Review: Conformation and folding of novel beta-structural elements in viral fiber proteins: The triple beta-spiral and triple beta-helix

Journal of Structural Biology

Volumn 137, Issue 1-2, 2002, Pages 236-247

  Mitraki, Anna ^a   Miller, Stefan ^b,c   Van Raaij, Mark J ^d  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b PROFOS AG   (Germany)

^c UNIVERSITY OF REGENSBURG   (Germany)

^d LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Beta structure; Fibrous proteins; Protein folding; Protein structure; Virus and bacteriophage fibers

Indexed keywords

VIRUS PROTEIN;

ALPHA HELIX; BACTERIOPHAGE; CONFERENCE PAPER; CONFORMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; TRIPLE HELIX;

EID: 0036446878     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.2002.4447     Document Type: Conference Paper

References (79)

1. Bassel-Duby, R., Jayasuriya, A., Chatterjee, D., Sonenberg, N., Maizel, J. V., Jr., and Fields, B. N. (1985) Sequence of reovirus haemagglutinin predicts a coiled-coil structure. Nature 315, 421-423.
2. Baxa, U., Steinbacher, S., Weintraub, A., Huber, R., and Seckler, R. (1999) Mutations improving the folding of phage P22 tail-spike protein affect its receptor binding activity. J. Mol. Biol. 293, 693-701.
3. Belnap, D. M., and Steven, A. C. (2000) "Déjà vu all over again": The similar structures of bacteriophage PRD1 and adenovirus. Trends Microbiol. 8, 91-93.
4. Benson, S. D., Bamford, J. K., Bamford, D. H., and Burnett, R. M. (1999) Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98, 825-833.
5. Betts, S., and King, J. (1999) There's a right way and a wrong way: In vivo and in vitro folding, misfolding and subunit assembly of the P22 tailspike. Structure Fold. Des. 7, R131-139.
6. Bewley, M. C., Springer, K., Zhang, Y.-B., Freimuth, P., and Flanagan, J. M. (1999) Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science 286, 1579-1583.
7. Blake, C., and Serpell, L. (1996) Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous beta-sheet helix. Structure 4, 989 -998.
8. Burda, M. R., and Miller, S. (1999) Folding of coliphage T4 short tail fiber in vitro. Analysing the role of a bacteriophage-encoded chaperone. Eur. J. Biochem. 265, 771-778.
9. Burda, M. R., Hindennach, I., and Miller, S. (2000) Stability of bacteriophage T4 short tail fiber. Biol. Chem. 381, 255-258.
10. Caldentey, J., Tuma, R., and Bamford, D. H. (2000) Assembly of bacteriophage PRD1 spike complex: Role of the multidomain protein P5. Biochemistry 39, 10566-10573.
11. Cerritelli, M. E., Wall, J. S., Simon, M. N., Conway, J. F., and Steven, A. C. (1996) Stoichiometry and domainal organization of the long tail-fiber of bacteriophage T4: A hinged viral adhesin. J. Mol. Biol. 260, 767-780.
12. Chappell, J. D., Prota, A. E., Dermody, T. S., and Stehle, T. (2002) Crystal structure of reovirus attachment protein sigmal reveals evolutionary relationship to adenovirus fiber. EMBO J. 21, 1-11.
13. Chen, B., and King, J. (1991) Thermal unfolding pathway for the thermostable P22 tailspike endorhamnosidase. Biochemistry 30, 6260-6269.
14. Coffey, M. C., Strong, J. E., Forsyth, P. A., and Lee, P. W. (1998) Reovirus therapy of tumors with activated Ras pathway. Science 282, 1332-1334.
15. Crowther, R. A., Lenk, E. V., Kikuchi, Y., and King, J. (1977) Molecular reorganization in the hexagon to star transition of the baseplate of bacteriophage T4. J. Mol. Biol. 116, 489-523.
16. Durmort, C., Stehlin, C., Schoehn, G., Mitraki, A., Drouet, E., Cusack, S., and Burmeister, W. P. (2001) Structure of the fiber head of Ad3, a non-CAR-binding serotype of adenovirus. Virology 285, 302-312.
17. Engel, J., and Prockop, D. J. (1991) The zipper-like folding of collagen triple helices and the effects of mutations that disrupt the zipper. Annu. Rev. Biophys. Biophys. Chem. 20, 137-152.
