysiological Systems for Drug Efficacy and Toxicity Testing in Human Health and Disease (UH2/UH3) FOA number: RFA-RM-11-022, NIH [Online]. Available: http://grants.nih.gov/grants/guide/rfa- files/RFA-RM-11-022.html
11. (2011, Dec. 12). Chemical and Biological Defense Innovations and Technologies [Online]. Available: http://www.grants.gov/search/search.do?mode= VIEW&oppId=133833
12. D. Huh, B. D. Matthews, A. Mammoto, M. Montoya-Zavala, H. Y. Hsin, and D. E. Ingber, "Reconstituting organ-level lung functions on a chip," Science, vol. 328, no. 5986, pp. 1662-1668, Jun. 2010.
13. K. Zeilinger, T. Schreiter, M. Darnell, T. Soderdahl, M. Lubberstedt, B. Dillner, D. Knobeloch, A. K. Nussler, J. C. Gerlach, and T. B. Andersson, "Scaling down of a clinical three-dimensional perfusion multicompartment hollow fiber liver bioreactor developed for extracorporeal liver support to an analytical scale device useful for hepatic pharmacological in vitro studies," Tissue Eng. Part C Methods, vol. 17, no. 5, pp. 549-556, 2011.
14. W. R. Stahl, "Organ weights in primates and other mammals," Science, vol. 150, no. 3699, pp. 1039-1042, Nov. 1965.
15. K. Schmidt-Nielsen, How Animals Work. Cambridge, U.K.: Cambridge Univ. Press, 1972.
16. K. Schmidt-Nielsen, "Organ size and tissue metabolism," in Scaling: Why is Animal Size so Important? New York, NY, USA Cambridge Univ. Press, 1984, pp. 90-98.
17. G. B. West, J. H. Brown, and B. J. Enquist, "A general model for the origin of allometric scaling laws in biology," Science, vol. 276, no. 5309, pp. 122-126, 1997.
18. G. B. West and J. H. Brown, "The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization," J. Exp. Biol., vol. 208, no. 9, pp. 1575-1592, 2005.
19. J. W. Prothero, "Organ scaling in mammals: The liver," Comp. Biochem. Physiol. A, Physiol., vol. 71, no. 4, pp. 567-577, 1982.
20. B. J. Anderson, A. D. Mckee, and N. H. G. Holford, "Size, myths and the clinical pharmacokinetics of analgesia in paediatric patients," Clin. Pharmacokinet., vol. 33, no. 5, pp. 313-327, 1997.
21. A. Bejan, Design in Nature: How the Constructal Law Governs Evolution in Biology, Physics, Technology, and Social Organization. New York, NY, USA: Doubleday, 2012.
22. T. N. Johnson, A. Rostami-Hodjegan, and G. T. Tucker, "Prediction of the clearance of eleven drugs and associated variability in neonates, infants and children," Clin. Pharmacokinet., vol. 45, no. 9, pp. 931-956, 2006. (Pubitemid 44299829)
23. M. Danhof, J. de Jongh, E. C. M. De Lange, O. Della Pasqua, B. A. Ploeger, and R. A. Voskuyl, "Mechanism-based pharmacokinetic- pharmacodynamic modeling: Biophase distribution, receptor theory, and dynamical systems analysis," Annu. Rev. Pharmacol. Toxicol., vol. 47, no. 1, pp. 357-400, Jan. 2007.
24. H. W. Leung, "Physiologically based pharmacokinetic modelling," in General, Applied and Systems Toxicology. New York, NY, USA: Wiley, 2009.
25. H. Boxenbaum and C. Dilea, "First-time-in-human dose selection - Allometric thoughts and perspectives," J. Clin. Pharmacol., vol. 35, no. 10, pp. 957-966, 1995.
