Oxygen-17 dynamic nuclear polarisation enhanced solid-state NMR spectroscopy at 18.8 T

Abstract

We report ¹⁷O dynamic nuclear polarisation (DNP) enhanced solid-state NMR experiments at 18.8 T. Several formulations were investigated on the Mg(OH)₂ compound. A signal enhancement factor of 17 could be obtained when the solid particles were incorporated into a glassy o-terphenyl matrix doped with BDPA using the Overhauser polarisation transfer scheme whilst the cross effect mechanism enabled by TEKPol yielded a slightly lower enhancement but more time efficient data acquisition.

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Solid-state nuclear magnetic resonance (NMR) spectroscopy involving quadrupolar nuclei, which account for more than 75% of all active nuclei, has become an essential analytical technique for the atomic-scale characterization of a wide range of inorganic, hybrid and organic materials such as glasses, zeolites, surface catalysts, metal–organic frameworks, battery materials or pharmaceuticals to name but a few.^1–4 While for spin I = 1/2 nuclei, the dipolar and chemical shift anisotropy (CSA) interactions are fully averaged out by magic angle spinning (MAS),⁵ producing sharp lines positioned at the isotropic chemical shifts, the second-order quadrupolar interaction observed for spin I > 1/2 is not fully removed by MAS,^6–8 yielding field-dependent shifts and broadened NMR lines. These are some of the major limitations to the widespread applicability of quadrupolar NMR.^7–10 The second-order quadrupolar broadening is inversely proportional to the strength of the external field B₀ and therefore very high magnetic fields allow high spectral resolution.¹¹ In parallel, a range of NMR experiments have been designed to completely average out the second-order broadenings. They are based on technically challenging NMR probes permitting sample double rotation (DOR)¹² or dynamic angle spinning (DAS),¹³ or consist of combining conventional MAS with the manipulation of the different nuclear spin transitions in techniques such as multiple quantum MAS (MQMAS)¹⁴ and satellite transition MAS (STMAS).¹⁵ Despite these sophisticated approaches and the increasing availability of high magnetic fields, the sensitivity of quadrupolar NMR remains often low for nuclei of poor natural abundance and/or of low gyromagnetic ratio γ, requiring prohibitively long experimental times (days) and/or expensive isotopic enrichment.

A spectacular approach to increase the solid-state NMR sensitivity is dynamic nuclear polarisation (DNP),^16,17 which involves the microwave-driven transfer of the large polarisation of unpaired electrons^18–21 (e.g. added to the samples as paramagnetic polarising agents)^22–28 to the surrounding nuclei in a glass-forming matrix at cryogenic temperatures, typically 100 K or below.^29,30 The drastic signal enhancements permitted by DNP have opened up ground breaking applications on an ever increasing range of systems^31–37 and the approach has been reviewed recently.^38–42 Recent developments have extended the temperature range in which the experiments can be conducted (>200 K).^24,43,44 One of the biggest drawbacks to MAS DNP under high magnetic fields results from the unfavorable evolution of the NMR signal enhancements with B₀ which scales as B₀⁻¹ and B₀⁻² for the two most common polarization transfer mechanisms, the cross effect (CE) and solid effect, respectively. However, large signal enhancements (>80) have recently been obtained at 18.8 T using the Overhauser effect (OE) DNP mechanism^16,44,45 and the narrow-line 1,3-bisdiphenylene-2-phenylallyl (BDPA) radical.⁴⁶ The apparent linear scaling of the OE signal enhancement with B₀ currently represents one of the most attractive approaches for DNP under very high fields and is an exciting opportunity for quadrupolar nuclei.

A quadrupolar nucleus of particular interest is ¹⁷O due to the ubiquity of oxygen in materials chemistry and biochemistry. However, its extremely low natural abundance (0.037%) makes its NMR detection near impossible unless samples are ¹⁷O-enriched.⁴⁷ The feasibility of MAS DNP on ¹⁷O has been recently reported.^48–52 In particular, we demonstrated that high S/N natural abundance ¹⁷O cross polarization (CP) MAS NMR spectra could be obtained on nanoparticles,⁴⁹ while more recently, the detection of ¹⁷O DNP NMR spectra of surface hydroxyl sites on mesoporous silica in natural abundance was reported.⁵² All these experiments were recorded at 9.4 T and relied on the CE mechanism with bTbk²³ or TEKPol²⁴ radicals in tetrachloroethane (TCE)⁵³ as a polarising agent.

