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Orientational Selectivity in Pulsed-EPR Does Not Have to be Complicated

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Abstract

The development of rigid spin labels and high-frequency spectrometers have improved the capabilities of pulsed-EPR distance measurements in the field of structural biology. Rigid spin labels provide distance constraints that better report on the conformations of the protein or DNA backbone. Additionally, spectrometers at high frequencies improve the sensitivity of pulsed-EPR, even enabling experiments at concentrations close to cellular conditions. Unfortunately, these advents can come with a complication in that the microwave pulse cannot completely sample all orientations of the spins. Consequently, insufficient sampling biases the dipolar frequencies in a manner that depends on the relative orientations of the intramolecularly interacting spins. These relative orientations are generally unknown a priori in a bilabeled biomolecule. This biasing effect, dubbed ‘orientational selectivity,’ is a bottleneck to interpreting distance measurements from the dipolar signal. This review provides an overview of orientational selectivity in the context of distance measurements using Double Electron–Electron Resonance. First, we discuss the genesis of orientational selectivity and briefly overview the literature on spin labels that have manifested orientational selectivity. Second, we outline the various strategies to account for orientational selectivity effects for extracting the distance constraints. Finally, we showcase a new perspective on analyzing orientational selectivity and designing efficient experimental schemes for overcoming orientational selectivity.

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The authors confirm that the datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  1. A.D. Milov, A.B. Ponomarev, Y.D. Tsvetkov, Chem. Phys. Lett. 110, 67 (1984)

    CAS  Google Scholar 

  2. A.D. Milov, A.G. Maryasov, Y.D. Tsvetkov, Appl Magn Reson 15, 107 (1998)

    CAS  Google Scholar 

  3. C. Altenbach, T. Marti, H.G. Khorana, W.L. Hubbell, Science 248, 1088 (1990)

    CAS  PubMed  Google Scholar 

  4. W.L. Hubbell, C.J. López, C. Altenbach, Z. Yang, Curr. Opin. Struct. Biol. 23, 725 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  5. S. Milikisyants, F. Scarpelli, M.G. Finiguerra, M. Ubbink, M. Huber, J. Magn. Reson. 201, 48 (2009)

    CAS  PubMed  Google Scholar 

  6. M. Pannier, S. Veit, A. Godt, G. Jeschke, H.W. Spiess, J. Magn. Reson. 142, 331 (2000)

    CAS  PubMed  Google Scholar 

  7. P.P. Borbat, J.H. Freed, Chem. Phys. Lett. 313, 145 (1999)

    CAS  Google Scholar 

  8. L.V. Kulik, S.A. Dzuba, I.A. Grigoryev, Y.D. Tsvetkov, Chem. Phys. Lett. 343, 315 (2001)

    CAS  Google Scholar 

  9. G. Jeschke, M. Pannier, A. Godt, H.W. Spiess, Chem. Phys. Lett. 331, 243 (2000)

    CAS  Google Scholar 

  10. S. Pribitzer, M. Sajid, M. Hülsmann, A. Godt, G. Jeschke, J. Magn. Reson. 282, 119 (2017)

    CAS  PubMed  Google Scholar 

  11. M. Bonora, J. Becker, S. Saxena, J. Magn. Reson. 170, 278 (2004)

    CAS  PubMed  Google Scholar 

  12. A.K. Upadhyay, P.P. Borbat, J. Wang, J.H. Freed, D.E. Edmondson, Biochemistry 47, 1554 (2008)

    CAS  PubMed  Google Scholar 

  13. A. Gamble Jarvi, T.F. Cunningham, S. Saxena, Phys. Chem. Chem. Phys. 21, 10238 (2019)

    CAS  PubMed  Google Scholar 

  14. D. Abdullin, N. Florin, G. Hagelueken, O. Schiemann, Angew. Chem. Int. Ed. 54, 1827 (2015)

    CAS  Google Scholar 

  15. B.J. Gaffney, M.D. Bradshaw, S.D. Frausto, F. Wu, J.H. Freed, P. Borbat, Biophys. J. 103, 2134 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  16. D.M. Yin, J.S. Hannam, A. Schmitz, O. Schiemann, G. Hagelueken, M. Famulok, Angew. Chem. Int. Ed. 56, 8417 (2017)

