Journal of Muscle Research & Cell Motility

, Volume 13, Issue 2, pp 132–145 | Cite as

Structure of actin observed by fluorescence resonance energy transfer spectroscopy

  • Masao Miki
  • Séan I. O'donoghue
  • Cristobal G. Dos Remedios
Review

Keywords

Energy Transfer Fluorescence Resonance Energy Transfer Resonance Energy Resonance Energy Transfer Transfer Spectroscopy 

Abbreviations

anthaniloyl-ATP

4-dimethylamino-phenylazophenyl-4′-maleimide

DABMI

5-(dimethylamino) naphthalene-1-sulphonyl chloride

Dansyl-Cl

N-(4-dimethylamino-3,5-dinitrophenyl) maleimide

DDPM

dansyl cadaverine

DNC

1, N6-etheno-adenosine 5′-triphosphate

ɛ-ATP

5-(iodoacetamide) eosin

EIA

fluorescein-5-isothiocyanate

FITC

formycin A 5′-triphosphate

FTP

5-[2-[(iodoacetyl)-amino]ethyl}amino naphthalene-1-sulphonic acid

IAEDANS

5-(iodoacetamido)-4-nitrobenzo-2-oxa-1,3-diazole

IAF

4-[N-(iodoacetoxy)ethyl-N-methyl]amino-7-nitrobenz-2-oxa-1,3-diazole

IANBD

N-methylanthraniloyl-ATP

MANT-ATP

monobromobimane

MBB

7-chloro-4-nitrobenzo-2-oxa-1,3-diazole

NBD-Cl

rhodamine cadaverine

RHC

tetramethyl rhodamine-5-iodacetamide

TMRI

2′(or 3′)-O-(2,4,6-trinitrophenyl) adenosine 5-diphosphate

ADP

4-dimethylaminoazobenzene-4′-sulphonyl chloride

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Banks, R. D., Blake C. C. F., Evans, P. R., Haser, R., Rice, D. W., Hardy, G. W., Merrett, M. &Phillips, A. W. (1979) Sequence, structure and activity of phosphoglycerate kinase: a possible hinge-bending enzyme.Nature (London) 279, 773–7.Google Scholar
  2. Barden, J. A. (1985) Fluorescence energy transfer between Tyr-69 and Cys-374 in actin.Biochem. Int.11, 583–9.Google Scholar
  3. Barden, J. A. &Dos Remedios, C. G. (1984) The environment of the high affinity cation binding site on actin and the separation between cation and ATP sites as revealed by proton NMR and fluorescence spectroscopy.J. Biochem. (Tokyo) 96, 913–21.Google Scholar
  4. Barden, J. A. &Dos Remedios, C. G. (1985) Conformational changes in actin resulting from Ca2+/Mg2+ exchange as detected by proton NMR spectroscopy.Eur. J. Biochem. 146, 5–8.Google Scholar
  5. Barden, J. A. &Miki, M. (1986) The distance separating Tyr-69 from the high affinity nucleotide and metal binding sites in actin.Biochem. Int. 12, 321–9.Google Scholar
  6. Barden, J. A. &Dos Remedios, C. G. (1987) Fluorescence resonance energy transfer between sites in G-actin. The spatial relationship between Cys-10, Try-69, Cys-374, the high affinity metal and the nucleotide.Eur. J. Biochem. 168, 103–9.Google Scholar
  7. Barden, J. A. &Phillips, L. (1990) 19F NMR study of the myosin and tropomyosin binding sites on actin.Biochemistry 29, 1348–54.Google Scholar
  8. Barden, J. A., Cooke, R. Wright, P. E. &Dos Remedios, C. G. (1980) Proton nuclear magnetic resonance and electron paramagnetic resonance studies on skeletal muscle actin indicate that the metal and nucleotide binding sites are separate.Biochemistry 19, 5912–16.Google Scholar
  9. Barden, J. A., Miki, M. &Dos Remedios, C. G. (1986) Selective labelling of Cys-10 on actin.Biochem. Int.12, 95–101.Google Scholar
  10. Barden, J. A., Phillips, L. Cornell, B. A. &Dos Remedios, C. G. (1989) 19F NMR study studies of the interaction of selectively labelled actin and myosin.Biochemistry 28, 5895–901.Google Scholar
