Wall teichoic acid protects Staphylococcus aureus from inhibition by Congo red and other dyes

Journal of Antimicrobial Chemotherapy

Volumn 67, Issue 9, 2012, Pages 2143-2151

  Suzuki, Takashi ^a   Campbell, Jennifer ^a   Kim, Younghoon ^b   Swoboda, Jonathan G ^a   Mylonakis, Eleftherios ^c   Walker, Suzanne ^a   Gilmore, Michael S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Chonbuk National University   (South Korea)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Antibiotics; Bacteria; S. aureus

Indexed keywords

AZO DYE; CONGO RED; TEICHOIC ACID; TUNICAMYCIN; UNCLASSIFIED DRUG; WALL TEICHOIC ACID;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; CAENORHABDITIS ELEGANS; CATALYSIS; CELL PROTECTION; CONTROLLED STUDY; DRUG PENETRATION; DRUG POTENTIATION; DRUG SYNTHESIS; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MINIMUM INHIBITORY CONCENTRATION; MUTATION; NONHUMAN; SENSITIZATION; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; AZO COMPOUNDS; CELL WALL; CONGO RED; HUMANS; MICROBIAL SENSITIVITY TESTS; STAPHYLOCOCCUS AUREUS; TEICHOIC ACIDS;

EID: 84865352241     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dks184     Document Type: Article

References (51)

