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Electronic Interfacing with Living Cells

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Whole Cell Sensing Systems I

Part of the book series: Advances in Biochemical Engineering / Biotechnology ((ABE,volume 117))

Abstract

The direct interfacing of living cells with inorganic electronic materials, components or systems has led to the development of two broad categories of devices that can (1) transduce biochemical signals generated by biological components into electrical signals and (2) transduce electronically generated signals into biochemical signals. The first category of devices permits the monitoring of living cells, the second, enables control of cellular processes. This review will survey this exciting area with emphasis on the fundamental issues and obstacles faced by researchers. Devices and applications that use both prokaryotic (microbial) and eukaryotic (mammalian) cells will be covered. Individual devices described include microbial biofuel cells that produce electricity, bioelectrical reactors that enable electronic control of cellular metabolism, living cell biosensors for the detection of chemicals and devices that permit monitoring and control of mammalian physiology.

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References

  1. Merrill DR, Bikson M, Jefferys JGR (2005) Electrical stimulation of excitable tissue:design of efficacious and safe protocols. J Neurosci Methods 141:171–198

    Article  Google Scholar 

  2. Thrash JC, Coates JD (2008) Review: direct and indirect electrical stimulation of microbial metabolism. Environ Sci Technol 42:3921–3931

    Article  CAS  Google Scholar 

  3. Schoen I, Fromherz P (2008) Extracellular stimulation of mammalian neurons through repetitive activation of Na + channels by weak capacitive currents on a silicon chip. J Neurophysiol 100:346–357

    Article  Google Scholar 

  4. He HQ, Chang DC, Lee YK (2007) Using a micro electroporation chip to determine the optimal physical parameters in the uptake of biomolecules in HeLa cells. Bioelectrochemistry 70:363–368

    Article  CAS  Google Scholar 

  5. Ryttsen F, Farre C, Brennan C, Weber SG, Nolkrantz K, Jardemark K, Chiu DT, Orwar O (2000) Characterization of single-cell electroporation by using patch-clamp and fluorescence microscopy. Biophys J 79:1993–2001

    Article  CAS  Google Scholar 

  6. Olofsson J, Nolkrantz K, Ryttsen F, Lambie BA, Weber SG, Orwar O (2003) Single-cell electroporation. Curr Opin Biotechnol 14:29–34

    Article  CAS  Google Scholar 

  7. Debabov VG (2008) Electricity from microorganisms. Microbiology 77:123–131

    Article  CAS  Google Scholar 

  8. Bettaieb F, Ponsonnet L, Lejeune P, Ben Ouada H, Martelet C, Bakhrouf A, Jaffrezic-Renault N, Othmane A (2007) Immobilization of E-coli bacteria in three-dimensional matrices for ISFET biosensor design. Bioelectrochemistry 71:118–125

    Article  CAS  Google Scholar 

  9. D’Souza SF (2001) Microbial biosensors. Biosens Bioelectron 16:337–353

    Article  Google Scholar 

  10. Wen G, Zheng J, Zhao C, Shuang S, Dong C, Choi MMF (2008) A microbial biosensing system for monitoring methane. Enzyme Microb Technol 43:257–261

    Article  CAS  Google Scholar 

  11. Lei Y, Chen W, Mulchandani A (2006) Microbial biosensors. Anal Chim Acta 568:200–210

    Article  CAS  Google Scholar 

  12. Lojou, E, Bianco P (2006) Application of the electrochemical concepts and techniques to amperometric biosensor devices. J Electroceram 16:79–91

    Article  CAS  Google Scholar 

  13. Premkumar JR, Lev O, Marks RS, Polyak B, Rosen R, Belkin S (2001) Antibody-based immobilization of bioluminescent bacterial sensor cells. Talanta 55:1029–1038

    Article  CAS  Google Scholar 

  14. Kirgoz UA, Timur S, Odaci D, Perez B, Alegret S, Merkoci A (2007) Carbon nanotube composite as novel platform for microbial biosensor. Electroanalysis 19:893–898

    Article  CAS  Google Scholar 

  15. Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ (2005) Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng 11:1–18

