Advertisement

Electrochemical measurement of quantal exocytosis using microchips

  • Kevin D. GillisEmail author
  • Xin A. Liu
  • Andrea Marcantoni
  • Valentina Carabelli
Invited Review

Abstract

Carbon-fiber electrodes (CFEs) are the gold standard for quantifying the release of oxidizable neurotransmitters from single vesicles and single cells. Over the last 15 years, microfabricated devices have emerged as alternatives to CFEs that offer the possibility of higher throughput, subcellular spatial resolution of exocytosis, and integration with other techniques for probing exocytosis including microfluidic cell handling and solution exchange, optical imaging and stimulation, and electrophysiological recording and stimulation. Here we review progress in developing electrochemical electrode devices capable of resolving quantal exocytosis that are fabricated using photolithography.

Keywords

bioMEMS Multi-electrode arrays 

Notes

Acknowledgements

We thank our colleagues who have partnered with us throughout the years in carrying out some of the work described in this manuscript.

Funding information

Work in the Gillis lab was supported by NIH grants R01NS048826, R01MH095046, and R44MH096650; Work in the Carabelli lab was supported by San Paolo Foundation, grant # CSTO 165284; and Italian Miur, grant # 2015 FNWP34.

Compliance with ethical standards

Conflict of interest

Kevin D. Gillis has an ownership interest in ExoCytronics, LLC, which is developing commercial microfabricated devices for assaying quantal exocytosis.

