Two-metal-ion catalysis in adenylyl cyclase

Science

Volumn 285, Issue 5428, 1999, Pages 756-760

  Tesmer, John J G ^a   Sunahara, Roger K ^b   Johnson, Roger A ^c   Gosselin, Gilles ^d   Gilman, Alfred G ^b   Sprang, Stephen R ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; DNA POLYMERASE; METAL ION;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; METAL BINDING; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ADENYLATE CYCLASE; ANIMALS; ASPARTIC ACID; BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; DEOXYADENINE NUCLEOTIDES; DIMERIZATION; ENZYME INHIBITORS; HYDROGEN BONDING; LIGANDS; MAGNESIUM; MANGANESE; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN FOLDING; RATS; THIONUCLEOTIDES; ZINC;

MAMMALIA;

EID: 0033618556     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.285.5428.756     Document Type: Article

References (48)

1. R. K. Sunahara, C. W. Dessauer, A. G. Gilman, Annu. Rev. Pharmacol. Toxicol. 36, 461 (1996); D. M. F. Cooper, Ed., Advances in Second Messenger and Phosphoprotein Research, vol. 32 (Lippincott-Raven, Philadelphia, PA, 1998).
2. R. K. Sunahara, C. W. Dessauer, A. G. Gilman, Annu. Rev. Pharmacol. Toxicol. 36, 461 (1996); D. M. F. Cooper, Ed., Advances in Second Messenger and Phosphoprotein Research, vol. 32 (Lippincott-Raven, Philadelphia, PA, 1998).
3. R. K. Sunahara, C. W. Dessauer, R. E. Whisnant, C. Kleuss, A. G. Gilman, J. Biol. Chem. 272, 22265 (1997).
4. R. E. Whisnant, A. G. Gilman, C. W. Dessauer, Proc. Natl. Acad. Sci. U.S.A. 93, 6621 (1996); S.-Z. Yan, D. Hahn, Z.-H. Huang, W.-J. Tang, J. Biol. Chem. 271, 10941 (1996).
5. R. E. Whisnant, A. G. Gilman, C. W. Dessauer, Proc. Natl. Acad. Sci. U.S.A. 93, 6621 (1996); S.-Z. Yan, D. Hahn, Z.-H. Huang, W.-J. Tang, J. Biol. Chem. 271, 10941 (1996).
6. C. W. Dessauer, J. J. Tesmer, S. R. Sprang, A. G. Gilman, J. Biol. Chem. 273, 25831 (1998).
7. J. J. G. T. Tesmer, R. K. Sunahara, A. G. Gilman, S. R. Sprang, Science 278, 1907 (1997).
8. D. L. Garbers and R. A. Johnson, J. Biol. Chem. 250, 8449 (1975); G. Zimmermann, D. Zhou, R. Taussig, ibid. 273, 19650 (1998).
9. D. L. Garbers and R. A. Johnson, J. Biol. Chem. 250, 8449 (1975); G. Zimmermann, D. Zhou, R. Taussig, ibid. 273, 19650 (1998).
10. P. J. Artymiuk, A. R. Poirrette, D. W. Rice, P. Willett, Nature 388, 33 (1997).
11. S. Doublié, S. Tabor, A. M. Long, C. C. Richardson, T. Ellenberger, ibid. 391, 251 (1998).
12. H. Huang, R. Chopra, G. L. Verdine, S. C. Harrison, Science 282, 1669 (1998).
13. Y. Li, S. Korotev, G. Waksman, EMBO J. 17, 7514 (1998).
14. N. Kaushik et al., Biochemistry 35, 11536 (1996); A. Y. Woody, S. S. Eaton, P. A. Osumi-Davis, R. W. Woody, ibid., p. 144.
15. N. Kaushik et al., Biochemistry 35, 11536 (1996); A. Y. Woody, S. S. Eaton, P. A. Osumi-Davis, R. W. Woody, ibid., p. 144.
