Modulation of Staphylococcus aureus response to antimicrobials by the Candida albicans quorum sensing molecule farnesol

Antimicrobial Agents and Chemotherapy

Volumn 61, Issue 12, 2017, Pages

  Kong, Eric F ^a,b   Tsui, Christina ^b   Kucharíková, Sona ^c,d   Van Dijck, Patrick ^c,d   Jabra Rizk, Mary Ann ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

C. albicans; Drug resistance; Microbial biofilms; Quorum sensing; S. aureus; Secreted molecules

Indexed keywords

ANTIINFECTIVE AGENT; FARNESOL; REACTIVE OXYGEN METABOLITE; VANCOMYCIN; BACTERIAL PROTEIN; ISOPROTEIN; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN; NORA PROTEIN, STAPHYLOCOCCUS;

ARTICLE; BIOFILM; CANDIDA ALBICANS; DRUG EXPOSURE; DRUG SENSITIZATION; EFFUSION; IN VITRO STUDY; IN VIVO STUDY; MEASUREMENT; MEMBRANE; MODULATION; MOLECULE; OXIDATIVE STRESS; PATHOGENICITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUORUM SENSING; STAPHYLOCOCCUS AUREUS; SURVIVAL; TREATMENT RESPONSE; UPREGULATION; AGONISTS; ANTAGONISTS AND INHIBITORS; CHEMISTRY; CONDITIONED MEDIUM; DRUG EFFECT; DRUG TOLERANCE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; PHARMACOLOGY; SYMBIOSIS;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOFILMS; CANDIDA ALBICANS; CULTURE MEDIA, CONDITIONED; DRUG TOLERANCE; FARNESOL; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PROTEIN ISOFORMS; QUORUM SENSING; REACTIVE OXYGEN SPECIES; STAPHYLOCOCCUS AUREUS; SYMBIOSIS; VANCOMYCIN;

EID: 85035056678     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01573-17     Document Type: Article

References (67)