    CAS  Google Scholar 

  17. D. Nguyen, D. Abdullin, C.A. Heubach, T. Pfaffeneder, A. Nguyen, A. Heine, K. Reuter, F. Diederich, O. Schiemann, G. Klebe, Angew. Chem. Int. Ed. 60, 23419 (2021)

    CAS  Google Scholar 

  18. T.E. Assafa, K. Anders, U. Linne, L.-O. Essen, E. Bordignon, Structure 26, 1534 (2018)

    CAS  PubMed  Google Scholar 

  19. Z. Liu, T.M. Casey, M.E. Blackburn, X. Huang, L. Pham, I.M.S. de Vera, J.D. Carter, J.L. Kear-Scott, A.M. Veloro, L. Galiano, G.E. Fanucci, Phys. Chem. Chem. Phys. 18, 5819 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  20. I. Hänelt, D. Wunnicke, E. Bordignon, H.-J. Steinhoff, D.J. Slotboom, Nat. Struct. Mol. Biol. 20, 210 (2013)

    PubMed  Google Scholar 

  21. O. Dalmas, P. Sompornpisut, F. Bezanilla, E. Perozo, Nat. Commun. 5, 3590 (2014)

    PubMed  Google Scholar 

  22. B. Verhalen, R. Dastvan, S. Thangapandian, Y. Peskova, H.A. Koteiche, R.K. Nakamoto, E. Tajkhorshid, H.S. Mchaourab, Nature 543, 738 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  23. B. Joseph, A. Sikora, D.S. Cafiso, J. Am. Chem. Soc. 138, 1844 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  24. K. Stone, J. Townsend, J. Sarver, P. Sapienza, S. Saxena, L. Jen-Jacobson, Angew. Chem. Int. Ed. 120, 10346 (2008)

    Google Scholar 

  25. T. Hett, T. Zbik, S. Mukherjee, H. Matsuoka, W. Bönigk, D. Klose, C. Rouillon, N. Brenner, S. Peuker, R. Klement, H.-J. Steinhoff, H. Grubmüller, R. Seifert, O. Schiemann, U.B. Kaupp, J. Am. Chem. Soc. 143, 6981 (2021)

    CAS  PubMed  Google Scholar 

  26. S. Milikisiyants, S. Wang, R.A. Munro, M. Donohue, M.E. Ward, D. Bolton, L.S. Brown, T.I. Smirnova, V. Ladizhansky, A.I. Smirnov, J. Mol. Biol. 429, 1903 (2017)

    CAS  PubMed  Google Scholar 

  27. S.-Y. Park, P.P. Borbat, G. Gonzalez-Bonet, J. Bhatnagar, A.M. Pollard, J.H. Freed, A.M. Bilwes, B.R. Crane, Nat. Struct. Mol. Biol. 13, 400 (2006)

    CAS  PubMed  Google Scholar 

  28. S. Valera, K. Ackermann, C. Pliotas, H. Huang, J.H. Naismith, B.E. Bode, Chem. Eur. J 22, 4700 (2016)

    CAS  PubMed  Google Scholar 

  29. H.A. DeBerg, J.R. Bankston, J.C. Rosenbaum, P.S. Brzovic, W.N. Zagotta, S. Stoll, Structure 23, 734 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  30. G.E. Fanucci, K.A. Coggshall, N. Cadieux, M. Kim, R.J. Kadner, D.S. Cafiso, Biochemistry 42, 1391 (2003)

    CAS  PubMed  Google Scholar 

  31. S. Ketter, A. Gopinath, O. Rogozhnikova, D. Trukhin, V.M. Tormyshev, E.G. Bagryanskaya, B. Joseph, Chem. Eur. J 27, 2299 (2021)

    CAS  PubMed  Google Scholar 

  32. I.D. Sahu, R.M. McCarrick, K.R. Troxel, R. Zhang, H.J. Smith, M.M. Dunagan, M.S. Swartz, P.V. Rajan, B.M. Kroncke, C.R. Sanders, G.A. Lorigan, Biochemistry 52, 6627 (2013)

    CAS  PubMed  Google Scholar 

  33. M.N. Kinde, Q. Chen, M.J. Lawless, D.D. Mowrey, J. Xu, S. Saxena, Y. Xu, P. Tang, Structure 23, 995 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  34. C. Pliotas, R. Ward, E. Branigan, A. Rasmussen, G. Hagelueken, H. Huang, S.S. Black, I.R. Booth, O. Schiemann, J.H. Naismith, Proc. Natl. Acad. Sci. USA 109, E2675 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  35. S. Kucher, C. Elsner, M. Safonova, S. Maffini, E. Bordignon, J. Phys. Chem. Lett. 12, 3679 (2021)