References

  1. 1.
    Alvarez de Toledo G, Fernandez-Chacon R, Fernandez JM (1993) Release of secretory products during transient vesicle fusion. Nature 363:554–558CrossRefPubMedGoogle Scholar
  2. 2.
    Amatore C, Arbault S, Chen Y, Crozatier C, Lemaitre F, Verchier Y (2006) Coupling of electrochemistry and fluorescence microscopy at indium tin oxide microelectrodes for the analysis of single exocytotic events. Angew Chem Int Ed Engl 45:4000–4003CrossRefPubMedGoogle Scholar
  3. 3.
    Amatore C, Klymenko OV, Svir I (2006) In situ and online monitoring of hydrodynamic flow profiles in microfluidic channels based upon microelectrochemistry: optimization of electrode locations. ChemPhysChem 7:482–487CrossRefPubMedGoogle Scholar
  4. 4.
    Amatore C, Arbault S, Lemaitre F, Verchier Y (2007) Comparison of apex and bottom secretion efficiency at chromaffin cells as measured by amperometry. Biophys Chem 127:165–171CrossRefPubMedGoogle Scholar
  5. 5.
    Amatore C, Delacotte J, Guille-Collignon M, Lemaitre F (2015) Vesicular exocytosis and microdevices—microelectrode arrays. Analyst 140:3687–3695CrossRefPubMedGoogle Scholar
  6. 6.
    Ayers S, Gillis KD, Lindau M, Minch BA (2007) Design of a CMOS potentiostat circuit for electrochemical detector arrays. IEEE Trans Circuits Syst I Regul Pap 54:736–744CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Ayers S, Berberian K, Gillis KD, Lindau M, Minch BA (2010) Post-CMOS fabrication of working electrodes for on-chip recordings of transmitter release. IEEE Trans Biomed Circuits Syst 4:86–92CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Barbour B, Isope P (2000) Combining loose cell-attached stimulation and recording. J Neurosci Methods 103:199–208CrossRefPubMedGoogle Scholar
  9. 9.
    Barizuddin S, Liu X, Mathai JC, Hossain M, Gillis KD, Gangopadhyay S (2010) Automated targeting of cells to electrochemical electrodes using a surface chemistry approach for the measurement of quantal exocytosis. ACS Chem Neurosci 1:590–597CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Berberian K, Kisler K, Fang Q, Lindau M (2009) Improved surface-patterned platinum microelectrodes for the study of exocytotic events. Anal Chem 81:8734–8740CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Bonnauron M, Saada S, Mer C, Gesset C, Williams OA, Rousseau L, Scorsone E, Mailley P, Nesladek M, Arnault JC, Bergonzo P (2008) Transparent diamond-on-glass micro-electrode arrays for ex-vivo neuronal study. Phys Status Solidi (A) 205:2126–2129CrossRefGoogle Scholar
  12. 12.
    Borges R, Camacho M, Gillis KD (2008) Measuring secretion in chromaffin cells using electrophysiological and electrochemical methods. Acta Physiol (Oxf) 192:173–184CrossRefGoogle Scholar
  13. 13.
    Bruns D, Riedel D, Klingauf J, Jahn R (2000) Quantal release of serotonin. Neuron 28:205–220CrossRefPubMedGoogle Scholar
  14. 14.
    Carabelli V, Gosso S, Marcantoni A, Xu Y, Colombo E, Gao Z, Vittone E, Kohn E, Pasquarelli A, Carbone E (2010) Nanocrystalline diamond microelectrode arrays fabricated on sapphire technology for high-time resolution of quantal catecholamine secretion from chromaffin cells. Biosens Bioelectron 26:92–98CrossRefPubMedGoogle Scholar
  15. 15.
    Carabelli V, Marcantoni A, Picollo F, Battiato A, Bernardi E, Pasquarelli A, Olivero P, Carbone E (2017) Planar diamond-based multiarrays to monitor neurotransmitter release and action potential firing: new perspectives in cellular neuroscience. ACS Chem Neurosci 8:252–264CrossRefPubMedGoogle Scholar
  16. 16.
    Chen P, Xu B, Tokranova N, Feng X, Castracane J, Gillis KD (2003) Amperometric detection of quantal catecholamine secretion from individual cells on micromachined silicon chips. Anal Chem 75:518–524CrossRefPubMedGoogle Scholar
  17. 17.
    Chen X, Gao Y, Hossain M, Gangopadhyay S, Gillis KD (2008) Controlled on-chip stimulation of quantal catecholamine release from chromaffin cells using photolysis of caged Ca2+ on transparent indium-tin-oxide microchip electrodes. Lab Chip 8:161–169CrossRefPubMedGoogle Scholar