Here, we show that DNP can be applied to efficiently enhance the ¹⁷O MAS NMR signal of Mg(OH)₂ in a glassy matrix at 18.8 T, via both the CE and OE mechanisms. We show that CE DNP (using TEKPol/TCE) gives enhancements up to ε_O CP = 14, and allows for the fast acquisition of the ¹⁷O spectrum of Mg(OH)₂ at natural abundance. Similarly, using the OE scheme, we demonstrate that polarisation can be transferred from BDPA in a glassy matrix (10% o-terphenyl (OTP), 90% o-terphenyl-d₁₄ (OTP-d₁₄)) to Mg(OH)₂ with excellent efficiency, giving enhancements of ε_O CP = 17. Both CP^13,54 and PRESTO-II⁵⁵ (herein referred to as PRESTO) experiments are reported.

Fig. 1a shows the 18.8 T DNP enhanced ¹⁷O MAS NMR spectrum of ¹⁷O enriched Mg(OH)₂ (i.e. Mg(¹⁷OH)₂), impregnated with TEKPol in TCE under the CE condition at ν₀(¹H) = 800.130 MHz. The ¹H enhancement obtained on TCE (ε_H = 23) is transferred to the protons of Mg(¹⁷OH)₂via spin diffusion and subsequently to the ¹⁷O nuclei via a selective CP Hahn echo to yield a maximum signal enhancement of ε_O CP = 14. In an attempt to be more representative in evaluating the increase in the NMR signal with DNP, we have estimated an overall DNP gain (see Section S2 of the ESI† for calculation details)^{29,41,56–58} to compare the benefit of 18.8 T DNP with standard NMR at 18.8 and 9.4 T. The ε_O CP = 14 of TEKPol in a TCE matrix translates into a of 72 at 18.8 T (Table 1), demonstrating substantial CE DNP efficiency despite the B₀⁻¹ dependency of the CE. It is worth noting that on freshly prepared samples lower enhancements were observed (ε_H = 16, ε_O CP = 9) and that the maximum values reported above were obtained after holding the sample at 253 K for 20 h before freeze–thaw cycling (see the ESI†) and inserting it into the probe (Fig. 1 and Fig. S4, ESI†).

Fig. 1 (a–d) ¹⁷O CE and (e and f) ¹⁷O OE MAS DNP at 18.8 T. CP (left column) and PRESTO (right column) spectra of Mg(¹⁷OH)₂ (a, b, e and f) and natural abundance Mg(OH)₂ (c and d) have been recorded at ν₀(¹H) = 800.130 MHz for the CE and at ν₀(¹H) = 800.215 MHz for the OE with microwave irradiation (μw) at ν₀(e⁻) = 527 GHz (green) at T = 131 K and without μw (red) at T = 115 K. For the CE, both samples were impregnated with 16 mM TEKPol in TCE and paramagnetic O₂ removed by freeze–thaw cycles (see Section S1 in the ESI† for details). For the OE, the sample was prepared with a matrix containing 1.4 wt% BPDA in 90 : 10 OTP-d₁₄ : OTP and five freeze–melt cycles (see the ESI†). Spectra (a and b), (c and d) and (e and f) are plotted in absolute intensity. The μw off PRESTO spectrum of Mg(OH)₂ was not recorded. Asterisks (*) denote spinning sidebands.

