Molecular recognition of human angiogenin by placental ribonuclease inhibitor - An X-ray crystallographic study at 2.0 Å resolution

EMBO Journal

Volumn 16, Issue 17, 1997, Pages 5162-5177

  Papageorgiou, Anastassios C ^a   Shapiro, Robert ^b   Acharya, K Ravi ^a  

^a University of Bath ^*  (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Angiogenin; Epitope mapping; Molecular recognition; Ribonuclease inhibitor; X ray crystallography

Indexed keywords

ANGIOGENIN; ESTERASE INHIBITOR; LEUCINE; RIBONUCLEASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; HUMAN; MOLECULAR RECOGNITION; MUTAGENESIS; PLACENTA; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BINDING SITES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLACENTAL HORMONES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEINS; RIBONUCLEASE, PANCREATIC; RIBONUCLEASES; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY;

SUIDAE;

EID: 0030864496     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.17.5162     Document Type: Article

References (80)

1. Acharya, K.R., Shapiro, R., Allen, S.C. Riordan, J.F. and 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. Barton, G.J. (1993) ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng., 6, 37-40.
3. Beintema, J.J., Hofsteenge, J., Iwama, M., Morita, T., Ohgi, K.,. Irie, M., Sugiyama, R.H., Schieven, G.L., Dekker, C.A. and Gleitz, D.G. (1988a) Amino acid sequence of the non-secretory ribonuclease of human urine. Biochemistry, 27, 4530-4538.
4. Beintema, J.J., Schuller, C., Irie, M. and Carsana, A. (1988b) Molecular evolution of the ribonuclease superfamily. Prog. Biophys. Mol. Biol., 51, 165-192.
5. Bicknell, R. and Vallee, B.L. (1988) Angiogenin activates endothelial cell phospholipase C. Proc. Natl Acad. Sci. USA, 85, 5961-5965.
6. 2. Proc. Natl Acad. Sci. USA, 86, 1573-1577.
7. Blackburn, P. (1979) Ribonuclease inhibitor from human placenta: rapid purification and assay. J. Biol. Chem., 254, 12484-12487.
8. Blackburn, P., Wilson, G. and 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. and Youle, R.J. (1996) Role of the N-terminus in RNase A homologs -differences in catalytic activity, ribonuclease inhibitor interaction and cytotoxicity. J. Mol. Biol., 257, 992-1007.
10. Brünger, A.T. (1992a) X-PLOR manual: Version 3.1. A System for Crystallography and NMR. Yale University Press, New Haven, CT.
11. Brunger, A.T. (1992b) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature, 355, 472-474.
12. Buckle, A.M., Schreiber, G. and Fersht, A.R. (1994) Protein-protein recognition: crystal structure analysis of a barnase-barstar complex at 2.0Å resolution. Biochemistry, 33, 8878-8889.
13. Chen, C.-Z. and Shapiro, R. (1997) Site-specific mutagenesis reveals differences in the structural bases for tight binding of ribonuclease inhibitor to angiogenin and ribonuclease A. Proc. Natl Acad. Sci. USA, 94, 1761-1766.
14. Chothia,C. (1976) The nature of the accessible and buried surfaces in proteins. J. Mol. Biol., 105, 1-12.
15. Clackson, T. and Wells, J.A. (1995) A hot spot of binding energy in a hormone-receptor interface. Science, 267, 383-386.
16. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr., D50, 760-763.
17. Curran, T.P. Shapiro, R. and Riordan, J.F. (1993) Alteration of the enzymatic specificity of human angiogenin by site-directed mutagenesis. Biochemistry, 32, 2307-2313.
18. S is alpha-marmopyranose. Biochemistry, 34, 11785-11789.