1. Brogden K, Guthmiller J, Taylor C. 2005. Human polymicrobial infections. Lancet 365:253–255. https://doi.org/10.1016/S0140-6736(05)70155-0.
2. Peters B, Jabra-Rizk MA, O’May G, Costerton J, Shirtliff M. 2012. Polymi-crobial interactions in biofilms: impact on pathogenesis and human disease. Clin Microbiol Rev 25:193–213. https://doi.org/10.1128/CMR.00013-11.
3. Jabra-Rizk MA. 2011. Pathogenesis of polymicrobial biofilms. Open My-col J 5:39–43. https://doi.org/10.2174/1874437001105010039.
4. O’Toole G, Kaplan H, Kolter R. 2000. Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79. https://doi.org/10.1146/annurev.micro.54.1.49.
5. Lewis K. 2001. Riddle of biofilm resistance. Antimicrob Agents Chemother 45:999–1007. https://doi.org/10.1128/AAC.45.4.999-1007.2001.
6. Ghannoum M, Roilides E, Katragkou A, Petraitis V, Walsh T. 2015. The role of echinocandins in Candida biofilm–related vascular catheter infections: in vitro and in vivo model systems. Clin Infect Dis Suppl 6:S618 –S621. https://doi.org/10.1093/cid/civ815.
7. Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890.
8. Jabra-Rizk MA, Kong E, Tsui C, Nguyen M, Clancy C, Fidel P, Noverr M. 2016. Candida albicans pathogenesis: fitting within the host-microbe damage response framework. Infect Immun 84:2724–2739. https://doi.org/10.1128/IAI.00469-16.
9. Ganguly S, Mitchell A. 2011. Mucosal biofilms of Candida albicans. Curr Opin Microbiol 14:380–385. https://doi.org/10.1016/j.mib.2011.06.001.
10. Pfaller M, Diekema D. 2007. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133–163. https://doi.org/10.1128/CMR.00029-06.
11. Jacobsen ID, Wilson D, Wächtler B, Brunke S, Naglik JR, Hube B. 2012. Candida albicans dimorphism as a therapeutic target. Expert Rev Anti Infect Ther 10:85–93. https://doi.org/10.1586/eri.11.152.
12. Mayer FL, Wilson D, Hube B. 2013. Candida albicans pathogenecity mechanisms. Virulence 4:119–128. https://doi.org/10.4161/viru.22913.
13. Tsui C, Kong E, Jabra-Rizk MA. 2016. Pathogenesis of Candida albicans biofilm. Pathog Dis https://doi.org/10.1093/femspd/ftw018.
14. Finkel J, Mitchell A. 2011. Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 9:109–118. https://doi.org/10.1038/ nrmicro2475.
15. Tournu H, Van Dijck P. 2012. Candida biofilms and the host: models and new concepts for eradication. Int J Microbiol https://doi.org/10.1155/2012/845352.
16. Morales D, Hogan D. 2010. Candida albicans interactions with bacteria in the context of human health and disease. PLoS Pathog 6:e1000886. https://doi.org/10.1371/journal.ppat.1000886.
17. McGavin MJ, Heinrichs DE. 2012. The staphylococci and staphylococcal pathogenesis. Front Cell Infect Microbiol https://doi.org/10.3389/fcimb.2012.00066.
18. Sakoulas G, Moellering RC. 2008. Increasing antibiotic resistance among methicillin-resistant Staphylococcus aureus strains. Clin Infect Dis 46: S360–S367. https://doi.org/10.1086/533592.
19. Gordon RJ, Lowy FD. 2008. Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis 46:S350 –S359. https://doi.org/10.1086/533591.
20. Kong E, Johnson J, Jabra-Rizk MA. 2016. Community-associated methicillin-resistant Staphylococcus aureus: an enemy amidst us. PLoS Pathog 12:e1005837. https://doi.org/10.1371/journal.ppat.1005837.
21. Peters B, Ovchinnikova E, Schlecht L, Hoyer L, Busscher H, van der Mei H, Krom B, Jabra-Rizk MA, Shirtliff M. 2012. Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiol 158:2975–2986. https://doi.org/10.1099/mic.0.062109-0.
22. Peters B, Jabra-Rizk MA, Scheper M, Leid J, Costerton J, Shirtliff M. 2010. Microbial interactions and differential protein expression in Staphylococcus aureus and Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol 59:493–503. https://doi.org/10.1111/j.1574-695X.2010.00710.x.
23. Kong E, Tsui C, Kucharíková S, Andes D, Van Dijck P, Jabra-Rizk MA. 2016. Commensal protection of Staphylococcus aureus against antimicrobials by Candida albicans biofilm matrix. mBio 7:e01365-16. https://doi.org/10.1128/mBio.01365-16.
24. Kong E, Kucharíková S, Van Dijck P, Peters B, Shirtliff M, Jabra-Rizk MA. 2015. Clinical implications of oral candidiasis: host tissue damage and disseminated bacterial disease. Infect Immun 83:604–613. https://doi .org/10.1128/IAI.02843-14.
25. Taff H, Nett J, Zarnowski R, Ross K, Sanchez H, Cain M, Hamaker J, Mitchell A, Andes D. 2012. A Candida biofilm-induced pathway for matrix glucan delivery: implications for drug resistance. PLoS Pathog 8:e1002848. https://doi.org/10.1371/journal.ppat.1002848.
