Structure-Based Identification of a Potent Inhibitor Targeting Stp1-Mediated Virulence Regulation in Staphylococcus aureus

Cell Chemical Biology

Volumn 23, Issue 8, 2016, Pages 1002-1013

  Zheng, Weihao ^a   Cai, Xiaodan ^a   Xie, Mingsheng ^a   Liang, Yujie ^a   Wang, Tao ^b   Li, Zigang ^a  

^a PEKING UNIVERSITY   (China)

^b SOUTHERN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AURINTRICARBOXYLIC ACID; TRANSCRIPTOME; VIRULENCE FACTOR; PHOSPHATASE;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG POTENCY; ENZYME ACTIVITY; IN VITRO STUDY; MOLECULAR DOCKING; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; FEMALE; METABOLISM; MICROBIOLOGY; MOLECULAR MODEL; PATHOGENICITY; STRUCTURE ACTIVITY RELATION; VIRULENCE;

ANIMALS; AURINTRICARBOXYLIC ACID; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PHOSPHORIC MONOESTER HYDROLASES; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; STRUCTURE-ACTIVITY RELATIONSHIP; VIRULENCE;

EID: 84982234746     PISSN: 24519456     EISSN: 24519448     Source Type: Journal    
DOI: 10.1016/j.chembiol.2016.06.014     Document Type: Article

References (46)

