Design Guidelines to Elongate Spin-Lattice Relaxation Times of Porphyrins with Large Triplet Electron Polarization

Porphyrins with Large Triplet Electron Polarization

Article

Design Guidelines to Elongate Spin−Lattice Relaxation Times of

Akio Yamauchi, Saiya Fujiwara, Koki Nishimura, Yoichi Sasaki, Kenichiro Tateishi,* Tomohiro Uesaka,

Nobuo Kimizuka,* and Nobuhiro Yanai *

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sı Supporting Information

ABSTRACT: The spin-polarized triplet state generated by light

irradiation has potential for applications such as triplet dynamic

nuclear polarization (triplet-DNP). Recently, we have reported

free-base porphyrins as versatile and biocompatible polarizing

agents for triplet-DNP. However, the electron polarization of free-

base porphyrins is not very high, and the dilemma is that the high

polarization of metalloporphyrins is accompanied by a too short

spin−lattice relaxation time to be used for triplet-DNP. We report

here that the introduction of electron-withdrawing ﬂuorine groups

into Zn porphyrins enables a long enough spin−lattice relaxation

time (>1 μs) while maintaining a high polarization (P :P :P =

:0:1.0) at room temperature. Interestingly, the spin−lattice

relaxation time of Zn porphyrin becomes much longer by

introducing ﬂuorine substituents, whereas the spin−lattice relaxation time of free-base porphyrin becomes shorter by the ﬂuorine

substitution. Theoretical calculations suggest that this is because the introduction of the electron-withdrawing ﬂuorine substituents

reduces the spin density on Zn atoms and weakens the spin−orbit interaction.

. INTRODUCTION

where T and T denote the spin−lattice relaxation time and

tri

the triplet lifetime, respectively. The relationship among T

T , and T is expressed as follows:

EPR

When there is a bias in the sublevel population, it is called spin

polarization. Since the populations of each sublevel follow a

Boltzmann distribution in thermal equilibrium, the electron

spin polarization is very small under ambient conditions.

Therefore, cryogenic conditions are required to obtain a large

tri

/T_E_P_R= 1/T + 1/T

(2)

tri

The derivation of this equation was based on a recent paper

−7

electron polarization in a thermal equilibrium state.

As one

by Matsuoka et al. and is brieﬂy summarized in the

Supporting Information. In most of the previous works,

pentacene has been commonly employed as the polarizing

agent of triplet-DNP owing to its suitable electron polarization

properties such as relatively large population diﬀerences in the

of the solutions to this problem, the nonequilibrium and

temperature-independent spin polarization of triplet electrons

is widely used for applications such as quantum computing,

0−12

room-temperature masers,

and triplet dynamic nuclear

The large polarization of a

3−17

zero ﬁeld (P :P :P = 0.76:0.16:0.08 in the p-terphenyl

polarization (triplet-DNP).

crystal) ^aⁿ^d^mⁱ^c^r^o^s^e^c^oⁿ^d^-^s^c^a^l^e^l^oⁿ^g^TEPR at room temper-

ature. Despite its potential, however, the applications of triplet-

DNP have been mainly limited to molecular crystals that can

be doped with pentacene due to pentacene’s poor stability in

air and very low solubility in solvents.

triplet state can be generated even at room temperature by

sublevel-selective intersystem crossing from the photoexcited

singlet state.

