Target with precision. · Silent Sparks The Wondrous World of Fireflies Sara Lewis Cloth $29.95...
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Upcoming Features
Exosomes/MicrovesiclesóJune 10
ProteomicsóJuly 15
GenomicsóOctober 7
LIFE SCIENCE TECHNOLOGIES
SUPERRESOLUTION MICROSCOPY
The latest superresolution
microscopes (GSDIM, PALM, SIM,
STED, STORM) bend a centuries-old
rule in the �eld as well as researchersí
minds on cellular structures they
thought they knew.
See the full story on page 850.
Superresolutionmicroscopy
850 sciencemag.org/custom-publishing SCIENCE
LIFE SCIENCE TECHNOLOGIES
SUPERRESOLUTION MICROSCOPY
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No, there hasnít been a breakdown in copy editing,
this sentence really does end with two periods..
Your brain caught that apparent mistake because
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power to distinguish objects spaced that close together.
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constrains the microscopeís power, and at some point, two
objects will appear as one.
In 2006, Xiaowei Zhuangís team at Harvard UniversityF���CF
described the superresolution technique known as stochastic
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the technique to make it multicolor, higher resolution, and 3D.
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Zhuang, a Howard Hughes Medical Institute Investigator and
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tion, light arising from a single molecule produces not a circle
but an ellipse, which indicates the moleculeís axial position
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further by positioning objectives above and below the sample,
which when combined with the cylindrical lens yielded axial
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campal neurons, they discovered something completely unex�
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copy, actin in the axons of these neurons appears as a uniform,
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beneath the plasma membrane of the axonal shaft they discov�
ered a literal cytoskeleton: periodic rings of green actin 180 nm
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cell can precisely position key membrane proteins, such as
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pulses. ìHaving these very important signaling molecules being
anchored on the structure gives you the possibility that this is
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Biology and Biomedical Engineering at the Yale University
School of Medicine, who builds superresolution microscopes
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body had seen these actin rings before, even though people
had looked with the electron microscope for 20 years to under�
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Superresolution explained
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the same fundamental principle.
ìIf you have freely propagating light, that light will always be
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and ground state depletion microscopy with individual
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and Leica�F�E��E�C�E��A��EF�C��D��C���F��������C����
based methods, using photoactivatable or photoswitchable
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at random while the majority remain dark. Under those
conditions, researchers can be relatively certain that
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molecule, thus making it possible to assign their positions
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complete dataset has been collected.
ìBasically we take advantage of what I typically call the
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Exosomes/MicrovesiclesóJune 10 ProteomicsóJuly 15 GenomicsóOctober 7
Upcoming Features
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ability to resolve two objects is constrained by the wavelength
of the light used to view them. But in 2000, researchers showed
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the next decade an alphabet soup of superresolution tech�
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resulting images are both beautiful and revealing, documenting
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LIFE SCIENCE TECHNOLOGIES Produced by the Science/AAAS Custom Publishing Office
SUPERRESOLUTION MICROSCOPY
like an optical zoom,î explains Silvio Rizzoli, a professor at the
University of Gˆttingen, Germany, who uses this technique (as
well as STED and STORM) in his neural synapse research.
���������������������������
Stefan Jakobs, head of the Mitochondrial Structure and
Dynamics Research Group at the Max Planck Institute for
Biophysical Chemistry, uses superresolution methodologies to
study the role mitochondria play in cell death or apoptosis. One
protein, called Bax, was known to induce mitochondrial mem-
brane disruption in response to apoptotic signals. What wasnít
clear was how the protein does that.
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Bax molecules assemble into rings in the mitochondrial outer
membrane, like diaphanous green halos crowning the red mem-
brane. That structure explains how Bax translocation during
apoptosis can cause the mitochondrial contents to spill, Jakobs
says. ìIt appears that these rings represent pores,î he explains.
Yet they were impossible to discern via conventional micros-
copy, in which the rings appear as ìa smear.î
To see those rings, Jakobs used anti-Bax antibodies labeled
��������78������������ ����88���78���������8���!8��7���-
resolution microscopy can be hard to come by. ìYou want to
have fast image acquisition and high resolution; you want to
have many colors and low phototoxicity. None of the tech-
niques is currently at the point where all of these parameters
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wavelengths of light. Such proteins are amenable to RESOLFT
and STED live-cell applications, he notes, as they require no
external antibody for labeling. But it is critical not to overex-
press these proteins, he says, as that can lead to artifacts. So,
Jakobsís team has used the gene-editing system known as
CRISPR/Cas9 to couple rsEGFP2 to protein-coding genes in
order to ensure endogenous expression levels. Such work is
ìchallenging,î he admits, ìbut I think it is very important for the
�6�����������8������"�
Another genetic labeling option involves tagging genes with
self-labeling protein tags, such as the SNAP-tag and CLIP-tag
(available from New England BioLabs) or Promegaís
indistinguishable objects are closely positioned in space, she
says, ìwe donít allow them to overlap in time.î
Stimulated emission depletion (STED), reversible saturable
8�����6��78���������������8��$%��+,5�'��������7��7�����6-
lumination microscopy (SIM), conversely, use ìpatterns of light
Ö that determine where the molecules are active and where
�����86��76������8��"����-�66����8���#�68�����8��������
and RESOLFT and cofounded a company called Abberior to
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tion methods. STED, for instance, is usually implemented as a
point-scanning approach that uses a ìdonutî of light, super-
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periphery of the illumination volume to stay dark via a process
called ìstimulated emission,î thereby shrinking the emitting
region to the donutís center. (RESOLFT uses photoswitchable
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According to Jochen Sieber, STED and GSDIM microscopy
product manager at Leica Microsystems, localization systems
������66��8�������������867��8������������8��%��+,5����7��
take far longer as they require the acquisition and merging of
thousands of frames to build a single image. (Indeed, National
Institutes of Health Distinguished Investigator Jennifer Lip-
pincott-Schwartz, in whose lab PALM was invented, notes that
��8�� ����������88���87���8��866���/��8��������������6�!�����
rate is about 5 minutes.)
