Photoirradiation and Microwave Irradiation NMR Spectroscopy

  • Akira Naito
  • Yoshiteru Makino
  • Yugo Tasei
  • Izuru Kawamura
Chapter

Abstract

In situ photoirradiation solid-state nuclear magnetic resonance (NMR) spectroscopy is designed for optical irradiation from the top part of a zirconia rotor through a glass cap, which makes it possible to efficiently irradiate the inside of the rotor. This experimental method has made it possible to observe photo-intermediates of sensory rhodopsins, such as sensory rhodopsin I (SRI) and sensory rhodopsin II (SRII), and bacteriorhodopsin (bR) Y185F mutant. In SRI, green light generates M-intermediates, which exhibit positive phototaxis, while blue light generates P-intermediates, which exhibit negative phototaxis. In SRII, green light generates M-intermediates and blue light generates O-intermediates. In Y185F-bR, O-intermediates were first observed using solid-state NMR spectroscopy. The microwave irradiation NMR spectrometer was developed in-house by modification of a commercial NMR spectrometer. A flat long copper ribbon was used as a capacitor and a half turn of copper ribbon at the edge was used as an inductor for the microwave resonance circuit, which was coaxially inserted inside the radiofrequency induction coil and allowed NMR signals to be observed under microwave irradiation conditions. The temperature of N-(4-methoxybenzylidene)-4-butylaniline (MBBA) during microwave irradiation was estimated by measuring the temperature-dependent chemical shifts, whereby different protons were found to indicate significantly different temperatures in the molecule. Liquid crystalline-isotropic phase correlation 2D NMR spectra were observed using pulsed microwave irradiation for rapid temperature jump experiments.

Keywords

Photoirradiation Microwave irradiation Photoreceptor membrane protein Liquid crystal 

Notes

Acknowledgements

This work was supported by grants-in-aid for Scientific Research in an Innovative Area (16H00756 to AN and 16H00828 to IK), and by a grant-in-aid for Scientific Research (C) (15K06963 to AN) and Research (B) (15H04336 to IK) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

References

  1. 1.
    Smith, S.O., de Groot, H.J.M., Gebhard, R., Courtin, J., Lugtenburg, J., Herzfeld, J., Griffin, R.G.: Structure and protein environment of the retinal chromophore in ligand- and dark-adapted bacteriorhodopsin studied by solid-state NMR. Biochemistry 28, 8897–8904 (1989)CrossRefGoogle Scholar
  2. 2.
    McDermott, A.E., Thompson, L.K., Winkel, C., Farrar, M.R., Pelletier, S., Lugtenburg, J., Herzfeld, J., Griffin, R.G.: Mechanism of proton pumping in bacteriorhodopsin by solid-state NMR: the protonation state of tyrosine in the light-adapted and M state. Biochemistry 30, 8366–8371 (1991)CrossRefGoogle Scholar
  3. 3.
    Farrar, M.R., Lakshmi, K.V., Smith, S.O., Brown, R.S., Raap, J., Lugtenburg, J., Griffin, R.G., Herzfeld, J.: Solid state NMR study of [ε-13C]Lys-bacteriorhodopsin: schiff base photoisomerization. Biophys. J. 65, 310–315 (1993)Google Scholar
  4. 4.
    Lakshmi, K.V., Farrar, M.R., Raap, J., Lugtenburg, J., Griffin, R.G., Herzfeld, J.: Solid state 13C and 15N NMR investigations of the N intermediate of bacteriorhodopsin. Biochemistry 33, 8853–8857 (1994)CrossRefGoogle Scholar
  5. 5.
    Feng, X., Verdegem, P.J.E., Eden, M., Sandstrom, D., Lee, Y.K., Bovee-Geurts, P.H.M., de Grip, W.J., Lugtenburg, J., de Groot, H.J.M., Levitt, M.H.: Determination of a molecular torsional angle in the metarhodopsin-I photointermediate of rhodopsin by double-quantum solid-state NMR. J. Biomol. NMR 16, 1–8 (2000)CrossRefGoogle Scholar
  6. 6.