  18. 18.
    Chow RH, Lv R (1995) Electrochemical detection of secretion from single cells. In: Sakmann B, Neher E (eds) Single channel recording. Plenum Press, New York, pp 245–275CrossRefGoogle Scholar
  19. 19.
    Chow RH, von Ruden L, Neher E (1992) Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356:60–63CrossRefPubMedGoogle Scholar
  20. 20.
    Ciolkowski EL, Maness KM, Cahill PS, Wightman RM, Evans DH, Fosset B, Amatore C (1994) Disproportionation during electrooxidation of catecholamines at carbon-fiber microelectrodes. Anal Chem 66:3611–3617CrossRefGoogle Scholar
  21. 21.
    Cole KS, Cole RH (1941) Dispersion and absorption in dielectrics: I. Alternating current characteristics. J Chem Phys 9:341–351CrossRefGoogle Scholar
  22. 22.
    Colliver TL, Hess EJ, Pothos EN, Sulzer D, Ewing AG (2000) Quantitative and statistical analysis of the shape of amperometric spikes recorded from two populations of cells. J Neurochem 74:1086–1097CrossRefPubMedGoogle Scholar
  23. 23.
    Cooper JM (1999) Towards electronic petri dishes and picolitre-scale single-cell technologies. Trends Biotechnol 17:226–230CrossRefPubMedGoogle Scholar
  24. 24.
    Cui HF, Ye JS, Chen Y, Chong SC, Sheu FS (2006) Microelectrode array biochip: tool for in vitro drug screening based on the detection of a drug effect on dopamine release from PC12 cells. Anal Chem 78:6347–6355CrossRefPubMedGoogle Scholar
  25. 25.
    Dias AF, Dernick G, Valero V, Yong MG, James CD, Craighead HG, Lindau M (2002) An electrochemical detector array to study cell biology on the nanoscale. Nanotechnology 13:285CrossRefGoogle Scholar
  26. 26.
    Dittami GM, Rabbitt RD (2010) Electrically evoking and electrochemically resolving quantal release on a microchip. Lab Chip 10:30–35CrossRefPubMedGoogle Scholar
  27. 27.
    Fiaccabrino GC, Koudelkahep M, Jeanneret S, Vandenberg A, Derooij NF (1994) Array of individually addressable microelectrodes. Sensor Actuators B Chem 19:675–677CrossRefGoogle Scholar
  28. 28.
    Finnegan JM, Pihel K, Cahill PS, Huang L, Zerby SE, Ewing AG, Kennedy RT, Wightman RM (1996) Vesicular quantal size measured by amperometry at chromaffin, mast, pheochromocytoma, and pancreatic beta-cells. J Neurochem 66:1914–1923CrossRefPubMedGoogle Scholar
  29. 29.
    Gao Y, Chen X, Gupta S, Gillis KD, Gangopadhyay S (2008) Magnetron sputtered diamond-like carbon microelectrodes for on-chip measurement of quantal catecholamine release from cells. Biomed Microdevices 10:623–629CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Gao Y, Bhattacharya S, Chen X, Barizuddin S, Gangopadhyay S, Gillis KD (2009) A microfluidic cell trap device for automated measurement of quantal catecholamine release from cells. Lab Chip 9:3442–3446CrossRefPubMedGoogle Scholar
  31. 31.
    Gao Z, Carabelli V, Carbone E, Colombo E, Demaria F, Dipalo M, Gosso S, Manfredotti C, Pasquarelli A, Rossi S, Xu Y, Vittone E, Kohn E (2010) Transparent diamond microelectrodes for biochemical application. Diam Relat Mater 19:1021–1026CrossRefGoogle Scholar
  32. 32.
    Gao Z, Carabelli V, Carbone E, Colombo E, Dipalo M, Manfredotti C, Pasquarelli A, Feneberg M, Thonke K, Vittone E, Kohn E (2011) Transparent microelectrode array in diamond technology. J Micro-Nano Mechatronics 6:33–37CrossRefGoogle Scholar
  33. 33.
    Gao C, Sun X, Gillis KD (2013) Fabrication of two-layer poly(dimethyl siloxane) devices for hydrodynamic cell trapping and exocytosis measurement with integrated indium tin oxide microelectrodes arrays. Biomed Microdevices 15:445–451Google Scholar
  34. 34.
    Ghosh J, Liu X, Gillis KD (2013) Electroporation followed by electrochemical measurement of quantal transmitter release from single cells using a patterned microelectrode. Lab Chip 13:2083–2090CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Gosso S, Turturici M, Franchino C, Colombo E, Pasquarelli A, Carbone E, Carabelli V (2014) Heterogeneous distribution of exocytotic microdomains in adrenal chromaffin cells resolved by high-density diamond ultra-microelectrode arrays. J Physiol 592:3215–3230CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Granado TC, Neusser G, Kranz C, Filho JBD, Carabelli V, Carbone E, Pasquarelli A (2015) Progress in transparent diamond microelectrode arrays. Phys Status Solidi (A) 212:2445–2453CrossRefGoogle Scholar