    CAS  PubMed  Google Scholar 

  36. P. Widder, J. Schuck, D. Summerer, M. Drescher, Phys. Chem. Chem. Phys. 22, 4875 (2020)

    CAS  PubMed  Google Scholar 

  37. Y. Yang, S.-N. Chen, F. Yang, X.-Y. Li, A. Feintuch, X.-C. Su, D. Goldfarb, Proc. Natl. Acad. Sci. USA 117, 20566 (2020)

    CAS  PubMed  PubMed Central  Google Scholar 

  38. G. Karthikeyan, A. Bonucci, G. Casano, G. Gerbaud, S. Abel, V. Thomé, L. Kodjabachian, A. Magalon, B. Guigliarelli, V. Belle, O. Ouari, E. Mileo, Angew. Chem. Int. Ed. 57, 1366 (2018)

    CAS  Google Scholar 

  39. R. Igarashi, T. Sakai, H. Hara, T. Tenno, T. Tanaka, H. Tochio, M. Shirakawa, J. Am. Chem. Soc. 132, 8228 (2010)

    CAS  PubMed  Google Scholar 

  40. K. Singewald, M.J. Lawless, S. Saxena, J. Magn. Reson. 299, 21 (2019)

    CAS  PubMed  Google Scholar 

  41. S. Jana, E.G.B. Evans, H.S. Jang, S. Zhang, H. Zhang, A. Rajca, S.E. Gordon, W.N. Zagotta, S. Stoll, R.A. Mehl, J. Am. Chem. Soc. 27, 14608–14620 (2023)

    Google Scholar 

  42. N. Fleck, C.A. Heubach, T. Hett, F.R. Haege, P.P. Bawol, H. Baltruschat, O. Schiemann, Angew. Chem. Int. Ed. 59, 9767 (2020)

    CAS  Google Scholar 

  43. O. Schiemann, C.A. Heubach, D. Abdullin, K. Ackermann, M. Azarkh, E.G. Bagryanskaya, M. Drescher, B. Endeward, J.H. Freed, L. Galazzo, D. Goldfarb, T. Hett, L. Esteban Hofer, L. Fábregas Ibáñez, E.J. Hustedt, S. Kucher, I. Kuprov, J.E. Lovett, A. Meyer, S. Ruthstein, S. Saxena, S. Stoll, C.R. Timmel, M. Di Valentin, H.S. Mchaourab, T.F. Prisner, B.E. Bode, E. Bordignon, M. Bennati, G. Jeschke, J. Am. Chem. Soc. 143, 17875 (2021)

    CAS  PubMed  Google Scholar 

  44. J.L. Sarver, J.E. Townsend, G. Rajapakse, L. Jen-Jacobson, S. Saxena, J. Phys. Chem. B 116, 4024 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  45. K. Sale, L. Song, Y.-S. Liu, E. Perozo, P. Fajer, J. Am. Chem. Soc. 127, 9334 (2005)

