Advances in Biochemistry

| Peer-Reviewed |

"MS-Patch-Clamp" or the Possibility of Mass Spectrometry Hybridization with Patch-Clamp Setups for Single Cell Metabolomics and Channelomics

Received: 26 August 2015    Accepted: 09 October 2015    Published: 30 October 2015
Views:       Downloads:

Share This Article

Abstract

In this projecting work we propose a mass spectrometric patch-clamp equipment with the capillary performing both a local potential registration at the cell membrane and the analyte suction simultaneously. This paper provides a current literature analysis comparing the possibilities of the novel approach proposed with the known methods, such as scanning patch-clamp, scanning ion conductance microscopy, patch clamp based on scanning probe microscopy technology, quantitative subcellular secondary ion mass spectrometry or "ion microscopy", live single-cell mass spectrometry, in situ cell-by-cell imaging, single-cell video-mass spectrometry, etc. We also consider the ways to improve the informativeness of these methods and particularly emphasize the trend at the increasing of the analysis complexity. We propose here the way to improve the efficiency of the cell trapping to the capillary during MS-path-clamp, as well as to provide laser surface ionization using laser trapping and tweezing of cells with the laser beam transmitted through the capillary as a waveguide. It is also possible to combine the above system with the microcolumn separation system or capillary electrophoresis as an optional direction of further development of the complex of analytical techniques emerging from the MS variation of patch-clamp.

DOI 10.11648/j.ab.20150306.11
Published in Advances in Biochemistry (Volume 3, Issue 6, December 2015)
Page(s) 66-71
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Patch-Clamp, Chanellomics, Scanning Ion Conductance Microscopy, Membrane Receptors, Ion Microscopy, Quantitative Subcellular Secondary Ion Mass Spectrometry, Single-Cell Video-Mass Spectrometry

