Dynamic Nuclear Polarization of Metal-Organic Frameworks Using Photoexcited Triplet Electrons

Article abstract of DOI:10.1021/jacs.8b10121

While dynamic nuclear polarization based on photoexcited triplet electrons (triplet-DNP) has the potential to hyperpolarize nuclear spins of target substrates in the low magnetic field at room temperature, there has been no triplet-DNP system offering str

Full text of DOI:10.1021/jacs.8b10121

Communication
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Cite This: J. Am. Chem. Soc. XXXX, XXX, XXX−XXX
Dynamic Nuclear Polarization of Metal−Organic Frameworks Using
Photoexcited Triplet Electrons
Saiya Fujiwara,†,§ Masanori Hosoyamada,†,§ Kenichiro Tateishi,*,‡,# Tomohiro Uesaka,‡,# Keiko Ideta,∥
Nobuo Kimizuka,*,† and Nobuhiro Yanai*,†,¶
†Department of Chemistry and Biochemistry, Graduate School of Engineering, Center for Molecular Systems (CMS), Kyushu
University, 744 Moto-oka, Nishi-ku, Fukuoka 819-0395, Japan
‡Cluster for Pioneering Research, RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan
#Nishina Center for Accelerator-Based Science, RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan
∥Institute for Materials Chemistry and Engineering, Kyushu University, 6-1 Kasuga-koen, Kasuga, Fukuoka 816-8580, Japan
¶PRESTO, JST, Honcho 4-1-8, Kawaguchi, Saitama 332-0012, Japan
S
* Supporting Information
ABSTRACT: While dynamic nuclear polarization based
on photoexcited triplet electrons (triplet-DNP) has the
potential to hyperpolarize nuclear spins of target
substrates in the low magnetic field at room temperature,
there has been no triplet-DNP system offering structural
rigidity and substrate accessibility. Here, we report the
first example of triplet-DNP of nanoporous metal−organic
frameworks. Accommodation of a carboxylate-modified
pentacene derivative in a partially deuterated ZIF-8 (D-
1
ZIF-8) results in a clear H NMR signal enhancement
over thermal equilibrium.
uclear magnetic resonance (NMR) spectroscopy and
magnetic resonance imaging (MRI) are versatile
Figure 1. (a) Typical scheme of triplet-DNP. Photoexcitation of the
N
polarizing agent is followed by spin-selective intersystem crossing
(ISC). The resulting large electron spin polarization is transferred to
the nuclear spin polarization through the integrated solid effect (ISE).
(b) Schematic illustration of triplet-DNP in MOFs accommodating
polarizing agents.
methods in modern chemistry and biology fields. Nevertheless,
they suffer from intrinsically limited sensitivity due to the low
nuclear spin polarization at ambient temperature. One of the
promising methods to overcome this limitation is dynamic
nuclear polarization (DNP), which enhances nuclear polar-
ization by transferring spin polarization from electrons to
nuclei.1,2 The application of DNP has opened up new
possibilities, in particular for molecular imaging with MRI.
For example, the use of DNP enables tumor imaging by
monitoring hyperpolarized metabolic small molecules, which is
currently under clinical trial.3−6 While significant polarization
enhancement (ε) has been achieved by using paramagnetic
radical compounds as the polarizing agents,7−9 the use of
cryogenic temperatures around 1 K inevitably increases the
cost of the instruments and makes it difficult to polarize fragile
biological substances.
The solution to this issue has been proposed by employing
nonthermal electron polarization in photoexcited triplet state
at room temperature.10−15 In the typical scheme of DNP based
on a photoexcited triplet (triplet-DNP, Figure 1a), spin-
selective intersystem crossing (ISC) produces a large electron
spin polarization in the excited triplet state sublevels regardless
of temperature,16 and this polarization is effectively transferred
to nuclear spins by the integrated solid effect (ISE).17,18
Following its first report,10 room-temperature triplet-DNP has
provided high enhancements in organic crystals such as p-
terphenyl with long spin−lattice relaxation time (T1).10−12,14
However, it remains difficult for such organic crystals to
accommodate target molecules to be monitored. While
amorphous solids such as o-terphenyl were employed as host
matrices to accommodate target substrates, the flexible
structure requires the cooling of the sample for triplet-DNP
(∼120 K).13 Therefore, despite these efforts, it remains a grand
challenge to develop a room-temperature triplet-DNP system
with accessibility for polarizing targets. While pioneering works
employed porous materials for low-temperature radical-based
DNP to accommodate target molecules,19−24 there have been
no examples of room-temperature DNP using porous matrices.