26. Nett JE, Sanchez H, Andes DR. 2011. Interface of Candida albicans biofilm matrix-associated drug resistance and cell wall integrity regulation. Eukaryot Cell 10:1660 –1669. https://doi.org/10.1128/EC.05126-11.
27. Demuyser L, Jabra-Rizk MA, Van Dijck P. 2014. Microbial cell surface proteins and secreted metabolites involved in multispecies biofilms. Pathog Dis 70:219–230. https://doi.org/10.1111/2049-632X.12123.
28. Williams P. 2007. Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153:3923–3938. https://doi.org/10.1099/mic.0.2007/012856-0.
29. Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R, Dussault P, Nickerson KW. 2001. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67:2982–2992. https://doi.org/10.1128/AEM.67.7.2982-2992.2001.
30. Sato T, Watanabe T, Mikami T, Matsumoto T. 2004. Farnesol, a morpho-genetic autoregulatory substance in the dimorphic fungus Candida albicans, inhibits hyphae growth through suppression of a mitogen-activated protein kinase cascade. Biol Pharm Bull 27:751–752. https://doi.org/10.1248/bpb.27.751.
31. Uppuluri P, Mekala S, Chaffin WL. 2007. Farnesol-mediated inhibition of Candida albicans yeast growth and rescue by adiacylglycerol analogue. Yeast 24:681–693. https://doi.org/10.1002/yea.1501.
32. Adam B, Baillie GS, Douglas LJ. 2002. Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J Med Microbiol 51:344–349. https://doi.org/10.1099/0022-1317-51-4-344.
33. Tawara Y, Honma K, Naito Y. 1996. Methicillin-resistant Staphylococcus aureus and Candida albicans on denture surfaces. Bull Tokyo Dent Coll 37:119–128.
34. Wargo MJ, Hogan DA. 2006. Fungal-bacterial interactions: a mixed bag of mingling microbes. Curr Opin Microbiol 9:359–364. https://doi.org/10.1016/j.mib.2006.06.001.
35. Pammi M, Liang R, Hicks J, Barrish J, Versalovic J. 2011. Farnesol decreases biofilms of Staphylococcus epidermidis and exhibits synergy with nafcillin and vancomycin. Pediatr Res 70:578 –583. https://doi.org/10.1203/PDR.0b013e318232a984.
36. Jabra-Rizk MA, Meiller T, James C, Shirtliff M. 2006. Effect of farnesol on Staphylococcus aureus biofilm formation and antimicrobial resistance. Antimicrob Agents Chemother 50:1463–1469. https://doi.org/10.1128/AAC.50.4.1463-1469.2006.
37. Cugini C, Calfee MW, Farrow JM, III, Morales DK, Pesci EC, Hogan DA. 2007. Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol 65:896–906. https://doi.org/10.1111/j.1365-2958.2007.05840.x.
38. Akiyama H, Oono T, Huh W, Yamasaki O, Ogawa S, Katsuyama M, Ichikawa H, Iwatsuki K. 2002. Actions of farnesol and xylitol against Staphylococcus aureus. Chemotherapy 48:122–128. https://doi.org/10.1159/000064916.
39. Zhu J, Krom B, Sanglard D, Intapa C, Dawson C, Peters B, Shirtliff M, Jabra-Rizk MA. 2011. Farnesol-induced apoptosis in Candida albicans is mediated by Cdr1-p extrusion and depletion of intracellular glutathione. PLoS One 6:e28830. https://doi.org/10.1371/journal.pone.0028830.
40. Scheper MA, Shirtliff ME, Meiller TF, Peters B, Jabra-Rizk MA. 2008. Farnesol a fungal quorum sensing molecule triggers apoptosis in human oral squamous carcinoma cells. Neoplasia 10:954 –963. https://doi.org/10.1593/neo.08444.
41. Shirtliff ME, Krom BP, Meijering RM, Peters BM, Zhu J, Scheper M, Jabra-Rizk MA. 2009. Farnesol-induced apoptosis in Candida albicans. Antimicrob Agents Chemother 53:2392–2401. https://doi.org/10.1128/AAC.01551-08.
42. Cerca N, Gomes F, Pereira S, Teixeira P, Oliveira R. 2012. Confocal laser scanning microscopy analysis of S. epidermidis biofilms exposed to farnesol, vancomycin and rifampicin. BMC Res Notes 16:244.
43. Inoue Y, Togashi N, Hamashima H. 2016. Farnesol-induced disruption of the Staphylococcus aureus cytoplasmic membrane. Biol Pharm Bull 39: 653–656. https://doi.org/10.1248/bpb.b15-00416.
44. Kaneko M, Togashi N, Hamashima H, Hirohara M, Inoue Y. 2011. Effect of farnesol on mevalonate pathway of Staphylococcus aureus. J Antibiot (Tokyo) 64:547–549. https://doi.org/10.1038/ja.2011.49.
45. Jabra-Rizk MA, Shirtliff M, James C, Meiller TF. 2006. Effect of farnesol on fluconazole resistance in Candida dubliniensis. FEMS Yeast Res 6:1063. https://doi.org/10.1111/j.1567-1364.2006.00121.x.
46. Enjalbert B, Whiteway M. 2005. Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot Cell 4:1203–1210. https://doi.org/10.1128/EC.4.7.1203-1210.2005.
47. Intapa CBJ, Jabra-Rizk MA. 2014. Farnesol-induced apoptosis in oral squamous carcinoma cells is mediated by MRP1 extrusion and depletion of intracellular glutathione. Trends Cancer Res 10:1–6.