The properties of a polarized triplet state are evaluated by

using two parameters, the population of the triplet sublevels in

Therefore, we have focused on porphyrins as a new family of

polarizing agents with good air stability and solubility and

high ﬁelds P , P , P and EPR decay time T_E_P_R, which can be

−1

determined by time-resolved electron paramagnetic resonance

TR-EPR) measurements. The EPR signal intensity is

(

proportional to the population diﬀerence P_Δbetween the

spin sublevels, and under the high ﬁeld and the condition of

fast relaxation, the decay of the signal intensity is expressed by

Received: March 1, 2021

Revised: April 19, 2021

Published: May 12, 2021

the following equation:

P = ±(P − P )exp{−(1/T + 1/T )t}

(1)

±1

tri

2021 American Chemical Society

J. Phys. Chem. A 2021, 125, 4334−4340

334

The Journal of Physical Chemistry A

(Figure 1 ). Very interestingly, the introduction of ﬂuorine

Article

succeeded in triplet-DNP of biomolecules using porphyrins for

(ZnTPP) was purchased from Frontier Scientiﬁc and used

without further puriﬁcations. Free-base tetrakis(2,6-

diﬂuorophenyl)porphyrin (H F TPP), zinc tetrakis(2,6-di-

the ﬁrst time. It had been known that porphyrins form a

21−23

polarized triplet state,

but this had not been applied to

triplet-DNP. In our previous report, we used a free-base

porphyrin derivative as a polarizing agent for triplet-DNP, but

ﬂuorophenylporphyrin) (ZnF TPP), and zinc tetrakis-

(pentaﬂuorophenyl)porphyrin (ZnF TPP) were prepared by

25,26

its polarization (P :P :P = 0.30:0.67:0.03) was not very high

following the literature methods

and characterized by H

and there is room for improvement. Although metalloporphyr-

ins such as Zn porphyrins are known to have very high

NMR measurements and mass spectroscopy. The porphyrins

were mixed with β-estradiol at a typical concentration of 0.1

mol %, heated at 300 °C, and then rapidly cooled with liquid

polarization (P :P :P = 0:0:1.0), they could not be used for

triplet-DNP due to their too fast EPR decay (<1 μs). Note that

N , giving porphyrin-doped β-estradiol glasses.

in the case of porphyrins, the spin−lattice relaxation time T

2.2. Synthesis of H F TPP. Pyrrole (340 μL, 4.04

2 8

(

∼μs) is much shorter than the triplet lifetime T (∼ms), and

mmol) and 2,6-diﬂuorobenzaldehyde (550 mg, 3.87 mmol)

were dissolved in 80 mL of dry CH Cl under N . BF ·O(Et)

tri

thus the inverse of the decay constant of the eq 1 T

EPR

becomes nearly equal to T . For simplicity, we refer to the

(60 μL, 0.476 mmol) was then added and stirred at room

temperature for 1 day. After adding p-chloronil (390 mg, 1.59

mmol), the reaction mixture was stirred at room temperature

for 18 h. After the reaction, the product was washed with

methanol. The residue was puriﬁed by silica gel column

decay time of the electron spin polarization of the porphyrin

triplet as the spin−lattice relaxation time T . From our

previous studies, the microsecond-order EPR decay time is

desired to gain a large enhancement by triplet-DNP.

Therefore, it is crucial to establish a design guideline to

achieve metalloporphyrins with both high polarization and

chromatography (eluent: chloroform/hexane (8/2 v/v)).

Yield: 13%. H NMR (400 MHz, CDCl , TMS): δ = 7.35−

long T in microseconds.

7.40 (t, 8H), 7.75−7.83 (quin, 4H), 8.86 (s, 8H), −2.77 (s,

Here, we show that the modiﬁcation of Zn porphyrins with

multiple electron-withdrawing ﬂuorine groups leads to polar-

2H). F NMR (376 MHz, CDCl ) δ = −108.08 (s, 8F).

MALDI-TOF-MAS (dithranol, m/z): calcd.: 758.17, found:

izing agents with long spin−lattice relaxation times T while

758.23.

maintaining their high polarization. We have systematically

studied the triplet polarization of Zn and free-base meso-

tetraphenylporphyrins with diﬀerent numbers of ﬂuorine

substitutions by TR-EPR in a glass matrix at room temperature

2.3. Synthesis of ZnF TPP. A saturated solution of zinc

acetate in methanol (2 mL) was added to H F TPP (50 mg) in

CHCl (10 mL). The reaction mixture was reﬂuxed for 7 h.