16. I. Shoshani, V. Boudou, C. Pierra, G. Gosselin, R. A. Johnson, unpublished data.
17. R. K. Sunahava and J. J. G. Tesmer, data not shown.
18. F. Eckstein, P. Romaniuk, W. Heideman, D. Storm, J. Biol. Chem. 256, 9118 (1981).
19. 2+. Much weaker density corresponding to a purine ring is observed in the purine binding pocket of these complexes. However, the purine and triphosphate densities are not continuous, and a single model of ATP cannot be built to accommodate both purine and triphosphate binding sites.
20. E. E. Kim and H. W. Wyckoff, J. Mol. Biol. 218, 449 (1991).
21. V. Derbyshire, J. K. Pinsonneault, C. M. Joyce, Methods Enzymol. 262, 363 (1995).
22. J. A Piccirilli, J. S. Vyle, M. H. Caruthers, T. R. Cech, Nature 361, 85 (1993).
23. H. Pelletier, M. R. Sawaya, W. Wolfle, S. H. Wilson, J. Kraut, Biochemistry 35, 12762 (1996); I. Slaby, B. Lind, A. Holmgren, Biochem. Biophys. Res. Commun. 122, 1410 (1984); G. C. King, C. T. Martin, T. T. Pham, J. E. Coleman, Biochemistry 25, 36 (1986); E. Ferrari et al., J. Virol. 73, 1649 (1999).
24. H. Pelletier, M. R. Sawaya, W. Wolfle, S. H. Wilson, J. Kraut, Biochemistry 35, 12762 (1996); I. Slaby, B. Lind, A. Holmgren, Biochem. Biophys. Res. Commun. 122, 1410 (1984); G. C. King, C. T. Martin, T. T. Pham, J. E. Coleman, Biochemistry 25, 36 (1986); E. Ferrari et al., J. Virol. 73, 1649 (1999).
25. H. Pelletier, M. R. Sawaya, W. Wolfle, S. H. Wilson, J. Kraut, Biochemistry 35, 12762 (1996); I. Slaby, B. Lind, A. Holmgren, Biochem. Biophys. Res. Commun. 122, 1410 (1984); G. C. King, C. T. Martin, T. T. Pham, J. E. Coleman, Biochemistry 25, 36 (1986); E. Ferrari et al., J. Virol. 73, 1649 (1999).
26. H. Pelletier, M. R. Sawaya, W. Wolfle, S. H. Wilson, J. Kraut, Biochemistry 35, 12762 (1996); I. Slaby, B. Lind, A. Holmgren, Biochem. Biophys. Res. Commun. 122, 1410 (1984); G. C. King, C. T. Martin, T. T. Pham, J. E. Coleman, Biochemistry 25, 36 (1986); E. Ferrari et al., J. Virol. 73, 1649 (1999).
27. S.-Z. Yan, Z.-H. Huang, R. S. Shaw, W.-J. Tang, J. Biol. Chem. 272, 12342 (1997).
28. Y. Liu, A. E. Ruoho, V. D. Rao, J. H. Hurley, Proc. Natl. Acad. Sci. U.S.A. 94, 13414 (1997).
29. W. S. Sheldrick and E. Rieke, Acta Cystallogr. B34, 2324 (1978); K. I. Varughese, C. T. Lu, G. Kartha, J. Am. Chem. Soc. 104, 3398 (1982); N. Padmaja, S. R. Ramakumar, M. A. Viswamitra, Bull. Chem. Soc. Jpn. 64, 1359 (1991).
30. W. S. Sheldrick and E. Rieke, Acta Cystallogr. B34, 2324 (1978); K. I. Varughese, C. T. Lu, G. Kartha, J. Am. Chem. Soc. 104, 3398 (1982); N. Padmaja, S. R. Ramakumar, M. A. Viswamitra, Bull. Chem. Soc. Jpn. 64, 1359 (1991).
