Small-molecule targeting of a diapophytoene desaturase inhibits S. aureus virulence

Nature Chemical Biology

Volumn 12, Issue 3, 2016, Pages 174-179

  Chen, Feifei ^a   Di, Hongxia ^a   Wang, Youxin ^b   Cao, Qiao ^a   Xu, Bin ^a   Zhang, Xue ^a   Yang, Nana ^a   Liu, Guijie ^a   Yang, Cai Guang ^a   Xu, Yong ^c   Jiang, Hualiang ^a   Lian, Fulin ^a   Zhang, Naixia ^a   Li, Jian ^b   Lan, Lefu ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c Humanwell Healthcare (Group) Co Ltd   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CAROTENOID; DIAPOPHYTOENE DESATURASE; ENZYME; NAFTIFINE; UNCLASSIFIED DRUG; ALLYLAMINE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CRTN PROTEIN, STAPHYLOCOCCUS AUREUS; OXIDOREDUCTASE; STAPHYLOXANTHIN; VIRULENCE FACTOR; XANTHOPHYLL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BIOSYNTHESIS; COLONY FORMING UNIT; COMPETITIVE INHIBITION; CONTROLLED STUDY; IC50; IN VIVO STUDY; MICHAELIS CONSTANT; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; THERMOSTABILITY; VITAMIN METABOLISM; WILD TYPE; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; ANTIBIOTIC RESISTANCE; BINDING COMPETITION; DRUG DESIGN; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PATHOGENICITY; STAPHYLOCOCCAL INFECTIONS;

ALLYLAMINE; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BINDING, COMPETITIVE; CAROTENOIDS; DRUG DESIGN; DRUG RESISTANCE, BACTERIAL; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; MICROBIAL SENSITIVITY TESTS; OXIDOREDUCTASES; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS; XANTHOPHYLLS;

EID: 84954518195     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2003     Document Type: Article

References (40)

