Rapid bactericidal action of alpha-mangostin against MRSA as an outcome of membrane targeting

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 2, 2013, Pages 834-844

  Koh, Jun Jie ^a,b   Qiu, Shengxiang ^c   Zou, Hanxun ^a   Lakshminarayanan, Rajamani ^a   Li, Jianguo ^a,d   Zhou, Xiaojun ^c   Tang, Charles ^e   Saraswathi, Padmanabhan ^a   Verma, Chandra ^a,d,f,g   Tan, Donald T H ^a,h   Tan, Ai Ling ^e   Liu, Shouping ^a   Beuerman, Roger W ^a,b,i  

^a SINGAPORE EYE RESEARCH INSTITUTE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c SOUTH CHINA INSTITUTE OF BOTANY   (China)

^d BIOINFORMATICS INSTITUTE   (Singapore)

^e SINGAPORE GENERAL HOSPITAL   (Singapore)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^g NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^h SINGAPORE NATIONAL EYE CENTRE   (Singapore)

ⁱ DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

Mangostin; Antimicrobial; Garcinia mangostana; Mangosteen; Membrane targeting; MRSA

Indexed keywords

ALPHA MANGOSTIN; ANTIINFECTIVE AGENT; CALCEIN; GARCINIA MANGOSTANA EXTRACT; PLANT EXTRACT; UNCLASSIFIED DRUG; XANTHONE DERIVATIVE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BIOPHYSICS; CELL COMPOSITION; CELL MEMBRANE; CELL VACUOLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENCY; DRUG STRUCTURE; FLUORESCENCE; GRAM POSITIVE BACTERIUM; HYDROPHOBICITY; IN VITRO STUDY; MEMBRANE DAMAGE; MEMBRANE PERMEABILITY; MEMBRANE POTENTIAL; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR DYNAMICS; MOLECULAR PROBE; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY;

ANIMALS; ANTI-BACTERIAL AGENTS; BIOPHYSICS; CELL MEMBRANE; CYTOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHIDIUM; FLUORESCEINS; FLUORESCENT DYES; GRAM-POSITIVE BACTERIA; HEMOLYSIS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MEMBRANE POTENTIALS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ELECTRON, SCANNING; MODELS, CHEMICAL; ORGANIC CHEMICALS; PERMEABILITY; RABBITS; TIME FACTORS; XANTHONES;

BACTERIA (MICROORGANISMS); GARCINIA MANGOSTANA; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; POSIBACTERIA;

EID: 84871738548     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.09.004     Document Type: Article

References (67)