    Article  CAS  Google Scholar 

  16. Kim L, Toh YC, Voldman J, Yu H (2007) A practical guide to microfluidic perfusion culture of adherent mammalian cells. Lab Chip 7:681–694

    Article  CAS  Google Scholar 

  17. Nicolelis MAL, Dimitrov D, Carmena JM, Crist R, Lehew G, Kralik JD, Wise SP (2003) Chronic, multisite, multielectrode recordings in macaque monkeys. Proc Natl Acad Sci U S A 100:11041–11046

    Article  CAS  Google Scholar 

  18. Polikov VS, Tresco PA, Reichert WM (2005) Response of brain tissue to chronically implanted neural electrodes. J Neurosci Methods 148:1–18

    Article  Google Scholar 

  19. Stroscio MA, Dutta M (2005) Integrated biological-semiconductor devices. Proc IEEE 93:1772–1783

    Article  CAS  Google Scholar 

  20. Purves D, Augustine GJ, Fitzpatrick D, Hall WC, LaMantia AS, McNamara JO, White LE (2004). Neuroscience. Sinauer Associates, Sunderland, MA

    Google Scholar 

  21. Brummer SB, Turner MJ (1977) Electrochemical considerations for safe electrical-stimulation of nervous-system with platinum-electrodes. IEEE Trans Biomed Eng 24:59–63

    Article  CAS  Google Scholar 

  22. Cogan SR (2008) Neural stimulation and recording electrodes. Annu Rev Biomed Eng 10:275–309

    Article  CAS  Google Scholar 

  23. Potter MC (1911) Electrical effects accompanying the decomposition of organic compounds. Proc R Soc Lond B Biol Sci 84:260–276

    Article  Google Scholar 

  24. Rabaey K, Rodriguez J, Blackall LL, Keller J, Gross P, Batstone D, Verstraete W, Nealson KH (2007) Microbial ecology meets electrochemistry: electricity-driven and driving communities. ISME J 1:9–18

    Article  CAS  Google Scholar 

  25. Clauwaert P, Aelterman P, Pham TH, De Schamphelaire L, Carballa M, Rabaey K, Verstraete W (2008) Minimizing losses in bio-electrochemical systems: the road to applications. Appl Microbiol Biotechnol 79:901–913

    Article  CAS  Google Scholar 

  26. Tender LM, Gray SA, Groveman E, Lowy DA, Kauffman P, Melhado J, Tyce RC, Flynn D et al (2008) The first demonstration of a microbial fuel cell as a viable power supply: powering a meteorological buoy. J Power Sources 179:571–575

    Article  CAS  Google Scholar 

  27. Rabaey K, Lissens G, Siciliano SD, Verstraete W (2003) A microbial fuel cell capable of converting glucose to electricity at high rate and efficiency. Biotechnol Lett 25: 1531–1535

    Article  CAS  Google Scholar 

  28. Ringeisen BR, Henderson E, Wu PK, Pietron J, Ray R, Little B, Biffinger JC, Jones-Meehan JM (2006) High power density from a miniature microbial fuel cell using Shewanella oneidensis DSP10. Environ Sci Technol 40:2629–2634

    Article  CAS  Google Scholar 

  29. Lovley, DR (2006) Bug Juice: harvesting electricity with microorganisms. Nature Rev. Micro. 4:497–508.

    Article  CAS  Google Scholar 

  30. Lies DP, Hernandez ME, Kappler A, Mielke RE, Gralnick JA, Newman DK (2005) Shewanella oneidensis MR-1 uses overlapping pathways for iron reduction at a distance and by direct contact under conditions relevant for biofilms. Appl Environ Microbiol 71:4414–4426

    Article  CAS  Google Scholar 

  31. Busalmen JP, Esteve-Nunez A, Berna A, Feliu JM (2008) C-type cytochromes wire electricity-producing bacteria to electrodes. Angew Chem Int Edit 47:4874–4877

    Article  CAS  Google Scholar 

  32. Nevin KP, Lovley DR (2000) Lack of production of electron-shuttling compounds or solubilization of Fe(III) during reduction of insoluble Fe(III) oxide by Geobacter metallireducens. Appl Environ Microbiol 66:2248–2251

