Cyclic adenosine 5′-diphosphate ribose analogs without a southern ribose inhibit ADP-ribosyl cyclase-hydrolase CD38

Journal of Medicinal Chemistry

Volumn 57, Issue 20, 2014, Pages 8517-8529

  Swarbrick, Joanna M ^a   Graeff, Richard ^b   Zhang, Hongmin ^b   Thomas, Mark P ^a   Hao, Quan ^b   Potter, Barry V L ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

6 CHLORO 9 (4 ACETOXYBUTYL)PURINE; 6 CHLOROPURINE; 9 (4 HYDROXYBUTYL)ADENINE; 9 (4 TERT BUTYLDIPHENYLSILYLBUTYL) 8 BROMOADENINE; 9 (4 TERT BUTYLDIPHENYLSILYLBUTYL) 8 BROMOHYPOXANTHINE; 9 (4 TERT BUTYLDIPHENYLSILYLBUTYL)ADENINE; ADENOSINE DERIVATIVE; ADENOSINE DIPHOSPHATE RIBOSYL CYCLASE; CD38 ANTIGEN; CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; HYDROLASE; LYASE INHIBITOR; N1 (2',3' O ISOPROPYLIDINE BETA DEXTRO RIBOFURANOSYL) N9 [4 (TERT BUTYLDIPHENYSILYL)OXYBUTYL] 8 BROMOHYPOXANTHINE; N1 (2',3',5' TRI O ACETYL BETA DEXTRO RIBOFURANOSYL) N9 [4 (TERT BUTYLDIPHENYLSILYL)OXYBUTYL] 8 BROMOHYPOXANTHINE; N1 (5' O PHOSPHORYL BETA DEXTRO RIBOFURANOSYL) N9 [4 [(DIPHENYLTHIO)PHOSPHORYL]HYDROXYBUTYL] 8 BROMOHYPOXANTHINE; N1 (BETA DEXTRO RIBOFURANOSYL) N9 [4 (TERT BUTYLDIPHENYLSILYL)OXYBUTYL] 8 BROMOHYPOXANTHINE; N1 CYCLIC 8 AMINOHYPOXANTHINE N9 HYDROXYBUTYL DIPHOSPHATE RIBOSE; N1 CYCLIC 8 AZIDOHYPOXANTHINE N9 HYDROXYBUTYL DIPHOSPHATE RIBOSE; N1 CYCLIC 8 BROMOHYPOXANTHINE N9 HYDROXYBUTYL DIPHOSPHATE RIBOSE; N1 CYCLIC HYPOXANTHINE N9 HYDROXYBUTYL DIPHOSPHATE RIBOSE; N1 [2',3' O ISOPROPYLIDINE 5' O (DI TERT BUTYL)PHOSPHORYL BETA DEXTRO RIBOFURANOSYL] N9 [4 [(DIPHENYLTHIO)PHOSPHORYL]HYDROXYBUTYL] 8 BROMOHYPOXANTHINE; N1 [2',3' O ISOPROPYLIDINE 5' O (DI TERT BUTYL)PHOSPHORYL BETA DEXTRO RIBOFURANOSYL] N9 [4(TERT BUTYLDIPHENYLSILYL)OXYBUTYL) 8 BROMOHYPOXANTHINE; N1 [2',3' O ISOPROPYLIDINE 5' O (DI TERT BUTYL)PHOSPHORYL BETA DEXTRO RIBOFURANOSYL]N9 (4 HYDROXYBUTYL) 8 BROMOHYPOXANTHINE; UNCLASSIFIED DRUG; CD38 PROTEIN, HUMAN; ENZYME INHIBITOR; MEMBRANE PROTEIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CRYSTALLOGRAPHY; DRUG POTENCY; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME INHIBITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IC50; PROTEIN HYDROLYSIS; STEREOCHEMISTRY; STRUCTURE ACTIVITY RELATION; SUBSTITUTION REACTION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; HYDROLYSIS; METABOLISM; SYNTHESIS; X RAY CRYSTALLOGRAPHY;

ANTIGENS, CD38; CATALYTIC DOMAIN; CHEMISTRY TECHNIQUES, SYNTHETIC; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRYSTALLOGRAPHY, X-RAY; CYCLIC ADP-RIBOSE; ENZYME INHIBITORS; HUMANS; HYDROLYSIS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR;

EID: 84908374193     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm501037u     Document Type: Article

References (66)

1. Clapper, D. L.; Walseth, T. F.; Dargie, P. J.; Lee, H. C. Pyridine-nucleotide metabolites stimulate calcium release from sea-urchin egg microsomes desensitized to inositol trisphosphate J. Biol. Chem. 1987, 262, 9561-9568