1. R.H. Deurenberg, and E.E. Stobberingh The molecular evolution of hospital- and community-associated methicillin-resistant Staphylococcus aureus Curr. Mol. Med. 9 2009 100 115
2. D.A. Talan, A. Krishnadasan, R.J. Gorwitz, G.E. Fosheim, B. Limbago, V. Albrecht, and G.J. Moran Comparison of Staphylococcus aureus from skin and soft-tissue infections in US emergency department patients, 2004 and 2008 Clin. Infect. Dis. 53 2011 144 149
3. G.J. Moran, A. Krishnadasan, R.J. Gorwitz, G.E. Fosheim, L.K. McDougal, R.B. Carey, and D.A. Talan Methicillin-resistant S. aureus infections among patients in the emergency department N. Engl. J. Med. 355 2006 666 674
4. M.Z. David, and R.S. Daum Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic Clin. Microbiol. Rev. 23 2010 616 687
5. J.A. Otter, and G.L. French Community-associated meticillin-resistant Staphylococcus aureus strains as a cause of healthcare-associated infection J. Hosp. Infect. 79 2011 189 193
6. R.L. Skov, and K.S. Jensen Community-associated meticillin-resistant Staphylococcus aureus as a cause of hospital-acquired infections J. Hosp. Infect. 73 2009 364 370
7. S.E. Cosgrove, Y. Qi, K.S. Kaye, S. Harbarth, A.W. Karchmer, and Y. Carmeli The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: mortality, length of stay, and hospital charges Infect. Control Hosp. Epidemiol. 26 2005 166 174
8. F. von Nussbaum, M. Brands, B. Hinzen, S. Weigand, and D. Habich Antibacterial natural products in medicinal chemistry - exodus or revival? Angew. Chem. Int. Ed. Engl. 45 2006 5072 5129
9. J. Pedraza-Chaverri, N. Cárdenas-Rodríguez, M. Orozco-Ibarra, and J.M. Pérez-Rojas Medicinal properties of mangosteen (Garcinia mangostana) Food Chem. Toxicol. 46 2008 3227 3239
10. D. Obolskiy, I. Pischel, N. Siriwatanametanon, and M. Heinrich Garcinia mangostana L.: a phytochemical and pharmacological review Phytother. Res. 23 2009 1047 1065
11. Y. Sakagami, M. Iinuma, K.G.N.P. Piyasena, and H.R.W. Dharmaratne Antibacterial activity of α-mangostin against vancomycin resistant enterococci (VRE) and synergism with antibiotics Phytomedicine 12 2005 203 208
12. N. Boonnak, C. Karalai, S. Chantrapromma, C. Ponglimanont, H.-K. Fun, A. Kanjana-Opas, and S. Laphookhieo Bioactive prenylated xanthones and anthraquinones from Cratoxylum formosum ssp. pruniflorum Tetrahedron 62 2006 8850 8859
13. S. Deachathai, W. Mahabusarakam, S. Phongpaichit, and W.C. Taylor Phenolic compounds from the fruit of Garcinia dulcis Phytochemistry 66 2005 2368 2375
14. M. Iinuma, H. Tosa, T. Tanaka, F. Asai, Y. Kobayashi, R. Shimano, and K. Miyauchi Antibacterial activity of xanthones from guttiferaeous plants against methicillin-resistant Staphylococcus aureus J. Pharm. Pharmacol. 48 1996 861 865
15. B.M. Sundaram, C. Gopalakrishnan, S. Subramanian, D. Shankaranarayanan, and L. Kameswaran Antimicrobial activities of Garcinia mangostana Planta Med. 48 1983 59 60
16. W. Mahabusarakam, P. Wiriyachitra, and S. Phongpaichit Antimicrobial activities of chemical constituents from Garcinia mangostana J. Sci. Soc. Thai. 12 1986 239 242
17. R. Kaomongkolgit, K. Jamdee, and N. Chaisomboon Antifungal activity of alpha-mangostin against Candida albicans J. Oral Sci. 51 2009 401 406
18. P.T.M. Nguyen, and R.E. Marquis Antimicrobial actions of α-mangostin against oral streptococci Can. J. Microbiol. 57 2011 217 225
19. P. Grohs, M.D. Kitzis, and L. Gutmann In vitro bactericidal activities of linezolid in combination with vancomycin, gentamicin, ciprofloxacin, fusidic acid, and rifampin against Staphylococcus aureus Antimicrob. Agents Chemother. 47 2003 418 420
20. Y. Bai, S. Liu, P. Jiang, L. Zhou, J. Li, C. Tang, C. Verma, Y. Mu, R.W. Beuerman, and K. Pervushin Structure-dependent charge density as a determinant of antimicrobial activity of peptide analogues of defensin Biochemistry 48 2009 7229 7239
21. S.P. Liu, L. Zhou, R. Lakshminarayanan, and R.W. Beuerman Multivalent antimicrobial peptides as therapeutics: design principles and structural diversities Int. J. Pept. Res. Ther. 16 2010 199 213
22. J. Isaksson, B.O. Brandsdal, M. Engqvist, G.E. Flaten, J.S. Svendsen, and W. Stensen A synthetic antimicrobial peptidomimetic (LTX 109): stereochemical impact on membrane disruption J. Med. Chem. 54 2011 5786 5795