References
[1] Cannon D. M., Winograd N., Ewing A.G., Quantitative chemical analysis of single cells. Ann. Rev. Biophys. Biomol. Struct. 2000, 29(1): 239-263.
[2] Neher E., Sakmann B. Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature. 1976, 260(5554): 799-802.
[3] Hamill O.P., Marty A., Neher E., Sakhman B., Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archiv. 1981, 391(2): 85-100.
[4] Barrett-Jolley R., Lewis R., Fallman R., Mobasheri A. The emerging chondrocyte channelome. Front. Physiol. 2010, 1, Art. No. 135, 1-11.
[5] Publicover S.J., Barratt C.L. Chloride channels join the sperm "channelome". Journ. Physiol. 2012, 590(11): 2553- 2554.
[6] Camerino D.C., Tricarico D., Desaphy J.F. Ion channel pharmacology. Neurotherapeut. 2007, 4(2): 184–198.
[7] Orwar O., Jardemark K., Jacobson I., Moscho A., Fishman H.A., Scheller R. H., Zare R.N. Patch-clamp detection of neurotransmitters in capillary electrophoresis. Science. 1996, 272(5269): 1779-1782.
[8] Jardemark K., Orwar O., Jacobson I., Moscho A., Fishman H.A., Hamberger A., Sandberg M., Scheller R.H., Zare R.N. Patch Clamp Detection of Neuroreceptor Modulators in Capillary Electrophoresis. In: "Neurochemistry: Cellular, Molecular and Clinical Aspects", Teelken, A., Korf, J, Eds.; "Springer": New York, 1997, pp. 1131-1138.
[9] Jardemark K., Orwar O., Jacobson I., Moscho A., Zare R.N. Patch clamp detection in capillary electrophoresis. Anal. Chem. 1997, 69(17): 3427-3434.
[10] Farre C., Sjöberg A., Jardemark K., Jacobson I., Orwar O. Screening of ion channel receptor agonists using capillary electrophoresis – patch clamp detection with resensitized detector cells. Anal Chem. 2001, 73(6): 1228-1233.
[11] Holland L.A., Lunte S. M. Capillary electrophoresis coupled to electrochemical detection: a review of recent advances. Anal. Commun. 1998, 35: 1H-4H.
[12] Kitamura K., Judkewitz B., Kano M., Denk W., Häusser M.Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nature Meth. 2008, 5(1): 61-67.
[13] Zabzdyr J.L., Lillard S.J. Measurement of single-cell gene expression using capillary electrophoresis. Anal. Chem. 2001, 73(23): 5771-5775.
[14] Spassova M., Tsoneva I., Petrov A.G, Petkova J.I., Neumann E. Dip patch clamp currents suggest electro- diffusive transport of the polyelectrolyte DNA through lipid bilayers. Biophys. Chem. 1994, 52(3): 267-2674.
[15] Sucher N.J., Deitcher D.L. PCR and patch-clamp analysis of single neurons. Neuron. 1995, 14(6): 1095-1100.
[16] Griffith W.H., Han S.-H., McCool B.A., Murchison D. Molecules and Membrane Activity: Single-Cell RT-PCR & Patch-Clamp Recording from Central Neurons. Neuroanat. Tract-Tracing. 2006, 3: 142-174.
[17] Korchev Y. E., Milovanovic M., Bashford C.L., Bennett D.C., Sviderskaya E.V., Vodyanoy I., Lab M.J. Specialized scanning ion-conductance microscope for imaging of living cells. Journ. Microsc. 1997, 188(1): 17-23.
[18] Gu Y., Gorelik J., Spohr H. A., Shevchuk A., Lab M.J., Harding S.E., Vodyanoy I., Klenerman D., Korchev Y.E. High-resolution scanning patch-clamp: new insights into cell function. FASEB Journ. 2002, 16(7): 748-750.
[19] Laskin J., Heath B.S., Roach P.J., Cazares L., Semmes O. Tissue imaging using nanospray desorption electrospray ionization mass spectrometry. Anal. Chem. 2012, 84(1): 141-148.
[20] Ausserer W.A., Ling Y.C., Chandra S., Morrison G.H. Quantitative imaging of boron, calcium, magnesium, potassium, and sodium distributions in cultured cells with ion microscopy. Anal. Chem. 1989, 61(24) 2690-2695.
[21] Bennett B.D., Zha X., Gay I., Morrison G.H. Intracellular boron localization and uptake in cell cultures using imaging secondary ion mass spectrometry (ion microscopy) for neutron capture therapy for cancer. Biol. Cell. 1992, 74(1): 105-108.