1. Lowy, F.D. Staphylococcus aureus infections. N. Engl. J. Med. 339, 520-532 (1998).
2. DeLeo, F.R., Chambers, H.F. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J. Clin. Invest. 119, 2464-2474 (2009).
3. Klein, E., Smith, D.L., Laxminarayan, R. Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999-2005. Emerg. Infect. Dis. 13, 1840-1846 (2007).
4. Arias, C.A., Murray, B.E. Antibiotic-resistant bugs in the 21st century-a clinical super-challenge. N. Engl. J. Med. 360, 439-443 (2009).
5. Kloos, W.E., Jorgensen, J.H. Staphylococci. in Manual of Clinical Microbiology edn. 4 (eds. Lennette, E.H., Balows, A., Hausler Jr., W.J., Shadomy, H.J.) 143-153 (American Society for Microbiology, Washington, DC, 1985).
6. Liu, C.I. et al. A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence. Science 319, 1391-1394 (2008).
7. Clauditz, A., Resch, A., Wieland, K.P., Peschel, A., Götz, F. Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect. Immun. 74, 4950-4953 (2006).
8. Liu, G.Y. et al. Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J. Exp. Med. 202, 209-215 (2005).
9. Pelz, A. et al. Structure and biosynthesis of staphyloxanthin from Staphylococcus aureus. J. Biol. Chem. 280, 32493-32498 (2005).
10. Kim, S.H., Lee, P.C. Functional expression and extension of staphylococcal staphyloxanthin biosynthetic pathway in Escherichia coli. J. Biol. Chem. 287, 21575-21583 (2012).
11. Bischoff, M., Berger-Bächi, B. Teicoplanin stress-selected mutations increasing sigma(B) activity in Staphylococcus aureus. Antimicrob. Agents Chemother. 45, 1714-1720 (2001).
12. Palma, M., Cheung, A.L. sigma(B) activity in Staphylococcus aureus is controlled by RsbU and an additional factor(s) during bacterial growth. Infect. Immun. 69, 7858-7865 (2001).
13. Lan, L., Cheng, A., Dunman, P.M., Missiakas, D., He, C. Golden pigment production and virulence gene expression are affected by metabolisms in Staphylococcus aureus. J. Bacteriol. 192, 3068-3077 (2010).
14. Fey, P.D. et al. A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. MBio 4, e00537-12 (2013).
15. Ding, Y. et al. Metabolic sensor governing bacterial virulence in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 111, E4981-E4990 (2014).
16. Liu, Y. et al. SsrA (tmRNA) acts as an antisense RNA to regulate Staphylococcus aureus pigment synthesis by base pairing with crtMN mRNA. FEBS Lett. 584, 4325-4329 (2010).
17. Duthie, E.S., Lorenz, L.L. Staphylococcal coagulase; mode of action and antigenicity. J. Gen. Microbiol. 6, 95-107 (1952).
18. Porretta, G.C. et al. Antifungal agents, Part 11. Biphenyl analogues of naftifine: synthesis and antifungal activities. Arch. Pharm. (Weinheim) 328, 667-672 (1995).
19. Gupta, A.K., Ryder, J.E., Cooper, E.A. Naftifine: a review. J. Cutan. Med. Surg. 12, 51-58 (2008).
20. Wieland, B. et al. Genetic and biochemical analyses of the biosynthesis of the yellow carotenoid 4,4-diaponeurosporene of Staphylococcus aureus. J. Bacteriol. 176, 7719-7726 (1994).
21. Russell, R.G. Ibandronate: pharmacology and preclinical studies. Bone 38 (suppl. 1), S7-S12 (2006).
22. Leejae, S., Hasap, L., Voravuthikunchai, S.P. Inhibition of staphyloxanthin biosynthesis in Staphylococcus aureus by rhodomyrtone, a novel antibiotic candidate. J. Med. Microbiol. 62, 421-428 (2013).
23. Pantoliano, M.W. et al. High-density miniaturized thermal shift assays as a general strategy for drug discovery. J. Biomol. Screen. 6, 429-440 (2001).
24. Martinez Molina, D. et al. Monitoring drug target engagement in cells and tissues using the cellular thermal shift assay. Science 341, 84-87 (2013).
25. Raisig, A., Sandmann, G. 4,4-diapophytoene desaturase: catalytic properties of an enzyme from the C30 carotenoid pathway of Staphylococcus aureus. J. Bacteriol. 181, 6184-6187 (1999).
26. Furubayashi, M., Li, L., Katabami, A., Saito, K., Umeno, D. Construction of carotenoid biosynthetic pathways using squalene synthase. FEBS Lett. 588, 436-442 (2014).
27. David, M.Z., Daum, R.S. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin. Microbiol. Rev. 23, 616-687 (2010).
28. Kuroda, M. et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357, 1225-1240 (2001).
29. El-Gohary, M. et al. Topical antifungal treatments for tinea cruris and tinea corporis. Cochrane Database Syst. Rev. 8, CD009992 (2014).
30. Belter, A. et al. Squalene monooxygenase-a target for hypercholesterolemic therapy. Biol. Chem. 392, 1053-1075 (2011).
31. Volkman, J.K. Sterols in microorganisms. Appl. Microbiol. Biotechnol. 60, 495-506 (2003).
32. Alsterholm, M., Karami, N., Faergemann, J. Antimicrobial activity of topical skin pharmaceuticals-an in vitro study. Acta Derm. Venereol. 90, 239-245 (2010).
33. Nolting, S., Braütigam, M. Clinical relevance of the antibacterial activity of terbinafine: a contralateral comparison between 1% terbinafine cream and 0.1% gentamicin sulphate cream in pyoderma. Br. J. Dermatol. 126 (suppl. 39), 56-60 (1992).
34. Ciftci, E., Guriz, H., Aysev, A.D. Mupirocin vs terbinafine in impetigo. Indian J. Pediatr. 69, 679-682 (2002).
35. Koning, S. et al. Interventions for impetigo. Cochrane Database Syst. Rev. 1, CD003261 (2012).
36. Hammond, R.K., White, D.C. Inhibition of vitamin K2 and carotenoid synthesis in Staphylococcus aureus by diphenylamine. J. Bacteriol. 103, 611-615 (1970).
37. Raisig, A., Sandmann, G. Functional properties of diapophytoene and related desaturases of C30 and C40 carotenoid biosynthetic pathways. Biochim. Biophys. Acta 1533, 164-170 (2001).
38. Bae, T. et al. Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc. Natl. Acad. Sci. USA 101, 12312-12317 (2004).
39. Schaub, P. et al. On the structure and function of the phytoene desaturase CRTI from Pantoea ananatis, a membrane-peripheral and FAD-dependent oxidase/isomerase. PLoS One 7, e39550 (2012).
40. Lineweaver, H., Burk, D. The determination of enzyme dissociation constants. J. Am. Chem. Soc. 56, 658-666 (1934).