The progress of the reaction was conﬁrmed by the

disappearance of the Q band in UV−vis absorption measure-

ments. After the reaction, the obtained crude was ﬁltered,

washed with water, dried over anhydrous Na SO , and puriﬁed

by silica gel column chromatography (eluent: chloroform).

Yield: 54%. H NMR (400 MHz, CDCl , TMS): δ = 7.36−

.41 (t, 8H), 7.76−7.84 (quin, 4H), 8.97 (s, 8H). F NMR

(

376 MHz, CDCl ) δ = −108.40 (s, 8F). MALDI-TOF-MAS

(

dithranol, m/z): calcd.: 820.09, found: 820.17.

.4. Synthesis of ZnF TPP. A saturated solution of zinc

acetate in methanol (2 mL) was added to H F TPP (50 mg)

in CHCl (10 mL). The reaction mixture was reﬂuxed for 12 h.

The progress of the reaction was conﬁrmed by the

disappearance of the Q band in UV−vis absorption measure-

ments. After the reaction, the obtained crude was ﬁltered,

washed with water, dried over anhydrous Na SO , and puriﬁed

by silica gel column chromatography (eluent: chloroform/

hexane (2/1 v/v)). Several reprecipitations (methanol/water)

were performed to obtain the ﬁnal compound. Yield: 68%. H

NMR (400 MHz, CDCl , TMS): δ = 9.00 (s, 8H). F NMR

Figure 1. (a) Schematic illustration of the generation and relaxation

of triplet polarization. (b) Chemical structures of meso-tetraphenyl-

porphyrins MTPP, MF TPP, and MF TPP (M = H and Zn).

(376 MHz, CDCl ) δ = −136.63 to −136.70 (d, 8F), −151.66

to −151.72 (d, 4F), −161.48 to −161.70 (t, 8F). MALDI-

TOF-MAS (dithranol, m/z): calcd.: 1035.97, found: 1035.87.

.5. General Characterizations. H NMR (400 MHz)

substituents in the Zn porphyrins resulted in a signiﬁcant

spectra were measured on a JEOL JNM-ECZ400 spectrometer

using TMS as the internal standard. UV−vis absorption spectra

were recorded on a JASCO V-670 spectrophotometer.

Fluorescence and phosphorescence spectra were measured by

using a JASCO FP-8700 ﬂuorescence spectrometer. Powder X-

ray diﬀraction (PXRD) patterns were measured on a Bruker

D2 Phaser (Cu-Kα, 30 kV, 10 mA). Transient absorption

measurements were conducted by using a UNISOKU TSP-

2000 system.

increase in the T , which was an opposite trend to that of the

free-base porphyrins. Density functional theory (DFT)

calculations suggest that the introduction of ﬂuorine reduces

the spin density around the Zn atom, which enables both high

polarization and long T₁.

. METHODS

.1. Experimental Details. Free-base tetraphenylporphyr-

in (H TPP) and free-base tetrakis(pentaﬂuorophenyl)-

Time-resolved EPR measurements were carried out using a

homebuilt ∼9 GHz dielectric resonator with a window for laser

irradiation at a magnetic ﬁeld generated using an electro-

porphyrin (H F TPP) were purchased from TCI and used

without further puriﬁcations. Zinc tetraphenylporphyrin

335

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J. Phys. Chem. A 2021, 125, 4334−4340

Article

Figure 2. UV−vis absorption (black) and ﬂuorescence (red) spectra at room temperature and phosphorescence spectra at 77 K (blue) of (a)

H TPP, H F TPP, and H F TPP (top to bottom) and (b) ZnTPP, ZnF TPP, and ZnF TPP (top to bottom) in toluene (20 μM for UV−vis

absorption and ﬂuorescence, 1 mM for phosphorescence). The shoulders on the short wavelength side of the phosphorescence spectra of free-base

porphyrins are due to ﬂuorescence.

