A high-throughput, multiplexed assay for superfamily-wide profiling of enzyme activity

Nature Chemical Biology

Volumn 10, Issue 8, 2014, Pages 656-663

  Bachovchin, Daniel A ^a   Koblan, Luke W ^a   Wu, Wengen ^b   Liu, Yuxin ^b   Li, Youhua ^b   Zhao, Peng ^b   Woznica, Iwona ^b   Shu, Ying ^b   Lai, Jack H ^b   Poplawski, Sarah E ^b   Kiritsy, Christopher P ^c   Healey, Sarah E ^b   Dimare, Matthew ^b   Sanford, David G ^b   Munford, Robert S ^d   Bachovchin, William W ^b,c   Golub, Todd R ^a,e,f,g  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b TUFTS UNIVERSITY   (United States)

^c Arisaph Pharmaceuticals ^*  (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e DANA FARBER CANCER INSTITUTE   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARI 2243; ARI 2408; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BOCEPREVIR; BORTEZOMIB; BROMOENOL LACTONE; CARFILZOMIB; CERULENIN; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; DABIGATRAN; DIPEPTIDYL PEPTIDASE IV; DIPEPTIDYL PEPTIDASE IV INHIBITOR; DONEPEZIL; EMETINE; ENZYME; ENZYME INHIBITOR; EPOXOMICIN; GABEXATE; MELAGATRAN; NITRILE; PHYSOSTIGMINE; RIVAROXABAN; SERINE HYDROLASE; SERINE HYDROLASE INHIBITOR; SITAGLIPTIN; TELAPREVIR; UNCLASSIFIED DRUG; VILDAGLIPTIN;

ANIMAL EXPERIMENT; ARTICLE; DEACYLATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; HIGH THROUGHPUT SCREENING; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

ANIMALIA;

ANIMALS; BORONIC ACIDS; CARBAMATES; CARBOXYLIC ESTER HYDROLASES; DIPEPTIDYL-PEPTIDASE IV INHIBITORS; DRUG DISCOVERY; ENZYME INHIBITORS; FEMALE; GLUCOSE TOLERANCE TEST; GLUTAMATES; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LIPOPOLYSACCHARIDES; MACACA FASCICULARIS; MALE; MICE, INBRED C57BL; NITRILES; OLIGOPEPTIDES; PIPERAZINES; PROLINE; SERINE PROTEASES; SERINE PROTEINASE INHIBITORS;

EID: 84904896801     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1578     Document Type: Article

References (53)

