Staphylococcus aureus chronic and relapsing infections: Evidence of a role for persister cells: An investigation of persister cells, their formation and their role in S. aureus disease

BioEssays

Volumn 36, Issue 10, 2014, Pages 991-996

  Conlon, Brian P ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Antibiotics; Biofilm; Persister; Relapse; Staphylococcus aureus; Tolerance; Toxin antitoxin (TA)

Indexed keywords

ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL CELL; BACTERIAL CLEARANCE; BACTERIOLOGY; BIOFILM; CELL FUNCTION; CELL MATURATION; DRUG TOLERANCE; DRUG TREATMENT FAILURE; ERADICATION THERAPY; NONHUMAN; PERSISTER CELL; RECURRENT INFECTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ANIMAL; CHRONIC DISEASE; CYTOLOGY; DRUG EFFECTS; HUMAN; MICROBIOLOGY; PHYSIOLOGY; RECURRENT DISEASE; STAPHYLOCOCCAL INFECTIONS;

ANIMALS; ANTI-BACTERIAL AGENTS; BIOFILMS; CHRONIC DISEASE; HUMANS; RECURRENCE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84908227247     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400080     Document Type: Article

References (71)

1. Bigger J. 1944. Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244: 497-500.
2. Balaban NQ, Merrin J, Chait R, Kowalik L, et al. 2004. Bacterial persistence as a phenotypic switch. Science 305: 1622-5.
3. Hansen S, Vulic M, Min J, Yen TJ, et al. 2012. Regulation of the Escherichia coli HipBA toxin-antitoxin system by proteolysis. PLoS One 7: e39185.
4. Germain E, Castro-Roa D, Zenkin N, Gerdes K. 2013. Molecular mechanism of bacterial persistence by HipA. Mol Cell 52: 248-54.
5. Maisonneuve E, Shakespeare LJ, Jorgensen MG, Gerdes K. 2011. Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci USA 108: 13206-11.
6. Helaine S, Cheverton AM, Watson KG, Faure LM, et al. 2014. Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science 343: 204-8.
7. Sevin EW, Barloy-Hubler F. 2007. RASTA-Bacteria: a web-based tool for identifying toxin-antitoxin loci in prokaryotes. Genome Biol 8: R155.
8. Chan WT, Moreno-Cordoba I, Yeo CC, Espinosa M. 2012. Toxin-antitoxin genes of the Gram-positive pathogen Streptococcus pneumoniae: so few and yet so many. Microbiol Mol Biol Rev 76: 773-91.
9. Donegan NP, Thompson ET, Fu Z, Cheung AL. 2010. Proteolytic regulation of toxin-antitoxin systems by ClpPC in Staphylococcus aureus. J Bacteriol 192: 1416-22.
10. Maisonneuve E, Castro-Camargo M, Gerdes K. 2013. (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154: 1140-50.
11. Potrykus K, Cashel M. 2008. (p)ppGpp: still magical? Annu Rev Microbiol 62: 35-51.
12. Hou Z, Cashel M, Fromm HJ, Honzatko RB. 1999. Effectors of the stringent response target the active site of Escherichia coli adenylosuccinate synthetase. J Biol Chem 274: 17505-10.
13. Artsimovitch I, Patlan V, Sekine S, Vassylyeva MN, et al. 2004. Structural basis for transcription regulation by alarmone ppGpp. Cell 117: 299-310.
14. Milon P, Tischenko E, Tomsic J, Caserta E, et al. 2006. The nucleotide-binding site of bacterial translation initiation factor 2 (IF2) as a metabolic sensor. Proc Natl Acad Sci USA 103: 13962-7.
15. Wang JD, Sanders GM, Grossman AD. 2007. Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128: 865-75.
16. Amato SM, Orman MA, Brynildsen MP. 2013. Metabolic control of persister formation in Escherchia coli. Mol. Cell 50: 475-87.
17. Amato SM, Brynildsen MP. 2014. Nutrient transitions are a source of persisters in Escherichia coli biofilms. PLoS One 9: e93110.
18. Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, et al. 2011. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334: 982-6.
19. Hoiby N, Koch C. 1990. Cystic fibrosis. 1. Pseudomonas aeruginosa infection in cystic fibrosis and its management. Thorax 45: 881-4.
20. Mulcahy LR, Burns JL, Lory S, Lewis K. 2010. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J Bacteriol 192: 6191-9.
21. Keren I, Kaldalu N, Spoering A, Wang Y, et al. 2004. Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 230: 13-8.