[22] Chandra S., Lorey D.R., Smith D.R. Quantitative subcellular secondary ion mass spectrometry (SIMS) imaging of boron-10 and boron-11 isotopes in the same cell delivered by two combined BNCT drugs: in vitro studies on human glioblastoma T98G cells. Rad. Res. 2002, 157(6): 700-710.
[23] Chandra S., Henderson J.E., Morrison G.H., Hess G.P. Imaging acetylcholine-receptor-induced influx of inorganic ions at single-cell resolution with ion microscopy. Anal. Biochem. 1991, 197(2): 284-289.
[24] Thoreson W.B., Nitzan R., Miller R.F. Chloride efflux inhibits single calcium channel open probability in vertebrate photoreceptors: chloride imaging and cell-attached patch-clamp recordings. Vis. Neurosci. 2000, 17(2): 197-206.
[25] Chandra S. Quantitative imaging of chemical composition in single cells by secondary ion mass spectrometry: cisplatin affects calcium stores in renal epithelial cells. Meth. Molec. Biol. 2010, 656: 113-130.
[26] Ostrowski S.G., Kurczy M.E., Roddy T.P., Winograd N., Ewing A.G.. Secondary ion MS imaging to relatively quantify cholesterol in the membranes of individual cells from differentially treated populations. Anal. Chem. 2007, 79(10): 3554-3560.
[27] Lorey D.R., Morrison G.H., Chandra S. Dynamic secondary ion mass spectrometry analysis of boron from boron neutron capture therapy drugs in co-cultures: single- cell imaging of two different cell types within the same ion microscopy field of imaging. Anal. Chem. 2001, 73(16): 3947-3953.
[28] Masujima T. Live single-cell mass spectrometry. Anal. Sci. 2009, 25: 953-960.
[29] Shrestha B., Vertes A. Direct analysis of single cells by mass spectrometry at atmospheric pressure. Journ. Vis Exp. 2010, 43: pii: 2144 [doi: 10.3791/2144].
[30] Tsuyama N., Mizuno H., Masujima T. Mass spectrometry for cellular and tissue analyses in a very small region. Anal Sci. 2011, 27(2): 163-170.
[31] Svatoš A. Single-cell metabolomics comes of age: new developments in mass spectrometry profiling and imaging. Anal. Chem. 2011, 83(13): 5037-5044.
[32] Wagner M. Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Ann. Rev. Microbiol. 2009, 63: 411-429.
[33] Kao L., Abuladze N., Shao X.M., Mc Keegan K., Kurtz I. A new technique for multiple re-use of planar patch clamp chips. Journ. Neurosci. Methods. 2012, 208(2): 205-210.
[34] Milligan C.J., Möller C. Automated planar patch-clamp. Meth. Mol. Biol. 2013, 998: 171-187.
[35] Xu B., Ye W., Zhang Y., Shi J., Chan C., Yao X., Yang M. A hydrophilic polymer based microfluidic system with planar patch clamp electrode array for electrophysiological measurement from cells. Biosens. Bioelectron. 2014, 53: 187-192.
[36] Nemes P., Barton A.A., Li Y., Vertes A. Ambient molecular imaging and depth profiling of live tissue by infrared laser ablation electrospray ionization mass spectrometry. Anal. Chem. 2008, 80(12): 4575-4582.
[37] Nemes P., Vertes A. Atmospheric-pressure molecular imaging of biological tissues and biofilms by LAESI mass spectrometry. Journ Vis Exp. 2010, 43: pii: 2097 [doi: 10.3791/2097].
[38] Liu J., Wang H., Cooks R.G., Ouyang Z. Leaf spray: direct chemical analysis of plant material and living plants by mass spectrometry. Anal Chem. 2011, 83(20): 7608- 7613.
[39] Shrestha B., Patt J.M., Vertes A. In situ cell-by-cell imaging and analysis of small cell populations by mass spectrometry. Anal Chem. 2011, 83(8): 2947-2955.
[40] Lorenzo T.M., Mizuno H., Tsuyama N., Harada T., Masujima T. In situ molecular analysis of plant tissues by live single-cell mass spectrometry. Anal Chem. 2012, 84(12): 5221-528.
[41] Mizuno H., Tsuyama N., Harada T., Masujima T. Live single-cell video-mass spectrometry for cellular and subcellular molecular detection and cell classification. Journ. Mass Spec. 2008, 43: 1692-1700.
