Tomatidine inhibits replication of Staphylococcus aureus small-colony variants in cystic fibrosis airway epithelial cells

Antimicrobial Agents and Chemotherapy

Volumn 55, Issue 5, 2011, Pages 1937-1945

  Mitchell, Gabriel ^a   Gattuso, Mariza ^a   Grondin, Gilles ^a   Marsault, Éric ^b   Bouarab, Kamal ^a   Malouin, François ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXY 2 HEPTYLQUINOLINE N OXIDE; LEUCINE; OXIDE; TOMATIDINE; TOMATINE; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOSTASIS; BIOSYNTHESIS; CONTROLLED STUDY; CYSTIC FIBROSIS; DRUG EFFECT; ELECTRON TRANSPORT; HUMAN; HUMAN CELL; MACROMOLECULE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; RESPIRATORY FAILURE; STAPHYLOCOCCUS AUREUS;

CELL LINE; CYSTIC FIBROSIS; GENTAMICINS; HUMANS; HYDROXYQUINOLINES; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, FLUORESCENCE; MOLECULAR STRUCTURE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TOMATINE;

EID: 79955532603     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01468-10     Document Type: Article

References (46)

1. Alexander, E. H., and M. C. Hudson. 2001. Factors influencing the internalization of Staphylococcus aureus and impacts on the course of infections in humans. Appl. Microbiol. Biotechnol. 56:361-366.
2. Archer, G. L. 1998. Staphylococcus aureus: a well-armed pathogen. Clin. Infect. Dis. 26:1179-1181.
3. Atalla, H., et al. 2008. Characterization of a Staphylococcus aureus small colony variant (SCV) associated with persistent bovine mastitis. Foodborne Pathog. Dis. 5:785-799.
4. Bednarek, P., and A. Osbourn. 2009. Plant-microbe interactions: chemical diversity in plant defense. Science 324:746-748.
5. Besier, S., et al. 2007. Prevalence and clinical significance of Staphylococcus aureus small-colony variants in cystic fibrosis lung disease. J. Clin. Microbiol. 45:168-172.
6. Bouarab, K., E. Ordi, M. M. Gattuso, H. Moisan, and F. Malouin. 2007. Plant stress response agents affect Staphylococcus aureus virulence genes. Abstr. 47th Intersci. Conf. Antimicrob. Agents Chemother., abstr. C1-1483.
7. Brouillette, E., A. Martinez, B. J. Boyll, N. E. Allen, and F. Malouin. 2004. Persistence of a Staphylococcus aureus small-colony variant under antibiotic pressure in vivo. FEMS Immunol. Med. Microbiol. 41:35-41.
8. Bryan, L. E., and S. Kwan. 1981. Aminoglycoside-resistant mutants of Pseudomonas aeruginosa deficient in cytochrome d, nitrite reductase, and aerobic transport. Antimicrob. Agents Chemother. 19:958-964.
9. Clinical and Laboratory Standards Institute. 2006. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard. Clinical and Laboratory Standards Institute, Wayne, PA.
10. Cowan, M. M. 1999. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12:564-582.
11. Friedman, M. 2002. Tomato glycoalkaloids: role in the plant and in the diet. J. Agric. Food Chem. 50:5751-5780.
12. Galli, J., et al. 2007. Recurrent upper airway infections and bacterial biofilms. J. Laryngol. Otol. 121:341-344.
13. Goering, R. V., A. Bauernfeind, W. Lenz, and B. Przyklenk. 1990. Staphylococcus aureus in patients with cystic fibrosis: an epidemiological analysis using a combination of traditional and molecular methods. Infection 18:57-60. (Pubitemid 20061344)
14. Goerke, C., and C. Wolz. 2004. Regulatory and genomic plasticity of Staphylococcus aureus during persistent colonization and infection. Int. J. Med. Microbiol. 294:195-202.
15. González-Lamothe, R., et al. 2009. Plant antimicrobial agents and their effects on plant and human pathogens. Int. J. Mol. Sci. 10:3400-3419.
16. Harrison, F. 2007. Microbial ecology of the cystic fibrosis lung. Microbiology 153:917-923. (Pubitemid 46605791)
17. Hoffman, L. R., et al. 2006. Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 103:19890-19895.
18. Kahl, B., et al. 1998. Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J. Infect. Dis. 177:1023-1029.
19. Kahl, B. C., et al. 2003. Population dynamics of persistent Staphylococcus aureus isolated from the airways of cystic fibrosis patients during a 6-year prospective study. J. Clin. Microbiol. 41:4424-4427.
20. Lightbown, J. W., and F. L. Jackson. 1956. Inhibition of cytochrome systems of heart muscle and certain bacteria by the antagonists of dihydrostreptomycin: 2-alkyl-4-hydroxyquinoline N-oxides. Biochem. J. 63:130-137.
21. Lowy, F. D. 2000. Is Staphylococcus aureus an intracellular pathogen? Trends Microbiol. 8:341-343.
22. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194-222.
23. Martin-Hernandez, A. M., M. Dufresne, V. Hugouvieux, R. Melton, and A. Osbourn. 2000. Effects of targeted replacement of the tomatinase gene on the interaction of Septoria lycopersici with tomato plants. Mol. Plant Microbe Interact. 13:1301-1311.
24. Massey, R. C., A. Buckling, and S. J. Peacock. 2001. Phenotypic switching of antibiotic resistance circumvents permanent costs in Staphylococcus aureus. Curr. Biol. 11:1810-1814.
25. Miller, M. H., S. C. Edberg, L. J. Mandel, C. F. Behar, and N. H. Steigbigel. 1980. Gentamicin uptake in wild-type and aminoglycoside-resistant small-colony mutants of Staphylococcus aureus. Antimicrob. Agents Chemother. 18:722-729.
26. Mitchell, G., G. Bilodeau, G. Grondin, A. Cantin, and F. Malouin. 2010. Defects in the cystic fibrosis transmembrane conductance regulator (CFTR) increase Staphylococcus aureus intracellular infection of human pulmonary Cells. Abstr. 100th Gen. Meet. Am. Soc. Microbiol., abstr. D-1179.
27. Mitchell, G., et al. 2010. A role for sigma factor B in the emergence of Staphylococcus aureus small-colony variants and elevated biofilm production resulting from an exposure to aminoglycosides. Microb. Pathog. 48:18-27.
28. Mitchell, G., M. Gattuso, K. Bouarab, and F. Malouin. 2009. Tomatidine (TO) affects virulence regulators of prototypical Staphylococcus aureus (SA) and small colony variants (SCV) of cystic fibrosis (CF) patients. Abstr. 49th Intersci. Conf. Antimicrob. Agents Chemother., abstr. C1-1341.
29. Mitchell, G., et al. 2010. Staphylococcus aureus sigma B-dependent emergence of small-colony variants and biofilm production following exposure to Pseudomonas aeruginosa 4-hydroxy-2-heptylquinoline-N-oxide. BMC Microbiol. 10:33.
30. Moisan, H., et al. 2006. Transcription of virulence factors in Staphylococcus aureus small-colony variants isolated from cystic fibrosis patients is influenced by SigB. J. Bacteriol. 188:64-76.
31. Osbourn, A. E. 1996. Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell 8:1821-1831. (Pubitemid 27012407)
32. Palmer, M. L., et al. 2006. Protease-activated receptor regulation of Cl-secretion in Calu-3 cells requires prostaglandin release and CFTR activation. Am. J. Physiol. Cell Physiol. 290:C1189-C1198.
33. Proctor, R. A., et al. 2006. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat. Rev. Microbiol. 4:295-305.
34. Ríos, J. L., and M. C. Recio. 2005. Medicinal plants and antimicrobial activity. J. Ethnopharmacol. 100:80-84.
35. Roddick, J. G. 1974. The steroidal glycoalkaloid α-tomatine. Phytochemistry 13:9-25.
36. Ruiz-Rubio, M., et al. 2001. Metabolism of the tomato saponin α-tomatine by phytopathogenic fungi, p. 293-326. In A. Rahman (ed.), Studies in natural products chemistry, vol. 25. Elsevier, Oxford, United Kingdom.
37. Sandrock, R. W., and H. D. Vanetten. 1998. Fungal sensitivity to and enzymatic degradation of the phytoanticipin α-tomatine. Phytopathology 88:137-143.
38. Schaaff, F., G. Bierbaum, N. Baumert, P. Bartmann, and H. G. Sahl. 2003. Mutations are involved in emergence of aminoglycoside-induced small colony variants of Staphylococcus aureus. Int. J. Med. Microbiol. 293:427-435.
39. Sendi, P., and R. A. Proctor. 2009. Staphylococcus aureus as an intracellular pathogen: the role of small colony variants. Trends Microbiol. 17:54-58.
40. Shah, P. M. 2005. The need for new therapeutic agents: what is the pipeline? Clin. Microbiol. Infect. 11 Suppl. 3:36-42.
41. Simons, V., et al. 2006. Dual effects of plant steroidal alkaloids on Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 50:2732-2740.
42. Singh, R., P. Ray, A. Das, and M. Sharma. 2010. Enhanced production of exopolysaccharide matrix and biofilm by a menadione-auxotrophic Staphylococcus aureus small-colony variant. J. Med. Microbiol. 59:521-527.
43. Singh, R., P. Ray, A. Das, and M. Sharma. 2009. Role of persisters and small-colony variants in antibiotic resistance of planktonic and biofilm-associated Staphylococcus aureus: an in vitro study. J. Med. Microbiol. 58:1067-1073.
44. Stewart, P. S. 2002. Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 292:107-113.
45. Talbot, G. H., et al. 2006. Bad bugs need drugs: an update on the development pipeline from the Antimicrobial Availability Task Force of the Infectious Diseases Society of America. Clin. Infect. Dis. 42:657-668.
46. Tuchscherr, L., et al. 2011. Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol. Med. 3:129-141.