1932

Abstract

The reduction in ion current as a fine pipette approaches a cell surface allows the cell surface topography to be imaged, with nanoscale resolution, without contact with the delicate cell surface. A variety of different methods have been developed and refined to scan the topography of the dynamic cell surface at high resolution and speed. Measurement of cell topography can be complemented by performing local probing or mapping of the cell surface using the same pipette. This can be done by performing single-channel recording, applying force, delivering agonists, using pipettes fabricated to contain an electrochemical probe, or combining with fluorescence imaging. These methods in combination have great potential to image and map the surface of live cells at the nanoscale.

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/content/journals/10.1146/annurev-anchem-091420-120101
2021-07-27
2024-04-15
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Literature Cited

  1. 1. 
    Hansma PK, Drake B, Marti O, Gould SA, Prater CB. 1989. The scanning ion-conductance microscope. Science 243:641–43
    [Google Scholar]
  2. 2. 
    Korchev YE, Bashford CL, Milovanovic M, Vodyanoy I, Lab MJ. 1997. Scanning ion conductance microscopy of living cells. Biophys. J. 73:653–58
    [Google Scholar]
  3. 3. 
    Novak P, Shevchuk A, Ruenraroengsak P, Miragoli M, Thorley AJ et al. 2014. Imaging single nanoparticle interactions with human lung cells using fast ion conductance microscopy. Nano Lett 14:1202–7
    [Google Scholar]
  4. 4. 
    Novak P, Li C, Shevchuk AI, Stepanyan R, Caldwell M et al. 2009. Nanoscale live-cell imaging using hopping probe ion conductance microscopy. Nat. Methods 6:279–81
    [Google Scholar]
  5. 5. 
    Happel P, Dietzel ID. 2009. Backstep scanning ion conductance microscopy as a tool for long term investigation of single living cells. J. Nanobiotechnol. 7:7
    [Google Scholar]
  6. 6. 
    McKelvey K, Perry D, Byers JC, Colburn AW, Unwin PR. 2014. Bias modulated scanning ion conductance microscopy. Anal. Chem. 86:3639–46
    [Google Scholar]
  7. 7. 
    Zhou Y, Saito M, Miyamoto T, Novak P, Shevchuk AI et al. 2018. Nanoscale imaging of primary cilia with scanning ion conductance microscopy. Anal. Chem. 90:2891–95
    [Google Scholar]
  8. 8. 
    Chen Y, Sukhorukov GB, Novak P. 2018. Visualising nanoscale restructuring of a cellular membrane triggered by polyelectrolyte microcapsules. Nanoscale 10:16902–10
    [Google Scholar]
  9. 9. 
    Nashimoto Y, Takahashi Y, Ida H, Matsumae Y, Ino K et al. 2015. Nanoscale imaging of an unlabeled secretory protein in living cells using scanning ion conductance microscopy. Anal. Chem. 87:2542–45
    [Google Scholar]
  10. 10. 
    Kim J, Kim S-O, Cho N-J. 2015. Alternative configuration scheme for signal amplification with scanning ion conductance microscopy. Rev. Sci. Instrum. 86:023706
    [Google Scholar]
  11. 11. 
    Jung G-E, Noh H, Shin YK, Kahng S-J, Baik KY et al. 2015. Closed-loop ARS mode for scanning ion conductance microscopy with improved speed and stability for live cell imaging applications. Nanoscale 7:10989–97
    [Google Scholar]
  12. 12. 
    Wang Z, Zhuang J, Gao Z, Liao X. 2018. A fast scanning ion conductance microscopy imaging method using compressive sensing and low-discrepancy sequences. Rev. Sci. Instrum. 89:113709
    [Google Scholar]
  13. 13. 
    Zhuang J, Jiao Y, Li Z, Lang J, Li F 2018. A continuous control mode with improved imaging rate for scanning ion conductance microscope (SICM). Ultramicroscopy 190:66–76
    [Google Scholar]
  14. 14. 
    Zhuang J, Jiao Y, Mugabo V. 2017. A new scanning mode to improve scanning ion conductance microscopy imaging rate with pipette predicted movement. Micron 101:177–85
    [Google Scholar]
  15. 15. 
    Zhuang J, Wang Z, Li Z, Liang P, Vincent M. 2018. Smart scanning ion-conductance microscopy imaging technique using horizontal fast scanning method. Microsc. Microanal. 24:264–76
    [Google Scholar]
  16. 16. 
    Zhuang J, Wang Z, Liao X, Gao B, Cheng L. 2019. Hierarchical spiral-scan trajectory for efficient scanning ion conductance microscopy. Micron 123:102683
    [Google Scholar]
  17. 17. 