19. de Vos, A.M., Ultsch, M. and Kossiakoff, A.A. (1992) Human growth hormone and extracellular domain of its receptor - crystal structure of the complex. Science, 255, 306-312.
20. Fett, J.W., Strydom, D.J., Lobb., R.R., Alderman, E.M., Bethune, J.L., Riordan, J.F. and Vallee, B.L. (1985) Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry, 24, 5480-5486.
21. Fields, B.A., Goldbaum, F.A., Ysern, X., Poljak, R.J. and Mariuzza, R.A. (1995) Molecular basis of antigen mimicry by an anti-idiotope. Nature, 374, 739-742.
22. Gleich, G.J., Loegering, D.A., Bell, M.P. Checkel, J.L., Ackerman, S.J. and McKean, D.J. (1986) Biochemical and functional similarities between human eosinophil derived neurotoxin and eosinophil cationic protein -homology with ribonuclease. Prof. Natl Acad. Sci. USA, 83, 3146-3150.
23. Goldman, E.R., Dall'Acqua, W., Braden, B.C. and Mariuzza, R.A. (1997) Analysis of binding interactions in an idiotope-antiidiotope protein-protein complex by double mutant cycles. Biochemistry. 36, 49-56.
24. Guillet, V., Lapthorn, A., Hartley, R.W. and Mauguen, Y. (1993) Recognition between bacterial ribonuclease, barnase, and its natural inhibitor, barstar. Structure, 1, 165-177.
25. Hallahan, T.W., Shapiro, R. and Vallee, B.L. (1991) Dual site model for the organogenic activity of angiogenin. Proc. Natl Acad. Sci. USA, 88, 2222-2226.
26. Hartley, R.W. (1993) Directed mutagenesis of barnase-barstar recognition. Biochemistry, 32, 5978-5984.
27. Hofsteenge, J. (1997) Ribonuclease inhibition. In D'Alessio, G. and Riordan, J.F. (eds). Ribonucleases, Structures and Functions. Academic Press, New York, pp. 621-658.
28. Hofsteenge, J., Kieffer, B., Matthies, R., Hemmings, B. and 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.
29. Howlin, B., Moss, D.S. and Harris, G.W. (1989) Segmented anisotropic refinement of bovine pancreatic ribonuclease A by the application of rigid body TLS model. Acta Crystallogr., A45, 851-861.
30. Hu, G.-F., Riordan, J.F. and Vallee, B.L. (1994) Angiogenin promotes invasiveness of cultured endothelial cells by stimulation of cell-associated proteolytic activities. Proc. Natl Acad. Sci. USA, 81, 12096-12100.
31. Hu, G.-F., Riordan, J.F. and Vallee, B.L. (1997) A putative angiogenin receptor in anaiogenin-responsive human endothelial cells. Proc. Natl Acad. Sci. USA, 94, 2204-2209.
32. Janin, J. (1995) Elusive affinities. Proteins: Struct. Funct. Genet., 21, 30-39.
33. Janin, J. and Chothia, C. (1990) The structures of protein-protein recognition sites. J. Biol Chem., 265, 16027-16030.
34. Jeffrey, P.D., Russo, A.A., Polyak, K., Gibbs, E., Hurwitz, J., Massague, J. and Pavletich, N.P. (1995) Mechanism of CDK activation revealed by the structure of a cyclin A-CDK2 complex. Nature, 376, 313-320.
35. Jimi, D.-i., Ito, K.-i., Kohno, K., Ono, M., Kuwano, M., Itagaki, Y. and Ishikawa, H. (1995) Modulation of bovine angiogenin of tubular morphogenesis and expression of plasminogen activator in bovine endothelial cells. Biochem. Biophys. Res. Commun., 211, 476-483.
36. Jones, S. and Thornton, M. (1996) Principles of protein-protein interactions. Proc. Natl Acad. Sci. USA, 93, 13-20.
37. Jones, T.A., Zou, J.Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., A47, 110-119.
38. Kabsch, W. and Sander, C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
39. Kraulis, P.J. (1991) MOLSCRIPT - a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