22. Conlon BP, Nakayasu ES, Fleck LE, LaFleur MD, et al. 2013. Activated ClpP kills persisters and eradicates a chronic biofilm infection. Nature 503: 365-70.
23. Ziran BH. 2007. Osteomyelitis. J Traum 62: S59-60.
24. Baldoni D, Haschke M, Rajacic Z, Zimmerli W, et al. 2009. Linezolid alone or combined with rifampin against methicillin-resistant Staphylococcus aureus in experimental foreign-body infection. Antimicrob Agents Chemother 53: 1142-8.
25. Cuesta AI, Jewtuchowicz V, Brusca MI, Nastri ML, et al. 2010. Prevalence of Staphylococcus spp and Candida spp in the oral cavity and periodontal pockets of periodontal disease patients. Acta Odontol Latinoam 23: 20-6.
26. Petti CA, Fowler VG, Jr. 2003. Staphylococcus aureus bacteremia and endocarditis. Cardiol Clin 21: 219-33, vii.
27. Davis SC, Ricotti C, Cazzaniga A, Welsh E, et al. 2008. Microscopic and physiologic evidence for biofilm-associated wound colonization in vivo. Wound Repair Regen 16: 23-9.
28. Otto M. 2008. Staphylococcal biofilms. Curr Top Microbiol Immunol 322: 207-28.
29. Cucarella C, Solano C, Valle J, Amorena B, et al. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183: 2888-96.
30. Kropec A, Maira-Litran T, Jefferson KK, Grout M, et al. 2005. Poly-N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect Immun 73: 6868-76.
31. Domenech M, Ramos-Sevillano E, Garcia E, Moscoso M, et al. 2013. Biofilm formation avoids complement immunity and phagocytosis of Streptococcus pneumoniae. Infect Immun 81: 2606-15.
32. Schommer NN, Christner M, Hentschke M, Ruckdeschel K, et al. 2011. Staphylococcus epidermidis uses distinct mechanisms of biofilm formation to interfere with phagocytosis and activation of mouse macrophage-like cells 774A.1. Infect Immun 79: 2267-76.
33. Thurlow LR, Hanke ML, Fritz T, Angle A, et al. 2011. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J Immunol 186: 6585-96.
34. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, et al. 1987. Bacterial biofilms in nature and disease. Annu Rev Microbiol 41: 435-64.
35. Gristina AG, Hobgood CD, Webb LX, Myrvik QN. 1987. Adhesive colonization of biomaterials and antibiotic resistance. Biomaterials 8: 423-6.
36. Vrany JD, Stewart PS, Suci PA. 1997. Comparison of recalcitrance to ciprofloxacin and levofloxacin exhibited by Pseudomonas aeruginosa bofilms displaying rapid-transport characteristics. Antimicrob Agents Chemother 41: 1352-8.
37. Anderl JN, Franklin MJ, Stewart PS. 2000. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44: 1818-24.
38. Darouiche RO, Dhir A, Miller AJ, Landon GC, et al. 1994. Vancomycin penetration into biofilm covering infected prostheses and effect on bacteria. J Infect Dis 170: 720-3.
39. Jefferson KK, Goldmann DA, Pier GB. 2005. Use of confocal microscopy to analyze the rate of vancomycin penetration through Staphylococcus aureus biofilms. Antimicrob Agents Chemother 49: 2467-73.
40. Lewis K. 2001. Riddle of biofilm resistance. Antimicrob Agents Chemother 45: 999-1007.
41. Resch A, Leicht S, Saric M, Pasztor L, et al. 2006. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 6: 1867-77.
42. Resch A, Rosenstein R, Nerz C, Gotz F. 2005. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl Environ Microbiol 71: 2663-76.
43. Georgopapadakou NH, Smith SA, Bonner DP. 1982. Penicillin-binding proteins in a Staphylococcus aureus strain resistant to specific beta-lactam antibiotics. Antimicrob Agents Chemother 22: 172-5.
44. Jevons M. 1961. Calbenin-resistant staphylococci. BMJ 1: 124-5.
45. Shorr AF. 2007. Epidemiology of staphylococcal resistance. Clin Infect Dis 45: S171-6.
46. Bozdogan B, Appelbaum PC. 2004. Oxazolidinones: activity, mode of action, and mechanism of resistance. Int J Antimicrob Agents 23: 113-9.
47. Boucher HW, Sakoulas G. 2007. Perspectives on Daptomycin resistance, with emphasis on resistance in Staphylococcus aureus. Clin Infect Dis 45: 601-8.
