Introducing structural flexibility into porphyrin-DNA zipper arrays

Article abstract of DOI:10.1039/c0ob00535e

A more flexible nucleotide building block for the synthesis of new DNA based porphyrin-zipper arrays is described. Changing the rigid acetylene linker between the porphyrin substituent and the 2′-deoxyuridine to a more flexible propargyl amide containing

Full text of DOI:10.1039/c0ob00535e

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PAPER
www.rsc.org/obc | Organic & Biomolecular Chemistry
Introducing structural flexibility into porphyrin–DNA zipper arrays†
Ashley Brewer,a Guiliano Siligardi,b,c Cameron Neylond and Eugen Stulz*a
Received 4th August 2010, Accepted 12th October 2010
DOI: 10.1039/c0ob00535e
A more flexible nucleotide building block for the synthesis of new DNA based porphyrin–zipper arrays
is described. Changing the rigid acetylene linker between the porphyrin substituent and the
2¢-deoxyuridine to a more flexible propargyl amide containing linkage leads in part to an increased
duplex stability. The CD spectra reveal different electronic interactions between the porphyrins
depending on the type of linker used. Molecular modelling suggests large variation of the relative
orientation of the porphyrins within the major groove of the DNA. The porphyrins can be metallated
post-synthetically with different metals as shown with zinc, cobalt and copper. The spectroscopic
features do not alter drastically upon metallation apart from the CD spectra, and the stability of the
metal complex is highly dependent on the nature of the metal. As shown by CD spectroscopy, the zinc
porphyrin is rapidly demetallated at high temperatures. Globular structure determination using SAXS
indicates that a molecular assembly comprised of a two to four helical bundle dominates in solution at
higher concentrations (≥50 mM) which is not observed by spectroscopy at lower concentrations (£1 mM).
to create DNA bundles and tubes,33,34 to form porphyrin dimers
Introduction
through hybridisation,35 or as chiral markers for the analysis of
DNA structure by CD spectroscopy.36,37
The synthesis of electronically active organic molecules on the
macromolecular scale1 is of major interest due to their promising
applications in light harvesting devices,2 photovoltaics,3 logic
gates4 and molecular wires.5 The limiting factor in the development
and refinement of these systems is often the speed of fabrication,
since the introduction of a minor change to the final compound
may dictate a completely different synthetic pathway. One solution
to this is the development of modular building blocks, whereby
the system as a whole can be tweaked and optimized through
the relatively facile substitution of a different building block
during the synthesis. Nature provides us with an abundant, easily
modified6,7 scaffold upon which to base our building blocks,
namely DNA. A great deal of research has been conducted
on modified DNA,8–12 with many different electronically active
molecules being covalently bound, for instance; pyrenes and
perylenes,13–16 and metallated bipyridines,17,18 to name but a few.
Many of these systems show efficient energy or electron transfer
between donor and acceptor groups.19–23 Our focus, however, is
on the multiple attachments of porphyrins to the DNA scaffold.
Porphyrins are an ideal choice for this purpose due to the facile
tunability of their electronic properties through modification of
the attached substituents or through metallation of the porphyrin
macrocycle,24 and they can easily be attached to a variety of
scaffolds.25–32 Other groups have used porphyrin–DNA constructs
Previous research in our group has focused on tetraphenyl
porphyrin (TPP, 1)38 or diphenyl porphyrin (DPP)39 moieties
connected via a rigid acetylene linker (Fig. 1).40,41 Positioning
all modifications on one strand leads to a destabilization of the
duplex,38,42 whereas when positioned on alternate strands (creating
a zipper system) the modifications provide a significant degree of
stabilization to the system,11,43 similar to other reported zipper-
DNA arrays.44–46 Here we present a zipper–porphyrin system with
a new linker to the nucleobase (2) which leads to a greater flexibility
in the porphyrin arrangement, and explore different metallation
states of the porphyrin arrays.
aSchool of Chemistry, University of Southampton, Highfield, Southampton,
UK, SO17 1BJ. E-mail: est@soton.ac.uk; Fax: +44-(0)23 80 59 68 05;
Tel: +44-(0)23 80 59 93 69
bDiamond Light Source, Harwell Science and Innovation Campus, Didcot,
Oxfordshire, UK, OX11 0DE
Fig. 1 Acetylene (1) and amide (2) linked building blocks, and synthesized
DNA strands.
cSchool of Biological Sciences, University of Liverpool, Liverpool, UK, L69
3BX
Results and Discussion
dScience and Technology Facilities Council, Rutherford Appleton Labora-
tory, Harwell Science and Innovation Campus, Didcot, UK, OX11 0QX;
Web: www.cameronneylon.net.
