The DOI matches its Crossref record; 51 of the 52 references it cites were found in a registry or an index.
In Vitro Resistance of Staphylococcus aureus to Thrombin-Induced Platelet Microbicidal Protein Is Associated with Alterations in Cytoplasmic Membrane Fluidity
Open accessAbstract
Platelet microbicidal proteins (PMPs) are small, cationic peptides which possess potent microbicidal activities against common bloodstream pathogens, such as Staphylococcus aureus. We previously showed that S. aureus strains exhibiting resistance to thrombin-induced PMP (tPMP-1) in vitro have an enhanced capacity to cause human and experimental endocarditis (T. Wu, M. R. Yeaman, and A. S. Bayer, Antimicrob. Agents Chemother. 38:729-732, 1994; A. S. Bayer et al., Antimicrob. Agents Chemother. 42:3169-3172, 1998; V. K. Dhawan et al., Infect. Immun. 65:3293-3299, 1997). However, the mechanisms mediating tPMP-1 resistance in S. aureus are not fully delineated. The S. aureus cell membrane appears to be a principal target for the action of tPMP-1. To gain insight into the basis of tPMP-1 resistance, we compared several parameters of membrane structure and function in three tPMP-1-resistant (tPMP-1(r)) strains and their genetically related, tPMP-1-susceptible (tPMP-1(s)) counterpart strains. The tPMP-1(r) strains were derived by three distinct methods: transposon mutagenesis, serial passage in the presence of tPMP-1 in vitro, or carriage of a naturally occurring multiresistance plasmid (pSK1). All tPMP-1(r) strains were found to possess elevated levels of longer-chain, unsaturated membrane lipids, in comparison to their tPMP-1(s) counterparts. This was reflected in corresponding differences in cell membrane fluidity in the strain pairs, with tPMP-1(r) strains exhibiting significantly higher degrees of fluidity as assessed by fluorescence polarization. These data provide further support for the concept that specific alterations in the cytoplasmic membrane of S. aureus strains are associated with tPMP-1 resistance in vitro.
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“The lipid profile of resting cells shows reorganisation after treatment with EO compounds, and many authors have described the bacterial fatty acid synthesis pathway as an optimal target of many antibacterial agents [73,74,75].”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [74]
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“An increase in the amount of SFAs in the membrane lipid bilayer results in a loss of membrane fluidity and a consequent increase in membrane rigidity [74].”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [74]
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Cites
Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility
Hiramatsu, K. (1997) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/40.1.135 · Cited by 1,984
Fluidity parameters of lipid regions determined by fluorescence polarization
Shinitzky, M., & Barenholz, Y. (1978) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/0304-4157(78)90010-2 · Cited by 1,885
Stubbs, C. D., & Smith, A. D. (1984) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/0304-4157(84)90005-4 · Cited by 1,618
Epidemiology of Drug Resistance: Implications for a Post—Antimicrobial Era
Cohen, M. L. (1992) · Science · doi:10.1126/science.257.5073.1050 · Cited by 1,310
The staphylococci in human disease
Crossley, K., & Archer, G. L. (1996) · Churchill Livingstone eBooks · Cited by 625
Prasad, R., De Wergifosse, P., Goffeau, A., & Balzi, E. (1995) · Current Genetics · doi:10.1007/bf00352101 · Cited by 486
Shafer, W. M., Qu, X. D., Waring, A. J., & Lehrer, R. I. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.4.1829 · Cited by 391
Ruhr, E., & Sahl, H. (1985) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.27.5.841 · Cited by 377
Bechinger, B., ZASLOFF, M. A., & Opella, S. J. (1993) · Protein Science · doi:10.1002/pro.5560021208 · Cited by 360
The Role of Platelets in Antimicrobial Host Defense
Yeaman, M. R. (1997) · Clinical Infectious Diseases · doi:10.1086/516120 · Cited by 308
Research works printed but not linked: 2
- 10.1001/archinte.1995.00430110089009 · DOI · Paper page
- Tang Y. Q. Yeaman M. R. Selsted M. E. Purification, characterization, and antimicrobial properties of peptides released from thrombin-induced human platelets.Blood861995556a (Abstract 3626.)