    Crocker, E., Eilers, M., Ahuja, S., Hornak, V., Hirshfeld, A., Sheves, M., Smith, S.O.: Location of Trp265 in metarhodopsin II: implications for the activation mechanism of the visual receptor rhodopsin. J. Mol. Biol. 357, 163–172 (2006)CrossRefGoogle Scholar
  7. 7.
    Ahuja, S., Crocker, E., Eilers, M., Hornak, V., Hirshfeld, A., Ziliox, M., Syrett, N., Reeves, P.J., Khorana, H.G., Sheves, M., Smith, S.O.: Location of the retinal chromophore in the Activated state of rhodopsin. J. Biol. Chem. 284, 10190–10201 (2009)CrossRefGoogle Scholar
  8. 8.
    Hu, J.G., Sun, B.Q., Bizounok, M., Hatcher, M.E., Lansing, J.C., Raap, J., Verdegen, P.J.E., Lugtenburg, J., Griffin, R.G., Herzfeld, J.: Early and late M intermediates in the bacteriorhodopsin photocycle: a solid-state NMR study. Biochemistry 37, 8088–8096 (1998)CrossRefGoogle Scholar
  9. 9.
    Petkova, A.T., Hatanaka, M., Jaroniec, C.P., Hu, J.G., Belenky, M., Verhoeven, M., Lugtenburg, J., Griffin, R.G., Herzfeld, J.: Tryptophan interaction in bacteriorhodopsin: a heteronuclear solid-state NMR study. Biochemistry 41, 2429–2437 (2002)CrossRefGoogle Scholar
  10. 10.
    Hu, J.G., Sun, B.Q., Petkova, A.T., Griffin, R.G., Herzfeld, J.: The predischarge chromophore in bacteriorhodopsin: a 15N solid-state NMR study of the L photointermediate. Biochemistry 36, 9316–9322 (1997)CrossRefGoogle Scholar
  11. 11.
    Mak-Jurkauskas, M.L., Bajaj, V.S., Hornstein, M.K., Blenky, M., Griffin, R.G., Herzfeld, J.: Energy transformations early in the bacteriorhodopsin photocycle revealed by DNP-enhanced solid-state NMR. Proc. Natl. Acad. Sci. U S A 105, 883–888 (2008)CrossRefGoogle Scholar
  12. 12.
    Bajaj, V.S., Mak-Jurkauskas, M.L., Belenky, M., Herzfeld, J., Griffin, R.G.: Functional and shunt state of bacteriorhodopsin resolved by 250 GHz dynamic nuclear polarization-enhanced solid-state NMR. Proc. Natl. Acad. Sci. U S A 106, 9244–9249 (2009)CrossRefGoogle Scholar
  13. 13.
    Becker-Baldus, J., Bamann, C., Saxena, K., Gustmann, H., Brown, L.J., Brown, R.C.D., Reiter, C., Bamberg, E., Wachtveitl, J., Schwalbe, H., Glaubitz, C.: Enlightening the photoactive site of channelrhodopsin-2 by DNP-enhanced solid-state NMR spectroscopy. Proc. Natl. Acad. Sci. U S A 112, 9896–9901 (2015)CrossRefGoogle Scholar
  14. 14.
    Kawamura, I., Kihara, N., Ohmine, M., Nishimura, K., Tuzi, S., Saitô, H., Naito, A.: Solid-state NMR studies of two backbone conformations at Tyr185 as a function of retinal configurations in the dark, light, and pressure adapted bacteriorhodopsin. J. Am. Chem. Soc. 129, 1016–1017 (2007)CrossRefGoogle Scholar
  15. 15.