In this work, we show the first example of employing metal−
organic frameworks (MOFs)25−33 as host materials for triplet-
DNP (Figure 1b). MOFs offer not only rigid crystalline
Received: September 18, 2018
© XXXX American Chemical Society
A
DOI: 10.1021/jacs.8b10121
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Journal of the American Chemical Society
Communication
structures but also nanopores for guest accommodation. For
the proof-of-concept, it is necessary to satisfy the following
conditions: (i) high dispersibility of polarizing agent in MOFs;
(ii) long 1H T1 of MOFs. Based on our previous work using a
soluble pentacene derivative (6, 13-diphenylpentacene (DPP))
for triplet-DNP,34 we modified the typical polarizing agent
pentacene with metal-coordinating carboxylate moieties (4,4′-
(pentacene-6,13-diyl)dibenzoic acid (PDBA)), Figure 2a) for
growth rate of ZIF-8 crystallization by the base addition
might kinetically trap PDBA molecules inside ZIF-8 before
aggregation of PDBA.
The dispersed accommodation of PDBA in ZIF-8 is further
supported by fluorescence studies. Time-resolved fluorescence
measurements of PDBA in DMF ([PDBA] = 50 μM) showed
a single-exponential decay with a lifetime of 7.8 ns (Figure S4b,
Supporting Information). No detectable fluorescence was
observed from bulk PDBA solids, probably due to the
fluorescence quenching by singlet fission among aggregated
PDBA molecules.40 On the other hand, ZIF-8 ⊃ PDBA clearly
showed fluorescence bands similar to those of the DMF
solution (Figure S4a, Supporting Information). The fluo-
rescence decay of ZIF-8 ⊃ PDBA could be fitted with three
components (2.0 ns (6.3%), 6.1 ns (56%), and 12.8 ns (37%),
Figure S4b, Supporting Information), which may reflect the
partial aggregation of PDBA molecules.
The included amount of PDBA inside ZIF-8 was quantified
from the UV−vis absorbance after digesting the composite
with HCl in methanol. The inclusion amount can be controlled
by changing the concentration of PDBA and NaOH (Figure
S5, Supporting Information). The included amount of PDBA
increased by increasing the NaOH concentration. As a control
experiment, no uptake of nonionic DPP into ZIF-8 was
observed, suggesting the accommodation of PDBA through
coordination of carboxylate moieties to Zn2+ ions of ZIF-8.
With reference to previously optimized systems including
0.01−0.05 mol % of pentacene in dense p-terphenyl
crystals,12,13 we prepared ZIF-8 samples containing 0.036
mol % of PDBA.
The structure of ZIF-8 synthesized in the presence of NaOH
(10 mol % of Zn2+ ions) was confirmed by scanning electron
microscopy (SEM), elemental analysis, powder X-ray dif-
fraction (PXRD), and N2 adsorption measurements. SEM
images showed that the addition of NaOH decreased the
crystal size from ca. 30 nm to 10 nm (Figure S6, Supporting
Information). This is in good agreement with previous reports
about the effect of the base upon crystallization of ZIF-8.41,42
The smaller crystal size of ZIF-8 by base addition was
explained by faster nucleation and growth of ZIF-8 due to the
enhanced deprotonation of MeIM ligands. The presence of
NaOH did not affect the phase purity of ZIF-8, as confirmed
by elemental analysis and PXRD patterns (Figure S7,
Supporting Information). PXRD patterns showed peak broad-
ening by the addition of NaOH, which agrees with the reduced
crystal size. The N2 adsorption isotherms for both ZIF-8
samples with/without NaOH showed N2 uptake in the low-
pressure region (P/P0 < 0.1), characteristic of microporous
materials (Figure 2c). The BET surface area of ZIF-8 was
mostly maintained when NaOH was used (1280 m2 g−1)
compared with that of the pristine ZIF-8 (1680 m2 g−1). Only
ZIF-8 synthesized with NaOH showed an additional N2
absorption in the middle-pressure region (P/P0 > 0.6) and a
hysteresis in the desorption process. This behavior is typical for
mesoporous materials, and the observed mesopores are
ascribed to the grain boundaries between ZIF-8 nanoparticles.
