Insights into specificity of cleavage and mechanism of cell entry from the crystal structure of the highly specific Aspergillus ribotoxin, restrictocin

Structure

Volumn 4, Issue 7, 1996, Pages 837-852

  Yang, Xiaojing ^a,b   Moffat, Keith ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

cell entry activity; Laue diffraction; protein RNA specific recognition; ribotoxins; SIRAS

Indexed keywords

ASPERGILLUS; ASPERGILLUS RESTRICTUS; EUKARYOTA; FUNGI;

EID: 0030586029     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(96)00090-1     Document Type: Article

References (67)

1. Schindler, D.G. & Davies, J. (1977). Specific cleavage of ribosomal RNA caused by alpha sarcin. Nucleic Acids Res. 4, 1097-1110.
2. Roga, V., Hedeman, L.P. & Olson, B.H. (1971). Evaluation of mitogillin (NSC-69529) in the treatment of naturally occurring canine neoplasms. Cancer Chemother. 55, 101-113.
3. Gavilanes, J., Vazquez, D., Soriano, F. & Mendez, E. (1983). Chemical and spectroscopic evidence on the homology of three antitumor proteins: α-sarcin, mitogillin and restrictocin. J. Protein Chem. 2, 251-261.
4. Rodriguez, R., Lopez-Otin, C., Barber, D., Fernandez-Luna, J.L., Gonzalez, G. & Mendez, E. (1982). Amino acid sequence homologies in α-sarcin, restrictocin and mitogillin. Biochim. Biophys. Res. Commn. 108, 315-321.
5. Chan, Y.L., Endo, Y. & Wool, I.G. (1983). The sequence of the nucleotides at the α-sarcin cleavage site in rat 28S ribosomal ribonucleic acid. J. Biol. Chem. 258, 12768-12770.
6. Furutani, M., Kashiwagi, K., Ito, K., Endo, Y. & Igarashi, K. (1992). Comparison of the modes of action of a vero toxin (a Shiga-like toxin) from Escherichia coli, of ricin, and of α-sarcin. Arch. Biochem. Biophys. 293, 140-146.
7. Lin, A., Chen, C.K. & Chen, Y.J. (1991). Molecular action of tricholin, a ribosome-inactivating protein isolated from Trichoderma viride. Mol. Microbiol. 5, 3007-3013.
8. Endo, Y., Glück, A. & Wool, I. (1991). Ribosomal RNA identity elements for ricin A-chain recognition and catalysis. J. Mol. Biol. 221, 193-207.
9. Brigotti, M., Rambelli, F., Zamboni, M. & Montanaro, L. (1989). Effect of α-sarcin and ribosome-inactivating proteins on the interaction of elongation factors with ribosomes. Biochem. J. 257, 723-727.
10. Moazed, D., Robertson, J.M. & Noller, H.F. (1988). Interaction of elongation factors EF-Tu with a conserved loop in 23S RNA. Nature 334, 362-364.
11. Cundliffe, E., Cannon, M. & Davies, J. (1974). Mechanism of inhibition of eukaryotic protein synthesis by trichothecene fungal toxins. Proc. Natl. Acad. Sci. USA 71, 30-34.
12. Lamy, B., Davies, J. & Schindler, D. (1992). The Aspergillus ribonucleolytic toxins (ribotoxins). In Genetically Engineered Toxins. (Frankel, A.E., ed), pp. 237-258, Marcel Dekker, Inc., NY.
13. Endo, Y. & Wool, I.G. (1982). The site of action of α-sarcin on eukaryotic ribosomes. J. Biol. Chem. 257, 9054-9060.
14. Wool, I.G. (1984). The mechanism of action of the cytotoxic nuclease α-sarcin and its use to analyse ribosome structure. Trends Biochem. Sci. 9, 14-17.
15. Endo, Y., Chan, Y.L., Lin, A., Tsurugi, K. & Wool, I.G. (1988). The cytotoxins α-sarcin and ricin retain their specificity when tested on a synthetic oligoribonucleotide (35-mer) that mimics a region of 28S ribosomal ribonucleic acid. J. Biol. Chem. 263, 7917-7920.
16. Endo, Y., Glück, A., Chan, Y.L., Tsurugi, K. & Wool, I.G. (1990). RNA-protein interaction: an analysis with RNA oligonucleotides of the recognition by α-sarcin of a ribosomal domain for function. J. Biol. Chem. 265, 2216-2222.
17. Glück, A. & Wool, I. (1996). Determination of the 28S ribosomal RNA identity element (G4319) for alpha-sarcin and the relationship of recognition to the selection of the catalytic site. J. Mol. Biol. 256, 838-848.
18. Choe, S., et al., & Eisenberg, D. (1992). The crystal structure of diphtheria toxin. Nature 357, 216-222.
