A new anti-infective strategy to reduce the spreading of antibiotic resistance by the action on adhesion-mediated virulence factors in Staphylococcus aureus

Microbial Pathogenesis

Volumn 63, Issue , 2013, Pages 44-53

  Papa, Rosanna ^a   Artini, Marco ^a   Cellini, Andrea ^a   Tilotta, Marco ^a   Galano, Eugenio ^b   Pucci, Pietro ^b,c   Amoresano, Angela ^b   Selan, Laura ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

Author keywords

Adhesion; Biofilm; Serratiopeptidase; Staphylococcus aureus; Virulence

Indexed keywords

ADHESIN; ATL PROTEIN; AUTOLYSIN; EF G PROTEIN; EFTU PROTEIN; MEMBRANE PROTEIN; SBI PROTEIN; SDRD PROTEIN; SERRATIOPEPTIDASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ADHERENCE; BIOFILM; CELL ADHESION; CELL INVASION; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEOMICS; SERRATIA MARCESCENS; STAPHYLOCOCCUS AUREUS;

ADHESION; BIOFILM; SERRATIOPEPTIDASE; STAPHYLOCOCCUS AUREUS; VIRULENCE;

ANTI-INFECTIVE AGENTS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CELL MEMBRANE; CYTOPLASM; ENDOCYTOSIS; EPITHELIAL CELLS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROBIAL SENSITIVITY TESTS; PEPTIDE HYDROLASES; PROTEOME; SERRATIA MARCESCENS; STAPHYLOCOCCUS AUREUS;

EID: 84880395337     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2013.05.003     Document Type: Article

References (63)

