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Histochemistry and Cell Biology

, Volume 150, Issue 5, pp 521–527 | Cite as

Visualization of internal in situ cell structure by atomic force microscopy

  • María L. Segura-Valdez
  • Lourdes T. Agredano-Moreno
  • Alma L. Zamora-Cura
  • Reyna Lara-Martínez
  • Luis F. Jiménez-García
Review

Abstract

Light and electron microscopy have been used to study cell structure for many years, but atomic force microscopy is a more recent technique used to analyze cells, mainly due to the absence of techniques to prepare the samples. Isolated molecules or organelles, whole cells, and to a lesser extent in situ cell structure have been observed by different atomic force microscopy imaging modes. Here, we review efforts intended to analyze in situ the cell structures using approaches involving imaging of the surface of semithin sections of samples embedded in resin and sections prepared with an ultramicrotome. The results of such studies are discussed in relation to their implications to analyze the fine structure of organelles at the nanoscale in situ at enhanced resolution compared to light microscopy.

Keywords

Atomic force microscopy Cell Nucleus Nucleolus RNA Ultramicrotome 

Notes

Acknowledgements

Support of PAPIIT-DGAPA-UNAM IN217917 and PAPIME PE213916 is acknowledged.

References

  1. Ando T (2014) High speed AFM imaging. Curr Op Struct Biol 28:63–68CrossRefGoogle Scholar
  2. Binnig G, Quate CF, Gerber Ch (1986) Atomic force microscope. Phys Rev Lett 56:930–933CrossRefGoogle Scholar
  3. Braga PC, Ricci D (eds) (2004) Atomic force microscopy. Biomedical methods and applications. Meth Mol Biol 242:1–394. Humana PressGoogle Scholar
  4. Butt HJ, Wolff EK, Gould SAC, Dixon Northern B, Peterson CM, Hansma PK (1990) Imaging cells with the atomic force microscope. J Struct Biol 105:54–61CrossRefGoogle Scholar
  5. Chen Y, Cai J, Zhao T, Wang C, Dong S, Luo S, Chen ZW (2005) Atomic force microscopy imaging and 3-D reconstructions of serial thin sections of a single cell and its interior structures. Ultramicroscopy 103:173–182CrossRefGoogle Scholar
  6. Dufrêne YF, Ando T, Garcia R, Alsteens D, Martinez-Martin D, Engel A, Gerber CH, Muller DJ (2017) Imaging modes of atomic force microscopy for application in molecular and cell biology. Nat Nanotech 12:295–307CrossRefGoogle Scholar
  7. Efimov AE, Tonevitsky AG, Dittrich M, Matsko NB (2007) Atomic force microscope (AFM) combined with the ultramicrotome: a novel devise for the serial section tomography and AFM/TEM complementary structural analysis of biological and polymer samples. J Microsc 226:207–217CrossRefGoogle Scholar
  8. Efimov AE, Agapov II, Agapova OI, Oleinikov VA, Mezin AV, Molinari M, Nabiev I, Mochalov KE (2017) A novel design of a scanning probe microscope integrated with an ultramicrotome for serial block-face nanotomography. J Microsc 226:207–217CrossRefGoogle Scholar
  9. Fragoso-Soriano RJ, Vázquez-López C, Pérez-García B, Jiménez-García LF (2009) Atomic force microscopy imaging of thin sections of Lacandonia granules. J Scann Probe Microsc 4:1–5CrossRefGoogle Scholar
  10. Fragoso-Soriano RJ, Jiménez-García LF, Vázquez-López C (2011) AFM study of cellular structure organelles of Lacandonia schismatica and visualization of images using the error signal. J Adv Microsc Res 6:1–6CrossRefGoogle Scholar
  11. Gavara N (2017) A beginners’s guide to atomic force microscopy probing for cell mechanics. Microsc Res Tech 80:75–84CrossRefGoogle Scholar
  12. Graham HK, Hodson NW, Hoyland JA, Millward-Sadler SJ, Garrod D, Scothern A, Griffiths CE, Watson RE, Cox TR, Erler JT, Trafford AW, Sherratt MJ (2010) Tissue section AFM: in situ ultrastructural imaging of native biomolecules. Matrix Biol 29:254–260CrossRefGoogle Scholar
  13. Hinterdorfer P (2002) Molecular recognition studies using the atomic force microscope. In: Jena BP, Hörber JKH (eds) Atomic force microscopy in cell biology. Meth Cell Biol, Academic Press, San DiegoGoogle Scholar
  14. Jena BP, Cho SJ (2002) The atomic force microscope in the study of membrane fusion and exocytosis. In: Jena BP, Hörber JKH (eds) Atomic force microscopy in cell biology. Meth Cell Biol Academic Press, San DiegoGoogle Scholar