26. I. Mahmood and J. D. Balian, "Interspecies scaling: predicting clearance of drugs in humans. Three different approaches," Xenobiotica, vol. 26, no. 9, pp. 887-895, Jan. 1996. (Pubitemid 26343083)
27. J. Mordenti, S. A. Chen, J. A. Moore, B. L. Ferraiolo, and J. D. Green, "Interspecies scaling of clearance and volume of distribution data for 5 therapeutic proteins," Pharm. Res., vol. 8, no. 11, pp. 1351-1359, 1991.
28. K. W. Ward and B. R. Smith, "A comprehensive quantitative and qualitative evaluation of extrapolation of intravenous pharmacokinetic parameters from rat, dog, and monkey to humans. I. Clearance," Drug Metab. Dispos., vol. 32, no. 6, pp. 603-611, 2004.
29. K. Ito and J. B. Houston, "Prediction of human drug clearance from in vitro and preclinical data using physiologically based and empirical approaches," Pharm. Res., vol. 22, no. 1, pp. 103-112, 2005. (Pubitemid 40558152)
30. V. Sharma and J. H. McNeill, "To scale or not to scale: The principles of dose extrapolation," Brit. J. Pharmacol., vol. 157, no. 6, pp. 907-921, 2009.
31. M. D. Thompson andD. A. Beard, "Development of appropriate equations for physiologically based pharmacokinetic modeling of permeability-limited and flow-limited transport," J. Pharmacokinet. Pharmacodyn., vol. 38, no. 4, pp. 405-421, 2011.
32. J. P. Wikswo, A. Prokop, F. Baudenbacher, D. Cliffel, B. Csukas, and M. Velkovsky, "Engineering challenges of BioNEMS: The integration of microfluidics, and micro- and nanodevices, models, and external control for systems biology," IEE Proc.-Nanobiotechnol., vol. 153, no. 4, pp. 81-101, 2006. (Pubitemid 44561841)
33. S. Faley, K. Seale, J. Hughey, D. K. Schaffer, S. VanCompernolle, B. McKinney, F. Baudenbacher, D. Unutmaz, and J. P. Wikswo, "Microfluidic platform for real-time signaling analysis of multiple single T cells in parallel," Lab Chip, vol. 8, no. 10, pp. 1700-1712, 2008.
34. S. Darby, M. Moore, J. P. Wikswo, R. Reiserer, T. Friedlander, D. K. Schaffer, and K. T. Seale, "A metering rotary nanopump for microfluidic systems," Lab Chip, vol. 10, no. 23, pp. 3218-3226, 2010.
35. G. Miesenbock, "The optogenetic catechism," Science, vol. 326, no. 5951, pp. 395-399, Oct. 2009.
36. R. M. Snider, J. R. McKenzie, L. Kraft, E. Kozlov, J. P. Wikswo, and D. E. Cliffel, "The effects of Cholera Toxin on cellular energy metabolism," Toxins, vol. 2, no. 4, pp. 632-648, 2010.
37. S. E. Eklund, D. E. Cliffel, E. Kozlov, A. Prokop, J. P. Wikswo, Jr., and F. J. Baudenbacher, "Modification of the cytosensor ™ microphysiometer to simultaneously measure extracellular acidification and oxygen consumption rates," Anal. Chim. Acta, vol. 496, no. 1-2, pp. 93-101, 2003. (Pubitemid 37352704)
38. L. A. Hiatt, J. R. McKenzie, L. F. Deravi, R. S. Harry, D. W. Wright, and D. E. Cliffel, "A printed superoxide dismutase coated electrode for the study of macrophage oxidative burst," Biosens. Bioelectron., vol. 33, pp. 128-133, 2012.
39. S. E. Eklund, D. Taylor, E. Kozlov, A. Prokop, and D. E. Cliffel, "A microphysiometer for simultaneous measurement of changes in extracellular glucose, lactate, oxygen, and acidification rate," Anal. Chem., vol. 76, no. 3, pp. 519-527, 2004. (Pubitemid 38166553)
40. S. E. Eklund, R. G. Thompson, R. M. Snider, C. K. Carney, D. W. Wright, J. Wikswo, and D. E. Cliffel, "Metabolic discrimination of select list agents by monitoring cellular responses in a multianalyte microphysiometer, " Sensors, vol. 9, no. 3, pp. 2117-2133, 2009.