  37. 37.
    Gubernator NG, Zhang H, Stall RG, Mosharov EV, Pereira DB, Yue M, Balsanek V, Vadola PA, Mukherjee B, Edwards RH, Sulzer D, Sames D (2009) Fluorescent false neurotransmitters visualize dopamine release from individual presynaptic terminals. Science 324:1441–1444CrossRefPubMedGoogle Scholar
  38. 38.
    Hafez I, Kisler K, Berberian K, Dernick G, Valero V, Yong MG, Craighead HG, Lindau M (2005) Electrochemical imaging of fusion pore openings by electrochemical detector arrays. Proc Natl Acad Sci U S A 102:13879–13884CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Haller M, Heinemann C, Chow RH, Heidelberger R, Neher E (1998) Comparison of secretory responses as measured by membrane capacitance and by amperometry. Biophys J 74:2100–2113CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Hayasaka T, Yoshida S, Inoue K, Nakano M, Matsue T, Esashi M, Tanaka S (2015) Integration of boron-doped diamond microelectrode on CMOS-based amperometric sensor array by film transfer technology. J Microelectromech Syst 24:958–967CrossRefGoogle Scholar
  41. 41.
    Hondebrink L, Verboven AH, Drega WS, Schmeink S, de Groot MW, van Kleef RG, Wijnolts FM, de Groot A, Meulenbelt J, Westerink RH (2016) Neurotoxicity screening of (illicit) drugs using novel methods for analysis of microelectrode array (MEA) recordings. Neurotoxicology 55:1–9CrossRefPubMedGoogle Scholar
  42. 42.
    Jacobs CB, Peairs MJ, Venton BJ (2010) Review: carbon nanotube based electrochemical sensors for biomolecules. Anal Chim Acta 662:105–127CrossRefPubMedGoogle Scholar
  43. 43.
    Janischowsky K, Ebert W, Kohn E (2003) Bias enhanced nucleation of diamond on silicon (100) in a HFCVD system. Diam Relat Mater 12:336–339CrossRefGoogle Scholar
  44. 44.
    Ji X, Banks CE, Crossley A, Compton RG (2006) Oxygenated edge plane sites slow the electron transfer of the ferro-/ferricyanide redox couple at graphite electrodes. ChemPhysChem 7:1337–1344CrossRefPubMedGoogle Scholar
  45. 45.
    van Kempen GT, vanderLeest HT, van den Berg RJ, Eilers P, Westerink RH (2011) Three distinct modes of exocytosis revealed by amperometry in neuroendocrine cells. Biophys J 100:968–977CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Kim BN, Herbst AD, Kim SJ, Minch BA, Lindau M (2013) Parallel recording of neurotransmitters release from chromaffin cells using a 10x10 CMOS IC potentiostat array with on-chip working electrodes. Biosens Bioelectron 41:736–744CrossRefPubMedGoogle Scholar
  47. 47.
    Kiran R, Rousseau L, Lissorgues G, Scorsone E, Bongrain A, Yvert B, Picaud S, Mailley P, Bergonzo P (2012) Multichannel boron doped nanocrystalline diamond ultramicroelectrode arrays: design, fabrication and characterization. Sensors (Basel, Switzerland) 12:7682–7700CrossRefGoogle Scholar
  48. 48.
    Kisler K, Kim BN, Liu X, Berberian K, Fang Q, Mathai CJ, Gangopadhyay S, Gillis KD, Lindau M (2012) Transparent electrode materials for simultaneous amperometric detection of exocytosis and fluorescence microscopy. J Biomater Nanobiotechnol 3:243–253CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Larsen ST, Taboryski R (2012) All polymer chip for amperometric studies of transmitter release from large groups of neuronal cells. Analyst 137:5057–5061CrossRefPubMedGoogle Scholar
  50. 50.
    Li LM, Wang W, Zhang SH, Chen SJ, Guo SS, Francais O, Cheng JK, Huang WH (2011) Integrated microdevice for long-term automated perfusion culture without shear stress and real-time electrochemical monitoring of cells. Anal Chem 83:9524–9530CrossRefPubMedGoogle Scholar
  51. 51.
