Antiadhesion agents against Gram-positive pathogens

Future Microbiology

Volumn 9, Issue 10, 2014, Pages 1209-1220

  Cascioferro, Stella ^a   Cusimano, Maria Grazia ^a   Schillaci, Domenico ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

Antiadhesion agents; Antivirulence drugs; Gram positive pathogens

Indexed keywords

ACYLTRANSFERASE INHIBITOR; ADHESIN; ANTIADHESION AGENT; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; CARBOHYDRATE; LIPOTEICHOIC ACID; LIPOTEICHOIC ACID INHIBITOR; MOLECULE TRANSPORT AGENT; NATURAL PRODUCT; PROTEIN; SMALL SYNTHETIC MOLECULE; SORTASE; SORTASE A; SORTASE A INHIBITOR; TEICHOIC ACID; UNCLASSIFIED DRUG; WALL TEICHOIC ACID INHIBITOR; ANTIINFECTIVE AGENT;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CARBOHYDRATE ANALYSIS; GRAM POSITIVE BACTERIUM; HOST PATHOGEN INTERACTION; HUMAN; NONHUMAN; PATHOGENESIS; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN TARGETING; REVIEW; TARA GENE; TARO GENE; DRUG DEVELOPMENT; DRUG EFFECTS; ISOLATION AND PURIFICATION; PHYSIOLOGY; PROCEDURES; TRENDS;

POSIBACTERIA;

ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; DRUG DISCOVERY; GRAM-POSITIVE BACTERIA;

EID: 84911480620     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/FMB.14.56     Document Type: Review

References (97)