Table 1 A comparison of DNP enhancements measured at 18.8 T using CP Hahn echo on Mg(¹⁷OH)₂ in a range of polarisation matrices (see the ESI). n/a indicates that these experiments were not run

Matrix	TCE	OTP	OTP/OTP-d14 (50 : 50)	OTP/OTP-d14 (90 : 10)	OTP/OTP-d14 (95 : 5)
Cross effect (1.3 wt% TEKPol)
ε O CP	14	6	12	11	12
	72	38	54	71	53
Overhauser effect (1.4 wt% BDPA)
ε O CP	5	2	n/a	17	3
	13	24	n/a	34	9

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It was recently shown that the use of a PRESTO (phase-shifted recoupling effects a smooth transfer of order) sequence⁵⁵ is more efficient for the ¹H–¹⁷O heteronuclear polarization transfer and yields for Mg(OH)₂, Ca(OH)₂ and silica surfaces⁵² line-shapes closer to simulations than with CP, including those in the context of MAS DNP.⁵⁹Fig. 1b shows the corresponding CE DNP ¹⁷O PRESTO spectra on the same Mg(¹⁷OH)₂ sample at 18.8 T. A maximum signal enhancement of ε_O PRESTO = 19 was obtained and is slightly higher than ε_O CP (14). However, in our hands and at 18.8 T, the overall signal intensity is lower than with ¹⁷O CP as predicted.⁵⁵ We also note that the asymmetric line shape and dephased spinning side bands are exacerbated by the addition of microwave irradiation (Fig. S3, ESI†). The lower intensity of PRESTO vs. CP and line shape disparity is also observed using the OE (Fig. 1e and f). The ¹⁷O signal enhancement factors obtained open the way to obtain natural abundance spectra using the CE at 18.8 T, and we were able to record ¹⁷O CP and PRESTO MAS NMR spectra of Mg(OH)₂ relatively quickly in 82 minutes (Fig. 1c and d), while the corresponding microwave off spectra show no signal (Fig. 1c).

Sample formulation is essential to achieve high DNP enhancement factors, and in particular the choice of the solvent is often critical.⁶⁰ It has been shown that OTP forms a highly effective glassy matrix⁶¹ and could be polarized by CE DNP with TEKPol and even more efficiently by OE DNP with BDPA.^44,45,61,62 In the next paragraphs, we report ¹⁷O enhancement factors using OTP with both TEKPol and BDPA as the polarising matrix. The Mg(¹⁷OH)₂ samples were prepared by grinding them with a mixture of protonated and fully deuterated OTP of various ratios containing TEKPol or BDPA radicals (1.3–1.4 wt% equivalent to 34 mM electron spins) followed by multiple cycles (typically 5) between a melt at ∼343 K⁶¹ and a frozen state at 77 K (in liquid N₂) before the melt was inserted into the precooled NMR probe at ∼115 K (see the ESI,† Section S1, for detailed sample preparation).

Fig. 2 plots the ¹³C and ¹⁷O CPMAS CE DNP signal enhancements of the Mg(¹⁷OH)₂/TEKPol/OTP glass matrix as a function of the percentage of OTP-d₁₄. The ¹³C and ¹⁷O enhancements correspond to the NMR signal amplification of, respectively, the OTP matrix and the Mg(¹⁷OH)₂ particles. The data show that with a fully protonated OTP matrix, the signal enhancements are similar (ε_C CP = 8 and ε_O CP = 6), revealing that the polarisation is efficiently transferred from the glassy matrix to Mg(¹⁷OH)₂ and that the polarisation is evenly distributed across the particles by ¹H–¹H spin diffusion mechanisms.⁶³ However, the enhancements are lower than with >50% OTP-d₁₄ matrices (vide infra) and are due to both the large size of the ¹H bath and the short ¹H polarisation time τ_DNP (∼3 s), yielding a fast decay of the enhanced polarization by relaxation before it can be transferred to Mg(¹⁷OH)₂. Increasing the content of OTP-d₁₄ in the matrix improves the signal enhancements of the sample (Table 1 and Fig. S2, ESI†), in agreement with the previous literature showing that deuteration improves DNP enhancements,^60,64 due to the decrease in ¹H–¹H spin diffusion and associated longer ¹H τ_DNP (∼31 s). This increase in enhancement plateaued by ε_O CP after 50% OTP-d₁₄ and dropped off beyond 90% OTP-d₁₄ in , suggesting that for the CE with TEKPol/OTP at 18.8 T, a 90 : 10 mixture of OTP-d₁₄ and OTP may be optimal for the signal to noise ratio per unit time per unit weight.