19. Sixma, T., Pronk, S., Kalk, K., Zanten, B., Berghuls, A. & Hol, W. (1992). Lactose binding to heat-labile enterotoxin revealed by X-ray crystallography. Nature 355, 561-564.
20. Olsnes, S. & Pihl, A. (1982). Toxic lectins and related proteins. In Molecular Action of Toxins and Viruses. (Cohen, P. & van Heyningen, S., eds), pp. 51-105, Elsevier Biomedical Press, Amsterdam.
21. Munoz, A., Castrillo, J.L. & Carrasco, L. (1985). Modification of membrane permeability during Semliki Forest virus infection. Virology 146, 203-212.
22. Otero, M. J. & Carrasco, L. (1985). Proteins are cointernalized with virion particles during early infection. Virology 160, 75-80.
23. Turnay, J., Olmo, N., Jimenez, A., Lizarbe, M. & Gavilanes, J. (1993). Kinetic study of the cytotoxic effect of α-sarcin, a ribosome inactivating protein from Aspergillus giganteus, on tumor cell lines: protein biosynthesis inhibition and cell binding. Mol. Cell. Biochem. 122, 39-47.
24. Otero, M.J. & Carrasco, L. (1988). Exogenous phospholipase C permeabilizes mammalian cells to proteins. Exp. Cell Res. 177, 154-161.
25. Gasset, M., Oñaderra, M., Thomas, P.G. & Gavilanes, J.G. (1990). Fusion of phospholipid vesicles produced by the anti-tumor protein α-sarcin. Biochem. J. 265, 815-822.
26. Gasset, M., Oñaderra, M., Goormaghtigh, E. & Gavilanes, J.G. (1991). Acid phospholipid vesicles produce conformational changes on the antitumor protein α-sarcin. Biochim. Biophys. Acta 1080, 51-58.
27. Oñaderra, M., Mancheno, J.M., Gasset, M., Lacadena, J. & Schiavo, G. (1993). Translocation of α-sarcin across the lipid bilayer of asolectin vesicles. Biochem. J. 295, 221-225.
28. Brandhorst, T., Dowd, P.F. & Kenealy, W. (1996). The ribosome-inactivating protein restrictocin deters insect feeding in Aspergillus restrictus. Microbiology 142, in press.
29. Lamy, L., Moutaouakil, M., Latge, J.P. & Davies, J. (1991). Secretion of a potential virulence factor, a fungal ribonucleotoxin, during human aspergillosis infections. Mol. Microbiol. 5, 1811-1815.
30. Arruda, L.K., Mann, B.J. & Chapman, M.D. (1992). Selective expression of a major allergen and cytotoxin, aspf I, in Aspergillus fumigatus. J. Immunol. 149, 3354-3359.
31. Brünger, A.T. (1993). X-PLOR Manual Version 3.1: A System for X-ray Crystallography and NMR. Yale University, New Haven, CT.
32. Hill, C., et al., & Pavlovsky, S. (1983). The structural and sequence homology of a family of microbial ribonucleases. Trends Biochem. Sci. 8, 364-369.
33. Heinemann, U. & Saenger, W. (1982). Specific protein-nucleic acid recognition in ribonuclease T1-2'-guanylic acid complex: an X-ray study. Nature 299, 27-31.
34. Gohda, K., Oka, K., Tomita, K. & Hakoshima, T. (1994). Crystal structure of Rnase T1 complexed with the product nucleotide 3'GMP. J. Biol. Chem. 269, 17531-17536.
35. Martinez-Oyanedel, J., Choe, H.W., Heinemann, U. & Saenger, W. (1991). Ribonuclease T1 with free recognition and catalytic site: crystal structure analysis at 1.5 Å resolution. J. Mol. Biol. 222, 335-352.
36. Sevcik, J., Dodson, E. & Dodson, G. (1991). Determination and restrained least-squares refinement of the structures of ribonuclease Sa and its complex with 3'-guanylic acid at 1.8 A resolution. Acta Cryst. B 47, 240-253.
37. Mauguen, Y., et al., & Jack, A. (1982). Molecular structure of a new family of ribonucleases. Nature 297, 162-164.
38. Zegers, I., Verhelst, P., Choe, H.W., Heinemann, U., Saenger, W. & Wyns, L. (1992). Role of Histidine-40 in ribonuclease T1 catalysis: three-dimensional structures of the partially active His40Lys mutant. Biochemistry 31, 11317-11325.
39. Noguchi, S., Satow, Y., Uchida, T., Sasaki, C. & Matsuzaki, T. (1995). Crystal structure of Ustilago sphaerogena ribonuclease U2 at 1.8 Å resolution. Biochemistry 3, 15583-15591.
40. Yang, R. & Kenealy, W. (1992). Effects of amino-terminal extensions and specific mutations on the activity of restrictocin. J. Biol. Chem. 267, 16801-16805.
41. Nishikawa, S., et al., & Ikehara, M. (1987). Two histidines are essential for ribonuclease T1 activity as is the case for ribonuclease A. Biochemistry 26, 8620-8624.
