Journal Home > Volume 1 , Issue 1

Nanobiotechnology such as atomic force microscopy (AFM) has a great application in various regimes of cell biology, offering an excellent avenue to study cellular nanotopography, nanomechanics, and nanointeraction. AFM nanotopography can provide a high resolution of nano-architectures of different cells. AFM nanomechanics have shed new light on characterizing mechanical properties of cellular structures and biological materials as well as monitoring the physiopathological processes. AFM nanointeraction measurement helps the understanding of the molecular interaction forces at a nanoscale.


menu
Abstract
Full text
Outline
About this article

Atomic force microscopy: A nanobiotechnology for cellular research

Show Author's information Guangzhao Guan1( )Yan He2Li Mei3( )
Department of Oral Sciences, Faculty of Dentistry, University of Otago, 310 Great King Street, Dunedin 9016, New Zealand
Department of Oral Maxillofacial Surgery, Massachusetts General Hospital and Harvard School of Dental Medicine, Boston, MA 02114, USA
Department of Oral Diagnostic and Surgical Sciences, Faculty of Dentistry, University of Otago, Dunedin 9016, New Zealand

Abstract

Nanobiotechnology such as atomic force microscopy (AFM) has a great application in various regimes of cell biology, offering an excellent avenue to study cellular nanotopography, nanomechanics, and nanointeraction. AFM nanotopography can provide a high resolution of nano-architectures of different cells. AFM nanomechanics have shed new light on characterizing mechanical properties of cellular structures and biological materials as well as monitoring the physiopathological processes. AFM nanointeraction measurement helps the understanding of the molecular interaction forces at a nanoscale.

Keywords: atomic force microscopy (AFM), nanomechanics, nanotopography, nanointeraction

References(82)

1

Kim, D. H.; Provenzano, P. P.; Smith, C. L.; Levchenko, A. Matrix nanotopography as a regulator of cell function. J. Cell Biol. 2012, 197, 351–360.

2

Unal, M.; Alapan, Y.; Jia, H.; Varga, A. G.; Angelino, K.; Aslan, M.; Sayin, I.; Han, C. J.; Jiang, Y. X.; Zhang, Z. H. et al. Micro and nano- scale technologies for cell mechanics. Nanobiomedicine 2014, 1, 5.

3

Müller, D. J.; Krieg, M.; Alsteens, D.; Dufrêne, Y. F. New frontiers in atomic force microscopy: Analyzing interactions from single-molecules to cells. Curr. Opin. Biotechnol. 2009, 20, 4–13.

4

Darling, E. M.; Di Carlo, D. High-throughput assessment of cellular mechanical properties. Annu. Rev. Biomed. Eng. 2015, 17, 35–62.

5

Kasza, K. E.; Rowat, A. C.; Liu, J. Y.; Angelini, T. E.; Brangwynne, C. P.; Koenderink, G. H.; Weitz, D. A. The cell as a material. Curr. Opin. Cell Biol. 2007, 19, 101–107.

6

Binnig, G.; Quate, C. F.; Gerber, C. Atomic force microscope. Phys. Rev. Lett. 1986, 56, 930–933.

7

Deng, X. Y.; Xiong, F.; Li, X. Y.; Xiang, B.; Li, Z.; Wu, X.; Guo, C.; Li, X. L.; Li, Y.; Li, G. Y. et al. Application of atomic force microscopy in cancer research. J. Nanobiotechnol. 2018, 16, 102.

8

Stylianou, A.; Kontomaris, S. V.; Grant, C.; Alexandratou, E. Atomic force microscopy on biological materials related to pathological conditions. Scanning 2019, 2019, 8452851.

9

Zemła, J.; Danilkiewicz, J.; Orzechowska, B.; Pabijan, J.; Seweryn, S.; Lekka, M. Atomic force microscopy as a tool for assessing the cellular elasticity and adhesiveness to identify cancer cells and tissues. Semin. Cell Dev. Biol. 2018, 73, 115–124.

10

Dufrêne, Y. F.; Evans, E.; Engel, A.; Helenius, J.; Gaub, H. E.; Müller, D. J. Five challenges to bringing single-molecule force spectroscopy into living cells. Nat. Methods 2011, 8, 123–127.

11

Prabhune, M.; Belge, G.; Dotzauer, A.; Bullerdiek, J.; Radmacher, M. Comparison of mechanical properties of normal and malignant thyroid cells. Micron 2012, 43, 1267–1272.