These PXRD and gas absorption results agree well with the
previous reports of ZIF-8 nanocrystals.41,42
Figure 2. (a) Synthetic scheme and a photograph of ZIF-8 ⊃ PDBA.
(b) Absorption spectra of a DMF solution of PDBA (50 μM, red),
ZIF-8 ⊃ PDBA (0.036 mol %, blue), and neat solid PDBA (black).
(c) N2 absorption (filled circles) and desorption (open circles)
isotherms at 77 K for ZIF-8 synthesized in the absence (red) and
presence (blue) of 10 mol % NaOH. (d) H spin−lattice relaxation
(T1) data of ZIF-8 (black) and D-ZIF-8 (red) acquired with the
saturation−recovery sequence.
1
1
its introduction into MOFs. A relatively long H T1 has been
reported for a prototypical diamagnetic Zn2+-based MOF,
[Zn(MeIM)2]n (ZIF-8; MeIM = 2-methylimidazolate).35−39
A
partial deuteration of MeIM ligands allows the elongation of T1
of partially deuterated D-ZIF-8. Polarization transfer from
1
PDBA triplet electrons to H nuclei in D-ZIF-8 resulted in a
clear enhancement (ε = 58) of 1H NMR signals of D-ZIF-8 at
a low magnetic field of 0.67 T and room temperature.
We synthesized the new pentacene derivative PDBA starting
from 6,13-pentacenequinone (Scheme S1, Supporting In-
formation). The PDBA molecules were successfully accom-
modated during the crystallization of ZIF-8 in methanol in the
presence of NaOH at room temperature (Figure 2a). It has
been reported that the aggregation of pentacene decreases the
effect of triplet-DNP.12 To gain insights into the dispersibility
of PDBA in ZIF-8, we measured absorption spectra. A
dimethylformamide (DMF) solution of PDBA ([PDBA] =
50 μM) exhibited structured π−π* absorption bands at 601.5,
557, and 518.5 nm (Figure 2b). The absorption bands in the
neat solid PDBA showed red-shifts to 616, 565.5, and 528 nm
and broadening due to intermolecular interactions among
aggregated PDBA. Interestingly, the absorption peak positions
of PDBA in ZIF-8 depend on the NaOH concentration and
became almost identical to those in solution in the presence of
10 mol % NaOH compared with Zn(II) ions (Figures 2b, S3,
Supporting Information). The enhanced nucleation and
In practice, the spin−lattice relaxation time (T1) is the major
factor in determining the attainable spin polarization since the
polarization accumulation competes with the spin−lattice
1
relaxation. To obtain the H T1 value, we carried out solid-
state magic angle spinning (MAS)-NMR measurements of
B
DOI: 10.1021/jacs.8b10121
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Journal of the American Chemical Society
Communication
ZIF-8 at room temperature (Figure S8a, Supporting
Information). Samples were packed in an Ar-filled glovebox
to exclude the relaxation effect by paramagnetic oxygen
1
molecules. The H T1 value of ZIF-8 was estimated as 31
0.1 s (Figure 2d).39 We confirmed that the inclusion of 0.036
mol % of PDBA did not significantly affect the 1H T1 value of
ZIF-8 (25 0.1 s, Figure S8b, Supporting Information). To
1
further increase the H T1 value, we synthesized a partially
deuterated MOF. For spin-1/2 systems, spin−lattice relaxation
is mainly caused by fluctuating local magnetic fields at the site
of nuclear spins due to the thermal motion of molecules.43
Generally, in solids, every spin is densely coupled to other
spins and the T1 values are averaged out over whole protons.