    Tomonaga, Y., Hidaka, T., Kawamura, I., Nishio, T., Ohsawa, K., Okitsu, T., Wada, A., Sudo, Y., Kamo, N., Ramamoorthy, A., Naito, A.: An active photoreceptor intermediate revealed by in situ photoirradiated solid-state NMR spectroscopy. Biophys. J. 101, L50–L52 (2011)CrossRefGoogle Scholar
  16. 16.
    Yomoda, H., Makino, Y., Tomonaga, Y., Hidaka, T., Kawamura, I., Okitsu, T., Wada, A., Sudo, Y., Naito, A.: Color-discriminating retinal configurations of sensory rhodopsin I by photo-irradiation solid-state NMR spectroscopy. Angew. Chem. Int. Ed. 53, 6960–6964 (2014)CrossRefGoogle Scholar
  17. 17.
    Naito, A., Kawamura, I.: Photoactivated structural changes in photoreceptor membrane proteins as revealed by in situ photoirradiation solid-state NMR spectroscopy. In: Separovic, F., Naito, A. (eds.) Advances in Biological Solid-State NMR: Proteins and Membrane Active Peptides, pp. 387–404. Royal Society of Chemistry, London (2014)CrossRefGoogle Scholar
  18. 18.
    Naito, A., Kawamura, I., Javkhlantugs, N.: Recent solid-state NMR studies of membrane-bound peptides and proteins. Annu. Rep. NMR Spectrosc. 86, 333–411 (2015)CrossRefGoogle Scholar
  19. 19.
    Oshima, K., Shigeta, A., Makino, Y., Kawamura, I., Okitsu, T., Wada, A., Tuzi, S., Iwasa, T., Naito, A.: Characterization of photo-intermediates in the photo-reaction pathways of a bacteriorhodopsin Y185F mutant using in situ photo-irradiation solid-state NMR spectroscopy. Photochem. Photobiol. Sci. 14, 1694–1702 (2015)CrossRefGoogle Scholar
  20. 20.
    Gedye, R., Smith, F., Westaway, K., All, H., Baldisers, L., Laberge, L., Rousell, J.: The use of microwave ovens for rapid organic synthesis. Tetrahedron Lett. 27, 279–282 (1986)CrossRefGoogle Scholar
  21. 21.
    Giguere, R.J., Bray, T.L., Duncan, S.M., Majetich, G.: Application of commercial microwave ovens to organic synthesis. Tetrahedron Lett. 27, 4945–4948 (1986)CrossRefGoogle Scholar
  22. 22.
    Adam, D.: Out of the kitchen. Nature 421, 571–572 (2003)CrossRefGoogle Scholar
  23. 23.
    Perreux, L., Loupy, A.: Atentative rationalization of microwave effects in organic synthesis according to the reaction medium, and mechanistic considerations. Tetrahedron 57, 9199–9223 (2001)CrossRefGoogle Scholar
  24. 24.
    Lidström, P., Tiemey, J., Wathey, B., Westman, J.: Microwave assisted organic synthesis. Tetrahedron 57, 9235–9283 (2001)Google Scholar
  25. 25.
    Bogdal, D., Lukasiewicz, M., Pielichowski, J., Miciak, A., Begdarz, Sz.: Microwave-assisted oxidation of alcohols using magtrieve. Tetrahedron 59, 649–653 (2003)Google Scholar
  26. 26.
    Kappe, G.O.: Controlled microwave heating in modern organic synthesis. Angew. Chem. Int. Ed. 43, 6250–6284 (2004)CrossRefGoogle Scholar
  27. 27.
    Yoshimura, Y., Shimizu, H., Hinou, H., Nishimura, S.-I.: A novel glycosylation concept: microwave-assisted acetal-exchange type glycosylation from methyl glycosides as donors. Tetrahedron Lett. 46, 4701–4705 (2005)CrossRefGoogle Scholar
  28. 28.