Synthesis of the building blocks and porphyrin–DNA
† Electronic supplementary information (ESI) available: Synthesis meth-
ods, molecular modelling, full spectroscopic analysis (UV-Vis, fluorescence
and CD studies). See DOI: 10.1039/c0ob00535e
The acetylene linked porphyrin building block 1 is readily obtained
via Sonogashira coupling between the acetylene porphyrin and
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5-iodo-2¢-deoxyuridine (5-I-dU).38 To synthesize nucleotide 2,
first propargylamine is coupled to 5-I-dU to obtain the amine
functionalised nucleoside (Scheme 1, Scheme S1, ESI†). It should
be noted that protection of the propargylamine (e.g. with Fmoc)
is not necessary. The coupling of the amino nucleoside with
the corresponding monocarboxylic acid functionalised porphyrin
proceeds smoothly using standard peptide coupling chemistry
(EDC, HOBt, DMAP), and the amide linked porphyrin-dU is
obtained in 80% yield. The free-base porphyrins were converted
into the phosphoramidite nucleosides for automated DNA syn-
thesis according to our protocols described earlier.38,39 Fig. 1 lists
the DNA strands that were synthesized in order to study the
influence of the new linker on structure and stability. The DNA
single strands contain only one type of linker, i.e. an acetylene or
an amide linker, but upon hybridization the different linkers can
be mixed in the zipper arrays. Three porphyrin modified DNA
duplexes were synthesised, where both strands contained either
the acetylene linker (3·4) or the amide linker (5·6), and a hybrid
system whereby one strand contained the acetylene linker while
the other contained the amide linker (3·6). These systems have
been designed to incorporate a ‘sticky end’ of eight bases at either
end of the duplex for potential hybridization of other functional
DNA strands.
Duplex stability of porphyrin–DNA
Two solvent systems (100% phosphate buffer and 9 : 1 phosphate
buffer : DMF) were used for UV-Vis and fluorescence melting
studies since discrete transitions for all systems in one solvent
system were not observed; in some cases the melting transitions
were much clearer when DMF was added to the system. The
inclusion of 10% DMF in the buffer leads to a lowering of the
duplexes’ Tm (see 7·8), DTm values were calculated with respect to
the unmodified duplex’s (7·8) Tm in the appropriate solvent.
Unexpectedly a stabilising effect is observed in duplexes con-
taining only one modified strand (3·8, 4·7, 5·8 and 6·7) and one
natural complementary strand, which is observed in UV-melting
and fluorescence-melting studies in both 100% buffered aqueous
solvent and 9 : 1 buffer : DMF. The stabilization can be as large as
+8.9 ◦C. The stabilizing effect of the porphyrins on these strands
in aqueous buffer is 4.1 ◦C to 6.1 ◦C, while the same systems
in 9 : 1 buffer : DMF show a stabilizing effect of 7.6 ◦C to 8.9
◦C; the porphyrin modified DNA appears to be less sensitive
to the destabilizing effect of DMF than natural DNA. Samples
5·8 and 6·7 also demonstrate that the difference in Tm between
UV melting studies and fluorescence melting studies is 2–3 ◦C,
with fluorescence melting studies giving the higher Tm value. The
stabilizing effects observed here could indicate a favorable pre-
organization of these strands towards the B-type duplex DNA.
