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Time-Resolved Detection of Protein Fluctuations During Reactions

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Molecular Science of Fluctuations Toward Biological Functions

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Abstract

Biological molecules fluctuate at room temperature in solution because of thermal motion not only at the ground state but also during their functions. Why can biological molecules perform selective and efficient reactions in life? A field of “fluctuation and molecular science of biological molecules” can be established to link the relationship between fluctuations and biological reactions, and for that purpose, studies that examine fluctuations and dynamics of biological molecules are essential. To detect protein fluctuations during reactions, we have developed time-resolved methods to measure thermodynamic properties, which are closely related with fluctuations. In this chapter, examples are presented that show enhanced fluctuations of proteins during reactions.

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References

  1. Nelson DL, Cox MM (2000) Lehninger principles of biochemistry. Worth Publishers, New York

    Google Scholar 

  2. Landau L, Lifsitz E (1969) Statistical physics, theoretical physics, vol 5. Pergamon Press, Oxford

    Google Scholar 

  3. Heremans K, Smeller L (1998) Protein structure and dynamics at high pressure. Biochim Biophys Acta 1386:353–370

    Article  CAS  Google Scholar 

  4. Terazima M (2002) Molecular volume and enthalpy changes associated with irreversible photo-reactions. J Photochem Photobiol C 3:81–108

    Article  CAS  Google Scholar 

  5. Terazima M (2004) Time-resolved thermodynamic properties of intermediate species during photochemical reactions. Bull Chem Soc Jpn 77:23–41

    Article  CAS  Google Scholar 

  6. Terazima M (2000) Translational diffusion of organic radicals in solution. Acc Chem Res 33:687–694

    Article  CAS  Google Scholar 

  7. Terazima M (2006) Diffusion coefficients as a monitor of reaction kinetics of biological molecules. Phys Chem Chem Phys 8:545–557

    Article  CAS  Google Scholar 

  8. Eichler HJ, Günter P, Pohl DW (1986) Laser induced dynamic gratings. Spirnger, Berlin

    Book  Google Scholar 

  9. Terazima M, Hirota N, Braslavsky SE, Mandelis A, Bialkowski SE, Diebold GJ, Miller RJD, Fournier D, Palmer RA, Tam A (2004) Quantities, terminology and symbols in photothermal and related spectroscopies. Pure Appl Chem 76:1083–1118

    Article  CAS  Google Scholar 

  10. Terazima M (1998) Transient lens spectroscopy in a fast time scale. Israel J Chem 38:143–157

    Article  CAS  Google Scholar 

  11. Bialkowski SE (1996) Photothermal methods for chemical analysis. Wiley, New York

    Google Scholar 

  12. Perman B, Anderson S, Schmidt M, Moffat K (2000) New techniques in fast time-resolved structure determination. Cell Mol Biol 46:895–913

    CAS  Google Scholar 

  13. Nagy AM, Raicu V, Miller RJ (2005) Nonlinear optical studies of heme protein dynamics: implications for proteins as hybrid states of matter. Biochim Biophys Acta 1749:148–172

    Article  CAS  Google Scholar 

  14. Hilinski EF, Rentzepis PM (1983) Biological applications of picosecond spectroscopy. Nature 302:481–487

    Article  CAS  Google Scholar 

  15. Hummer G, Schotte F, Anfinrud PA (2004) Unveiling functional protein motions with picosecond x-ray crystallography and molecular dynamics simulations. Proc Natl Acad Sci U S A 101:15330–15334

    Article  CAS  Google Scholar 

  16. Lim M, Jackson TA, Anfinrud PA (1997) Ultrafast rotation and trapping of carbon monoxide dissociated from myoglobin. Nat Struct Biol 4:209–214

    Article  CAS  Google Scholar 

  17. Kuczera K, Lambry JC, Martin JL, Karplus M (1993) Nonexponential relaxation after ligand dissociation from myoglobin: a molecular dynamics simulation. Proc Natl Acad Sci U S A 90(12):5805–5807

    Article  CAS  Google Scholar 

  18. Tian WD, Sage JT, Champion PM (1993) Investigations of ligand association and dissociation rates in the “open” and “closed” states of myoglobin. J Mol Biol 233:155–166

    Article  CAS  Google Scholar 

  19. Hagen SJ, Hofrichter J, Eaton WA (1995) Protein reaction kinetics in a room-temperature glass. Science 269:959–962

    Article  CAS  Google Scholar 

  20. Frauenfelder H, Young RD, Fenimore PW (2013) Dynamics and the free-energy landscape of proteins, explored with the Mössbauer effect and quasi-elastic neutron scattering. J Phys Chem B 117:13301–13307