Fig. 2 ε _O CP (black) and ε_C CP (blue) measured on Mg(¹⁷OH)₂ and the OTP matrix (with the radical and concentration in brackets) at both CE (square) and OE (triangle) magnetic field strength B₀ positions as a function of the OTP-d₁₄ component of the OTP matrix.

Fig. 2 also displays the ¹³C and ¹⁷O DNP signal enhancements under the OE condition of Mg(¹⁷OH)₂ prepared in an OTP matrix (with various concentrations of OTP-d₁₄) and using monoradical BDPA as a polarising agent, providing a comparison between CE and OE mechanisms at 18.8 T. At 90 : 10 OTP-d₁₄ : OTP, large matrix enhancements are observed (ε_H = 44, ε_C CP = 71), and subsequently the ¹⁷O enhancement of Mg(¹⁷OH)₂ (ε_O CP = 17, Fig. 1e and 2) is substantially larger than with BDPA in a TCE matrix (ε_O CP = 5, Table 1 and Fig. S5, ESI†). The multiple freeze–melt cycles appear to improve the quality of the glassy matrix, and thus improve the enhancement values on the OTP matrix and sample, compared to directly inserting the sample into the probe (Fig. S5, ESI†). Contrary to the results observed under the CE condition with TEKPol, a further increase in OTP-d₁₄ concentration to 95% yields a decrease in matrix enhancement factors (ε_H = 21, ε_C CP = 30), and very limited transfer of polarisation to the ¹⁷O of Mg(¹⁷OH)₂.

Despite the maximum ε_O CP reported in Table 1 being for Mg(¹⁷OH)₂/BDPA/90 : 10 OTP-d₁₄ : OTP, the corresponding value is still lower than the maximum values for ¹⁷O obtained with the CE (using the same matrix). This is due to the much shorter τ_DNP in the CE system (∼11 s) than that of the OE in OTP-d₁₄ (∼31 s), allowing for more scans to be accumulated per unit time.

In conclusion, we have shown that it is possible to transfer the OE DNP enhanced polarisation of OTP doped with BDPA to the ¹⁷O spins of Mg(¹⁷OH)₂ hydroxides at 18.8 T with good efficiency by mixing both solids together. We have also demonstrated that despite the lower ε values obtained with the CE, TEKPol/OTP and TEKPol/TCE provide time efficient signal enhancement. This has enabled a large gain in absolute sensitivity, permitting the challenging detection of natural abundance ¹⁷O NMR spectra. This study paves the way to a wider application of ¹⁷O DNP enhanced NMR under a high magnetic field and its transposition to other quadrupolar nuclei in a variety of crystalline and amorphous inorganic materials with strong second-order quadrupolar broadenings hampering the spectral resolution under a low field.

Financial support from the EPSRC for a DTA studentship for N. J. B. and grant EP/M00869X/1 to F. B., ERC Advanced Grant No. 320860 for L. E. and EQUIPEX contract ANR-10-EQPX-47-01 for A. L. and L. E. is acknowledged. We thank Dr Sachin R. Chaudhari (CRMN Lyon), Kenneth K. Inglis (University of Liverpool), and Dr O. Ouari and Prof. P. Tordo (Aix-Marseille Université, CNRS) for valuable technical assistance, sample preparation, and radicals, respectively. F. B. thanks the TGIR-RMN-THC Fr3050 CNRS for access to the 18.8 T DNP NMR facility at the CRMN. The experimental data are provided as a supporting dataset from the University of Liverpool Data Catalogue portal at http://datacat.liverpool.ac.uk/245/.

