Sensitization of Staphylococcus aureus to Methicillin and Other Antibiotics In Vitro and In Vivo in the Presence of HAMLET

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Marks, Laura R ^a   Clementi, Emily A ^a   Hakansson, Anders P ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADJUVANT; ANTIBIOTIC AGENT; CALCIUM ION; ERYTHROMYCIN; GENTAMICIN; HAMLET PROTEIN; METICILLIN; PENICILLIN DERIVATIVE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTON; SODIUM ION; UNCLASSIFIED DRUG; VANCOMYCIN; ANTIINFECTIVE AGENT; BOCILLIN FL; BORON DERIVATIVE; HAMLET COMPLEX, HUMAN; LACTALBUMIN; OLEIC ACID; UNCOUPLING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BIOFILM; CALCIUM TRANSPORT; CELL DEATH; CONTROLLED STUDY; DRUG POTENTIATION; DRUG SENSITIZATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE DEPOLARIZATION; MOUSE; NASOPHARYNX; NONHUMAN; PLANKTON; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; ANIMAL; CALCIUM SIGNALING; DRUG EFFECTS; MEMBRANE POTENTIAL; METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; MICROBIOLOGY; PENICILLIN RESISTANCE; PHYSIOLOGY; RESPIRATORY TRACT INFECTIONS; STAPHYLOCOCCAL INFECTIONS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; ANTI-BACTERIAL AGENTS; BIOFILMS; BORON COMPOUNDS; CALCIUM SIGNALING; DRUG SYNERGISM; GENTAMICINS; LACTALBUMIN; MEMBRANE POTENTIALS; METHICILLIN; METHICILLIN RESISTANCE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; NASOPHARYNX; OLEIC ACIDS; PENICILLINS; RESPIRATORY TRACT INFECTIONS; STAPHYLOCOCCAL INFECTIONS; UNCOUPLING AGENTS; VANCOMYCIN;

EID: 84877032645     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063158     Document Type: Article

References (70)

1. Calfee DP (2012) Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci, and other Gram-positives in healthcare. Curr Opin Infect Dis.
2. Gould IM, David MZ, Esposito S, Garau J, Lina G, et al. (2012) New insights into meticillin-resistant Staphylococcus aureus (MRSA) pathogenesis, treatment and resistance. Int J Antimicrob Agents 39: 96-104.
3. McGavin MJ, Heinrichs DE (2012) The Staphylococci and Staphylococcal Pathogenesis. Front Cell Inf Microbio 2.
4. de Kraker ME, Wolkewitz M, Davey PG, Koller W, Berger J, et al. (2011) Clinical impact of antimicrobial resistance in European hospitals: excess mortality and length of hospital stay related to methicillin-resistant Staphylococcus aureus bloodstream infections. Antimicrob Agents Chemother 55: 1598-1605.
5. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, et al. (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763-1771.
6. Fischbach MA, Walsh CT, (2009) Antibiotics for emerging pathogens. Science 325: 1089-1093.
7. Braine T, (2011) Race against time to develop new antibiotics. Bull World Health Organ 89: 88-89.
8. Alanis AJ, (2005) Resistance to antibiotics: are we in the post-antibiotic era? Arch Med Res 36: 697-705.
9. Kristiansen JE, Thomsen VF, Martins A, Viveiros M, Amaral L, (2010) Non-antibiotics reverse resistance of bacteria to antibiotics. In Vivo 24: 751-754.
10. Falcao-Silva VS, Silva DA, Souza Mde F, Siqueira-Junior JP, (2009) Modulation of drug resistance in Staphylococcus aureus by a kaempferol glycoside from Herissantia tiubae (Malvaceae). Phytother Res 23: 1367-1370.
11. Kaatz GW, Moudgal VV, Seo SM, Kristiansen JE, (2003) Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus. Antimicrob Agents Chemother 47: 719-726.
12. Fadli M, Chevalier J, Saad A, Mezrioui NE, Hassani L, et al. (2011) Essential oils from Moroccan plants as potential chemosensitisers restoring antibiotic activity in resistant Gram-negative bacteria. Int J Antimicrob Agents 38: 325-330.
13. Lonnerdal B, (2004) Human milk proteins: key components for the biological activity of human milk. Adv Exp Med Biol 554: 11-25.