1. WHO. Antimicrobial resistance: global report on surveillance 2014. WHO World Health Organistaion
2. Fitzgerald-Hughes D, Devocelle M, Humphreys H. Beyond conventional antibiotics for the future treatment of methicillin-resistant Staphylococcus aureus infections: two novel alternatives. FEMS Immunol. Med. Microbiol. 65(3), 399-412 (2012).
3. Rasko DA, Sperandio V. Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. Drug Discov. 9(2), 117-128 (2010).
4. Cozens D, Read RC. Anti-adhesion methods as novel therapeutics for bacterial infections. Expert Rev. Anti Infect. Ther. 10(12), 1457-1468 (2012).
5. Brumbaugh AR, Mobley HLT. Preventing urinary tract infection: progress toward an effective Escherichia coli vaccine. Expert Rev. Vaccines 11(6), 663-676 (2012).
6. Maresso AW, Schneewind O. Sortase as a target of anti-infective therapy. Pharmacol. Rev. 60(1), 128-141 (2008).
7. Dodson KW, Pinkner JS, Rose T, Magnusson G, Hultgren SJ, Waksman G. Structural basis of the interaction of the pyelonephritic E. coli adhesin to its human kidney receptor. Cell 105(6), 733-743 (2001).
8. Linke-Winnebeck C, Paterson NG, Young PG et al. Structural model for covalent adhesion of the Streptococcuspyogenes pilus through a thioester bond. J. Biol. Chem. 289(1), 177-189 (2014).
9. Comfort D, Clubb RT. A comparative genome analysis identifies distinct sorting pathways in Gram-positive bacteria. Infect. Immun. 72(5), 2710-2722 (2004).
10. Ton-That H, Schneewind O. Assembly of pili on the surface of Corynebacterium diphtheriae. Mol. Microbiol. 50(4), 1429-1438 (2003).
11. Linke C, Young PG, Kang HJ et al. Crystal structure of the minor pilin FctB reveals determinants of Group A streptococcal pilus anchoring. J. Biol. Chem. 285(26), 20381-20389 (2010).
12. Nielsen HV, Flores-Mireles AL, Kau AL et al. Pilin and sortase residues critical for endocarditis- and biofilm-associated pilus biogenesis in Enterococcus faecalis. J. Bacteriol. 195(19), 4484-4495 (2013).
13. Vengadesan K, Narayana SVL. Structural biology of Gram-positive bacterial adhesins. Protein Sci. Publ. Protein Soc. 20(5), 759-772 (2011).
14. Krishnan V, Narayana SVL. Crystallography of Gram-positive bacterial adhesins. Adv. Exp. Med. Biol. 715, 175-195 (2011).
15. Perry AM, Ton-That H, Mazmanian SK, Schneewind O. Anchoring of surface proteins to the cell wall of Staphylococcus aureus. III. Lipid II is an in vivo peptidoglycan substrate for sortase-catalyzed surface protein anchoring. J. Biol. Chem. 277(18), 16241-16248 (2002).
16. Nandakumar R, Nandakumar MP, Marten MR, Ross JM. Proteome analysis of membrane and cell wall associated proteins from Staphylococcus aureus. J. Proteome Res. 4(2), 250-257 (2005).
17. Bowden MG, Heuck AP, Ponnuraj K et al. Evidence for the 'dock, lock, and latch' ligand binding mechanism of the staphylococcal microbial surface component recognizing adhesive matrix molecules (MSCRAMM) SdrG. J. Biol. Chem. 283(1), 638-647 (2008).
18. Chhatwal GS. Anchorless adhesins and invasins of Gram-positive bacteria: a new class of virulence factors. Trends Microbiol. 10(5), 205-208 (2002).
19. Holmes AR, McNab R, Millsap KW et al. The pavA gene of Streptococcus pneumoniae encodes a fibronectin-binding protein that is essential for virulence. Mol. Microbiol. 41(6), 1395-1408 (2001).
20. Torelli R, Serror P, Bugli F et al. The PavA-like fibronectin-binding protein of Enterococcus faecalis, EfbA, is important for virulence in a mouse model of ascending urinary tract infection. J. Infect. Dis. 206(6), 952-960 (2012).
21. Swoboda JG, Campbell J, Meredith TC, Walker S. Wall teichoic acid function, biosynthesis, and inhibition. Chembiochem 11(1), 35-45 (2010).
22. Koyama N, Inokoshi J, Tomoda H. Anti-infectious agents against MRSA. Molecules. 18(1), 204-224 (2012).
23. Campbell J, Singh AK, Swoboda JG, Gilmore MS, Wilkinson BJ, Walker S. An antibiotic that inhibits a late step in wall teichoic acid biosynthesis induces the cell wall stress stimulon in Staphylococcus aureus. Antimicrob. Agents Chemother. 56(4), 1810-1820 (2012).
24. Suzuki T, Swoboda JG, Campbell J, Walker S, Gilmore MS. In vitro antimicrobial activity of wall teichoic acid biosynthesis inhibitors against Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 55(2), 767-774 (2011).
25. D'Elia MA, Millar KE, Beveridge TJ, Brown ED. Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J. Bacteriol. 188(23), 8313-8316 (2006).