    Li G, Fang X 2018. A fast imaging method of scanning ion conductance microscopy. Micron 114:8–13
    [Google Scholar]
  18. 18. 
    Zhu C, Shi W, Daleke DL, Baker LA. 2018. Monitoring dynamic spiculation in red blood cells with scanning ion conductance microscopy. Analyst 143:1087–93
    [Google Scholar]
  19. 19. 
    Nakajima M, Mizutani Y, Iwata F, Ushiki T. 2018. Scanning ion conductance microscopy for visualizing the three-dimensional surface topography of cells and tissues. Semin. Cell Dev. Biol. 73:125–31
    [Google Scholar]
  20. 20. 
    Momotenko D, Byers JC, McKelvey K, Kang M, Unwin PR. 2015. High-speed electrochemical imaging. ACS Nano 9:8942–52
    [Google Scholar]
  21. 21. 
    Novak P, Li C, Shevchuk AI, Stepanyan R, Caldwell M et al. 2009. Nanoscale live-cell imaging using hopping probe ion conductance microscopy. Nat. Methods 6:279–81
    [Google Scholar]
  22. 22. 
    Seifert J, Rheinlaender J, Lang F, Gawaz M, Schäffer TE. 2017. Thrombin-induced cytoskeleton dynamics in spread human platelets observed with fast scanning ion conductance microscopy. Sci. Rep. 7:4810
    [Google Scholar]
  23. 23. 
    Shevchuk AI, Novak P, Taylor M, Diakonov IA, Ziyadeh-Isleem A et al. 2012. An alternative mechanism of clathrin-coated pit closure revealed by ion conductance microscopy. J. Cell Biol. 197:499–508
    [Google Scholar]
  24. 24. 
    Watanabe S, Ando T. 2017. High-speed XYZ-nanopositioner for scanning ion conductance microscopy. Appl. Phys. Lett. 111:113106
    [Google Scholar]
  25. 25. 
    Simeonov S, Schäffer TE. 2019. High-speed scanning ion conductance microscopy for sub-second topography imaging of live cells. Nanoscale 11:8579–87
    [Google Scholar]
  26. 26. 
    Bednarska J, Pelchen-Matthews A, Novak P, Burden JJ, Summers PA et al. 2020. Rapid formation of human immunodeficiency virus-like particles. PNAS 117:21637–46
    [Google Scholar]
  27. 27. 
    Simeonov S, Schäffer TE. 2019. Ultrafast imaging of cardiomyocyte contractions by combining scanning ion conductance microscopy with a microelectrode array. Anal. Chem. 91:9648–55
    [Google Scholar]
  28. 28. 
    Bednarska J, Novak P, Korchev Y, Rorsman P, Tarasov AI, Shevchuk A. 2021. Release of insulin granules by simultaneous, high-speed correlative SICM-FCM. J. Microsc 282:2129
    [Google Scholar]
  29. 29. 
    Shevchuk AI, Novak P, Velazquez MA, Fleming TP, Korchev YE. 2013. Combined ion conductance and fluorescence confocal microscopy for biological cell membrane transport studies. J. Opt. 15:094005
    [Google Scholar]
  30. 30. 
    Ali T, Bednarska J, Vassilopoulos S, Tran M, Diakonov IA et al. 2019. Correlative SICM-FCM reveals changes in morphology and kinetics of endocytic pits induced by disease-associated mutations in dynamin. FASEB J. 33:8504–18
    [Google Scholar]
  31. 31. 
    Nikolaev VO, Moshkov A, Lyon AR, Miragoli M, Novak P et al. 2010. 2-Adrenergic receptor redistribution in heart failure changes cAMP compartmentation. Science 327:1653–57
    [Google Scholar]
  32. 32. 
    Subramanian H, Froese A, Jönsson P, Schmidt H, Gorelik J, Nikolaev VO. 2018. Distinct submembrane localisation compartmentalises cardiac NPR1 and NPR2 signalling to cGMP. Nat. Commun. 9:2446
    [Google Scholar]
  33. 33. 
    Bastug-Özel Z, Wright PT, Kraft AE, Pavlovic D, Howie J et al. 2018. Heart failure leads to altered β2-adrenoceptor/cyclic adenosine monophosphate dynamics in the sarcolemmal phospholemman/Na,K ATPase microdomain. Cardiovasc. Res. 115:546–55
    [Google Scholar]
  34. 34. 
    Shevchuk A, Tokar S, Gopal S, Sanchez-Alonso JL, Tarasov AI et al. 2016. Angular approach scanning ion conductance microscopy. Biophys. J. 110:2252–65
    [Google Scholar]
  35. 35. 
    Leo-Macias A, Agullo-Pascual E, Sanchez-Alonso JL, Keegan S, Lin X et al. 2016. Nanoscale visualization of functional adhesion/excitability nodes at the intercalated disc. Nat. Commun. 7:10342
    [Google Scholar]
  36. 36. 