1. Collins, I. & Workman, P. New approaches to molecular cancer therapeutics. Nat. Chem. Biol. 2, 689-700 (2006).
2. Goldstein, D.M., Gray, N.S. & Zarrinkar, P.P. High-throughput kinase profling as a platform for drug discovery. Nat. Rev. Drug Discov. 7, 391-397 (2008).
3. Fabian, M.A. et al. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol. 23, 329-336 (2005).
4. Davis, M.I. et al. Comprehensive analysis of kinase inhibitor selectivity. Nat. Biotechnol. 29, 1046-1051 (2011).
5. Anastassiadis, T., Deacon, S.W., Devarajan, K., Ma, H. & Peterson, J.R. Comprehensive assay of kinase catalytic activity reveals features of kinase inhibitor selectivity. Nat. Biotechnol. 29, 1039-1045 (2011).
6. Bachovchin, D.A. & Cravatt, B.F. Te pharmacological landscape and therapeutic potential of serine hydrolases. Nat. Rev. Drug Discov. 11, 52-68 (2012).
7. Long, J.Z. & Cravatt, B.F. Te metabolic serine hydrolases and their functions in mammalian physiology and disease. Chem. Rev. 111, 6022-6063 (2011).
8. Cravatt, B.F., Wright, A.T. & Kozarich, J.W. Activity-based protein profling: from enzyme chemistry to proteomic chemistry. Annu. Rev. Biochem. 77, 383-414 (2008).
9. Liu, Y., Patricelli, M.P. & Cravatt, B.F. Activity-based protein profling: the serine hydrolases. Proc. Natl. Acad. Sci. USA 96, 14694-14699 (1999).
10. Leung, D., Hardouin, C., Boger, D.L. & Cravatt, B.F. Discovering potent and selective reversible inhibitors of enzymes in complex proteomes. Nat. Biotechnol. 21, 687-691 (2003).
11. Bachovchin, D.A., Brown, S.J., Rosen, H. & Cravatt, B.F. Identifcation of selective inhibitors of uncharacterized enzymes by high-throughput screening with fuorescent activity-based probes. Nat. Biotechnol. 27, 387-394 (2009).
12. Bachovchin, D.A. et al. Superfamily-wide portrait of serine hydrolase inhibition achieved by library-versus-library screening. Proc. Natl. Acad. Sci. USA 107, 20941-20946 (2010).
13. Bachovchin, D.A. et al. Academic cross-fertilization by public screening yields a remarkable class of protein phosphatase methylesterase-1 inhibitors. Proc. Natl. Acad. Sci. USA 108, 6811-6816 (2011).
14. Fenteany, G. et al. Inhibition of proteasome activities and subunit-specifc amino-terminal threonine modifcation by lactacystin. Science 268, 726-731 (1995).
15. Ostrowska, H., Wojcik, C., Omura, S. & Worowski, K. Lactacystin, a specifc inhibitor of the proteasome, inhibits human platelet lysosomal cathepsin A-like enzyme. Biochem. Biophys. Res. Commun. 234, 729-732 (1997).
16. Ostrowska, H. et al. Separation of cathepsin A-like enzyme and the proteasome: evidence that lactacystin/beta-lactone is not a specifc inhibitor of the proteasome. Int. J. Biochem. Cell Biol. 32, 747-757 (2000).
17. Fenteany, G. & Schreiber, S.L. Lactacystin, proteasome function, and cell fate. J. Biol. Chem. 273, 8545-8548 (1998).
18. Adams, J. Te development of proteasome inhibitors as anticancer drugs. Cancer Cell 5, 417-421 (2004).
19. Arastu-Kapur, S. et al. Nonproteasomal targets of the proteasome inhibitors bortezomib and carflzomib: a link to clinical adverse events. Clin. Cancer Res. 17, 2734-2743 (2011).
20. Roujeau, J.C. et al. Telaprevir-related dermatitis. JAMA Dermatol. 149, 152-158 (2013).
21. Schlütter, J. Terapeutics: new drugs hit the target. Nature 474, S5-S7 (2011).
22. Talas, U., Dunlop, J., Khalaf, S., Leigh, I.M. & Kelsell, D.P. Human elastase 1: evidence for expression in the skin and the identifcation of a frequent frameshif polymorphism. J. Invest. Dermatol. 114, 165-170 (2000).
23. Tani, T., Ohsumi, J., Mita, K. & Takiguchi, Y. Identifcation of a novel class of elastase isozyme, human pancreatic elastase III, by cDNA and genomic gene cloning. J. Biol. Chem. 263, 1231-1239 (1988).
24. Sawyer, L. et al. Te atomic structure of crystalline porcine pancreatic elastase at 2.5-Å resolution: comparisons with the structure of α-chymotrypsin. J. Mol. Biol. 118, 137-208 (1978).
25. Lindenbach, B.D. & Rice, C.M. Unravelling hepatitis C virus replication from genome to function. Nature 436, 933-938 (2005).
26. Liverton, N.J. et al. MK-7009, a potent and selective inhibitor of hepatitis C virus NS3/4A protease. Antimicrob. Agents Chemother. 54, 305-311 (2010).
27. Soisson, S.M. et al. Structural defnition and substrate specifcity of the S28 protease family: the crystal structure of human prolylcarboxypeptidase. BMC Struct. Biol. 10, 16 (2010).
28. Zhou, C. et al. Design and synthesis of prolylcarboxypeptidase (PrCP) inhibitors to validate PrCP as a potential target for obesity. J. Med. Chem. 53, 7251-7263 (2010).