1. Verhoef J.F., Schmitz F.J. Staphylococci and other Micrococcaceae 2004, Elsevier, Mosby Inc, St. Louis.
2. Waldvogel F.A. Staphylococcus aureus (including toxic shock syndrome) 1995, Churchill Livingstone, New York.
3. Lowy F.D. Staphylococcus aureus infections. NEngl J Med 1998, 339:520-532.
4. Burlak C., Hammer C.H., Robinson M.A., Whitney A.R., McGavin M.J., Kreiswirth B.N., et al. Global analysis of community-associated methicillin-resistant Staphylococcus aureus exoproteins reveals molecules produced invitro and during infection. Cell Microbiol 2007, 9:1172-1190.
5. Jeffery C.J. Moonlighting proteins: old proteins learning new tricks. Trends Genet 2003, 19:415-417.
6. O'Gara J.P. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett 2007, 270:179-188.
7. Romanò C.L., Romanò D., Logoluso N., Drago L. Bone and joint infections in adults: a comprehensive classification proposal. Eur Orthop Traumatol 2011, 1:207-217.
8. Arciola C.R., Campoccia D., Speziale P., Montanaro L., Costerton J.W. Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials 2012, 33:5967-5982.
9. Montanaro L., Speziale P., Campoccia D., Ravaioli S., Cangini I., Pietrocola G., et al. Scenery of Staphylococcus implant infections in orthopedics. Future Microbiol 2011, 6:1329-1349.
10. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science 1999, 284:1318-1322.
11. Lewis K. Riddle of biofilm resistance. Antimicrob Agents Chemother 2001, 45:999-1007.
12. Stewart P.S., Costerton J.W. Antibiotic resistance of bacteria in biofilms. Lancet 2001, 358:135-138.
13. Arciola C.R., Hänsch G.M., Visai L., Testoni F., Maurer S., Campoccia D., et al. Interactions of staphylococci with osteoblasts and phagocytes in the pathogenesis of implant-associated osteomyelitis. Int J Artif Organs 2012, 35:713-726.
14. Boles B.R., Horswill A.R. agr-Mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 2008, 4:e1000052.
15. Costerton J.W., Montanaro L., Arciola C.R. Bacterial communications in implant infections: a target for an intelligence war. Int J Artif Organs 2007, 30:757-763.
16. Artini M., Papa R., Scoarughi G.L., Galano E., Barbato G., Pucci P., et al. Comparison of the action of different proteases on virulence properties related to the staphylococcal surface. JAppl Microbiol 2013, 114:266-277.
17. Artini M., Papa R., Barbato G., Scoarughi G.L., Cellini A., Morazzoni P., et al. Bacterial biofilm formation inhibitory activity revealed for plant derived natural compounds. Bioorg Med Chem 2012, 20:920-926.
18. Vergara-Irigaray M., Valle J., Merino N., Latasa C., García B., Ruiz de Los Mozos I., et al. Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections. Infect Immun 2009, 77:3978-3991.
19. Rohde H., Burandt E.C., Siemssen N., Frommelt L., Burdelski C., Wurster S., et al. Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 2007, 28:1711-1720.
20. Iwase T., Uehara Y., Shinji H., Tajima A., Seo H., Takada K., et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 2010, 465:346-349.
21. Salamone P.R., Wodzinski R.J. Production, purification and characterization of a 50-kDa extracellular metalloprotease from Serratia marcescens. Appl Microbiol Biotechnol 1997, 48:317-324.
22. Baumann U. Crystal structure of the 50kDa metallo protease from Serratia marcescens. JMol Biol 1994, 242:244-251.
23. Kee W.H., Tan S.L., Lee V., Salmon Y.M. The treatment of breast engorgement with serrapeptase (Danzen): a randomised double-blind controlled trial. Singapore Med J 1989, 30:48-54.
24. Mazzone A., Catalani M., Costanzo M., Drusian A., Mandoli A., Russo S., et al. Evaluation of Serratia peptidase in acute or chronic inflammation of otorhinolaryngology pathology: a multicentre, double-blind, randomized trial versus placebo. JInt Med Res 1990, 18:379-388.
25. Longhi C., Scoarughi G.L., Poggiali F., Cellini A., Carpentieri A., Seganti L., et al. Protease treatment affects both invasion ability and biofilm formation in Listeria monocytogenes. Microb Pathog 2008, 45:45-52.
26. Maheshwari M., Miglani G., Mali A., Paradkar A., Yamamura S., Kadam S. Development of tetracycline-serratiopeptidase-containing periodontal gel: formulation and preliminary clinical study. AAPS PharmSciTech 2006, 7:76.
27. Selan L., Berlutti F., Passariello C., Comodi-Ballanti M.R., Thaller M.C. Proteolytic enzymes: a new treatment strategy for prosthetic infections?. Antimicrob Agents Chemother 1993, 37:2618-2621.
28. Artini M., Scoarughi G.L., Papa R., Cellini A., Carpentieri A., Pucci P., et al. Anew anti-infective strategy to reduce adhesion-mediated virulence in Staphylococcus aureus affecting surface proteins. Int J Immunopathol Pharmacol 2011, 24:661-672.
29. Diep B.A., Gill S.R., Chang R.F., Phan T.H., Chen J.H., Davidson M.G., et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 2006, 367:731-739.
30. Christensen G.D., Baldassarri L., Simpson W.A. Colonization of medical devices by coagulase-negative staphylococci 1994, ASM Press, Washington, D.C.
31. Tabouret M., de Rycke J., Dubray G. Analysis of surface proteins of Listeria in relation to species, serovar and pathogenicity. JGen Microbiol 1992, 138:743-753.
32. Sambrook J., Russell D.W. Molecular cloning: a laboratory manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
33. Lauderdale K.J., Boles B.R., Cheung A.L., Horswill A.R. Interconnections between sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect Immun 2009, 77:1623-1635.