42. Campbell, R. & Petsko, G. (1987). Ribonuclease structure and catalysis: crystal structure of sulfate-free native ribonuclease A at 1.5 Å resolution. Biochemistry 26, 8579-8584.
43. Steyaert, J., Hallenga, K., Wyns, L. & Stanssens, P. (1990). Histidine-40 of ribonuclease T1 acts as base catalyst when the true catalytic base, glutamic acid-58, is replaced by alanine. Biochemistry 29, 9064-9072.
44. Ding, J., Koellner, G., Grunert, H.P. & Saenger, W. (1991). Crystal structure of ribonuclease T1 complexed with adenosine 2'-monophosphate at 1.8 Å resolution. J. Biol. Chem. 266, 15128-15134.
45. Kostrewa, D., Choe, H.W., Heinemann, U. & Saenger, W. (1989). Crystal structure of guanosine-free ribonuclease T1 complexed with vanadate (V) suggests conformational change upon substrate binding. Biochemistry 28, 7592-7600.
46. Szewczak, A., Moore, P., Chan, Y.L. & Wool, I.G. (1993). The conformation of the sarcin/ricin loop from 28S ribosomal RNA, Proc. Natl. Acad. Sci. USA 90, 9581-9585.
47. Montfort, W., et al., & Robertus, J. (1987). The three-dimensional structure of ricin at 2.8 A. J. Biol. Chem. 262, 5398-5403.
48. Rutenber, E., Ready, M. & Robertus, J. (1987). Structure and evolution of ricin B chain. Nature 326, 624-626.
49. Rutenber, E. & Robertus, J. (1991). Structure of ricin B-chain at 2.5 A resolution. Proteins- Struct. Funct. and Genet. 10, 260-269.
50. Weis, W., Kahn, R., Fourme, R., Drickamer, K. & Hendrickson, W. (1991). Structure of the calcium-dependent lectin domain from a rat mannose-binding protein determined by MAD phasing. Science 254, 1608-1615.
51. Rini, J., Hardman, K., Einspahr, H., Suddath, F. & Carver, J. (1993). X-ray crystal structure of a pea lectin-trimannoside complex at 2.6 Å resolution. J. Biol. Chem. 268, 10126-10132.
52. Banerjee, R., et al., & Vijayan, M. (1994). Crystal structure of peanut lectin, a protein with an unusual quaternary structure. Proc. Natl. Acad. Sci. USA 91, 227-231.
53. Weis, W. (1994). Lectins on a roll: the structure of E-selectin. Structure 2, 147-150.
54. Bajorath, J. & Aruffo, A. (1994). Molecular model of the extracellular lectin-like domain in CD69. J. Biol. Chem. 269, 32457-32463.
55. Hollenbaugh, D., Bajorath, J., Stenkamp, R. & Aruffo, A. (1993). Interactions of P-selectin (CD62) and its cellular ligand: analysis of critical residues. Biochemistry 32, 2960-2966.
56. Martinez, S. & Smith, J. (1991). Crystallization and preliminary characterization of mitogillin, a ribosomal ribonuclease from Aspergillus restrictus. J. Mol. Biol. 218, 489-492.
57. Getzoff, E.D., et al., & Westbrook, E.M. (1993). Laue diffraction protein crystallography at the National Synchrotron Light Source. Nucl. Instrum. Meth. Phys. Res. B 79, 249-55.
58. Ren, Z. & Moffat, K. (1995). Quantitative analysis of synchrotron Laue diffraction patterns in macromolecular crystallography. J. Appl. Cryst. 28, 461-481.
59. Ren, Z. & Moffat, K. (1995). Deconvolution of energy overlaps in Laue diffraction, J. Appl. Cryst. 28, 482-493.
60. Ren, Z. & Moffat, K. (1994). Laue crystallography for studying rapid reactions. J. Synchrotron Rad. 1, 78-82.
61. McRee, D.E. (1992). A visual protein crystallographic software system for X11/XView. J. Mol. Graph. 10, 44-46.
62. Collaborative Computational Project, Number 4. (1994). The CCP4 suite: programs for protein crystallography. Acta Cryst. D 50, 760-763.
63. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check the stereochemistry of protein structures. J. Appl. Cryst. 26, 283-291.
64. Jones, T.A., Zhou, J.Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A 47, 110-119.
65. Nicholls, A., Sharp, K.A. & Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons, Proteins- Struct. Funct. Genet. 11, 281-296.
66. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
67. Evans, S.V. (1993). SETOR: hardware lighted three-dimensional solid model representation of macromolecules. J. Mol. Graph. 11, 134-138.