29. Wallingford, N. et al. Prolylcarboxypeptidase regulates food intake by inactivating alpha-MSH in rodents. J. Clin. Invest. 119, 2291-2303 (2009).
30. Mallela, J., Yang, J. & Shariat-Madar, Z. Prolylcarboxypeptidase: a cardioprotective enzyme. Int. J. Biochem. Cell Biol. 41, 477-481 (2009).
31. Long, J.Z. et al. Dual blockade of FAAH and MAGL identifes behavioral processes regulated by endocannabinoid crosstalk in vivo. Proc. Natl. Acad. Sci. USA 106, 20270-20275 (2009).
32. Munford, R.S. & Hall, C.L. Purifcation of acyloxyacyl hydrolase, a leukocyte enzyme that removes secondary acyl chains from bacterial lipopolysaccharides. J. Biol. Chem. 264, 15613-15619 (1989).
33. Long, J.Z., Jin, X., Adibekian, A., Li, W. & Cravatt, B.F. Characterization of tunable piperidine and piperazine carbamates as inhibitors of endocannabinoid hydrolases. J. Med. Chem. 53, 1830-1842 (2010).
34. Lu, M., Varley, A.W., Ohta, S., Hardwick, J. & Munford, R.S. Host inactivation of bacterial lipopolysaccharide prevents prolonged tolerance following Gram-negative bacterial infection. Cell Host Microbe 4, 293-302 (2008).
35. Lu, M. et al. Lipopolysaccharide deacylation by an endogenous lipase controls innate antibody responses to Gram-negative bacteria. Nat. Immunol. 6, 989-994 (2005).
36. Munford, R.S. & Erwin, A.L. Eukaryotic lipopolysaccharide deacylating enzyme. Methods Enzymol. 209, 485-492 (1992).
37. Perrier, J., Durand, A., Giardina, T. & Puigserver, A. Catabolism of intracellular N-terminal acetylated proteins: involvement of acylpeptide hydrolase and acylase. Biochimie 87, 673-685 (2005).
38. Woitach, J.T., Zhang, M., Niu, C.H. & Torgeirsson, S.S. A retinoblastoma-binding protein that afects cell-cycle control and confers transforming ability. Nat. Genet. 19, 371-374 (1998).
39. Shields, D.J. et al. RBBP9: a tumor-associated serine hydrolase activity required for pancreatic neoplasia. Proc. Natl. Acad. Sci. USA 107, 2189-2194 (2010).
40. Bachovchin, D.A. et al. Oxime esters as selective, covalent inhibitors of the serine hydrolase retinoblastoma-binding protein 9 (RBBP9). Bioorg. Med. Chem. Lett. 20, 2254-2258 (2010).
41. Mentlein, R., Gallwitz, B. & Schmidt, W.E. Dipeptidyl-peptidase IV hydrolyses gastric inhibitory polypeptide, glucagon-like peptide-1(7-36) amide, peptide histidine methionine and is responsible for their degradation in human serum. Eur. J. Biochem. 214, 829-835 (1993).
42. Choy, M. & Lam, S. Sitagliptin: a novel drug for the treatment of type 2 diabetes. Cardiol. Rev. 15, 264-271 (2007).
43. Tareja, S. et al. Saxagliptin: a new drug for the treatment of type 2 diabetes. Mini Rev. Med. Chem. 10, 759-765 (2010).
44. Flentke, G.R. et al. Inhibition of dipeptidyl aminopeptidase IV (DP-IV) by Xaa-boroPro dipeptides and use of these inhibitors to examine the role of DP-IV in T-cell function. Proc. Natl. Acad. Sci. USA 88, 1556-1559 (1991).
45. Connolly, B.A. et al. Dipeptide boronic acid inhibitors of dipeptidyl peptidase IV: determinants of potency and in vivo efcacy and safety. J. Med. Chem. 51, 6005-6013 (2008).
46. Lankas, G.R. et al. Dipeptidyl peptidase IV inhibition for the treatment of type 2 diabetes: potential importance of selectivity over dipeptidyl peptidases 8 and 9. Diabetes 54, 2988-2994 (2005).
47. Li, W., Blankman, J.L. & Cravatt, B.F. A functional proteomic strategy to discover inhibitors for uncharacterized hydrolases. J. Am. Chem. Soc. 129, 9594-9595 (2007).
48. Ahn, K. et al. Discovery and characterization of a highly selective FAAH inhibitor that reduces infammatory pain. Chem. Biol. 16, 411-420 (2009).
49. Alexander, J.P. & Cravatt, B.F. Mechanism of carbamate inactivation of FAAH: implications for the design of covalent inhibitors and in vivo functional probes for enzymes. Chem. Biol. 12, 1179-1187 (2005).
50. Hoover, H.S., Blankman, J.L., Niessen, S. & Cravatt, B.F. Selectivity of inhibitors of endocannabinoid biosynthesis evaluated by activity-based protein profling. Bioorg. Med. Chem. Lett. 18, 5838-5841 (2008).
51. Yang, X. et al. A public genome-scale lentiviral expression library of human ORFs. Nat. Methods 8, 659-661 (2011).
52. Martin, B.R., Giepmans, B.N., Adams, S.R. & Tsien, R.Y. Mammalian cell-based optimization of the biarsenical-binding tetracysteine motif for improved fuorescence and afnity. Nat. Biotechnol. 23, 1308-1314 (2005).
53. Munford, R., Lu, M. & Varley, A. Chapter 2: Kill the bacteria and also their messengers? Adv. Immunol. 103, 29-48 (2009).