1. Aburai, N., Yoshida, M., Ohnishi, M., Kimura, K., Sanguinarine as a potent and specific inhibitor of protein phosphatase 2C in vitro and induces apoptosis via phosphorylation of p38 in HL60 cells. Biosci. Biotechnol. Biochem. 74 (2010), 548–552.
2. Alfonso, L., Ai, G., Spitale, R.C., Bhat, G.J., Molecular targets of aspirin and cancer prevention. Br. J. Cancer 111 (2014), 61–67.
3. Archer, G.L., Staphylococcus aureus: a well-armed pathogen. Clin. Infect. Dis. 26 (1998), 1179–1181.
4. Arya, R., Ravikumar, R., Santhosh, R.S., Princy, S.A., SarA based novel therapeutic candidate against Staphylococcus aureus associated with vascular graft infections. Front. Microbiol., 6, 2015, 416.
5. Balaban, N., Goldkorn, T., Nhan, R.T., Dang, L.B., Scott, S., Ridgley, R.M., Rasooly, A., Wright, S.C., Larrick, J.W., Rasooly, R., et al. Autoinducer of virulence as a target for vaccine and therapy against Staphylococcus aureus. Science 280 (1998), 438–440.
6. Benchokroun, Y., Couprie, J., Larsen, A.K., Aurintricarboxylic acid, a putative inhibitor of apoptosis, is a potent inhibitor of DNA topoisomerase II in vitro and in Chinese hamster fibrosarcoma cells. Biochem. Pharmacol. 49 (1995), 305–313.
7. Burnside, K., Lembo, A., de Los Reyes, M., Iliuk, A., Binhtran, N.T., Connelly, J.E., Lin, W.J., Schmidt, B.Z., Richardson, A.R., Fang, F.C., et al. Regulation of hemolysin expression and virulence of Staphylococcus aureus by a serine/threonine kinase and phosphatase. PLoS One, 5, 2010, e11071.
8. Cameron, D.R., Ward, D.V., Kostoulias, X., Howden, B.P., Moellering, R.C. Jr., Eliopoulos, G.M., Peleg, A.Y., Serine/threonine phosphatase Stp1 contributes to reduced susceptibility to vancomycin and virulence in Staphylococcus aureus. J. Infect. Dis. 205 (2012), 1677–1687.
9. Chen, P.R., Bae, T., Williams, W.A., Duguid, E.M., Rice, P.A., Schneewind, O., He, C., An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus. Nat. Chem. Biol. 2 (2006), 591–595.
10. Clatworthy, A.E., Pierson, E., Hung, D.T., Targeting virulence: a new paradigm for antimicrobial therapy. Nat. Chem. Biol. 3 (2007), 541–548.
11. Das, A.K., Helps, N.R., Cohen, P.T., Barford, D., Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution. EMBO J. 15 (1996), 6798–6809.
12. Debarbouille, M., Dramsi, S., Dussurget, O., Nahori, M.A., Vaganay, E., Jouvion, G., Cozzone, A., Msadek, T., Duclos, B., Characterization of a serine/threonine kinase involved in virulence of Staphylococcus aureus. J. Bacteriol. 191 (2009), 4070–4081.
13. DeLeo, F.R., Diep, B.A., Otto, M., Host defense and pathogenesis in Staphylococcus aureus infections. Infect. Dis. Clin. North. Am. 23 (2009), 17–34.
14. Echenique, J., Kadioglu, A., Romao, S., Andrew, P.W., Trombe, M.C., Protein serine/threonine kinase StkP positively controls virulence and competence in Streptococcus pneumoniae. Infect. Immun. 72 (2004), 2434–2437.
15. Escaich, S., Antivirulence as a new antibacterial approach for chemotherapy. Curr. Opin. Chem. Biol. 12 (2008), 400–408.
16. Fjeld, C.C., Denu, J.M., Kinetic analysis of human serine/threonine protein phosphatase 2Calpha. J. Biol. Chem. 274 (1999), 20336–20343.
17. Fujimoto, D.F., Bayles, K.W., Opposing roles of the Staphylococcus aureus virulence regulators, Agr and Sar, in Triton X-100- and penicillin-induced autolysis. J. Bacteriol. 180 (1998), 3724–3726.
18. Gilmartin, A.G., Faitg, T.H., Richter, M., Groy, A., Seefeld, M.A., Darcy, M.G., Peng, X., Federowicz, K., Yang, J., Zhang, S.Y., et al. Allosteric Wip1 phosphatase inhibition through flap-subdomain interaction. Nat. Chem. Biol. 10 (2014), 181–187.
19. Groicher, K.H., Firek, B.A., Fujimoto, D.F., Bayles, K.W., The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J. Bacteriol. 182 (2000), 1794–1801.
20. Hallick, R.B., Chelm, B.K., Gray, P.W., Orozco, E.M. Jr., Use of aurintricarboxylic acid as an inhibitor of nucleases during nucleic acid isolation. Nucleic Acids Res. 4 (1977), 3055–3064.
21. Kobir, A., Shi, L., Boskovic, A., Grangeasse, C., Franjevic, D., Mijakovic, I., Protein phosphorylation in bacterial signal transduction. Biochim. Biophys. Acta 1810 (2011), 989–994.
22. Kristich, C.J., Wells, C.L., Dunny, G.M., A eukaryotic-type Ser/Thr kinase in Enterococcus faecalis mediates antimicrobial resistance and intestinal persistence. Proc. Natl. Acad. Sci. USA 104 (2007), 3508–3513.
23. Kupferwasser, L.I., Yeaman, M.R., Nast, C.C., Kupferwasser, D., Xiong, Y.Q., Palma, M., Cheung, A.L., Bayer, A.S., Salicylic acid attenuates virulence in endovascular infections by targeting global regulatory pathways in Staphylococcus aureus. J. Clin. Investig. 112 (2003), 222–233.