    Article  CAS  Google Scholar 

  21. Frauenfelder H, McMahon BH, Fenimore PW (2003) Myoglobin: the hydrogen atom of biology and a paradigm of complexity. Proc Natl Acad Sci U S A 100:8615–8617

    Article  CAS  Google Scholar 

  22. Frauenfelder H, McMahon BH, Austin RH, Chu K, Groves JT (2001) The role of structure, energy landscape, dynamics, and allostery in the enzymatic function of myoglobin. Proc Natl Acad Sci U S A 98:2370–2374

    Article  CAS  Google Scholar 

  23. Frauenfelder H (1995) Complexity in proteins. Nat Struct Biol 2:821–823

    Article  CAS  Google Scholar 

  24. Sakakura M, Yamaguchi S, Hirota N, Terazima N (2001) Dynamics of structure and energy of horse carboxymyoglobin after photodissociation of the carbon monoxide. J Am Chem Soc 123:4286–4294

    Article  CAS  Google Scholar 

  25. Sakakura M, Morishima I, Terazima M (2002) Structural dynamics of distal histidine replaced mutants of myoglobin accompanied with the photodissociation reaction of the ligand. Biochemistry 41:4837–4846

    Article  CAS  Google Scholar 

  26. Sakakura M, Morishima I, Terazima M (2001) The structural dynamics and ligand releasing process after the photodissociation of sperm whale carboxymyoglobin. J Phys Chem B 105:10424–10434

    Article  CAS  Google Scholar 

  27. Nishihara Y, Sakakura M, Kimura Y, Terazima M (2004) The escape process of carbon monoxide from myoglobin to solution at physiological temperature. J Am Chem Soc 126:11877–11888

    Article  CAS  Google Scholar 

  28. Zipp A, Kauzmann W (1973) Pressure denaturation of metmyoglobin. Biochemistry 12:4217–4228

    Article  CAS  Google Scholar 

  29. Meyer TE, Fitch JC, Bartsch RG, Tollin G, Cusanovich MA (1990) Soluble cytochromes and a photoactive yellow protein isolated from the moderately halophilic purple phototrophic bacterium, Rhodospirillum salexigens. Biochim Biophys Acta 1016:364–370

    Article  CAS  Google Scholar 

  30. Sprenger WW, Hoff WD, Armitage JP, Hellingwerf KJ (1993) The eubacterium Ectothiorhodospira halophila is negatively phototactic, with a wavelength dependence that fits the absorption spectrum of the photoactive yellow protein. J Bacteriol 175:3096–3104

    CAS  Google Scholar 

  31. Borgstahl GE, Williams DR, Getzoff ED (1995) 1.4 A structure of photoactive yellow protein, a cytosolic photoreceptor: unusual fold, active site, and chromophore. Biochemistry 34:6278–6287

    Article  CAS  Google Scholar 

  32. Hoff WD, Düx P, Hård K, Devreese B, Nugteren-Roodzant IM, Crielaard W, Boelens R, Kaptein R, van Beeumen J, Hellingwerf KJ (1994) Thiol ester-linked p-coumaric acid as a new photoactive prosthetic group in a protein with rhodopsin-like photochemistry. Biochemistry 33:13959–13962

    Article  CAS  Google Scholar 

  33. Hoff WD, van Stokkum IH, van Ramesdonk HJ, van Brederode ME, Brouwer AM, Fitch JC, Meyer TE, van Grondelle R, Hellingwerf KJ (1994) Measurement and global analysis of the absorbance changes in the photocycle of the photoactive yellow protein from Ectothiorhodospira halophila. Biophys J 67:1691–1705

    Article  CAS  Google Scholar 

  34. Meyer TE, Tollin G, Hazzard JH, Cusanovich MA (1989) Photoactive yellow protein from the purple phototrophic bacterium, Ectothiorhodospira halophila. Quantum yield of photobleaching and effects of temperature, alcohols, glycerol, and sucrose on kinetics of photobleaching and recovery. Biophys J 56:559–564

    Article  CAS  Google Scholar 

  35. Imamoto Y, Kataoka M, Tokunaga F (1996) Photoreaction cycle of photoactive yellow protein from Ectothiorhodospira halophila studied by low-temperature spectroscopy. Biochemistry 35:14047–14053

