Mussel-Inspired Dendritic Polymers as Universal Multifunctional Coatings

Article abstract of DOI:10.1002/anie.201407113

A rapid and universal approach for multifunctional material coatings was developed based on a mussel-inspired dendritic polymer. This new kind of polymer mimics not only the functional groups of mussel foot proteins (mfps) but also their molecular weight and molecular structure. The large number of catechol and amine groups set the basis for heteromultivalent anchoring and crosslinking. The molecular weight reaches 10 kDa, which is similar to the most adhesive mussel foot protein mfp-5. Also, the dendritic structure exposes its functional groups on the surface like the folded proteins. As a result, a very stable coating can be prepared on virtually any type of material surface within 10 min by a simple dip-coating method, which is as fast as the formation of mussel byssal threads in nature.

Full text of DOI:10.1002/anie.201407113

.
Angewandte
Communications
DOI: 10.1002/anie.201407113
Bioinspired Materials
Mussel-Inspired Dendritic Polymers as Universal Multifunctional
Coatings**
Qiang Wei, Katharina Achazi, Hendrik Liebe, Andrea Schulz, Paul-Ludwig Michael Noeske,
Ingo Grunwald, and Rainer Haag*
Dedicated to Professor Rolf Mꢀlhaupt on the occasion of his 60th birthday
Abstract: A rapid and universal approach for multifunctional
material coatings was developed based on a mussel-inspired
dendritic polymer. This new kind of polymer mimics not only
the functional groups of mussel foot proteins (mfps) but also
their molecular weight and molecular structure. The large
number of catechol and amine groups set the basis for
heteromultivalent anchoring and crosslinking. The molecular
weight reaches 10 kDa, which is similar to the most adhesive
mussel foot protein mfp-5. Also, the dendritic structure exposes
its functional groups on the surface like the folded proteins. As
a result, a very stable coating can be prepared on virtually any
type of material surface within 10 min by a simple dip-coating
method, which is as fast as the formation of mussel byssal
threads in nature.
specialized proteins including mfp-1, which is a key protein to
+
3
form the byssal cuticle and is usually crosslinked by Fe
[
11]
ions. Mfp-5, the most adhesive protein, is localized near the
[12]
interface between the plaques and the substrates. These
proteins contribute greatly to byssusꢀ rapid solidification and
adhesion. Both proteins contain a large quantify of 3,4-
dihydroxyphenyl-l-alanine (DOPA) 15 mol% and 28 mol%,
[
13]
respectively, as well as a high amount of lysine.
The
catechol group in DOPA forms strong covalent or non-
[
14]
covalent interactions with substrates for adhesion. In the
3
+
meantime, they can be coordinatively crosslinked with Fe
ions or covalently crosslinked by themselves or amine groups
[
15]
in lysines, which leads to solidification of the byssus.
However, a dopamine coating takes very long time to form
[
7]
a thick and dense film. Therefore, it is still necessary to
identify a better mimic of the mfps and further accelerate the
surface coating.
S
urface modification of solid materials plays an increasingly
important role in modern physical, chemical, biological, and
[
1,2]
materials science.
modification, such as self-assembled monolayer (SAM),
irradiation,
The common methods for surface
Herein we report on a heteromultivalent catechol- and
amine-functionalized dendritic polymer that mimics not only
the functional groups of mfp-1 and mfp-5 but also their
molecular weight and molecular structure, for a rapid and
universal surface coating by both covalent and coordinative
crosslinking (Scheme 1). Although many catecholic polymers
have already been developed for surface modification, the
majority of them are only linear polymers with a low density
[3]
[
4]
[5]
layer-by-layer assembly,
and Langmuir–
[
6]
Blodgett deposition, have worked effectively, but still
cannot modify a broad range of material surfaces. Mussel-
inspired surface chemistry is one of the most remarkable
methods to solve this problem. Dopamine and its derivatives,
which mimic the composition of mussel foot proteins (mfps),
can form surface-adherent films on virtually any material
[16]
of catechol groups. Individually catechol and amine groups
fail to induce significant oxidative polymerization. Both
catechol and amine functional groups must be presented to
[
7–9]
surface.