    Lin Y, Trouillon R, Svensson MI, Keighron JD, Cans AS, Ewing AG (2012) Carbon-ring microelectrode arrays for electrochemical imaging of single cell exocytosis: fabrication and characterization. Anal Chem 84:2949–2954CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Liu X, Barizuddin S, Shin W, Mathai CJ, Gangopadhyay S, Gillis KD (2011) Microwell device for targeting single cells to electrochemical microelectrodes for high-throughput amperometric detection of quantal exocytosis. Anal Chem 83:2445–2451CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Luong JH, Male KB, Glennon JD (2009) Boron-doped diamond electrode: synthesis, characterization, functionalization and analytical applications. Analyst 134:1965–1979CrossRefPubMedGoogle Scholar
  54. 54.
    Macpherson JV (2015) A practical guide to using boron doped diamond in electrochemical research. Phys Chem Chem Phys 17:2935–2949CrossRefPubMedGoogle Scholar
  55. 55.
    Mellander LJ, Trouillon R, Svensson MI, Ewing AG (2012) Amperometric post spike feet reveal most exocytosis is via extended kiss-and-run fusion. Sci Rep 2:907CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Meunier A, Jouannot O, Fulcrand R, Fanget I, Bretou M, Karatekin E, Arbault S, Guille M, Darchen F, Lemaitre F, Amatore C (2011) Coupling amperometry and total internal reflection fluorescence microscopy at ITO surfaces for monitoring exocytosis of single vesicles. Angew Chem Int Ed Engl 50:5081–5084CrossRefPubMedGoogle Scholar
  57. 57.
    Meunier A, Fulcrand R, Darchen F, Guille Collignon M, Lemaitre F, Amatore C (2012) Indium tin oxide devices for amperometric detection of vesicular release by single cells. Biophys Chem 162:14–21CrossRefPubMedGoogle Scholar
  58. 58.
    Mosharov EV, Sulzer D (2005) Analysis of exocytotic events recorded by amperometry. Nat Methods 2:651–658CrossRefPubMedGoogle Scholar
  59. 59.
    Moulton SE, Barisci JN, Bath A, Stella R, Wallace GG (2004) Studies of double layer capacitance and electron transfer at a gold electrode exposed to protein solutions. Electrochim Acta 49:4223–4230CrossRefGoogle Scholar
  60. 60.
    Nambiar S, Yeow JT (2011) Conductive polymer-based sensors for biomedical applications. Biosens Bioelectron 26:1825–1832CrossRefPubMedGoogle Scholar
  61. 61.
    Nebel CE, Shin D, Rezek B, Tokuda N, Uetsuka H, Watanabe H (2007) Diamond and biology. J R Soc Interface 4:439–461CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Nemani KV, Moodie KL, Brennick JB, Su A, Gimi B (2013) In vitro and in vivo evaluation of SU-8 biocompatibility. Mater Sci Eng C Mater Biol Appl 33:4453–4459CrossRefPubMedGoogle Scholar
  63. 63.
    Omiatek DM, Bressler AJ, Cans AS, Andrews AM, Heien ML, Ewing AG (2013) The real catecholamine content of secretory vesicles in the CNS revealed by electrochemical cytometry. Sci Rep 3:1447CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Pasquarelli A, Carabelli V, Xu Y, Colombo E, Gao Z, Scharpf J, Carbone E, Kohn E (2011) Diamond microelectrodes arrays for the detection of secretory cell activity. Int J Environ Anal Chem 91:150–160CrossRefGoogle Scholar
  65. 65.
    Picollo F, Gosso S, Vittone E, Pasquarelli A, Carbone E, Olivero P, Carabelli V (2013) A new diamond biosensor with integrated graphitic microchannels for detecting quantal exocytic events from chromaffin cells. Adv Mater 25:4696–4700CrossRefPubMedGoogle Scholar
  66. 66.
    Picollo F, Battiato A, Carbone E, Croin L, Enrico E, Forneris J, Gosso S, Olivero P, Pasquarelli A, Carabelli V (2015) Development and characterization of a diamond-insulated graphitic multi electrode array realized with ion beam lithography. Sensors 15:515–528CrossRefGoogle Scholar
  67. 67.
    Picollo F, Battiato A, Bernardi E, Marcantoni A, Pasquarelli A, Carbone E, Olivero P, Carabelli V (2016) Microelectrode arrays of diamond-insulated graphitic channels for real-time detection of exocytotic events from cultured chromaffin cells and slices of adrenal glands. Anal Chem 88:7493–7499CrossRefPubMedGoogle Scholar
  68. 68.
    Picollo F, Battiato A, Bernardi E, Plaitano M, Franchino C, Gosso S, Pasquarelli A, Carbone E, Olivero P, Carabelli V (2016) All-carbon multi-electrode array for real-time in vitro measurements of oxidizable neurotransmitters. Sci Rep 6:20682CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Pothos EN, Davila V, Sulzer D (1998) Presynaptic recording of quanta from midbrain dopamine neurons and modulation of the quantal size. J Neurosci 18:4106–4118PubMedGoogle Scholar