    Shimizu, H., Yoshimura, Y., Hinou, H., Nishimura, S.-I.: A new glycosylation method part 3: study of microwave effects at low temperatures to control reaction pathways and reduce byproducts. Tetrahedron 64, 10091–10096 (2008)Google Scholar
  29. 29.
    Kappe, C.O., Pieber, B., Dallinger, D.: Microwave effect in organic synthesis: myth or reality. Angew. Chem. Int. Ed. 52, 1088–1094 (2013)CrossRefGoogle Scholar
  30. 30.
    Hoogenboom, R., Wiesbrock, F., Huang, H., Leenen, M.A.M., Thijis, H.M.L., van Nispen, S.F.G.M., van der Loop, M., Fustin, C.-A., Jonas, A.M., Gohy, J.-F., Schubert, U.S.: Microwave-assisted cationic ring-opening polymerization of 2-oxazolines: a powerful method for the synthesis of amphiphilic triblock copolymers. Maclomolecules 39, 4719–4725 (2006)CrossRefGoogle Scholar
  31. 31.
    Iwamura, T., Ashizawa, K., Sakaguchi, M.: Efficient and echo-friendly anionic polymerization of acrylamide under microwave irradiation and hydrolysis of the obtained polymers by microwave irradiation. Macromolecules 42, 5001–5006 (2009)CrossRefGoogle Scholar
  32. 32.
    Kajiwara, Y., Nagai, A., Chujo, Y.: Microwave-assisted synthesis of poly(2-hydroxyethyl methacrylate)(HEMA)/Silica hybrid using in situ polymerization method. Polymer J. 41, 1080–1084 (2009)CrossRefGoogle Scholar
  33. 33.
    Yamada, S., Takasu, A., Takayama, S., Kawamura, K.: Microwave-assisted solution polycondensation of L-lactic acid using a Dean-Stark apparatus for a non-thermal microwave polymerization effect induced by the electric field. Polym. Chem. 5, 5283–5288 (2014)Google Scholar
  34. 34.
    Pramanik, B.N., Mirza, U.A., Ing, Y.H., Liu, Y.-H., Bartner, P.L., Weber, P.C., Bose, A.K.: Microwave-enhanced enzyme reaction for protein mapping by mass spectrometry: a new approach to protein digestion in minutes. Protein Sci. 11, 2676–2687 (2002)CrossRefGoogle Scholar
  35. 35.
    Huang, W., Xia, Y.-M., Gao, H., Fang, T.-J., Wang, Y., Fang, Y.J.: Enzymatic esterification between n-alcohol homologs and n-caprylic acid in non-aqueous medium under microwave irradiation. Mol. Catal. 35, 115–116 (2005)Google Scholar
  36. 36.
    Herrero, M.A., Kremsner, J.M., Kappe, C.O.: Nonthermal microwave effects revised: on the importance of internal temperature monitoring and agitation in microwave chemistry. J. Org. Chem. 73, 36–49 (2008)CrossRefGoogle Scholar
  37. 37.
    Obermayer, D., Gutmann, B., Kappe, C.O.: Microwave chemistry in silicon carbide reaction vials: separating thermal from nonthermal effects. Angew. Chem. Int. Ed. 48, 8321–8324 (2009)CrossRefGoogle Scholar
  38. 38.
    Tanaka, M., Sato, M.: Microwave heating of water, ice, and saline solution: molecular dynamic study. J. Chem. Phys. 126, 034509 (2007)CrossRefGoogle Scholar
  39. 39.
    Kanno, M., Nakamura, K., Kanai, K., Hoki, K., Kono, H., Tanaka, M.: Theoretical verification of nonthermal microwave effects on intramolecular reactions. J. Phys. Chem. A 116, 2177–2183 (2012)CrossRefGoogle Scholar
  40. 40.
