
f Antibacterial activity of diacetylcurcumin against Staphylococcus aureus results in decreased biofilm and cellular adhesion
- Authors: Janaina de Cássia Orlandi Sardi1 , Carlos Roberto Polaquini2 , Irlan Almeida Freires1 , Livia Câmara de Carvalho Galvão1 , Josy Goldoni Lazarini1 , Guilherme Silva Torrezan2 , Luis Octávio Regasini2 , Pedro Luiz Rosalen1
-
- VIEW AFFILIATIONS
-
1 1Department of Physiological Sciences, Piracicaba Dental School, University of Campinas, 13414 903 Piracicaba, São Paulo, Brazil 2 2Department of Chemistry and Environmental Sciences, São Paulo State University Júlio de Mesquita Filho, São Jose do Rio Preto, São Paulo, Brazil
- *Correspondence: Pedro Luiz Rosalen, [email protected]
- First Published Online: 09 June 2017, Journal of Medical Microbiology 66: 816-824, doi: 10.1099/jmm.0.000494
- Subject: Prevention and Therapy
- Received:
- Accepted:
- Cover date:




Antibacterial activity of diacetylcurcumin against Staphylococcus aureus results in decreased biofilm and cellular adhesion, Page 1 of 1
< Previous page | Next page > /docserver/preview/fulltext/jmm/66/6/816_jmm000494-1.gif
-
Purpose. Staphylococcus aureus infections have contributed to the global healthcare burden, particularly with regard to hospital-acquired meticillin-resistant S. aureus (MRSA) infections.
Methodology. This study describes the antibacterial activity of diacetylcurcumin (DAC) against meticillin-susceptible S. aureus/MRSA biofilm formation, survival, metabolic activity and structure; its ability to prevent bacterial adhesion to human cells; and toxicity in Galleria mellonella larvae.
Results. DAC showed excellent antibacterial activity, with MIC ranging between 17.3 and 34.6 µmol l−1, and minimum bactericidal concentration ranging between 69 and 277 µmol l−1. It significantly reduced bacterial biofilm survival – by 22–63 % (at MIC, 10×MIC or 100×MIC) as compared to the 25–42 % reduction by vancomycin (P<0.0001) – and severely affected biofilm cell structures, leading to damaged architecture and the formation of amorphous cell clusters. Treatment with DAC (MIC/4) decreased bacterial adhesion to HaCaT keratinocytes from 1 to 5 h (P<0.0001). Finally, DAC demonstrated low toxicity in G. mellonella at its effective anti-biofilm concentrations.
Conclusion. These findings open new avenues for the study of this curcumin derivative as an excellent prototype with anti-MRSA activity.
- Keyword(s): anti-adhesion, diacetylcurcumin, Staphylococcus aureus, curcumin, antibiofilm, toxicity
© 2017 The Authors | Published by the Microbiology Society
-
1. De La Calle C, Morata L, Cobos-Trigueros N, Martinez JA, Cardozo C et al. Staphylococcus aureus bacteremic pneumonia. Eur J Clin Microbiol Infect Dis 2016;35:497–502 [CrossRef][PubMed]
-
2. Bradley SF. MRSA colonisation (eradicating colonisation in people without active invasive infection). BMJ Clin Evid 2015;2015:0923[PubMed]
-
3. Jeremiah CJ, Kandiah JP, Spelman DW, Giffard PM, Coombs GW et al. Differing epidemiology of two major healthcare-associated meticillin-resistant Staphylococcus aureus clones. J Hosp Infect 2016;92:183–190 [CrossRef][PubMed]
-
4. Sollid JU, Furberg AS, Hanssen AM, Johannessen M. Staphylococcus aureus: determinants of human carriage. Infect Genet Evol 2014;21:531–541 [CrossRef][PubMed]
-