12

Rianna, C.; Radmacher, M. Comparison of viscoelastic properties of cancer and normal thyroid cells on different stiffness substrates. Eur. Biophys. J. 2017, 46, 309–324.

13

Li, Q. S.; Lee, G. Y. H.; Ong, C. N.; Lim, C. T. AFM indentation study of breast cancer cells. Biochem. Biophys. Res. Commun. 2008, 374, 609–613.

14

Lasalvia, M.; D'Antonio, P.; Perna, G.; Capozzi, V.; Mariggiò, M.; Perrone, D.; Gallo, C.; Quartucci, G.; Lo Muzio, L. Discrimination of different degrees of oral squamous cell carcinoma by means of Raman microspectroscopy and atomic force microscopy. Anal. Methods 2015, 7, 699–707.

15

Canetta, E.; Riches, A.; Borger, E.; Herrington, S.; Dholakia, K.; Adya, A. K. Discrimination of bladder cancer cells from normal urothelial cells with high specificity and sensitivity: Combined application of atomic force microscopy and modulated Raman spectroscopy. Acta Biomater. 2014, 10, 2043–2055.

16

Cross, S. E.; Jin, Y. S.; Rao, J. Y.; Gimzewski, J. K. Nanomechanical analysis of cells from cancer patients. Nat. Nanotechnol. 2007, 2, 780–783.

17

Stylianou, A.; Lekka, M.; Stylianopoulos, T. AFM assessing of nanomechanical fingerprints for cancer early diagnosis and classification: From single cell to tissue level. Nanoscale 2018, 10, 20930–20945.

18

Dufrêne, Y. F.; Pelling, A. E. Force nanoscopy of cell mechanics and cell adhesion. Nanoscale 2013, 5, 4094–4104.

19

Martin, Y.; Williams, C. C.; Wickramasinghe, H. K. Atomic force microscope-force mapping and profiling on a sub 100-Å scale. J. Appl. Phys. 1987, 61, 4723–4729.

20

Putman, C. A. J.; Van der Werf, K. O.; De Grooth, B. G.; Van Hulst, N. F.; Greve, J. Tapping mode atomic force microscopy in liquid. Appl. Phys. Lett. 1994, 64, 2454–2456.

21

Dufrêne, Y. F. Atomic force microscopy, a powerful tool in microbiology. J. Bacteriol. 2002, 184, 5205–5213.

22

Penedo, M.; Miyazawa, K.; Okano, N.; Furusho, H.; Ichikawa, T.; Alam, M. S.; Miyata, K.; Nakamura, C.; Fukuma, T. Visualizing intracellular nanostructures of living cells by nanoendoscopy-AFM. Sci. Adv. 2021, 7, eabj4990.

23

Roduit, C.; Sekatski, S.; Dietler, G.; Catsicas, S.; Lafont, F.; Kasas, S. Stiffness tomography by atomic force microscopy. Biophys. J. 2009, 97, 674–677.

24

Girasole, M.; Pompeo, G.; Cricenti, A.; Longo, G.; Boumis, G.; Bellelli, A.; Amiconi, S. The how, when, and why of the aging signals appearing on the human erythrocyte membrane: An atomic force microscopy study of surface roughness. Nanomedicine 2010, 6, 760–768.

25

Turner, R. D.; Mesnage, S.; Hobbs, J. K.; Foster, S. J. Molecular imaging of glycan chains couples cell-wall polysaccharide architecture to bacterial cell morphology. Nat. Commun. 2018, 9, 1263.

26

Andre, G.; Deghorain, M.; Bron, P. A.; Van Swam, I. I.; Kleerebezem, M.; Hols, P.; Dufrêne, Y. F. Fluorescence and atomic force microscopy imaging of wall teichoic acids in Lactobacillus plantarum. ACS Chem. Biol. 2011, 6, 366–376.

27

Dufrêne, Y. F. Atomic force microscopy in microbiology: New structural and functional insights into the microbial cell surface. mBio 2014, 5, e01363–e01314.

28

Pi, J.; Cai, J. Y. Cell topography and its quantitative imaging by AFM. Methods Mol. Biol. 2019, 1886, 99–113.

29

Gaman, A.; Osiac, E.; Rotaru, I.; Taisescu, C. Surface morphology of leukemic cells from chronic myeloid leukemia under atomic force microscopy. Curr. Health Sci. J. 2013, 39, 45–47.