    CAS  PubMed  Google Scholar 

  46. A. Gamble Jarvi, X. Bogetti, K. Singewald, S. Ghosh, S. Saxena, Acc. Chem. Res. 54, 1481 (2021)

    CAS  PubMed  Google Scholar 

  47. A.J. Fielding, M.G. Concilio, G. Heaven, M.A. Hollas, Molecules 19, 16998 (2014)

    PubMed  PubMed Central  Google Scholar 

  48. W.L. Hubbell, C. Altenbach, Curr. Opin. Struct. Biol. 4, 566 (1994)

    CAS  Google Scholar 

  49. T.F. Cunningham, M.R. Putterman, A. Desai, W.S. Horne, S. Saxena, Angew. Chem. Int. Ed. Engl. 127, 6428 (2015)

    Google Scholar 

  50. T.F. Cunningham, M.R. Putterman, A. Desai, W.S. Horne, S. Saxena, Angew. Chem. Int. Ed. 54, 6330 (2015)

    CAS  Google Scholar 

  51. H. Ghimire, R.M. McCarrick, D.E. Budil, G.A. Lorigan, Biochemistry 48, 5782 (2009)

    CAS  PubMed  Google Scholar 

  52. J.L. Wort, K. Ackermann, A. Giannoulis, A.J. Stewart, D.G. Norman, B.E. Bode, Angew. Chem. Int. Ed. 58, 11681 (2019)

    CAS  Google Scholar 

  53. N. Fleck, C. Heubach, T. Hett, S. Spicher, S. Grimme, O. Schiemann, Chem. Eur. J 27, 5292 (2021)

    CAS  PubMed  Google Scholar 

  54. I. Tkach, G. Sicoli, C. Höbartner, M. Bennati, J. Magn. Reson. 209, 341 (2011)

    CAS  PubMed  Google Scholar 

  55. D. Akhmetzyanov, P. Schöps, A. Marko, N.C. Kunjir, S.T. Sigurdsson, T.F. Prisner, Phys. Chem. Chem. Phys. 17, 24446 (2015)

    CAS  PubMed  Google Scholar 

  56. A. Potapov, H. Yagi, T. Huber, S. Jergic, N.E. Dixon, G. Otting, D. Goldfarb, J. Am. Chem. Soc. 132, 9040 (2010)

    CAS  PubMed  Google Scholar 

  57. G.W. Reginsson, R.I. Hunter, P.A.S. Cruickshank, D.R. Bolton, S.T. Sigurdsson, G.M. Smith, O. Schiemann, J. Magn. Reson. 216, 175 (2012)

    CAS  PubMed  Google Scholar 

  58. C.L. Motion, J.E. Lovett, S. Bell, S.L. Cassidy, P.A.S. Cruickshank, D.R. Bolton, R.I. Hunter, H. El Mkami, S. Van Doorslaer, G.M. Smith, J. Phys. Chem. Lett. 7, 1411 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  59. M.H. Tessmer, S. Stoll, PLoS Comput. Biol. 19, e1010834 (2023)

    CAS  PubMed  PubMed Central  Google Scholar 

  60. X. Bogetti, S. Ghosh, A. Gamble Jarvi, J. Wang, S. Saxena, J. Phys. Chem. B 124, 2788 (2020)

    CAS  PubMed  Google Scholar 

  61. P.E. Spindler, Y. Zhang, B. Endeward, N. Gershernzon, T.E. Skinner, S.J. Glaser, T.F. Prisner, J. Magn. Reson. 218, 49 (2012)

    CAS  PubMed  Google Scholar 

  62. F.D. Breitgoff, K. Keller, M. Qi, D. Klose, M. Yulikov, A. Godt, G. Jeschke, J. Magn. Reson. 308, 106560 (2019)

    CAS  PubMed  Google Scholar 

  63. A. Doll, G. Jeschke, J. Magn. Reson. 246, 18 (2014)

    CAS  PubMed  Google Scholar 

  64. I. Kaminker, R. Barnes, S. Han, J. Magn. Reson. 279, 81 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  65. V. Denysenkov, P. van Os, T.F. Prisner, Appl Magn Reson 48, 1263 (2017)

    Google Scholar 

  66. J.W. Sidabras, T. Sarna, R.R. Mett, J.S. Hyde, J. Magn. Reson. 282, 129 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  67. M. Ji, S. Ruthstein, S. Saxena, Acc. Chem. Res. 47, 688 (2014)

    CAS  PubMed  Google Scholar 

  68. C.M. Grytz, A. Marko, P. Cekan, S.T. Sigurdsson, T.F. Prisner, Phys. Chem. Chem. Phys. 18, 2993 (2016)

    CAS  PubMed  Google Scholar 

  69. A. Godt, M. Schulte, H. Zimmermann, G. Jeschke, Angew. Chem. Int. Ed. 45, 7560 (2006)

    CAS  Google Scholar 

  70. T.F. Prisner, A. Marko, S.T. Sigurdsson, J. Magn. Reson. 252, 187 (2015)

    CAS  PubMed  Google Scholar 

  71. A.M. Bowen, A. Bertran, K.B. Henbest, M. Gobbo, C.R. Timmel, M. Di Valentin, J. Phys. Chem. Lett. 12, 3819 (2021)

    CAS  PubMed  PubMed Central  Google Scholar 

  72. I. Kaminker, I. Tkach, N. Manukovsky, T. Huber, H. Yagi, G. Otting, M. Bennati, D. Goldfarb, J. Magn. Reson. 227, 66 (2013)