41. I. A. Ges, K. P. Currie, and F. Baudenbacher, "Electrochemical detection of catecholamine release using planar iridium oxide electrodes in nanoliter microfluidic cell culture volumes," Biosens. Bioelectron., vol. 34, no. 1, pp. 30-36, 2012.
42. I. A. Ges and F. Baudenbacher, "Enzyme-coated microelectrodes to monitor lactate production in a nanoliter microfluidic cell culture device," Biosens. Bioelectron., vol. 26, no. 2, pp. 828-833, Oct. 2010.
43. I. A. Ges and F. Baudenbacher, "Enzyme electrodes to monitor glucose consumption of single cardiac myocytes in sub-nanoliter volumes," Biosens. Bioelectron., vol. 25, no. 5, pp. 1019-1024, Jan. 2010.
44. M. R. Warnement, S. L. Faley, J. P. Wikswo, and S. J. Rosenthal, "Quantum dot probes for monitoring dynamic cellular response: Reporters of T cell activation," IEEE Trans. NanoBiosci., vol. 5, no. 4, pp. 268-272, 2006.
45. S. L. Faley, M. Copland, D. Wlodkowic, W. Kolch, K. T. Seale, J. P. Wikswo, and J. M. Cooper, "Microfluidic single cell arrays to interrogate signalling dynamics of individual, patient-derived hematopoietic stem cells," Lab Chip, vol. 9, no. 18, pp. 2659-2664, 2009.
46. A. H. Diercks, A. Ozinsky, C. L. Hansen, J. M. Spotts, D. J. Rodriguez, and A. Aderem, "A microfluidic device for multiplexed protein detection in nano-liter volumes," Anal. Biochem., vol. 386, no. 1, pp. 30-35, Mar. 2009.
47. Y. Noguchi, J. D. Young, J. O. Aleman, M. E. Hansen, J. K. Kelleher, and G. Stephanopoulos, "Tracking cellular metabolomics in lipoapoptosis- and steatosis-developing liver cells," Mol. Biosyst., vol. 7, no. 5, pp. 1409-1419, 2011.
48. J. R. Enders, C. R. Goodwin, C. C. Marasco, K. T. Seale, J. P. Wikswo, and J. A. Mclean, "Advanced structural mass spectrometry for systems biology: Pulling the needles from haystacks," Spectrosc. Supp. Curr. Trends Mass Spectrom., pp. 18-23, Jul. 2011.
49. J. R. Enders, C. C. Marasco, A. Kole, B. Nguyen, S. Sundarapandian, K. T. Seale, J. P. Wikswo, and J. A. Mclean, "Towards monitoring real-time cellular response using an integrated microfluidics-MALDI/NESI-ion mobility-mass spectrometry platform," IET Syst. Biol., vol. 4, no. 6, pp. 416-427, 2010.
50. J. R. Enders, C. C. Marasco, J. P. Wikswo, and J. A. Mclean, "A Dual-column solid phase extraction strategy for online collection and preparation of continuously flowing effluent streams for mass spectrometry," Anal. Chem., vol. 84, no. 20, pp. 8467-8474, 2012.
51. G. S. Eichler, S. Huang, and D. E. Ingber, "Gene expression dynamics inspector (GEDI): For integrative analysis of expression profiles," Bioinformatics, vol. 19, no. 17, pp. 2321-2322, Nov. 2003. (Pubitemid 37483992)
52. B. MacLean, D. M. Tomazela, N. Shulman, M. Chambers, G. L. Finney, B. Frewen, R. Kern, D. L. Tabb, D. C. Liebler, and M. J. MacCoss, "Skyline: An open source document editor for creating and analyzing targeted proteomics experiments," Bioinformatics, vol. 26, no. 7, pp. 966-968, Apr. 2010.