18. Fraser, R. D. B., Furlong, D. B., Trus, B. L., Nibert, M. L., Fields, B. N., and Steven, A. C. (1990) Molecular structure of the cell-attachment protein of reovirus: Correlation of computer-processed electron micrographs with sequence-based predictions. J. Virol. 64, 2990-3000.
19. Fuchs, A., Seiderer, C., and Seckler, R. (1991) In vitro folding pathway of phage P22 tailspike protein. Biochemistry 30, 6598-6604.
20. Georgopoulos, C. P., and Linder, C. H. (1994) Molecular chaperones in T4 assembly. In J. D. Karam et al. (Eds.), Molecular Biology of Bacteriophage T4, pp. 213-217, Am. Soc. Microbiol. Press, Washington, DC.
21. Gilmore, R., Coffey, M. C., and Lee, P. W. K. (1998) Active participation of Hsp90 in the biogenesis of the trimeric reovirus cell attachment protein sigma1. J. Biol. Chem. 273, 15227-15233.
22. Green, N. M., Wrigley, N. G., Russel, W. C., Martin, S. R., and McLachlan, A. D. (1983) Evidence for a repeating cross-beta sheet structure in the adenovirus fiber. EMBO J. 2, 1357-1365.
23. Hashemolhosseini, S., Stierhof, Y. D., Hindennach, I., and Henning, U. (1996) Characterization of the helper proteins for the assembly of tail fibers of coliphages T4 and lambda. J. Bacteriol. 178, 6258-6265.
24. Henry, L. J., Xia, D., Wilke, M. E., Deisenhofer, J., and Gerard, R. D. (1994) Characterization of the knob domain of the adenovirus type 5 fiber protein expressed in Escherichia coli. J. Virol. 68, 5239-5246.
25. Hitt, M. M., and Graham, F. L. (2000) Adenovirus vectors for human gene therapy. Adv. Virus Res. 55, 479-505.
26. Hong, J. S., and Engler, J. A. (1991) The amino terminus of the adenovirus fiber protein encodes the nuclear localization signal. Virology 185, 758-767.
27. Hong, J. S., and Engler, J. A. (1996) Domains required for assembly of adenovirus type 2 fiber trimers. J. Virol. 70, 7071-7078.
28. Horwitz, M. S. (1996) Adenoviruses. In Fields, B. N., Knipe, D. M., and Howley, P. M. (Eds.), Virology, pp. 2149-2171, Lippincott-Raven, Philadelphia.
29. Hu, J., Toft, D. O., and Seeger, C. (1997) Hepadnavirus assembly and reverse transcription require a multi-component chaperone complex which is incorporated into nucleocapsids. EMBO J. 16, 59-68.
30. Hunt, J. F., van der Vies, S. M., Henry, L., and Deisenhofer, J. (1997) Structural adaptations in the specialized bacteriophage T4 co-chaperonin Gp31 expand the size of the Anfinsen cage. Cell 90, 361-371.
31. Iwashita, S., and Kanegasaki, S. (1976) Enzymic and molecular properties of baseplate parts of bacteriophage P22. Eur. J. Biochem. 65, 87-94.
32. Jayaraman, A., De Bernardez Clark, E., and Goldberg, E. (1997) Thermal unfolding of bacteriophage T4 short tail fibers. Biotechnol. Prog. 13, 837-843.
33. Jones, E. Y., Stuart, D. I., and Walker, N. P. (1989) Structure of tumor necrosis factor. Nature 338, 225-228.
34. Kanamaru, S., Leiman, P. G., Kostyuchenko, V. A., Chipman, P. R., Mesyanzhinov, V. V., Arisaka, F., and Rossmann, M. R. (2002) The structure of the bacteriophage T4 cell-puncturing device. Nature 415, 553-557.
35. Kato, H., Fujisawa, H., and Minagawa, T. (1985) Genetic analysis of subunit assembly of the tail fiber of bacteriophage T3. Virology 146, 12-21.
36. Kells, S. S., and Haselkorn, R. (1974) Bacteriophage T4 short tail fibers are the product of gene 12. J. Mol. Biol. 83, 473-485.
37. King, J., and Casjens, S. (1974) Catalytic head assembling protein in virus morphogenesis. Nature 251, 112-119.
38. King, J., and Laemmli, U. K. (1971) Polypeptides of the tail fibers of bacteriophage T4. J. Mol. Biol. 62, 465-477.
39. Krasnykh, V., Belousova, N., Korokhov, N., Mikheeva, G., and Curiel, D. T. (2001) Genetic targeting of an adenovirus vector via replacement of the fiber protein with the phage T4 fibritin. J. Virol. 75, 4176-4183.