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Schmidt, R., Ding, Y., & Hoffmann, R. (2017) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2017.11.008 · Cited by 20
Fang, Y., Blair, H. T., Zhong, R., Sun, H., & Zhou, D. (2016) · Small Ruminant Research · doi:10.1016/j.smallrumres.2016.04.012 · Cited by 18
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“an increased level of longerchain, unsaturated fatty acid leads to an altered fluidity of the membrane, which results in decreased sensitivity for platelet-derived CaMPs [1].”
BackgroundRamírez, G. A. T., & Osório, J. C. C. (2010) · Infectio · doi:10.1016/s0123-9392(10)70093-x · Cited by 15
Studies on the Mechanism of Telavancin Decreased Susceptibility in a Laboratory-Derived Mutant
Song, Y., Lunde, C. S., Benton, B. M., & Wilkinson, B. J. (2013) · Microbial Drug Resistance · doi:10.1089/mdr.2012.0195 · Cited by 15
Nakonieczna, J., Kossakowska-Zwierucho, M., Filipiak, M., Hewelt-Belka, W., Grinholc, M., & Bielawski, K. P. (2015) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-7145-5 · Cited by 14
“5-hexatriane (DPH) probe (Sigma-Aldrich, Munich, Germany), according to modified protocols described by Bayer and Voss (Bayer et al. 2000; Voss and Montville 2014).”
BackgroundMethodInfluentialLesmes, L. P., Bohorquez, M. Y., Carreño, L. F., Patarroyo, M. E., & Lozano, J. M. (2009) · Peptides · doi:10.1016/j.peptides.2009.08.011 · Cited by 14
“aureus ISP479VC and ISP479R, it did not induce membrane permeabilization [4], but did induce pore formation in other strains such as S.”
Douglas, E. J. A., Palk, N., Rudolph, E. R., & Laabei, M. (2025) · Microbiology · doi:10.1099/mic.0.001563 · Cited by 19
“For example, S. aureus strains with higher levels of saturated membrane lipids have increased membrane rigidity compared with strains with elevated levels of polyunsaturated lipids [64].”
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Balatti, G. E., Domene, C., Martini, M. F., & Pickholz, M. (2020) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.0c00855 · Cited by 13
Narayanaswamy, V. P., Giatpaiboon, S., Uhrig, J. P., Orwin, P. M., Wiesmann, W. P., Baker, S., & Townsend, S. M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0191522 · Cited by 14
Lu, Q., Xie, Y., Gu, F., Tu, C., He, J., Guo, Q., Wu, Y., Xu, M., & Ji, L. H. (2023) · Physiological and Molecular Plant Pathology · doi:10.1016/j.pmpp.2023.102117 · Cited by 12
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“8 U of lysostaphin (A&A Biotechnology, Poland) in the presence of 3 U of DNase I (EURx, Poland) for 1 h at 37 °C [29].”
BackgroundMethodLi, J., Cui, Z., Zhao, S., & Sidman, R. L. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0308 · Cited by 12
He, L., Lv, Y., Xu, J., Chen, C., & Shuntang, G. (2021) · Food & Function · doi:10.1039/d0fo03478a · Cited by 11
Lew, C. I., Mishra, N. N., Bayer, A. S., & Rose, W. E. (2021) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00356-21 · Cited by 12
“Methods for DPH incorporation into the CM, measurement of fluorescence polarization, and calculation of the polarization index have been previously described in detail (44).”
MethodLipid tails modulate antimicrobial peptide membrane incorporation and activity
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Zhang, H., Morikawa, K., Ohta, T., & Kato, Y. (2005) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dki070 · Cited by 11
Zhao, J., Qian, J., Zhuang, H., Luo, J., Huang, M., Yan, W., & Zhang, J. (2021) · Foods · doi:10.3390/foods10122976 · Cited by 10
“It is well known that the fatty acid composition in lipids directly influences the fluidity of the cell membrane [31].”