53. M. A. Unger, H. P. Chou, T. Thorsen, A. Scherer, and S. R. Quake, "Monolithic microfabricated valves and pumps by multilayer soft lithography," Science, vol. 288, no. 5463, pp. 113-116, 2000. (Pubitemid 30203039)
54. P. A. Gould, L. T. Hoang, J. R. Scherrer, W. J. Matloff, K. T. Seale, E. L. Curtis, D. K. Schaffer, D. J. Hall, A. Kole, R. S. Reiserer, H. Tidwell, P. C. Samson, J. P. Wikswo, "Peristaltic micropump and related systems and methods," Pat. Appl. No. PCT/US2011/055432, Apr. 12, 2012.
55. D. Huh, D. C. Leslie, B. D. Matthews, J. P. Fraser, S. Jurek, G. A. Hamilton, K. S. Thorneloe, M. A. Mcalexander, and D. E. Ingber, "A human disease model of drug toxicity-induced pulmonary edema in a lung-on-a-chip microdevice," Sci. Transl. Med., vol. 4, no. 159, p. 159ra147, 2012.
56. P. R. LeDuc, W. C. Messner, and J. P. Wikswo, "How do control-based approaches enter into biology?" Annu. Rev. Biomed. Eng., vol. 13, pp. 369-396, 2011.
57. C. K. Griffith, C. Miller, R. C. A. Sainson, J. W. Calvert, N. L. Jeon, C. C. W. Hughes, and S. C. George, "Diffusion limits of an in vitro thick prevascularized tissue," Tissue Eng., vol. 11, no. 1/2, pp. 257-266, 2005. (Pubitemid 40515193)
58. X. Yan, D. J. Bergstrom, and X. B. Chen, "Modeling of cell cultures in perfusion bioreactors," IEEE Trans. Biomed. Eng., vol. 59, no. 9, pp. 2568-2575, Sep. 2012.
59. D. A. Markov, J. Q. Lu, P. C. Samson, J. P. Wikswo, and L. J. McCawley, "Thick-tissue bioreactor as a platform for long-term organotypic culture and drug delivery," Lab Chip, vol. 12, no. 21, pp. 4560-4568, 2012.
60. M. Martins-Green, Q. J. Li, and M. Yao, "A new generation organ culture arising from cross-talk between multiple primary human cell types," FASEB J., vol. 18, no. 15, pp. 222-224, 2005. (Pubitemid 40189262)
61. L. B. Wood, A. Das, R. D. Kamm, and H. H. Asada, "A stochastic broadcast feedback approach to regulating cell population morphology for microfluidic angiogenesis platforms," IEEE Trans. Biomed. Eng., vol. 56, no. 9, pp. 2299-2303, Sep. 2009.
62. Y. Liu, D. Markov, J. Wikswo, and L. McCawley, "Microfabricated scaffold-guided endothelial morphogenesis in three-dimensional culture," Biomed. Microdevices, vol. 13, no. 5, pp. 837-846, Jun. 2011.
63. J. H. Yeon, H. R. Ryu, M. Chung, Q. P. Hu, and N. L. Jeon, "In vitro formation and characterization of a perfusable three-dimensional tubular capillary network in microfluidic devices," Lab Chip, vol. 12, no. 16, pp. 2815-2822, 2012.
64. Y. H. Hsu, M. L. Moya, P. Abiri, C. C. W. Hughes, S. C. George, and A. P. Lee, "Full range physiological mass transport control in 3-D tissue cultures," Lab Chip, vol. 13, no. 1, pp. 81-89, 2013.
65. M. L. Moya, Y.-H. Hsu, A. P. Lee, C. C. W. Hughes, and S. C. George, "In vitro perfused human capillary networks," Tissue Eng. Part C, (Feb. 21, 2013). [Online]. 19(9).