Accordingly, we assumed that the rotation of methyl groups in
1
ZIF-8 decreases the H T1 value and synthesized a partially
deuterated ligand, MeIM-d3 (Figure 2d, Scheme S2, SI), to
construct methyl-deuterated ZIF-8 (denoted as D-ZIF-8). As
1
expected, a longer H T1 value of 53 1.0 s was successfully
obtained for D-ZIF-8 (Figures 2d, S8c, Supporting Informa-
tion). In the following experiments, D-ZIF-8 ⊃ PDBA
containing 0.036 mol % of PDBA was used.
The generation of electron spin polarization in photoexcited
triplet state was investigated by time-resolved electron spin
resonance (ESR) measurements at room temperature. Under
pulsed laser irradiation at 589 nm, the ESR spectrum of D-ZIF-
8 ⊃ PDBA showed a characteristic line shape of spin-polarized
triplet state at room temperature, in which the T1,0 triplet
sublevel is populated preferentially and Δm = 1 T1,0 → T1,‑1
and T1,0 → T1,+1 transitions were observed as emission at 305
mT and absorption at 355 mT, respectively (Figure 3a). The
1
Figure 4. (a) Sequence of the triplet-DNP process. (b) H NMR
signals of D-ZIF-8 ⊃ PDBA under thermal conditions (300 scans
every 3 min) and after triplet-DNP (ISE sequence for 50 s and 1 scan)
at room temperature and 220 K. (c) 1H polarization buildup curve of
D-ZIF-8 ⊃ PDBA at room temperature and 220 K. The enhancement
factors were calculated by comparing the peak area after triplet-DNP
with that of thermal equilibrium at room temperature.
After repeating this process to accumulate the spin
1
polarization, H NMR spectra were immediately measured.
Because the accumulation of spin polarization by ISE competes
1
with spin−lattice relaxation, the H spin polarization becomes
saturated by elongating the triplet-DNP process (Figure 4c).
1
The H NMR signal intensity of D-ZIF-8 ⊃ PDBA showed a
large enhancement factor of 58, and the signal-to-noise ratio of
1H NMR spectra was significantly improved by the triplet-
DNP process (Figure 4b). Besides, we investigated the triplet-
DNP process at a lower temperature (220 K), which is relevant
to adsorption of the 129Xe gas probe.46,47 As a result, 85 and
102 times enhancement were achieved compared to the
thermal equilibrium at 220 K and room temperature,
respectively. The change in the noise level of the NMR signal
by reducing the temperature is mainly attributed to the thermal
controller. The polarization buildup curve was fit to A[1 −
exp(−t/TB)], giving a buildup constant TB of 13 s at 220 K,
which was increased relative to room temperature (8.5 s). This
indicates that the increase in the 1H NMR signal enhancement
at low temperature is mainly due to the reduced molecular
mobility and prolonged 1H T1. We note that D-ZIF-8 ⊃ PDBA
was unstable in repeated long-term laser irradiation, which
would be solved by improving the dispersibility and chemical
stability of the polarizing agent.
Figure 3. (a) Time-resolved ESR spectrum of D-ZIF-8 ⊃ PDBA at
room temperature just after photoexcitation at 589 nm. (b) Decay of
the ESR peak at 355 mT under pulsed photoexcitation at 589 nm.
signal intensity of the peak at 355 mT showed microsecond-
scale decay profiles characteristic of the triplet excited state
(Figure 3b). The negative components derived from T1,−1
→
S0/T1,+1 → S0 transitions were also observed at around 50 μs,
supporting the spin-selective ISC.44,45
The transfer of spin polarization from photoexcited triplet
1
1
electrons to H nuclei was evaluated by comparing the H
NMR signal with and without the triplet-DNP process at 0.67
T and room temperature (see Supporting Information for
detailed measurement setup). PDBA molecules were photo-
excited by a pulsed 589 nm laser (500 Hz), followed by
microwave irradiation (18.1 GHz) and field sweep ( 100 G)
for polarization transfer (ISE sequence, Figure 4a). The
duration of microwave irradiation (10 μs) was optimized based
on the enhancement of the 1H NMR signal intensity. The extra
time of 2 ms was employed to avoid the sample degradation.