2. Lee, H. C.; Aarhus, R.; Levitt, D. The crystal structure of cyclic ADP-ribose Nat. Struct. Biol. 1994, 1, 143-144
3. 2+ stores: a perspective from cyclic ADP-ribose and NAADP Curr. Mol. Med. 2004, 4, 227-237
4. Guse, A. H. Biochemistry, biology, and pharmacology of cyclic adenosine diphosphoribose (cADPR) Curr. Med. Chem. 2004, 11, 847-855
5. Potter, B. V. L.; Walseth, T. F. Medicinal chemistry and pharmacology of cyclic ADP-ribose Curr. Mol. Med. 2004, 4) 303-311
6. Guse, A. H. Second messenger function and the structure-activity relationship of cyclic adenosine diphosphoribose (cADPR) FEBS J. 2005, 272, 4590-4597
7. Zhao, Y. J.; Lam, C. M. C.; Lee, H. C. The membrane-bound enzyme CD38 exists in two opposing orientations Sci. Signaling 2012, 5, ra67
8. Perraud, A. L.; Fleig, A.; Dunn, C. A.; Bagley, L. A.; Launay, P.; Schmitz, C.; Stokes, A. J.; Zhu, Q. Q.; Bessman, M. J.; Penner, R.; Kinet, J. P.; Scharenberg, A. M. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology Nature 2001, 411, 595-599
9. Kim, H.; Jacobson, E. L.; Jacobson, M. K. Synthesis and degradation of cyclic ADP-ribose by NAD glycohydrolases Science 1993, 261, 1330-1333
10. Howard, M.; Grimaldi, J.; Bazan, J.; Lund, F.; Santos-Argumedo, L.; Parkhouse, R.; Walseth, T.; Lee, H. Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38 Science 1993, 262, 1056-1059
11. 2+ mobilization from lysosomes in pancreatic acinar cells J. Biol. Chem. 2010, 285, 38251-38259
12. Savarino, A.; Bensi, T.; Chiocchetti, A.; Bottarel, F.; Mesturini, R.; Ferrero, E.; Calosso, L.; Deaglio, S.; Ortolan, E.; Buttò, S.; Cafaro, A.; Katada, T.; Ensoli, B.; Malavasi, F.; Dianzani, U. Human CD38 interferes with HIV-1 fusion through a sequence homologous to the V3 loop of the viral envelope glycoprotein gp120 FASEB J. 2003, 17, 461-463
13. Malavasi, F.; Deaglio, S.; Damle, R.; Cutrona, G.; Ferrarini, M.; Chiorazzi, N. CD38 and chronic lymphocytic leukemia: a decade later Blood 2011, 118, 3470-3478
14. Aksoy, P.; White, T. A.; Thompson, M.; Chini, E. N. Regulation of intracellular levels of NAD: a novel role for CD38 Biochem. Biophys. Res. Commun. 2006, 345, 1386-1392
15. -/- mouse Biochem. Biophys. Res. Commun. 2006, 346, 188-192
16. Chini, E. N. CD38 as a regulator of cellular NAD: a novel potential pharmacological target for metabolic conditions Curr. Pharm. Des. 2009, 15, 57-63
17. Jin, D.; Liu, H. X.; Hirai, H.; Torashima, T.; Nagai, T.; Lopatina, O.; Shnayder, N. A.; Yamada, K.; Noda, M.; Seike, T.; Fujita, K.; Takasawa, S.; Yokoyama, S.; Koizumi, K.; Shiraishi, Y.; Tanaka, S.; Hashii, M.; Yoshihara, T.; Higashida, K.; Islam, M. S.; Yamada, N.; Hayashi, K.; Noguchi, N.; Kato, I.; Okamoto, H.; Matsushima, A.; Salmina, A.; Munesue, T.; Shimizu, N.; Mochida, S.; Asano, M.; Higashida, H. CD38 is critical for social behaviour by regulating oxytocin secretion Nature 2007, 446, 41-45
18. 2+ signaling Messenger 2013, 2, 19-32
19. Sauve, A. A.; Schramm, V. L. Mechanism-based inhibitors of CD38: a mammalian cyclic ADP-ribose synthetase Biochemistry 2002, 41, 8455-8463