Porphyrins have been shown to be able to stabilize an induced
helical structure in the single strands.38 Interestingly this effect has
a large positive effect on the duplex stability, presumably due to the
attachment of the porphyrins onto alternating bases rather than in
a continuous manner on each nucleotide as studied previously.38
The melting studies (Fig. 2 and Table 1) demonstrate a
stabilising effect of +0.3 ◦C to +0.4 ◦C per porphyrin modification
for duplexes containing two modified strands, presumably due
to stacking interactions, which is in agreement with previous
obser◦vations.43 Overall, this leads to a stabilisation of around
+4.5 C in the porphyrin modified DNA duplexes compared to
the natural DNA strand (7·8). The amide system (5·6) displays
the largest DTm, which may be caused by a stabilisation effect
due to the introduction of flexibility within the system or due to
the less sensitive nature of porphyrin DNA to DMF. However,
a contribution of both factors is likely since the hybrid system
(3·6) demonstrates a greater stabilising effect than the all acetylene
system (3·4), due to the introduction of flexibility in some of the
porphyrin modified nucleotides. In the UV-Vis spectra, porphyrin
stacking interactions manifest themselves as a broadening of the
porphyrin Soret band (B band) which, on heating above the
duplex’s Tm, narrows again; this is consistent with our previously
Scheme 1 Reagents and conditions: a) 4,4¢-Dimethoxytrityl chloride,
pyridine, CH2CL2; b) i) BF3·Et2O, CHCl3, dark, ii) DDQ; c) propargy-
lamine, Pd(PPh3)4, CuI, NEt3, DMF; d) pyridine, KOH, H2O, 40 ◦C; e)
EDC, HOBt, DMAP, CH2Cl2, dark; f) (N(iPr)2)P(Cl)OEtCN, DIPEA,
CH2Cl2, dark.
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Table 1 Melting temperatures of the porphyrin–DNA duplexes
Tm/◦Ca
Buffer Buffer : DMF 9 : 1 DTm/◦Cd
DTm per porphyrin/◦Cd
3·4 50.8c
5·6 n.d.e
3·6 51.3c
7·8 47.2b
3·8 53.3c
4·7 51.4c
5·8 51.8c
6·7 52.1c
n.d.e
45.9b
3.6
4.7
4.1
—
6.1
0.3
0.4
0.3
—
1.0
n.d.e
41.2b
n.d.e
n.d.e
4.1
0.7
46.2b 48.8c
47.3b 50.1c
4.6, 5.0, 7.6
4.9, 6.1, 8.9
0.8, 0.8, 1.3
0.8, 1.0, 1.5
a buffer solution: 100 mM NaH2PO4/Na2HPO4, 100 mM NaCl, 1 mM
Na2-EDTA, pH 7.0, [DNA] = 1 mM; b UV melting; c fluorescence melting;
d DTm calculated with respect to the unmodified duplex (7·8); e no discrete
transition detected.
Fig. 3 a) CD spectra of the porphyrin regions of the duplexes 3·4, 5·6
and 3·6. b) CD spectra of the thermal demetallation of 3Zn at 80 ◦C.
Fig. 2 UV and fluorescence melting curves of 5·8 as a representative
example (9 : 1 buffer : DMF solution, conditions as in Table 1).
transitions are not discrete and can be thought of as simple
dipoles.47 As such these give a simple -/+ bisignate spectrum
(from longer wavelengths) with maxima at l = -438/+419 nm and
-436/+412 nm for 5·6 and 3·6 respectively. Duplex 3·4, containing
only the shorter, more conformationally restricted acetylene linked
monomer, gives a more complex +/-/+ trisignate signal at l =
+441/-425/+405 nm. The porphyrins in this system have to be
considered as circular oscillators, that is, the perpendicular Bx and
By transitions will both contribute significantly to the excitonic
coupling. Multisignates of the Soret band have also been ascribed
to p–p stacking between two close porphyrins when attached to a
chiral scaffold with restricted conformational flexibility,47 and this
may also contribute to the CD band.
Facile metallation of strands 3 and 5 by zinc, cobalt and copper
was achieved to give xZn, xCo and xCu (x = 3, 5), similar
to previous work reported by Berova et al.48 The strands were
hybridized with 4 and 6 to form the alternating mixed metal-
free base porphyrin arrays. Only small lmax shifts of 2–7 nm were
observed in the UV-Vis spectra upon metallation (Fig. S8, ESI†).
The CD spectra of 5M2+·6 were largely unaffected; however the
systems 3M2+·6 and 3M2+·4 are more sensitive to metallation (Fig.