23. Y. Zhang, Z. Song, J. Hao, S. Qiu, and Z. Xu Two new prenylated xanthones and a new prenylated tetrahydroxanthone from the pericarp of Garcinia mangostana Fitoterapia 81 2010 595 599
24. X.J. Zhou, R.M. Huang, J. Hao, H.J. Huang, M.Q. Fu, Z.F. Xu, Y.M. Zhou, X.E. Li, and S.X. Qiu Two new prenylated xanthones from the pericarp of Garcinia mangostana (mangosteen) Helv. Chim. Acta 94 2011 2092 2098
25. G.J. Bennett, H.H. Lee, and L.P. Lee Synthesis of minor xanthones from Garcinia mangostana J. Nat. Prod. 53 1990 1463 1470
26. S.X. Chen, M. Wan, and B.N. Loh Active constituents against HIV-1 protease from Garcinia mangostana Planta Med. 62 1996 381 382
27. S. Sakai, M. Katsura, H. Takayama, N. Aimi, N. Chokethaworn, and M. Suttajit The structure of garcinone E Chem. Pharm. Bull. (Tokyo) 41 1993 958 960
28. W. Mahabusarakam, and P. Wiriyachitra Chemical constituents of Garcinia mangostana J. Nat. Prod. 50 1987 474 478
29. S. Suksamrarn, O. Komutiban, P. Ratananukul, N. Chimnoi, N. Lartpornmatulee, and A. Suksamrarn Cytotoxic prenylated xanthones from the young fruit of Garcinia mangostana Chem. Pharm. Bull. (Tokyo) 54 2006 301 305
30. D.J. Farrell, M. Robbins, W. Rhys-Williams, and W.G. Love Investigation of the potential for mutational resistance to XF-73, retapamulin, mupirocin, fusidic acid, daptomycin, and vancomycin in methicillin-resistant Staphylococcus aureus isolates during a 55-passage study Antimicrob. Agents Chemother. 55 2011 1177 1181
31. M. Wu, and R.E. Hancock Interaction of the cyclic antimicrobial cationic peptide bactenecin with the outer and cytoplasmic membrane J. Biol. Chem. 274 1999 29 35
32. D. Liu, and W.F. DeGrado De novo design, synthesis, and characterization of antimicrobial beta-peptides J. Am. Chem. Soc. 123 2001 7553 7559
33. Y. Jin, H. Mozsolits, J. Hammer, E. Zmuda, F. Zhu, Y. Zhang, M.I. Aguilar, and J. Blazyk Influence of tryptophan on lipid binding of linear amphipathic cationic antimicrobial peptides Biochemistry 42 2003 9395 9405
34. Avanti Polar Lipids, Inc, Extrusion technique http://www.avantilipids. com/index.php?option=com-content&view=article&id=1686&Itemid=405 assessed on 23 May 2012
35. Avanti Polar Lipids, Inc, determination of total phosphorus http://www.avantilipids.com/index.php?option=com-content&view= article&id=1686&Itemid=405 accessed on 23 May 2012
36. D.E. Vance, and J. Vance Biochemistry of Lipids, Lipoproteins and Membranes 2nd ed. 1991 Elsevier Science Amsterdam
37. W. Zhao, T. Rog, A.A. Gurtovenko, I. Vattulainen, and M. Karttunen Role of phosphatidylglycerols in the stability of bacterial membranes Biochimie 90 2008 930 938
38. C. Oostenbrink, A. Villa, A.E. Mark, and W.F. van Gunsteren A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6 J. Comput. Chem. 25 2004 1656 1676
39. H. Berendsen, J. Postma, W.v. Gunsteren, and J. Hermans B. Pullman, Intermolecular Forces 1981 Reidel Dordrecht
40. A.K. Malde, L. Zuo, M. Breeze, M. Stroet, D. Poger, P.C. Nair, C. Oostenbrink, and A.E. Mark An automated force field topology builder (ATB) and repository: version 1.0 J. Chem. Theory Comput. 2011 111115094412000
41. P. Bjelkmar, P. Larsson, M.A. Cuendet, B. Hess, and E. Lindahl Implementation of the CHARMM force field in GROMACS: analysis of protein stability effects from correction maps, virtual interaction sites, and water models J. Chem. Theory Comput. 6 2010 459 466
42. CLSI Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement CLSI document M100-S21 31 2011
43. R.W. Finberg, R.C. Moellering, F.P. Tally, W.A. Craig, G.A. Pankey, E.P. Dellinger, M.A. West, M. Joshi, P.K. Linden, K.V. Rolston, J.C. Rotschafer, and M.J. Rybak The importance of bactericidal drugs: future directions in infectious disease Clin. Infect. Dis. 39 2004 1314 1320
44. E.A. Coyle, and M.J. Rybak Activity of oritavancin (LY333328), an investigational glycopeptide, compared to that of vancomycin against multidrug-resistant Streptococcus pneumoniae in an in vitro pharmacodynamic model Antimicrob. Agents Chemother. 45 2001 706 709
45. L.T. Nguyen, E.F. Haney, and H.J. Vogel The expanding scope of antimicrobial peptide structures and their modes of action Trends Biotechnol. 29 2011 464 472
46. C.R. Dawson, A.F. Drake, J. Helliwell, and R.C. Hider The interaction of bee melittin with lipid bilayer membranes Biochim. Biophys. Acta 510 1978 75 86