14. Newburg DS, (1999) Human milk glycoconjugates that inhibit pathogens. Curr Med Chem 6: 117-127.
15. Newburg DS, (2005) Innate immunity and human milk. J Nutr 135: 1308-1312.
16. Svensson M, Sabharwal H, Hakansson A, Mossberg AK, Lipniunas P, et al. (1999) Molecular characterization of alpha-lactalbumin folding variants that induce apoptosis in tumor cells. J Biol Chem 274: 6388-6396.
17. Svensson M, Hakansson A, Mossberg AK, Linse S, Svanborg C, (2000) Conversion of alpha-lactalbumin to a protein inducing apoptosis. Proc Natl Acad Sci U S A 97: 4221-4226.
18. Jensen RG, Clark RM, Ferris AM, (1980) Composition of the lipids in human milk: a review. Lipids 15: 345-355.
19. Jensen RG, Ferris AM, Lammi-Keefe CJ, Henderson RA, (1990) Lipids of bovine and human milks: a comparison. J Dairy Sci 73: 223-240.
20. Hakansson A, Zhivotovsky B, Orrenius S, Sabharwal H, Svanborg C, (1995) Apoptosis induced by a human milk protein. Proc Natl Acad Sci U S A 92: 8064-8068.
21. Hakansson A, Andreasson J, Zhivotovsky B, Karpman D, Orrenius S, et al. (1999) Multimeric alpha-lactalbumin from human milk induces apoptosis through a direct effect on cell nuclei. Exp Cell Res 246: 451-460.
22. Kohler C, Gogvadze V, Hakansson A, Svanborg C, Orrenius S, et al. (2001) A folding variant of human alpha-lactalbumin induces mitochondrial permeability transition in isolated mitochondria. Eur J Biochem 268: 186-191.
23. Hakansson A, Svensson M, Mossberg AK, Sabharwal H, Linse S, et al. (2000) A folding variant of alpha-lactalbumin with bactericidal activity against Streptococcus pneumoniae. Mol Microbiol 35: 589-600.
24. Clementi EA, Marks LR, Duffey ME, Hakansson AP, (2012) A Novel Initiation Mechanism of Death in Streptococcus pneumoniae Induced by the Human Milk Protein-Lipid Complex HAMLET and Activated during Physiological Death. J Biol Chem 287: 27168-27182.
25. Hakansson AP, Roche-Hakansson H, Mossberg AK, Svanborg C, (2011) Apoptosis-Like Death in Bacteria Induced by HAMLET, a Human Milk Lipid-Protein Complex. PLoS One 6: e17717.
26. Marks LR, Clementi EA, Hakansson AP, (2012) The Human Milk Protein-Lipid Complex HAMLET Sensitizes Bacterial Pathogens to Traditional Antimicrobial Agents. PLoS ONE 7: e43514.
27. Reiter KC, Villa B, Paim TG, Sambrano GE, de Oliveira CF, et al. (2012) Enhancement of antistaphylococcal activities of six antimicrobials against sasG-negative methicillin-susceptible Staphylococcus aureus: an in vitro biofilm model. Diagn Microbiol Infect Dis 74: 101-105.
28. Parra-Ruiz J, Vidaillac C, Rose WE, Rybak MJ, (2010) Activities of high-dose daptomycin, vancomycin, and moxifloxacin alone or in combination with clarithromycin or rifampin in a novel in vitro model of Staphylococcus aureus biofilm. Antimicrob Agents Chemother 54: 4329-4334.
29. Paulsen IT, Brown MH, Skurray RA, (1996) Proton-dependent multidrug efflux systems. Microbiol Rev 60: 575-608.
30. Putman M, van Veen HW, Konings WN, (2000) Molecular properties of bacterial multidrug transporters. Microbiol Mol Biol Rev 64: 672-693.
31. Martins A, Couto I, Aagaard L, Martins M, Viveiros M, et al. (2007) Prolonged exposure of methicillin-resistant Staphylococcus aureus (MRSA) COL strain to increasing concentrations of oxacillin results in a multidrug-resistant phenotype. Int J Antimicrob Agents 29: 302-305.
32. Liu C, Bayer A, Cosgrove SE, Daum RS, Fridkin SK, et al. (2011) Clinical practice guidelines by the infectious diseases society of america for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin Infect Dis 52: e18-55.