[42] Lorenzo T.M., Mizuno H., Tsuyama N., Harada T., Masujima T. Direct single-cell molecular analysis of plant tissues by video mass spectrometry. Anal Sci. 2009, 25(9): 1053- 1055.
[43] Date S., Mizuno H., Tsuyama N., Harada T., Masujima T. Direct drug metabolism monitoring in a live single hepatic cell by video mass spectrometry. Anal. Sci. 2012, 28(3): 201-203.
[44] Augustine G.J. Combining patch-clamp and optical methods in brain slices. Journ. Neurosci. Meth. 1994, 54(2): 163-169.
[45] Park M.K., Tepikin A.V., Petersen O.H. What can we learn about cell signalling by combining optical imaging and patch clamp techniques? Pflugers Arch: Eur Journ Physiol. 2002, 444(3): 305-316.
[46] Demuro A., Parker I. "Optical patch-clamping": single- channel recording by imaging Ca2+ flux through individual muscle acetylcholine receptor channels. Journ. Gen. Phys. 2005, 126(3): 179-192.
[47] Ishikawa D., Takahashi N., Sasaki T., Usami A., Matsuki N., Ikegaya Y. Fluorescent pipettes for optically targeted patch-clamp recordings. Neur. Net. 2010, 23(6): 669-672.
[48] Qian F., Ermilov S., Murdock D., Brownell W. E., Anvari B. Combining optical tweezers and patch clamp for studies of cell membrane electromechanics. Rev. Sci. Instr. 2004, 75(9): 2937-2942.
[49] Sokabe M., Nunogaki K., Naruse K., Soga H. Mechanics of patch clamped and intact cell-membranes in relation to SA channel activation. Journ. Physiol. 1993, 43(1): S197- S204.
[50] Suchyna T.M., Sachs F. Mechanosensitive channel properties and membrane mechanics in mouse dystrophic myotubes. Journ. Physiol., 2007, 581(1): 369-387.
[51] Belyy V., Kamaraju K., Akitake B., Anishkin A., Sukharev S. Adaptive behavior of bacterial mechanosensitiv channels is coupled to membrane mechanics. Journ. Gen. Physiol. 2010, 135(6): 641-652.
[52] Akashi S., Naito Y., Takio K. Observation of hydrogen- deuterium exchange of ubiquitin by direct analysis of electrospray capillary-skimmer dissociation with Fourier transform ion cyclotron resonance mass spectrometry. Anal. Chem. 1999, 71(21): 4974-4980.
[53] McDonald L.A., Barbieri L.R., Carter G.T., Kruppa G., Feng X., Lotvin J.A., Siegel M.M.. FTMS structure elucidation of natural products: application to muraymycin antibiotics using ESI multi-CHEF SORI-CID FTMS(n), the top-down / bottom-up approach, and HPLC ESI capillary- skimmer CID FTMS. Anal Chem. 2003, 75(11): 2730-2739.
[54] Li J., Wang Z., Altman E. In-source fragmentation and analysis of polysaccharides by capillary electrophoresis / mass spectrometry. Rap. Com. Mass Spec. 2005, 19(10): 1305-1314.
[55] Jedrzejewski P.T., Lehmann W.D. Detection of modified peptides in enzymatic digests by capillary liquid chromatography/electrospray mass spectrometry and a programmable skimmer CID acquisition routine. Anal. Chem. 1997, 69(3): 294-301.
[56] Tsugoshi T., Furukawa M., Ohashi M., Iida Y. Comparison of Capillary and Skimmer Interfaces in Evolved Gas Analysis-Mass Spectrometry (EGA-MS) with Regard to Impurities in Ceramic Raw Materials. Journ. Therm. Anal. Calorim. 2001, 64(3): 1127-1132.
[57] Edbey K., Moran G., Willett G. The effect of capillary - skimmer potential difference and the ion trap time in the hexapole on the attachment of the metal-ions to the surfactants: an electrospray ionisation mass spectrometry study. Ras Journ Chem. 2009, 2(4): 769-775.
[58] Denisov E.V., Shustryakov V., Nikolaev E.N., Winkler F.J, Medina R. FT ICR investigations of chiral supramolecular propellers of dialkyltartrate trimers with methylammonium ions. Int. Journ. Mass. Spec. & Ion Proc. 1997, 167-168: 259-268.