    CAS  PubMed  Google Scholar 

  73. A. Gamble Jarvi, K. Ranguelova, S. Ghosh, R.T. Weber, S. Saxena, J. Phys. Chem. B 122, 10669 (2018)

    CAS  PubMed  Google Scholar 

  74. V.P. Denysenkov, T.F. Prisner, J. Stubbe, M. Bennati, Proc. Natl. Acad. Sci. USA 103, 13386 (2006)

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Z. Yang, D. Kise, S. Saxena, J. Phys. Chem. B 114, 6165 (2010)

    CAS  PubMed  Google Scholar 

  76. D. Abdullin, G. Hagelueken, R.I. Hunter, G.M. Smith, O. Schiemann, Mol. Phys. 113, 544 (2015)

    CAS  Google Scholar 

  77. A. Marko, T.F. Prisner, Phys. Chem. Chem. Phys. 15, 619 (2013)

    CAS  PubMed  Google Scholar 

  78. A. Potapov, J. Magn. Reson. 316, 106769 (2020)

    CAS  PubMed  Google Scholar 

  79. A.G. Maryasov, Y.D. Tsvetkov, J. Raap, Appl. Magn. Reson. 14, 101 (1998)

    CAS  Google Scholar 

  80. Z. Hasanbasri, N.A. Moriglioni, S. Saxena, Phys. Chem. Chem. Phys. 25(19), 13275–13288 (2023)

    CAS  PubMed  Google Scholar 

  81. X. Bogetti, Z. Hasanbasri, H.R. Hunter, S. Saxena, Phys. Chem. Chem. Phys. 24, 14727 (2022)

    CAS  PubMed  Google Scholar 

  82. P. Roser, M.J. Schmidt, M. Drescher, D. Summerer, Org. Biomol. Chem. 14, 5468 (2016)

    CAS  PubMed  Google Scholar 

  83. D. Goldfarb, Phys. Chem. Chem. Phys. 16, 9685 (2014)

    CAS  PubMed  Google Scholar 

  84. S. Jun, J.S. Becker, M. Yonkunas, R. Coalson, S. Saxena, Biochemistry 45, 11666 (2006)

    CAS  PubMed  Google Scholar 

  85. Z. Yang, J. Becker, S. Saxena, J. Magn. Reson. 188, 337 (2007)

    CAS  PubMed  Google Scholar 

  86. T.F. Cunningham, M.D. Shannon, M.R. Putterman, R.J. Arachchige, I. Sengupta, M. Gao, C.P. Jaroniec, S. Saxena, J. Phys. Chem. B 119, 2839 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  87. S. Ghosh, M.J. Lawless, H.J. Brubaker, K. Singewald, M.R. Kurpiewski, L. Jen-Jacobson, S. Saxena, Nucleic Acids Res. 48, e49 (2020)

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Y. Polyhach, A. Godt, C. Bauer, G. Jeschke, J. Magn. Reson. 185, 118 (2007)