20. Dong, M.; Si, Y. Q.; Sun, S. Y.; Pu, X. P.; Yang, Z. J.; Zhang, L. R.; Zhang, L. H.; Leung, F. P.; Lam, C. M. C.; Kwong, A. K. Y.; Yue, J. B.; Zhou, Y. Y.; Kriksunov, I. A.; Hao, Q.; Lee, H. C. Design, synthesis and biological characterization of novel inhibitors of CD38 Org. Biomol. Chem. 2011, 9, 3246-3257
21. + glycohydrolase activity of CD38 by carbocyclic NAD analogues Biochem. J. 1998, 335, 631-636
22. Kellenberger, E.; Kuhn, I.; Schuber, F.; Muller-Steffner, H. Flavonoids as inhibitors of human CD38 Bioorg. Med. Chem. Lett. 2011, 21, 3939-3942
23. Zhou, Y.; Ting, K. Y.; Lam, C. M. C.; Kwong, A. K. Y.; Xia, J.; Jin, H.; Liu, Z.; Zhang, L.; Lee, H. C.; Zhang, L. Design, synthesis and biological evaluation of noncovalent inhibitors of human CD38 NADase ChemMedChem 2012, 7, 223-228
24. Sauve, A. A.; Deng, H. T.; Angeletti, R. H.; Schramm, V. L. A covalent intermediate in CD38 in responsible for ADP-ribosylation and cyclisation reactions J. Am. Chem. Soc. 2000, 122, 7855-7859
25. 2+-release Biochemistry 1997, 36, 9509-9517
26. Guse, A. H.; Cakir-Kiefer, C.; Fukuoka, M.; Shuto, S.; Weber, K.; Bailey, V. C.; Matsuda, A.; Mayr, G. W.; Oppenheimer, N.; Schuber, F.; Potter, B. V. L. Novel hydrolysis-resistant analogues of cyclic ADP-ribose: modification of the "northern" ribose and calcium release activity Biochemistry 2002, 41, 6744-6751
27. 2+-mobilising mimic of cyclic adenosine diphosphate ribose FEBS Lett. 1996, 379, 227-230
28. Wagner, G. K.; Guse, A. H.; Potter, B. V. L. Rapid synthetic route toward structurally modified derivatives of cyclic adenosine 5′-diphosphate ribose J. Org. Chem. 2005, 70, 4810-4819
29. Wagner, G. K.; Black, S.; Guse, A. H.; Potter, B. V. L. First enzymatic synthesis of an N 1-cyclised cADPR (cyclic ADP-ribose) analogue with a hypoxanthine partial structure: discovery of a membrane permeant cADPR agonist Chem. Commun. 2003, 1944-1945
30. Kirchberger, T.; Moreau, C.; Wagner, G. K.; Fliegert, R.; Siebrands, C. C.; Nebel, M.; Schmid, F.; Harneit, A.; Odoardi, F.; Flugel, A.; Potter, B. V. L.; Guse, A. H. 8-Bromo-cyclic inosine diphosphoribose: towards a selective cyclic ADP-ribose agonist Biochem. J. 2009, 422, 139-149
31. 2+-mobilizing second messenger cyclic ADP-ribose J. Am. Chem. Soc. 2001, 123, 8750-8759
32. Shuto, S.; Shirato, M.; Sumita, Y.; Ueno, Y.; Matsuda, A. Synthesis of cyclic IDP-carbocyclic-ribose, a stable mimic of cyclic ADP-ribose. Significant facilitation of the intramolecular condensation reaction of N 1-(carbocyclic-ribosyl)inosine 5′,6′-diphosphate derivatives by an 8-bromo-substitution at the hypoxanthine moiety J. Org. Chem. 1998, 63, 1986-1994
33. Fukuoka, M.; Shuto, S.; Minakawa, N.; Ueno, Y.; Matsuda, A. An efficient synthesis of cyclic IDP and cyclic 8-bromo-IDP-carbocyclic-riboses using a modified Hata condensation method to form an intramolecular pyrophosphate linkage as a key step. An entry to a general method for the chemical synthesis of cyclic ADP-ribose analogues J. Org. Chem. 2000, 65, 5238-5248