byssus as the holdfast. The formation of mussel byssal threads
Mussels adhere to solid surfaces with mfp-rich
[
10]
[17]
only needs approximately 3–10 min. Byssus have a set of
achieve universal and stable coatings. Furthermore, intra-
coating interactions have been less researched and rapid
coatings are still elusive. To solve this problem, dendritic
polyglycerol (dPG), which has a highly branched architecture,
exhibits a relatively distinct “interior”, and exposes functional
[
*] Q. Wei, Dr. K. Achazi, H. Liebe, A. Schulz, Prof. Dr. R. Haag
Department of Chemistry and Biochemistry, Freie Universitꢀt Berlin
Takustrasse 3, 14195 Berlin (Germany)
[
18]
E-mail: haag@chemie.fu-berlin.de
groups on its surface, just like folded proteins do, was used
[
19,20]
as a scaffold for multivalent anchoring and crosslinking.
Q. Wei, Prof. Dr. R. Haag
Multifunctional Biomaterials for Medicine
Helmholtz Virtual Institute
Kantstrasse 55, 14513 Teltow-Seehof (Germany)
The hydroxy groups present on the dPG scaffold were
converted into amine groups, 40% of them were further
functionalized by catecholic groups. The large amount of
remaining amine groups enhanced the intra-layer interaction
of the coatings, and afforded more functional groups for
secondary modifications of the coatings. In polydopamine,
most amine groups form indole rings or couple with quinone
groups by Michael addition and Schiffꢀs base reactions, thus
Dr. P.-L. M. Noeske, Dr. I. Grunwald
Fraunhofer Institute for Manufacturing Technology and Advanced
Materials (IFAM), Adhesive Bonding Technology and Surfaces
Wiener Strasse 12, 28359 Bremen (Germany)
[
**] This work was supported by the Helmholtz Virtual Institute and the
SFB 765. We thank Dr. Florian Paulus for synthesizing dPG, Dr. Paul
Wafula for the support in cell culture experiments, and Dr. Pamela
Winchester for proofreading this manuscript.
[
21,22]
becoming inactive.
The average molecular weight (M ) of
n
our mussel-inspired dPG (MI-dPG) is about 10 kDa, which is
[
23]
in the same range as the mfp-5 (ca. 9 kDa). Because of the
exposed multivalent functional groups and a suitable initial
Supporting information for this article is available on the WWW
under http://dx.doi.org/10.1002/anie.201407113.
1
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Chemie
Scheme 1. Top left: Structural formula of the mussel foot proteins mfp-1 and mfp-5 showing the alternating amino acids that contain amine (blue)
[12]
and catechol (red) units in their side chains. Top right: the chemical mimicry of synthesized mussel-inspired dendritic polyglycerol (MI-dPG).
Bottom: the covalent (postulated structure) and coordinative crosslinking for universal surface coatings. a) 0.1 mm MI-dPG in MeOH solution
À1
with 3-(N-morpholino)propanesulfonic acid (MOPS) buffer (4v/1v) at pH 8.5; b) 0.1 mm MI-dPG in MeOH solution with 0.54 mgmL FeCl3
3+
aqueous solution (4v/1v, catechol:Fe ꢀ6:1)
molecular weight, the MI-dPG can form a highly stable
coating on virtually all types of material surfaces within
immediately oxidized to quinones and subsequently cross-
linked with each other or amine groups by Michael addition
[15,23]
1
0 min or a micrometer scale coating in just hours by
or Schiffꢀs base reactions
under weak basic conditions.
polydopamine-type covalent crosslinking. Furthermore, a col-
orless mfp-1 type Fe coordinatively crosslinked coating has
been developed based on MI-dPG (Scheme 1).
The crosslinking process was monitored by IR spectroscopy
3
+
(Figure S2). The band for the deformational vibration of OÀH
À1
at about 1360 cm dramatically decreased in intensity after
Covalently crosslinked coatings were prepared by oxidiz-
ing catechols to quinones in a weak basic buffer near pH 8.5.