    Article  CAS  Google Scholar 

  36. Genick UK, Borgstahl GE, Ng K, Ren Z, Pradervand C, Burke PM, Srajer V, Teng TY, Schildkamp W, McRee DE, Moffat K, Getzoff ED (1997) Structure of a protein photocycle intermediate by millisecond time-resolved crystallography. Science 275:1471–1475

    Article  CAS  Google Scholar 

  37. Brudler R, Rammelsberg R, Woo TT, Getzoff ED, Gerwert K (2001) Structure of the I1 early intermediate of photoactive yellow protein by FTIR spectroscopy. Nat Struct Biol 8:265–270

    Article  CAS  Google Scholar 

  38. Rubinstenn G, Vuister GW, Mulder FA, Düx PE, Boelens R, Hellingwerf KJ, Kaptein R (1998) Structural and dynamic changes of photoactive yellow protein during its photocycle in solution. Nat Struct Biol 5:568–570

    Article  CAS  Google Scholar 

  39. Takeshita K, Hirota N, Imamoto Y, Kataoka M, Tokunaga F, Terazima M (2000) Temperature dependent volume change of initial step of the photoreaction of photoactive yellow protein studied by the transient grating. J Am Chem Soc 122:8524–8528

    Article  CAS  Google Scholar 

  40. Takeshita K, Hirota N, Imamoto Y, Kataoka M, Tokunaga F, Terazima M (2002) Thermodynamic and transport properties of intermediate states of photo-cyclic reaction of photoactive yellow protein. Biochemistry 41:3037–3048

    Article  CAS  Google Scholar 

  41. Takeshita K, Imamoto Y, Kataoka M, Mihara K, Tokunaga F, Terazima M (2002) Structural change of site-directed mutants of PYP: new dynamics during pR state. Biophys J 83:1567–1577

    Article  CAS  Google Scholar 

  42. van Brederode ME, Gensch T, Hoff WD, Hellingwerf KJ, Braslavsky SE (1995) Photoinduced volume change and energy storage associated with the early transformations of the photoactive yellow protein from Ectothiorhodospira halophila. Biophys J 68:1101–1109

    Article  Google Scholar 

  43. Perman B, Srajer V, Ren Z, Teng T, Pradervand C, Ursby T, Bourgeois D, Schotte F, Wulff M, Kort R, Hellingwerf K, Moffat K (1998) Energy transduction on the nanosecond time scale: early structural events in a xanthopsin photocycle. Science 279:1946–1950

    Article  CAS  Google Scholar 

  44. Xie A, Kelemen L, Hendriks J, White BJ, Hellingwerf KJ, Hoff WD (2001) Formation of a new buried charge drives a large-amplitude protein quake in photoreceptor activation. Biochemistry 40:1510–1517

    Article  CAS  Google Scholar 

  45. Bernard C, Houben K, Derix NM, Marks D, van der Horst MA, Hellingwerf KJ, Boelens R, Kaptein R, van Nuland NAJ (2005) The solution structure of a transient photoreceptor intermediate: 25 photoactive yellow protein. Structure 13:953–962

    Article  CAS  Google Scholar 

  46. Khan JS, Imamoto Y, Harigai M, Kataoka M, Terazima M (2006) Conformational changes of PYP monitored by diffusion coefficient: effect of N-terminal α-helices. Biophys J 90:3686–3693

    Article  CAS  Google Scholar 

  47. Hoshihara Y, Imamoto Y, Kataoka M, Tokunaga F, Terazima M (2008) Conformational changes in the N-terminal region of photoactive yellow protein: a time-resolved diffusion study. Biophys J 94:2187–2193

    Article  CAS  Google Scholar 

  48. Christie JM, Reymond P, Powell GK, Bernasconi P, Raibekas AA, Liscum E, Briggs WR (1998) Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282:1698–1701

    Article  CAS  Google Scholar 

  49. Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci U S A 98:6969–6974

    Article  CAS  Google Scholar 

  50. Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141

    Article  CAS  Google Scholar 

  51. Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954

    Article  CAS  Google Scholar 

  52. Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660

    Article  CAS  Google Scholar 

  53. Cheng P, He Q, Yang Y, Wang L, Liu Y (2003) Functional conservation of light, oxygen, or voltage domains in light sensing. Proc Natl Acad Sci U S A 100:5938–5943

    Article  CAS  Google Scholar 

  54. Crosson S, Rajagopal S, Moffat K (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42:2–10

    Article  CAS  Google Scholar 

  55. Huala E, Oeller PW, Liscum E, Han IS, Larsen E, Briggs WR (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278:2120–2123

