Abstract
Among various microscopic techniques for characterizing protein structures and functions, high-speed atomic force microscopy (HS-AFM) is a unique technique in that it allows direct visualization of structural changes and molecular interactions of proteins without any labeling in a liquid environment. Since the development of the HS-AFM was first reported in 2001, it has been applied to analyze the dynamics of various types of proteins, including motor proteins, membrane proteins, DNA-binding proteins, amyloid proteins, and artificial proteins. This method has now become a versatile tool indispensable for biophysical research. This short review summarizes some bioimaging applications of HS-AFM reported in the last few years and novel applications of HS-AFM utilizing the unique ability of AFM to gain mechanical properties of samples in addition to structural information.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alessandrini A, Facci P (2005) AFM: a versatile tool in biophysics. Meas Sci Technol 16:R65–R92. https://doi.org/10.1088/0957-0233/16/6/R01
Ando T (2018) High-speed atomic force microscopy and its future prospects. Biophys Rev 10:285–292. https://doi.org/10.1007/s12551-017-0356-5
Ando T, Kodera N, Takai E et al (2001) A high-speed atomic force microscope for studying biological macromolecules. Proc Natl Acad Sci 98:12468–12472. https://doi.org/10.1073/pnas.211400898
Ando T, Uchihashi T, Fukuma T (2008) High-speed atomic force microscopy for nano-visualization of dynamic biomolecular processes. Prog Surf Sci 83:337–437
Ando T, Uchihashi T, Scheuring S (2014) Filming biomolecular processes by high-speed atomic force microscopy. Chem Rev 114:3120–3188. https://doi.org/10.1021/cr4003837
Casuso I, Khao J, Chami M et al (2012) Characterization of the motion of membrane proteins using high-speed atomic force microscopy. Nat Nanotechnol 7:525–529. https://doi.org/10.1038/nnano.2012.109
Cho C, Jang J, Kang Y et al (2019) Structural basis of nucleosome assembly by the Abo1 AAA+ ATPase histone chaperone. Nat Commun 10:5764. https://doi.org/10.1038/s41467-019-13743-9
Colom A, Casuso I, Boudier T, Scheuring S (2012) High-speed atomic force microscopy: cooperative adhesion and dynamic equilibrium of Junctional microdomain membrane proteins. J Mol Biol 423:249–256. https://doi.org/10.1016/j.jmb.2012.07.004
Deville C, Carroni M, Franke KB et al (2017) Structural pathway of regulated substrate transfer and threading through an Hsp100 disaggregase. Sci Adv 3:e1701726. https://doi.org/10.1126/sciadv.1701726
Dufrêne YF, Martínez-Martín D, Medalsy I et al (2013) Multiparametric imaging of biological systems by force-distance curve–based AFM. Nat Methods 10:847–854. https://doi.org/10.1038/nmeth.2602
Frederix PLTM, Akiyama T, Staufer U et al (2003) Atomic force bio-analytics. Curr Opin Chem Biol 7:641–647. https://doi.org/10.1016/j.cbpa.2003.08.010
Fukuda S, Uchihashi T, Iino R et al (2013) High-speed atomic force microscope combined with single-molecule fluorescence microscope. Rev Sci Instrum 84:073706. https://doi.org/10.1063/1.4813280
Ganser C, Uchihashi T (2019) Microtubule self-healing and defect creation investigated by in-line force measurements during high-speed atomic force microscopy imaging. Nanoscale 11:125–135. https://doi.org/10.1039/C8NR07392A
Joo C, Balci H, Ishitsuka Y et al (2008) Advances in single-molecule fluorescence methods for molecular biology. Annu Rev Biochem 77:51–76. https://doi.org/10.1146/annurev.biochem.77.070606.101543
Kasas S, Dietler G (2008) Probing nanomechanical properties from biomolecules to living cells. Pflugers Arch - Eur J Physiol 456:13–27. https://doi.org/10.1007/s00424-008-0448-y
Kodera N, Yamamoto D, Ishikawa R, Ando T (2010) Video imaging of walking myosin V by high-speed atomic force microscopy. Nature 468:72–76. https://doi.org/10.1038/nature09450
Lee S, Sowa ME, Watanabe Y et al (2003) The structure of ClpB. Cell 115:229–240. https://doi.org/10.1016/S0092-8674(03)00807-9