1,32

magnet. A Spectra Physics Quanta-Lay Nd:YAG laser was used

for excitation. The wavelength, repetition rate, pulse width, and

pulse energy were 532 nm, 10 Hz, ∼8 ns, and ∼12 mJ/pulse,

respectively. The electromagnet was purchased from Takano

S1 ).

A similar substituent eﬀect was also observed in the

triplet state, where the phosphorescence peak positions of free-

base and Zn porphyrins were blueshifted by the ﬂuorine

substitution.

(

MC160A-16). The gap and the pole size were 50 and 120

To characterize the room-temperature polarization proper-

ties, all the porphyrins were dispersed in a β-estradiol glass

matrix at room temperature (Figure 3a). We employed β-

estradiol since its rigid room-temperature glass has an excellent

ability to disperse various dyes and to avoid the oxygen

mm, respectively. A power supply PAG60-55 (Kikusui) with a

−

stability of 10 was used. A microwave was generated from an

SG22000Pro (DS instruments) with a power of ∼10 μW. The

EPR signal was converted to DC using a diode detector,

ampliﬁed with a low noise ampliﬁer (ALN0905-12-3010,

Dynamic RF Inc.), and detected using an oscilloscope

33,34

quenching of the photoexcited triplet state,

although its

short H spin−lattice relaxation time (∼3 s at 0.6 T) makes it

diﬃcult to be directly used for triplet-DNP. Then, 0.1 mol %

porphyrins were dissolved in a β-estradiol melt at 300 °C

(

DSOX3024T, Keysight). The samples were put into

capillaries and were measured at room temperature. The

zero-ﬁeld populations and zero-ﬁeld splitting parameters were

determined by the ﬁtting of spectra by using the EasySpin

above the melting point of β-estradiol (T = 176 °C) and then

quenched with liquid nitrogen. This process provided room-

temperature glass with high transparency doped with

porphyrins (Figure 3b). Powder X-ray diﬀraction (PXRD)

measurements of the porphyrin-doped β-estradiol samples did

not show any sharp crystalline peaks, con ﬁ rming the

amorphous structure of the glass matrix (Figure S1).

toolbox in MATLAB.

.6. Computational Details. The optimized structures of

porphyrins in the ground state and the lowest triplet state were

obtained with the B3LYP exchange−correlation functional as

implemented in the Gaussian 16 software using the 6-31G*

basis set. Time-dependent DFT for the calculation of the

energies and the conﬁgurations was employed with B3LYP/

SDD for Zn and EPR-II for others. Molecular orbitals and spin

The dispersibility of the porphyrins in the β-estradiol glass

matrix was examined by comparing the absorption and

ﬂuorescence spectra of the porphyrins in toluene solution, β-

estradiol glass, and neat solid at room temperature. The

absorption spectra of all the porphyrins were redshifted and

broadened in the neat state compared to the solution state,

suggesting the presence of interchromophore interactions in

the neat sample (Figure S2). The absorption spectra of the

three free-base porphyrins in β-estradiol glass did not change

from the solution state, suggesting that they are in the

molecularly dispersed state. The three Zn porphyrins showed a

change in the shape of their spectra in β-estradiol glass

compared to the solution state, but the broadening did not

occur in β-estradiol glass as much as in the neat state. We

measured the concentration dependence of the absorption

spectra of ZnF TPP in β-estradiol glass and found that there

densities were visualized by GaussView 6.0.