40. Kobe, B. and Deisenhofer, J. (1993) Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature, 366, 751-756.
41. Kobe, B. and Deisenhofer, J. (1995) A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature, 374, 183-186.
42. Kobe, B. and Deisenhofer, J. (1996) Mechanism of ribonuclease inhibition by ribonuclease inhibitor protein based on the crystal structure of its complex with ribonuclease A. J. Mol. Biol., 264, 1028-1043.
43. Laskowski, R.A., MacArthur, M.W., Moss, D.S. and Thornton, J.M. (1993) PROCHECK: a program to check stereochemical quality of protein structures. J. Appl. Crystallogr., 26, 283-291.
44. Lawrence, M.C. and Colman, P.M. (1993) Shape complementarity at protein-protein interfaces. J. Mol. Biol., 234, 946-950.
45. Lee, F.S. and Vallee, B.L. (1989) Binding of placental ribonuclease inhibitor to the active site of angiogenin. Biochemistry, 28, 3556-3561.
46. Lee, F.S. and Vallee, B.L. (1990) Kinetic characterization of two active mutants of placental ribonuclease inhibitor that lack internal repeats. Biochemistry, 29, 6633-6638.
47. Lee, F.S. and Vallee, B.L. (1993) Structure and action of mammalian ribonuclease (angiogenin) inhibitor. Prog. Nucleic Acid Res., 44, 1-30.
48. Lee, F.S., Fox, E.A., Zhou, H.-M., Strydom, D.J. and Vallee, B.L. (1988) Primary structure of human placental ribonuclease inhibitor. Biochemistry, 27, 8545-8553.
49. Lee, F.S., Shapiro, R. and Vallee, B.L. (1989a) Tight-binding inhibiton of angiogenin and ribonuclease A by placental ribonuclease inhibitor. Biochemistry, 28, 225-230.
50. Lee, F.S., Auld, D.S. and Vallee, B.L. (1989b) Tryptophan fluorescence as a probe of placental ribonuclease inhibitor binding to angiogenin. Biochemistry, 28, 219-224.
51. Moroianu, J. and 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.
52. Mosimann, S.C., Newton, D.L., Youle, R.J. and James, M.N.G. (1996) X-ray crystallographic structure of recombinant eosinophil-derived neurotoxin at 1.83Å resolution. J. Mol. Biol., 260, 540-552.
53. Navaza, J. (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr., A50, 157-163.
54. Neumann, U. and Hofsteenge, J. (1994) Interaction of semisynthetic variants of RNase A with ribonuclease inhibitor. Protein Sci., 3, 248-256.
55. Nicholls, A. and Honig, B. (1991) A rapid unite difference algorithm, utilising successive over relaxation to solve the Poisson-Boltzmann equation. J. Comput. Chem., 12, 435-445.
56. Olson, K.A. and Fett, J.W. (1996) Prostatic carcinoma therapy with angiogenin antagonists. Proc. Am. Assoc. Cancer Res., 37, 57.
57. Olson, K.A., French, T.C., Vallee, B.L. and Fett, J.W. (1994) A monoclonal antibody to human angiogenin suppresses tumor growth in athymic mice. Cancer Res., 54, 4576-4579.
58. Olson, K.A., Fett, J.W., French, T.C., Key, M.E. and Vallee, B.L. (1995) Angiogenin antagonists prevent tumor growth in vivo. Proc. Natl Acad. Sci. USA, 92, 442-446.
59. Otwinowski, Z., (1993) Oscillation data reduction program. In Sawyer, L., Isaacs, N. and Bailey, S. (eds), Data Collection and Processing, Proceedings of CCP4 Study Weekend. SERC Daresbury Laboratory, Warrington, UK, pp. 56-62.
60. Polakowski, I.J., Lewis, M.K., Muthukkaruppan, V., Erdman, B., Kubai, L. and Auerbach, R. (1993) A ribonuclease inhibitor expresses anti-angiogenic properties and leads to reduced tumor growth in mice. Am. J. Pathol., 143, 507-517.
61. Read, R.J. (1986) Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr., A42, 140-149.