Though the mechanism of this crosslinking is still debated, it is
believed that covalent bonding is the main interaction,
hydrogen bonding and p-stacking are subsidiary interac-
the covalent crosslinking of MI-dPG, indicating that the
catechols may be oxidized to quinones. This assumption is
À1
supported by the strengthened signal at 1645 cm and
À1
À1
À1
weakened signal at 1602 cm . The 1645 cm
peak is
a characteristic signal for quinines. The 1602 cm peak can
[
21,22,24,25]
tions.
As analyzed by UV/Vis spectroscopy (Fig-
be explained by the valence vibration (C=C) of the phenyl of
ure S1, Supporting Information), catechol groups can be
the catechol groups. The weakened bands of the isolated H
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Angewandte
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À1
atom on the aryl ring at 912 cm and the ortho-H atom on the
À1
aryl ring at 845 cm further indicate the crosslinking of the
catechol moieties. Additionally, the change of the substitution
pattern of the aromatic systems was also shown by the signal
À1
between 729 and 814 cm . Owing to the strong crosslinking,
MI-dPG molecules rapidly aggregated in the solution (Fig-
ure S3) and spontaneously deposited on the solid surfaces,
including complex surface shapes (Figure S4). The MI-dPG
molecules can directly anchor to the substrate surface, then
other molecules can be immobilized to the first layer of
anchored molecules by crosslinking as a ꢁgrafting fromꢀ
approach. Meanwhile, the crosslinked aggregates can also
anchor to the surface via a ꢁgrafting toꢀ approach. The
thickness of the MI-dPG films rapidly increased during
incubation and reached 60 nm after 10 min and a maximum
value of 3.4 mm after 4 h on silica surfaces (Figure 1a). This
growth is much faster than the crosslinking of dopamine
[7,26]
coatings under basic and even oxidative conditions.
It
took 24 h to obtain a 50 nm dopamine coating under similar
[7]
basic conditions, and 2 h for a 70 nm dopamine coating in
[
26]
the more rigorous oxidative condition.
In the case of coordinatively crosslinked coatings, MI-
3
+
dPGs can be crosslinked by metal ions, such as Fe , which
prevents the rapid oxidation of catechols and forms a tris-
3
+
[27,28]
catechol Fe complex at pH 10.
About 1:6 equivalents of
3
+
Fe to catechol groups in MI-dPG was employed to induce
the crosslinking of the coatings. Thus half of the catechol
groups can form the complex for crosslinking. The remaining
half can still work as anchors. As a result of the fewer
crosslinking groups and related weak crosslinking, the thick-
ness of the coordination-based coatings only reached about
1
0 nm after 12 h of incubation (Figure 1b). Meanwhile, the
free catechols inside the coatings could be slowly oxidized to
cause the covalent crosslinking. Thus these coordinatively
crosslinked coatings were stable in a solution of ethylenedia-
minetetraacetic acid (EDTA) (Figure S5), which was able to
3
+
[27]
decompose the catechol Fe complex in solution.
The static water contact angles of both covalently and
coordinatively crosslinked MI-dPG-coated silica wafers
decreased with the incubation time, which is relevant for
the thickness of the coatings (Figure S6). Similar to the
thickness variation, the contact angles also reached the
equilibrium value. Various substrates that included metals
(
Al and TiO ), inorganic non-metals (SiO and glass), and
2 2
Figure 1. Time-dependent thickness of the a) covalently and b) coordi-
natively crosslinked MI-dPG coatings on silica surfaces. c) Average
static water-contact angle of the covalently (4 h) and coordinatively
polymers (polytetrafluoroethene (PTFE), polystyrene (PS))
were tested in the coating experiments (Figure 1c). Under
equilibrium conditions, the water contact angles on these
substrates reached to 20–308 for covalently crosslinked
coatings and were also dramatically altered for the coordina-
tively crosslinked coatings. This indicates that the original
wetting property of these substrates was completely changed
by the MI-dPG coatings. Moreover, the contact angles of both
covalently and coordinatively crosslinked MI-dPG coated
PTFE were hardly affected by incubating in PBS buffer for
(12 h) crosslinked MI-dPG coated surfaces. d) Optical transmittance
(wavelength 350–1000 nm) of the covalently and coordinatively cross-
linked coating.
indicated a dramatic change of signals for the respective
substrates compared to the bare surfaces (Table S1). The C, N,
and O compositions of the coated surfaces changed to the
values of the bulk MI-dPGs. This change suggests that the
composition of the MI-dPG coatings is independent of the
substrate. The coordinatively crosslinked coatings on PS
surfaces exhibited nearby the same signal changes for C, N,
and O as the covalently crosslinked coatings, but the addi-
tional Fe signal was detected.