4), which could be due to a different porphyrin stacking along the
DNA (vide infra). The duplex 3M2+·4 seems particularly sensitive
to metallation, and the CD bands show the most dramatic change
compared to the corresponding free base porphyrin modified
duplex. On metallation with cobalt or copper, the band remains
as a +/-/+ trisignate with maxima at l = +436/-423/+405 nm
and +433/-422/+410 nm, respectively, but with a significant shift
in peak maxima and intensities. In contrast, on metallation with
investigated porphyrin arrays. The different strands all exhibit
identical spectroscopic behaviour, thus the linker does not have any
influence on the electronic properties of the porphyrin. This also
indicates that the porphyrin is electronically disconnected from
the base stacking region of the DNA in all cases. Also, the 12-
porphyrin systems do not show efficient energy transfer in steady-
state fluorescence spectroscopy due to the unfavorable spectral
overlap (vide infra); this is only observed in short porphyrin
arrays.43 Hysteresis of 3–5 ◦C between melting and annealing
traces is observed in the UV and fluorescence thermal studies
for all porphyrin modified duplexes, indicating differing kinetics
of melting and annealing processes. A hysteresis of 1 ◦C or less
is observed for the unmodified duplex (7·8), which would suggest
that the melting and annealing transitions of porphyrin modified
duplexes are different to the those undergone by 7·8.
Circular dichroism spectroscopy of free base and metallated
porphyrin–DNA
Circular dichroism (CD) spectroscopy showed the characteristic
B-type DNA signatures for all duplexes, with a bisignate signal
displaying maxima at l = +276/-252 nm; little perturbation of
these was observed for modified duplexes 3·4, 5·6 and 3·6, demon-
strating that the conformation of the helix is not significantly
altered even when modified with twelve porphyrins. Excitonic
coupling of the porphyrin B band can be observed (Fig. 3a)
in all samples. Duplexes containing the amide linked monomer
(5·6 and 3·6) appear to act as linear oscillators, the Bx and By
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Fig. 5 Molecular modelling of porphyrin–DNA zipper systems (Macro-
Model, AMBER*).49
oriented at an angle of 110◦ to the helical axis. Interestingly, when
the two different linkers are combined in the duplex 3·6, pairwise
stacking is no longer pronounced, with closest inter-porphyrin
˚
˚
distances of 4.5 A and 5.5 A. Also the plane of the porphyrin
rings is nearly perpendicular to the helical axis, at an angle of 94◦,
giving the appearance of a slipped stack and predicting a much
better fit in the duplex. In contrast to what might be predicted from
the models, the more even distribution of the porphyrins in 3·6,
which would provide more even interstrand interactions across the
length of the modified section of the duplex, does not lead to a
significantly enhanced stabilisation of the duplex.
Fig. 4 Comparison of the CD spectra of the metallated porphyrin–DNA
strands 3·4 (a) and 3·6 (b).
zinc the trisignate becomes a -/+/-/+ tetrasignate signal (l =
-444/+433/-425/+411 nm). As has previously been mentioned,
the CD bands of 3·4 are not a simple couplet and it is presumably
these other interactions which cause the complexity of the CD
band of 3Zn2+·4. In these cases CD spectroscopy serves as a much
better diagnostic tool to confirm metallation, as compared to UV-
vis spectroscopy where only small differences were detected.
Here we also found that copper and cobalt metallated por-
phyrins are thermally stable up to 80 ◦C, but the zinc porphyrins
are unstable at 80 ◦C, with a significant proportion reverting
to the free base after 20 min (Fig. 3b). This effect is again
much more pronounced in the CD spectra compared to the
changes in absorbance. Zinc porphyrins have shown to be stable
to demetallation up to 60 ◦C.
Solution phase association
The overall structure of the DNA construct in solution was
examined for 3·4 using laboratory small angle X-ray scattering
(SAXS). The data were consistent with an elongated monodisperse
aggregate. The simplest model to provide an adequate fit is a
cylinder with a length of 13 nm and a radius of 3.9 nm (Fig.