Notes and references

1. D. D. Laws, H.-M. L. Bitter and A. Jerschow, Angew. Chem., Int. Ed., 2002, 41, 3096.
2. F. Blanc, C. Copéret, A. Lesage and L. Emsley, Chem. Soc. Rev., 2008, 37, 518.
3. S. P. Brown and H. W. Spiess, Chem. Rev., 2001, 101, 4125.
4. J. Gath, G. L. Hoaston, R. L. Vold, R. Berthoud, C. Copéret, M. Grellier, S. Sabo-Etienne, A. Lesage and L. Emsley, Phys. Chem. Chem. Phys., 2009, 11, 6962.
5. E. R. Andrew, A. Bradbury and R. G. Eades, Nature, 1958, 182, 1659.
6. M. E. Smith and E. R. H. van Eck, Prog. Nucl. Magn. Reson. Spectrosc., 1999, 34, 159.
7. S. E. Ashbrook, Phys. Chem. Chem. Phys., 2009, 11, 6892.
8. NMR of Quadrupolar Nuclei in Solid Materials, ed. R. E. Wasylishen, S. E. Ashbrook and S. Wimperis, Wiley, 2012, pp. 3–17.
9. S. E. Ashbrook and D. M. Dawson, Acc. Chem. Res., 2013, 46, 1964.
10. S. E. Ashbrook and S. Sneddon, J. Am. Chem. Soc., 2014, 136, 15440.
11. Z. Gan, P. Gor'kov, T. A. Cross, A. Samoson and D. Massiot, J. Am. Chem. Soc., 2002, 124, 5634.
12. A. Samoson, E. Lippmaa and A. Pines, Mol. Phys., 1988, 65, 1013.
13. K. T. Mueller, B. Q. Sun, G. C. Chingas, J. W. Zwanziger, T. Terao and A. Pines, J. Magn. Reson., 1990, 86, 470.
14. A. Medek, J. S. Harwood and L. Frydman, J. Am. Chem. Soc., 1995, 117, 12779.
15. Z. Gan, J. Am. Chem. Soc., 2000, 122, 3242.
16. A. W. Overhauser, Phys. Rev., 1953, 92, 411.
17. T. R. Carver and C. P. Slichter, Phys. Rev., 1956, 102, 975.
18. D. A. Hall, D. C. Maus, G. J. Gerfen, S. J. Inati, L. R. Becerra, F. W. Dahlquist and R. G. Griffin, Science, 1997, 276, 930.
19. T. Maly, G. T. Debelouchina, V. S. Bajaj, K.-N. Hu, C.-G. Joo, M. L. Mak-Jurkauskas, J. R. Sirigiri, P. C. A. van der Wel, J. Herzfeld, R. J. Temkin and R. G. Griffin, J. Chem. Phys., 2008, 128, 52211.
20. M. Rosay, L. Tometich, S. Pawsey, R. Bader, R. Schauwecker, M. Blank, P. M. Borchard, S. R. Cauffman, K. L. Felch, R. T. Weber, R. J. Temkin, R. G. Griffin and W. E. Maas, Phys. Chem. Chem. Phys., 2010, 12, 5850.
21. M. Rosay, M. Blank and F. Engelke, J. Magn. Reson., 2016, 264, 88.
22. K.-N. Hu, Solid State Nucl. Magn. Reson., 2011, 40, 31.
23. Y. Matsuki, T. Maly, O. Ouari, H. Karoui, F. Le Moigne, E. Rizzato, S. Lyubenova, J. Herzfeld, T. Prisner, P. Tordo and R. G. Griffin, Angew. Chem., Int. Ed., 2009, 48, 4996.
24. A. Zagdoun, G. Casano, O. Ouari, M. Schwarzwälder, A. J. Rossini, F. Aussenac, M. Yulikov, G. Jeschke, C. Copéret, A. Lesage, P. Tordo and L. Emsley, J. Am. Chem. Soc., 2013, 135, 12790.
25. C. Sauvée, M. Rosay, G. Casano, F. Aussenac, R. T. Weber, O. Ouari and P. Tordo, Angew. Chem., Int. Ed., 2013, 125, 11058.