1
month (Figure S7). This demonstrated the coatingsꢀ high
stability under physiological conditions.
X-ray photoelectron spectroscopy (XPS) analysis of four
kinds of surfaces (PS, PTFE, glass, and TiO ), which were
treated with covalently crosslinked coatings for 10 min,
2
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coatings must be combined with micro- and nano-metal
[
33]
particles to achieve these properties, whereas the covalent
crosslinked MI-dPGs can directly construct the lotus-like
coatings with hierarchical roughness. Therefore, bare glass
surfaces were alternately incubated in fresh MI-dPG solution
for 60 then 10 min. Initially, several micrometer-sized aggre-
gated clusters (Figure 2d) were formed on the substrates. In
the 10 min step, many nanometer-sized aggregated particles
(
Figure 2b) were formed on top of the micrometer-scale
aggregates which resulted in a hierarchically rough surface
Figure 3). The apparent water contact angle decreased to
(
Figure 2. Scanning electron microscopy (SEM) images of a) the bare
silica surface and the silica coated by covalently crosslinked MI-dPG
for b) 10 min, d) 60 min, and c) coordinatively crosslinked MI-dPG for
1
2 h (magnification 20000ꢁ).
The surface morphology for the two types of coatings was
observed by scanning electron microscopy (SEM). As shown
in Figure 2, the morphology of the silica surface was
completely altered to a rough structure by the MI-dPG
coatings, which confirms the hypothesis that the mussel-
inspired coatings were formed by crosslinked aggregates.
Large aggregates could be observed on the covalently cross-
linked coatings, and their size increased to the micrometer
scale over time. Much smaller aggregates were observed on
the coordinatively crosslinked coatings (The high-resolution
atomic force microscopy (AFM) images are shown in Fig-
ure S8). Their size was still observed in the nanometer range
after 12 hꢀ coating time. Note that a colorless coating was
achieved by coordinative crosslinking (Figure 1d), owing to
weak aggregation and low thickness. Only a very few
material-independent colorless coatings (for example, poly-
phenols and a mixture of 2-bromoisobutyryl-substituted
[29,30]
dopamine and dopamine) have been reported.
The
transmittance of the coordinatively crosslinked coatings
reached about 97% after 12 h of coating time. For compar-
ison, the transmittance of the covalent crosslinked coatings
already decreased to 90% after 5 min of coating and quickly
decreased to 68% after 10 min. After 60 min coating time the
transmittance reached only 12%.
Figure 3. a) Scheme of the MI-dPG constructed superhydrophilic or
perfluoroalkyl-functionalized superhydrophobic coatings. 1) 1 mgmL
heptadecafluoroundecanoyl chloride with 10 equiv of triethylamine
dissolved in diethyl ether. b) The surface morphology of the bare glass
and the superhydrophilic and superhydrophobic coatings on glass,
upper: magnification 1000ꢁ, lower: 20000ꢁ. c) The related static
water contact angle of the surfaces that shown above.
À1
MI-dPG coatings can be used as a universal modifiable
platform for various purposes. Functional molecules can be
added to the surface of the coatings or to the MI-dPG
molecules for a one-step coating (Figure S9). Besides cou-
pling thiol- or amine-containing molecules to catechol
near 08 for a superhydrophilic surface. After perfluoroalkyl-
functionalization, the surface morphology was not changed,
however, the water contact angle increased to about 166.58
[7,31]
groups,
other functional groups can be coupled to the
plenty of remaining amine groups in the coatings. Further-
more, the physical characteristics of the coatings can be
adjusted by the surface morphology which is controllable by
the size of the covalently crosslinked aggregates.
