Introduction: Super-Resolution and Single-Molecule Imaging

Jun 14, 2017 - ... impact biological and chemical super-resolution imaging by creating super-resolution maps of the local environment, ... [Google Sch...
1 downloads 0 Views 2MB Size
Editorial pubs.acs.org/CR

Introduction: Super-Resolution and Single-Molecule Imaging

T

the models and data analysis strategies that have emerged to interpret the large data sets acquired during localization-based super-resolution imaging and obtain accurate representations of the underlying sample.12 Finally, Landes and co-workers describe both theory and applications in which single-molecule localization is extended with single-particle tracking to follow single-molecule dynamics in real time, with applications in both biophysics and materials science.13 In contrast to single-molecule localization microscopy, another approach to achieve super-resolution optical imaging uses patterned illumination to effectively squeeze the diffraction limit to subwavelength dimensions. Widengren and co-workers present one such strategy, stimulated emission depletion (STED) microscopy, in a review that details the instrumentation, sample preparation, and applications.14 STED is a twobeam technique that uses nonlinear optics to shape the excitation beam into an effective subdiffraction-limited excitation volume, leading to subdiffraction-limited resolution in a confocal geometry.9 An alternative beam patterning approach is structured illumination microscopy (SIM). Here, a patterned excitation source is introduced to the sample, transforming high-frequency spatial information from the sample into low-frequency content that can be collected through the imaging optics of the system and then mathematically recovered during image processing.15,16 Incorporating nonlinearities like saturation into SIM significantly increases the resolution in super-resolution structured illumination microscopy (SR-SIM).17 While each of the super-resolution optical imaging techniques offer significant advantages on their own, the review from Xu and co-workers explores how careful sample preparation and experimental design allow the various forms of super-resolution imaging to be correlated with other imaging modalities, such as electron microscopy or atomic force microscopy, to obtain further nanoscopic information.18 The remaining reviews in this special issue are dedicated to the applications that benefit from achieving optical resolution below the wavelength of light. Biological and biophysical studies in particular have benefitted from the emergence of super-resolution imaging, and thus several reviews showcase how super-resolution imaging has advanced cellular studies. For example, the review from Veatch and co-workers examines the role of super-resolution imaging in understanding the composition of, and intermolecular interactions on, cell membranes,19 while Heilemann and co-workers describe how super-resolution imaging allows both intracellular structure and function to be imaged at the molecular level in eukaryotic cells.20 More recently, problems in chemistry and materials science have also been addressed by super-resolution techniques. Fang and co-workers discuss how super-resolution imaging enables visualization of reactions at the single-molecule level, allowing improved characterization of catalytic processes and reaction kinetics.21 Willets and co-workers describe the