BackgroundHost Defense Peptides: Bridging Antimicrobial and Immunomodulatory Activities*
Kindrachuk, J., Nijnik, A., & Hancock, R. E. W. (2010) · Elsevier eBooks · doi:10.1016/b978-008045382-8.00112-x · Cited by 10
Hong-liang, Y., Liu, X., & Liu, Y. (2015) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2014.15.23.10469 · Cited by 10
“…2014 10471 Transplanted Tumor Erythrocyte Membrane Fluidity and Blocking Degree of Functionality activities in accordance with the membrane structure and function of the plasma membrane, or cell membrane fluidity is important in maintaining normal cell physiological function (Bayer et al., 2000).”
BackgroundPlatelets and platelet inhibitors in infective endocarditis
Hoen, B. (2002) · Current Infectious Disease Reports · doi:10.1007/s11908-002-0021-3 · Cited by 10
“Bayer et al. [12, 13 ] also described clinical S. aureus strains with naturally occurring reductions in their in vitro tPMP susceptibility.”
BackgroundGodlewska, A., Pawlak, K., & Jańczewski, D. (2025) · Advances in Colloid and Interface Science · doi:10.1016/j.cis.2025.103738 · Cited by 9
Fluorescence Polarization (FP) Assay for Measuring Staphylococcus aureus Membrane Fluidity
Tiwari, K. B., Sen, S., Gatto, C., & Wilkinson, B. J. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1550-8_8 · Cited by 9
Effects of SecDF on the antimicrobial functions of cathelicidins against Staphylococcus aureus
Blodkamp, S., Kadlec, K., Gutsmann, T., Quiblier, C., Naim, H. Y., Schwarz, Š., & von Köckritz‐Blickwede, M. (2016) · Veterinary Microbiology · doi:10.1016/j.vetmic.2016.03.021 · Cited by 9
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“It was previously reported that UFAs and BCFAs fluidized the bacterial membranes because of the loose and disordered arrangement within their molecular structures, while SFAs associated with reduced membrane fluidity and increased rigidity due to the tighter degree of molecular packing order (Bayer et al. 2000).”
BackgroundMechanisms and Significance of Bacterial Resistance to Human Cationic Antimicrobial Peptides
Goytia, M., Kandler, J. L., & Shafer, W. (2013) · Springer eBooks · doi:10.1007/978-3-0348-0541-4_9 · Cited by 9
Meena, S., Mehla, J., Kumar, R., & Sood, S. K. (2016) · Current Microbiology · doi:10.1007/s00284-016-1090-0 · Cited by 6
Microbiology of Infective Endocarditis and Clinical Correlates: Gram-Positive Organisms
Brusch, J. L. (2007) · Infectious disease and therapy · doi:10.3109/9781420019834.002 · Cited by 5
Membrane viscosity is a major modulating factor of the enterocin CRL35 activity
Minahk, C. J., Saavedra, L., Sesma, F. J. M., & Morero, R. D. (2004) · Biochimie · doi:10.1016/j.biochi.2004.10.013 · Cited by 4
Köhler, C., Proctor, R. A., Bayer, A. S., Yeaman, M. R., Lalk, M., Engelmann, S., & Mishra, N. N. (2019) · Antibiotics · doi:10.3390/antibiotics8040169 · Cited by 4
“Bacterial growth entails a substantial portion of the acyl chains of lipids in membrane to maintain the optimum level of fluidity/rigidity [9,10,24].”
BackgroundResultBacterial Resistance to Host Defence Peptides
Phoenix, D. A., Dennison, S. R., & Harris, F. (2016) · Springer eBooks · doi:10.1007/978-3-319-32949-9_7 · Cited by 4
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Tirant, M., Tirant, H., & Wollina, U. (2024) · Open Access Macedonian Journal of Medical Sciences · doi:10.3889/oamjms.2024.11888 · Cited by 3
“These effects are exerted simultaneously with the aid of essential oil components rather than a single phytochemical compound, and this would ultimately increase the amount of fatty acids, decrease membrane fluidity, and increase membrane rigidity [189].”