6a). While the length is consistent with that predicted from the
modelling of the DNA, the radius suggests an association complex
of two to four double helices forming in solution. We propose a
model for the formation of a two to four helical bundle as shown
in Fig. 6a, which seems to dominate at higher concentrations
and is most likely induced by weak hydrophobic intermolecular
interactions between the porphyrins. Similar formation of higher
order assemblies induced by porphyrin–porphyrin interactions in
DNA have recently been reported to occur at high ionic strength.37
According to the SAXS data, these helical bundles are discrete
entities, and solubility is not affected by this molecular association;
no precipitation or light scattering was observed. It should be
noted that the SAXS experiments were performed at a rather high
concentration of 50 mM. The spectroscopic data (absorbance, CD)
are distinctly different at high concentration (Fig. 6b) compared
to low concentration. At 56 mM, the absorbance shows a clear
maximum at l = 419 nm and a shoulder at l ~ 409 nm,
whereas at 1 mM the absorbance is very broad (lmax = 410
nm). The CD spectrum appears sharper and more intense in the
normalised spectrum, but most notably the bisignate spectrum
changes to a trisignate spectrum. These differences suggest that the
intermolecular interactions occur only at higher concentrations,
and that the spectroscopic data (absorbance, CD) discussed above
reflect the single porphyrin–DNA behaviour rather than that of
the aggregates.
Molecular modelling
In order to detect differences in the relative orientation of the
porphyrins as a function of the linker composition, molecular
modelling was conducted on the duplexes 3·4, 5·6 and 3·6 (Fig.
5). The energy minima were calculated from identical starting
geometries (B-type DNA). The models predicted three very
different structures with 3·4 and 5·6 both showing stacking of
the porphyrins in a pairwise manner, with closest inter-porphyrin
˚
˚
˚
˚
distances of 4.3 A and 6.5 A for 3·4, and 4.4 A and 7.9 A
for 5·6. Pairwise stacking arises due to the modifications being
bound to alternate strands with linkers of the same length, thus
the porphyrins create two spirals in the major groove which are
offset with respect to one another. This is not observed when
all modifications are on the same strand.38,39 The plane of the
porphyrin rings in 3·4 are orientated at an angle of 71◦ with respect
to the helical axis, while the plane of the porphyrin rings in 5·6 are
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Fig. 6 a) SAXS data recorded on a solution of porphyrin modified DNA (3·4) at 50 mM. The fit is to a simple rigid cylinder with a radius of 3.9 nm and
a length of 13 nm, which is consistent with a two to four helical bundle; b) Absorbance (top) and CD (bottom) spectra of 3·4 at both 56 mM and 1 mM
concentration.
Service Centre Swansea University, and all members of the Stulz
Conclusions
and Siligardi research groups for their help and support. We thank
To summarize, we have demonstrated the synthesis of zipper-like
Prof. Nina Berova (Columbia University) for helpful discussions
porphyrin modified DNA containing two different linkers. The
on the interpretation of the CD spectra.
arrays contain 12 porphyrins and span a full helical turn, where
the inter-porphyrin distance and torsion angles with respect to
the helical axis are dependant on the linker incorporated. The
Notes and references
porphyrins are easily metallated post-synthetically with various 3d
transition metals. The complexes’ thermal stability varies between
metals with Co(II) and Cu(II) being stable but Zn(II) being
unstable and reverting back to the free base within minutes at
80 ◦C. The duplexes studied seem to adopt markedly different
conformations of the porphyrins within the major groove of
the DNA, shown by CD and molecular modelling. Using the
same linker in both strands results in a pairwise stacking of
the porphyrins, whereas the hybrid systems give a more even
distribution of the porphyrins. However, this does not affect the
spectroscopic properties, and the differences are probably too
subtle to be detected. The thermal stability of the duplexes, on
the other hand, are dependent on the structure of the linker
and the nature of the solvent. The precise arrangement of large
hydrophobic substituents within the major groove of the DNA
is therefore a very important factor in determining the stability
of modified DNA. It should also be noted that the porphyrin–
DNA systems tend to associate to higher ordered arrays at higher
concentrations, which might also be the case for other synthetic
DNA systems which bear hydrophobic groups. The systems are
now under investigation for their photoinduced electron transfer
efficiency and ability to perform as electronic wires.
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