he invention of the light microscope propelled science forward by granting researchers the ability to magnify objects and study features with resolution well below that of the naked eye. However, despite centuries of improvements to imaging systems, optical microscopes could never surpass the fundamental diffraction limit of light, which prevents features smaller than roughly half a wavelength (several hundreds of nanometers) from being resolved.1 Previously, this resolution limit was circumvented with near-field optics: light was squeezed through a nanosized aperture or focused to the end of a sharpened tip.2,3 Yet, this resolution enhancement came at the price of low signals, difficult aperture or tip fabrication, the need for a scanning probe geometry, and the perturbative nature of the tip upon the sample.4 However, in the last three decades, optical microscopy has been transformed, first through the first observation of single molecules,5 and then through the rapid expansion of a suite of far-field imaging techniques known collectively as superresolution microscopy.6−10 Unlike near-field imaging, the current class of super-resolution techniques is based on farfield optics; through elegant optical tricks, each achieves resolution well below the wavelength of light. The rapid expansion and acceptance of super-resolution microscopy as a transformative technology was marked in 2014 when the Nobel Prize in Chemistry was awarded to Eric Betzig, Stefan Hell, and W. E. Moerner, three pioneers of single-molecule and superresolution imaging. Thus, this thematic issue of Chemical Reviews dedicated to super-resolution imaging is timely, and we intend it to provide perspective on how the field has developed over a relatively short time, as well as look to the future for new developments and emerging applications. This thematic issue has two primary objectives: first, to introduce the main classes of super-resolution imaging, including instrumentation, sample preparation, and data analysis; and second, to highlight the broad range of applications that have benefitted from these emerging techniques in the last decades, from biology to chemistry to materials science. While the basic approaches to super-resolved microscopy have been commercialized and are now available as “black box” instruments, these reviews go beyond commercial instrumentation to capture the evolution of the techniques, the current state-of-the-art, and future directions. Much of this special issue describes the various approaches to super-resolution imaging. One such approach circumvents the diffraction limit by localizing emission from fluorescent molecules one at a time, and then reconstructs an image with subdiffraction-limited features after multiple localization events. Variants of these single-molecule super-resolution approaches are known by a range of acronyms, including STORM, PALM, FPALM, dSTORM, fPALM, SMACM, and GSDIM. The review from Moerner and co-workers describes single-molecule super-resolution microscopy in detail, highlighting how the technique has evolved from simple two-dimensional projections to fully resolved three-dimensional images.11 To complement this review, Presse á nd co-workers present an in-depth look at © 2017 American Chemical Society

Special Issue: Super-Resolution and Single-Molecule Imaging Published: June 14, 2017 7241

DOI: 10.1021/acs.chemrev.7b00242 Chem. Rev. 2017, 117, 7241−7243

Chemical Reviews

Editorial

Julie Biteen

synergistic relationship between plasmonics and superresolution imaging, illustrating how super-resolution techniques provide better mechanistic understanding of plasmon-coupled emission, while also describing how the integration of plasmonic nanostructures can further improve resolution across the various super-resolution platforms.22 Finally, for comparison with the primary classes of super-resolution imaging, we include a review from Van Duyne and co-workers on alternative strategies for achieving improved spatial resolution using plasmon-enhanced excitation fields for surface-enhanced Raman scattering (SERS) and tip-enhanced Raman scattering (TERS).23 The discussion of TERS introduces many of the advantages and challenges of using scanning probe techniques for achieving subwavelength resolution by confining the excitation fields, similar to near-field optical approaches. We believe that this thematic issue is timely because it highlights a class of techniques that have significantly transformed how we interact with and understand the nanoscopic world across a wide range of fields in little over a decade. Many of the reviews in this thematic issue cross paths with one another, which highlights the interdisciplinary character of super-resolution imaging and the ways in which insight from one field drives discovery in another. As we look toward the future of the field, it is clear that several key developments will impact these technologies. First, improved fluorescent reporters with increased brightness, stability, specificity, and biocompatibility will enhance both localization precision and time resolution across a variety of experimental platforms. Furthermore, increasing the library of available probes with engineered responses to stimuli will greatly impact biological and chemical super-resolution imaging by creating super-resolution maps of the local environment, including pH, ion concentration, and electric potential, as well as of chemical changes, such as catalysis or redox chemistry. Second, the ability to super-resolve three-dimensional images has expanded in recent years, but new tools and strategies that increase the precision in the axial dimension below 10 nm while maintaining a large depth of field are still required to obtain true superresolution information from thicker samples, including tissue and whole organs. Third, we anticipate improvements in realtime dynamic imaging, combining the spatial resolution of wide-field imaging with fast temporal resolution to follow timedependent processes. Recently, sCMOS cameras have emerged as an alternative to the EMCCDs typically used in the field, and as the sensitivity, noise, quantum yield, and price of these detectors continue to improve, faster frame rates and larger pixel arrays will become generally accessible. Thus, we envision an increasing push to image below 5 nm spatial resolution and with microsecond temporal resolution. Finally, the rise of machine learning will improve data analysis strategies. The massive data sets generated by super-resolution imaging will only continue to increase in size based on the advances described above, and employing advanced computational strategies will significantly impact the field by efficiently providing accurate results. Overall, we believe that the transformation afforded by the rise of super-resolution imaging has only just begun, and the coming years will see continued advances across the various techniques, allowing new and diverse applications to emerge. We thank all of the authors, editors, and staff at Chemical Reviews for the time and energy they have put into this thematic issue, and we hope that even specialists will learn something new through the collection of reviews we have compiled.