31. W. S. Sheldrick and E. Rieke, Acta Cystallogr. B34, 2324 (1978); K. I. Varughese, C. T. Lu, G. Kartha, J. Am. Chem. Soc. 104, 3398 (1982); N. Padmaja, S. R. Ramakumar, M. A. Viswamitra, Bull. Chem. Soc. Jpn. 64, 1359 (1991).
32. C. W. Dessauer and A. G. Gilman, J. Biol. Chem. 272, 27787 (1997).
33. W.-J. Tang M. Stanzel, A. G. Gilman, Biochemistry 34, 14563 (1995).
34. J. J. Tesmer and S. R. Sprang, Curr. Opin. Struct Biol. 8, 713 (1998).
35. L. S. Beese and T. A. Steitz, EMBO J. 10, 25 (1991); T. A. Steitz, Curr. Opin. Struct. Biol. 3, 31 (1993); H. Pelletier, M. R. Sawaya, A. Kumar, S. H. Wilson, J. Kraut. Science 264, 1891 (1994).
36. L. S. Beese and T. A. Steitz, EMBO J. 10, 25 (1991); T. A. Steitz, Curr. Opin. Struct. Biol. 3, 31 (1993); H. Pelletier, M. R. Sawaya, A. Kumar, S. H. Wilson, J. Kraut. Science 264, 1891 (1994).
37. L. S. Beese and T. A. Steitz, EMBO J. 10, 25 (1991); T. A. Steitz, Curr. Opin. Struct. Biol. 3, 31 (1993); H. Pelletier, M. R. Sawaya, A. Kumar, S. H. Wilson, J. Kraut. Science 264, 1891 (1994).
38. S. Doublié, M. R. Sawaya, T. Ellenberger, Structure 7, R31 (1999).
39. S. Doublié and T. Ellenberger, Curr. Opin. Struct. Biol. 8, 704 (1998).
40. S. G. Sarafianos, V. N. Pandey, N. Kaushik, M. J. Modak, J. Biol. Chem. 270, 19729 (1995); V. N. Pandey, N. Kaushik, M. J. Modak, ibid. 269, 13259 (1994).
41. S. G. Sarafianos, V. N. Pandey, N. Kaushik, M. J. Modak, J. Biol. Chem. 270, 19729 (1995); V. N. Pandey, N. Kaushik, M. J. Modak, ibid. 269, 13259 (1994).
42. R. K. Sunahara et al., J. Biol. Chem. 273, 16332 (1998).
43. Single-letter abbreviations for the amino acid residues are as follows: D, Asp; I, Ile; K, Lys; N, Asn; R, Arg.
44. A. G. W. Leslie, MOSFLM 5.50 for image plate data (1997).
45. S. Bailey, Acta Crystallogr. D50, 760 (1994).
46. A. T. Brünger et al., ibid. D54, 905 (1998).
47. T. A. Jones, J. Y. Zou, S. W. Cowan, M. Kjeldgaard, ibid. A47, 110 (1991).
48. p; J. Collins for technical assistance; C. Brautigam for helpful discussion and for reading the manuscript; D. Coleman and the MacCHESS staff for their assistance with data collection at the Cornell High Energy Synchrotron Source (CHESS); and L. Esser for his assistance in preparing figures. R.K.S. was supported by a postdoctoral fellowship from the Medical Research Council of Canada. This work was supported by grants from the Agence Nationale de Recherche sur le SIDA (ANRS, France) to G.G.; by NIH grants DK38828 (R.A.J.), GM34497 (A.G.G.), and DK46371 (S.R.S.); by an Innovative Technology Grant from the Stony Brook Center for Biotechnology to R.A.J.; by Welch Foundation grants I-1271 (A.G.G.) and I-1229 (S.R.S.); and by the Raymond and Ellen Willie Distinguished Chair of Molecular Neuropharmacology (A.G.G.). Coordinates for the four models have been deposited in the Protein Data Bank with the codes 1CJT, 1CJU, 1CJV, and 1CJK.