33. Jean SS, Hsueh PR, (2011) Current review of antimicrobial treatment of nosocomial pneumonia caused by multidrug-resistant pathogens. Expert Opin Pharmacother 12: 2145-2148.
34. Rand KH, Houck HJ, (2004) Synergy of daptomycin with oxacillin and other beta-lactams against methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 48: 2871-2875.
35. Rose WE, Poppens PT, (2009) Impact of biofilm on the in vitro activity of vancomycin alone and in combination with tigecycline and rifampicin against Staphylococcus aureus. J Antimicrob Chemother 63: 485-488.
36. Tang HJ, Chen CC, Ko WC, Yu WL, Chiang SR, et al. (2011) In vitro efficacy of antimicrobial agents against high-inoculum or biofilm-embedded meticillin-resistant Staphylococcus aureus with vancomycin minimal inhibitory concentrations equal to 2 mug/mL (VA2-MRSA). Int J Antimicrob Agents 38: 46-51.
37. Kaatz GW, Moudgal VV, Seo SM, (2002) Identification and characterization of a novel efflux-related multidrug resistance phenotype in Staphylococcus aureus. J Antimicrob Chemother 50: 833-838.
38. Heine WE, Klein PD, Reeds PJ, (1991) The importance of alpha-lactalbumin in infant nutrition. J Nutr 121: 277-283.
39. Lonnerdal B, (1985) Biochemistry and physiological function of human milk proteins. Am J Clin Nutr 42: 1299-1317.
40. Simor AE, (2011) Staphylococcal decolonisation: an effective strategy for prevention of infection? Lancet Infect Dis 11: 952-962.
41. Lovell DL, (1945) Skin bacteria; their role in contamination and infection of wounds. Arch Surg 51: 78-80.
42. Moss B, Squire JR, Topley E, Johnston CM, (1948) Nose and skin carriage of Staphylococcus aureus in patients receiving penicillin. Lancet 1: 320-325.
43. Varga DT, White A, (1961) Suppression of nasal, skin, and aerial staphylococci by nasal application of methicillin. J Clin Invest 40: 2209-2214.
44. Glotzer DJ, Goodman WS, Geronimus LH, (1970) Topical antibiotic prophylaxis in contaminated wounds. Experimental evaluation. Arch Surg 100: 589-593.
45. Roe E, Jones RJ, (1972) Effects of topical chemoprophylaxis on transferable antibiotic resistance in burns. Lancet 2: 109-111.
46. Ramon-Garcia S, Mick V, Dainese E, Martin C, Thompson CJ, et al. (2012) Functional and genetic characterization of the tap efflux pump in Mycobacterium bovis BCG. Antimicrob Agents Chemother 56: 2074-2083.
47. Zhang Z, Liu ZQ, Zheng PY, Tang FA, Yang PC, (2010) Influence of efflux pump inhibitors on the multidrug resistance of Helicobacter pylori. World J Gastroenterol 16: 1279-1284.
48. Rafii F, Park M, (2008) Detection and characterization of an ABC transporter in Clostridium hathewayi. Arch Microbiol 190: 417-426.
49. Montville TJ, Bruno ME, (1994) Evidence that dissipation of proton motive force is a common mechanism of action for bacteriocins and other antimicrobial proteins. Int J Food Microbiol 24: 53-74.
50. Ramon-Garcia S, Martin C, Ainsa JA, De Rossi E, (2006) Characterization of tetracycline resistance mediated by the efflux pump Tap from Mycobacterium fortuitum. J Antimicrob Chemother 57: 252-259.
51. Mahamoud A, Chevalier J, Alibert-Franco S, Kern WV, Pages JM, (2007) Antibiotic efflux pumps in Gram-negative bacteria: the inhibitor response strategy. J Antimicrob Chemother 59: 1223-1229.
52. Gustafsson L, Leijonhufvud I, Aronsson A, Mossberg AK, Svanborg C, (2004) Treatment of skin papillomas with topical alpha-lactalbumin-oleic acid. N Engl J Med 350: 2663-2672.
53. Fischer W, Gustafsson L, Mossberg AK, Gronli J, Mork S, et al. (2004) Human alpha-lactalbumin made lethal to tumor cells (HAMLET) kills human glioblastoma cells in brain xenografts by an apoptosis-like mechanism and prolongs survival. Cancer Res 64: 2105-2112.