    Tsukahara, Y., Higashi, A., Yamauchi, T., Nakamura, T., Yasuda, M., Baba, A., Wada, Y.: In situ observation of nonequilibrium local heating as an origin of spherical effect of microwave on chemistry. J. Phys. Chem. C 114, 8965–8970 (2010)CrossRefGoogle Scholar
  41. 41.
    Tasei, Y., Yamakami, T., Kawamura, I., Fujito, T., Ushida, K., Sato, M., Naito, A.: Mechanism for microwave heating of 1-(4′-cyanophenyl)-4-propylcyclohexane characterized by in situ microwave irradiation NMR spectroscopy. J. Magn. Reson. 254, 27–34 (2015)CrossRefGoogle Scholar
  42. 42.
    Tasei, Y., Tanigawa, F., Kawamura, I., Fujito, T., Sato, M., Naito, A.: The microwave heating mechanism of N-(4-methoxybenzyliden)-4-butylaniline in liquid crystalline and isotropic phases as determined using in situ microwave irradiation NMR spectroscopy. Phys. Chem. Chem. Phys. 17, 9082–9089 (2015)CrossRefGoogle Scholar
  43. 43.
    Naito, A., Imanari, M., Akasaka, K.: Separation of local magnetic fields of individual protons in nematic phase by state-correlated 2D NMR spectroscopy. J. Magn. Reson. 92, 85–93 (1991)Google Scholar
  44. 44.
    Naito, A., Imanari, M., Akasaka, K.: State-correlated two-dimensional NMR spectroscopy: separation of local dipolar fields of protons in nematic phase of 4′-methoxybenzylidene-4-acetoxyaniline. J. Chem. Phys. 105, 4502–4510 (1996)CrossRefGoogle Scholar
  45. 45.
    Akasaka, K., Kimura, M., Naito, A., Kawahara, H., Imanari, M.: Local order, conformation, and interaction in nematic 4-(n-pentyloxy-4′-cyanobiphenyl and its one-to-one mixture with 1-(4′-cyanophenyl)-4-propylcyclohexane. A study by state-correlated 1H two-dimensional NMR spectroscopy. J. Phys. Chem. 99, 9523–9529 (1995)CrossRefGoogle Scholar
  46. 46.
    Naito, A., Ramamoorthy, A.: Structural studies of liquid crystalline materials using a solid state NMR technique. Thermotropic Liquid Crystal: Recent Advances, pp. 85–116, Springer, Berlin (2007)Google Scholar
  47. 47.
    Naito, A., Tasei, Y.: Separation of local fields of individual protons in nematic phase of 4′-ethoxybenzylidene-4-n-butylaniline by microwave heating 2D NMR spectroscopy. Mater. Sci. Technol. (MS&T) 2010, 2886–2894 (2010)Google Scholar
  48. 48.
    Akasaka, K., Naito, A., Imanari, M.: Novel method for NMR spectral correlation between the native and the denatured states of a protein. Application to ribonuclease A. J. Am. Chem. Soc. 113, 4688–4689 (1991)CrossRefGoogle Scholar
  49. 49.
    Spudich, J.L., Bogomolni, R.A.: Mechanism of colour discrimination by a bacterial sensory rhodopsin. Nature 312, 509–513 (1984)CrossRefGoogle Scholar
  50. 50.
    Suzuki, D., Irieda, H., Honma, M., Kawagishi, I., Sudo, Y.: Phototactic and chemotactic signal transduction by transmembrane receptors and transducers in microorganisms. Sensors 10, 4010–4039 (2010)CrossRefGoogle Scholar
  51. 51.
    Chen, X., Spudich, J.L.: Demonstration of 2:2 stoichiometry in the functional SRI-HtrI signaling complex in Halobacterium membrane by gene fusion analysis. Biochemistry 41, 3891–3896 (2002)CrossRefGoogle Scholar
  52. 52.
    Szundi, I., Swartz, T.E., Bogomoni, R.A.: Multicolored protein conformation state in the photocycle of transducer-free sensory rhodopsin-I. Biophys. J. 80, 469–479 (2001)CrossRefGoogle Scholar
  53. 53.