    Hennig S, van de Linde S, Bergmann S, Huser T, Sauer M. 2015. Quantitative super-resolution microscopy of nanopipette-deposited fluorescent patterns. ACS Nano 9:8122–30
    [Google Scholar]
  37. 37. 
    Hagemann P, Gesper A, Happel P. 2018. Correlative stimulated emission depletion and scanning ion conductance microscopy. ACS Nano 12:5807–15
    [Google Scholar]
  38. 38. 
    Clarke RW, Novak P, Zhukov A, Tyler EJ, Cano-Jaimez M et al. 2016. Low stress ion conductance microscopy of sub-cellular stiffness. Soft Matter 12:7953–58
    [Google Scholar]
  39. 39. 
    Clarke RW, Zhukov A, Richards O, Johnson N, Ostanin V, Klenerman D. 2013. Pipette-surface interaction: current enhancement and intrinsic force. J. Am. Chem. Soc. 135:322–29
    [Google Scholar]
  40. 40. 
    Bulbul G, Chaves G, Olivier J, Ozel RE, Pourmand N. 2018. Nanopipettes as monitoring probes for the single living cell: state of the art and future directions in molecular biology. Cells 7:55
    [Google Scholar]
  41. 41. 
    Bruckbauer A, Zhou D, Ying L, Korchev YE, Abell C, Klenerman D. 2003. Multicomponent submicron features of biomolecules created by voltage controlled deposition from a nanopipet. J. Am. Chem. Soc. 125:9834–39
    [Google Scholar]
  42. 42. 
    Seger RA, Actis P, Penfold C, Maalouf M, Vilozny B, Pourmand N. 2012. Voltage controlled nano-injection system for single-cell surgery. Nanoscale 4:5843–46
    [Google Scholar]
  43. 43. 
    Actis P, Maalouf MM, Kim HJ, Lohith A, Vilozny B et al. 2014. Compartmental genomics in living cells revealed by single-cell nanobiopsy. ACS Nano 8:546–53
    [Google Scholar]
  44. 44. 
    Actis P, Tokar S, Clausmeyer J, Babakinejad B, Mikhaleva S et al. 2014. Electrochemical nanoprobes for single-cell analysis. ACS Nano 8:875–84
    [Google Scholar]
  45. 45. 
    Rodolfa KT, Bruckbauer A, Zhou D, Korchev YE, Klenerman D. 2005. Two-component graded deposition of biomolecules with a double-barreled nanopipette. Angew. Chem. Int. Ed. 117:7014–19
    [Google Scholar]
  46. 46. 
    Babakinejad B, Jönsson P, López Córdoba A, Actis P, Novak P et al. 2013. Local delivery of molecules from a nanopipette for quantitative receptor mapping on live cells. Anal. Chem. 85:9333–42
    [Google Scholar]
  47. 47. 
    Kang M, Momotenko D, Page A, Perry D, Unwin PR. 2016. Frontiers in nanoscale electrochemical imaging: faster, multifunctional, and ultrasensitive. Langmuir 32:7993–8008
    [Google Scholar]
  48. 48. 
    Page A, Perry D, Unwin PR. 2017. Multifunctional scanning ion conductance microscopy. Proc. R. Soc. A 473:20160889
    [Google Scholar]
  49. 49. 
    Zhang Y, Takahashi Y, Hong SP, Liu F, Bednarska J et al. 2019. High-resolution label-free 3D mapping of extracellular pH of single living cells. Nat. Commun. 10:5610
    [Google Scholar]
  50. 50. 
    Novak P, Gorelik J, Vivekananda U, Shevchuk AI, Ermolyuk YS et al. 2013. Nanoscale-targeted patch-clamp recordings of functional presynaptic ion channels. Neuron 79:1067–77
    [Google Scholar]
  51. 51. 
    Shevchuk A, Tokar S, Gopal S, Sanchez-Alonso JL, Tarasov AI et al. 2016. Angular approach scanning ion conductance microscopy. Biophys. J. 110:2252–65
    [Google Scholar]
  52. 52. 
    Leo-Macias A, Agullo-Pascual E, Sanchez-Alonso JL, Keegan S, Lin X et al. 2016. Nanoscale visualization of functional adhesion/excitability nodes at the intercalated disc. Nat. Commun. 7:10342
    [Google Scholar]
  53. 53. 
    Torres-Perez JV, Naeem H, Thompson CL, Knight MM, Novak P. 2020. Nanoscale mapping reveals functional differences in ion channels populating the membrane of primary cilia. Cell Physiol. Biochem. 54:15–26
    [Google Scholar]
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