À1
and the surface energy reached about 0.5 mNm , which is in
the range of a superhydrophobic surface (Figure 3 and
[
34]
Table S2). Furthermore, the contact angle hysteresis was
only 6.68. Because of these properties, this coating, which has
been inspired by both natureꢀs water-repellent lotus leaf and
adhesive mussel foot proteins, can be potentially applied as
a new self-cleaning surface.
A hierarchical surface structure with two-tier (micro and
nano) roughness such as the micromorphology of a lotus leaf
shows superhydrophilic or superhydrophobic properties
[
32]
depending on their surface functionality.
Polydopamine
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Collagen A, which improves the adhesion of endothelial
ing. Standard HUVEC culture dishes, that is, collagen A
coated TCPS dishes, were used for comparison. After three
days of culturing, there were fewer cells observed (45.6 Æ
[35]
cells on surfaces, can be covalently bound to the MI-dPG
coatings by both amide and amine-catechol couplings. A
quartz crystal microbalance (QCM) with dissipation monitor-
ing was employed to determine the amount of collagen A that
2
13.2 mm ), because the adsorbed collagen A was not stable
on the TCPS in cell culture media and therefore could be
2
immobilized on the MI-dPG coatings. About 6.9 and
washed away by rinsing with buffer. Only 12.0 Æ 6.4 mm of
À2
7
.0 mgcm collagen A was immobilized on the covalent and
cells could be counted from the rinsed dishes, which was
similar for the cells on the bare TCPS. MI-dPG coatings
without immobilization of collagen A also improved the
the coordinative coatings, respectively, after washing by
sodium dodecyl sulfate (SDS) 1% (w/w) aqueous solution
Figure S10). The coupling reagents N-hydroxysuccinimide
NHS) and 1-ethyl-3-(3-dimethylaminopropyl)carbodiimide
EDC) may cause slight crosslinking of the proteins, but as the
2
(
(
(
attachment of HUVEC (33.2 Æ 7.2 and 30.0 Æ 9.6 mm of cells
on covalently and coordinatively crosslinked coatings, respec-
tively) but not so significant. This demonstrates that MI-dPG
coating has as good cytocompatibility as already shown for
experimental results show the effectivity of the proteins was
not hindered. For comparison, quite a small amount of
[
36]
polydopamine coatings.
À2
collagen A (0.1 mgcm ) was adsorbed on the bare polystyr-
In summary, we developed a new mussel-inspired den-
dritic polyglycerol (MI-dPG) that effectively mimics mussel
foot proteins with regard to their functional groups, molecular
weight, and molecular structure. Compared to the first
generation of mussel-inspired coating material, polydop-
amine, this new MI-dPG benefits from its heteromultivalent
character and molecular weight, which provide a strong
adhesive power. It can rapidly adhere on virtually all kinds of
material surfaces and form a thick film by covalent cross-
linking within 10 min, which is close to the time of byssal
thread formation in nature. Meanwhile, ion-based coordina-
tive crosslinking of MI-dPG generated thin and colorless
coatings. Until now only polyphenol tannic acid achieved
ene surfaces, after washing by SDS 1% (w/w) solution.
After culturing human umbilical-vein endothelial cells
HUVECs) for 3 days (Figure 4 and Figure S11), only a few
(
cells could be observed on bare-tissue culture polystyrene
À2
(
TCPS) surfaces (11.2 Æ 4.8 cellsmm ). In contrast, a large
number of cells had been attached to both the collagen A
immobilized covalently crosslinked and coordinatively cross-
linked MI-dPG coated TCPS surfaces (101.2 Æ 22.8 and
À2
6
2.0 Æ 17.2 cellsmm , respectively) with a regularly spread-
[
37]
similar coatings. Furthermore, the multiple active groups in
the coatings and the controllable surface morphology could
induce many kinds of secondary modification for diverse
functional applications.
Besides catecholic surface chemistry, mussels employ
Mfp-6 to reduce quinones back to catechols to adjust the
[
38]
binding and crosslinking, and Mfp-3 “slow” (Mfp-3s) to
enhance the hydrophobic interaction because of the facile
[39]
autoxidation of catechols. The adhesion of mussel byssus,
however, is more complicated than a simple catechol-
mediated recipe. Therefore, the biomimicry of mussels will
continue to be a source of inspiration.