    Kitajima-Ihara, T., Furutani, Y., Suzuki, D., Ihara, K., Kandori, H., Honma, M., Sudo, Y.: Salinibacter sensory rhodopsin: sensory rhodopsin I-like protein from a eubacterium. J. Biol. Chem. 283, 23533–23541 (2008)CrossRefGoogle Scholar
  54. 54.
    Suzuki, D., Sudo, Y., Furutani, Y., Takahashi, H., Honnma, M., Kandori, H.: Structural changes of salinibacter sensory rhodopsin I upon formation of the K and M photointermediates. Biochemistry 47, 12750–12759 (2008)Google Scholar
  55. 55.
    Harbison, G.S., Smith, S.O., Pardoen, J.A., Mudder, P.P.J., Lugtenburg, J., Herzfeld, J., Mishien, G.S., Griffin, R.G.: Solid-state 13C NMR studies of retinal in bacteriorhodopsin. Biochemistry 23, 2662–2687 (1984)Google Scholar
  56. 56.
    Sineshchekov, O.A., Sasaki, J., Philip, S.B.J., Spudich, J.L.: A Schiff base connectivity switch in sensory rhodopsin signaling. Proc. Natl. Acad. Sci. U S A 105, 16159–16164 (2008)CrossRefGoogle Scholar
  57. 57.
    Spudich, J.L., Luecke, H.: Sensory rhodopsin II: functional insight from structure. Curr. Opin. Struct. Biol. 12, 540–546 (2002)CrossRefGoogle Scholar
  58. 58.
    Kamo, N., Shimono, K., Iwamoto, M., Sudo, Y.: Photochemistry and photoinduced proton-transfer by pharaonis phoborhodopsin. Biochemistry (Mosc.) 66, 1277–1282 (2001)CrossRefGoogle Scholar
  59. 59.
    Gordelly, V.L., Labahn, J., Moukhametzianov, R., Efremov, R., Granzin, J., Schleslnger, R., Buldt, G., Sevopol, T., Scheldlg, A.J., Klarr, J.P., Engelhart, M.: Molecular basis of transmembrane signalling by sensory rhodopsin II-transducer complex. Nature 419, 484–487 (2002)CrossRefGoogle Scholar
  60. 60.
    Shimono, K., Hayashi, T., Ikehara, Y., Sudo, Y., Iwamoto, M., Kamo, N.: Importance of the broad regional interaction for spectral tuning in Natronobacterium pharaonic phoborhodopsin (sensory rhodopsin II). J. Biol. Chem. 278, 23882–23889 (2003)CrossRefGoogle Scholar
  61. 61.
    Sudo, Y., Furutani, Y., Kandori, H., Spudich, J.L.: Functional importance of the interhelical hydrogen bond between Thr204 and Tyr174 of sensory rhodopsin II and its alteration during the signalling process. J. Biol. Chem. 281, 34239–34245 (2006)CrossRefGoogle Scholar
  62. 62.
    Sudo, Y., Furutani, Y., Wada, A., Ito, M., Kamo, N., Kandori, H.: Steric constraint in the primary photoproduct of an archaeal rhodopsin from regiospecific perturbation of C-D stretching vibration of the retinyl chromophore. J. Am. Chem. Soc. 127, 16036–16037 (2005)CrossRefGoogle Scholar
  63. 63.
    Furutani, Y., Kamada, K., Sudo, Y., Shimono, K., Kamo, N., Kandori, H.: Structural changes of the complex between pharaonic phoborhodopsin and its cognate transducer upon formation of the M photointermediate. Biochemistry 44, 2909–2915 (2005)CrossRefGoogle Scholar
  64. 64.