48. Gaupp R, Ledala N, Somerville G. 2012. Staphylococcal response to oxidative stress. Front Cell Infect Microbiol 2:33. https://doi.org/10.3389/fcimb.2012.00033.
49. Goerke C, Köller J, Wolz C. 2006. Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob Agents Chemother 50:171–177. https://doi.org/10.1128/AAC.50.1.171-177.2006.
50. Kaatz G, Thyagarajan R, Seo S. 2005. Effect of promoter region mutations and mgrA overexpression on transcription of norA, which encodes a Staphylococcus aureus multidrug efflux transporter. Antimicrob Agents Chemother 49:161–169. https://doi.org/10.1128/AAC.49.1.161-169.2005.
51. Jang S. 2016. Multidrug efflux pumps in Staphylococcus aureus and their clinical implications. J Microbiol 54:1– 8. https://doi.org/10.1007/s12275-016-5159-z.
52. Costa S, Viveiros M, Amaral L, Couto I. 2013. Multidrug efflux pumps in Staphylococcus aureus: an update. Open Microbiol J 7:59 –71. https://doi.org/10.2174/1874285801307010059.
53. Deng X, Sun F, Ji Q. 2012. Expression of multidrug resistance efflux pump gene norA is iron responsive in Staphylococcus aureus. J Bacteriol 194:1753–1762. https://doi.org/10.1128/JB.06582-11.
54. Alcalde-Rico M, Hernando-Amado S, Blanco P, Martínez J. 2016. Multidrug efflux pumps at the crossroad between antibiotic resistance and bacterial virulence. Front Microbiol 21:1483.
55. Truong-Bolduc Q, Zhang X, Hooper D. 2003. Characterization of NorR protein, a multifunctional regulator of norA expression in Staphylococcus aureus. J Bacteriol 185:3127–3138. https://doi.org/10.1128/JB.185.10.3127-3138.2003.
56. Truong-Bolduc Q, Bolduc G, Okumura R. 2011. Implication of the NorB efflux pump in the adaptation of Staphylococcus aureus to growth at acid pH and in resistance to moxifloxacin. Antimicrob Agents Chemother 55:3214–3219. https://doi.org/10.1128/AAC.00289-11.
57. Reipert A, Ehlert K, Kast T, Bierbaum G. 2003. Morphological and genetic differences in two isogenic Staphylococcus aureus strains with decreased susceptibilities to vancomycin. Antimicrob Agents Chemother 47: 568 –576. https://doi.org/10.1128/AAC.47.2.568-576.2003.
58. Zhang S, Sun X, Chang W, Dai Y, Ma X. 2015. Systematic review and meta-analysis of the epidemiology of vancomycin-intermediate and heterogeneous vancomycin-intermediate Staphylococcus aureus isolates. PLoS One 10:e0136082. https://doi.org/10.1371/journal.pone.0136082.
59. Howden BP, Peleg AY, Stinear TP. 2014. The evolution of vancomycin intermediate Staphylococcus aureus (VISA) and heterogenous-VISA. Infect Genet Evol 21:575–582. https://doi.org/10.1016/j.meegid.2013.03.047.
60. Howden BP, Johnson PD, Ward PB, Stinear TP, Davies JK. 2006. Isolates with low-level vancomycin resistance associated with persistent methicillin-resistant Staphylococcus aureus bacteremia. Antimicrob Agents Chemother 50:3039–3047. https://doi.org/10.1128/AAC.00422-06.
61. Luong T, Dunman P, Murphy E, Projan S, Lee C. 2006. Transcription profiling of the mgrA regulon in Staphylococcus aureus. J Bacteriol 188:1899–1910. https://doi.org/10.1128/JB.188.5.1899-1910.2006.
62. Truong-Bolduc Q, Dunman P, Strahilevitz J, Projan S, Hooper D. 2005. MgrA is a multiple regulator of two new efflux pumps in Staphylococcus aureus. J Bacteriol 187:2395–2405. https://doi.org/10.1128/JB.187.7.2395-2405.2005.
63. Chen P, Bae T, Williams W, Duguid E, Rice P, Schneewind O, He C. 2006. An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus. Nat Chem Biol 2:591–595. https://doi.org/10.1038/nchembio820.
64. Lemaire S, Kosowska-Shick K, Appelbaum P, Glupczynski Y, Van Bambeke F, Tulkens P. 2011. Activity of moxifloxacin against intracellular community-acquired methicillin-resistant Staphylococcus aureus: comparison with clindamycin, linezolid and co-trimoxazole and attempt at defining an intracellular susceptibility breakpoint. J Antimicrob Chemother 66:596–607. https://doi.org/10.1093/jac/dkq478.
65. Gillum AM, Tsay EY, Kirsch DR. 1984. Isolation of the Candida albicans gene for orotidine 5=-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198: 179–182. https://doi.org/10.1007/BF00328721.
66. Krause J, Geginat G, Tammer I. 2015. Prostaglandin E2 from Candida albicans stimulates the growth of Staphylococcus aureus in mixed biofilms. PLoS One 10:e0135404. https://doi.org/10.1371/journal.pone .0135404.
67. Ding Y, Onodera Y, Lee J, Hooper D. 2008. NorB, an efflux pump in Staphylococcus aureus strain MW2 contributes to bacterial fitness in abscesses. J Bacteriol 190:7123–7129. https://doi.org/10.1128/JB.00655-08.