Orientation and interactions of an essential tryptophan (Trp-38) in the capsid subunit of Pf3 filamentous virus

Biophysical Journal

Volumn 84, Issue 3, 2003, Pages 1969-1976

  Tsuboi, Masamichi ^a,b   Overman, Stacy A ^a   Nakamura, Koji ^a,c   Rodriguez Casado, Arantxa ^a   Thomas Jr , George J ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b IWAKI MEISEI UNIVERSITY   (Japan)

^c Gifu College of Medical Technology   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CAPSID PROTEIN; CATION; GUANIDINE; INDOLE; SINGLE STRANDED DNA; TRYPTOPHAN;

ALPHA HELIX; ARTICLE; BACTERIOPHAGE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; FLUORESCENCE; MOLECULAR MODEL; NONHUMAN; PROTEIN CONFORMATION; PSEUDOMONAS AERUGINOSA; RAMAN SPECTROMETRY; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; X RAY DIFFRACTION;

FILAMENTOUS BACTERIOPHAGE; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS PHAGE PF3; UNIDENTIFIED BACTERIOPHAGE;

EID: 0037340562     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)75005-X     Document Type: Article

References (43)

1. Arp, Z., D. Autrey, J. Laane, S. A. Overman, and G. J. Thomas, Jr. 2001. Tyrosine Raman signatures of the filamentous virus Ff are diagnostic of non-hydrogen-bonded phenoxyls: demonstration by Raman and infrared spectroscopy of p-Cresol vapor. Biochemistry. 40:2522-2529.
2. Aubrey, K. L., and G. J. Thomas, Jr. 1991. Raman spectroscopy of filamentous bacteriophage Ff (fd, M13, f1) incorporating specifically-deuterated alanine and tryptophan side chains: assignments and structural interpretation. Biophys. J. 61:1337-1349.
3. Benevides, J. M., M. Tsuboi, A. H. J. Wang, and G. J. Thomas, Jr. 1993. Local Raman tensors of double-helical DNA in the crystal: a basis for determining DNA residue orientations. J. Am. Chem. Soc. 115:5351-5359.
4. Blanch, E. W., A. F. Bell, L. Hecht, L. A. Day, and L. D. Barron. 1999. Raman optical activity of filamentous bacteriophages: hydration of alphahelices. J. Mol. Biol. 290:1-7.
5. Blanch, E. W., L. Hecht, L. A. Day, D. M. Pederson, and L. D. Barron. 2001. Tryptophan absolute stereochemistry in viral coat proteins from Raman optical activity. J. Am. Chem. Soc. 123:4863-4864.
6. Brunger, A. T., P. D. Adams, G. M. Clore, W. L. Delano, P. Gross, R. W. Grosse-Kunstleve, J.-S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simmonson, and G. L. Warren. 1998. Crystallography and NMR system. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
7. Day, L. A., C. J. Marzec, S. A. Reisberg, and A. Casadevall. 1988. DNA packing in filamentous bacteriophages. Annu. Rev. Biophys. Biophys. Chem. 17:509-539.
8. Feng, J. N., P. Model, and M. Russel. 1999. A trans-envelope protein complex needed for filamentous phage assembly and export. Mol. Microbiol. 34:745-755.
9. Gallivan, J. P., and D. A. Dougherty. 1999. Cation-π interactions in structural biology. Proc. Natl. Acad. Sci. USA. 96:9459-9464.
10. Hubbard, S. R., L. Wei, L. Ellis, and W. A. Hendrickson. 1994. Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature. 372:746-754.
11. Kiefer, D., X. Hu, R. Dalbey, and A. Kuhn. 1997. Negatively charged amino acid residues play an active role in orienting the Sec-independent Pf3 coat protein in the Escherichia coli inner membrane. EMBO J. 16:2197-2204.
12. Kiefer, D., and A. Kuhn. 1999. Hydrophobic forces drive spontaneous membrane insertion of the bacteriophage Pf3 coat protein without topological control. EMBO J. 18:6299-6306.
13. Kraulis, P. J. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946-950.
14. Kuhn, A. 1995. Major coat proteins of bacteriophage Pf3 and M13 as model systems for Sec-independent protein transport. FEMS Microbiol. Rev. 17:185-190.
15. Ma, J. C., and D. A. Dougherty. 1997. The cation-π interaction. Chem. Rev. 97:1303-1324.
16. Marvin, D. A. 1998. Filamentous phage structure, infection and assembly. Curr. Opin. Struct. Biol. 8:150-158.
17. Marvin, D. A., R. D. Hale, C. Nave, and M. H. Citterich. 1994. Molecular models and structural comparisons of native and mutant Class I filamentous bacteriophages: Ff (fd, f1, M13), If1 and IKe. J. Mol. Biol. 235:260-286.
18. Matsuno, M., H. Takeuchi, S. A. Overman, and G. J. Thomas, Jr. 1998. Orientations of Tyrosines 21 and 24 in coat subunits of Ff filamentous virus: determination by Raman linear intensity difference spectroscopy and implications for subunit packing. Biophys. J. 74:3217-3225.
19. Overman, S. A., and G. J. Thomas. Jr. 1995. Raman spectroscopy of the filamentous virus Ff (fd, f1, M13): structural interpretation for coat protein aromatics. Biochemistry. 34:5440-5451.
20. Overman, S. A., M. Tsuboi, and G. J. Thomas, Jr. 1996. Subunit orientation in the filamentous virus Ff (fd, f1, M13). J. Mol. Biol. 259:331-336.