University of Michigan

Katherine A. Willets Temple University

AUTHOR INFORMATION ORCID

Katherine A. Willets: 0000-0002-1417-4656 Notes

Views expressed in this editorial are those of the authors and not necessarily the views of the ACS. Biographies

Julie Biteen is an Assistant Professor of Chemistry and Biophysics at the University of Michigan, where her research program develops single-molecule and super-resolution microscopy for applications to microbiology and plasmonics. Dr. Biteen earned her A.B. in Chemistry at Princeton University and a Masters in Applied Physics as well as a Ph.D. in Chemistry at California Institute of Technology in the laboratories of Harry Atwater and Nathan Lewis. Dr. Biteen then trained as a postdoc in the lab of W. E. Moerner at Stanford University. In her independent career, Biteen has been recognized by numerous awards, including the Margaret Oakley Dayhoff Award for Women in Biophysical Sciences (2017), the Journal of Physical Chemistry Award Lectureship (2016), a Scialog fellowship from the Moore Foundation and the Research Corporation for Science Advancement (2015−16), a Burroughs Wellcome Fund Career Award at the Scientific Interface (2009−14), an NSF CAREER Award (2013−18), and a PicoQuant Young Investigator Award (2011).

Katherine A. (Kallie) Willets is the Robert L. Smith Early Career Professor in the department of chemistry at Temple University. She 7242

DOI: 10.1021/acs.chemrev.7b00242 Chem. Rev. 2017, 117, 7241−7243

Chemical Reviews

Editorial

(17) Allen, J. R.; Ross, S. T.; Davidson, M. W. Structured Illumination Microscopy for Superresolution. ChemPhysChem 2014, 15, 566−576. (18) Hauser, M.; Wojcik, M.; Kim, D.; Mahmoudi, M.; Li, W.; Xu, K. Correlative Super-Resolution Microscopy: New Dimensions and New Opportunities. Chem. Rev. 2017, 10.1021/acs.chemrev.6b00604. (19) Stone, M. B.; Shelby, S. A.; Veatch, S. L. Super-Resolution Microscopy: Shedding Light on the Cellular Plasma Membrane. Chem. Rev. 2017, 10.1021/acs.chemrev.6b00716. (20) Sauer, M.; Heilemann, M. Single-Molecule Localization Microscopy in Eukaryotes. Chem. Rev. 2017, 10.1021/acs.chemrev.6b00667. (21) Chen, T.; Dong, B.; Chen, K.; Zhao, F.; Cheng, X.; Ma, C.; Lee, S.; Zhang, P.; Kang, S. H.; Ha, J. W.; Xu, W.; Fang, N. Optical SuperResolution Imaging of Surface Reactions. Chem. Rev. 2017, 10.1021/ acs.chemrev.6b00673. (22) Willets, K. A.; Wilson, A. J.; Sundaresan, V.; Joshi, P. B. SuperResolution Imaging and Plasmonics. Chem. Rev. 2017, 10.1021/ acs.chemrev.6b00547. (23) Zrimsek, A. B.; Chiang, N.; Mattei, M.; Zaleski, S.; McAnally, M. O.; Chapman, C. T.; Henry, A.-I.; Schatz, G. C.; Van Duyne, R. P. Single-Molecule Chemistry with Surface- and Tip-Enhanced Raman Spectroscopy. Chem. Rev. 2016, 10.1021/acs.chemrev.6b00552.

