1932

Abstract

Electrochemical impedance spectroscopy (EIS) measures the frequency spectrum of an electrochemical interface to resist an alternating current. This method allows label-free and noninvasive studies on interfacial adsorption and molecular interactions and has applications in biosensing and drug screening. Although powerful, traditional EIS lacks spatial resolution or imaging capability, hindering the study of heterogeneous electrochemical processes on electrodes. We have recently developed a plasmonics-based electrochemical impedance technique to image local electrochemical impedance with a submicron spatial resolution and a submillisecond temporal resolution. In this review, we provide a systematic description of the theory, instrumentation, and data analysis of this technique. To illustrate its present and future applications, we further describe several selected samples analyzed with this method, including protein microarrays, two-dimensional materials, and single cells. We conclude by summarizing the technique's unique features and discussing the remaining challenges and new directions of its application.

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2017-06-12
2024-06-23
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Literature Cited

  1. Chang BY, Park SM. 1.  2010. Electrochemical impedance spectroscopy. Annu. Rev. Anal. Chem. 3:207–29 [Google Scholar]
  2. Lisdat F, Schäfer D. 2.  2008. The use of electrochemical impedance spectroscopy for biosensing. Anal. Bioanal. Chem. 391:1555–67 [Google Scholar]
  3. Randviir EP, Banks CE. 3.  2013. Electrochemical impedance spectroscopy: an overview of bioanalytical applications. Anal. Methods 5:1098–115 [Google Scholar]
  4. Giaever I, Keese CR. 4.  1993. A morphological biosensor for mammalian cells. Nature 366:591–92 [Google Scholar]
  5. Yu NC, Atienza JM, Bernard J, Blanc S, Zhu J. 5.  et al. 2006. Real-time monitoring of morphological changes in living cells by electronic cell sensor arrays: an approach to study G protein-coupled receptors. Anal. Chem. 78:35–43 [Google Scholar]
  6. Hong J, Kandasamy K, Marimuthu M, Choi CS, Kim S. 6.  2011. Electrical cell-substrate impedance sensing as a non-invasive tool for cancer cell study. Analyst 136:237–45 [Google Scholar]
  7. Rothermel A, Nieber M, Müller J, Wolf P, Schmidt M, Robitzki AA. 7.  2006. Real-time measurement of PMA-induced cellular alterations by microelectrode array-based impedance spectroscopy. Biotechniques 41:445–50 [Google Scholar]
  8. Chai KTC, Davies JH, Cumming DRS. 8.  2007. Electrical impedance tomography for sensing with integrated microelectrodes on a CMOS microchip. Sens. Actuators B 127:97–101 [Google Scholar]
  9. Jahnke HG, Rothermel A, Sternberger I, Mack TGA, Kurz RG. 9.  et al. 2009. An impedimetric microelectrode-based array sensor for label-free detection of tau hyperphosphorylation in human cells. Lab Chip 9:1422–28 [Google Scholar]
  10. Sun T, Tsuda S, Zauner KP, Morgan H. 10.  2010. On-chip electrical impedance tomography for imaging biological cells. Biosens. Bioelectron. 25:1109–15 [Google Scholar]
  11. Meir A, Rubinsky B. 11.  2014. Electrical impedance tomographic imaging of a single cell electroporation. Biomed. Microdev 16427–37 [Google Scholar]
  12. Swisher SL, Lin MC, Liao A, Leeflang EJ, Khan Y. 12.  et al. 2015. Impedance sensing device enables early detection of pressure ulcers in vivo. Nat. . Commun. 6:6575 [Google Scholar]
  13. Alpuche-Aviles MA, Wipf DO. 13.  2001. Impedance feedback control for scanning electrochemical microscopy. Anal. Chem. 73:4873–81 [Google Scholar]
  14. Amemiya S, Bard AJ, Fan FRF, Mirkin MV, Unwin PR. 14.  2008. Scanning electrochemical microscopy. Annu. Rev. Anal. Chem. 1:95–131 [Google Scholar]