[59] Nikolaev E.N., Goginashvili G.T., Tal’ Rose V.L., Kostyanovsky R.G. Investigation of asymmetric gas-phase ion/molecule reactions by FT-ICR spectrometry. Int. Journ. Mass Spec. & Ion Proc. 1988, 86: 249-252.
[60] Belov M.E., Rakov V.S., Nikolaev E.N., Goshe M.B., Anderson G.A., Smith R.D.. Initial implementation of external accumulation liquid chromatography / electrospray ionization Fourier transform ion cyclotron resonance with automated gain control. Rap. Com. Mass Spec. 2003, 17(7): 627-636.
[61] Tsvetkov P.O., Makarov A.A., Kozin S.A., Popov I.A., Nikolaev E.N., Archakov A.I. Isomerization of the ASP7 residue results in zinc-induced oligomerization of Alzheimer's disease amyloid β (1-16) peptide. Chembiochem: Eur. Journ. Chem. Biol. 2008, 9(10): 1564- 1567.
[62] Makarov A., Denisov E., Kholomeev A., Balschun W., Lange O., Strupat K., Horning S. Performance evaluation of a hybrid linear ion trap/orbitrap mass spectrometer. Anal. Chem., 2006, 78(7): 2113–2120.
[63] Makarov A., Denisov E., Lange O., Horning S. Dynamic range of mass accuracy in LTQ Orbitrap hybrid mass spectrometer. J. Am. Soc. Mass Spectrom , 2006, 17(7): 977–982.
[64] Belov M.E., Gorshkov M.V., Udseth H.R., Anderson G.A., Smith R.D. Zeptomole-sensitivity electrospray ionization-Fourier transform ion cyclotron resonance mass spectrometry of proteins. Anal. Chem., 2000, 72(10): 2271-2279.
[65] Salehpour M., Forsgard N., Possnert G. FemtoMolar measurements using accelerator mass spectrometry // Rapid Com. Mass Spectrom., 2009, 23(5): 557-563.
[66] DeGregorio M.W., Dingley K.H., Wurz G.T., Ubick E., Turteltaub K.W. Accelerator mass spectrometry allows for cellular quantification of doxorubicin at femtomolar concentrations // Can. Chem. Pharm., 2006, 57(3), 335-342.
[67] Dingley K.H., Roberts M.L., Velsko C.A., Turteltaub K.W. Attomole detection of 3H in biological samples using accelerator mass spectrometry: application in low-dose, dual-isotope tracer studies in conjunction with 14C accelerator mass spectrometry // Chem. Res. Tox., 1998, 11(10): 1217-1222.
[68] Vogel J.S., Grant P.G., Buchholz B.A., Dingley K., Turteltaub K.W. Attomole quantitation of protein separations with accelerator mass spectrometry // Electrophoresis, 2001, 22(10), 2037-2045.
[69] Salehpour M., Possnert G., Bryhni H. Subattomole sensitivity in biological accelerator mass spectrometry // Anal. Chem., 80(10), 2008, 3515-3521.
[70] Salehpour M. FemtoMolar and zeptomole sensitivity in Biological Accelerator Mass Spectrometry // BIO-Ångström 2008 [http://www.uppsalabio.com/graphics/18746.pdf], pp. 19, 45.
[71] Salehpour M. Zeptomole Sensitivity in Biological Accelerator Mass Spectrometry // In: Proc. of “Mass Spectrometry of Small Molecular Drugs”, April 8-9, Uppsala [http://www.apotekarsocieteten.se/upload/lma].
[72] Barker J., Garner R.C. Biomedical applications of accelerator mass spectrometry-isotope measurements at the level of the atom // Rap. Comm. Mass Spectrom., 13(4), 1999, 285-293.
[73] Schiermeier Q. Ukranian science: DIY, Kiev style. Nature. 2002, 416: 675-676.
[74] Mery P.F., Lechêne P., Fischmeister R. A loudspeaker-driven system for rapid and multiple solution exchanges in patch-clamp experiments. Pflügers Archiv. 1992, 420: 529-535.
[75] Lau A.Y., Hung P.J., Wu A.R., Lee L.P. Open-access microfluidic patch-clamp array with raised lateral cell trapping sites. Lab on a Chip. 2006, 6(12): 1510-1515.
[76] Tu T.Y., Chen C.Y., Jong D.S., Wo A.M. A lab-use microfluidic planar patch-clamp system. Proc. of 14th Int. Conf. on Miniatur. Syst. for Chem. & Life. Sci., Groningen, Netherlands, Oct. 3-7, 2010 [ISBN: 978-0-9798064-3-8]: 929-931.
Author Information
  • Talrose Institute for Energy Problems of Chemical Physics, Russian Academy of Sciences, Moscow, Russia

