Mechanism of ribonuclease inhibition by ribonuclease inhibitor protein based on the crystal structure of its complex with ribonuclease A

Journal of Molecular Biology

Volumn 264, Issue 5, 1996, Pages 1028-1043

  Kobe, Bostjan ^a,b   Deisenhofer, Johann ^b  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Crystal structure; Interaction; Leucine rich repeats; Ribonuclease inhibitor; RNase A

Indexed keywords

DIMER; ESTERASE INHIBITOR; INHIBITOR PROTEIN; LEUCINE; RIBONUCLEASE A; SULFATE;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRICITY; ENZYME ACTIVE SITE; ENZYME INHIBITOR INTERACTION; HYDROGEN BOND; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE;

EID: 0030596012     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0694     Document Type: Article

References (89)

1. Acharya, K. R., Shapiro, R., Allen, S. C., Riordan, J. F. & Vallee, B. L. (1994). Crystal structure of human angiogenin reveals the structural basis for its functional divergence from ribonuclease. Proc. Natl Acad. Sci. USA, 91, 2915-2919.
2. Bernstein, F. C., Koetzle, K. F., Williams, G. J. B., Meyer, E. F., Jr, Brice, M. D., Rodgers, J. R., Kennard, O., Shimanouchi, T. & Tasumi, M. (1977). The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112, 535-542.
3. Birdsall, D. L. & McPherson, A. (1992). Crystal structure disposition of thymidilic acid tetramer in complex with ribonuclease A. J. Biol. Chem. 267, 22230-22236.
4. Blackburn, P. & Gavilanes, J. G. (1980). The role of lysine-41 of ribonuclease A in the interaction with RNase inhibitor from human placenta. J. Biol. Chem. 255, 10959-10965.
5. Blackburn, P. & Gavilanes, J. G. (1982). Identification of lysine residues in the binding domain of ribonuclease A for the RNase inhibitor from human placenta. J. Biol. Chem. 257, 316-321.
6. Blackburn, P. & Jailkhani, B. L. (1979). Ribonuclease inhibitor from human placenta: Interaction with derivatives of ribonuclease A. J. Biol. Chem. 254, 12488-12493.
7. Blackburn, P. & Moore, S. (1982). Pancreatic ribonuclease. In The Enzymes, vol. 15, pp. 317-433, Academic Press, Orlando, FA.
8. Blackburn, P., Wilson, G. & Moore, S. (1977). Ribonuclease inhibitor from human placenta. J. Biol. Chem. 252, 5904-5910.
9. Boix, E., Wu, Y., Vasandani, V. M., Saxena, S. K., Ardelt, W., Ladner, J. & Youle, R. J. (1996). Role of the N terminus in RNase A homologues: differences in catalytic activity, ribonuclease inhibitor interaction and cytotoxicity. J. Mol. Biol. 257, 992-1007.
10. Borkakoti, N. (1983). The active site of ribonuclease A from the crystallographic studies of ribonuclease-A-inhibitor complexes. Eur. J. Biochem. 132, 89-94.
11. Brünger, A. T. (1990). Extension of molecular replacement: A new search strategy base on Patterson correlation coefficient. Acta Crystallog. sect. A, 46, 46-57.
12. Brünger, A. T. (1992). X-PLOR Version 3.1. Yale University, New Haven, CT.
13. Brünger, A. T., Kuriyan, J. & Karplus, M. (1987). Crystallographic R-factor refinement by molecular dynamics. Science, 235, 458-460.
14. Buckle, A. M. & Fersht, A. R. (1994). Substrate binding in an RNase: structure of a barnase-tetranucleotide complex at 1.76-Å resolution. Biochemistry, 33, 1644-1653.
15. Buckle, A. M., Schreiber, G. & Fersht, A. R. (1994). Protein-protein recognition: crystal structural analysis of a barnase-barstar complex at 2.0-Å resolution. Biochemistry, 33, 8878-8889.
16. CCP4 (1994). The CCP4 suite: Programs for protein crystallography. Acta Crystallog. sect. D, 50, 760-763.
17. Campbell, I. D. & Bork, P. (1993). Epidermal growth factor-like modules. Curr. Opin. Struct. Biol. 3, 385-392.
18. Capasso, S., Giordano, F., Mattia, C. A., Mazzarella, L. & Zagari, A. (1983). Refinement of the structure of bovine seminal ribonuclease. Biopolymers, 22, 327-332.