    Article  CAS  Google Scholar 

  33. Lovley DR (2008) Extracellular electron transfer: wires, capacitors, iron lungs, and more. Geobiology 6:225–231

    Article  CAS  Google Scholar 

  34. Gregory KB, Bond DR, Lovley DR (2004) Graphite electrodes as electron donors for anaerobic respiration. Environ Microbiol 6:596–604

    Article  CAS  Google Scholar 

  35. Sadoff HL, Halvorson HO, Finn RK (1956) Electrolysis as a means of aerating submerged cultures of microorganisms. Appl Microbiol 4:164–170

    CAS  Google Scholar 

  36. Park DH, Zeikus JG (1999) Utilization of electrically reduced neutral red by Actinobacillus succinogenes: physiological function of neutral red in membrane-driven fumarate reduction and energy conservation. J Bacteriol 181:2403–2410

    CAS  Google Scholar 

  37. Shin HS, Jain MK, Chartrain M, Zeikus JG (2001) Evaluation of an electrochemical bioreactor system in the biotransformation of 6-bromo-2-tetralone to 6-bromo-2-tetralol. Appl Microbiol Biotechnol 57:506–510

    Article  CAS  Google Scholar 

  38. Thrash JC, Van Trump JI, Weber KA, Miller E, Achenbach LA, Coates JD (2007) Electrochemical stimulation of microbial perchlorate reduction. Environ Sci Technol 41:1740–1746

    Article  CAS  Google Scholar 

  39. Aulenta F, Catervi A, Majone M, Panero S, Reale P, Rossetti S (2007) Electron transfer from a solid-state electrode assisted by methyl viologen sustains efficient microbial reductive dechlorination of TCE. Environ Sci Technol 41:2554–2559

    Article  CAS  Google Scholar 

  40. Pang HL, Kwok HY, Chan PH, Yeung CH, Lo WH, Wong KY (2007) High-throughput determination of biochemical oxygen demand (BOD) by a microplate-based biosensor. Environ Sci Technol 41:4038–4044

    Article  CAS  Google Scholar 

  41. Tkac J, Vostiar I, Gemeiner P, Sturdik E (2002) Monitoring of ethanol during fermentation using a microbial biosensor with enhanced selectivity. Bioelectrochemistry 56:127–129

    Article  CAS  Google Scholar 

  42. Tkac J, Vostiar I, Gorton L, Gemeiner P, Sturdik E (2003) Improved selectivity of microbial biosensor using membrane coating. Application to the analysis of ethanol during fermentation. Biosens Bioelectron 18:1125–1134

    Article  CAS  Google Scholar 

  43. Held M, Schuhmann W, Jahreis K, Schmidt HL (2002) Microbial biosensor array with transport mutants of Escherichia coli K12 for the simultaneous determination of mono-and disaccharides. Biosens Bioelectron 17:1089–1094

    Article  CAS  Google Scholar 

  44. Timur S, Pazarlioglu N, Pilloton R, Telefoncu A (2003) Detection of phenolic compounds by thick film sensors based on Pseudomonas putida. Talanta 61:87–93

    Article  CAS  Google Scholar 

  45. Mulchandani, A, Mulchandani P, Chauhan S, Kaneva I, Chen W (1998) A potentiometric microbial biosensor for direct determination of organaphosphate nerve agents. Electroanalysis 10:733–737

    Article  CAS  Google Scholar 

  46. Rotariu L, Bala C, Magearu V (2004) New potentiometric microbial biosensor for ethanol determination in alcoholic beverages. Anal Chim Acta 513:119–123

    Article  CAS  Google Scholar 

  47. Hassan SSM, El-Baz AE, Abd-Rabboh HSM (2007) A novel potentiometric biosensor for selective L-cysteine determination using L-cysteiine-desulfhydrase producing Trichosporon jirovecii yeast cells coupled with sulfide electrode. Anal Chim Acta 602:108–113

