Tannic acid inhibits staphylococcus aureus surface colonization in an isaA-dependent manner

Infection and Immunity

Volumn 81, Issue 2, 2013, Pages 496-504

  Payne, David E ^a   Martin, Nicholas R ^a   Parzych, Katherine R ^a   Rickard, Alex H ^a   Underwood, Adam ^a   Boles, Blaise R ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLTRANSFERASE; TANNIN;

ANIMAL MODEL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BIOFILM; CATALYSIS; CELL GROWTH; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENOTYPE; GROWTH; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MILK; MOLECULAR LIBRARY; NONHUMAN; OROPHARYNX; PHARYNGITIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STAPHYLOCOCCUS INFECTION; TEA;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BIOFILMS; CATALYTIC DOMAIN; FEMALE; RATS; SIGMODONTINAE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TANNINS; TEA;

EID: 84873034894     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00877-12     Document Type: Article

References (55)

1. Acton DS, Plat-Sinnige MJ, van Wamel W, de Groot N, van Belkum A. 2009. Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact? Eur. J. Clin. Microbiol. Infect. Dis. 28:115-127.
2. Lee CJ, Sankaran S, Mukherjee DV, Apa ZL, Hafer CA, Wright L, Larson EL, Lowy FD. 2011. Staphylococcus aureus oropharyngeal carriage in a prison population. Clin. Infect. Dis. 52:775-778.
3. Peters PJ, Brooks JT, Limbago B, Lowery HK, McAllister SK, Mindley R, Fosheim G, Gorwitz RJ, Guest JL, Hageman J, Fridge J, Rimland D. 2010. Methicillin-resistant Staphylococcus aureus colonization in HIVinfected outpatients is common and detection is enhanced by groin culture. Epidemiol. Infect., p 1-11.
4. Parsek MR, Singh PK. 2003. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57:677-701.
5. Schwartz K, Syed AK, Stephenson RE, Rickard AH, Boles BR. 2012. Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms. PLoS Pathog. 8:e1002744. doi:10.1371 /journal.ppat.1002744.
6. Boles BR, Horswill AR. 2011. Staphylococcal biofilm disassembly. Trends Microbiol. 19:449-455.
7. Zuluaga AF, Galvis W, Saldarriaga JG, Agudelo M, Salazar BE, Vesga O. 2006. Etiologic diagnosis of chronic osteomyelitis: a prospective study. Arch. Intern. Med. 166:95-100.
8. Fowler VG, Jr, Miro JM, Hoen B, Cabell CH, Abrutyn E, Rubinstein E, Corey GR, Spelman D, Bradley SF, Barsic B, Pappas PA, Anstrom KJ, Wray D, Fortes CQ, Anguera I, Athan E, Jones P, van der Meer JT, Elliott TS, Levine DP, Bayer AS. 2005. Staphylococcus aureus endocarditis: a consequence of medical progress. JAMA 293:3012-3021.
9. Gomez-Barrena E, Esteban J, Medel F, Molina-Manso D, Ortiz-Perez A, Cordero-Ampuero J, Puertolas JA. 2012. Bacterial adherence to separated modular components in joint prosthesis: a clinical study. J. Orthop. Res. 30:1634 -1639.
10. del Pozo JL, Patel R. 2007. The challenge of treating biofilm-associated bacterial infections. Clin. Pharmacol. Ther. 82:204 -209.
11. Boles BR, Horswill AR. 2008. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4:e1000052. doi:10.1371/journal.ppat .1000052.
12. Gotz F. 2002. Staphylococcus and biofilms. Mol. Microbiol. 43:1367- 1378.
13. Pynnonen M, Stephenson RE, Schwartz K, Hernandez M, Boles BR. 2011. Hemoglobin promotes Staphylococcus aureus nasal colonization. PLoS Pathog. 7:e1002104. doi:10.1371/journal.ppat.1002104.
14. Lorenz U, Ohlsen K, Karch H, Hecker M, Thiede A, Hacker J. 2000. Human antibody response during sepsis against targets expressed by methicillin resistant Staphylococcus aureus. FEMS Immunol. Med. Microbiol. 29:145-153.