26. B. Corzilius, A. A. Smith, A. B. Barnes, C. Luchinat, I. Bertini and R. G. Griffin, J. Am. Chem. Soc., 2011, 133, 5648.
27. Q. Z. Ni, E. Daviso, T. V. Can, E. Markhasin, S. K. Jawla, T. M. Swager, R. J. Temkin, J. Herzfeld and R. G. Griffin, Acc. Chem. Res., 2013, 46, 1933.
28. D. J. Kubicki, G. Casano, M. Schwarzwälder, S. Abel, C. Sauvée, K. Ganesan, M. Yulikov, A. J. Rossini, G. Jeschke, C. Copéret, A. Lesage, P. Tordo, O. Ouari and L. Emsley, Chem. Sci., 2016, 7, 550.
29. K. R. Thurber, W.-M. Yau and R. Tycko, J. Magn. Reson., 2010, 204, 303.
30. E. Bouleau, P. Saint-Bonnet, F. Mentink-Vigier, H. Takahashi, J.-F. Jacquot, M. Bardet, F. Aussenac, A. Purea, F. Engelke, S. Hediger, D. Lee and G. De Paëpe, Chem. Sci., 2015, 6, 6806.
31. A. Lesage, M. Lelli, D. Gajan, M. A. Caporini, V. Vitzthum, P. Miéville, J. Alauzun, A. Roussey, C. Thieuleux, A. Mehdi, G. Bodenhausen, C. Copéret and L. Emsley, J. Am. Chem. Soc., 2010, 132, 15459.
32. M. Lelli, D. Gajan, A. Lesage, M. A. Caporini, V. Vitzthum, P. Miéville, F. Héroguel, F. Rascón, A. Roussey, C. Thieuleux, M. Boualleg, L. Veyre, G. Bodenhausen, C. Copéret and L. Emsley, J. Am. Chem. Soc., 2011, 133, 2104.
33. D. Lee, H. Takahashi, A. S. L. Thankamony, J.-P. Dacquin, M. Bardet, O. Lafon and G. De Paëpe, J. Am. Chem. Soc., 2012, 134, 18491.
34. F. Blanc, S. Y. Chong, T. O. McDonald, D. J. Adams, S. Pawsey, M. A. Caporini and A. I. Cooper, J. Am. Chem. Soc., 2013, 135, 15290.
35. F. Ziarelli, M. Casciola, M. Pica, A. Donnadio, F. Aussenac, C. Sauvée, D. Capitani and S. Viel, Chem. Commun., 2014, 50, 10137.
36. F. Blanc, L. Sperrin, D. Lee, R. Dervişoğlu, Y. Yamazaki, S. M. Haile, G. De Paëpe and C. P. Grey, J. Phys. Chem. Lett., 2014, 5, 2431.
37. T.-C. Ong, W.-C. Liao, V. Mougel, D. Gajan, A. Lesage, L. Emsley and C. Copéret, Angew. Chem., Int. Ed., 2016, 55, 4743.
38. A. J. Rossini, A. Zagdoun, M. Lelli, A. Lesage, C. Copéret and L. Emsley, Acc. Chem. Res., 2013, 46, 1942.
39. Ü. Akbey and H. Oschkinat, J. Magn. Reson., 2016, 269, 213.
40. T. Polenova, R. Gupta and A. Goldbourt, Anal. Chem., 2015, 87, 5458.
41. D. Lee, S. Hediger and G. De Paëpe, Solid State Nucl. Magn. Reson., 2015, 66–67, 6.
42. J.-H. Ardenkjaer-Larsen, G. S. Boebinger, A. Comment, S. Duckett, A. S. Edison, F. Engelke, C. Griesinger, R. G. Griffin, C. Hilty, H. Maeda, G. Parigi, T. Prisner, E. Ravera, J. van Bentum, S. Vega, A. Webb, C. Luchinat, H. Schwalbe and L. Frydman, Angew. Chem., Int. Ed., 2015, 54, 9162.
43. Ü. Akbey, A. H. Linden and H. Oschkinat, Appl. Magn. Reson., 2012, 43, 81.
44. M. Lelli, S. R. Chaudhari, D. Gajan, G. Casano, A. J. Rossini, O. Ouari, P. Tordo, A. Lesage and L. Emsley, J. Am. Chem. Soc., 2015, 137, 14558.