34. Gu, X.; Yang, Z.; Zhang, L.; Kunerth, S.; Fliegert, R.; Weber, K.; Guse, A. H. Synthesis and biological evaluation of novel membrane-permeant cyclic ADP-ribose mimics: N 1-[(5′- O -phosphorylethoxy)methyl]-5′- O -phosphorylinosine-5′,5′-cyclicpyrophosphate (cIDPRE) and 8-substituted derivatives J. Med. Chem. 2004, 47, 5674-5682
35. Guse, A. H.; Gu, X. F.; Zhang, L. R.; Weber, K.; Kramer, E.; Yang, Z. J.; Jin, H. W.; Li, Q.; Carrier, L.; Zhang, L. H. A minimal structural analogue of cyclic ADP-ribose: synthesis and calcium release activity in mammalian cells J. Biol. Chem. 2005, 280, 15952-15959
36. Huang, L. J.; Zhao, Y. Y.; Yuan, L.; Min, J. M.; Zhang, L. H. Syntheses and calcium-mobilizing evaluations of N 1-glycosyl-substituted stable mimics of cyclic ADP-ribose J. Med. Chem. 2002, 45, 5340-5352
37. Swarbrick, J. M.; Potter, B. V. L. Total Synthesis of a cyclic adenosine 5′-diphosphate ribose receptor agonist J. Org. Chem. 2012, 77, 4191-4197
38. Graeff, R. M.; Walseth, T. F.; Hill, H. K.; Lee, H. C. Fluorescent analogs of cyclic ADP-ribose: synthesis, spectral characterization, and use Biochemistry 1996, 35, 379-386
39. Graeff, R.; Liu, Q.; Kriksunov, I. A.; Kotaka, M.; Oppenheimer, N.; Hao, Q.; Lee, H. C. Mechanism of cyclizing NAD to cyclic ADP-ribose by ADP-ribosyl cyclase and CD38 J. Biol. Chem. 2009, 284, 27629-27636
40. Graeff, R.; Liu, Q.; Kriksunov, I. A.; Hao, Q.; Lee, H. C. Acidic residues at the active sites of CD38 and ADP-ribosyl cyclase determine nicotinic acid adenine dinucleotide phosphate (NAADP) synthesis and hydrolysis activities J. Biol. Chem. 2006, 281, 28951-28957
41. Liu, Q.; Kriksunov, I. A.; Graeff, R.; Munshi, C.; Lee, H. C.; Hao, Q. Crystal structure of human CD38 extracellular domain Structure 2005, 13, 1331-1339
42. Liu, Q.; Kriksunov, I. A.; Moreau, C.; Graeff, R.; Potter, B. V. L.; Lee, H. C.; Hao, Q. Catalysis associated conformational changes revealed by human CD38 complexed with a non-hydrolysable substrate analog J. Biol. Chem. 2007, 282, 24825-24832
43. Moreau, C.; Liu, Q.; Graeff, R.; Wagner, G. K.; Thomas, M. P.; Swarbrick, J. M.; Shuto, S.; Lee, H. C.; Hao, Q.; Potter, B. V. L. CD38 structure-based inhibitor design using the N 1-cyclic inosine 5′-diphosphate ribose template PLoS One 2013, 8, e66247
44. Graeff, R. M.; Munshi, C.; Aarhus, R.; Johns, M.; Lee, H. C. A single residue at the active site of CD38 determines its NAD cyclizing and hydrolyzing activities J. Biol. Chem. 2001, 276, 12169-12173
45. Munshi, C.; Aarhus, R.; Graeff, R.; Walseth, T. F.; Levitt, D.; Lee, H. C. Identification of the enzymatic active site of CD38 by site-directed mutagenesis J. Biol. Chem. 2000, 275, 21566-21571
46. + glycohydrolase by site directed mutagenesis of key active site residues Biochim. Biophys. Acta, Proteins Proteomics 2014, 1844, 1317-1331
47. Moreau, C.; Woodman, T. J.; Potter, B. V. L. Unusual entry to the novel 8-halo- N 1-ribosyl hypoxanthine system by degradation of a cyclic adenosine 5′-diphosphate ribose analogue Chem. Commun. 2006, 1127-1129