5. Bhattacharya M, Wozniak DJ, Stoodley P, Hall-Stoodley L. Prevention and treatment of Staphylococcus aureus biofilms. Expert Rev Anti Infect Ther 2015;13:1499–1516 [CrossRef][PubMed]
-
6. McConoughey SJ, Howlin R, Granger JF, Manring MM, Calhoun JH et al. Biofilms in periprosthetic orthopedic infections. Future Microbiol 2014;9:987–1007 [CrossRef][PubMed]
-
7. Arciola CR, Hänsch GM, Visai L, Testoni F, Maurer S et al. Interactions of staphylococci with osteoblasts and phagocytes in the pathogenesis of implant-associated osteomyelitis. Int J Artif Organs 2012;35:713–726 [CrossRef][PubMed]
-
8. Lebeaux D, Ghigo JM, Lortholary O. Infections related to implanted medical devices: the down-side of medical progress. Rev Prat 2014;64:617–619 (in French)[PubMed]
-
9. Rendeková K, Fialová S, Jánošová L, Mučaji P, Slobodníková L. The activity of Cotinus coggygria Scop. leaves on Staphylococcus aureus strains in planktonic and biofilm growth forms. Molecules 2015;21:E50 [CrossRef][PubMed]
-
10. Saginur R, Stdenis M, Ferris W, Aaron SD, Chan F et al. Multiple combination bactericidal testing of staphylococcal biofilms from implant-associated infections. Antimicrob Agents Chemother 2006;50:55–61 [CrossRef][PubMed]
-
11. Vuong C, Otto M. Staphylococcus epidermidis infections. Microbes Infect 2002;4:481–489 [CrossRef][PubMed]
-
12. Ziebuhr W, Lössner I, Rachid S, Dietrich K, Götz F et al. Modulation of the polysaccharide intercellular adhesin (PIA) expression in biofilm forming Staphylococcus epidermidis. Analysis of genetic mechanisms. Adv Exp Med Biol 2000;485:151–157 [CrossRef][PubMed]
-
13. Rosenthal VD, Maki DG, Salomao R, Moreno CA, Mehta Y et al. Device-associated nosocomial infections in 55 intensive care units of eight developing countries. Ann Intern Med 2006;145:582–591 [CrossRef][PubMed]
-
14. Borra SK, Mahendra J, Gurumurthy P, Jayamathi, Iqbal SS et al. Effect of curcumin against oxidation of biomolecules by hydroxyl radicals. J Clin Diagn Res 2014;8:CC01–CC05 [CrossRef][PubMed]
-
15. Anand P, Thomas SG, Kunnumakkara AB, Sundaram C, Harikumar KB et al. Biological activities of curcumin and its analogues (congeners) made by man and Mother Nature. Biochem Pharmacol 2008;76:1590–1611 [CrossRef][PubMed]
-
16. Alok A, Singh ID, Singh S, Kishore M, Jha PC. Curcumin – pharmacological actions and its role in oral submucous fibrosis: a review. J Clin Diagn Res 2015;9:ZE01–ZE03 [CrossRef][PubMed]
-
17. Sandur SK, Pandey MK, Sung B, Ahn KS, Murakami A et al. Curcumin, demethoxycurcumin, bisdemethoxycurcumin, tetrahydrocurcumin and turmerones differentially regulate anti-inflammatory and anti-proliferative responses through a ROS-independent mechanism. Carcinogenesis 2007;28:1765–1773 [CrossRef][PubMed]
-
18. Prakash P, Misra A, Surin WR, Jain M, Bhatta RS et al. Anti-platelet effects of curcuma oil in experimental models of myocardial ischemia-reperfusion and thrombosis. Thromb Res 2011;127:111–118 [CrossRef][PubMed]
-
19. Mun SH, Joung DK, Kim YS, Kang OH, Kim SB et al. Synergistic antibacterial effect of curcumin against methicillin-resistant Staphylococcus aureus. Phytomedicine 2013;20:714–718 [CrossRef][PubMed]
-
20. Sharma G, Raturi K, Dang S, Gupta S, Gabrani R. Combinatorial antimicrobial effect of curcumin with selected phytochemicals on Staphylococcus epidermidis. J Asian Nat Prod Res 2014;16:535–541 [CrossRef][PubMed]
-