15. Stapleton MR, Horsburgh MJ, Hayhurst EJ, Wright L, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ. 2007. Characterization of IsaA and SceD, two putative lytic transglycosylases of Staphylococcus aureus. J. Bacteriol. 189:7316 -7325.
16. Holtje JV, Mirelman D, Sharon N, Schwarz U. 1975. Novel type of murein transglycosylase in Escherichia coli. J. Bacteriol. 124:1067-1076.
17. Bateman BT, Donegan NP, Jarry TM, Palma M, Cheung AL. 2001. Evaluation of a tetracycline-inducible promoter in Staphylococcus aureus in vitro and in vivo and its application in demonstrating the role of sigB in microcolony formation. Infect. Immun. 69:7851-7857.
18. Duthie ES, Lorenz LL. 1952. Staphylococcal coagulase; mode of action and antigenicity. J. Gen. Microbiol. 6:95-107.
19. Peng HL, Novick RP, Kreiswirth B, Kornblum J, Schlievert P. 1988. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol. 170:4365- 4372.
20. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J. 12:3967-3975.
21. Reiser RF, Hinzman SJ, Bergdoll MS. 1987. Production of toxic shock syndrome toxin 1 by Staphylococcus aureus restricted to endogenous air in tampons. J. Clin. Microbiol. 25:1450 -1452.
22. CDC. 1999. Four pediatric deaths from community-acquired methicillinresistant Staphylococcus aureus-Minnesota and North Dakota, 1997- 1999. MMWR Morb. Mortal. Wkly. Rep. 48:707-710.
23. Voyich JM, Braughton KR, Sturdevant DE, Whitney AR, Said-Salim B, Porcella SF, Long RD, Dorward DW, Gardner DJ, Kreiswirth BN, Musser JM, DeLeo FR. 2005. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175:3907-3919.
24. Gillaspy AF, Hickmon SG, Skinner RA, Thomas JR, Nelson CL, Smeltzer MS. 1995. Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect. Immun. 63:3373-3380.
25. Husmann LK, Yung DL, Hollingshead SK, Scott JR. 1997. Role of putative virulence factors of Streptococcus pyogenes in mouse models of long-term throat colonization and pneumonia. Infect. Immun. 65:1422- 1430.
26. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academies Press, Washington, DC.
27. Nurjadi D, Lependu J, Kremsner PG, Zanger P. 2012. Staphylococcus aureus throat carriage is associated with ABO-/secretor status. J. Infect. 65:310 -317.
28. Ohara-Nemoto Y, Haraga H, Kimura S, Nemoto TK. 2008. Occurrence of staphylococci in the oral cavities of healthy adults and nasal oral trafficking of the bacteria. J. Med. Microbiol. 57:95-99.
29. Salminen J-P, Karonen M. 2011. Chemical ecology of tannins and other phenolics: we need a change in approach. Funct. Ecol. 25:325-338.
30. Corrigan RM, Foster TJ. 2009. An improved tetracycline-inducible expression vector for Staphylococcus aureus. Plasmid 61:126 -129.
31. Blackburn NT, Clarke AJ. 2001. Identification of four families of peptidoglycan lytic transglycosylases. J. Mol. Evol. 52:78-84.
32. Thunnissen AM, Dijkstra AJ, Kalk KH, Rozeboom HJ, Engel H, Keck W, Dijkstra BW. 1994. Doughnut-shaped structure of a bacterial muramidase revealed by X-ray crystallography. Nature 367:750 -753.
33. Monteiro C, Fang X, Ahmad I, Gomelsky M, Romling U. 2011. Regulation of biofilm components in Salmonella enterica serovar Typhimurium by lytic transglycosylases involved in cell wall turnover. J. Bacteriol. 193:6443- 6451.
34. Haslam E, Lilley TH, Cai Y, Martin R, Magnolato D. 1989. Traditional herbal medicines-the role of polyphenols. Planta Med. 55:1- 8.
35. Scalbert A. 1991. Antimicrobial properties of tannins. Phytochemistry 30:3875-3883.
36. Bandyopadhyay P, Ghosh AK, Ghosh C. 2012. Recent developments on polyphenol-protein interactions: effects on tea and coffee taste, antioxidant properties and the digestive system. Food Funct. 3:592- 605.