54. Mossberg AK, Wullt B, Gustafsson L, Mansson W, Ljunggren E, et al. (2007) Bladder cancers respond to intravesical instillation of HAMLET (human alpha-lactalbumin made lethal to tumor cells). Int J Cancer 121: 1352-1359.
55. Mossberg AK, Hou Y, Svensson M, Holmqvist B, Svanborg C, (2010) HAMLET Treatment Delays Bladder Cancer Development. J Urol 183: 1590-1597.
56. Dantas G, Sommer MO, Oluwasegun RD, Church GM, (2008) Bacteria subsisting on antibiotics. Science 320: 100-103.
57. Lemaire S, Fuda C, Van Bambeke F, Tulkens PM, Mobashery S, (2008) Restoration of susceptibility of methicillin-resistant Staphylococcus aureus to beta-lactam antibiotics by acidic pH: role of penicillin-binding protein PBP 2a. J Biol Chem 283: 12769-12776.
58. Ricci V, Tzakas P, Buckley A, Piddock LJ, (2006) Ciprofloxacin-resistant Salmonella enterica serovar Typhimurium strains are difficult to select in the absence of AcrB and TolC. Antimicrob Agents Chemother 50: 38-42.
59. Markham PN, Neyfakh AA, (1996) Inhibition of the multidrug transporter NorA prevents emergence of norfloxacin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 40: 2673-2674.
60. Lomovskaya O, Warren MS, Lee A, Galazzo J, Fronko R, et al. (2001) Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: novel agents for combination therapy. Antimicrob Agents Chemother 45: 105-116.
61. Harigaya Y, Ngo D, Lesse AJ, Huang V, Tsuji BT, (2011) Characterization of heterogeneous vancomycin-intermediate resistance, MIC and accessory gene regulator (agr) dysfunction among clinical bloodstream isolates of Staphyloccocus aureus. BMC Infect Dis 11: 287.
62. Fuchs PC, Barry AL, Brown SD, (2002) In vitro bactericidal activity of daptomycin against staphylococci. J Antimicrob Chemother 49: 467-470.
63. Bakar NS, Zin NM, Basri DF, (2012) Synergy of flavone with vancomycin and oxacillin against vancomycin-intermediate Staphyloccus aureus. Pak J Pharm Sci 25: 633-638.
64. Nobmann P, Bourke P, Dunne J, Henehan G, (2010) In vitro antimicrobial activity and mechanism of action of novel carbohydrate fatty acid derivatives against Staphylococcus aureus and MRSA. J Appl Microbiol 108: 2152-2161.
65. Nuryastuti T, van der Mei HC, Busscher HJ, Iravati S, Aman AT, et al. (2009) Effect of cinnamon oil on icaA expression and biofilm formation by Staphylococcus epidermidis. Appl Environ Microbiol 75: 6850-6855.
66. Margolis E, (2009) Hydrogen peroxide-mediated interference competition by Streptococcus pneumoniae has no significant effect on Staphylococcus aureus nasal colonization of neonatal rats. J Bacteriol 191: 571-575.
67. Marks LR, Parameswaran GI, Hakansson AP, (2012) Pneumococcal interactions with epithelial cells are crucial for optimal biofilm formation and colonization in vitro and in vivo. Infect Immun 80: 2744-2760.
68. Breeuwer P, Drocourt J, Rombouts FM, Abee T, (1996) A Novel Method for Continuous Determination of the Intracellular pH in Bacteria with the Internally Conjugated Fluorescent Probe 5 (and 6-)-Carboxyfluorescein Succinimidyl Ester. Appl Environ Microbiol 62: 178-183.
69. Corvini PF, Gautier H, Rondags E, Vivier H, Goergen JL, et al. (2000) Intracellular pH determination of pristinamycin-producing Streptomyces pristinaespiralis by image analysis. Microbiology 146: 2671-2678.
70. Cottagnoud P, Cottagnoud M, Tauber MG, (2003) Vancomycin acts synergistically with gentamicin against penicillin-resistant pneumococci by increasing the intracellular penetration of gentamicin. Antimicrob Agents Chemother 47: 144-147.