. RESULTS AND DISCUSSION

The electronic structures of porphyrins were characterized in

toluene by measuring absorption and ﬂuorescence spectra at

room temperature and phosphorescence spectra at 77 K

(Figure 2). It is well documented that Zn porphyrins have an

approximate D₄_hsymmetry, with two highest occupied

molecular orbitals (HOMOs) and two lowest unoccupied

molecular orbitals (LUMOs) degenerated, but in free-base

porphyrins, the symmetry drops to D , and the HOMO and

LUMO degenerations are resolved. Accordingly, ZnTPP

showed one prominent absorption peak in the Q-band region,

was no change in the spectral shape up to 0.1 mol %, but above

0.5 mol %, the spectra gradually broadened and became closer

to the neat state (Figure S3). This result suggests that the Zn

porphyrins are not aggregated in β-estradiol glass at 0.1 mol %,

and the change of the absorption spectra would be due to the

slight structural distortion in β-estradiol glass. In the

whereas H TPP showed separated peaks due to the symmetry

breaking. The absorption and ﬂuorescence peaks of free-base

and Zn porphyrins in toluene were slightly blueshifted by

introducing the ﬂuorine substituents due to the stabilization of

HOMOs by ﬂuorine substitution via an inductive eﬀect (Table

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Table 1. Relative Zero-Field Populations, Zero-Field

Splitting Parameters, and Spin−Lattice Relaxation Times T

(

≈T ) of the Free-Base and Zn Porphyrins

EPR

compound

P :P :P

|D| (MHz)

|E| (MHz)

T₁(μs)

H TPP

0.29:0.71:0

0.18:0.82:0

0:0.75:0.25

0:0:1.00

1125

1219

1292

955

1046

961

221

147

316

352

121

9.3

6.3

4.9

0.30

0.17

1.7

H F TPP

ZnTPP

ZnF TPP

(

P :P :P = 0:0:1.0). Importantly, this highly selective

x y z

population of the out-of-plane sublevel was maintained in

the ﬂuorinated Zn porphyrins.

The spin−lattice relaxation time T was obtained by single

exponential ﬁtting of the EPR decays. As the number of

ﬂuorine substitution increased, T of free-base porphyrins

became shorter from 9.3 to 4.9 μs. This trend is consistent with

the change of the D value that became larger from 1125 to

1292 MHz with the increase in the number of ﬂuorine atoms.

A similar trend, a shorter T and a larger D value by ﬂuorine

substitution, was also observed for ZnTPP and ZnF TPP. It

has been reported that the modulation of the electron spin

dipolar interaction is mainly responsible for the spin−lattice

relaxation of photoexcited triplets of organic molecules without

any heavy atoms, and the spin−lattice relaxation rate is

proportional to the square of zero-ﬁeld splitting parame-

38,39

ters.

Interestingly, a totally diﬀerent behavior was observed

for ZnF TPP that showed a much longer T of 1.7 μs than

ZnTPP (0.30 μs) and ZnF TPP (0.17 μs). This unexpected

result cannot be explained by the D value since the D value of

ZnF TPP (961 MHz) was close to that of ZnTPP (955

MHz). Rather, this behavior can be explained by changes in

the spin−orbit interaction, as discussed later. Note that the

Figure 3. (a) Chemical structure of β-estradiol. (b) Picture of β-

lifetime of the triplet excited state T of all the examined

tri

estradiol glass doped with 0.1 mol % ZnF TPP. (c, e) Time-resolved

porphyrins was in the millisecond-scale from transient

absorption measurements (Figure S5), which does not limit

EPR spectra and (d, f) decays of the EPR peaks of the free-base

porphyrins and Zn porphyrins. Black lines are experimental data, and

red lines are ﬁtting results. The EPR decays were recorded at 328,

the EPR decay time T_E_P_R(T_E_P_R≈ T ). It is remarkable that

ZnF TPP achieves both of the high polarization and the long

32, 338, 354, 356, and 335 mT for H TPP, H F TPP, H F TPP,

2 2 8 2 20

^T1 ^o^v^e^r¹^μ^s^.

ZnTPP, ZnF TPP, and ZnF TPP, respectively.