26. 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. 10(3), 243-245 (2004).
27. Burian M, Rautenberg M, Kohler T et al. Temporal expression of adhesion factors and activity of global regulators during establishment of Staphylococcus aureus nasal colonization. J. Infect. Dis. 201(9), 1414-1421 (2010).
28. Weidenmaier C, Peschel A, Xiong Y-Q 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. 191(10), 1771-1777 (2005).
29. 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. IJMM. 298(5-6), 505-513 (2008).
30. Edwards AM, Massey RC, Clarke SR. Molecular mechanisms of Staphylococcus aureus nasopharyngeal colonization. Mol. Oral Microbiol. 27(1), 1-10 (2012).
31. Kiriukhin MY, Debabov DV, Shinabarger DL, Neuhaus FC. Biosynthesis of the glycolipid anchor in lipoteichoic acid of Staphylococcus aureus RN4220: role of YpfP, the diglucosyldiacylglycerol synthase. J. Bacteriol. 183(11), 3506-3514 (2001).
32. Gründling A, Schneewind O. Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus. J. Bacteriol. 189(6), 2521-2530 (2007).
33. Peschel A, Vuong C, Otto M, Götz F. The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob. Agents Chemother. 44(10), 2845-2847 (2000).
34. Gründling A, Schneewind O. Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus. Proc. Natl Acad. Sci. USA 104(20), 8478-8483 (2007).
35. Reichmann NT, Cassona CP, Gründling A. Revised mechanism of D-alanine incorporation into cell wall polymers in Gram-positive bacteria. Microbiol. Read. Engl. 159(Pt 9), 1868-1877 (2013).
36. Klemm P, Vejborg RM, Hancock V. Prevention of bacterial adhesion. Appl. Microbiol. Biotechnol. 88(2), 451-459 (2010).
37. Aberg V, Almqvist F. Pilicides - small molecules targeting bacterial virulence. Org. Biomol. Chem. 5(12), 1827-1834 (2007).
38. Chen L, Wen Y. The role of bacterial biofilm in persistent infections and control strategies. Int. J. Oral Sci. 3(2), 66-73 (2011).
39. Mazmanian SK, Liu G, Jensen ER, Lenoy E, Schneewind O. Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc. Natl Acad. Sci. USA 97(10), 5510-5515 (2000).
40. O'Neill E, Pozzi C, Houston P et al. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J. Bacteriol. 190(11), 3835-3850 (2008).
41. Sibbald MJJB, Yang X-M, Tsompanidou E et al. Partially overlapping substrate specificities of staphylococcal group A sortases. Proteomics. 12(19-20), 3049-3062 (2012).
42. Rahman O, Dover LG, Sutcliffe IC. Lipoteichoic acid biosynthesis: two steps forwards, one step sideways? Trends Microbiol. 17(6), 219-225 (2009).
43. Donelli G, Francolini I, Romoli D et al. Synergistic activity of dispersin B and cefamandole nafate in inhibition of staphylococcal biofilm growth on polyurethanes. Antimicrob. Agents Chemother. 51(8), 2733-2740 (2007).
44. Kim S-W, Chang I-M, Oh K-B. Inhibition of the bacterial surface protein anchoring transpeptidase sortase by medicinal plants. Biosci. Biotechnol. Biochem. 66(12), 2751-2754 (2002).
45. Kim S-H, Shin D-S, Oh M-N et al. Inhibition of sortase, a bacterial surface protein anchoring transpeptidase, by beta-sitosterol-3-O-glucopyranoside from Fritillaria verticillata. Biosci. Biotechnol. Biochem. 67(11), 2477-2479 (2003).
46. Huang P, Hu P, Zhou SY, Li Q, Chen WM. Morin inhibits sortase A and subsequent biofilm formation in Streptococcus mutans. Curr. Microbiol. 68(1), 47-52 (2013).
47. Park B-S, Kim J-G, Kim M-R et al. Curcuma longa L. constituents inhibit sortase A and Staphylococcus aureus cell adhesion to fibronectin. J. Agric. Food Chem. 53(23), 9005-9009 (2005).
48. Hu P, Huang P, Chen WM. Curcumin inhibits the sortase A activity of the Streptococcus mutans UA159. Appl. Biochem. Biotechnol. 171(2), 396-402 (2013).
49. Hu P, Huang P, Chen MW. Curcumin reduces Streptococcus mutans biofilm formation by inhibiting sortase A activity. Arch. Oral Biol. 58(10), 1343-1348 (2013).
50. Jenkinson HF, Demuth DR. Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol. Microbiol. 23(2), 183-190 (1997).
51. Kim S-H, Shin D-S, Oh M-N, Chung S-C, Lee J-S, Oh K-B. Inhibition of the bacterial surface protein anchoring transpeptidase sortase by isoquinoline alkaloids. Biosci. Biotechnol. Biochem. 68(2), 421-424 (2004).
52. Oh K-B, Mar W, Kim S et al. Bis(indole) alkaloids as sortase A inhibitors from the sponge Spongosorites sp. Bioorg. Med. Chem. Lett. 15(22), 4927-4931 (2005).
