Crystal structure of a four-layer aggregate of engineered TMV CP implies the importance of terminal residues for oligomer assembly

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Li, Xiangyang ^a   Song, Baoan ^a   Chen, Xi ^a   Wang, Zhenchao ^a   Zeng, Mengjiao ^b   Yu, Dandan ^a   Hu, Deyu ^a   Chen, Zhuo ^a   Jin, Linhong ^a   Yang, Song ^a   Yang, Caiguang ^c   Chen, Baoen ^c  

^a GUIZHOU UNIVERSITY   (China)

^b SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

^c SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; ARGININE; ASPARTIC ACID; CARBOXY TERMINAL TELOPEPTIDE; COAT PROTEIN; GLUTAMINE; HYDROGEN; N HIS TOBACCO MOSAIC VIRUS COAT PROTEIN 19; OLIGOMER; POLYHISTIDINE TAG; RNA; THREONINE; TOBACCO MOSAIC VIRUS COAT PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMICAL BINDING; COMPARATIVE STUDY; CRYSTAL STRUCTURE; HANGING DROP VAPOR DIFFUSION METHOD; NONHUMAN; OLIGOMERIZATION; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; TOBACCO MOSAIC VIRUS; TRANSGENIC ORGANISM; VIRUS PARTICLE;

CAPSID PROTEINS; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; PROTEIN ENGINEERING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; STRUCTURAL HOMOLOGY, PROTEIN; TOBACCO MOSAIC VIRUS;

EID: 84892388612     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077717     Document Type: Article

References (51)