  15. Schulte A, Nebel M, Schuhmann W. 15.  2010. Scanning electrochemical microscopy in neuroscience. Annu. Rev. Anal. Chem. 3:299–318 [Google Scholar]
  16. Diakowski PM, Chen M. 16.  2012. Surface analysis of materials in aqueous solution by localized alternating current impedance measurements. Anal. Chem. 84:7622–25 [Google Scholar]
  17. Zhou LS, Zhou Y, Shi WQ, Baker LA. 17.  2015. Alternating current potentiometric scanning ion conductance microscopy (AC-PSICM). J. Phys. Chem. C 119:14392–99 [Google Scholar]
  18. Foley KJ, Shan X, Tao NJ. 18.  2008. Surface impedance imaging technique. Anal. Chem. 80:5146–51 [Google Scholar]
  19. Wang W, Foley K, Shan X, Wang SP, Eaton S. 19.  et al. 2011. Single cells and intracellular processes studied by a plasmonic-based electrochemical impedance microscopy. Nat. Chem. 3:249–55 [Google Scholar]
  20. Lu J, Wang W, Wang SP, Shan XN, Li JH, Tao NJ. 20.  2012. Plasmonic-based electrochemical impedance spectroscopy: application to molecular binding. Anal. Chem. 84:327–33 [Google Scholar]
  21. Homola J. 21.  2008. Surface plasmon resonance sensors for detection of chemical and biological species. Chem. Rev. 108:462–93 [Google Scholar]
  22. Brockman JM, Nelson BP, Corn RM. 22.  2000. Surface plasmon resonance imaging measurements of ultrathin organic films. Annu. Rev. Phys. Chem. 51:41–63 [Google Scholar]
  23. Kretschmann E, Raether H. 23.  1968. Radiative decay of non radiative surface plasmons excited by light. Z. Naturforsch. 230:2135–36 [Google Scholar]
  24. Rothenhäusler B, Knoll W. 24.  1988. Surface plasmon microscopy. Nature 332:615–17 [Google Scholar]
  25. Scarano S, Mascini M, Turner APF, Minunni M. 25.  2010. Surface plasmon resonance imaging for affinity-based biosensors. Biosens. Bioelectron. 25:957–66 [Google Scholar]
  26. Abbas A, Linman MJ, Cheng QA. 26.  2011. New trends in instrumental design for surface plasmon resonance-based biosensors. Biosens. Bioelectron. 26:1815–24 [Google Scholar]
  27. Huang B, Yu F, Zare RN. 27.  2007. Surface plasmon resonance imaging using a high numerical aperture microscope objective. Anal. Chem. 79:2979–83 [Google Scholar]
  28. Wang W, Wang SP, Liu Q, Wu J, Tao NJ. 28.  2012. Mapping single-cell-substrate interactions by surface plasmon resonance microscopy. Langmuir 28:13373–79 [Google Scholar]
  29. Wang W, Yang YZ, Wang SP, Nagaraj VJ, Liu Q. 29.  et al. 2012. Label-free measuring and mapping of binding kinetics of membrane proteins in single living cells. Nat. Chem. 4:846–53 [Google Scholar]
  30. Yang YZ, Yu H, Shan XN, Wang W, Liu XW. 30.  et al. 2015. Label-free tracking of single organelle transportation in cells with nanometer precision using a plasmonic imaging technique. Small 11:2878–84 [Google Scholar]
  31. Syal K, Iriya R, Yang YZ, Yu H, Wang SP. 31.  et al. 2016. Antimicrobial susceptibility test with plasmonic imaging and tracking of single bacterial motions on nanometer scale. ACS Nano 10:845–52 [Google Scholar]
  32. Syal K, Wang W, Shan XN, Wang SP, Chen HY, Tao NJ. 32.  2015. Plasmonic imaging of protein interactions with single bacterial cells. Biosens. Bioelectron. 63:131–37 [Google Scholar]
  33. Wang SP, Shan XN, Patel U, Huang XP, Lu J. 33.  et al. 2010. Label-free imaging, detection, and mass measurement of single viruses by surface plasmon resonance. PNAS 107:16028–32 [Google Scholar]
  34. Shan XN, Diez-Pérez I, Wang LJ, Wiktor P, Gu Y. 34.  et al. 2012. Imaging the electrocatalytic activity of single nanoparticles. Nat. Nanotechnol. 7:668–72 [Google Scholar]
  35. Fang YM, Wang W, Wo X, Luo YS, Yin SW. 35.  et al. 2014. Plasmonic imaging of electrochemical oxidation of single nanoparticles. J. Am. Chem. Soc. 136:12584–87 [Google Scholar]
  36. Halpern AR, Wood JB, Wang Y, Corn RM. 36.  2014. Single-nanoparticle near-infrared surface plasmon resonance microscopy for real-time measurements of DNA hybridization adsorption. ACS Nano 8:1022–30 [Google Scholar]