  15. Jiménez-García LF, Fragoso-Soriano R (2000) Atomic force microscopy of the cell nucleus. J Struct Biol 129:218–222CrossRefGoogle Scholar
  16. Jiménez-García LF, Segura-Valdez ML (2004) Visualizing nuclear structure in situ by atomic force microscopy. In: Braga PC, Ricci D (eds) Atomic force microscopy: methods and protocols in biomedical applications. Methods in molecular medicine. Humana Press, New Jersey, pp 191–199Google Scholar
  17. Jiménez-Ramírez J, Agredano-Moreno LT, Segura-Valdez ML, Jiménez-García LF (2002) Lacandonia granules are present in Ginkgo biloba cell nuclei. Biol Cell 94:511–518CrossRefGoogle Scholar
  18. Lee G, Jeong JH, Lee S, Choi S, Pak YK, Kim W, Park HK (2013) Quantitative and qualitative analysis of heart mitochondria for evaluating the degree of myocardial injury utilizing atomic force microscopy. Micron 44:167–173CrossRefGoogle Scholar
  19. Mariani T, Musio A, Frediani C, Sbrana I, Ascoli C (1994) An atomic force microscope for cytological and histological investigations. J Microsc 176:121–131CrossRefGoogle Scholar
  20. Matsko N, Mueller M (2004) AFM of biological material embedded in epoxy resin. J Struct Biol 146:334–343CrossRefGoogle Scholar
  21. Morris VJ, Kirby AR, Gunning AP (eds) (1999) Atomic force microscopy for biologists. Imperial College Press, pp 1–332Google Scholar
  22. Müller DJ, Schoenenberger CA, Büldt G, Engel A (1996) Immunoatomic force microscopy in purple membrane. Biophys J 70:1796–1802CrossRefGoogle Scholar
  23. Ohnesorge FM, Hörber JKH, Häberle W, Czerny CP, Smith DPE, Binnig G (1997) AFM review study on pox viruses and living cells. Biophys J 73:2183–2194CrossRefGoogle Scholar
  24. Roth J (1986) Post-embedding cytochemistry with gold-labeled reagents. A review. J Microsc 143:125–137CrossRefGoogle Scholar
  25. Roth J (1989) Postembedding labeling on Lowicryl K4M tissue sections: Detection and modification of cellular components. In: Tartakoff AM (ed) Vesicular transport, part B Meth. Cell Biol (part A), vol 31 Academic Press, San Diego, pp 513–551Google Scholar
  26. Schneider SW, Shritaran KC, Geibel JP, Oberleithner H (1997) Surface dynamics in living acinar cells imaged by atomic force microscopy: identification of plasma membrane structures involved in exocytosis. Proc Natl Acad Sci USA 94:316–321CrossRefGoogle Scholar
  27. Segura-Valdez ML, Zamora-Cura A, Gutiérrez-Quintanar N, Villalobos-Nájera E, Rodríguez-Vázquez JB, Galván-Arrieta TC, Jiménez-Rodríguez D, Agredano-Moreno LT, Lara-Martínez R, Jiménez-García LF (2010) Visualization of cell structure in situ by atomic force microscopy. In: Méndez-Vilas A, Díaz J (eds) Microscopy: science, technology, applications and education (Microscopy Book Series), Formatex, Badajoz, SpainGoogle Scholar
  28. Shan Y, Wang H (2015) The structure and function of cell membranes examined by atomic force microscopy and single-molecule force spectroscopy. Chem Soc Rev 44:3617–3638CrossRefGoogle Scholar
  29. Shao Z, Zhang Y (1996) Biological cryo atomic force microscopy: a brief review. Ultramicroscopy 66:141–152CrossRefGoogle Scholar
  30. Ushiki T, Hitomi J, Ogura S, Umemoto T, Shigeno M (1996) Atomic force microscopy in histology and cytology. Arch Histol Cytol 59:421–431CrossRefGoogle Scholar
  31. Usukura E, Narita A, Yagi A, Ito S, Usukura J (2016) An Unroofing method to observe the cytoskeleton directly at molecular resolution using Atomic force microscopy. Sci Rep 6:27472CrossRefGoogle Scholar
  32. Usukura E, Narita A, Yagi A, Sakai N, Uekusa Y, Imaoka Y, Ito S, Usukura J (2017) A cryosectioning technique for the observation of intracellular structures and immunocytochemistry of tissues in atomic force microscopy (AFM). Sci Rep 7:6462CrossRefGoogle Scholar
  33. Xu H, Su W, Cai M, Jiang J, Zeng X, Wang H (2013) The asymmetrical structure of Golgi apparatus membranes revealed by in situ atomic force microscope. PLoS One 8:e61596CrossRefGoogle Scholar
  34. Zamora-Cura A, Jiménez-García LF (2014) Visualization of interchromatin granules by atomic force microscopy. J Adv Micros Res 9:296–300CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Cell Biology, Faculty of SciencesNational Autonomous University of Mexico (UNAM)Mexico CityMexico

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