  11. Bender, N., Fasold, H., Kenmoku, A., Middlehoff, G. &Volk, K. E. (1976) The selective blocking of the polymerization reaction of striated muscle actin leading to a derivative suitable for crystallization.Eur. J. Biochem. 64, 215–18.Google Scholar
  12. Botts, J., Takashi, R., Torgerson, P., Hozumi, T., Muhlrad, A., Mornet, D. &Morales, M. R. (1984) On the mechanism of energy transduction in myosin subfragment-1.Proc. Natl. Acad. Sci. USA 81, 2060–4.Google Scholar
  13. Botts, J., Thomason, J. R. &Morales, M. F. (1989) On the origin and transmission of force in actomyosin subfragment-1.Proc. Natl. Acad. Sci USA 86, 2204–8.Google Scholar
  14. Brauer, M. &Sykes, B. D. (1981) Phosphorus-31 nuclear magnetic resonance studies of adenosine 5′-triphosphate bound to a nitrated derivative of G-actin.Biochemistry 20, 6764–75.Google Scholar
  15. Brauer, M. &Sykes, B. D. (1982) Effects of manganous ion on the phosphorus-31 nuclear magnetic resonance spectrum of adenosine triphosphate bound to nitrated actin.Biochemistry 21, 5934–9.Google Scholar
  16. Burtnick, L. (1984) Modification of actin with fluorescein isothiocyanate.Biochim. Biophys. Acta 791, 57–62.Google Scholar
  17. Chantler, P. &Grazter, W. B. (1975) Effects of specific chemical modification of actin.Eur. J. Biochem. 60, 67–72.Google Scholar
  18. Cheung, H. C. &Liu, B. M. (1984) Distance between the nucleotide site and cysteine 374 of G-actin by resonance energy transfer.J. Muscle Res. Cell Motil. 5, 65–80.Google Scholar
  19. Dale, R. E. &Eisinger, J. (1974) Intramolecular distance determinations by energy transfer. Dependence on orientational freedom of donor and acceptor.Biopolymers 13, 1573–605.Google Scholar
  20. Dale, R. E., Eisinger, J. &Blumberg, W. E. (1979) The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer.Biophys. J. 26, 161–94.Google Scholar
  21. Dos Remedios, C. G. &Dickens, M. J. (1978) Actin microcrystals and tubes formed in the presence of gadolinium ions.Nature (London) 276, 731–3.Google Scholar
  22. Dos Remedios, C. G. &Cooke, R. (1984) Fluorescence energy transfer between probes on actin and probes on myosin.Biochim. Biophys. Acta 188, 193–205.Google Scholar
  23. Dos Remedios, C. G. &Mihashi, K. (1985) A new fluorescent labelled site on skeletal muscle actin.Proc. Aust. Biochem. Soc. 17, 45.Google Scholar
  24. Dos Remedios, C. G., Hambly, B. D. &Barden, J. A. (1985) On the nucleotide binding site of actin. InCell Motility: Mechanism and Regulation (edited by Ishikawa, H., Hatano, S. & Sato, H.) pp. 31–8. University of Tokyo Press.Google Scholar
  25. Dos Remedios, C. G., Miki, M. &Barden, J. A. (1987) Fluorescence resonance energy transfer measurements of distances in actin and myosin. A critical evaluation.J. Muscle Res. Cell Motil. 8, 97–117.Google Scholar
  26. Dos Remedios, C. G., O'donoghue, S. I., Barden, J. A. &Miki, M. (1988) Fluorescent labelling of actin with rhodamine-X-maleimide.Biophys. J. 53, 28a.Google Scholar
  27. Egelman, E. (1985) The structure of F-actin.J. Muscle Res. Cell Motil. 6, 129–51.Google Scholar
  28. Elzinga, M. &Phelan, J. J. (1984) F-actin is intermolecularly crosslinked by N,N′-p-phenylenedimaleimide through lysine-191 and cysteine-374.Proc. Natl Acad. Sci. USA 81, 6599–602.Google Scholar
  29. Förster, T. (1948) Zwischenmolekulare energiewanderung und fluoreszenz.Ann. Phys. 9, 21–33.Google Scholar