40. Kreisberg, J. F., Betts, S. D., and King, J. (2000) Beta-helix core packing within the triple-stranded oligomerization domain of the P22 tailspike. Protein Sci. 9, 2338 -2343.
41. Lee, P. W. K., and Gilmore, R. (1998) Reovirus cell attachment protein sigma1: Structure-function relationships and biogenesis. Curr. Top. Microbiol. Immunol. 233, 137-153.
42. Leiman, P. G., Kostyuchenko, V. A., Shneider, M. M., Kurochkina, L. P., Mesyanzhinov, V. V., and Rossmann, M. G. (2000) Structure of bacteriophage T4 gene product 11, the interface between the baseplate and short tail fibers. J. Mol. Biol. 301, 975-985.
43. Letarov, A. V., Londer, Y. Y., Boudko, S. P., and Mesyanzhinov, V. V. (1999) The carboxy-terminal domain initiates trimerization of bacteriophage T4 fibritin. Biochemistry 64, 817-823.
44. Louis, N., Fender, P., Barge, A., Kitts, P., and Chroboczek, J. (1994) Cell-binding domain of adenovirus serotype 2 fiber. J. Virol. 68, 4104-4106.
45. Luckey, M., Hernandez, J., Arlaud, G., Forsyth, V. T., Ruigrok, R. W., and Mitraki, A. (2000) A peptide from the adenovirus fiber shaft forms amyloid-type fibrils. FEBS Lett. 468, 23-27.
46. Macejak, D. G., and Luftig, R. B. (1991) Association of HSP70 with the adenovirus type 5 fiber protein in infected HEp-2 cells. Virology 180, 120-125.
47. Makhov, A. M., Trus, B. L., Conway, J. F., Simon, M. N., Zurabishvili, T. G., Mesyanzhinov, V. V., and Steven, A. C. (1993) The short tail-fiber of bacteriophage T4: Molecular structure and a mechanism for its conformational transition. Virology 194, 117-127.
48. Mason, W. S., and Haselkorn, R. (1972) Product of T4 gene 12. J. Mol. Biol. 66, 445-469.
49. Mathews, C. K. (1994) An overview of the T4 developmental program. In J. D. Karam et al. (Eds.), Molecular Biology of Bacteriophage T4, pp. 1-8, Am. Soc. Microbiol. Press, Washington, DC.
50. McLaughlin, S. H., and Bulleid, N. J. (1998) Molecular recognition in procollagen chain assembly. Matrix Biol. 16, 369-377.
51. Miller, S., Schuler, B., and Seckler, R. (1998) Phage P22 tailspike protein: Removal of head-binding domain unmasks effects of folding mutations on native-state thermal stability. Protein Sci. 7, 2223-2232.
52. Miroshnikov, K. A., Marusich, E. I., Cerritelli, M. E., Cheng, N., Hyde, C. C., Steven, A. C., and Mesyanzhinov, V. V. (1998) Engineering trimeric fibrous proteins based on bacteriophage T4 adhesins. Protein Eng. 11, 329-332.
53. Mitraki, A., Barge, A., Chroboczek, J., Andrieu, J. P., Gagnon, J., and Ruigrok, R. W. H. (1999) Unfolding studies of human adenovirus type 2 fiber trimers. Evidence for a stable domain. Eur. J. Biochem. 264, 599-606.
54. Mitraki, A., Fane, B., Haase-Pettingell, C., Sturtevant, J., and King, J. (1991) Global suppression of protein folding defects and inclusion body formation. Science 253, 54-58.
55. Nibert, M. L., Schiff, L. A., and Fields, B. N. (1996) Reoviruses and their replication. In Fields, B. N., Knipe, D. M., and Howley, P. M. (Eds.), Virology, pp. 1557-1596, Lippincott-Raven, Philadelphia.
56. Novelli, A., and Boulanger, P. A. (1991a) Deletion analysis of functional domains in baculovirus-expressed adenovirus type 2 fiber. Virology 185, 365-376.
57. Novelli, A., and Boulanger, P. A. (1991b) Assembly of adenovirus type 2 fiber synthesized in cell-free translation system. J. Biol. Chem. 266, 9299-9303.
58. Philipson, L., Lonberg-Holm, K., and Petterson, U. (1986) Virus-receptor interaction in an adenovirus system. J. Virol. 2, 1064-1075.
59. Raetz, C. R., and Roderick, S. L. (1995) A left-handed parallel beta helix in the structure of UDP-N-acetylglucosamine acyl-transferase. Science 270, 997-1000.