In conclusion, we demonstrate the first spin hyperpolariza-
tion of MOF protons based on triplet-DNP. The selective
deuteration of the framework effectively suppressed the spin
1
relaxation, giving a long H T1 value over 50 s. The newly
synthesized polarizing agent PDBA allowed the generation of
electron spin polarization by photoexcitation in D-ZIF-8. As a
result, by applying triplet-DNP, the significant 1H NMR signal
enhancement factor (ε) of 58 was achieved at room
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ASSOCIATED CONTENT
■
S
* Supporting Information
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/jacs.8b10121.
(12) Takeda, K. Triplet State Dynamic Nuclear Polarization; VDM
Verlag Dr. Muller: Saarbrucken, Germany, 2009.
̈ ̈
Experimental details, NMR spectra, UV−vis absorption
spectra, fluorescence spectra, fluorescence decays, SEM
images, PXRD patterns (PDF)
(13) Tateishi, K.; Negoro, M.; Kagawa, A.; Kitagawa, M. Dynamic
Nuclear Polarization with Photoexcited Triplet Electrons in a Glassy
Matrix. Angew. Chem., Int. Ed. 2013, 52, 13307−13310.
(14) Tateishi, K.; Negoro, M.; Nishida, S.; Kagawa, A.; Morita, Y.;
Kitagawa, M. Room temperature hyperpolarization of nuclear spins in
bulk. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 7527−7530.
(15) Eichhorn, T. R.; Niketic, N.; van den Brandt, B.; Filges, U.;
Panzner, T.; Rantsiou, E.; Wenckebach, W. Th.; Hautle, P. Proton
polarization above 70% by DNP using photo-excited triplet states, a
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AUTHOR INFORMATION
Corresponding Authors
*kenichiro.tateishi@riken.jp
*n-kimi@mail.cstm.kyushu-u.ac.jp
*yanai@mail.cstm.kyushu-u.ac.jp
■
ORCID
(16) Sloop, D. J.; Yu, H.-L.; Lin, T.-S.; Weissman, S. I. Electron spin
echoes of a photoexcited triplet: Pentacene in p-terphenyl crystals. J.
Chem. Phys. 1981, 75, 3746−3757.
(17) Henstra, A.; Wenckebach, W. Th. Dynamic nuclear polarisation
via the integrated solid effect I: theory. Mol. Phys. 2014, 112, 1761−
1772.
Kenichiro Tateishi: 0000-0001-5566-526X
Nobuo Kimizuka: 0000-0001-8527-151X
Nobuhiro Yanai: 0000-0003-0297-6544
Author Contributions
§S. Fujiwara and M. Hosoyamada contributed equally.
(18) Can, T. V.; Weber, R. T.; Walish, J. J.; Swager, T. M.; Griffin, R.
G. Frequency-Swept Integrated Solid Effect. Angew. Chem. 2017, 129,
6848−6852.
Notes
The authors declare no competing financial interest.
(19) Lesage, A.; Lelli, M.; Gajan, D.; Caporini, M. A.; Vitzthum, V.;
ACKNOWLEDGMENTS
́
Mieville, P.; Alauzun, J.; Roussey, A.; Thieuleux, C.; Mehdi, A.;
■
́
Bodenhausen, G.; Coperet, C.; Emsley, L. Surface Enhanced NMR
This work was partly supported by JSPS KAKENHI grant
numbers JP25220805, JP17H04799, and JP16H06513 and the
Tobe Maki Scholarship Foundation. K.T. acknowledges partial
support from the RIKEN Pioneering Project “Dynamic
Structural Biology”.
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DOI: 10.1021/jacs.8b10121
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