    Wagner, A.-A., Chzhov, I., Engelhard, M., Steinhoff, H.-J.: Time-resolved detection of transient movement of helix F in spin-labelled pharaonic sensory rhodopsin II. J. Mol. Biol. 301, 881–891 (2000)CrossRefGoogle Scholar
  65. 65.
    Spudih, J.I.: Variations on a molecular switch: transport and sensory signalling by archaeal rhodopsin. Mol. Mictrobiol. 28, 1051–1058 (1998)CrossRefGoogle Scholar
  66. 66.
    Yoshida, H., Sudo, Y., Shimono, K., Iwamoto, M., Kamo, N.: Transient movement of helix F revealed by photo-induced inactivation by reaction of a bulky SH-regent to cysteine-introduced pharaonis phoborhodopsin (sensory rhodopsin II). Photochem. Photobiol. Sci. 3, 537–542 (2004)CrossRefGoogle Scholar
  67. 67.
    Moukhametzianov, R., Klare, J.P., Efremov, R., Baeken, C., Göppner, A., Labahn, J., Engelhard, M., Büldt, G., Gordeliy, V.I.: Development of the signal in sensory rhodopsin and its transducer to the cognate transducer. Nature 440, 115–119 (2006)CrossRefGoogle Scholar
  68. 68.
    Etzkom, M., Seidel, K., Li, L., Martell, S., Geyer, M., Engelhard, M., Baldus, M.: Complex formation and light activation in membrane-embedded sensory rhodopsin II as seen by solid-state NMR spectroscopy. Structure 18, 293–300 (2010)CrossRefGoogle Scholar
  69. 69.
    Kawamura, I., Yoshida, H., Ikeda, Y., Yamaguchi, S., Tuzi, S., Saitô, H., Kamo, N., Naito, A.: Dynamic change of phoborhodopsin and transducer by activation: study using D75N mutant of the receptor by site-directed solid-state 13C NMR. Photochem. Photobiol. 84, 921–930 (2008)Google Scholar
  70. 70.
    Roy, S., Kikukawa, T., Sharma, P., Ksmo, N.: All-optical switching in pharaonic phoborhodopsin protein molecules. IEEE Trans. Nanobiosci. 5, 178–187 (2006)CrossRefGoogle Scholar
  71. 71.
    Tateishi, Y., Abe, T., Tamogami, J., Nakano, Y., Kikukawa, T., Kamo, N., Unno, M.: Spectroscopic evidence for the formation of an N intermediate during the photocycle of sensory rhodopsin II (phoborhodopsin) from Natronobacterium pharaonic. Biochemistry 50, 2135–2143 (2011)CrossRefGoogle Scholar
  72. 72.
    Lanyi, J.K.: Proton transfers in the bacteriorhodopsin photocycle. Biochim. Biophys. Acta 1757, 1012–1018 (2006)CrossRefGoogle Scholar
  73. 73.
    Lanyi, J.K.: Molecular mechanism of ion transport in bacteriorhodopsin: insights from crystallographic, spectroscopic, kinetic, and mutational studies. J. Phys. Chem. B 48, 11441–11448 (2000)CrossRefGoogle Scholar
  74. 74.
    Morgan, J.E., Vakkasoglu, A.S., Lanyi, J.K., Lugtenburg, J., Gennis, R.B., Maeda, G.A.: Structure changes upon deprotonation of the proton release group in the bacteriorhodopsin photocycle. Biophys. J. 103, 444–452 (2012)CrossRefGoogle Scholar
  75. 75.
    Nango, E., Royant, A., Kubo, M., Nakane, T., Wlckstrand, C., Kimura, T., Tanaka, T., Tono, K., Soug, C., Tanaka, R., et al.: A three-dimensional movie of structural changes in bacteriorhodopsin. Science 354, 1552–1557 (2016)CrossRefGoogle Scholar
  76. 76.