60. Riede, I. (1987) Receptor specificity of the short tail fibers (gp12) of T-even type Escherichia coli phages. Mol. Gen. Genet. 206, 110-115.
61. Ruigrok, R. W. H., Barge, A., Albiges-Rizo, C., and Dayan, S. (1990) Structure of adenovirus fiber. II. Morphology of single fibers. J. Mol. Biol. 215, 589-596.
62. Seckler, R. (1998) Folding and function of repetitive structure in the homotrimeric phage P22 tailspike protein. J. Struct. Biol. 122, 216-222.
63. Selivanov, N. A., Ben'yaminov, S. Y., Golitsina, N. L., Nikolaeva, L. I., and Mesyanzhinov, V. V. (1987) Structure and regulation of the assembly of bacteriophage T4 fibrillar proteins. I. Isolation and spectral properties of long fibers. Mol. Biol. 21, 1258-1267.
64. Sokolova, A., Malfois, M., Caldentey, J., Svergun, D. I., Koch, M. H. J., Bamford, D. H., and Tuma, R. (2001) Solution structure of bacteriophage PRD1 vertex complex. J. Biol. Chem. 276, 46187-46195.
65. Steinbacher, S., Seckler, R., Miller, S., Steipe, B., Huber, R., and Reinemer, P. (1994) Crystal structure of P22 tailspike protein: Interdigitated subunits in a thermostable trimer. Science 265, 383-386.
66. Stewart, P. L., Burnett, R. M., Cyrklaff, M., and Fuller, S. D. (1991) Image reconstruction reveals the complex molecular organization of adenovirus. Cell 67, 145-154.
67. Stouten, P. F., Sander, C., Ruigrok, R. W. H., and Cusack, S. (1992) New triple-helical model for the shaft of the adenovirus fiber. J. Mol. Biol. 226, 1073-1084.
68. Tao, Y., Strelkov, S. V., Mesyanzhinov, V. V., and Rossmann, M. G. (1997) Structure of bacteriophage T4 fibritin: A segmented coiled coil and the role of the C-terminal domain. Structure 5, 789-798.
69. Tyler, K. L., and Fields, B. N. (1996) Reoviruses. In Fields, B. N., Knipe, D. M., and Howley, P. M. (Eds.), Virology, pp. 1597-1623, Lippincott-Raven, Philadelphia.
70. van der Vies, S. M., Gatenby, A. A., and Georgopoulos, C. (1994) Bacteriophage T4 encodes a co-chaperonin that can substitute for Escherichia coli GroES in protein folding. Nature 368, 654-656.
71. van Raaij, M. J., Louis, N., Chroboczek, C., and Cusack, S. (1999a) Structure of the human adenovirus serotype 2 fiber head domain at 1.5 Å resolution. Virology 262, 333-343.
72. van Raaij, M. J., Mitraki, A., Lavigne, G., and Cusack, S. (1999b) A triple beta-spiral in the adenovirus fiber shaft reveals a new structural motif for a fibrous protein. Nature 401, 935-938.
73. van Raaij, M. J., Schoehn, G., Jaquinod, M., Ashman, K., Burda, M. R., and Miller, S. (2001a) Identification and crystallisation of a heat- and protease-stable fragment of the bacteriophage T4 short tail fiber. Biol. Chem. 382, 1049-1055.
74. van Raaij, M. J., Schoehn, G., Burda, M. R., and Miller, S. (2001b) Crystal structure of a heat- and protease-stable part of the bacteriophage T4 short tail fiber. J. Mol. Biol. 314, 1137-1146.
75. Ward, S., and Dickson, R. C. (1971) Assembly of bacteriophage T4 tail fibers. 3. Genetic control of the major tail fiber polypeptides. J. Mol. Biol. 62, 479-492.
76. Wickham, T. J., Mathias, P., Cheresh, D. A., and Nemerow, G. R. (1993) Integrins αvβ3 and αvβ5 promote adenovirus internalization but not virus attachment. Cell 73, 309-319.
77. Xia, D., Henry, L. J., Gerard, R. D., and Deisenhofer, J. (1994) Crystal structure of the receptor-binding domain of adenovirus type 5 fiber protein at 1.5 Å resolution. Structure 2, 1259-1270.
78. Yeung, M. C., Gill, M. J., Alibhai, S. S., Shahrabadi, M. S., and Lee, P. W. (1987) Purification and characterization of the reovirus cell attachment protein sigma 1. Virology 156, 377-385.
79. Yoder, M. D., Keen, N. T., and Jurnak, F. (1993) New domain motif: The structure of pectate lyase C, a secreted plant virulence factor. Science 260, 1503-1507.