19. Chothia, C. (1974). Hydrophobic bonding and accessible surface area in proteins. Nature, 248, 338-339.
20. Chothia, C. (1975). Structural invariants in protein folding. Nature, 254, 304-308.
21. Crawford, D., Haggerty, K. & Beutler, B. (1989). Multiple splice forms of ribonuclease-inhibitor mRNA differ in the 5′-untranslated region. Gene, 85, 525-531.
22. Fett, J. W., Strydom, D. J., Lobb, R. R., Alderman, E. M., Bethune, J. L., Riordan, J. F. & Vallee, B. L. (1985). Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry, 24, 5480-5486.
23. Fontecilla-Camps, J. C., De Llorens, R., Le Du, M. H. & Cuchillo, C. M. (1994). Crystal structure of ribonuclease A·d(ApTpApApG) complex. Direct evidence for extended substrate recognition. J. Biol. Chem. 269, 21526-21531.
24. Furie, B. & Furie, B. C. (1988). The molecular basis of blood coagulation. Cell, 53, 505-518.
25. Guillet, V., Lapthorn, A., Hartley, R. W. & Mauguen, Y. (1993). Recognition between a bacterial ribonuclease, barnase, and its natural inhibitor, barstar. Structure, 1, 165-176.
26. Harper, J. W. & Vallee, B. L. (1989). A covalent angiogenin/ribonuclease hybrid with a fourth disulfide bond generated by regional mutagenesis. Biochemistry, 28, 1875-1884.
27. Hartley, R. W. (1989). Barnase and barstar: two small proteins to fold and fit together. Trends Biochem. Sci. 14, 450-454.
28. Hill, C., Dodson, G., Heinemann, U., Saenger, W., Mitsui, Y., Nakamura, K., Borisov, S., Tischenko, G., Polyakov, G. & Pavlovsky, S. (1983). The structural and sequence homology of a family of microbial ribonucleases. Trends Biochem. Sci. 8, 364-369.
29. Hofsteenge, J., Kieffer, B., Matthies, R., Hemmings, B. A. & Stone, S. R. (1988). Amino acid sequence of the ribonuclease inhibitor from porcine liver reveals the presence of leucine-rich repeats. Biochemistry, 27, 8537-8544.
30. Hofsteenge, J., Matthies, R. & Stone, S. R. (1989). Primary structure of ribonuclease from porcine liver, a new member of ribonuclease superfamily. Biochemistry, 28, 9806-9813.
31. Hofsteenge, J., Servis, C. & Stone, S. R. (1991a). Studies on the interaction of ribonuclease inhibitor with pancreatic ribonuclease involving differential labeling of cysteinyl residues. J. Biol. Chem. 266, 24198-24204.
32. Hofsteenge, J., Vincentini, A. & Stone, S. R. (1991b). Purification and characterization of truncated ribonuclease inhibitor. Biochem. J. 275, 541-543.
33. Howlin, B., Moss, D. S. & Harris, G. W. (1989). Segmented anisotropic refinement of bovine ribonuclease A by the application of the rigid-body TLS model. Acta Crystallog. sect. A, 45, 851-861.
34. Huber, R. (1985). Experience with the application of Patterson search techniques. In Molecular Replacement, Proceedings of the Daresbury Study Weekend (Machin, P. A., ed.), pp. 58-61, Daresbury Laboratory, Daresbury.
35. Janin, J. (1995). Elusive affinities. Proteins: Struct. Funct. Genet. 21, 30-39.
36. Janin, J. & Chothia, C. (1990). The structure of protein-protein recognition sites. J. Biol. Chem. 265, 16027-16030.
37. Janin, J., Miller, S. & Chothia, C. (1988). Surface, subunit interfaces and interior of oligomeric proteins. J. Mol. Biol. 204, 155-164.
38. Jones, T. A., Bergdoll, M. & Kjeldgaard, M. (1990). O: a macromolecule modeling environment. In Crystallographic and Modeling Methods in Molecular Design (Bugg, C. E. & Ealick, S. E., eds), pp. 189-195, Springer-Verlag, New York.
39. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
40. Kartha, G., Bello, J. & Harker, D. (1967). Tertiary structure of ribonuclease. Nature, 213, 862-865.
41. Kawanomoto, M., Motojima, K., Sasaki, M., Hattori, H. & Goto, S. (1992). cDNA cloning and sequence of rat ribonuclease inhibitor, and tissue distribution of the mRNA. Biochim. Biophys. Acta, 1129, 335-338.
42. Kim, J.-S., Soucek, J., Matousek, J. & Raines, R. T. (1995). Structural basis for the biological activities of bovine seminal ribonuclease. J. Biol Chem. 270, 10525-10530.
