Structure-activity relationships for the interactions of 2′- and 3′-(O)-(N-methyl)anthraniloyl-substituted purine and pyrimidine nucleotides with mammalian adenylyl cyclases

Biochemical Pharmacology

Volumn 82, Issue 4, 2011, Pages 358-370

  Pinto, Cibele ^a   Lushington, Gerald H ^a   Richter, Mark ^a   Gille, Andreas ^a   Geduhn, Jens ^b   König, Burkhard ^b   Mou, Tung Chung ^c   Sprang, Stephen R ^c   Seifert, Roland ^d  

^a UNIVERSITY OF KANSAS   (United States)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c UNIVERSITY OF MONTANA   (United States)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Adenylyl Cyclase; Conformational landscape; Fluorescence spectroscopy; MANT nucleotides; Molecular modelling

Indexed keywords

ADENINE; ADENYLATE CYCLASE; ADENYLATE CYCLASE INHIBITOR; CYTOSINE; GUANINE; HETERODIMER; HOMODIMER; HYPOXANTHINE; PURINE NUCLEOSIDE DERIVATIVE; PYRIMIDINE NUCLEOSIDE DERIVATIVE; RECOMBINANT ADENYLATE CYCLASE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; URACIL; XANTHINE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORESCENCE SPECTROSCOPY; MOLECULAR MODEL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

ADENOSINE TRIPHOSPHATE; ADENYLATE CYCLASE; ANIMALS; ANTHRANILIC ACIDS; CATALYTIC DOMAIN; CELL LINE; GUANOSINE TRIPHOSPHATE; MAMMALS; MODELS, MOLECULAR; PROTEIN BINDING; PURINE NUCLEOTIDES; PYRIMIDINE NUCLEOTIDES; SPECTROMETRY, FLUORESCENCE; SPODOPTERA; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 79960380978     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2011.05.010     Document Type: Article

References (50)