  30. Förster, T. (1965) Delocalized excitation and excitation energy transfer. InModern Quantum Chemistry (edited by Sinanoglu, O.) partiii, pp. 93–137. New York: Academic Press.Google Scholar
  31. Frankel, S., Condeelis, J. &Leinwand, L. (1990) Expression of actin inEscherichia coli. Aggregation, solubilization, and functional analysis.J. Biol. Chem. 15, 17980–7.Google Scholar
  32. Frieden, C., Lieberman, D. &Gilbert, H. R. (1980) A fluorescent probe for conformational changes in skeletal muscle G-actin.J. Biol. Chem. 255, 8991–3.Google Scholar
  33. Hambly, B. D., Barden, J. A., Miki, M. &Dos Remedios, C. G. (1986) Structural and functional domains on actin.Bioessays 4, 124–8.Google Scholar
  34. Hanson, J. &Lowey, J. (1964) The structure of actin filaments and the origin of the axial periodicity in the 1-substance of vertebrate striated muscle.Proc. R. Soc. Lond. B 160, 449–60.Google Scholar
  35. Hatano, S., Owaribe, K., Matsumura, F., Hasegawa, T. &Takahashi, S. (1980) Characterization of actin, actinin and myosin isolated fromPhysarum.Can. J. Botany 58, 750–9.Google Scholar
  36. Hiratsuka, T. (1983) New ribose-modified fluorescent analogs of adenine and guanidine nucleotides available as substrates for various enzymes.Biochim. Biophys. Acta 742, 496–508.Google Scholar
  37. Holmes, K. C., Popp, D., Gebhard, W. &Kabsch, W. (1990) Atomic model of the actin filament.Nature (London) 347, 44–9.Google Scholar
  38. Kabsch, W., Mannherz, H. G., Suck, D., Pai, E. F. &Holmes, K. C. (1990) Atomic structure of the actin: DNase I complex.Nature (London) 47, 37–44.Google Scholar
  39. Kasprzak, A. A., Takashi, R. &Morales, M. F. (1988) Orientation of the actin monomer in the F-actin filament: radial co-ordinate of glutamine-41 and effect of myosin subfragment-1 binding on the monomer orientation.Biochemistry 27, 4512–22.Google Scholar
  40. Kenner, R. A. &Neurath, H. (1971) Activity and fluorescent derivatives of aminotyrosyl trypsin and trypsinogen.Biochemistry 10, 551–7.Google Scholar
  41. Kuwayama, H. &Yount, R. G. (1986) Photoaffinity labelling of skeletal muscle actin by 2-N3ADP.Biophys. J. 49, 454a.Google Scholar
  42. Lehrer, S. S. &Elzinga, M. (1972) Fluorescence studies on nitrated actin.Fed. Proc. 31, 502.Google Scholar
  43. Lin, T-I. &Dowben, R. M. (1982) Fluorescence spectroscopic studies of pyrene-actin adducts.Biophys. Chem. 15, 289–98.Google Scholar
  44. Loscalzo, J. &Reed, G. H. (1976) Spectroscopic studies of actin-metal-nucleotide complexes.Biochemistry 15, 5407–13.Google Scholar
  45. Lu, R. &Zilagyi, L. (1981) Change of reactivity of lysine residues upon actin polymerization.Biochemistry 20, 5914–19.Google Scholar
  46. Mannherz, H. G., Kabsch, W. &Leberman, R. (1977) Crystals of skeletal muscle actin: pancreatic DNAase I complex.FEBS Lett. 73, 141–3.Google Scholar
  47. Miki, M. (1987) The recovery of the polymerization of Lys-61-labelled actin by the addition of phalloidin.Eur. J. Biochem. 164, 229–35.Google Scholar
  48. Miki, M. (1989) Interaction of Lys-61 labelled actin with myosin subfragment 1 and the regulatory proteins.J. Biochem. (Tokyo) 106, 651–5.Google Scholar
  49. Miki, M. (1990) Resonance energy transfer between points in a reconstituted skeletal muscle thin filament.Eur. J. Biochem. 187, 155–62.Google Scholar
  50. Miki, M. (1991) Detection of conformational changes in actin. e.g. fluorescence resonance energy transfer between Tyr-69 and Cys-374.Biochemistry (in press).Google Scholar