48. Galeone, A.; Mayol, L.; Oliviero, G.; Piccialli, G.; Varra, M. Synthesis of a novel N 1-carbocyclic, N 9 butyl analogue of cyclic ADP-ribose (cADPR) Tetrahedron 2002, 58, 363-368
49. Volpini, R.; Mishra, R. C.; Kachare, D. D.; Ben, D. D.; Lambertucci, C.; Antonini, I.; Vittori, S.; Marucci, G.; Sokolova, E.; Nistri, A.; Cristalli, G. Adenine-based acyclic nucleotides as novel P2X3 receptor ligands J. Med. Chem. 2009, 52, 4596-4603
50. Laufer, S. A.; Domeyer, D. M.; Scior, T. R. F.; Albrecht, W.; Hauser, D. R. J. Synthesis and biological testing of purine derivatives as potential ATP-competitive kinase inhibitors J. Med. Chem. 2005, 48, 710-722
51. Nolsoe, J. M. J.; Gundersen, L.-L.; Rise, F. Synthesis of 8-halopurines by reaction of lithiated purines with appropriate halogen donors Synth. Commun. 1998, 28, 4303-4315
52. Graeff, R. M.; Lee, H. C. A novel cycling assay for cellular cADP-ribose with nanomolar sensitivity Biochem. J. 2002, 361, 379-384
53. Liu, Q.; Kriksunov, I. A.; Graeff, R.; Munshi, C.; Lee, H. C.; Hao, Q. Structural basis for the mechanistic understanding of human CD38-controlled multiple catalysis J. Biol. Chem. 2006, 281, 32861-32869
54. Zhang, H.; Graeff, R.; Lee, H. C.; Hao, Q. Crystal structures of human CD38 in complex with NAADP and ADPRP Messenger 2013, 2, 44-53
55. Sauve, A. A.; Munshi, C.; Lee, H. C.; Schramm, V. L. The reaction mechanism for CD38. A single intermediate is responsible for cyclization, hydrolysis, and base-exchange chemistries Biochemistry 1998, 37, 13239-13249
56. Kim, H.; Jacobson, E. L.; Jacobson, M. K. Position of cyclization in cyclic ADP-ribose Biochem. Biophys. Res. Commun. 1993, 194, 1143-1147
57. Ames, B. N.; Dubin, D. T. The role of polyamines in the neutralization of bacteriophage deoxyribonucleic acid J. Biol. Chem. 1960, 235, 769-775
58. Jones, G.; Willett, P.; Glen, R. C.; Leach, A. R.; Taylor, R. Development and validation of a genetic algorithm for flexible docking J. Mol. Biol. 1997, 267, 727-748
59. Otwinowski, Z.; Minor, W. Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 1997, 307-325
60. McCoy, A.; Grosse-Kunstleve, R.; Adams, P.; Winn, M.; Storoni, L.; Read, R. Phaser crystallographic software J. Appl. Crystallogr. 2007, 40, 658-674
61. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50, 760-763
62. Murshudov, G.; Vagin, A.; Dodson, E. Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 1997, 53, 240-255
63. Emsley, P.; Lohkamp, B.; Scott, W. G.; Cowtan, K. Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 486-501
64. Schuttelkopf, A.; Van Aalten, D. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 1355-1363
65. Painter, J.; Merritt, E. TLSMD Web server for the generation of multi-group TLS models J. Appl. Crystallogr. 2006, 39, 109-111
66. Chen, V. B.; Arendall, W. B., 3rd; Headd, J. J.; Keedy, D. A.; Immormino, R. M.; Kapral, G. J.; Murray, L. W.; Richardson, J. S.; Richardson, D. C. MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 12-21