30

Kaul-Ghanekar, R.; Singh, S.; Mamgain, H.; Jalota-Badhwar, A.; Paknikar, K. M.; Chattopadhyay, S. Tumor suppressor protein SMAR1 modulates the roughness of cell surface: Combined AFM and SEM study. BMC Cancer 2009, 9, 350.

31

Calzado-Martín, A.; Encinar, M.; Tamayo, J.; Calleja, M.; San Paulo, A. Effect of actin organization on the stiffness of living breast cancer cells revealed by peak-force modulation atomic force microscopy. ACS Nano 2016, 10, 3365–3374.

32

Platet, N.; Hinkel, I.; Richert, L.; Murdamoothoo, D.; Moufok-Sadoun, A.; Vanier, M.; Lavalle, P.; Gaiddon, C.; Vautier, D.; Freund, J. N. et al. The tumor suppressor CDX2 opposes pro-metastatic biomechanical modifications of colon cancer cells through organization of the actin cytoskeleton. Cancer Lett. 2017, 386, 57–64.

33

Wang, Z.; Wu, X. L.; Wang, X.; Tian, H. X.; Chen, Z. H.; Li, Y. Q. The biophysical property of A549 cells transferred by VEGF-D. Scanning 2014, 36, 202–208.

34

Frederix, P. L. T. M.; Bosshart, P. D.; Engel, A. Atomic force microscopy of biological membranes. Biophys. J. 2009, 96, 329–338.

35

Alsteens, D.; Pfreundschuh, M.; Zhang, C.; Spoerri, P. M.; Coughlin, S. R.; Kobilka, B. K.; Müller, D. J. Imaging G protein-coupled receptors while quantifying their ligand-binding free-energy landscape. Nat. Methods 2015, 12, 845–851.

36

Dufrêne, Y. F.; Ando, T.; Garcia, R.; Alsteens, D.; Martinez-Martin, D.; Engel, A.; Gerber, C.; Müller, D. J. Imaging modes of atomic force microscopy for application in molecular and cell biology. Nat. Nanotechnol. 2017, 12, 295–307.

37

Scheuring, S.; Sturgis, J. N. Chromatic adaptation of photosynthetic membranes. Science 2005, 309, 484–487.

38

Basoli, F.; Giannitelli, S. M.; Gori, M.; Mozetic, P.; Bonfanti, A.; Trombetta, M.; Rainer, A. Biomechanical characterization at the cell scale: Present and prospects. Front. Physiol. 2018, 9, 1449.

39

Zhu, C.; Bao, G.; Wang, N. Cell mechanics: Mechanical response, cell adhesion, and molecular deformation. Annu. Rev. Biomed. Eng. 2000, 2, 189–226.

40

Garcia, R. Nanomechanical mapping of soft materials with the atomic force microscope: Methods, theory and applications. Chem. Soc. Rev. 2020, 49, 5850–5884.

41

Weber, A.; Iturri, J.; Benitez, R.; Toca-Herrera, J. L. Measuring biomaterials mechanics with atomic force microscopy. 1. influence of the loading rate and applied force (pyramidal tips). Microsc. Res. Tech. 2019, 82, 1392–1400.

42

Yang, F.; Su, X. H.; Pi, J.; Liao, K. S.; Zhou, H.; Sun, Y.; Liu, J.; Guo, X. X.; Jiang, J. H.; Jin, H. et al. Atomic force microscopy technique used for assessment of the anti-arthritic effect of licochalcone a via suppressing NF-κB activation. Biomed. Pharmacother. 2018, 103, 1592–1601.

43

Su, Z. H.; Sun, H.; Ao, M.; Zhao, C. Y. Atomic force microscopy study of the anti-inflammatory effects of triptolide on rheumatoid arthritis fibroblast-like synoviocytes. Microsc. Microanal. 2017, 23, 1002–1012.

44

Kiio, T. M.; Park, S. Nano-scientific application of atomic force microscopy in pathology: From molecules to tissues. Int. J. Med. Sci. 2020, 17, 844–858.

45

Suresh, S. Biomechanics and biophysics of cancer cells. Acta Biomater. 2007, 3, 413–438.

46

Goetz, J. G.; Minguet, S.; Navarro-Lérida, I.; Lazcano, J. J.; Samaniego, R.; Calvo, E.; Tello, M.; Osteso-Ibáñez, T.; Pellinen, T.; Echarri, A. et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011, 146, 148–163.