43. Kleywegt, G. J. & Jones, T. A. (1994). Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallog. sect. D, 50, 178-185.
44. Kobe, B. (1994). Crystal structure of ribonuclease inhibitor, a protein with leucine-rich repeats. PhD dissertation, The University of Texas Southwestern Medical Center, Dallas, TX.
45. Kobe, B. & Deisenhofer, J. (1993a). Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature, 366, 751-756.
46. Kobe, B. & Deisenhofer, J. (1993b). Crystallization and preliminary X-ray analysis of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. J. Mol. Biol. 231, 137-140.
47. Kobe, B. & Deisenhofer, J. (1994). The leucine-rich repeat: a versatile binding motif. Trends Biochem. Sci. 19, 415-421.
48. Kobe, B. & Deisenhofer, J. (1995a). Proteins with leucine-rich repeats. Curr. Opin. Struct. Biol. 5, 409-416.
49. Kobe, B. & Deisenhofer, J. (1995b). A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature, 374, 183-186.
50. Kobe, B., Ma, Z. & Deisenhofer, J. (1994). Complex between bovine ribonuclease A and porcine ribonuclease inhibitor crystallizes in a similar unit cell as free ribonuclease inhibitor. J. Mol. Biol. 241, 288-291.
51. Kraulis, P. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
52. Laskowski, M., Jr & Kato, I. (1980). Protein inhibitors of proteinases. Annu. Rev. Biochem. 49, 593-626.
53. Lawrence, M. C. & Colman, P. M. (1993). Shape complementarity at protein/protein interfaces. J. Mol. Biol. 234, 946-950.
54. Lee, F. S. & Vallee, B. L. (1989). Binding of placental ribonuclease inhibitor to the active site of angiogenin. Biochemistry, 28, 3556-3561.
55. Lee, F. S. & Vallee, B. L. (1990a). Kinetic characterization of two active mutants of placental ribonuclease inhibitor that lack internal repeats. Biochemistry, 29, 6633-6638.
56. Lee, F. S. & Vallee, B. L. (1990b). Modular mutagenesis of human placental ribonuclease inhibitor, a protein with leucine-rich repeats. Proc. Natl Acad. Sci. USA, 87, 1879-1883.
57. Lee, F. S. & Vallee, B. L. (1993). Structure and action of mammalian ribonuclease (angiogenin) inhibitor. Prog. Nucl Acid Res. MoI. Biol. 44, 1-30.
58. Lee, F. S., Fox, E. A., Zhou, H.-M., Strydom, D. J. & Vallee, B. L. (1988). Primary structure of human placental ribonuclease inhibitor. Biochemistry, 27, 8545-8553.
59. Lee, F. S., AuId, D. S. & Vallee, B. L. (1989a). Tryptophan fluorescence as a probe of placental ribonuclease inhibitor binding to angiogenin. Biochemistry, 28, 219-224.
60. Lee, F. S., Shapiro, R. & Vallee, B. L. (1989b). Tight-binding inhibition of angiogenin and ribonuclease A by placental ribonuclease inhibitor. Biochemistry, 28, 225-230.
61. Luzzati, P. V. (1952). Traitements statistique des erreurs dans la détermination des structures cristallines. Acta Crystallog. 5, 802-810.
62. Miller, S., Janin, J., Lesk, A. M. & Chothia, C. (1987). Interior and surface of monomeric proteins. J. Mol. Biol. 196, 641-656.
63. Moroianu, J. & Riordan, J. F. (1994). Nuclear translocation of angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc. Natl Acad. Sci. USA, 91, 1677-1681.
64. Mosimann, S. C., Ardelt, W. & James, M. N. G. (1994). Refined 1.7 Å X-ray crystallographic structure of P-30 protein, an amphibian ribonuclease with anti-tumor activity. J. Mol. Biol. 236, 1141-1153.
65. Murthy, B. S. & Sirdeshmukh, R. (1992). Sensitivity of monomeric and dimeric forms of bovine seminal ribonuclease to human placental ribonuclease inhibitor. Biochem. J. 281, 343-348.
66. Nachman, J., Miller, M., Gilliland, G. L., Carty, R., Pincus, M. & Wlodawer, A. (1990). Crystal structure of two covalent nucleoside derivatives of ribonuclease A. Biochemistry, 29, 928-937.