1. R.K. Sunahara, C.W. Dessauer, and A.G. Gilman Complexity and diversity of mammalian adenylyl cyclases Annu Rev Pharmacol Toxicol 36 1996 461 480 (Pubitemid 26168706)
2. J. Hanoune, and N. Defer Regulation and role of adenylyl cyclase isoforms Annu Rev Pharmacol Toxicol 41 2001 145 174 (Pubitemid 32385886)
3. W.J. Tang, and J.H. Hurley Catalytic mechanism and regulation of mammalian adenylyl cyclases Mol Pharmacol 54 1998 231 240 (Pubitemid 28368811)
4. C. Pinto, D. Papa, M. Hübner, T.C. Mou, G.H. Lushington, and R. Seifert Activation and inhibition of adenylyl cyclase isoforms by forskolin analogs J Pharmacol Exp Ther 325 2008 27 36 (Pubitemid 351439155)
5. R. Sadana, and C.W. Dessauer Physiological roles for G protein-regulated adenylyl cyclase isoforms: insights from knockout and overexpression studies Neurosignals 17 2009 5 22
6. H. Wang, B. Gong, K.I. Vadakkan, H. Toyoda, B.K. Kaang, and M. Zhuo Genetic evidence for adenylyl cyclase 1 as a target for preventing neuronal exitotoxicity mediated by N-methyl-d-aspartae receptors J Biol Chem 282 2007 1507 1517 (Pubitemid 47076580)
7. V.J. Watts Adenylyl cyclase isoforms as novel therapeutic targets: an exciting example of excitotoxicity neuroprotection Mol Interv 7 2007 70 73 (Pubitemid 46683176)
8. J.A. Chester, and V.J. Watts Adenylyl cyclase 5: a new clue in the search for the "fountain of youth"? Sci STKE 413 2007 pe64
9. S. Okumura, G. Takagi, J. Kawabe, G. Yang, M.C. Lee, and C. Hong Disruption of type 5 adenylyl cyclase gene preserves cardiac function against pressure overload Proc Natl Acad Sci USA 100 2003 9986 9990 (Pubitemid 37087055)
10. K.S. Kim, J. Kim, S.K. Back, J.Y. Im, H.S. Na, and P.L. Han Markedly attenuated acute and chronic pain responses in mice lacking adenylyl cyclase-5 Genes Brain Behav 6 2007 120 127 (Pubitemid 46328583)
11. L. Yan, D.E. Vatner, J.P. O'Connor, A. Ivessa, H. Ge, and W. Chen Type 5 adenylyl cyclase disruption increases longevity and protects against stress Cell 130 2007 247 258 (Pubitemid 47081133)
12. D. Rottländer, J. Matthes, S.F. Vatner, R. Seifert, and S. Herzig Functional adenyly cyclase inhibition in murine cardiomyocytes by 2′(3′)-O-(N-methylanthraniloyl)-guanosine 5′-[γ-thio] triphosphate J Pharmacol Exp Ther 321 2007 608 615 (Pubitemid 46624491)
13. A. Gille, and R. Seifert 2′(3′)-O-(N-Methylanthraniloyl)- substituted GTP analogs: a novel class of potent competitive adenylyl cyclase inhibitors J Biol Chem 278 2003 12672 12679 (Pubitemid 36800027)
14. A. Gille, G.H. Lushington, T.C. Mou, M.B. Doughty, R.A. Johnson, and R. Seifert Differential inhibition of adenylyl cyclase isoforms and soluble guanylyl cyclase by purine and pyrimidine nucleotides J Biol Chem 279 2004 19955 19969 (Pubitemid 38623438)
15. D.M. Jameson, and J.F. Eccleston Fluorescent nucleotide analogs: synthesis and applications Methods Enzymol 278 1997 363 390 (Pubitemid 27229929)
16. T.C. Mou, A. Gille, D.A. Fancy, R. Seifert, and S.R. Sprang Structural basis for the inhibition of mammalian membrane adenylyl cyclase by 2′(3′)-O-(N-methylanthraniloyl)-guanosine 5′-triphosphate J Biol Chem 280 2005 7253 7261 (Pubitemid 40341283)
17. T.C. Mou, A. Gille, S. Suryanarayana, M. Richter, R. Seifert, and S.R. Sprang Broad specificity of mammalian adenylyl cyclase for interaction with 2′,3′-substituted purine- and pyrimidine nucleotide inhibitors Mol Pharmacol 70 2006 878 886 (Pubitemid 44268445)
18. A. Gille, J. Guo, T.C. Mou, M.B. Doughty, G.H. Lushington, and R. Seifert Differential interactions of G-proteins and adenylyl cyclase with nucleoside 5′-triphosphates, nucleoside 5′-[γ-thio]triphosphates and nucleoside 5′-[β,γ-imido]triphosphates Biochem Pharmacol 71 2005 89 97 (Pubitemid 41713530)
19. J.L. Wang, J.-X. Guo, Q.-Y. Zhang, J.J.-Q. Wu, R. Seifert, and G.H. Lushington A Conformational transition in the adenylyl cyclase catalytic site yields different binding modes for ribosyl-modified and unmodified nucleotide inhibitors Bioorg Med Chem 15 2007 2993 3002 (Pubitemid 46400467)
20. S. Suryanarayana, M. Göttle, M. Hübner, A. Gille, T.C. Mou, and S.R. Sprang Differential inhibition of various adenylyl cyclase isoforms and soluble guanylyl cyclase by 2′,3′-O-(2,4,6-trinitrophenyl)- substituted nucleoside 5′-triphosphates J Pharmacol Exp Ther 330 2009 687 695
21. M. Göttle, J. Geduhn, B. König, A. Gille, K. Höcherl, and R. Seifert Characterization of mouse heart adenylyl cyclase J Pharmacol Exp Ther 329 2009 1156 1165
22. S. Suryanarayana, C. Pinto, T.C. Mou, M. Richter, G.H. Lushington, and R. Seifert The C1 homodimer of adenylyl cyclase binds nucleotides with high affinity but possess exceedingly low catalytic activity Neurosci Lett 467 2009 1 5