    Article  CAS  Google Scholar 

  48. Spegel C, Heiskanen A, Skjolding LHD, Emneus J (2008) Chip based electroanalytical systems for cell analysis. Electroanalysis 20:680–702

    Article  CAS  Google Scholar 

  49. Giaever I, Keese CR (1991) Micromotion of mammalian-cells measured electrically. Proc Natl Acad Sci U S A 88:7896–7900

    Article  CAS  Google Scholar 

  50. Arndt S, Seebach J, Psathaki K, Galla HJ, Wegener J (2004) Bioelectrical impedance assay to monitor changes in cell shape during apoptosis. Biosens Bioelectron 19:583–594

    Article  CAS  Google Scholar 

  51. Hartmann C, Zozulya A, Wegener J, Galla HJ (2007) The impact of glia-derived extracellular matrices on the barrier function of cerebral endothelial cells: an in vitro study. Exp Cell Res 313:1318–1325

    Article  CAS  Google Scholar 

  52. Schoning MJ, Poghossian A (2006) Bio FEDs (field-effect devices): state-of-the-art and new directions. Electroanalysis 18:1893–1900

    Article  Google Scholar 

  53. Lehmann M, Baumann W, Brischwein M, Ehret R, Kraus M, Schwinde A, Bitzenhofer M, Freund I, Wolf B (2000) Non-invasive measurement of cell membrane associated proton gradients by ion-sensitive field effect transistor arrays for microphysiological and bioelectronical applications. Biosens Bioelectron 15:117–124

    Article  CAS  Google Scholar 

  54. Lehmann M, Baumann W, Brischwein M, Gahle HJ, Freund I, Ehret R, Drechsler S, Palzer H et al (2001) Simultaneous measurement of cellular respiration and acidification with a single CMOS ISFET. Biosens Bioelectron 16:195–203

    Article  CAS  Google Scholar 

  55. Martinez M, Hilding-Ohlsson A, Viale AA, Corton E (2007) Membrane entrapped Saccharomyces cerevisiae in a biosensor-like device as a generic rapid method to study cellular metabolism. J Biochem Biophys Methods 70:455–464

    Article  CAS  Google Scholar 

  56. Thedinga E, Kob A, Holst H, Keuer A, Drechsler S, Niendorf R, Baumann W, Freund I et al (2007) Online monitoring of cell metabolism for studying pharmacodynamic effects. Toxicol Appl Pharmacol 220:33–44

    Article  CAS  Google Scholar 

  57. Teulon J (2004) Patch-clamp techniques. M S-Med Sci 20:550

    Google Scholar 

  58. Thomas CA, Springer PA, Okun LM, Berwaldn Y, Loeb GE (1972) Miniature microelectrode array to monitor bioelectric activity of cultured cells. Exp Cell Res 74:61–69

    Article  Google Scholar 

  59. Israel D, Barry WH, Edell DJ, Mark RG (1984) An array of microelectrodes to stimulate and record from cardiac cells in culture. Am J Physiol 247:H669–H674

    CAS  Google Scholar 

  60. Dale N, Hatz S, Tian FM, Llaudet E (2005) Listening to the brain: microelectrode biosensors for neurochemicals. Trends Biotechnol 23:420–428

    Article  CAS  Google Scholar 

  61. Pothos EN, Davila V, Sulzer D (1998) Presynaptic recording of quanta from midbrain dopamine neurons and modulation of the quantal size. J Neurosci 18:4106–4118

    CAS  Google Scholar 

  62. Jaffe EH, Marty A, Schulte A, Chow RH (1998) Extrasynaptic vesicular transmitter release from the somata of substantia nigra neurons in rat midbrain slices. J Neurosci 18:3548–3553

    CAS  Google Scholar 

  63. Heer F, Hafizovic S, Franks W, Blau A, Ziegler C, Hierlemann A (2006) CMOS microelectrode array for bidirectional interaction with neuronal networks. IEEE J Solid State Circuits 41:1620–1629

    Article  Google Scholar 

  64. Li YL, Zhou W, Li XN, Zeng SQ, Liu M, Luo QM (2007) Characterization of synchronized bursts in cultured hippocampal neuronal networks with learning training on microelectrode arrays. Biosens Bioelectron 22:2976–2982