45. T. V. Can, M. A. Caporini, F. Mentink-Vigier, B. Corzilius, J. J. Walish, M. Rosay, W. E. Maas, M. Baldus, S. Vega, T. M. Swager and R. G. Griffin, J. Chem. Phys., 2014, 141, 64202.
46. C. F. Koelsch, J. Am. Chem. Soc., 1957, 79, 4439.
47. S. E. Ashbrook and M. E. Smith, Chem. Soc. Rev., 2006, 35, 718.
48. V. K. Michaelis, E. Markhasin, E. Daviso, J. Herzfeld and R. G. Griffin, J. Phys. Chem. Lett., 2012, 3, 2030.
49. F. Blanc, L. Sperrin, D. A. Jefferson, S. Pawsey, M. Rosay and C. P. Grey, J. Am. Chem. Soc., 2013, 135, 2975.
50. V. K. Michaelis, B. Corzilius, A. A. Smith and R. G. Griffin, J. Phys. Chem. B, 2013, 117, 14894.
51. F. A. Perras, T. Kobayashi and M. Pruski, J. Am. Chem. Soc., 2015, 137, 8336.
52. F. A. Perras, U. Chaudhary, I. I. Slowing and M. Pruski, J. Phys. Chem. C, 2016, 120, 11535.
53. A. Zagdoun, A. J. Rossini, D. Gajan, A. Bourdolle, O. Ouari, M. Rosay, W. E. Maas, P. Tordo, M. Lelli, L. Emsley, A. Lesage and C. Copéret, Chem. Commun., 2012, 48, 654.
54. A. Pines, M. G. Gibby and J. S. Waugh, Chem. Phys. Lett., 1972, 15, 373.
55. X. Zhao, W. Hoffbauer, J. Schmedt auf der Günne and M. H. Levitt, Solid State Nucl. Magn. Reson., 2004, 26, 57.
56. A. J. Rossini, A. Zagdoun, M. Lelli, D. Gajan, F. Rascón, M. Rosay, W. E. Maas, C. Copéret, A. Lesage and L. Emsley, Chem. Sci., 2012, 3, 108.
57. A. J. Rossini, A. Zagdoun, F. Hegner, M. Schwarzwälder, D. Gajan, C. Copéret, A. Lesage and L. Emsley, J. Am. Chem. Soc., 2012, 134, 16899.
58. H. Takahashi, D. Lee, L. Dubois, M. Bardet, S. Hediger and G. De Paëpe, Angew. Chem., Int. Ed., 2012, 51, 11766.
59. F. A. Perras, T. Kobayashi and M. Pruski, Phys. Chem. Chem. Phys., 2015, 17, 22616.
60. Ü. Akbey, W. T. Franks, A. Linden, S. Lange, R. G. Griffin, B.-J. van Rossum and H. Oschkinat, Angew. Chem., Int. Ed., 2010, 49, 7803.
61. K. A. Earle, J. K. Moscicki, A. Polimeno and J. H. Freed, J. Chem. Phys., 1997, 106, 9996.
62. T.-C. Ong, M. L. Mak-Jurkauskas, J. J. Walish, V. K. Michaelis, B. Corzilius, A. A. Smith, A. M. Clausen, J. C. Cheetham, T. M. Swager and R. G. Griffin, J. Phys. Chem. B, 2013, 117, 3040.
63. M. Negoro, K. Nakayama, K. Tateishi, A. Kagawa, K. Takeda and M. Kitagawa, J. Chem. Phys., 2010, 133, 154504.
64. A. Zagdoun, A. J. Rossini, M. P. Conley, W. R. Grüning, M. Schwarzwälder, M. Lelli, W. T. Franks, H. Oschkinat, C. Copéret, L. Emsley and A. Lesage, Angew. Chem., Int. Ed., 2013, 52, 1222.

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Footnote

† Electronic supplementary information (ESI) available: Materials and methods, DNP sensitivity gain and additional figures. See DOI: 10.1039/c6cc09743j

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