  51. Miki, M. &Mihashi, K. (1978) Fluorescence energy transfer between ɛ-ATP at the nucleotide site and N-(4-dimethylamino-3,5-dinitrophenyl)-maleimide at Cys-374 of G-actin.Biochim. Biophys. Acta 533, 163–72.Google Scholar
  52. Miki, M. &Iio, T. 1984) Fluorescence energy transfer measurements between the nucleotide binding site and Cys-373 in actin and their application to the kinetics of actin polymerization.Biochim. Biophys. Acta 790, 201–7.Google Scholar
  53. Miki, M. &Wahl, P. (1984) Flurorescence energy transfers in labelled G-actin and F-actin.Biochim. Biophys. Acta 786, 188–96.Google Scholar
  54. Miki, M. &Wahl, P. (1985) Fluorescence energy transfers between points in G-actin: the nucleotide binding site, the metal-binding site and Cys-373.Biochim. Biophys. Acta 828, 188–95.Google Scholar
  55. Miki, M. &Dos Remedios, C. G. (1990) A determination of the radial coordinate of Tyr-69 in F-actin using fluorescence energy transfer.Biochem. Int. 22, 125–32.Google Scholar
  56. Miki, M. &Hozumi, T. (1991) Interaction of maleimido-benzoyl actin with myosin subfragment 1 and tropomyosintroponin.Biochemistry 30, 5625–30.Google Scholar
  57. Miki, M., Barden, J. A. &Dos Remedios, C. G. (1986a) Fluorescence resonance energy transfer between the nucleotide binding site and Cys-10 in G-actin and F-actin.Biochim. Biophys. Acta 872, 76–82.Google Scholar
  58. Miki, M., Barden, J. A. &Dos Remedios, C. G. (1986b) The distance separating Cys-10 from the high-affinity metal binding site in actin.Biochem. Int. 12, 807–13.Google Scholar
  59. Miki, M., Barden, J. A., Hambly, B. D. &Dos Remedios, C. G. (1986c) Fluorescence energy transfer between Cys-10 residues in F-actin filaments.Biochem. Int. 12, 725–31.Google Scholar
  60. Miki, M., Hambly, B. D. &Dos Remedios, C. G. (1986d) Fluorescence energy transfer between nucleotide binding sites in an F-actin filament.Biochim. Biophys. Acta 871, 137–41.Google Scholar
  61. Miki, M., Barden, J. A. &Dos Remedios, C. G., Phillips, L. &Hambly, B. D. (1987a) Interaction of chemically modified actin with phalloidin.Eur. J. Biochem. 165, 125–30.Google Scholar
  62. Miki, M., Dos Remedios, C. G. &Barden, J. A. (1987b) Spatial relationship between the nucleotide-binding site, Lys-61 and Cys-374 in actin and a conformational change induced by myosin subfragment-1 binding.Eur. J. Biochem. 168, 339–45.Google Scholar
  63. Milligan, R. A. &Flicker, P. (1987) Structural relationships of actin, myosin and tropomyosin revealed by cryo-electron microscopy.J. Cell Biol. 105, 29–39.Google Scholar
  64. Nowak, E., Strzelecka-Golaszewska, H. &Goody, R. S. (1988) Kinetics of nucleotide and metal ion interaction with G-actin.Biochemistry 8, 1785–92.Google Scholar
  65. O'Brien, E. J., Couch, J., Johnson, G. R. P. &Morris, E. P. (1983) Structure of actin and the thin filament. InStructure of Actin In Muscle And Non-Muscle Cells (edited by Dos Remedios, C. G. & Barden, J. A.) pp. 3–15. Sydney: Academic Press.Google Scholar
  66. O'Donoghue, S. I. (1991) Structural interpretation of fluorescence resonance-energy transfer measurements.Comput. Applic. Biosci. 7, 471–7.Google Scholar
  67. O'Donoghue, S. I., Miki, M. &Dos Remedios, C. G. (1992) Removing the two C-terminal residues of actin affects the filament structure.Arch. Biochem. Biophys (in press).Google Scholar