Lin Y-C, Guo YR, Miyagi A et al (2019) Force-induced conformational changes in PIEZO1. Nature 573:230–234. https://doi.org/10.1038/s41586-019-1499-2
Miller H, Zhou Z, Shepherd J et al (2018) Single-molecule techniques in biophysics: a review of the progress in methods and applications. Rep Prog Phys 81:024601. https://doi.org/10.1088/1361-6633/aa8a02
Miyagi A, Chipot C, Rangl M, Scheuring S (2016) High-speed atomic force microscopy shows that annexin V stabilizes membranes on the second timescale. Nat Nanotechnol 11:783–790. https://doi.org/10.1038/nnano.2016.89
Mori T, Sugiyama S, Byrne M et al (2018) Revealing circadian mechanisms of integration and resilience by visualizing clock proteins working in real time. Nat Commun 9:3245. https://doi.org/10.1038/s41467-018-05438-4
Nakajima M, Imai K, Ito H et al (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science (80-) 308:414–415. https://doi.org/10.1126/science.1108451
Nakazaki Y, Watanabe Y-H (2014) ClpB chaperone passively threads soluble denatured proteins through its central pore. Genes Cells 19:891–900. https://doi.org/10.1111/gtc.12188
Owa M, Uchihashi T, Yanagisawa H et al (2019) Inner lumen proteins stabilize doublet microtubules in cilia and flagella. Nat Commun 10:1143. https://doi.org/10.1038/s41467-019-09051-x
Rangl M, Miyagi A, Kowal J et al (2016) Real-time visualization of conformational changes within single MloK1 cyclic nucleotide-modulated channels. Nat Commun 7:12789. https://doi.org/10.1038/ncomms12789
Ruan Y, Miyagi A, Wang X et al (2017) Direct visualization of glutamate transporter elevator mechanism by high-speed AFM. Proc Natl Acad Sci 114:1584–1588. https://doi.org/10.1073/pnas.1616413114
Shibata M, Yamashita H, Uchihashi T et al (2010) High-speed atomic force microscopy shows dynamic molecular processes in photoactivated bacteriorhodopsin. Nat Nanotechnol 5:208–212. https://doi.org/10.1038/nnano.2010.7
Sumino A, Sumikama T, Uchihashi T, Oiki S (2019) High-speed AFM reveals accelerated binding of agitoxin-2 to a K + channel by induced fit. Sci Adv 5:eaax0495. https://doi.org/10.1126/sciadv.aax0495
Uchihashi T, Iino R, Ando T, Noji H (2011) High-speed atomic force microscopy reveals rotary catalysis of rotorless F 1-ATPase. Science (80-) 333:755–758. https://doi.org/10.1126/science.1205510
Uchihashi T, Scheuring S (2018) Applications of high-speed atomic force microscopy to real-time visualization of dynamic biomolecular processes. Biochim Biophys Acta, Gen Subj 1862:229–240. https://doi.org/10.1016/j.bbagen.2017.07.010
Umakoshi T, Fukuda S, Iino R et al (2020) High-speed near-field fluorescence microscopy combined with high-speed atomic force microscopy for biological studies. Biochim Biophys Acta, Gen Subj 1864:S0304-4165(19)30061-3. https://doi.org/10.1016/j.bbagen.2019.03.011
Watanabe Y, Motohashi K, Yoshida M (2002) Roles of the two ATP binding sites of ClpB from Thermus thermophilus. J Biol Chem 277:5804–5809. https://doi.org/10.1074/jbc.M109349200
Zou JX, Revenko AS, Li LB et al (2007) ANCCA, an estrogen-regulated AAA+ ATPase coactivator for ER , is required for coregulator occupancy and chromatin modification. Proc Natl Acad Sci 104:18067–18072. https://doi.org/10.1073/pnas.0705814104
Acknowledgments
We thank Prof. Toshio Ando for his long-term dedication to the development of HS-AFM and its application.
Funding
This work was partly supported by JST/CREST (#JPMJCR13M1); KAKENHI from the Ministry of Education, Culture, Sports, Science and Technology, Japan (19H05389, 18H04512 and 18H01837 to TU, and 19K23737 to CG); and the Joint Research of the Exploratory Research Center on Life and Living Systems (ExCELLS) (ExCELLS program No. 18-101 to T.U.).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Uchihashi, T., Ganser, C. Recent advances in bioimaging with high-speed atomic force microscopy. Biophys Rev 12, 363–369 (2020). https://doi.org/10.1007/s12551-020-00670-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12551-020-00670-z