47

Fletcher, D. A.; Mullins, R. D. Cell mechanics and the cytoskeleton. Nature, 2010, 463, 485–492.

48

Paszek, M. J.; Weaver, V. M. The tension mounts: Mechanics meets morphogenesis and malignancy. J. Mammary Gland Biol. Neoplasia 2004, 9, 325–342.

49

Kumar, S.; Weaver, V. M. Mechanics, malignancy, and metastasis: The force journey of a tumor cell. Cancer Metastasis Rev. 2009, 28, 113–127.

50

Lekka, M. Discrimination between normal and cancerous cells using AFM. BioNanoScience 2016, 6, 65–80.

51

Plodinec, M.; Loparic, M.; Monnier, C. A.; Obermann, E. C.; Zanetti-Dallenbach, R.; Oertle, P.; Hyotyla, J. T.; Aebi, U.; Bentires-Alj, M.; Lim, R. Y. H. et al. The nanomechanical signature of breast cancer. Nat. Nanotechnol. 2012, 7, 757–765.

52

Zhao, X. Q.; Zhong, Y. X.; Ye, T.; Wang, D. J.; Mao, B. W. Discrimination between cervical cancer cells and normal cervical cells based on longitudinal elasticity using atomic force microscopy. Nanoscale Res. Lett. 2015, 10, 482.

53

Lekka, M.; Pabijan, J. Measuring elastic properties of single cancer cells by AFM. Methods Mol. Biol. 2019, 1886, 315–324.

54

Moeendarbary, E.; Valon, L.; Fritzsche, M.; Harris, A. R.; Moulding, D. A.; Thrasher, A. J.; Stride, E.; Mahadevan, L.; Charras, G. T. The cytoplasm of living cells behaves as a poroelastic material. Nat. Mater. 2013, 12, 253–261.

55

Nematbakhsh, Y.; Pang, K. T.; Lim, C. T. Correlating the viscoelasticity of breast cancer cells with their malignancy. Converg. Sci. Phys. Oncol. 2017, 3, 034003.

56

Chen, M. D.; Zeng, J. S.; Ruan, W. W.; Zhang, Z. H.; Wang, Y. H.; Xie, S. S.; Wang, Z. C.; Yang, H. Q. Examination of the relationship between viscoelastic properties and the invasion of ovarian cancer cells by atomic force microscopy. Beilstein J. Nanotechnol. 2020, 11, 568–582.

57

Kwon, T.; Gunasekaran, S.; Eom, K. Atomic force microscopy-based cancer diagnosis by detecting cancer-specific biomolecules and cells. Biochim. Biophys. Acta Rev. Cancer 2019, 1871, 367–378.

58

Ritzefeld, M.; Walhorn, V.; Anselmetti, D.; Sewald, N. Analysis of DNA interactions using single-molecule force spectroscopy. Amino Acids 2013, 44, 1457–1475.

59

Li, M.; Xiao, X. B.; Liu, L. Q.; Xi, N.; Wang, Y. C.; Dong, Z. L.; Zhang, W. J. Atomic force microscopy study of the antigen-antibody binding force on patient cancer cells based on ROR1 fluorescence recognition. J. Mol. Recognit. 2013, 26, 432–438.

60

Best, R. B.; Clarke, J. What can atomic force microscopy tell us about protein folding? Chem. Commun. 2002, 183–192.

61

Skliar, M.; Chernyshev, V. S. Imaging of extracellular vesicles by atomic force microscopy. J. Vis. Exp. 2019, 151, e59254.

62

Mei, L.; Van Der Mei, H. C.; Ren, Y. J.; Norde, W.; Busscher, H. J. Poisson analysis of streptococcal bond strengthening on stainless steel with and without a salivary conditioning film. Langmuir 2009, 25, 6227–6231.

63

Mei, L.; Ren, Y.; Busscher, H. J.; Chen, Y.; Van Der Mei, H. C. Poisson analysis of streptococcal bond-strengthening on saliva-coated enamel. J. Dent. Res. 2009, 88, 841–845.

64

Ruggeri, F. S.; Šneideris, T.; Vendruscolo, M.; Knowles, T. P. J. Atomic force microscopy for single molecule characterisation of protein aggregation. Arch. Biochem. Biophy. 2019, 664, 134–148.

65

Heupel, W. M.; Zillikens, D.; Drenckhahn, D.; Waschke, J. Pemphigus vulgaris IgG directly inhibit desmoglein 3-mediated transinteraction. J. Immunol. 2008, 181, 1825–1834.