    Article  CAS  Google Scholar 

  56. Swartz TE, Corchnoy SB, Christie JM, Lewis JW, Szundi I, Briggs WR, Bogomolni RA (2001) The photocycle of a flavin-binding domain of the blue light photoreceptor phototropin. J Biol Chem 276:36493–36500

    Article  CAS  Google Scholar 

  57. Swartz TE, Wenzel PJ, Corchnoy SB, Briggs WR, Bogomolni RA (2002) Vibration spectroscopy reveals light-induced chromophore and protein structural changes in the LOV2 domain of the plant blue-light receptor phototropin 1. Biochemistry 41:7183–7189

    Article  CAS  Google Scholar 

  58. Crosson S, Moffat K (2001) Structure of a flavin-binding plant photoreceptor domain: insights into light-mediated signal transduction. Proc Natl Acad Sci U S A 98:2995–3000

    Article  CAS  Google Scholar 

  59. Crosson S, Moffat K (2002) Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch. Plant Cell 14:1067–1075

    Article  CAS  Google Scholar 

  60. Fedorov R, Schlichting I, Hartmann E, Domratcheva T, Fuhrmann M, Hegemann P (2003) Crystal structures and molecular mechanism of a light-induced signaling switch: the Phot-LOV1 domain from Chlamydomonas reinhardtii. Biophys J 84:2474–2482

    Article  CAS  Google Scholar 

  61. Eitoku T, Nakasone Y, Matsuoka D, Tokutomi S, Terazima M (2005) Conformational dynamics of phototropin 2 LOV2 domain with the linker upon photoexcitation. J Am Chem Soc 127:13238–13244

    Article  CAS  Google Scholar 

  62. Nakasone Y, Eitoku T, Matsuoka D, Tokutomi S, Terazima M (2007) Dynamics of conformational changes of Arabidopsis phototropin 1 LOV2 with the linker domain. J Mol Biol 367:432–442

    Article  CAS  Google Scholar 

  63. Kasahara M, Swartz TE, Olney MA, Onodera A, Mochizuki N, Fukuzawa H, Asamizu E, Tabata S, Kanegae H, Takano M, Christie JM, Nagatani A, Briggs WR (2002) Photochemical properties of the flavin mononucleotide-binding domains of the phototropins from Arabidopsis, rice, and Chlamydomonas reinhardtii. Plant Physiol 129:762–773

    Article  CAS  Google Scholar 

  64. Harper SM, Neil LC, Gardner KH (2003) Structural basis of a phototropin light switch. Science 301:1541–1544

    Article  CAS  Google Scholar 

  65. Eitoku T, Nakasone Y, Zikihara K, Matsuoka D, Tokutomi S, Terazima M (2007) Photochemical intermediates of Arabidopsis phototropin 2 LOV domains associated with conformational changes. J Mol Biol 371:1290–1303

    Article  CAS  Google Scholar 

  66. Schuttrigkeit TA, Kompa CK, Salomon M, Rudiger W, Michel-Beyerle ME (2003) Primary photophysics of the FMN binding LOV2 domain of the plant blue light receptor phototropin of Avena sativa. Chem Phys 294:501–508

    Article  CAS  Google Scholar 

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Acknowledgments

The author is deeply indebted to coauthors of the papers contained in this article. This work was supported by a Grant-in-Aid for Scientific Research on Innovative Areas (research in a proposed research area) (20107003) from the Ministry of Education, Culture, Sports, Science and Technology in Japan.

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Authors and Affiliations

  1. Department of Chemistry, Graduate School of Science, Kyoto University, Kyoto, 606-8502, Japan

    Masahide Terazima

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  1. Masahide Terazima
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Correspondence to Masahide Terazima .

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Editors and Affiliations

  1. Kyoto University, Kyoto, Japan

    Masahide Terazima

  2. Nara Institute of Science and Tech, Ikoma, Japan

    Mikio Kataoka

  3. Sojo University, Kumamoto, Japan

    Ryuichi Ueoka

  4. Nagoya University, Nagoya, Japan

    Yuko Okamoto

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Terazima, M. (2016). Time-Resolved Detection of Protein Fluctuations During Reactions. In: Terazima, M., Kataoka, M., Ueoka, R., Okamoto, Y. (eds) Molecular Science of Fluctuations Toward Biological Functions . Springer, Tokyo. https://doi.org/10.1007/978-4-431-55840-8_1

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