Received: July 11, 2014
Published online: September 8, 2014
Keywords: bioinspired materials · dendrimers ·
.
multifunctionalization · polymers · surface chemistry
[
[
1] S. R. Meyers, M. W. Grinstaff, Chem. Rev. 2012, 112, 1615 – 1632.
2] Q. Wei, T. Becherer, S. Angioletti-Uberti, J. Dzubiella, C.
Wischke, A. Neffe, A. Lendlein, M. Ballauff, R. Haag, Angew.
Chem. Int. Ed. 2014, 53, 8004 – 8031; Angew. Chem. 2014, 126,
8138 – 8169.
[
3] C. D. Bain, G. M. Whitesides, Science 1988, 240, 62 – 63.
Figure 4. a) Scheme of post-functionalization with collagen Abny
[4] M. Ulbricht, M. Riedel, U. Marx, J. Membr. Sci. 1996, 120, 239 –
259.
[5] G. Decher, Science 1997, 277, 1232 – 1237.
[6] G. L. Gaines, R. W. Roberts, Nature 1963, 197, 787 – 788.
[7] H. Lee, S. M. Dellatore, W. M. Miller, P. B. Messersmith, Science
2007, 318, 426 – 430.
À1
amide bonding to MI-dPG coatings. 1) 0.1 mgmL collagen A,
À1
À1
0
.01 mgmL N-hydroxysuccinimide (NHS), and 0.01 mgmL 1-ethyl-
3
-(3-dimethylaminopropyl)carbodiimide (EDC) in PBS buffer for 4 h.
b) Human umbilical-vein endothelial cell (HUVEC) adhesion on bare
and collagen A modified tissue-culture polystyrene (TCPS) surfaces
after 3 days culturing. c) HUVEC numbers on bare and different
functionalized TCPS surfaces after 3 days culturing (*: p<0.0001).
[8] S. M. Kang, J. Rho, I. S. Choi, P. B. Messersmith, H. Lee, J. Am.
Chem. Soc. 2009, 131, 13224 – 13225.
1
1654 www.angewandte.org
ꢀ 2014 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
Angew. Chem. Int. Ed. 2014, 53, 11650 –11655

Angewandte
Chemie
[
9] D. R. Dreyer, D. J. Miller, B. D. Freeman, D. R. Paul, C. W.
[25] S. Hong, Y. S. Na, S. Choi, I. T. Song, W. Y. Kim, H. Lee, Adv.
Bielawski, Chem. Sci. 2012, 4, 3796 – 3802.
Funct. Mater. 2012, 22, 4711 – 4717.
[
[
10] J. H. Waite, Results Probl. Cell Differ. 1992, 19, 27 – 54.
11] M. J. Harrington, A. Masic, N. Holten-Andersen, J. H. Waite, P.
Fratzl, Science 2010, 328, 216 – 220.
12] E. W. Danner, Y. J. Kan, M. U. Hammer, J. N. Israelachvili, J. H.
Waite, Biochemistry 2012, 51, 6511 – 6518.
13] B. P. Lee, P. B. Messersmith, J. N. Israelachvili, J. H. Waite,
Annu. Rev. Mater. Res. 2011, 41, 99 – 132.
14] H. Lee, N. F. Scherer, P. B. Messersmith, Proc. Natl. Acad. Sci.
USA 2006, 103, 12999 – 13003.
[26] Q. Wei, F. L. Zhang, J. Li, B. J. Li, C. S. Zhao, Polym. Chem.
2010, 1, 1430 – 1433.
[27] N. Holten-Andersen, M. J. Harrington, H. Birkedal, B. P. Lee,
P. B. Messersmith, K. Y. C. Lee, J. H. Waite, Proc. Natl. Acad.
Sci. USA 2011, 108, 2651 – 2655.
[28] H. Xu, J. Nishida, W. Ma, H. Wu, M. Kobayashi, H. Otsuka, A.
Takahara, ACS Macro Lett. 2012, 1, 457 – 460.
[29] M. Kohri, H. Kohma, Y. Shinoda, M. Yamauchi, S. Yagai, T.