66

Edwardson, J. M.; Henderson, R. M. Atomic force microscopy and drug discovery. Drug Discov. Today 2004, 9, 64–71.

67

Begat, P.; Morton, D. A. V.; Staniforth, J. N.; Price, R. The cohesive- adhesive balances in dry powder inhaler formulations I: Direct quantification by atomic force microscopy. Pharm. Res. 2004, 21, 1591–1597.

68

Leite, F. L.; Bueno, C. C.; Da Róz, A. L.; Ziemath, E. C.; Oliveira, O. N. Jr. Theoretical models for surface forces and adhesion and their measurement using atomic force microscopy. Int. J. Mol. Sci. 2012, 13, 12773–12856.

69

Ramachandran, S.; Arce, F. T.; Lal, R. Potential role of atomic force microscopy in systems biology. Wiley Interdiscip. Rev. Syst. Biol. Med. 2011, 3, 702–716.

70

Hoogenboom, B. W. Stretching the resolution limit of atomic force microscopy. Nat. Struct. Mol. Biol. 2021, 28, 629–630.

71

Kisielowski, C.; Freitag, B.; Bischoff, M.; Van Lin, H.; Lazar, S.; Knippels, G.; Tiemeijer, P.; Van Der Stam, M.; Von Harrach, S.; Stekelenburg, M. et al. Detection of single atoms and buried defects in three dimensions by aberration-corrected electron microscope with 0.5-Å information limit. Microsc. Microanal. 2008, 14, 469–477.

72

Dwyer, C.; Maunders, C.; Zheng, C. L.; Weyland, M.; Tiemeijer, P. C.; Etheridge, J. Sub-0.1 nm-resolution quantitative scanning transmission electron microscopy without adjustable parameters. Appl. Phy. Lett. 2012, 100, 191915.

73

Wang, L.; Li, C. S.; Li, J. T.; Zhang, X. F.; Li, X. C.; Cui, Y. R.; Xia, Y.; Zhang, Y. Q.; Mao, S. C.; Ji, Y. et al. Liquid-phase scanning electron microscopy for single membrane protein imaging. Biochem. Biophys. Res. Commun. 2022, 590, 163–168.

74

Tizro, P.; Choi, C.; Khanlou, N. Sample preparation for transmission electron microscopy. Methods Mol. Biol. 2019, 1897, 417–424.

75

Winey, M.; Meehl, J. B.; O'Toofle, E. T.; Giddings Jr., T. H. Conventional transmission electron microscopy. Mol. Biol. Cell 2014, 25, 319–323.

76

Jones, C. G. Scanning electron microscopy: Preparation and imaging for SEM. Methods Mol. Biol. 2012, 915, 1–20.

77

Lipiec, E.; Sofińska, K.; Seweryn, S.; Wilkosz, N.; Szymonski, M. Revealing DNA structure at liquid/solid interfaces by AFM-based high-resolution imaging and molecular spectroscopy. Molecules, 2021, 26, 6476.

78

Van Doren, E. A.; De Temmerman, P. J. R.; Francisco, M. A. D.; Mast, J. Determination of the volume-specific surface area by using transmission electron tomography for characterization and definition of nanomaterials. J. Nanobiotechnol. 2011, 9, 17.

79

Ponce, A.; Mejía-Rosales, S.; José-Yacamán, M. Scanning transmission electron microscopy methods for the analysis of nanoparticles. Methods Mol. Biol. 2012, 906, 453–471.

80

Lapshin, R. V. Feature-oriented scanning methodology for probe microscopy and nanotechnology. Nanotechnology 2004, 15, 1135–1151.

81

Franken, L. E.; Boekema, E. J.; Stuart, M. C. A. Transmission electron microscopy as a tool for the characterization of soft materials: Application and interpretation. Adv. Sci. 2017, 4, 1600476.

82

Fischer, E. R.; Hansen, B. T.; Nair, V.; Hoyt, F. H.; Dorward, D. W. Scanning electron microscopy. Curr. Protoc. Microbiol. 2012, Chapter 2, Unit 2B. 2.

Publication history
Copyright
Rights and permissions

Publication history

Received: 26 January 2022
Revised: 21 February 2022
Accepted: 28 February 2022
Published: 08 March 2022
Issue date: March 2022

Copyright

© The Author(s) 2022. Nano TransMed published by Tsinghua University Press.

Rights and permissions

The articles published in this open access journal are distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Return