1. Fridkin SK, Hageman JC, Morrison M et al. Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med 2005; 352: 1436-44.
2. Tenover FC, Goering RV. Methicillin-resistant Staphylococcus aureus strain USA300: origin and epidemiology. J Antimicrob Chemother 2009; 64: 441-6.
3. Neuhaus FC, Baddiley J. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 2003; 67: 686-723.
4. Swoboda JG, Campbell J, Meredith TC et al. Wall teichoic acid function, biosynthesis, and inhibition. Chembiochem 2010; 11: 35-45.
5. Suzuki T, Campbell J, Swoboda JG et al. Role of wall teichoic acids in Staphylococcus aureus endophthalmitis. Invest Ophthalmol Vis Sci 2011; 52: 3187-92.
6. Suzuki T, Swoboda JG, Campbell J et al. In vitro antimicrobial activity of wall teichoic acid biosynthesis inhibitors against Staphylococcus aureus isolates. Antimicrob Agents Chemother 2011; 55: 767-74.
7. Weidenmaier C, Kokai-Kun JF, Kristian SA et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 2004; 10: 243-5.
8. Weidenmaier C, Kokai-Kun JF, Kulauzovic E et al. Differential roles of sortase-anchored surface proteins and wall teichoic acid in Staphylococcus aureus nasal colonization. Int J Med Microbiol 2008; 298: 505-13.
9. Weidenmaier C, Peschel A. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 2008; 6: 276-87.
10. Weidenmaier C, Peschel A, Xiong YQ et al. Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 2005; 191: 1771-7.
11. Brown S, Zhang YH, Walker S. A revised pathway proposed for Staphylococcus aureus wall teichoic acid biosynthesis based on in vitro reconstitution of the intracellular steps. Chem Biol 2008; 15: 12-21.
12. Meredith TC, Swoboda JG, Walker S. Late-stage polyribitol phosphate wall teichoic acid biosynthesis in Staphylococcus aureus. J Bacteriol 2008; 190: 3046-56.
13. D'Elia MA, Pereira MP, Chung YS et al. Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal gain of function in the otherwise dispensable pathway. J Bacteriol 2006; 188: 4183-9.
14. Fournier B, Philpott D. Recognition of Staphylococcus aureus by the innate immune system. Clin Microbiol Rev 2005; 18: 521-40.
15. Grundling A, Schneewind O. Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus. Proc Natl Acad Sci USA 2007; 104: 8478-83.
16. Chiu T, Arnold B, Kim S et al. Phosphatidyl glycerolphosphate serves as glycerolphosphate donor in polymer synthesis. Biochem Biophys Res Commun 1985; 128: 906-12.
17. Koch HU, Haas R, Fischer W. The role of lipoteichoic acid biosynthesis in membrane lipid metabolism of growing Staphylococcus aureus. Eur J Biochem 1984; 138: 357-63.
18. Oku Y, Kurokawa K, Matsuo M et al. Pleiotropic roles of polyglycerolphosphate synthase of lipoteichoic acid in growth of Staphylococcus aureus cells. J Bacteriol 2009; 191: 141-51.
19. Moller P, Wallin H. Genotoxic hazards of azo pigments and other colorants related to 1-phenylazo-2-hydroxynaphthalene. Mutat Res 2000; 462: 13-30.
20. Frid P, Anisimov SV, Popovic N. Congo red and protein aggregation in neurodegenerative diseases. Brain Res Rev 2007; 53: 135-60.
21. Freeman DJ, Falkiner FR, Keane CT. New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 1989; 42: 872-4.
22. Ziebuhr W, Heilmann C, Gotz F et al. Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun 1997; 65: 890-6.
23. Lee K, Campbell J, Swoboda JG et al. Development of improved inhibitors of wall teichoic acid biosynthesis with potent activity against Staphylococcus aureus. Bioorg Med Chem Lett 2010; 20: 1767-70.
24. Swoboda JG, Meredith TC, Campbell J et al. Discovery of a small molecule that blocks wall teichoic acid biosynthesis in Staphylococcus aureus. ACS Chem Biol 2009; 4: 875-83.
25. Hubscher J, McCallum N, Sifri CD et al. MsrR contributes to cell surface characteristics and virulence in Staphylococcus aureus. FEMS Microbiol Lett 2009; 295: 251-60.
26. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Sixteenth Informational Supplement M100-S16. CLSI, Wayne, PA, USA, 2006.
27. Lorian V. Antibiotics in Laboratory Medicine. 4th edn. Baltimore, MD: Williams & Wilkins Co., 1996.
28. Breger J, Fuchs BB, Aperis G et al. Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLoS Pathog 2007; 3: e18.
29. Miyata S, Begun J, Troemel ER et al. DAF-16-dependent suppression of immunity during reproduction in Caenorhabditis elegans. Genetics 2008; 178: 903-18.
30. Kim DH, Feinbaum R, Alloing G et al. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 2002; 297: 623-6.
31. Peng HL, Novick RP, Kreiswirth B et al. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol 1988; 170: 4365-72.
32. Koprivnjak T, Weidenmaier C, Peschel A et al. Wall teichoic acid deficiency in Staphylococcus aureus confers selective resistance to mammalian group IIA phospholipase A2 and human b-defensin 3. Infect Immun 2008; 76: 2169-76.
33. Price NP, Tsvetanova B. Biosynthesis of the tunicamycins: a review. J Antibiot (Tokyo) 2007; 60: 485-91.
34. Garsin DA, Sifri CD, Mylonakis E et al. A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci USA 2001; 98: 10892-7.
35. Moy TI, Ball AR, Anklesaria Z et al. Identification of novel antimicrobials using a live-animal infection model. Proc Natl Acad Sci USA 2006; 103: 10414-9.
36. Morin MJ, Bernacki RJ. Biochemical effects and therapeutic potential of tunicamycin in murine L1210 leukemia. Cancer Res 1983; 43: 1669-74.
37. Wood PJ. Specificity in the interaction of direct dyes with polysaccharides. Carb Res 1980; 85: 271-87.
38. Herth W. Calcofluor white and Congo red inhibit chitin microfibril assembly of Poterioochromonas: evidence for a gap between polymerization and microfibril formation. J Cell Biol 1980; 87: 442-50.
39. Roncero C, Duran A. Effect of calcofluor white and Congo red on fungal cell wall morphogenesis: in vivo activation of chitin polymerization. J Bacteriol 1985; 163: 1180-5.
40. Vannini GL, Poli P, Donini A et al. Effects of Congo red on wall synthesis and morphogenesis in Saccharomyces cerevisiae. Plant Sci Lett 1983; 31: 9-17.
41. Damveld RA, Arentshorst M, Franken A et al. The Aspergillus niger MADS-box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress. Mol Microbiol 2005; 58: 305-19.
42. Damveld RA, vanKuyk PA, Arentshorst M et al. Expression of agsA, one of five 1,3-a-D-glucan synthase-encoding genes in Aspergillus niger, is induced in response to cell wall stress. Fungal Genet Biol 2005; 42: 165-77.
43. Pancaldi S, Poli F, Dall'Olio G et al. Morphological anomalies induced by Congo red in Aspergillus niger. Arch Microbiol 1984; 137: 185-7.
44. Levin DE. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 2005; 69: 262-91.
45. Campbell J, Singh AK, Santa Maria JP Jr et al. Synthetic lethal compound combinations reveal a fundamental connection between wall teichoic acid and peptidoglycan biosyntheses in Staphylococcus aureus. ACS Chem Biol 2011; 6: 106-16.
46. McKay G, Otterburn MS, Aga DA. Fuller's earth and fired clay as adsorbent for dye stuffs. Equilibrium and rate constants. Water Air Soil Pollut 1985; 24: 307-22.
47. Sanchez I, Mahlke C, Yuan J. Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Nature 2003; 421: 373-9.
48. Kreiswirth BN, Lofdahl S, Betley MJ et al. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 1983; 305: 709-12.
49. Duthie ES, Lorenz LL. Staphylococcal coagulase: mode of action and antigenicity. J Gen Microbiol 1952; 6: 95-107.
50. Grundling A, Schneewind O. Cross-linked peptidoglycan mediates lysostaphin binding to the cell wall envelope of Staphylococcus aureus. J Bacteriol 2006; 188: 2463-72.
51. Chang S, Sievert DM, Hageman JC et al. Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N Engl J Med 2003; 348: 1342-7.