  37. Shan XN, Chen S, Wang H, Chen ZX, Guan Y. 37.  et al. 2015. Mapping local quantum capacitance and charged impurities in graphene via plasmonic impedance imaging. Adv. Mater. 27:6213–19 [Google Scholar]
  38. Fang YM, Chen S, Wang W, Shan XN, Tao NJ. 38.  2015. Real-time monitoring of phosphorylation kinetics with self-assembled nano-oscillators. Angew. Chem. Int. Ed. 54:2538–42 [Google Scholar]
  39. Cho K, Fasoli JB, Yoshimatsu K, Shea KJ, Corn RM. 39.  2015. Measuring melittin uptake into hydrogel nanoparticles with near-infrared single nanoparticle surface plasmon resonance microscopy. Anal. Chem. 87:4973–79 [Google Scholar]
  40. Laplatine L, Leroy L, Calemczuk R, Baganizi D, Marche PN. 40.  et al. 2014. Spatial resolution in prism-based surface plasmon resonance microscopy. Opt. Exp. 22:22771–85 [Google Scholar]
  41. Abadian PN, Kelley CP, Goluch ED. 41.  2014. Cellular analysis and detection using surface plasmon resonance techniques. Anal. Chem. 86:2799–812 [Google Scholar]
  42. Orlowski R, Raether H. 42.  1976. The total reflection of light at smooth and rough silver films and surface plasmons. Surf. Sci. 54:303–8 [Google Scholar]
  43. Heaton RJ, Peterson AW, Georgiadis RM. 43.  2001. Electrostatic surface plasmon resonance: direct electric field-induced hybridization and denaturation in monolayer nucleic acid films and label-free discrimination of base mismatches. PNAS 98:3701–4 [Google Scholar]
  44. Wang SP, Huang XP, Shan XN, Foley KJ, Tao NJ. 44.  2010. Electrochemical surface plasmon resonance: basic formalism and experimental validation. Anal. Chem. 82:935–41 [Google Scholar]
  45. Fang YM, Wang H, Yu H, Liu XW, Wang W. 45.  et al. 2016. Plasmonic imaging of electrochemical reactions of single nanoparticles. Acc. Chem. Res. 49:2614–24 [Google Scholar]
  46. Shan XN, Patel U, Wang SP, Iglesias R, Tao NJ. 46.  2010. Imaging local electrochemical current via surface plasmon resonance. Science 327:1363–66 [Google Scholar]
  47. Manesse M, Stambouli V, Boukherroub R, Szunerits S. 47.  2008. Electrochemical impedance spectroscopy and surface plasmon resonance studies of DNA hybridization on gold/SiOx interfaces. Analyst 133:1097–103 [Google Scholar]
  48. Vandenryt T, Pohl A, van Grinsven B, Thoelen R, De Ceuninck W. 48.  et al. 2013. Combining electrochemical impedance spectroscopy and surface plasmon resonance into one simultaneous read-out system for the detection of surface interactions. Sensors 13:14650–61 [Google Scholar]
  49. Patskovsky S, Latendresse V, Dallaire AM, Doré-Mathieu L, Meunier M. 49.  2014. Combined surface plasmon resonance and impedance spectroscopy systems for biosensing. Analyst 139:596–602 [Google Scholar]
  50. Giebel KF, Bechinger C, Herminghaus S, Riedel M, Leiderer P. 50.  et al. 1999. Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy. Biophys. J. 76:509–16 [Google Scholar]
  51. Peterson AW, Halter M, Tona A, Bhadriraju K, Plant AL. 51.  2009. Surface plasmon resonance imaging of cells and surface-associated fibronectin. BMC Cell Biol 10:16–32 [Google Scholar]
  52. MacGriff C, Wang SP, Wiktor P, Wang W, Shan XN, Tao NJ. 52.  2013. Charge-based detection of small molecules by plasmonic-based electrochemical impedance microscopy. Anal. Chem. 85:6682–87 [Google Scholar]
  53. Shan XN, Fang YM, Wang SP, Guan Y, Chen HY, Tao NJ. 53.  2014. Detection of charges and molecules with self-assembled nano-oscillators. Nano Lett 14:4151–57 [Google Scholar]
  54. Liang WB, Wang SP, Festa F, Wiktor P, Wang W. 54.  et al. 2014. Measurement of small molecule binding kinetics on a protein microarray by plasmonic-based electrochemical impedance imaging. Anal. Chem. 86:9860–65 [Google Scholar]
  55. Lu J, Li J. 55.  2014. Monitoring DNA conformation and charge regulations by plasmonic-based electrochemical impedance platform. Electrochem. Commun. 45:5–8 [Google Scholar]