67. Nagano, H., Kiuchi, H., Abe, Y. & Shukuya, R. (1976). Purification and properties of an alkaline ribonuclease from hepatic cytosol fraction of bullfrog, Rana catesbeiana. J. Biochem. 80, 19-26.
68. Neumann, U. & Hofsteenge, J. (1993). Interaction of semisynthetic variants of RNase A with ribonuclease inhibitor. Protein Sci. 3, 248-256.
69. 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.
70. Nitta, K., Oyama, F., Oyama, R., Sekiguchi, K., Kawauchi, H., Takayanagi, Y., Hakomori, S. & Titani, K. (1993). Ribonuclease activity of sialic acid-binding lectin from Rana catesbeiana eggs. Glycobiology, 3, 37-45.
71. Patthy, L. (1991). Modular exchange principles in proteins. Curr. Opin. Struct. Biol. 1, 351-361.
72. Polakowski, I. J., Lewis, M. K., Muthukkaruppan, V., Erdman, B., Kubai, L. & Auerbach, R. (1993). A ribonuclease inhibitor expresses anti-angiogenic properties and leads to reduced tumor growth in mice. Am. J. Pathol. 143, 507-517.
73. Powell, M. J. D. (1977). Restart procedures for the conjugate gradient method. Math. Prog. 12, 241-254.
74. Read, R. J. (1986). Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallog. sect. A, 42, 140-149.
75. Roth, J. S. (1958). Ribonuclease VII. Partial purification and characterization of a ribonuclease inhibitor in rat liver supernatant fraction. J. Biol. Chem. 231, 1085-1095.
76. Roth, J. S. (1962). Ribonuclease IX. Further studies on ribonuclease inhibitor. Biochim. Biophys. Acta, 61, 903-915.
77. Schneider, R., Schneider-Scherzer, E., Thurnher, M., Auer, B. & Schweiger, M. (1988). The primary structure of human ribonuclease/angiogenin inhibitor (RAI) discloses a novel highly diversified protein superfamily with a common repetitive module. EMBO J. 7, 4151-4156.
78. Schreiber, G. & Fersht, A. R. (1993). Interaction of barnase with its polypeptide inhibitor barstar studied by protein engineering. Biochemistry, 32, 5145-5150.
79. Shapiro, R. & Vallee, B. L. (1991). Interaction of human placental ribonuclease with placental ribonuclease inhibitor. Biochemistry, 30, 2246-2255.
80. Shapiro, R. & Vallee, B. L. (1992). Identification of functional arginines in human angiogenin by site-directed mutagenesis. Biochemistry, 31, 12477-12485.
81. Shapiro, R., Fett, J. W., Strydom, D. J. & Vallee, B. L. (1986). Isolation and characterization of a human colon carcinoma-secreted enzyme with pancreatic ribonuclease-like activity. Biochemistry, 25, 7255-7264.
82. Shapiro, R., Riordan, J. F. & Vallee, B. L. (1995). LRRning the RIte of springs. Nature Struct. Biol. 2, 350-354.
83. Shortman, K. (1962). Studies on cellular inhibitors of ribonuclease. III. The levels of ribonuclease inhibitor during the regeneration of rat liver. Biochim. Biophys. Acta, 61, 50-55.
84. Strynadka, N. C. J., Jensen, S. E., Alzari, P. M. & James, M. N. G. (1996). A potent new mode of β-lactamase inhibition revealed by the 1.7 Å X-ray crystallographic structure of the TEM-1-BLIP complex. Nature Struct. Biol. 3, 290-297.
85. Vicentini, A. M., Kieffer, B., Matthies, R., Meyhack, B., Hemmings, B. A., Stone, S. R. & Hofsteenge, J. (1990). Protein chemical and kinetic characterization of recombinant porcine ribonuclease inhibitor expressed in Saccharomyces cerevisiae. Biochemistry, 29, 8827-8834.
86. Williams, A. F. & Barclay, A. N. (1988). The immunoglobulin superfamily-domains for cell surface recognition. Annu. Rev. Immunol. 6, 381-405.
87. Wlodawer, A., Svensson, L. A., Sjolin, L. & Gilliland, G. L. (1988). Structure of phosphate-free ribonuclease A refined at 1.26 Å. Biochemistry, 27, 2705-2717.
88. Wu, Y., Mikulski, S. M., Ardelt, W., Rybak, S. M. & Youle, R. J. (1993). A cytotoxic ribonuclease. J. Biol. Chem. 268, 10686-10693.
89. Zegers, L, Maes, D., Dao-Thi, M.-H., Poortmans, F., Palmer, R. & Wyns, L. (1994). The structure of RNase A complexed with 3′-CMP and d(CpA): active site conformation and conserved water molecules. Protein Sci. 3, 2322-2339.