23. Hübner M, Mou TC, Lushington GH, Pinto C, Gille A, Geduhn J, König B, Sprang SR, Seifert R. Structural basis for the high-affinity inhibition of mammalian adenylyl cyclase by 2′,3′-O-(N- methylanthraniloyl)-inosine 5′-triphosphate. Mol Pharmacol; in press.
24. S. Suryanarayana, J.L. Wang, M. Richter, Y. Shen, W.J. Tang, and G.H. Lushington Distinct interactions of 2′- and 3′-O-(N-methyl) anthraniloyl-isomers of ATP and GTP with the adenylyl cyclase toxin of Bacillus anthracis, edema factor Biochem Pharmacol 78 2009 224 230
25. T. Hiratsuka New ribose-modified fluorescent analogs of adenine and guanine nucleotides available as substrates for various enzymes Biochim Biophys Acta 742 1983 496 508 (Pubitemid 13154050)
26. M. Göttle, S. Dove, P. Steindel, Y. Shen, W.J. Tang, and J. Geduhn Molecular analysis of the interaction of Bordetella pertussis adenylyl cyclase with fluorescent nucleotides Mol Pharmacol 72 2007 526 535 (Pubitemid 47347287)
27. H. Taha, J. Schmidt, M. Göttle, S. Suryanarayana, Y. Shen, and W.J. Tang Molecular analysis of the interaction of anthrax adenylyl cyclase toxin, edema factor, with 2′(3′)-O-(N-(methyl)anthraniloyl)-substituted purine and pyrimidine nucleotides Mol Pharmacol 75 2009 693 703
28. sα with the cytosolic domains of mammalian adenylyl cyclase J Biol Chem 272 1987 22265 22271
29. sα fusion protein Eur J Biochem 255 1998 369 382 (Pubitemid 28340245)
30. SYBYL 8.0, The Tripos Associates, St. Louis. MO, USA, 2008.
31. J. Gasteiger, and M. Marsili A new model for calculating atomic charges in molecules Tetrahedron 36 1978 3219 3228
32. G.M. Morris, D.S. Goodsell, R.S. Halliday, R. Huey, W.E. Hart, and R.K. Belew Automated docking using a Lamarckian genetic algorithm and and empirical binding free energy function J. Comput Chem 19 1998 1639 1662 (Pubitemid 128590223)
33. J. Gasteiger, and M. Marsili A new model for calculating atomic charges in molecules Tetrahedron Lett 34 1978 3181 3184
34. M. Clark, R.D. Cramer, and N. Van Opdenbosch III Validation of the general purpose Tripos 5.2 force field J Comp Chem 10 1989 982 1012
35. sα-GTPγS Science 278 1997 1907 1916 (Pubitemid 28013225)
36. M.A. Marti-Renom, A.C. Stuart, A. Fiser, R. Sanchez, F. Melo, and A. Sali Comparative protein structure modeling of genes and genomes Annu Rev Biophys Biomol Struct 29 2000 291 325 (Pubitemid 30599596)
37. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 1994 4673 4680 (Pubitemid 24354800)
38. S. Henikoff, and J.G. Henikoff Performance evaluation of amino acid substitution matrices Proteins 17 1993 49 61 (Pubitemid 23261057)
39. T. Higashijima, K.M. Ferguson, P.C. Sternweis, E.M. Ross, M.D. Smigel, and A.G. Gilman The effects of activating ligands on the intrinsic fluorescence of guanine nucleotide-binding regulatory proteins J Biol Chem 262 1987 752 756 (Pubitemid 17005248)
40. oα tryptophans in GTP hydrolysis, GDP release, and fluorescence signals Biochemistry 37 1998 837 843 (Pubitemid 28060464)
41. J. Geduhn, S. Dove, Y. Shen, W.J. Tang, B. König, and R. Seifert Bis-halogen-anthraniloyl-substituted nucleoside 5′-triphosphates as potent and selective inhibitors of Bordetella pertussis adenylyl cyclase toxin J Pharmacol Exp Ther 336 2011 104 115
42. G. Zhang, Y. Liu, A.R. Ruoho, and J.H. Hurley Structure of the adenylyl cyclase catalytic core Nature 386 1997 247 253 (Pubitemid 27142504)
43. J.P. Pieroni, A. Harry, J. Chen, O. Jacobowitz, R.P. Magnusson, and R. Iyengar Distinct characteristics of the basal activities of adenylyl cyclases 2 and 6 J Biol Chem 270 1995 1368 1373
44. W.H. Laux, P. Pande, I. Shoshani, J. Gao, V. Boudou-Vivet, and G. Gosselin Pro-nucleotide inhibitors of adenylyl cyclases in intact cells J Biol Chem 279 2004 13317 13332 (Pubitemid 38468854)
45. M. Göttle, S. Dove, F. Kees, J. Schlossmann, J. Geduhn, and B. König Cytidylyl and uridylyl cyclase activity of Bacillus anthracis edema factor and Bordetella pertussis CyaA Biochemistry 49 2010 5494 5503
46. C. Pinto, M. Hübner, A. Gille, M. Richter, T.C. Mou, and S.R. Sprang Differential interactions of the catalytic subunits of adenylyl cyclase with forskolin analogs Biochem Pharmacol 78 2009 62 69
47. B.K. Kobilka, and X. Deupi Conformational complexity of G-protein-coupled receptors Trends Pharmacol Sci 28 2007 397 406 (Pubitemid 47087966)
48. S. Galandrin, G. Oligny-Longre, and M. Bouvier The evasive nature of drug efficacy: implications for drug discovery Trends Pharmacol Sci 28 2007 423 430 (Pubitemid 47087968)
49. R. Seifert, and S. Dove Functional selectivity of GPCR ligand stereoisomers: new pharmacological opportunities Mol Pharmacol 75 2009 13 18
50. T. Kenakin, and L.J. Miller Seven transmembrane receptors as shapeshifting proteins: the impact of allosteric modulation and functional selectivity on new drug discovery Pharmacol Rev 62 2010 265 304