  56. Moore CD, Ajala OZ, Zhu H. 56.  2016. Applications in high-content functional protein microarrays. Curr. Opin. Chem. Biol. 30:21–27 [Google Scholar]
  57. Dallaire AM, Patskovsky S, Vallée-Bélisle A, Meunier M. 57.  2015. Electrochemical plasmonic sensing system for highly selective multiplexed detection of biomolecules based on redox nanoswitches. Biosens. Bioelectron. 71:75–81 [Google Scholar]
  58. Polonschii C, David S, Gáspár S, Gheorghiu M, Rosu-Hamzescu M, Gheorghiu E. 58.  2014. Complementarity of EIS and SPR to reveal specific and nonspecific binding when interrogating a model bioaffinity sensor; perspective offered by plasmonic based EIS. Anal. Chem. 86:8553–62 [Google Scholar]
  59. Wang YX, Shan XN, Wang SP, Tao NJ, Blanchard PY. 59.  et al. 2016. Imaging local electric field distribution by plasmonic impedance microscopy. Anal. Chem. 88:1547–52 [Google Scholar]
  60. Xia JL, Chen F, Li JH, Tao NJ. 60.  2009. Measurement of the quantum capacitance of graphene. Nat. Nanotechnol. 4:505–9 [Google Scholar]
  61. Wu CY, Rehman FU, Li JY, Ye J, Zhang YY. 61.  et al. 2015. Real-time evaluation of live cancer cells by an in situ surface plasmon resonance and electrochemical study. ACS Appl. Mater. Interf. 7:24848–54 [Google Scholar]
  62. Gamal W, Borooah S, Smith S, Underwood I, Srsen V. 62.  et al. 2015. Real-time quantitative monitoring of hiPSC-based model of macular degeneration on Electric Cell-substrate Impedance Sensing microelectrodes. Biosens. Bioelectron. 71:445–55 [Google Scholar]
  63. Xu YC, Xie XW, Duan Y, Wang L, Cheng Z, Cheng J. 63.  2016. A review of impedance measurements of whole cells. Biosens. Bioelectron. 77:824–36 [Google Scholar]
  64. Keese CR, Wegener J, Walker SR, Giaever L. 64.  2004. Electrical wound-healing assay for cells in vitro. . PNAS 101:1554–59 [Google Scholar]
  65. Xiao CD, Lachance B, Sunahara G, Luong JHT. 65.  2002. Assessment of cytotoxicity using electric cell-substrate impedance sensing: concentration and time response function approach. Anal. Chem. 74:5748–53 [Google Scholar]
  66. Shah P, Zhu XN, Zhang XJ, He J, Li CZ. 66.  2016. Microelectromechanical system-based sensing arrays for comparative in vitro nanotoxicity assessment at single cell and small cell-population using electrochemical impedance spectroscopy. ACS Appl. Mater. Interf. 8:5804–12 [Google Scholar]
  67. Amatore C, Arbault S, Guille M, Lemaître F. 67.  2008. Electrochemical monitoring of single cell secretion: vesicular exocytosis and oxidative stress. Chem. Rev. 108:2585–621 [Google Scholar]
  68. Lu J, Li JH. 68.  2015. Label-free imaging of dynamic and transient calcium signaling in single cells. Angew. Chem. Int. Ed. 54:13576–80 [Google Scholar]
  69. Méjard R, Griesser HJ, Thierry B. 69.  2014. Optical biosensing for label-free cellular studies. TRAC Trend. Anal. Chem. 53:178–86 [Google Scholar]
  70. Yanase Y, Hiragun T, Ishii K, Kawaguchi T, Yanase T. 70.  et al. 2014. Surface plasmon resonance for cell-based clinical diagnosis. Sensors 14:4948–59 [Google Scholar]
  71. Wang W, Yin LL, Gonzalez-Malerva L, Wang SP, Yu XB. 71.  et al. 2014. In situ drug-receptor binding kinetics in single cells: a quantitative label-free study of anti-tumor drug resistance. Sci. Rep. 4:6609 [Google Scholar]
  72. Yin LL, Yang YZ, Wang SP, Wang W, Zhang ST, Tao NJ. 72.  2015. Measuring binding kinetics of antibody-conjugated gold nanoparticles with intact cells. Small 11:3782–88 [Google Scholar]
  73. Zhang FN, Wang SP, Yin LL, Yang YZ, Guan Y. 73.  et al. 2015. Quantification of epidermal growth factor receptor expression level and binding kinetics on cell surfaces by surface plasmon resonance imaging. Anal. Chem. 87:9960–65 [Google Scholar]
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