21. Pederson, D. M., L. C. Welsh, D. A. Marvin, M. Sampson, R. N. Perham, M. Yu, and M. R. Slater. 2001. The protein capsid of filamentous bacteriophage PH75 from Thermus thermophilus. J. Mol. Biol. 309:401-421.
22. Ridder, A. N., S. Morein, J. G. Stam, A. Kuhn, B. de Kruijff, and J. A. Killian. 2000. Analysis of the role of interfacial tryptophan residues in controlling the topology of membrane proteins. Biochemistry. 39:6521-6528.
23. Symmons, M. F., L. C. Welsh, C. Nave, D. A. Marvin, and R. N. Perham. 1995. Matching electrostatic charge between DNA and coat protein in filamentous bacteriophage. Fibre difraction of charge-deletion mutants. J. Mol. Biol. 245:86-91.
24. Takeuchi, H., M. Matsuno, S. A. Overman, and G. J. Thomas, Jr. 1996. Raman linear intensity difference of flow-oriented macromolecules: orientation of the indole ring of Tryptophan-26 in filamentous virus fd. J. Am. Chem. Soc. 118:3498-3507.
25. Thomas, G. J., Jr., J. M. Benevides, S. A. Overman, T. Ueda, K. Ushizawa, M. Saitoh, and M. Tsuboi. 1995. Polarized Raman spectra of oriented fibers of A DNA and B DNA: anisotropic and isotropic local Raman tensors of base and backbone vibrations. Biophys. J. 68:1073-1088.
26. Thomas, G. J., Jr., B. Prescott, and L. A. Day. 1983. Structure similarity, difference and variability in the filamentous viruses fd, If1, IKe, Pf1, Xf and Pf3. J. Mol. Biol. 165:321-356.
27. Tsuboi, M., T. Ikeda, and T. Ueda. 1991. Raman microscopy of a small unixial crystal: tetragonal aspartame. J. Raman Spectrosc. 22:619-626.
28. Tsuboi, M., S. A. Overman, and G. J. Thomas, Jr. 1996a. Orientation of Tryptophan-26 in coat protein subunits of the filamentous virus Ff by polarized Raman microspectroscopy. Biochemistry. 35:10403-10410.
29. -1 as an indicator of protein α-helix orientation: application to Pf1 filamentous virus. Biochemistry. 39:2677-2684.
30. Tsuboi, M., and G. J. Thomas, Jr. 1997. Raman scattering tensors in biological molecules and their assemblies. Appl. Spectrosc. Revs. 32:263-299.
31. Tsuboi, M., T. Ueda, K. Ushizawa, Y. Ezaki, S. A. Overman, and G. J. Thomas, Jr. 1996b. Raman tensors for the tryptophan side chain in proteins determined by polarized Raman microspectroscopy of oriented N-Acetyl-L-Tryptophan crystals. J. Mol. Struct. 379:43-50.
32. Tsuboi, M., K. Ushizawa, K. Nakamura, J. M. Benevides, S. A. Overman, and G. J. Thomas, Jr. 2001. Orientations of Tyr 21 and Tyr 24 in the capsid of filamentous virus Ff determined by polarized Raman spectroscopy. Biochemistry. 40:1238-1247.
33. Webster, R. E. 1996. Biology of the filamentous bacteriophage. In Phage Display of Peptides and Proteins. B. K. Kay, J. Winter, and J. McCaffery, editors. Academic Press, London. 1-20.
34. Welsh, L. C., M. F. Symmons, and D. A. Marvin. 2000. The molecular structure and structure transition of the α-helical capsid in filamentous bacteriophage Pf1. Acta Crystallogr. D Biol. Crystallogr. 56:137-150.
35. Welsh, L. C., M. F. Symmons, J. M. Sturtevant, D. A. Marvin, and R. N. Perham. 1998. Structure of the capsid of Pf3 filamentous phage determined from x-ray fibre diffraction data at 3.1 Å resolution. J. Mol. Biol. 283:155-177.
36. Wen, Z. Q., A. Armstrong, and G. J. Thomas, Jr. 1999. Demonstration by ultraviolet resonance Raman spectroscopy of differences in DNA organization and interactions in filamentous viruses Pf1 and fd. Biochemistry. 38:3148-3156.
37. Wen, Z. Q., S. A. Overman, P. Bondre, and G. J. Thomas, Jr. 2001. Structure and organization of bacteriophage Pf3 probed by Raman and ultraviolet resonance Raman spectroscopy. Biochemistry. 40:449-458.
38. Wen, Z. Q., S. A. Overman, and G. J. Thomas, Jr. 1997. Structure and interactions of the single-stranded DNA genome of filamentous virus fd: investigation by ultraviolet resonance Raman spectroscopy. Biochemistry. 36:7810-7820.
39. Wen, Z. Q., and G. J. Thomas, Jr. 2000. Ultraviolet-resonance Raman spectroscopy of the filamentous virus Pf3: interactions of Trp 38 specific to the assembled virion subunit. Biochemistry. 39:146-152.
40. Williams, K. A., and C. M. Deber. 1996. Biophysical characterization of wild-type and mutant bacteriophage IKe major coat protein in the virion and in detergent micelles. Biochemistry. 35:10472-10483.
41. Williams, K. A., N. A. Farrow, C. M. Deber, and L. E. Kay. 1996. Structure and dynamics of bacteriophage IKe major coat protein in MPG micelles by solution NMR. Biochemistry. 35:5145-5157.
42. Williams, K. A., M. Glibowicka, Z. Li, H. Li, A. R. Khan, Y. M. Chen, J. Wang, D. A. Marvin, and C. M. Deber. 1995. Packing of coat protein amphipathic and transmembrane helices in filamentous bacteriophage M13: role of small residues in protein oligomerization. J. Mol. Biol. 252:6-14.
43. Yuen, C. T., A. R. Davidson, and C. M. Deber. 2000. Role of aromatic residues at the lipid-water interface in micelle-bound bacteriophage M13 major coat protein. Biochemistry. 39:16155-16162.