    CAS  PubMed  Google Scholar 

  89. A. Gamble Jarvi, A. Sargun, X. Bogetti, J. Wang, C. Achim, S. Saxena, J. Phys. Chem. B 124, 7544 (2020)

    CAS  PubMed  Google Scholar 

  90. S. Ghosh, M.J. Lawless, G.S. Rule, S. Saxena, J. Magn. Reson. 286, 163 (2018)

    CAS  PubMed  Google Scholar 

  91. M.J. Lawless, S. Ghosh, T.F. Cunningham, A. Shimshi, S. Saxena, Phys. Chem. Chem. Phys. 19, 20959 (2017)

    CAS  PubMed  Google Scholar 

  92. K. Singewald, J.A. Wilkinson, A.S. Saxena, Bio Protoc 11, e4258 (2021)

    CAS  PubMed  PubMed Central  Google Scholar 

  93. W. R. Hagen, Biomolecular EPR Spectroscopy (CRC Press, 2008)

  94. K. Singewald, X. Bogetti, K. Sinha, G.S. Rule, S. Saxena, Angew. Chem. Int. Ed. 59, 23040 (2020)

    CAS  Google Scholar 

  95. A. Gamble Jarvi, J. Casto, S. Saxena, J. Magn. Reson. 320, 106848 (2020)

    CAS  PubMed  Google Scholar 

  96. S. Stoller, G. Sicoli, T.Y. Baranova, M. Bennati, U. Diederichsen, Angew. Chem. Int. Ed. 50, 9743 (2011)

    CAS  Google Scholar 

  97. K. Halbmair, J. Wegner, U. Diederichsen, M. Bennati, Biophys. J. 111, 2345 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  98. M.R. Fleissner, M.D. Bridges, E.K. Brooks, D. Cascio, T. Kálai, K. Hideg, W.L. Hubbell, Proc. Natl. Acad. Sci. USA 108, 16241 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  99. M.A. Stevens, J.E. McKay, J.L.S. Robinson, H. El Mkami, G.M. Smith, D.G. Norman, Phys. Chem. Chem. Phys. 18, 5799 (2016)

    CAS  PubMed  Google Scholar 

  100. H. Sameach, S. Ghosh, L. Gevorkyan-Airapetov, S. Saxena, S. Ruthstein, Angew. Chem. Int. Ed. 58, 3053 (2019)

    CAS  Google Scholar 

  101. B.G. Dzikovski, P.P. Borbat, J.H. Freed, J. Phys. Chem. B 115, 176 (2011)

    CAS  PubMed  Google Scholar 

  102. B. Endeward, J.A. Butterwick, R. MacKinnon, T.F. Prisner, J. Am. Chem. Soc. 131, 15246 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  103. M.V. Fedin, G.Y. Shevelev, D.V. Pyshnyi, V.M. Tormyshev, G. Jeschke, M. Yulikov, E.G. Bagryanskaya, Phys. Chem. Chem. Phys. 18, 29549 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  104. D. Abdullin, G. Hagelueken, O. Schiemann, Phys. Chem. Chem. Phys. 18, 10428 (2016)

    CAS  PubMed  Google Scholar 

  105. P. Cekan, E.O. Jonsson, S.T. Sigurdsson, Nucleic Acids Res. 37, 3990 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  106. M. Heinz, N. Erlenbach, L.S. Stelzl, G. Thierolf, N.R. Kamble, S.T. Sigurdsson, T.F. Prisner, G. Hummer, Nucleic Acids Res. 48, 924 (2020)

    CAS  PubMed  Google Scholar 

  107. L.S. Stelzl, N. Erlenbach, M. Heinz, T.F. Prisner, G. Hummer, J. Am. Chem. Soc. 139, 11674 (2017)

    CAS  PubMed  Google Scholar 

  108. D.M. Engelhard, A. Meyer, A. Berndhäuser, O. Schiemann, G.H. Clever, Chem. Commun. 54, 7455 (2018)

    CAS  Google Scholar 

  109. L.M. Stratmann, Y. Kutin, M. Kasanmascheff, G.H. Clever, Angew. Chem. Int. Ed. 60, 4939 (2021)

    CAS  Google Scholar 

  110. M.P. Donohue, V.A. Szalai, Phys. Chem. Chem. Phys. 18, 15447 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  111. C.M. Grytz, S. Kazemi, A. Marko, P. Cekan, P. Güntert, S.T. Sigurdsson, T.F. Prisner, Phys. Chem. Chem. Phys. 19, 29801 (2017)

    CAS  PubMed  Google Scholar 

  112. G.W. Reginsson, S.A. Shelke, C. Rouillon, M.F. White, S.T. Sigurdsson, O. Schiemann, Nucleic Acids Res. 41, e11 (2013)

    CAS  PubMed  Google Scholar 

  113. S. Stoll, A. Schweiger, J. Magn. Reson. 178, 42 (2006)

    CAS  PubMed  Google Scholar 

  114. D. Abdullin, Appl Magn Reson 51, 725 (2020)

    CAS  Google Scholar 

  115. A.M. Bowen, M.W. Jones, J.E. Lovett, T.G. Gaule, M.J. McPherson, J.R. Dilworth, C.R. Timmel, J.R. Harmer, Phys. Chem. Chem. Phys. 18, 5981 (2016)

    CAS  PubMed  Google Scholar 

  116. J.E. Lovett, A.M. Bowen, C.R. Timmel, M.W. Jones, J.R. Dilworth, D. Caprotti, S.G. Bell, L.L. Wong, J. Harmer, Phys. Chem. Chem. Phys. 11, 6840 (2009)