62. Richards, F.M. and Wyckoff, H.W. (1973) Ribonuclease S. Phillips, D.C. and Richards, F.M. (eds), The Atlas of Molecular Structures in Biology. Volume I. Clarendon Press, Oxford.
63. Russo, N., Shapiro, R., Acharya, K.R., Riordan, J.F. and Vallee, B.L. (1994) The role of glutamine-117 in the ribonucleolytic activity of human angiogenin. Proc. Natl Acad. Sci. USA, 91, 2920-2924.
64. Russo, N., Acharya, K.R., Vallee, B.L. and Shapiro, R. (1996) A combined kinetic and modeling study of the catalytic center subsites of human angiogenin. Proc. Natl Acad. Sci. USA, 93, 804-808.
65. Rydel, T.J., Tulinsky, A., Bode, W. and Huber, R. (1991) Refined structure of the hirudin-thrombin complex. J. Mol. Biol., 221, 583-601.
66. Saxena, S.K., Rybak, S.M., Winkler, G., Meads, H.M., McGray, P., Youle, R.J. and Ackerman, E.J. (1991) Comparison of ribonucleases and toxins upon injection into Xenopus oocytes. J. Biol Chem., 266, 21208-21214.
67. Schreiber, G. and Fersht, A.R. (1993) Interaction of barnase with its polypeptide inhibitor barstar studies by protein engineering. Biochemistry, 32, 5145-5150.
68. Schreiber, G. and Fersht, A.R. (1995) Energetics of protein-protein interactions: analysis of the barnase-barstar interface by single mutations and double mutant cycles. J. Mol. Biol., 248, 478-486.
69. Shapiro, R. and Vallee, B.L. (1987) Human placental ribonuclease inhibitor abolishes both angiogenic and ribonucleolytic activities of angiogenin. Proc. Natl Acad. Sci. USA, 84, 2238-2241.
70. Shapiro, R. and Vallee, B.L. (1989) Site-directed mutagenesis of histidine-13 and histidine-114 of human angiogenin. Alanine derivatives inhibit angiogenin-induced angiogenesis. Biochemistry, 28, 7401-7408.
71. Shapiro, R. and Vallee, B.L. (1991) Interaction of human placental ribonuclease with placental ribonuclease inhibitor. Biochemistry, 30, 2246-2255.
72. Shapiro, R. and Vallee, B.L. (1992) Identification of functional arginines in human angiogenin by site-directed mutagenesis. Biochemistry, 31, 12477-12485.
73. Shapiro, R., Fett, J.W., Strydom, D.J. and Vallee, B.L. (1986) Isolation and characterization of a human-colon carcinoma secreted enzyme with ribonuclease-like activity. Biochemistry, 25, 7255-7264.
74. Shapiro, R., Weremowicz, S., Riordan, J.F. and Vallee, B.L. (1987) Ribonucleolytic activity of angiogenin - essential histidine, lysine and arginine residues. Proc. Natl Acad. Sci. USA, 84, 8783-8787.
75. Shapiro, R., Harper, J.W., Fox, E.A., Jansen, H.-W., Hein, F. and Uhlmann, E. (1988) Expression of Met-(-1) angiogenin in Escherichia coli -conversion to the authentic
76. Shapiro, R., Fox, E.A. and Riordan, J.F. (1989) Role of lysines and human angiogenin - chemical modification and site-directed mutagenesis. Biochemistry, 28, 1726-1732.
77. Shapiro, R., Riordan, J.F. and Vallee, B.L. (1995) LRRning the RIte of springs. Nature Struct. Biol., 2, 350-354.
78. Soncin, F. (1992) Angiogenin supports endothelial and fibroblast cell adhesion. Proc. Natl Acad. Sci. USA, 89, 2232-2236.
79. Strydom, D.J., Fett, J.W., Lobb, R.R., Alderman, E.M., Bethune, J.L., Riordan, J.F. and Vallee, B.L. (1985) Amino-acid sequence of human-tumor derived angiogenin. Biochemistry, 24, 5486-5494.
80. Strynadka, N.C.J., Jensen, S.E., Alzari, P.M. and James, M.N.G. (1996) A potent new mode of β-lactamase inhibition revealed by the 1.7Å X-ray crystallographic structure of the TEM-1-BLIP complex. Nature Struct. Biol., 3, 290-297.