  70. 70.
    Rothe J, Frey O, Stettler A, Chen Y, Hierlemann A (2014) Fully integrated CMOS microsystem for electrochemical measurements on 32 x 32 working electrodes at 90 frames per second. Anal Chem 86:6425–6432CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Rozlosnik N (2009) New directions in medical biosensors employing poly(3,4-ethylenedioxy thiophene) derivative-based electrodes. Anal Bioanal Chem 395:637–645CrossRefPubMedGoogle Scholar
  72. 72.
    Schroeder TJ, Jankowski JA, Kawagoe KT, Wightman RM, Lefrou C, Amatore C (1992) Analysis of diffusional broadening of vesicular packets of catecholamines released from biological cells during exocytosis. Anal Chem 64:3077–3083CrossRefPubMedGoogle Scholar
  73. 73.
    Schroeder TJ, Borges R, Finnegan JM, Pihel K, Amatore C, Wightman RM (1996) Temporally resolved, independent stages of individual exocytotic secretion events. Biophys J 70:1061–1068CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Segura F, Brioso MA, Gomez JF, Machado JD, Borges R (2000) Automatic analysis for amperometrical recordings of exocytosis. J Neurosci Methods 103:151–156CrossRefPubMedGoogle Scholar
  75. 75.
    Sen A, Barizuddin S, Hossain M, Polo-Parada L, Gillis KD, Gangopadhyay S (2009) Preferential cell attachment to nitrogen-doped diamond-like carbon (DLC:N) for the measurement of quantal exocytosis. Biomaterials 30:1604–1612CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Shi BX, Wang Y, Zhang K, Lam TL, Chan HL (2011) Monitoring of dopamine release in single cell using ultrasensitive ITO microsensors modified with carbon nanotubes. Biosens Bioelectron 26:2917–2921CrossRefPubMedGoogle Scholar
  77. 77.
    Sigworth FJ (1995) Electronic design of the patch clamp. In: Sakmann B, Neher E (eds) Single-channel recording. Plenum Press, New York, pp 95–127CrossRefGoogle Scholar
  78. 78.
    Spégel C, Heiskanen A, Acklid J, Wolff A, Taboryski R, Emnéus J, Ruzgas T (2007) On-chip determination of dopamine exocytosis using mercaptopropionic acid modified microelectrodes. Electroanalysis 19:263–271CrossRefGoogle Scholar
  79. 79.
    Spegel C, Heiskanen A, Pedersen S, Emneus J, Ruzgas T, Taboryski R (2008) Fully automated microchip system for the detection of quantal exocytosis from single and small ensembles of cells. Lab Chip 8:323–329CrossRefPubMedGoogle Scholar
  80. 80.
    Stotter J, Zak J, Behler Z, Show Y, Swain GM (2002) Optical and electrochemical properties of optically transparent, boron-doped diamond thin films deposited on quartz. Anal Chem 74:5924–5930CrossRefPubMedGoogle Scholar
  81. 81.
    Sun X, Gillis KD (2006) On-chip amperometric measurement of quantal catecholamine release using transparent indium tin oxide electrodes. Anal Chem 78:2521–2525CrossRefPubMedGoogle Scholar
  82. 82.
    Suzuki I, Fukuda M, Shirakawa K, Jiko H, Gotoh M (2013) Carbon nanotube multi-electrode array chips for noninvasive real-time measurement of dopamine, action potentials, and postsynaptic potentials. Biosens Bioelectron 49:270–275CrossRefPubMedGoogle Scholar
  83. 83.
    Wang J, Ewing AG (2014) Simultaneous study of subcellular exocytosis with individually addressable multiple microelectrodes. Analyst 139:3290–3295CrossRefPubMedGoogle Scholar
  84. 84.
    Wang CT, Bai J, Chang PY, Chapman ER, Jackson MB (2006) Synaptotagmin-Ca2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: fusion pore opening and fusion pore dilation. J Physiol 570:295–307CrossRefPubMedGoogle Scholar
  85. 85.
    Wang J, Trouillon R, Lin Y, Svensson MI, Ewing AG (2013) Individually addressable thin-film ultramicroelectrode array for spatial measurements of single vesicle release. Anal Chem 85:5600–5608CrossRefPubMedGoogle Scholar
  86. 86.