SIMócommercialized by Nikon, GE Healthcare Life Scienc-
es, and Zeissóis generally regarded as the fastest approach
available and also the easiest, as it requires no special sample
preparation. But at 100 nm, it also yields the poorest resolution.
Recently, Janelia Research Campus Investigator Eric
0��.������8������-�66�����1�66�������28������8!�����!8�����-
versity won the 2014 Nobel Prize in Chemistry for his work
on superresolution, demonstrated that even that limit is not
insurmountable. In late 2015, Betzig and his team documented
two strategies, including ìnonlinear SIM with patterned activa-
tion,î to increase the methodís resolution to about 45 nm. ìMy
personal feeling is that SIM is the superresolution method that
is likely to answer the most biological questions in the next de-
cade,î Betzig says, laughing. ìAnd yet itís the one that wasnít
involved in the Nobel Prize.î
Raman Das, Medical Research Council (MRC) Career De-
velopment Fellow at the University of Manchester, United
Kingdom, answered one such question in 2014 when he used
SIM (among other methods) to document a new form of cell
subdivision called ìapical abscission.î Das was interested in
�8����8�����8����66�������������8��������6��8����������������
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those proteins in one shotóa process that Das likens to closing
a draw-string purse. ìThis results in an acute loss of cell polar-
ity in these cells,î he explains, leading to the formation of func-
tional neuronal architecture.
Perhaps the simplest, and certainly least expensive, super-
resolution option is expansion microscopy. Developed by Ed
Boyden of the Massachusetts Institute of Technology, the
technique improves imaging resolution by encasing samples in
a ìswellable polymerî gel that causes the sample to grow iso-
��8����66����87�� #�!86��6�������57����8��66�������������������
increasing resolution from 200 nm down to 40 nm. ìItís kind of IMA
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When [Zhuangís team] used STORM to zoom in, just beneath
the plasma membrane of the axonal shaft they discovered
a literal cytoskeleton: periodic rings of green actin 180 nm
apart, separated by magenta spectrin spacers.
cont.>
852 sciencemag.org/custom-publishing SCIENCE
LIFE SCIENCE TECHNOLOGIES
SUPERRESOLUTION MICROSCOPY
Produced by the Science/AAAS Custom Publishing Office
One solution is replacing traditional charge-coupled devices
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semiconductor (sCMOS) cameras, which can capture thou-
sands of frames per second. In 2013, Bewersdorf and col-
leagues demonstrated noise-handling algorithms that allowed
an sCMOS camera to record superresolved images at up to 32
frames per second, for instance. Today, Leicaís GSDIM instru-
ment includes an sCMOS camera that reduces data acquisition
times to ìwell below a minute,î says product manager Peter
Laskey, thus putting live-cell applications ìwithin reach.î So too
does Nikonís new N-STORM 4.0, which also boasts a brighter
��?�������������������������������?���������������������
ing to general manager Stephen Ross.
Researchers also have devised alternative strategies to
circumvent the speed problem. Melike Lakadamyali, a group
leader at the Institute of Photonic Sciences in Barcelona,
�������������?������?���?�������������?�����������������?��
�� ��������������������������?�����?����������?��?���?�����
������������?������������ ��?����������������������
of a living cell.î
To answer that question, Lakadamyali plays to her systemís
strengths. By recording a live-cell movie of the vesicles at high
temporal (but low spatial) resolution, her team can track vesicle
���������������������?���� �����?�������!"#$���������
microtubule positions.
The researchers found that vesicles tend to pause at mi-
crotubule intersections; the pausing ìcorrelates with tight in-
tersections in which the separation of the two microtubules is
small,î says Lakadamyali. But they also found that motors can
eventually navigate through the intersection. The group is now
using 3D particle tracking to focus on microtubule-associated
����� ������?���������������������������������?����������
skirting roadblocks.
��?���=����#������������%����?����#?�����&��������
Kingís College London, is similarly interested in live-cell local-
�'�����������?����(�)������������*�����������������'��=�����?�
developed an algorithm, called ìBayesian analysis of blinking
and bleaching (3B),î that allows researchers to image more
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tially overlapping, thereby reducing the number of images re-
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looked at systems like cardiac myocytes, [and] been able to
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Still, for all that high resolution can teach, microscopy is
�������������?(�/������?��0�'���?��?��������������?����?���
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his samples. Thatís why he has edged away from pure super-
resolution toward ultrahigh-speed imaging with a new (albeit
superresolution-compatible) design called ìlattice light-sheet
microscopy,î soon to be commercialized by Zeiss and 3i. "���?������������������������������������������?(�
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future has never looked brighteróor sharper.
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of interest in live cells by adding cell-permeable dyes linked
to the appropriate substrate. The trick, of course, is that such
dyes must be both bright and cell-permeable, and few current
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at the Institute of Chemical Sciences and Engineering at
…cole Polytechnique FÈdÈrale de Lausanne in Switzerland.
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rhodamine variants, which are compatible with HaloTag chem-
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commercialized by Spirochrome.
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Featured Participants
Massachusetts Institute of Technologywww.mit.edu
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