66. C. L. Hansen, M. O. A. Sommer, and S. R. Quake, "Systematic investigation of protein phase behavior with a microfluidic formulator," Proc. Nat. Acad. Sci. USA, vol. 101, no. 40, pp. 14431-14436, 2004.
67. P. Hunter, K. Burrowes, P. N. Fernandez, N. Smith, and M. Tawhai, "The IUPS physiome project: Progress and plans," in Computational Systems Biology, A. Kriete and R. Eils, Eds. Amsterdam, The Netherlands: Elsevier, 2006, pp. 383-393.
68. R. Kannan and A. Przekwas, "A computational model to detect and quantify a primary blast lung injury using near-infrared optical tomography," Int. J. Numer. Methods Biomed. Eng., vol. 27, no. 1, pp. 13-28, 2011.
69. Technologies for Future Micro-Nano Manufacturing, The Manufacturing Technologies 2011 Workshop, Napa, CA, 2011.
70. R. D. King, J. Rowland, S. G. Oliver, M. Young, W. Aubrey, E. Byrne, M. Liakata, M. Markham, P. Pir, L. N. Soldatova, A. Sparkes, K. E. Whelan, and A. Clare, "The automation of science," Science, vol. 324, no. 5923, pp. 85-89, Apr. 2009.
71. M. D. Schmidt, R. R. Vallabhajosyula, J. W. Jenkins, J. E. Hood, A. S. Soni, J. P. Wikswo, and H. Lipson, "Automated refinement and inference of analytical models for metabolic networks," Phys. Biol., vol. 8, no. 5, p. 055011, 2011.
72. R. A. Miller, "Medical diagnostic decision-support systems - past, present, and future: A threaded bibliography and brief commentary," J. Amer. Med. Inform. Assoc., vol. 1, no. 1, pp. 8-27, 1994.
73. K. Balachandran, P. W. Alford, J. Wylie-Sears, J. A. Goss, A. Grosberg, J. Bischoff, E. Aikawa, R. A. Levine, and K. K. Parker, "Cyclic strain induces dual-mode endothelial-mesenchymal transformation of the cardiac valve," Proc. Nat. Acad. Sci. USA, vol. 108, no. 50, pp. 19943-19948, 2011.
74. A. Grosberg, P. W. Alford, M. L. McCain, and K. K. Parker, "Ensembles of engineered cardiac tissues for physiological and pharmacological study: Heart on a chip," Lab Chip, vol. 11, no. 24, pp. 4165-4173, 2011.
75. P. W. Alford, A. W. Feinberg, S. P. Sheehy, and K. K. Parker, "Biohybrid thin films for measuring contractility in engineered cardiovascular muscle," Biomaterials, vol. 31, no. 13, pp. 3613-3621, May 2010.
76. G. Mathews, C. Sondergaard, A. Jeffreys, W. Childs, B. L. Le, A. Sahota, S. Najibi, J. Nolta, and M. S. Si, "Computational analysis of contractility in engineered heart tissue," IEEE Trans. Biomed. Eng., vol. 59, no. 5, pp. 1429-1435, May 2012.
77. C. S. Sondergaard, G. Mathews, L. Wang, A. Jeffreys, A. Sahota, M. Wood, C. M. Ripplinger, and M. S. Si, "Contractile and electrophysiologic characterization of optimized self-organizing engineered heart tissue," Ann. Thorac. Surg., vol. 94, no. 4, pp. 1241-1249, 2012.
78. K. Y. Seng, I. Nestorov, and P. Vicini, "Fuzzy least squares for identification of individual pharmacokinetic parameters," IEEE Trans. Biomed. Eng., vol. 56, no. 12, pp. 2796-2805, Dec. 2009.
79. J. L. Borges and N. T. tr- Di Giovanni, "Of exactitude in science," in A Universal History of Infamy. London, U.K.: Penguin, 1975.
80. A. Rosenblueth and N. Wiener, "The role of models in science," Philosophy Sci., vol. 12, no. 4, pp. 316-321, Oct. 1945.