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NATURE METHODS | ADVANCE ONLINE PUBLICATION | 1
isoforms. Nanobody-mediated targeting of organic dyes to GFP-
fusion constructs would combine the molecular specificity of
genetic tagging with the high photon yield of organic dyes and
minimal linkage error.
We covalently coupled anti-GFP nanobodies to Alexa Fluor
647 (AF647) and added them to MDCK cells expressing GFP
anchored via glycosylphosphatidylinositol to the plasma mem-
brane (GPI-GFP). The nanobodies bound to transfected cells
readily at low concentrations but did not bind to untransfected
cells (Supplementary Fig. 1). Labeled nanobodies exhibited
highly specific and saturable binding at about 0.6 nanobodies
per GFP (Online Methods).
Under specific buffer conditions, many organic dyes become
photoswitchable
6,7
. This fact is the basis for several single-molecule
nanoscopy approaches
2–4
. To compare the nanobody-based approach
to established methods, we labeled microtubules in fixed Ptk2 cells
that stably expressed tubulin-YFP with AF647–anti-GFP nanobod-
ies and imaged these cells by single-molecule nanoscopy. Individual
microtubules were densely labeled with a full-width half maximum
(FWHM) of 26.9 nm 3.7 nm (s.d.) (Fig. 1a), compatible with a
microtubule diameter of 25 nm. This was significantly less (Fig. 1a)
than what we achieved in parallel experiments using AF647-coupled
secondary antibodies to detect microtubules either via anti-GFP
(42.7 nm 7.0 nm) or anti-tubulin (45.6 nm 5.8 nm) antibodies,
suggesting that the use of nanobodies led to minimal linkage error.
We next used the bright AF647–anti-GFP nanobodies for
three-dimensional single-molecule nanoscopy with the bi-plane
method
8
, which requires thousands of detected photons for good
axial resolution. Nanobody-mediated labeling of microtubules
in Ptk2 cells allowed us to resolve crossing microtubules with an
axial separation of ~100 nm (Fig. 1b).
The use of bright labels not only increased localization preci-
sion (statistics in Supplementary Fig. 2), but also allowed the
high frame rates required for imaging dynamic (live) samples.
To realize this advantage, we transiently expressed GPI-GFP
in primary hippocampal rat neurons and detected it via AF647–
anti-GFP nanobodies. Single-particle tracking PALM (sptPALM)
9
allowed us to follow the trajectories of hundreds of molecules in
the neuronal plasma membrane. We assembled a time series of
super-resolution images and detected dynamic changes in the
neuronal morphology over time (Fig. 1c).
Next, we used nanobodies for dual-color imaging. We realized
this approach by using anti-GFP nanobodies labeled with Alexa
Fluor 700 (AF700) and anti-RFP nanobodies (that also recognize
monomeric (m)Cherry) labeled with AF647. We then labeled CV-1
cells expressing Septin7-mCherry and Caveolin1-YFP with these
labels and could image both structures with high resolution and
specificity (Fig. 1d).
A simple, versatile
method for GFP-based
super-resolution
microscopy via nanobodies
Jonas Ries, Charlotte Kaplan, Evgenia Platonova,
Hadi Eghlidi & Helge Ewers
We developed a method to use any GFP-tagged construct in
single-molecule super-resolution microscopy. By targeting
GFP with small, high-affinity antibodies coupled to organic
dyes, we achieved nanometer spatial resolution and minimal
linkage error when analyzing microtubules, living neurons and
yeast cells. We show that in combination with libraries
encoding GFP-tagged proteins, virtually any known protein
can immediately be used in super-resolution microscopy and
that simplified labeling schemes allow high-throughput super-
resolution imaging.
The single-molecule localization–based super-resolution imag-
ing techniques such as photoactivated localization microscopy
(PALM) and stochastic optical reconstruction microscopy
1–4
(here referred to as ‘single-molecule nanoscopy’) require specific
and efficient delivery of bright fluorophores into close proximity
of the target structure without adding substantial background.
Present labeling techniques usually involve a tradeoff between
these properties. Bright organic dyes can be delivered via anti-
bodies, but their large size displaces the dye from the target in a
‘linkage error’ of ~10 nm, and highly specific antibodies are avail-
able only for some proteins. Methods based on photoactivatable
fluorescent proteins or enzymatic labeling schemes demand the
generation of new fusion constructs, which should be character-
ized and may not be functional.
We demonstrate a simple, efficient and versatile method that
optimizes several labeling parameters and can be used with any of
the thousands of functionally tested GFP constructs available. We
used very small and high-affinity camelid antibodies (nanobod-
ies) to GFP
5
to deliver bright organic fluorophores to GFP-tagged
proteins for use in single-molecule nanoscopy.
Organic dyes are conventionally delivered to target struc-
tures via antibodies, which are ~150 kDa, ~10 nm in size and
of varying affinity. In contrast, the 13-kDa anti-GFP nanobod-
ies are smaller (1.5 nm × 2.5 nm) and have a high affinity for
GFP (0.59 nM; ref. 5; Supplementary Fig. 1) and several of its
Institute of Biochemistry and Laboratory of Physical Chemistry, ETH Zurich, Zurich, Switzerland. Correspondence should be addressed to H.Ewers (helge.ewers@bc.biol.ethz.ch).
RECEIVED 2 DECEMBER 2011; ACCEPTED 28 MARCH 2012; PUBLISHED ONLINE 29 APRIL 2012; DOI:10.1038/NMETH.1991