53. Jang KH, Chung S-C, Shin J et al. Aaptamines as sortase A inhibitors from the tropical sponge Aaptos aaptos. Bioorg. Med. Chem. Lett. 17(19), 5366-5369 (2007).
54. Jeon J-E, Na Z, Jung M et al. Discorhabdins from the Korean marine sponge Sceptrella sp. J. Nat. Prod. 73(2), 258-262 (2010).
55. Bae J, Jeon J-E, Lee Y-J et al. Sesterterpenes from the tropical sponge Coscinoderma sp. J. Nat. Prod. 74(8), 1805-1811 (2011).
56. Won TH, Jeon J, Kim S-H et al. Brominated aromatic furanones and related esters from the ascidian Synoicum sp. J. Nat. Prod. 75(12), 2055-2061 (2012).
57. Won TH, Jeon J-E, Lee S-H, Rho BJ, Oh K-B, Shin J. Beta-carboline alkaloids derived from the ascidian Synoicum sp. Bioorg. Med. Chem. 20(13), 4082-4087 (2012).
58. Oh K-B, Kim S-H, Lee J, Cho W-J, Lee T, Kim S. Discovery of diarylacrylonitriles as a novel series of small molecule sortase A inhibitors. J. Med. Chem. 47(10), 2418-2421 (2004).
59. Tian B-X, Eriksson LA. Catalytic mechanism and roles of Arg197 and Thr183 in the Staphylococcus aureus sortase A enzyme. J. Phys. Chem. B 115(44), 13003-13011 (2011).
60. Oh K-B, Nam K-W, Ahn H, Shin J, Kim S, Mar W. Therapeutic effect of (Z)-3-(2,5-dimethoxyphenyl)-2-(4-methoxyphenyl) acrylonitrile (DMMA) against Staphylococcus aureus infection in a murine model. Biochem. Biophys. Res. Commun. 396(2), 440-444 (2010).
61. Oh K-B, Oh M-N, Kim J-G, Shin D-S, Shin J. Inhibition of sortase-mediated Staphylococcus aureus adhesion to fibronectin via fibronectin-binding protein by sortase inhibitors. Appl. Microbiol. Biotechnol. 70(1), 102-106 (2006).
62. Maresso AW, Wu R, Kern JW et al. Activation of inhibitors by sortase triggers irreversible modification of the active site. J. Biol. Chem. 282(32), 23129-23139 (2007).
63. Suree N, Yi SW, Thieu W et al. Discovery and structure-activity relationship analysis of Staphylococcus aureus sortase A inhibitors. Bioorg. Med. Chem. 17(20), 7174-7185 (2009).
64. Barnett TC, Scott JR. Differential recognition of surface proteins in Streptococcuspyogenes by two sortase gene homologs. J. Bacteriol. 184(8), 2181-2191 (2002).
65. 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. 4(10), 875-883 (2009).
66. Koyama N, Tokura Y, Munch D et al. The nonantibiotic small molecule cyslabdan enhances the potency of β-lactams against MRSA by inhibiting pentaglycine interpeptide bridge synthesis. PLoS ONE 7(11), e48981 (2012).
67. Campbell J, Singh AK, Santa Maria JP et al. Synthetic lethal compound combinations reveal a fundamental connection between wall teichoic acid and peptidoglycan biosyntheses in Staphylococcus aureus. ACS Chem. Biol. 6(1), 106-116 (2011).
68. Balibar CJ, Shen X, McGuire D, Yu D, McKenney D, Tao J. cwrA, a gene that specifically responds to cell wall damage in Staphylococcus aureus. Microbiology 156(5), 1372-1383 (2010).
69. Wilkinson BJ, Muthaiyan A, Jayaswal RK. The cell wall stress stimulon of Staphylococcus aureus and other Gram-positive bacteria. Curr. Med. Chem. Anti-Infect. Agents 4(3), 259-276 (2005).
70. Farha MA, Leung A, Sewell EW et al. Inhibition of WTA synthesis blocks the cooperative action of PBPs and sensitizes MRSA to β-lactams. ACS Chem. Biol. 8(1), 226-233 (2013).
71. 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. MMBR 67(4), 686-723 (2003).
72. Koprivnjak T, Mlakar V, Swanson L, Fournier B, Peschel A, Weiss JP. Cation-induced transcriptional regulation of the dlt operon of Staphylococcus aureus. J. Bacteriol. 188(10), 3622-3630 (2006).
73. May JJ, Finking R, Wiegeshoff F et al. Inhibition of the D-alanine: D-alanyl carrier protein ligase from Bacillus subtilis increases the bacterium's susceptibility to antibiotics that target the cell wall. FEBS J. 272(12), 2993-3003 (2005).
74. Richter SG, Elli D, Kim HK et al. Small molecule inhibitor of lipoteichoic acid synthesis is an antibiotic for Gram-positive bacteria. Proc. Natl Acad. Sci. USA 110(9), 3531-3536 (2013).
75. Pieters RJ. Intervention with bacterial adhesion by multivalent carbohydrates. Med. Res. Rev. 27(6), 796-816 (2007).
76. Haataja S, Tikkanen K, Hytönen J, Finne J. The Gal alpha 1-4 Gal-binding adhesin of Streptococcus suis, a Gram-positive meningitis-associated bacterium. Adv. Exp. Med. Biol. 408, 25-34 (1996).