24. Liang, F., Huang, Z., Lee, S.Y., Liang, J., Ivanov, M.I., Alonso, A., Bliska, J.B., Lawrence, D.S., Mustelin, T., Zhang, Z.Y., Aurintricarboxylic acid blocks in vitro and in vivo activity of YopH, an essential virulent factor of Yersinia pestis, the agent of plague. J. Biol. Chem. 278 (2003), 41734–41741.
25. Manna, A.C., Ingavale, S.S., Maloney, M., van Wamel, W., Cheung, A.L., Identification of sarV (SA2062), a new transcriptional regulator, is repressed by SarA and MgrA (SA0641) and involved in the regulation of autolysis in Staphylococcus aureus. J. Bacteriol. 186 (2004), 5267–5280.
26. Martinez Molina, D., Jafari, R., Ignatushchenko, M., Seki, T., Larsson, E.A., Dan, C., Sreekumar, L., Cao, Y., Nordlund, P., Monitoring drug target engagement in cells and tissues using the cellular thermal shift assay. Science 341 (2013), 84–87.
27. Munoz-Dorado, J., Inouye, S., Inouye, M., A gene encoding a protein serine/threonine kinase is required for normal development of M. xanthus, a gram-negative bacterium. Cell 67 (1991), 995–1006.
28. Oh, E.T., So, J.S., A rapid method for RNA preparation from Gram-positive bacteria. J. Microbiol. Methods 52 (2003), 395–398.
29. Ohlsen, K., Donat, S., The impact of serine/threonine phosphorylation in Staphylococcus aureus. Int. J. Med. Microbiol. 300 (2010), 137–141.
30. Pato, M.D., Kerc, E., Regulation of smooth muscle phosphatase-II by divalent cations. Mol. Cell Biochem 101 (1991), 31–41.
31. Pereira, S.F., Goss, L., Dworkin, J., Eukaryote-like serine/threonine kinases and phosphatases in bacteria. Microbiol. Mol. Biol. Rev. 75 (2011), 192–212.
32. Proctor, R.A., Challenges for a universal Staphylococcus aureus vaccine. Clin. Infect. Dis. 54 (2012), 1179–1186.
33. Schlicker, C., Fokina, O., Kloft, N., Grune, T., Becker, S., Sheldrick, G.M., Forchhammer, K., Structural analysis of the PP2C phosphatase tPphA from Thermosynechococcus elongatus: a flexible flap subdomain controls access to the catalytic site. J. Mol. Biol. 376 (2008), 570–581.
34. Shi, Y., Serine/threonine phosphatases: mechanism through structure. Cell 139 (2009), 468–484.
35. Soon, F.F., Ng, L.M., Zhou, X.E., West, G.M., Kovach, A., Tan, M.H., Suino-Powell, K.M., He, Y., Xu, Y., Chalmers, M.J., et al. Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335 (2012), 85–88.
36. Stock, A.M., Robinson, V.L., Goudreau, P.N., Two-component signal transduction. Annu. Rev. Biochem. 69 (2000), 183–215.
37. Sully, E.K., Malachowa, N., Elmore, B.O., Alexander, S.M., Femling, J.K., Gray, B.M., DeLeo, F.R., Otto, M., Cheung, A.L., Edwards, B.S., et al. Selective chemical inhibition of agr quorum sensing in Staphylococcus aureus promotes host defense with minimal impact on resistance. PLoS Pathog., 10, 2014, e1004174.
38. Sun, F., Zhou, L., Zhao, B.-C., Deng, X., Cho, H., Yi, C., Jian, X., Song, C.-X., Luan, C.-H., Bae, T., Targeting MgrA-mediated virulence regulation in Staphylococcus aureus. Chem. Biol. 18 (2011), 1032–1041.
39. Sun, F., Ding, Y., Ji, Q., Liang, Z., Deng, X., Wong, C.C., Yi, C., Zhang, L., Xie, S., Alvarez, S., Protein cysteine phosphorylation of SarA/MgrA family transcriptional regulators mediates bacterial virulence and antibiotic resistance. Proc. Natl. Acad. Sci. USA 109 (2012), 15461–15466.
40. Tamber, S., Schwartzman, J., Cheung, A.L., Role of PknB kinase in antibiotic resistance and virulence in community-acquired methicillin-resistant Staphylococcus aureus strain USA300. Infect. Immun. 78 (2010), 3637–3646.
41. Tanoue, K., Miller Jenkins, L.M., Durell, S.R., Debnath, S., Sakai, H., Tagad, H.D., Ishida, K., Appella, E., Mazur, S.J., Binding of a third metal ion by the human phosphatases PP2Cα and Wip1 is required for phosphatase activity. Biochemistry 52 (2013), 5830–5843.
42. Wang, B., Muir, T.W., Regulation of virulence in Staphylococcus aureus: molecular mechanisms and remaining puzzles. Cell Chem. Biol. 23 (2016), 214–224.
43. Wang, J., Li, C., Yang, H., Mushegian, A., Jin, S., A novel serine/threonine protein kinase homologue of Pseudomonas aeruginosa is specifically inducible within the host infection site and is required for full virulence in neutropenic mice. J. Bacteriol. 180 (1998), 6764–6768.
44. Wehenkel, A., Bellinzoni, M., Grana, M., Duran, R., Villarino, A., Fernandez, P., Andre-Leroux, G., England, P., Takiff, H., Cervenansky, C., et al. Mycobacterial Ser/Thr protein kinases and phosphatases: physiological roles and therapeutic potential. Biochim. Biophys. Acta 1784 (2008), 193–202.
45. Wright, D.P., Ulijasz, A.T., Regulation of transcription by eukaryotic-like serine-threonine kinases and phosphatases in Gram-positive bacterial pathogens. Virulence 5 (2014), 863–885.
46. Zheng, W., Liang, Y., Zhao, H., Zhang, J., Li, Z., 5,5'-Methylenedisalicylic acid (MDSA) modulates SarA/MgrA phosphorylation by targeting Ser/Thr phosphatase Stp1. ChemBioChem 16 (2015), 1035–1040.