Kojima, T. Taniguchi, K. Kishikawa, Polym. Chem. 2013, 4,
2696 – 2702.
[30] T. S. Sileika, D. G. Barrett, R. Zhang, K. H. A. Lau, P. B.
Messersmith, Angew. Chem. Int. Ed. 2013, 52, 10766 – 10770;
Angew. Chem. 2013, 125, 10966 – 10970.
[31] Q. Wei, B. J. Li, N. Yi, B. H. Su, Z. H. Yin, F. L. Zhang, J. Li, C. S.
Zhao, J. Biomed. Mater. Res. Part A 2011, 96, 38 – 45.
[32] X. J. Feng, L. Jiang, Adv. Mater. 2006, 18, 3063 – 3078.
[33] L. Zhang, J. J. Wu, Y. X. Wang, Y. H. Long, N. Zhao, J. Xu, J.
Am. Chem. Soc. 2012, 134, 9879 – 9881.
[
[
[
[
[
15] L. A. Burzio, J. H. Waite, Biochemistry 2000, 39, 11147 – 11153.
16] E. Faure, C. Falentin-Daudrꢂ, C. Jꢂrꢃme, J. Lyskawa, D.
Fournier, P. Woisel, C. Detrembleur, Prog. Polym. Sci. 2013,
3
8, 236 – 270.
17] J. R. Jeon, J. H. Kim, Y. S. Chang, J. Mater. Chem. B 2013, 1,
501 – 6509.
18] M. Calderꢄn, M. A. Quadir, S. K. Sharma, R. Haag, Adv. Mater.
010, 22, 190 – 218.
[
[
[
6
2
19] C. Fasting, C. A. Schalley, M. Weber, O. Seitz, S. Hecht, B.
Koksch, J. Dernedde, C. Graf, E. W. Knapp, R. Haag, Angew.
Chem. Int. Ed. 2012, 51, 10472 – 10498; Angew. Chem. 2012, 124,
[34] X. Zhang, F. Shi, J. Niu, Y. Jiang, Z. Wang, J. Mater. Chem. 2008,
18, 621 – 633.
1
0622 – 10650.
[35] G. A. Di Lullo, S. M. Sweeney, J. Korkko, L. Ala-Kokko, J. D.
San Antonio, J. Biol. Chem. 2002, 277, 4223 – 4231.
[36] K. Kang, I. S. Choi, Y. Nam, Biomaterials 2011, 32, 6374 – 6380.
[37] H. Ejima, J. J. Richardson, K. Liang, J. P. Best, M. P. van Koe-
verden, G. K. Such, J. W. Cui, F. Caruso, Science 2013, 341, 154 –
157.
[
[
[
20] Q. Wei, T. Becherer, P.-L. M. Noeske, I. Grunwald, R. Haag,
Adv. Mater. 2014, 26, 2688 – 2693.
21] N. F. Della Vecchia, R. Avolio, M. Alfꢅ, M. E. Errico, A.
Napolitano, M. dꢀIschia, Adv. Funct. Mater. 2013, 23, 1331 – 1340.
22] J. Liebscher, R. Mrꢄwczy n´ ski, H. A. Scheidt, C. Filip, N. D.
H a˘ dade, R. Turcu, A. Bende, S. Beck, Langmuir 2013, 29,
[38] J. Yu, W. Wei, E. Danner, R. K. Ashley, J. N. Israelachvili, J. H.
Waite, Nat. Chem. Biol. 2011, 7, 588 – 590.
10539 – 10548.
[
[
23] M. J. LaVoie, B. L. Ostaszewski, A. Weihofen, M. G. Schloss-
macher, D. J. Selkoe, Nat. Med. 2005, 11, 1214 – 1221.
24] D. R. Dreyer, D. J. Miller, B. D. Freeman, D. R. Paul, C. W.
Bielawski, Langmuir 2012, 28, 6428 – 6435.
[39] W. Wei, J. Yu, C. Broomell, J. N. Israelachvili, J. H. Waite, J. Am.
Chem. Soc. 2013, 135, 377 – 383.
Angew. Chem. Int. Ed. 2014, 53, 11650 –11655
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