The stronger dipole−dipole interactions between electrons

in the ﬂuorinated free-base porphyrins, which is indicated by

0,41

ﬂuorescence spectra, all the porphyrins showed a redshift in

the neat state compared to the solution state, but the shape of

the spectra in the β-estradiol glass was similar to that in the

solution state, supporting their molecularly dispersed state in

the glass (Figure S4).

the larger D value,

would result in the shorter spin−lattice

relaxation time T . It has been reported that the larger D value

in the ﬂuorinated Mg porphyrins is due to the enhanced

mixing of (a e ) and (a e ) conﬁgurations by the ﬂuorine

1u g

substitution. We performed DFT calculations for free-base

The TR-EPR spectra and ﬁtting results of the porphyrins

doped in β-estradiol glass at room temperature are shown in

Figure 3. The relative population, zero-ﬁeld splitting

porphyrins using B3LYP/6-31G* for geometry optimizations,

and we used B3LYP/EPR-II for time-dependent DFT

calculations. The four frontier orbitals in the lowest triplet

state are shown in Figure S6. In the triplet state, both the

HOMO and LUMO are singly occupied molecular orbitals

(SOMOs), but we retain the ground state labeling for clarity.

The ﬂuorine substituents largely increased the excitation

energy to the lowest triplet state (Table S2). The main

parameters, and spin−lattice relaxation time T are summar-

ized in Table 1. It has been known that in-plane sublevels are

dominantly populated for free-base porphyrins due to the in-

plane components of spin−orbit coupling (SOC). We also

observed the in-plane (P and P ) selective population for

H TPP and H F TPP. For H F TPP, some population of the

conﬁguration of the lowest triplet state of H TPP was (LUMO

out-of-plane (P ) sublevel was also generated. Since the n and

← HOMO), but the contribution of the (LUMO+1 ←

HOMO−1) conﬁguration (HOMO−1: the second highest

molecular orbital, LUMO+1: the second lowest unoccupied

molecular orbital) was increased with ﬂuorination. The

increased excitation energy to the triplet state and the

enhanced contribution of the (LUMO+1 ← HOMO−1)

σ orbitals of the F atoms are oriented in various directions,

they can also contribute to the production of the P

2,36

population.

Due to the strong interaction between the d

orbital of the central Zn ion and the π* orbital of the porphyrin

ligand, the strong out-of-plane component of SOC is generated

337

The Journal of Physical Chemistry A

J. Phys. Chem. A 2021, 125, 4334−4340

https://pubs.acs.org/doi/10.1021/acs.jpca.1c01839.

Article

Figure 4. Spin densities (isovalue = 0.00015) of (a) H TPP, (b) H F TPP, (c) H F TPP, (d) ZnTPP, (e) ZnF TPP, and (f) ZnF TPP in the

lowest triplet state calculated by B3LYP/6-31G*.

conﬁguration by the ﬂuorine substitutions are consistent with

4. CONCLUSIONS

the observed blueshift of the phosphorescence peaks (Figure

We have found a design guideline to extend the spin−lattice

). Therefore, we expect that the larger D value by the

relaxation time T , which was previously very short, to longer

ﬂuorine substitutions of the free-base porphyrins is derived

from the mixing of the conﬁgurations.

than 1 μs at room temperature while maintaining the high

polarization (P :P :P = 0:0:1.0) of metalloporphyrins. In

A much shorter T of 0.30 μs was observed for ZnTPP

addition to generating a strong out-of-plane spin−orbit

coupling by using a central metal ion with d orbitals, it is

important to weaken the spin−orbit interaction by introducing

electron-withdrawing substituents to reduce the spin density at

the metal atom. In our previous work, we have reported that an

EPR decay time of a few microseconds is suﬃcient for the

compared with H TPP (9.3 μs). Since the D value of ZnTPP

was smaller than that of H TPP, another relaxation mechanism

that is not dipole−dipole interaction should be occurring to Zn

porphyrins. In the case of organic molecules without heavy

atoms, the eﬀect of the spin−orbit interaction on spin−lattice

39,44

relaxation is known to be insigniﬁcant.