    Wang J, Trouillon R, Dunevall J, Ewing AG (2014) Spatial resolution of single-cell exocytosis by microwell-based individually addressable thin film ultramicroelectrode arrays. Anal Chem 86:4515–4520CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Wang L, Xu H, Song Y, Luo J, Wei W, Xu S, Cai X (2015) Highly sensitive detection of quantal dopamine secretion from pheochromocytoma cells using neural microelectrode array electrodeposited with polypyrrole graphene. ACS Appl Mater Interfaces 7:7619–7626CrossRefPubMedGoogle Scholar
  88. 88.
    Wightman RM, Jankowski JA, Kennedy RT, Kawagoe KT, Schroeder TJ, Leszczyszyn DJ, Near JA, Diliberto EJ Jr, Viveros OH (1991) Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc Natl Acad Sci U S A 88:10754–10758CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Wightman RM, Schroeder TJ, Finnegan JM, Ciolkowski EL, Pihel K (1995) Time course of release of catecholamines from individual vesicles during exocytosis at adrenal medullary cells. Biophys J 68:383–390CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Wigstrom J, Dunevall J, Najafinobar N, Lovric J, Wang J, Ewing AG, Cans AS (2016) Lithographic microfabrication of a 16-electrode array on a probe tip for high spatial resolution electrochemical localization of exocytosis. Anal Chem 88:2080–2087CrossRefPubMedGoogle Scholar
  91. 91.
    Yakushenko A, Schnitker J, Wolfrum B (2012) Printed carbon microelectrodes for electrochemical detection of single vesicle release from PC12 cells. Anal Chem 84:4613–4617CrossRefPubMedGoogle Scholar
  92. 92.
    Yakushenko A, Katelhon E, Wolfrum B (2013) Parallel on-chip analysis of single vesicle neurotransmitter release. Anal Chem 85:5483–5490CrossRefPubMedGoogle Scholar
  93. 93.
    Yang SY, Kim BN, Zakhidov AA, Taylor PG, Lee JK, Ober CK, Lindau M, Malliaras GG (2011) Detection of transmitter release from single living cells using conducting polymer microelectrodes. Adv Mater 23:H184–H188CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Yao J, Gillis KD (2012) Quantification of noise sources for amperometric measurement of quantal exocytosis using microelectrodes. Analyst 137:2674–2681CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Yao J, Liu XA, Gillis KD (2015) Two approaches for addressing electrochemical electrode arrays with reduced external connections. Anal Methods 7:5760–5766CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Zachek MK, Hermans A, Wightman RM, McCarty GS (2008) Electrochemical dopamine detection: comparing gold and carbon fiber microelectrodes using background subtracted fast scan cyclic voltammetry. J Electroanal Chem (Lausanne Switz) 614:113–120CrossRefGoogle Scholar
  97. 97.
    Zhang B, Adams KL, Luber SJ, Eves DJ, Heien ML, Ewing AG (2008) Spatially and temporally resolved single-cell exocytosis utilizing individually addressable carbon microelectrode arrays. Anal Chem 80:1394–1400CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Zhang B, Heien ML, Santillo MF, Mellander L, Ewing AG (2011) Temporal resolution in electrochemical imaging on single PC12 cells using amperometry and voltammetry at microelectrode arrays. Anal Chem 83:571–577CrossRefPubMedGoogle Scholar
  99. 99.
    Zhao Y, Fang Q, Herbst AD, Berberian KN, Almers W, Lindau M (2013) Rapid structural change in synaptosomal-associated protein 25 (SNAP25) precedes the fusion of single vesicles with the plasma membrane in live chromaffin cells. Proc Natl Acad Sci U S A 110:14249–14254CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Zhou Z, Misler S, Chow RH (1996) Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys J 70:1543–1552CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Kevin D. Gillis
    • 1
    • 2
    • 3
    Email author
  • Xin A. Liu
    • 3
  • Andrea Marcantoni
    • 4
  • Valentina Carabelli
    • 4
  1. 1.Department of BioengineeringUniversity of MissouriColumbiaUSA
  2. 2.Department of Medical Pharmacology and PhysiologyUniversity of MissouriColumbiaUSA
  3. 3.Dalton Cardiovascular Research CenterUniversity of MissouriColumbiaUSA
  4. 4.Department of Drug Science and “NIS” Inter-departmental CentreUniversity of TorinoTorinoItaly

Personalised recommendations