48. Sievert DM, Rudrik JT, Patel JB, McDonald LC, et al. 2008. Vancomycin-resistant Staphylococcus aureus in the United States, 2002-2006. Clin Infect Dis 46: 668-74.
49. Shields RK, Clancy CJ, Minces LR, Kwak EJ, et al. 2012. Staphylococcus aureus infections in the early period after lung transplantation: epidemiology, risk factors, and outcomes. J Heart Lung Transplant 31: 1199-206.
50. Senneville E, Joulie D, Legout L, Valette M, et al. 2011. Outcome and predictors of treatment failure in total hip/knee prosthetic joint infections due to Staphylococcus aureus. Clin Infect Dis 53: 334-40.
51. Welsh KJ, Skrobarcek KA, Abbott AN, Lewis CT, et al. 2011. Predictors of relapse of methicillin-resistant Staphylococcus aureus bacteremia after treatment with vancomycin. J Clin Microbiol 49: 3669-72.
52. Corne P, Marchandin H, Macia JC, Jonquet O. 2005. Treatment failure of methicillin-resistant Staphylococcus aureus endocarditis with linezolid. Scand J Infect Dis 37: 946-9.
53. Ruiz ME, Guerrero IC, Tuazon CU. 2002. Endocarditis caused by methicillin-resistant Staphylococcus aureus: treatment failure with linezolid. Clin Infect Dis 35: 1018-20.
54. Darley ES, MacGowan AP. 2004. Antibiotic treatment of gram-positive bone and joint infections. J Antimicrob Chemother 53: 928-35.
55. Kutscha-Lissberg F, Hebler U, Muhr G, Koller M. 2003. Linezolid penetration into bone and joint tissues infected with methicillin-resistant staphylococci. Antimicrob Agents Chemother 47: 3964-6.
56. Graziani AL, Lawson LA, Gibson GA, Steinberg MA, et al. 1988. Vancomycin concentrations in infected and noninfected human bone. Antimicrob Agents Chemother 32: 1320-2.
57. Lewis K. 2010. Persister cells. Annu Rev Microbiol 64: 357-72.
58. Kaspy I, Rotem E, Weiss N, Ronin I, et al. 2013. HipA-mediated antibiotic persistence via phosphorylation of the glutamyl-tRNA-synthetase. Nat Commun 4: 3001.
59. Dorr T, Vulic M, Lewis K. 2010. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8: E1000317.
60. Davis BD. 1987. Mechanism of bactericidal action of aminoglycosides. Microbiol Rev 51: 341-50.
61. Tipper DJ, Strominger JL. 1965. Mechanism of action of penicillins: a proposal based on their structural similarity to acyl-D-alanyl-D-alanine. Proc Natl Acad Sci USA 54: 1133-41.
62. Drlica K, Zhao X. 1997. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61: 377-92.
63. Steenbergen JN, Alder J, Thorne GM, Tally FP. 2005. Daptomycin: a lipopeptide antibiotic for the treatment of serious Gram-positive infections. J Antimicrob Chemother 55: 283-8.
64. Mascio CT, Alder JD, Silverman JA. 2007. Bactericidal action of daptomycin against stationary-phase and nondividing Staphylococcus aureus cells. Antimicrob Agents Chemother 51: 4255-60.
65. Allison KR, Brynildsen MP, Collins JJ. 2011. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 473: 216-20.
66. Schmitz FJ, Fluit AC, Gondolf M, Beyrau R, et al. 1999. The prevalence of aminoglycoside resistance and corresponding resistance genes in clinical isolates of staphylococci from 19 European hospitals. J Antimicrob Chemother 43: 253-9.
67. Brotz-Oesterhelt H, Beyer D, Kroll HP, Endermann R, et al. 2005. Dysregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat Med 11: 1082-7.
68. Kirstein J, Hoffmann A, Lilie H, Schmidt R, et al. 2009. The antibiotic ADEP reprogrammes ClpP, switching it from a regulated to an uncontrolled protease. EMBO Mol Med 1: 37-49.
69. Pascoe B, Dams L, Wilkinson TS, Harris LG, et al. 2014. Dormant cells of Staphylococcus aureus are resuscitated by spent culture supernatant. PLoS One 9: E85998.
70. Mwangi MM, Wu SW, Zhou Y, Sieradzki K, et al. 2007. Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Natl Acad Sci USA 104: 9451-6.
71. Howden BP, McEvoy CR, Allen DL, Chua K, et al. 2011. Evolution of multidrug resistance during Staphylococcus aureus infection involves mutation of the essential two component regulator WalKR. PLoS Pathog 7: E1002359.