    CAS  PubMed  Google Scholar 

  117. D. Margraf, B.E. Bode, A. Marko, O. Schiemann, T.F. Prisner, Mol. Phys. 105, 2153 (2007)

    CAS  Google Scholar 

  118. C. Abé, D. Klose, F. Dietrich, W.H. Ziegler, Y. Polyhach, G. Jeschke, H.-J. Steinhoff, J. Magn. Reson. 216, 53 (2012)

    PubMed  Google Scholar 

  119. A. Savitsky, A.A. Dubinskii, M. Flores, W. Lubitz, K. Möbius, J. Phys. Chem. B 111, 6245 (2007)

    CAS  PubMed  Google Scholar 

  120. A.M. Bowen, E.O.D. Johnson, F. Mercuri, N.J. Hoskins, R. Qiao, J.S.O. McCullagh, J.E. Lovett, S.G. Bell, W. Zhou, C.R. Timmel, L.L. Wong, J.R. Harmer, J. Am. Chem. Soc. 140, 2514 (2018)

    CAS  PubMed  Google Scholar 

  121. A. Marko, D. Margraf, H. Yu, Y. Mu, G. Stock, T. Prisner, J. Chem. Phys. 130, 064102 (2009)

    CAS  PubMed  Google Scholar 

  122. G. Jeschke, V. Chechik, P. Ionita, A. Godt, H. Zimmermann, J. Banham, C.R. Timmel, D. Hilger, H. Jung, Appl Magn Reson 30, 473 (2006)

    CAS  Google Scholar 

  123. A. Giannoulis, C.L. Motion, M. Oranges, M. Bühl, G.M. Smith, B.E. Bode, Phys. Chem. Chem. Phys. 20, 2151 (2018)

    CAS  PubMed  Google Scholar 

  124. A. Meyer, D. Abdullin, G. Schnakenburg, O. Schiemann, Phys. Chem. Chem. Phys. 18, 9262 (2016)

    CAS  PubMed  Google Scholar 

  125. D. Abdullin, P. Brehm, N. Fleck, S. Spicher, S. Grimme, O. Schiemann, Chem. Eur. J 25, 14388 (2019)

    CAS  PubMed  Google Scholar 

  126. H.L. Flanagan, G.J. Gerfen, A. Lai, D.J. Singel, J. Chem. Phys. 88, 2162 (1988)

    CAS  Google Scholar 

  127. G.H. Rist, J.S. Hyde, J. Chem. Phys. 52, 4633 (1970)

    CAS  Google Scholar 

  128. A. Kehl, M. Hiller, F. Hecker, I. Tkach, S. Dechert, M. Bennati, A. Meyer, J. Magn. Reson. 333, 107091 (2021)

    CAS  PubMed  Google Scholar 

  129. G.E. Cutsail, J. Telser, B.M. Hoffman, Biochim. Biophys. Acta 1853, 1370 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  130. R. Kappl, G. Bracic, J. Hüttermann, in High Resolution EPR. ed. by L. Berliner, G. Hanson (Springer, New York, New York, NY, 2009), pp.63–103

    Google Scholar 

  131. T. Iwasaki, A. Kounosu, T. Uzawa, R.I. Samoilova, S.A. Dikanov, J. Am. Chem. Soc. 126, 13902 (2004)

    CAS  PubMed  Google Scholar 

  132. N. Wili, S. Richert, B. Limburg, S.J. Clarke, H.L. Anderson, C.R. Timmel, G. Jeschke, Phys. Chem. Chem. Phys. 21, 11676 (2019)

    CAS  PubMed  Google Scholar 

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Funding

This review was financially supported by National Science Foundation [NSF BSF MCB-2006154].

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  1. Department of Chemistry, University of Pittsburgh, Pittsburgh, PA, 15260, USA

    Zikri Hasanbasri & Sunil Saxena

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  1. Zikri Hasanbasri
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ZH: writing—original draft, writing—review and editing, visualization. SS: writing—review and editing, supervision.

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Correspondence to Sunil Saxena.

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Hasanbasri, Z., Saxena, S. Orientational Selectivity in Pulsed-EPR Does Not Have to be Complicated. Appl Magn Reson 55, 61–78 (2024). https://doi.org/10.1007/s00723-023-01594-z

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