  68. Offer, G., Baker, H. &Baker, L. (1972) Interaction of monomeric and polymeric actin with myosin subfragment-1.J. Mol. Biol. 66, 435–44.Google Scholar
  69. Oosawa, F. (1983) Macromolecular assembly of actin. InMuscle and Non-muscle Motility (edited by Stracher, A.), Vol. 1, pp. 151–216. New York: Academic Press.Google Scholar
  70. Phil, A. &Lange, R. (1962) The interaction of oxidized gluthathione, cystamine monosulfoxide, and tetrathionate with the -SH groups of rabbit muscle D-glyceraldehyde 3-phosphate dehydrogenase.J. Biol. Chem. 237, 1356–62.Google Scholar
  71. Pollard, T. D. (1990) Actin.Curr. Opin. Cell Biol. 2, 33–40.Google Scholar
  72. Press, W. H., Flannery, B. P., Teukolsky, S. A. &Vetterling, W. T. (1986)Numerical Recipes: The Art of Scientific Computing. Cambridge: Cambridge University Press.Google Scholar
  73. Sakabe, N., Sakabe, K., Sasaki, K., Kondo, H., Ema, T., Kamiya, N. &Matsushima, M. (1979) Crystallographic studies of the chicken gizzard G-actin-DNase I complex at 5 Å resolution.J. Biochem. (Tokyo) 93, 299–302.Google Scholar
  74. Schiller, P. W. (1975) The measurement of intramolecular distances by energy transfer. InBiochemical Fluorescence: Concepts (edited by Chen, R. F. & Edelhoch, H.), Vol. 1, pp. 285–303. New York: Marcel Decker.Google Scholar
  75. Schutt, C., Lindberg, U., Myslik, J. &Strauss, N. (1989) Molecular packing in profilin-actin crystals and its implications.J. Mol. Biol. 209, 735–46.Google Scholar
  76. Sleigh, R. W. &Burleigh, R. W. (1973) Site of action of sulphydryl spin labels with skeletal actin.Arch. Biochem. Biophys. 159, 792–801.Google Scholar
  77. Stryer, L. (1978) Fluorescence energy transfer as a spectroscopic ruler.Ann. Rev. Biochem. 47, 819–46.Google Scholar
  78. Straub, F. B. (1942) Actin.Studies Med. Inst. Szeged. 2, 3–15.Google Scholar
  79. Suck, D., Kabsch, W. &Mannherz, H. G. (1981) Three-dimensional structure of the complex of skeletal muscle actin with bovine pancreatic DNase I at 6 Å resolution.Proc. Natl. Acad. Sci. USA 78, 4319–23.Google Scholar
  80. Sugino, H., Sakabe, N., Sakabe, K., Hatano, S., Oosawa, F., Mikawa, T. &Ebashi, S. (1979) Crystallization and preliminary crystallographic data of chicken gizzard G-actin: DNase I complex andPhysarum G-actin: DNase I complex.Biochem. J. (Tokyo) 86, 257–60.Google Scholar
  81. Sutoh, K. (1982) Identification of myosin binding sites on the actin sequence.Biochemistry 27, 938–43.Google Scholar
  82. Takashi, R. (1988) A novel actin label. A fluorescent probe at glutamine 41 and its consequences.Biochemistry 27, 938–43.Google Scholar
  83. Tao, T. &Lamkin, M. (1981) Excitation energy transfer studies on the proximity between SHI and the adeniosinetriphosphatase site in myosin subfragment 1.Biochemistry 20, 5051–55.Google Scholar
  84. Taylor, D. L., Reidler, J., Spudich, J. A. &Stryer, L. (1981) Detection of actin assembly by fluorescence energy transfer.J. Cell Biol. 89, 362–7.Google Scholar
  85. Yang, C. &Soll, D. (1974) Studies of transfer RNA tertiary structure by singlet-singlet energy transfer.Proc. Natn Acad. Sci. USA 71, 2838–42.Google Scholar

Copyright information

© Chapman & Hall 1992

Authors and Affiliations

  • Masao Miki
    • 1
  • Séan I. O'donoghue
    • 1
  • Cristobal G. Dos Remedios
    • 1
  1. 1.Muscle Research Unit, Department of AnatomyUniversity of SydneySydneyAustralia

Personalised recommendations