37. Vidal S, Francis L, Noble A, Kwiatkowski M, Cheynier V, Waters E. 2004. Taste and mouth-feel properties of different types of tannin-like polyphenolic compounds and anthocyanins in wine. Anal. Chim. Acta 513:57- 65.
38. Thomas AW, Frieden A. 1923. The gelatin-tannin reaction. Ind. Eng. Chem. 15:839-841.
39. Anderson RA, Polansky MM. 2002. Tea enhances insulin activity. J. Agric. Food Chem. 50:7182-7186.
40. Morton JF. 1979. Tea with milk. Science 204:909.
41. Kokai-Kun JF. 2008. The cotton rat as a model for Staphylococcus aureus nasal colonization in humans: cotton rat S. aureus nasal colonization model. Methods Mol. Biol. 431:241-254.
42. Henis Y, Volcani R, Tagari H. 1964. Effect of water extracts of carob pods, tannic acid, and their derivatives on morphology and growth of microorganisms. Appl. Microbiol. 12:204 -209.
43. Quan S, Koldewey P, Tapley T, Kirsch N, Ruane KM, Pfizenmaier J, Shi R, Hofmann S, Foit L, Ren G, Jakob U, Xu Z, Cygler M, Bardwell JC. 2011. Genetic selection designed to stabilize proteins uncovers a chaperone called Spy. Nat. Struct. Mol. Biol. 18:262-269.
44. Zoetendal EG, Smith AH, Sundset MA, Mackie RI. 2008. The BaeSR two-component regulatory system mediates resistance to condensed tannins in Escherichia coli. Appl. Environ. Microbiol. 74:535-539.
45. Chusri S, Phatthalung PN, Voravuthikunchai SP. 2012. Anti-biofilm activity of Quercus infectoria G. Olivier against methicillin-resistant Staphylococcus aureus. Lett. Appl. Microbiol. 54:511-517.
46. Lin MH, Chang FR, Hua MY, Wu YC, Liu ST. 2011. Inhibitory effects of 1, 2, 3, 4, 6-penta-O-galloyl-beta-D-glucopyranose on biofilm formation by Staphylococcus aureus. Antimicrob. Agents Chemother. 55:1021- 1027.
47. Quave CL, Estevez-Carmona M, Compadre CM, Hobby G, Hendrickson H, Beenken KE, Smeltzer MS. 2012. Ellagic acid derivatives from Rubus ulmifolius inhibit Staphylococcus aureus biofilm formation and improve response to antibiotics. PLoS One 7:e28737. doi:10.1371/journal .pone.0028737.
48. Scheurwater E, Reid CW, Clarke AJ. 2008. Lytic transglycosylases: bacterial space-making autolysins. Int. J. Biochem. Cell Biol. 40:586 -591.
49. Shah IM, Laaberki MH, Popham DL, Dworkin J. 2008. A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135:486-496.
50. Munoz P, Hortal J, Giannella M, Barrio JM, Rodriguez-Creixems M, Perez MJ, Rincon C, Bouza E. 2008. Nasal carriage of S. aureus increases the risk of surgical site infection after major heart surgery. J. Hosp. Infect. 68:25-31.
51. Stanaway S, Johnson D, Moulik P, Gill G. 2007. Methicillin-resistant Staphylococcus aureus (MRSA) isolation from diabetic foot ulcers correlates with nasal MRSA carriage. Diabetes Res. Clin. Pract. 75:47-50.
52. von Eiff C, Becker K, Machka K, Stammer H, Peters G. 2001. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N. Engl. J. Med. 344:11-16.
53. Wertheim HF, Vos MC, Ott A, van Belkum A, Voss A, Kluytmans JA, van Keulen PH, Vandenbroucke-Grauls CM, Meester MH, Verbrugh HA. 2004. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364:703-705.
54. Lee BY, Bailey RR, Smith KJ, Muder RR, Strotmeyer ES, Lewis GJ, Ufberg PJ, Song Y, Harrison LH. 2010. Universal methicillin-resistant Staphylococcus aureus (MRSA) surveillance for adults at hospital admission: an economic model and analysis. Infect. Control Hosp. Epidemiol. 31:598-606.
55. Matheson EM, Mainous AG, III, Everett CJ, King DE. 2011. Tea and coffee consumption and MRSA nasal carriage. Ann. Fam. Med. 9:299- 304.