received her Ph.D. from Stanford University in 2005, working in the lab of W. E. Moerner, where she fostered her interest in singlemolecule imaging as a tool to reveal local heterogeneity. From there she conducted postdoctoral research with Richard Van Duyne at Northwestern University from 2005 to 2007, developing her interests in plasmonic nanostructures. After beginning her career at the University of Texas at Austin in 2007, where she was promoted to Associate Professor in 2014, she moved to Temple University in 2015, where her lab continues to use single-molecule techniques to understand how nanoscale features of plasmonic nanostructures impact ligand binding, surface-enhanced Raman scattering, and electrochemical reactions at surfaces. She has been recognized with the Department of Energy Early Career Award and the Air Force Office of Scientific Research Young Investigator Award, and is currently a member of the Defense Science Study Group.

REFERENCES (1) Abbe, E. Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung. Archiv für mikroskopische Anatomie 1873, 9, 413−418. (2) Betzig, E.; Trautman, J. K. Near-Field Optics: Microscopy, Spectroscopy, and Surface Modification Beyond the Diffraction Limit. Science 1992, 257, 189. (3) Zenhausern, F.; O’Boyle, M. P.; Wickramasinghe, H. K. Apertureless near-field optical microscope. Appl. Phys. Lett. 1994, 65, 1623−1625. (4) Dragnea, B.: Near-Field Scanning Optical Microscopy: Chemical Imaging. In Dekker Encyclopedia of Nanoscience and Nanotechnology, 3rd ed.; CRC Press, 2014; pp 3371−3379. (5) Moerner, W. E.; Kador, L. Optical detection and spectroscopy of single molecules in a solid. Phys. Rev. Lett. 1989, 62, 2535−2538. (6) Betzig, E.; Patterson, G. H.; Sougrat, R.; Lindwasser, O. W.; Olenych, S.; Bonifacino, J. S.; Davidson, M. W.; Lippincott-Schwartz, J.; Hess, H. F. Imaging Intracellular Fluorescent Proteins at Nanometer Resolution. Science 2006, 313, 1642. (7) Rust, M. J.; Bates, M.; Zhuang, X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 2006, 3, 793−796. (8) Zanacchi, F. C.; Diaspro, A.: Fluorescence Photoactivation Localization Microscopy. In Encyclopedia of Biophysics; Roberts, G. C. K., Ed.; Springer Berlin Heidelberg: Berlin, Heidelberg, 2013; pp 812− 814. (9) Hell, S. W.; Wichmann, J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 1994, 19, 780−782. (10) Bailey, B.; Farkas, D. L.; Taylor, D. L.; Lanni, F. Enhancement of axial resolution in fluorescence microscopy by standing-wave excitation. Nature 1993, 366, 44−48. (11) von Diezmann, A.; Shechtman, Y.; Moerner, W. E. ThreeDimensional Localization of Single Molecules for Super-Resolution Imaging and Single-Particle Tracking. Chem. Rev. 2017, 10.1021/ acs.chemrev.6b00629 (12) Lee, A.; Tsekouras, K.; Calderon, C.; Bustamante, C.; Pressé, S. Unraveling the Thousand Word Picture: An Introduction to SuperResolution Data Analysis. Chem. Rev. 2017, 10.1021/acs.chemrev.6b00729. (13) Shen, H.; Tauzin, L.; Baiyasi, R.; Wang, W.; Moringa, N.; Shuang, B.; Landes, C. Single Particle Tracking: From Theory to Biophysical Applications. Chem. Rev. 2017. (14) Blom, H.; Widengren, J. Stimulated Emission Depletion Microscopy. Chem. Rev. 2017, 10.1021/acs.chemrev.6b00653. (15) Neil, M. A. A.; Juškaitis, R.; Wilson, T. Method of obtaining optical sectioning by using structured light in a conventional microscope. Opt. Lett. 1997, 22, 1905−1907. (16) Gustafsson, M. G. L. Extended resolution fluorescence microscopy. Curr. Opin. Struct. Biol. 1999, 9, 627−628. 7243

DOI: 10.1021/acs.chemrev.7b00242 Chem. Rev. 2017, 117, 7241−7243