77. Haataja S, Tikkanen K, Liukkonen J, Franc¸ois-Gerard C, Finne J. Characterization of a novel bacterial adhesion specificity of Streptococcus suis recognizing blood group P receptor oligosaccharides. J. Biol. Chem. 268(6), 4311-4317 (1993).
78. Haataja S, Tikkanen K, Nilsson U, Magnusson G, Karlsson KA, Finne J. Oligosaccharide-receptor interaction of the Gal alpha 1-4Gal binding adhesin of Streptococcus suis. Combining site architecture and characterization of two variant adhesin specificities. J. Biol. Chem. 269(44), 27466-27472 (1994).
79. Haataja S, Zhang Z, Tikkanen K, Magnusson G, Finne J. Determination of the cell adhesion specificity of Streptococcus suis with the complete set of monodeoxy analogues of globotriose. Glycoconj. J. 16(1), 67-71 (1999).
80. Ohlsson J, Larsson A, Haataja S et al. Structure-activity relationships of galabioside derivatives as inhibitors of E. coli and S. suis adhesins: nanomolar inhibitors of S. suis adhesins. Org. Biomol. Chem. 3(5), 886-900 (2005).
81. Joosten JAF, Loimaranta V, Appeldoorn CCM et al. Inhibition of Streptococcus suis adhesion by dendritic galabiose compounds at low nanomolar concentration. J. Med. Chem. 47(26), 6499-6508 (2004).
82. Andersson B, Dahmén J, Frejd T et al. Identification of an active disaccharide unit of a glycoconjugate receptor for pneumococci attaching to human pharyngeal epithelial cells. J. Exp. Med. 158(2), 559-570 (1983).
83. Andersson B, Porras O, Hanson LA, Lagerga˚rd T, Svanborg-Edén C. Inhibition of attachment of Streptococcus pneumoniae and Haemophilus influenzae by human milk and receptor oligosaccharides. J. Infect. Dis. 153(2), 232-237 (1986).
84. Barthelson R, Mobasseri A, Zopf D, Simon P. Adherence of Streptococcus pneumoniae to respiratory epithelial cells is inhibited by sialylated oligosaccharides. Infect. Immun. 66(4), 1439-1444 (1998).
85. Al-Makhlafi H, McGuire J, Daeschel M. Influence of preadsorbed milk proteins on adhesion of Listeriamonocytogenes to hydrophobic and hydrophilic silica surfaces. Appl. Environ. Microbiol. 60(10), 3560-3565 (1994).
86. Vacca-Smith AM, Van Wuyckhuyse BC, Tabak LA, Bowen WH. The effect of milk and casein proteins on the adherence of Streptococcus mutans to saliva-coated hydroxyapatite. Arch. Oral Biol. 39(12), 1063-1069 (1994).
87. Mamo W, Fröman G. Adhesion of Staphylococcus aureus to bovine mammary epithelial cells induced by growth in milk whey. Microbiol. Immunol. 38(4), 305-308 (1994).
88. Shmuely H, Ofek I, Weiss EI, Rones Z, Houri-Haddad Y. Cranberry components for the therapy of infectious disease. Curr. Opin. Biotechnol. 23(2), 148-152 (2012).
89. Weiss EI, Lev-Dor R, Kashamn Y, Goldhar J, Sharon N, Ofek I. Inhibiting interspecies coaggregation of plaque bacteria with a cranberry juice constituent [published erratam appear in J. Am. Dent. Assoc. 1999 Jan;130(1):36 and 1999 Mar;130(3):332]. J. Am. Dent. Assoc. 129(12), 1719-1723 (1998).
90. Rozalski M, Micota B, Sadowska B et al. Antiadherent and antibiofilm activity of Humulus lupulus L. derived products: new pharmacological properties. BioMed Res. Int. 2013, 101089 (2013).
91. Ooshima T, Minami T, Aono W et al. Oolong tea polyphenols inhibit experimental dental caries in SPF rats infected with mutans streptococci. Caries Res. 27(2), 124-129 (1993).
92. Ooshima T, Osaka Y, Sasaki H et al. Caries inhibitory activity of cacao bean husk extract in in-vitro and animal experiments. Arch. Oral Biol. 45(8), 639-645 (2000).
93. Schwender N, Huber K, Marrawi FA, Hannig M, Ziegler C. Initial bioadhesion on surfaces in the oral cavity investigated by scanning force microscopy. Appl. Surf. Sci. 252(1), 117-122 (2005).
94. Müller R, Ruhl S, Hiller K-A, Schmalz G, Schweikl H. Adhesion of eukaryotic cells and Staphylococcus aureus to silicon model surfaces. J. Biomed. Mater. Res. A. 84(3), 817-827 (2008).
95. Müller R, Eidt A, Hiller K-A et al. Influences of protein films on antibacterial or bacteria-repellent surface coatings in a model system using silicon wafers. Biomaterials. 30(28), 4921-4929 (2009).
96. Ribeiro M, Monteiro FJ, Ferraz MP. Staphylococcus aureus and Staphylococcus epidermidis adhesion to nanohydroxyapatite in the presence of model proteins. Biomed. Mater. Bristol Engl. 7(4), 045010 (2012).
97. An YH, Friedman RJ. Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. J. Biomed. Mater. Res. 43(3), 338-348 (1998).