  • Semenov Institute of Chemical Physics, Russian Academy of Sciences, Moscow, Russia

Cite This Article
  • APA Style

    Oleg Gradov, Margaret Gradova. (2015). "MS-Patch-Clamp" or the Possibility of Mass Spectrometry Hybridization with Patch-Clamp Setups for Single Cell Metabolomics and Channelomics. Advances in Biochemistry, 3(6), 66-71. https://doi.org/10.11648/j.ab.20150306.11

    Copy | Download

    ACS Style

    Oleg Gradov; Margaret Gradova. "MS-Patch-Clamp" or the Possibility of Mass Spectrometry Hybridization with Patch-Clamp Setups for Single Cell Metabolomics and Channelomics. Adv. Biochem. 2015, 3(6), 66-71. doi: 10.11648/j.ab.20150306.11

    Copy | Download

    AMA Style

    Oleg Gradov, Margaret Gradova. "MS-Patch-Clamp" or the Possibility of Mass Spectrometry Hybridization with Patch-Clamp Setups for Single Cell Metabolomics and Channelomics. Adv Biochem. 2015;3(6):66-71. doi: 10.11648/j.ab.20150306.11

    Copy | Download

  • @article{10.11648/j.ab.20150306.11,
      author = {Oleg Gradov and Margaret Gradova},
      title = {"MS-Patch-Clamp" or the Possibility of Mass Spectrometry Hybridization with Patch-Clamp Setups for Single Cell Metabolomics and Channelomics},
      journal = {Advances in Biochemistry},
      volume = {3},
      number = {6},
      pages = {66-71},
      doi = {10.11648/j.ab.20150306.11},
      url = {https://doi.org/10.11648/j.ab.20150306.11},
      eprint = {https://download.sciencepg.com/pdf/10.11648.j.ab.20150306.11},
      abstract = {In this projecting work we propose a mass spectrometric patch-clamp equipment with the capillary performing both a local potential registration at the cell membrane and the analyte suction simultaneously. This paper provides a current literature analysis comparing the possibilities of the novel approach proposed with the known methods, such as scanning patch-clamp, scanning ion conductance microscopy, patch clamp based on scanning probe microscopy technology, quantitative subcellular secondary ion mass spectrometry or "ion microscopy", live single-cell mass spectrometry, in situ cell-by-cell imaging, single-cell video-mass spectrometry, etc. We also consider the ways to improve the informativeness of these methods and particularly emphasize the trend at the increasing of the analysis complexity. We propose here the way to improve the efficiency of the cell trapping to the capillary during MS-path-clamp, as well as to provide laser surface ionization using laser trapping and tweezing of cells with the laser beam transmitted through the capillary as a waveguide. It is also possible to combine the above system with the microcolumn separation system or capillary electrophoresis as an optional direction of further development of the complex of analytical techniques emerging from the MS variation of patch-clamp.},
     year = {2015}
    }
    

    Copy | Download

  • TY  - JOUR
    T1  - "MS-Patch-Clamp" or the Possibility of Mass Spectrometry Hybridization with Patch-Clamp Setups for Single Cell Metabolomics and Channelomics
    AU  - Oleg Gradov
    AU  - Margaret Gradova
    Y1  - 2015/10/30
    PY  - 2015
    N1  - https://doi.org/10.11648/j.ab.20150306.11
    DO  - 10.11648/j.ab.20150306.11
    T2  - Advances in Biochemistry
    JF  - Advances in Biochemistry
    JO  - Advances in Biochemistry
    SP  - 66
    EP  - 71
    PB  - Science Publishing Group
    SN  - 2329-0862
    UR  - https://doi.org/10.11648/j.ab.20150306.11
    AB  - In this projecting work we propose a mass spectrometric patch-clamp equipment with the capillary performing both a local potential registration at the cell membrane and the analyte suction simultaneously. This paper provides a current literature analysis comparing the possibilities of the novel approach proposed with the known methods, such as scanning patch-clamp, scanning ion conductance microscopy, patch clamp based on scanning probe microscopy technology, quantitative subcellular secondary ion mass spectrometry or "ion microscopy", live single-cell mass spectrometry, in situ cell-by-cell imaging, single-cell video-mass spectrometry, etc. We also consider the ways to improve the informativeness of these methods and particularly emphasize the trend at the increasing of the analysis complexity. We propose here the way to improve the efficiency of the cell trapping to the capillary during MS-path-clamp, as well as to provide laser surface ionization using laser trapping and tweezing of cells with the laser beam transmitted through the capillary as a waveguide. It is also possible to combine the above system with the microcolumn separation system or capillary electrophoresis as an optional direction of further development of the complex of analytical techniques emerging from the MS variation of patch-clamp.
    VL  - 3
    IS  - 6
    ER  - 

    Copy | Download

  • Sections