1. Stubbs G, Kendall A (2012) Helical viruses. Adv Exp Med Biol 726: 631-58.
2. Bloomer AC, Butler PJG (1986) Tobacco mosaic virus structure and self-assembly: The plant viruses. In: Regenmortel MHV, Fraenkel-Conrat H. editors. New York: Plenum Press. 19-57.
3. Mandelkow E, Holmes KC, Gallawitz U (1976) A new helical aggregate of tobacco mosaic virus protein. J Mol Biol 102: 265-285.
4. Jonathan P, Butler G, Durham AC (1977) Tobacco mosaic virus protein aggregation and the virus assembly. Adv Protein Chem 31: 188-251.
5. Mandelkow E, Stubbs G, Warren S (1981) Structures of the helical aggregates of tobacco mosaic virus protein. J Mol Biol 152: 375-386.
6. Butler PJG (1984) The current picture of the structure and assembly of tobacco mosaic virus. J Gen Virol 65: 253-279.
7. Caspar DLD, Namba K (1990) Switching in the self-assembly of tobacco mosaic virus. Adv Biophys 26: 157-185.
8. Okada Y (1986) Molecular assembly of tobacco mosaic virus in vitro. Advances in Biophysics 22: 95-145.
9. Schuster TM, Scheele RB, Adams ML, Shire SJ, Steckert JJ, et al. (1980) Studies on the mechanism of assembly of tobacco mosaic virus. Biophys J 10: 313-317.
10. Kegel WK, Schoot P (2006) Physical regulation of the self-assembly of tobacco mosaic virus coat protein. Biophys J 91: 1501-1512.
11. Bloomer AC, Champness JN, Bricogne G, Stoden R, Klug A (1978) Protein disk of tobacco mosaic virus at 2.8 Å resolution showing the interaction within and between subunits. Nature 276: 362-368.
12. Bhyravbhatla B, Stanley JW, Caspar DLD (1998) Refined atomic model of the four-layer aggregate of the tobacco mosaic virus coat protein at 2.4 Å resolution. Biophys J 74: 604-615.
13. Namba K, Pattanegek R, Stubbs G (1989) Visualization of protein RNA interaction in a virus: Refined structure of TMV at 2.9 Å resolution by X-ray fiber diffraction. J Mol Biol 208: 307-325.
14. Sachse C, Chen JZ, Coureux PD, Stroupe ME, Fändrich M, et al. (2007) High-resolution electron microscopy of helical specimens: A fresh look at tobacco mosaic virus. J Mol Biol 371: 812-835.
15. 2 strain of tobacco mosaic virus refined at 3.5 Å resolution using x-ray fiber diffraction. J Mol Biol 228: 516-528.
16. Stubbs G, Warren S, Holmes K (1997) Structure of RNA and RNA binding site in tobacco mosaic virus from a 4 Å map calculated from X-ray fiber diagrams. Nature 267: 216-221.
17. Namba K, Stubbs G (1986) Structure of tobacco mosaic virus at 3.6 Å resolution: implications for assembly. Science 231: 1401-1406.
18. Clare DK, Orlova EV (2010) 4.6 Å cryo-EM reconstruction of tobacco mosaic virus from images recorded at 300 keV on a 4kx4k CCD camera. J Struct Biol 171: 303-308.
19. Ge P, Zhou ZH (2011) Hydrogen-bonding networks and RNA bases revealed by cryo electron microscopy suggest a triggering mechanism for calcium switches. Proc Natl Acad Sci USA 1008: 9637-9642.
20. Sperling R, Klug A (1975) States of aggregation of the Dahlemense strain of tobacco mosaic virus protein and their relation to crystal formation. J Mol Biol 96: 425-430.
21. Raghavendra K, Adams ML, Schuster TM (1985) Tobacco mosaic virus protein aggregates in solution: Structural comparison of 20S aggregates with those near conditions for disk crystallization. Biochemistry 24: 3298-3304.
22. Raghavendra K, Kelly JA, Khairallah L, Schuster TM (1988) Structure and function of disk aggregates of the coat protein of tobacco mosaic virus. Biochemistry 27: 7583-7588.
23. Bergfors TE (2009) Protein crystallization. La Jolla: International University Line. 95-108.
24. Li XY, Song BA, Hu DY, Chen X, Wang ZC, et al. (2012) The development and application of new crystallization method for tobacco mosaic virus coat protein. Virology J In press.
25. Luzzati V (1952) Traitement statistique des erreurs dans la determination des structures cristallines. Acta Crystallogr 5: 802-810.
26. Bruckman MA, Soto CM, McDowell H, Liu JL, Ratna BR, et al. (2011) Role of hexahistidine in directed nanoassemblies of tobacco mosaic virus coat protein. Nano Lett 5(3): 1606-1616.
27. Gooding GV, Hebert TT (1967) A simple technique for purification of tobacco mosaic virus in large quantities. Phytopathology 57(11): 1285.
28. Hebert TT (1963) Precipitation of plant viruses by polyethylene glycol. Phytopathology 53: 36.
29. Shire SJ, Steckert JJ, Schuster TM (1979) Mechanism of self assembly of tobacco mosaic virus protein. II. Characterization of the metastable polymerization nucleus and the initial stages of helix formation. J Mol Biol 127: 487-506.
30. Fraenkel-Conrat H, Singer B, Tsugita A (1961) Purification of viral RNA by means of bentonite. Virology 14: 54-58.
31. Wilcockson JRH (1974) The rapid isolation of plant virus RNAs using sodium perchlorate. J Gen Virol 23: 107-111.
32. Shire SJ, Steckert JJ, Adams ML, Schuster TM (1979) Kinetics and mechanism of tobacco mosaic virus assembly: Direct measurement of relative rates of incorporation of 4S and 20S protein. Proc Natl Acad Sci USA 76(6): 2745-2749.
33. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72: 248-254.
34. Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9: 255-262.
35. Castellanos-Serra LR, Fernandez-Patron C, Hardy E, Huerta V (1996) A procedure for protein elution from reverse-stained polyarcylamide gels applicable at the low picomole level: An alternative route to the preparation of low abundance proteins for microanalysis. Electrophoresis 17: 1564-1572.
36. Bruckman MA, Soto CM, McDowell H, Liu JL, Ratna BR, et al. (2011) Role of hexahistidine in directed nanoassemblies of tobacco mosaic virus coat protein. ACS Nano 5: 1606-1616.
37. Geiger FC, Eber FJ, Eiben S, Mueller A, Jeske H, et al. (2013) TMV nanorods with programmed longitudinal domains of differently addressable coat proteins. Nanoscale 5: 3808-3816.
38. Kadri A, Maiss E, Amsharov N, Bittner AM, Balci S, et al. (2011) Engineered Tobacco mosaic virus mutants with distinct physical characteristics in planta and enhanced metallization properties. Virus Res 157: 35-46.
39. Kadri A, Wege C, Jeske H (2013) In vivo self-assembly of TMV-like particles in yeast and bacteria for nanotechnological applications. J Virol Methods 189: 328-340.
40. Mueller A, Kadri A, Jeske H, Wege C (2010) In vitro assembly of Tobacco mosaic virus coat protein variants derived from fission yeast expression clones or plants. J Virol Methods 166: 77-85.
41. Mancini EJ, Tuma R (2012) Mechanism of RNA packaging motor. Adv Exp Med Biol 726: 609-629.
42. Kainov DE, Pirttimaa M, Tuma R, Butcher SJ, Thomas GJ Jr, et al. (2003) RNA packaging device of double-stranded RNA bacteriophages, possibly as simple as hexamer of P4 protein. J Biol Chem 278: 48084-48091.
43. Kainov DE, Lisal J, Bamford DH, Tuma R (2004) Packaging motor from double-stranded RNA bacteriophage phi12 acts as an obligatory passive conduit during transcription. Nucleic Acids Res 32: 3515-3521.
44. Dedeo MT, Duderstadt KE, Berger JM, Francis MB (2010) Nanoscale protein assemblies from a circular permutant of the tobacco mosaic virus. Nano Lett 10: 181-186.
45. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology 276: 307-326.
46. Collaborative Computational Project N (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
47. Read RJ (2001) Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr D Biol Crystallogr 57: 1373-1382.
48. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr, 60: 2126-2132.
49. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
50. DeLano WL (2002) The PyMOL Molecular Graphics System.
51. Kleywegt GJ, Brunger AT (1996) Checking your imagination: applications of the free R value. Structure 4: 897-904.