21. Moghadamtousi SZ, Kadir HA, Hassandarvish P, Tajik H, Abubakar S et al. A review on antibacterial, antiviral, and antifungal activity of curcumin. Biomed Res Int 2014;2014:186864 [CrossRef][PubMed]
-
22. Neelofar K, Shreaz S, Rimple B, Muralidhar S, Nikhat M et al. Curcumin as a promising anticandidal of clinical interest. Can J Microbiol 2011;57:204–210 [CrossRef][PubMed]
-
23. Changtam C, Hongmanee P, Suksamrarn A. Isoxazole analogs of curcuminoids with highly potent multidrug-resistant antimycobacterial activity. Eur J Med Chem 2010;45:4446–4457 [CrossRef][PubMed]
-
24. Sahoo BK, Ghosh KS, Bera R, Dasgupta S. Studies on the interaction of diacetylcurcumin with calf thymus-DNA. Chem Phys 2008;351:163–169 [CrossRef]
-
25. Scorzoni L, Benaducci T, Almeida AMF, Silva DHS, Bolzani Vdas et al. The use of standard methodology for determination of antifungal activity of natural products against medical yeasts Candida sp. and Cryptococcus sp. Braz J Microbiol 2007;38:391–397 [CrossRef]
-
26. CLSI. Reference Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standard, 9th edn, M07-A9 Wayne, PA: Clinical and Laboratory Standards Institute; 2012;. p.70.
-
27. Sardi JC, Duque C, Mariano FS, Marques MR, Höfling JF et al. Adhesion and invasion of Candida albicans from periodontal pockets of patients with chronic periodontitis and diabetes to gingival human fibroblasts. Med Mycol 2012;50:43–49 [CrossRef][PubMed]
-
28. Limsuwan S, Homlaead S, Watcharakul S, Chusri S, Moosigapong K et al. Inhibition of microbial adhesion to plastic surface and human buccal epithelial cells by Rhodomyrtus tomentosa leaf extract. Arch Oral Biol 2014;59:1256–1265 [CrossRef][PubMed]
-
29. Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 2007;115:891–899 [CrossRef][PubMed]
-
30. Ibarra-Trujillo C, Villar-Vidal M, Gaitán-Cepeda LA, Pozos-Guillen A, Mendoza-de Elias R et al. Formation and quantification assay of Candida albicans and Staphylococcus aureus mixed biofilm. Rev Iberoam Micol 2012;29:214–222 (in Spanish) [CrossRef][PubMed]
-
31. Freires Ide A, Murata RM, Furletti VF, Sartoratto A, Alencar SM et al. Coriandrum sativum L. (coriander) essential oil: antifungal activity and mode of action on Candida spp., and molecular targets affected in human whole-genome expression. PLoS One 2014;9:e99086 [CrossRef][PubMed]
-
32. Megaw J, Thompson TP, Lafferty RA, Gilmore BF. Galleria mellonella as a novel in vivo model for assessment of the toxicity of 1-alkyl-3-methylimidazolium chloride ionic liquids. Chemosphere 2015;139:197–201 [CrossRef][PubMed]
-
33. Pathare NA, Tejani S, Asogan H, Al Mahruqi G, Al Fakhri S et al. Comparison of methicillin resistant Staphylococcus aureus in healthy community hospital visitors (CA-MRSA) and hospital staff (HA-MRSA). Mediterr J Hematol Infect Dis 2015;7:e2015053 [CrossRef][PubMed]
-
34. Liu C, Bayer A, Cosgrove SE, Daum RS, Fridkin SK et al. Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children: executive summary. Clin Infect Dis 2011;52:285–292 [CrossRef][PubMed]
-
35. Pizarro-Cerdá J, Cossart P. Bacterial adhesion and entry into host cells. Cell 2006;124:715–727 [CrossRef][PubMed]
-
36. Conrady DG, Brescia CC, Horii K, Weiss AA, Hassett DJ et al. A zinc-dependent adhesion module is responsible for intercellular adhesion in staphylococcal biofilms. Proc Natl Acad Sci USA 2008;105:19456–19461 [CrossRef][PubMed]
-