    Article  CAS  Google Scholar 

  65. Kovacs GTA (2003) Electronic sensors with living cellular components. Proc IEEE 91:915–929

    Article  CAS  Google Scholar 

  66. Fromherz P, Offenhausser A, Vetter T, Weis J (1991) A neuron-silicon junction – a retzius cell of the leech on an insulated-gate field-effect transistor. Science 252:1290–1293

    Article  CAS  Google Scholar 

  67. Fromherz P, Stett A (1995) Silicon-neuron junction – capacitive stimulation of an individual neuron on a silicon chip. Phys Rev Lett 75:1670–1673

    Article  CAS  Google Scholar 

  68. Vassanelli S, Fromherz P (1998) Transistor records of excitable neurons from rat brain. Appl Phys A Mater Sci Process 66:459–463

    Article  CAS  Google Scholar 

  69. Offenhausser A, Knoll W (2001) Cell-transistor hybrid systems and their potential applications. Trends Biotechnol 19:62–66

    Article  CAS  Google Scholar 

  70. Koester P, Sakowski J, Baumann W, Glock HW, Gimsa J (2007) A new exposure system for the in vitro detection of GHz field effects on neuronal networks. Bioelectrochemistry 70:104–114

    Article  CAS  Google Scholar 

  71. Chapin JK, Moxon KA, Markowitz RS, Nicolelis MAL (1999) Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex. Nat Neurosci 2:664–670

    Article  CAS  Google Scholar 

  72. Lebedev MA, Nicolelis MAL (2006) Brain-machine interfaces: past, present and future. Trends Neurosci 29:536–546

    Article  CAS  Google Scholar 

  73. Ignatius MJ, Sawhney N, Gupta A, Thibadeau BM, Monteiro OR, Brown IG (1998) Bioactive surface coatings for nanoscale instruments: effects on CNS neurons. J Biomed Mater Res 40:264–274

    Article  CAS  Google Scholar 

  74. Kam L, Shain W, Turner JN, Bizios R (2002) Selective adhesion of astrocytes to surfaces modified with immobilized peptides. Biomaterials 23:511–515

    Article  CAS  Google Scholar 

  75. Yang JY, Martin DC (2004) Microporous conducting polymers on neural microelectrode arrays – I – Electrochemical deposition. Sens Actuator B Chem 101:133–142

    Article  Google Scholar 

  76. Maynard EM, Fernandez E, Normann RA (2000) A technique to prevent dural adhesions to chronically implanted microelectrode arrays. J Neurosci Methods 97:93–101

    Article  CAS  Google Scholar 

  77. Gheith MK, Sinani VA, Wicksted JP, Matts RL, Kotov NA (2005) Single-walled carbon nanotube polyelectrolyte multilayers and freestanding films as a biocompatible platformfor neuroprosthetic implants. Adv Mater 17:2663

    Article  CAS  Google Scholar 

  78. Dubin RA, Callegari GC, Kohn J, Neimark AV (2008) Carbon nanotube fibers are compatible with mammalian cells and neurons. IEEE Trans Nanobiosci 7:11–14

    Article  CAS  Google Scholar 

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  1. University of Tennessee, Center for Environmental Biotechnology, 676 Dabney Hall, Knoxville, 37996, TN, USA

    James T. Fleming

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Correspondence to James T. Fleming .

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  1. , Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, 91904, Israel

    Shimshon Belkin

  2. , College of Life Sciences & Biotechnology, Korea University, Amam-dong 5-ga, Seoul, 136-701, Korea, Republic of (South Korea)

    Man Bock Gu

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© 2009 Springer-Verlag Berlin Heidelberg

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Fleming, J.T. (2009). Electronic Interfacing with Living Cells. In: Belkin, S., Gu, M. (eds) Whole Cell Sensing Systems I. Advances in Biochemical Engineering / Biotechnology, vol 117. Springer, Berlin, Heidelberg. https://doi.org/10.1007/10_2009_5

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