BackgroundPalraj, R., Knoll, B. M., Baddour, L. M., & Wilson, W. R. (2015) · Elsevier eBooks · doi:10.1016/b978-1-4557-4801-3.00083-7 · Cited by 4
Zhang, L., Xiaolin, L., Wang, Z., Liu, Z., Chen, J., Zhang, Y., Cao, B. W., Fu, Y., Yin, Z., Peng, D., et al. (2025) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5c02951 · Cited by 2
Stress responses of Gram-positive bacteria to cationic antimicrobial peptides
Pietiäinen, M. (2010) · Työväentutkimus Vuosikirja · Cited by 2
Canè, C., Gallucci, N., Amoresano, A., Fontanarosa, C., Paduano, L., Gregorio, E. D., Duilio, A., & Somma, A. D. (2024) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2024.101808 · Cited by 1
“…involved in fatty acid biosynthesis were also found upregulated in a S. aureus mutant with a decreased telavancin susceptibility [30] and increased amounts of longer-chain, unsaturated fatty acids were found in S. aureus strains resistant to thrombin-induced platelet microbicidal proteins [31].”
BackgroundStaphylococcus aureus Cell Envelope as a Target of (‐)‐Globulol
Liu, R., Yang, H., Qi, W., Wang, H., He, X., Yi, Q., & Wang, L. (2026) · Cellular Microbiology · doi:10.1155/cmi/8895641 · Cited by 1
Díaz, D. A. R. (2012) · instname:Universidad de los Andes · Cited by 1
Boudjemaa, R., Briandet, R., Steenkeste, K., & Fontaine‐Aupart, M. (2017) · Wiley eBooks · doi:10.1002/9780470027318.a9606 · Cited by 1
Review Arming the enemy: the evolution of resistance to self-proteins
Bell, G., & Gouyon, P. (2003)
Grkovic, S., Jones, T., Mukhopadhay, K., Yeaman, M. R., Bayer, A. S., Kupferwasser, L. I., Brown, M. H., & Skurray, R. A. (2012)
Santoro, D. (2013) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Antibacterial activity and mechanism of action of lipophilic antioxidants.
Ooi, N. (2013) · White Rose eTheses Online (University of Leeds, The University of Sheffield, University of York)
D’Asta, F. (2018) · University of Birmingham Institutional Research Archive (University of Birmingham)
Identification of antimicrobial resistance genes in Escherichia coli through network diffusion
Mansouri, A., Durazzi, F., Ihsan, M. N., Griffin, S., Manfreda, G., Valdramidis, V., Pasquali, F., & Remondini, D. (2025) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkaf404
Metadata
- Authors
- Bayer, A. S., Prasad, R., Chandra, J., Koul, A., Smriti, M., Varma, A., Skurray, R. A., Firth, N., Brown, M. H., Koo, S.-P., & Yeaman, M. R.
- Affiliations
- University of California, Los Angeles (US)
- Jawaharlal Nehru University (IN)
- The University of Sydney (AU)
- ORCID
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2000-06
- Volume
- 68
- Issue
- 6
- Pages
- 3548-3553
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC97641
- OpenAlex
- W2156172406
- Cited by
- 150
- References
- 52
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 4 · 2023: 4 · 2022: 2 · 2021: 8 · 2020: 5 · 2019: 5 · 2018: 7 · 2017: 7 · 2016: 11 · 2015: 7 · 2014: 6 · 2013: 9 · 2012: 14
- FWCI
- 3.64
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Infection and Immunity (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (AI 39108, AI-39001, R01AI039108, R29AI039001, R01AI039001)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
- Life Sciences › Immunology and Microbiology › Microbiology › Antimicrobial Peptides and Activities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Staphylococcus aureus, antimicrobial resistance, membrane lipid composition, endocarditis, cationic antimicrobial peptides, multiresistance plasmid
- MeSH terms
- Amino Acids, Anti-Bacterial Agents, beta-Thromboglobulin, Biological Transport, Blood Proteins, Cell Membrane, DNA Transposable Elements, Drug Resistance, Microbial, Fatty Acids, Membrane Fluidity, Phenotype, Phospholipids, Species Specificity, Staphylococcus aureus, Mutagenesis, Insertional, Chemokines
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