37. Mun SH, Kim SB, Kong R, Choi JG, Kim YC et al. Curcumin reverse methicillin resistance in Staphylococcus aureus. Molecules 2014;19:18283–18295 [CrossRef][PubMed]
-
38. Marasini BP, Baral P, Aryal P, Ghimire KR, Neupane S et al. Evaluation of antibacterial activity of some traditionally used medicinal plants against human pathogenic bacteria. Biomed Res Int 2015;2015:265425 [CrossRef][PubMed]
-
39. Afrose R, Saha SK, Banu LA, Ahmed AU, Shahidullah AS et al. Antibacterial effect of Curcuma longa (turmeric) against Staphylococcus aureus and Escherichia coli. Mymensingh Med J 2015;24:506–515[PubMed]
-
40. Mishra S, Narain U, Mishra R, Misra K. Design, development and synthesis of mixed bioconjugates of piperic acid–glycine, curcumin–glycine/alanine and curcumin–glycine–piperic acid and their antibacterial and antifungal properties. Bioorg Med Chem 2005;13:1477–1486 [CrossRef][PubMed]
-
41. Ettmayer P, Amidon GL, Clement B, Testa B. Lessons learned from marketed and investigational prodrugs. J Med Chem 2004;47:2393–2404 [CrossRef][PubMed]
-
42. Rautio J, Kumpulainen H, Heimbach T, Oliyai R, Oh D et al. Prodrugs: design and clinical applications. Nat Rev Drug Discov 2008;7:255–270 [CrossRef][PubMed]
-
43. Teow SY, Liew K, Ali SA, Khoo AS, Peh SC. Antibacterial action of curcumin against Staphylococcus aureus: a brief review. J Trop Med 2016;2016:2853045 [CrossRef][PubMed]
-
44. Girard LP, Ceri H, Gibb AP, Olson M, Sepandj F. MIC versus MBEC to determine the antibiotic sensitivity of Staphylococcus aureus in peritoneal dialysis peritonitis. Perit Dial Int 2010;30:652–656 [CrossRef][PubMed]
-
45. Howlin RP, Brayford MJ, Webb JS, Cooper JJ, Aiken SS et al. Antibiotic-loaded synthetic calcium sulfate beads for prevention of bacterial colonization and biofilm formation in periprosthetic infections. Antimicrob Agents Chemother 2015;59:111–120 [CrossRef][PubMed]
-
46. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999;284:1318–1322 [CrossRef][PubMed]
-
47. Brilhante RS, de Lima RA, Marques FJ, Silva NF, Caetano ÉP et al. Histoplasma capsulatum in planktonic and biofilm forms: in vitro susceptibility to amphotericin B, itraconazole and farnesol. J Med Microbiol 2015;64:394–399 [CrossRef][PubMed]
-
48. Sardi J D, Pitangui N D, Rodríguez-Arellanes G, Taylor ML, Fusco-Almeida AM et al. Highlights in pathogenic fungal biofilms. Rev Iberoam Micol 2014;31:22–29 [CrossRef][PubMed]
-
49. Manner S, Vahermo M, Skogman ME, Krogerus S, Vuorela PM et al. New derivatives of dehydroabietic acid target planktonic and biofilm bacteria in Staphylococcus aureus and effectively disrupt bacterial membrane integrity. Eur J Med Chem 2015;102:68–79 [CrossRef][PubMed]
-
50. Freires IA, Sardi JC, de Castro RD, Rosalen PL. Alternative animal and non-animal models for drug discovery and development: bonus or burden?. Pharm Res 2017;34:681–686 [CrossRef][PubMed]

Supplementary Data
Data loading....

Article metrics loading...

Full text loading...
Author and Article Information
-
This Journal
/content/journal/jmm/10.1099/jmm.0.000494dcterms_title,dcterms_subject,pub_serialTitlepub_serialIdent:journal/jmm AND -contentType:BlogPost104 -
Other Society Journals
/content/journal/jmm/10.1099/jmm.0.000494dcterms_title,dcterms_subject-pub_serialIdent:journal/jmm AND -contentType:BlogPost104 -
PubMed
-
Google Scholar
Figure data loading....