    Duriach, M., Marti, T., Khorana, H.G., Rothschild, K.J.: UV-visible spectroscopy of bacteriorhodopsin mutants: substitution of Arg-82, Asp-85, Tyr-185, and Asp-212 results in abnormal light-dark adaptation. Proc. Natl. Acad. Sci. U S A 87, 9873–9877 (1990)CrossRefGoogle Scholar
  77. 77.
    Sonar, S., Krebs, M.P., Khorana, H.G., Rothchild, K.J.: Static and time-resolved absorption spectroscopy of the bacteriorhodopsin mutant Tyr185 → Phe: evidence for an equilibrium between bR570 and O-like species. Biochemistry 32, 223–2271 (1993)Google Scholar
  78. 78.
    Rath, P., Krebs, M.P., He, Y., Khorana, H.G., Rothchild, K.J.: Fourier transform raman spectroscopy of the bacteriorhodopsin mutant Tyr185 → Phe: formation of a stable O-like species during light adaptation and detection of its transient N-like photoproduct. Biochemistry 32, 2272–2281 (1993)CrossRefGoogle Scholar
  79. 79.
    Richter, H.-T., Needleman, R., Lanyi, J.K.: Perturbed interaction between residues 85 and 204 in Tyr185 → Phe and Asp85 → Glu bacteriorhodopsin. Biophys. J. 71, 3392–3398 (1996)Google Scholar
  80. 80.
    Iwasa, T., Tokunaga, F., Yoshizawa, T.: Photochemical reaction of 13-cis-bacteriorhodopsin studied by low temperature spectroscopy. Photochem. Photobiol. 33, 539–545 (1981)CrossRefGoogle Scholar
  81. 81.
    Roepe, P.D., Ahl, P.L., Herzfeld, J., Lugtenburg, J., Rothchild, K.J.: Tyrosine protonation changes in bacteriorhodopsin, a Fourier transform infrared study of BR648 and its primary photoproduct. J. Biol. Chem. 263, 5110–5117 (1988)Google Scholar
  82. 82.
    Van Greet, A.L.: Calbration of the methanol and glycol nuclear magnetic resonance thermometers with a static thermistor probe. Anal. Chem. 40, 2227–2229 (1968)CrossRefGoogle Scholar
  83. 83.
    Van Greet, A.L.: Calibration of methanol nuclear magnetic resonance thermometer at low temperature. Anal. Chem. 42, 679–680 (1970)CrossRefGoogle Scholar
  84. 84.
    Bielecki, A., Burum, D.P.: Temperature dependence of 207Pb MAS spectra of solid lead nitrate. An accurate, sensitive thermometer for variable-temperature MAS. J. Magn. Reson. A 116, 215–220 (1995)CrossRefGoogle Scholar
  85. 85.
    Zuo, C.S., Metz, K.R., Sun, Y., Sherry, A.D.: NMR temperature measurements using a paramagnetic Lanthanide complex. J. Magn. Reson. 133, 53–60 (1998)CrossRefGoogle Scholar
  86. 86.
    Schuff, N.: Haeberlen, 2D Correlation spectroscopy in homonuclear dipolar-coupled solids. J. Magn. Reson. 52, 267–281 (1983)Google Scholar
  87. 87.
    Bodenhausen, G., Freeman, R., Morris, G.A., Turner, D.L.: NMR spectra of some simple spin systems studied by two-dimensional Fourier transformation of spin echoes. J. Magn. Reson. 31, 75–95 (1978)Google Scholar
  88. 88.
    Prasad, J.S.: Orientational order parameters and conformation of nematic p-ethoxybenzyliden-p-n-butylaniline. J. Chem. Phys. 65, 941 (1976)CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Akira Naito
    • 1
  • Yoshiteru Makino
    • 2
  • Yugo Tasei
    • 2
  • Izuru Kawamura
    • 1
  1. 1.Faculty of EngineeringYokohama National UniversityYokohamaJapan
  2. 2.Graduate School of EngineeringYokohama National UniversityYokohamaJapan

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