47. D.A. Beauregard, D.H. Williams, M.N. Gwynn, and D.J. Knowles Dimerization and membrane anchors in extracellular targeting of vancomycin group antibiotics Antimicrob. Agents Chemother. 39 1995 781 785
48. C.W. Stratton, C. Liu, H.B. Ratner, and L.S. Weeks Bactericidal activity of deptomycin (LY146032) compared with those of ciprofloxacin, vancomycin, and ampicillin against enterococci as determined by kill-kinetic studies Antimicrob. Agents Chemother. 31 1987 1014 1016
49. G.N. Tew, D. Clements, H. Tang, L. Arnt, and R.W. Scott Antimicrobial activity of an abiotic host defense peptide mimic Biochim. Biophys. Acta 1758 2006 1387 1392
50. K. Nusslein, L. Arnt, J. Rennie, C. Owens, and G.N. Tew Broad-spectrum antibacterial activity by a novel abiogenic peptide mimic Microbiology 152 2006 1913 1918
51. N. Cotroneo, R. Harris, N. Perlmutter, T. Beveridge, and J.A. Silverman Daptomycin exerts bactericidal activity without lysis of Staphylococcus aureus Antimicrob. Agents Chemother. 52 2008 2223 2225
52. E. Martinez-Abundis, N. Garcia, F. Correa, S. Hernandez-Resendiz, J. Pedraza-Chaverri, and C. Zazueta Effects of alpha-mangostin on mitochondrial energetic metabolism Mitochondrion 10 2010 151 157
53. 2 +-ATPase-dependent apoptosis via mitochondrial pathway in PC12 cells J. Pharmacol. Sci. 95 2004 33 40
54. R. Hovius, H. Lambrechts, K. Nicolay, and B. de Kruijff Improved methods to isolate and subfractionate rat liver mitochondria. Lipid composition of the inner and outer membrane Biochim. Biophys. Acta 1021 1990 217 226
55. M. Dathe, and T. Wieprecht Structural features of helical antimicrobial peptides: their potential to modulate activity on model membranes and biological cells Biochim. Biophys. Acta 1462 1999 71 87
56. R.F. Epand, J.E. Pollard, J.O. Wright, P.B. Savage, and R.M. Epand Depolarization, bacterial membrane composition, and the antimicrobial action of ceragenins Antimicrob. Agents Chemother. 54 2010 3708 3713
57. J.A. Silverman, N.G. Perlmutter, and H.M. Shapiro Correlation of daptomycin bactericidal activity and membrane depolarization in Staphylococcus aureus Antimicrob. Agents Chemother. 47 2003 2538 2544
58. X.Z. Lai, Y. Feng, J. Pollard, J.N. Chin, M.J. Rybak, R. Bucki, R.F. Epand, R.M. Epand, and P.B. Savage Ceragenins: cholic acid-based mimics of antimicrobial peptides Acc. Chem. Res. 41 2008 1233 1240
59. M.K. Hayden, K. Rezai, R.A. Hayes, K. Lolans, J.P. Quinn, and R.A. Weinstein Development of daptomycin resistance in vivo in methicillin-resistant Staphylococcus aureus J. Clin. Microbiol. 43 2005 5285 5287
60. L.Y. Hsu, M. Leong, M. Balm, D.S. Chan, P. Huggan, T.Y. Tan, T.H. Koh, P.Y. Hon, and M.M. Ng Six cases of daptomycin-non-susceptible Staphylococcus aureus bacteraemia in Singapore J. Med. Microbiol. 59 2010 1509 1513
61. D.J. Skiest Treatment failure resulting from resistance of Staphylococcus aureus to daptomycin J. Clin. Microbiol. 44 2006 655 656
62. L. Friedman, J.D. Alder, and J.A. Silverman Genetic changes that correlate with reduced susceptibility to daptomycin in Staphylococcus aureus Antimicrob. Agents Chemother. 50 2006 2137 2145
63. U. Bertsche, C. Weidenmaier, D. Kuehner, S.J. Yang, S. Baur, S. Wanner, P. Francois, J. Schrenzel, M.R. Yeaman, and A.S. Bayer Correlation of daptomycin resistance in a clinical Staphylococcus aureus strain with increased cell wall teichoic acid production and d-alanylation Antimicrob. Agents Chemother. 55 2011 3922 3928
64. A. Peschel, R.W. Jack, M. Otto, L.V. Collins, P. Staubitz, G. Nicholson, H. Kalbacher, W.F. Nieuwenhuizen, G. Jung, A. Tarkowski, K.P. van Kessel, and J.A. van Strijp Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine J. Exp. Med. 193 2001 1067 1076
65. H.R.W. Dharmaratne, Y. Sakagami, K.G.P. Piyasena, and V. Thevanesam Antibacterial activity of xanthones from Garcinia mangostana (L.) and their structure-activity relationship studies Nat. Prod. Res. 2012 1 4
66. Y. Wang, Z. Xia, J.R. Xu, Y.X. Wang, L.N. Hou, Y. Qiu, and H.Z. Chen Alpha-mangostin, a polyphenolic xanthone derivative from mangosteen, attenuates beta-amyloid oligomers-induced neurotoxicity by inhibiting amyloid aggregation Neuropharmacology 62 2012 871 881
67. OECD Test No. 117: Partition Coefficient (n-Octanol/Water), HPLC Method 2004 OECD Publishing