On the other hand,

in the case of Zn porphyrins, the large spin−orbit interaction

between the electrons and the heavy Zn atom may have a

polarization transfer to nuclear spins. Therefore, the

achievement of a spin−lattice relaxation time exceeding 1 μs

in the current work is a critical milestone, while the further

elongation of the spin−lattice relaxation time by optimizing

molecular structures is an important future task. The current

strategy is expected to lead to the creation of a variety of

biocompatible polarizing agents with both high polarization

and long spin−lattice relaxation time, which allows the

hyperpolarization of various biomolecules at room temperature

for NMR and MRI applications.

signiﬁcant eﬀect on spin−lattice relaxation. The T of

ZnF TPP (0.17 μs) was shorter than that of ZnTPP (0.30

μs). The DFT calculation results show that the mixing of the

conﬁgurations were done by ﬂuorine substitution, which may

result in the increase in the D value and the shortening of T₁,

similar to the case of free-base porphyrins.

On the other hand, by increasing the number of ﬂuorine

atoms, a signiﬁcantly longer T of 1.7 μs was observed for

ZnF TPP than ZnTPP and ZnF TPP, which cannot be

explained by the change of the D value. To understand the

observed large elongation of T by the ﬂuorine substitutions on

ASSOCIATED CONTENT

■

Zn porphyrins, we estimated their spin density in the lowest

triplet state. The spin density of Zn atoms in ZnF TPP was

sı Supporting Information

signiﬁcantly reduced compared to other Zn porphyrins (Figure

and Table S3 ). Therefore, the long T of ZnF TPP can be

The Supporting Information is available free of charge at

attributed to the electron-withdrawing ﬂuorine substituents

that reduce the spin density on Zn atoms and weaken the

spin−orbit interaction. In free-base porphyrins, no large

change in spin density was observed due to ﬂuorine

substitution, suggesting that the mixing of conﬁgurations

does not aﬀect the spin density signiﬁcantly.

PXRD patterns, absorption and ﬂuorescence spectra,

absorption/ﬂuorescence/phosphorescence peak posi-

tions, transient absorption decays, shapes of frontier

orbitals, main con ﬁ gurations, and spin densities of

porphyrin triplets (PDF )

338

J. Phys. Chem. A 2021, 125, 4334−4340

The Journal of Physical Chemistry A

Saitama 351-0198, Japan; orcid.org/0000-0001-5566-

Article

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AUTHOR INFORMATION

Corresponding Authors

Kenichiro Tateishi − Cluster for Pioneering Research, RIKEN,

RIKEN Nishina Center for Accelerator-Based Science, Wako,

■

(

Hansson, L.; Lerche, M. H.; Servin, R.; Thaning, M.; Golman, K.

Increase in signal-to-noise ratio of >10,000 times in liquid-state NMR.

Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 10158 −10163.

26X ; Email: kenichiro.tateishi@riken.jp

(3) Golman, K.; Zandt, R.; Thaning, M. Real-time metabolic

imaging. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 11270−11275.

Nobuo Kimizuka − Department of Chemistry and

Biochemistry, Graduate School of Engineering, Center for

Molecular Systems (CMS), Kyushu University, Fukuoka 819-

(4) Gallagher, F. A.; Kettunen, M. I.; Day, S. E.; Hu, D.-E.;

Ardenkjær-Larsen, J. H.; Zandt, R. i.’t.; Jensen, P. R.; Karlsson, M.;

Golman, K.; Lerche, M. H.; et al. Magnetic resonance imaging of pH

395, Japan; orcid.org/0000-0001-8527-151X;

in vivo using hyperpolarized C-labelled bicarbonate. Nature 2008,

53, 940−943.