34. Cafiso V., Bertuccio T., Santagati M., Demelio V., Spina D., Nicoletti G., et al. agr-Genotyping and transcriptional analysis of biofilm-producing Staphylococcus aureus. FEMS Immunol Med Microbiol 2007, 51:220-227.
35. Bercic R.L., Slavec B., Lavric M., Narat M., Bidovec A., Dovc P., et al. Identification of major immunogenic proteins of Mycoplasma synoviae isolates. Vet Microbiol 2008, 127:147-154.
36. Glowalla E., Tosetti B., Kronke M., Krut O. Proteomics-based identification of anchorless cell wall proteins as vaccine candidates against Staphylococcus aureus. Infect Immun 2009, 77:2719-2729.
37. Biswas R., Voggu L., Simon U.K., Hentschel P., Thumm G., Gotz F. Activity of the major staphylococcal autolysin Atl. FEMS Microbiol Lett 2006, 259:260-268.
38. Foster T.J. Immune evasion by staphylococci. Nat Rev Microbiol 2005, 3:948-958.
39. Pinheiro V.B., Ellar D.J. How to kill a mocking bug?. Cell Microbiol 2006, 8:545-557.
40. Roche F.M., Meehan M., Foster T.J. The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology 2003, 149:2759-2767.
41. Navarre W.W., Schneewind O. Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 1999, 63:174-229.
42. Tjalsma H., Lambooy L., Hermans P.W., Swinkels D.W. Shedding & shaving: disclosure of proteomic expressions on a bacterial face. Proteomics 2008, 8:1415-1428.
43. Otto M. Looking toward basic science for potential drug discovery targets against community-associated MRSA. Med Res Rev 2010, 30:1-22.
44. Nakamura S., Hashimoto Y., Mikami M., Yamanaka E., Soma T., Hino M., et al. Effect of the proteolytic enzyme serrapeptase in patients with chronic airway disease. Respirology 2003, 8:316-320.
45. Fitzpatrick F., Humphreys H., O'Gara J.P. Evidence for icaADBC-independent biofilm development mechanism in methicillin-resistant Staphylococcus aureus clinical isolates. JClin Microbiol 2005, 43:1973-1976.
46. Sinha B., Herrmann M. Mechanism and consequences of invasion of endothelial cells by Staphylococcus aureus. Thromb Haemost 2005, 94:266-277.
47. Hauck C.R., Agerer F., Muenzner P., Schmitter T. Cellular adhesion molecules as targets for bacterial infection. Eur J Cell Biol 2006, 85:235-242.
48. Clarke S.R., Foster S.J. Surface adhesins of Staphylococcus aureus. Adv Microb Physiol 2006, 51:187-224.
49. Cucarella C., Solano C., Valle J., Amorena B., Lasa I., Penades J.R. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. JBacteriol 2001, 183:2888-2896.
50. Hirschhausen N., Schlesier T., Schmidt M.A., Götz F., Peters G., Heilmann C. Anovel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell Microbiol 2010, 12:1746-1764.
51. Haupt K., Reuter M., van den Elsen J., Burman J., Hälbich S., Richter J., et al. The Staphylococcus aureus protein Sbi acts as a complement inhibitor and forms a tripartite complex with host complement factor H and C3b. PLoS Pathog 2008, 4:e1000250.
52. Atkins K.L., Burman J.D., Chamberlain E.S., Cooper J.E., Poutrel B., Bagby S., et al. S.aureus IgG-binding proteins SpA and Sbi: host specificity and mechanisms of immune complex formation. Mol Immunol 2008, 45:1600-1611.
53. Wang X., Ge J., Liu B., Hu Y., Yang M. Structures of SdrD from Staphylococcus aureus reveal the molecular mechanism of how the cell surface receptors recognize their ligands. Protein Cell 2013, 4:277-285.
54. Granato D., Bergonzelli G.E., Pridmore R.D., Marvin L., Rouvet M., Corthesy-Theulaz I.E. Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun 2004, 72:2160-2169.
55. Marques M.A., Chitale S., Brennan P.J., Pessolani M.C. Mapping and identification of the major cell wall-associated components of Mycobacterium leprae. Infect Immun 1998, 66:2625-2631.
56. Balasubramanian S., Kannan T.R., Baseman J.B. The surface-exposed carboxyl region of Mycoplasma pneumoniae elongation factor Tu interacts with fibronectin. Infect Immun 2008, 76:3116-3123.
57. Dallo S.F., Kannan T.R., Blaylock M.W., Baseman J.B. Elongation factor Tu and E1 beta subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumonia. Mol Microbiol 2002, 46:1041-1051.
58. Schaumburg J., Diekmann O., Hagendorff P., Bergmann S., Rohde M., Hammerschmidt S., et al. The cell wall subproteome of Listeria monocytogenes. Proteomics 2004, 4:2991-3006.
59. Arciola C.R., Collimati S., Donati E., Montanaro L. Arapid PCR method for the detection of slime-producing strains of Staphylococcus epidermidis and S.aureus in periprosthesis infections. Diagn Mol Pathol 2001, 10:130-137.
60. Kiem S., Oh W.S., Peck K.R., Lee N.Y., Lee J.Y., Song J.H., et al. Phase variation of biofilm formation in Staphylococcus aureus by IS 256 insertion and its impact on the capacity adhering to polyurethane surface. Korean Med Sci 2004, 19:779-782.
61. Valle J., Toledo-Arana A., Berasain C., Ghigo J.M., Amorena B., Penadés J.R., et al. SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus. Mol Microbiol 2003, 48:1075-1087.
62. Wolz C., Goerke C., Landmann R., Zimmerli W., Fluckiger U. Transcription of clumping factor A in attached and unattached Staphylococcus aureus invitro and during device-related infection. Infect Immun 2002, 70:2758-2762.
63. Wootton M., Bennett P.M., MacGowan A.P., Walsh T.R. Reduced expression of the Atl autolysin gene and susceptibility to autolysis in clinical heterogeneous glycopeptide-intermediate Staphylococcus aureus (hGISA) and GISA strains. JAntimicrob Chem 2005, 56:944-947.