5) Rossini, A. J.; Zagdoun, A.; Lelli, M.; Lesage, A.; Copéret, C.;

Email: n-kimi@mail.cstm.kyushu-u.ac.jp

(

Nobuhiro Yanai − Department of Chemistry and

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Akio Yamauchi − Department of Chemistry and Biochemistry,

Graduate School of Engineering, Center for Molecular

Systems (CMS), Kyushu University, Fukuoka 819-0395,

Japan

Saiya Fujiwara − Department of Chemistry and Biochemistry,

Graduate School of Engineering, Center for Molecular

Systems (CMS), Kyushu University, Fukuoka 819-0395,

Japan

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solid-state maser. Nature 2012, 488, 353−356.

Koki Nishimura − Department of Chemistry and

Biochemistry, Graduate School of Engineering, Center for

Molecular Systems (CMS), Kyushu University, Fukuoka 819-

(

Alford, N. M. Enhanced magnetic Purcell effect in room-temperature

395, Japan

masers. Nat. Commun. 2015, 6, 6215.

Yoichi Sasaki − Department of Chemistry and Biochemistry,

Graduate School of Engineering, Center for Molecular

Systems (CMS), Kyushu University, Fukuoka 819-0395,

Japan

Tomohiro Uesaka − Cluster for Pioneering Research, RIKEN,

RIKEN Nishina Center for Accelerator-Based Science, Wako,

Saitama 351-0198, Japan

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(

Complete contact information is available at:

https://pubs.acs.org/10.1021/acs.jpca.1c01839

(

Kitagawa, M. Room temperature hyperpolarization of nuclear spins in

bulk. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 7527−7530.

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K.; Kimizuka, N.; Yanai, N. Dynamic Nuclear Polarization of Metal-

Organic Frameworks Using Photoexcited Triplet Electrons. J. Am.

Chem. Soc. 2018, 140, 15606−15610.

Author Contributions

A.Y. and S.F. contributed equally.

Notes

The authors declare no competing ﬁnancial interest.

(17) Nishimura, K.; Kouno, H.; Kawashima, Y.; Orihashi, K.;

Fujiwara, S.; Tateishi, K.; Uesaka, T.; Kimizuka, N.; Yanai, N.

Materials chemistry of triplet dynamic nuclear polarization. Chem.

Commun. 2020, 56, 7217−7232.

ACKNOWLEDGMENTS

■

We are grateful to Dr. Yuki Kurashige of Kyoto University for

his useful suggestions on DFT calculations. This work was

partly supported by the JST-PRESTO program on “Creation

of Life Science Basis by Using Quantum Technology” (grant

number: JPMJPR18GB), JSPS KAKENHI (grant numbers:

JP20H02713, JP20K21211, and JP20H05676), The Shinnihon

Foundation of Advanced Medical Treatment Research,

RIKEN-Kyushu Univ Science and Technology Hub Collabo-

rative Research Program, the RIKEN Cluster for Science,

Technology and Innovation Hub (RCSTI), and the RIKEN

Pioneering Project “Dynamic Structural Biology”.

(

18) Matsuoka, H.; Retegan, M.; Schmitt, L.; Höger, S.; Neese, F.;

Schiemann, O. Time-Resolved Electron Paramagnetic Resonance and

Theoretical Investigations of Metal-Free Room-Temperature Triplet

Emitters. J. Am. Chem. Soc. 2017, 139, 12968−12975.

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(20) Hamachi, T.; Nishimura, K.; Kouno, H.; Kawashima, Y.;

Tateishi, K.; Uesaka, T.; Kimizuka, N.; Yanai, N. Porphyrins as

Versatile, Aggregation-Tolerant, and Biocompatible Polarizing Agents

for Triplet Dynamic Nuclear Polarization of Biomolecules. J. Phys.

Chem. Lett. 2021, 12, 2645−2650.

(21) Gonen, O.; Levanon, H. Time-Resolved EPR Spectroscopy of

Electron Spin Polarized ZnTPP Triplets Oriented in a Liquid Crystal.

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