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Correlation between Mutations in liaFSR of Enterococcus faecium and MIC of Daptomycin: Revisiting Daptomycin Breakpoints
Open accessAbstract
Mutations in liaFSR , a three-component regulatory system controlling cell-envelope stress response, were recently linked with the emergence of daptomycin (DAP) resistance in enterococci. Our previous work showed that a liaF mutation increased the DAP MIC of a vancomycin-resistant Enterococcus faecalis strain from 1 to 3 μg/ml (the DAP breakpoint is 4 μg/ml), suggesting that mutations in the liaFSR system could be a pivotal initial event in the development of DAP resistance. With the hypothesis that clinical enterococcal isolates with DAP MICs between 3 and 4 μg/ml might harbor mutations in liaFSR , we studied 38 Enterococcus faecium bloodstream isolates, of which 8 had DAP MICs between 3 and 4 μg/ml by Etest in Mueller-Hinton agar. Interestingly, 6 of these 8 isolates had predicted amino acid changes in the LiaFSR system. Moreover, we previously showed that among 6 DAP-resistant E. faecium isolates (MICs of >4 μg/ml), 5 had mutations in liaFSR . In contrast, none of 16 E. faecium isolates with a DAP MIC of ≤2 μg/ml harbored mutations in this system ( P < 0.0001). All but one isolate with liaFSR changes exhibited DAP MICs of ≥16 μg/ml by Etest using brain heart infusion agar (BHIA), a medium that better supports enterococcal growth. Our findings provide a strong association between DAP MICs within the upper susceptibility range and mutations in the liaFSR system. Concomitant susceptibility testing on BHIA may be useful for identifying these E. faecium first-step mutants. Our results also suggest that the current DAP breakpoint for E. faecium may need to be reevaluated.
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“Furthermore, the majority (75%) of DAP-susceptible E. faecium isolates recovered from bacteremic patients whose MIC was in the higher range of susceptibility (i.e. between 3 and 4 μg/mL) harbored mutations in LiaFSR.”
From Mechanisms of Antibiotic Resistance (2016) · cites this paper as [91]
In the citing paper
“Conversely, none of the isolates of the same collection with DAP MIC ≤ 2 μg/mL exhibited changes in this system (91).”
From Mechanisms of Antibiotic Resistance (2016) · cites this paper as [91]
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“The protocol for PCR amplification, DNA purification, sequencing, and analysis has been previously described (8).”
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“On the basis of this case, as well as our previous findings [1], we propose that 2 μg/mL may be a better cutoff for DAP nonsusceptibility in E.”
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“Interestingly, in enterococci the ability of several -lactams, especially ampicillin (AMP), ceftaroline (CPT), and ertapenem (ERT), to provide synergistic activity with DAP and prevent the emergence of DAP nonsusceptibility has also been demonstrated (43, 44).”
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“One area of uncertainty is the use of daptomycin to treat patients with VRE BSI who have daptomycin MICs close to the established susceptibility breakpoint (4 μg/mL), as these organisms frequently harbor mutations associated with daptomycin resistance and tolerance and are most likely to fail daptomycin therapy [34, 3…”
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“At these MICs, mutations that confer DAP inactivity are more prevalent than at lower MIC values, necessitating caution when treating these isolates (18).”
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“These changes are often observed in VREfm strains with DAP MICs below the susceptibility breakpoint that, therefore, are considered susceptible by current standards (27).”
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“These isolates harbor point mutations in the liaFSR genes, which encode a three-component regulatory system involved in cell membrane stress response (10, 11).”
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“Similarly, we were unable to identify a cutoff by Etest or MTS, despite prior data suggesting that these tests are superior to BMD for testing enterococci (11).”
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“Similarly, changes in LiaFSR in clinical strains of Enterococcus faecium led to a loss of DAP bactericidal activity and preceded the emergence of clinical resistance (Munita et al., 2012; 2013).”
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“Among the mutations identified, substitutions in LiaR (W73C), LiaS (T120A) and Cls (H215R and R218Q) are among the most frequently observed [15, 20, 22], although mutations in either gene alone are not sufficient to confer a resistant phenotype in enterococci [16, 19, 21].”
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“It is possible that mutations in other genes such as gdpD and cls (18, 19, 30) contributed to daptomycin heteroresistance.”
Jahanbakhsh, S., Singh, N. B., Yim, J., Kebriaei, R., Smith, J. R., Lev, K. L., Tran, T. T., Rose, W. E., Arias, C. A., & Rybak, M. J. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02074-19 · Cited by 32
“faecium isolates with MIC values between 3 and 4 g/ml harbor changes in the liaFSR system but that these substitutions are rarely found at lower DAP MIC values (26, 27).”
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“faecium clinical isolates) [17, 23] has a direct effect on LiaR oligomerization.”
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“Mutations in liaFSR genes are frequently detected in daptomycin-resistant enterococci (34, 35, 71, 72), and the LiaFSR system is activated and protective of B.”
BackgroundTargeting cell membrane adaptation as a novel antimicrobial strategy
Tran, T. T., Miller, W. R., Shamoo, Y. E., & Arias, C. A. (2016) · Current Opinion in Microbiology · doi:10.1016/j.mib.2016.07.002 · Cited by 22
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“daptomycin (34, 35), coresistance is common in some settings (36).”
BackgroundEcheverría-Esnal, D., Sorlí, L., Navarrete-Rouco, M. E., Prim, N., Barceló‐Vidal, J., Conde‐Estévez, D., Montero, M., Martín‐Ontiyuelo, C., Horcajada, J. P., & Grau, S. (2023) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2023.2223977 · Cited by 22
“faecium bacteremia when MIC of 3–4 mg/L were treated with daptomycin [20,24,122,123].”
MethodEgli, A., Schmid, H., Kuenzli, E., Widmer, A. F., Battegay, M., Plagge, H., Frei, R., Achermann, R., & Weisser, M. (2016) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2016.10.003 · Cited by 22
“in vivo development of daptomycin resistance (17).”
Chong, P. P., van Duin, D., Bangdiwala, A. S., Ivanova, A., Miller, W. C., Weber, D. J., Gilligan, P. H., & Shea, T. C. (2016) · Clinical Therapeutics · doi:10.1016/j.clinthera.2016.09.011 · Cited by 20
Chilambi, G. S., Hinks, J., Matysik, A. S., Zhu, X., Choo, P. Y., Liu, X., Chan‐Park, M. B. E., Bazan, G. C., Kline, K. A., & Rice, S. A. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00155 · Cited by 18
Optimizing therapy for vancomycin-resistant enterococcal bacteremia in children
Tamma, P. D., & Hsu, A. J. (2014) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0000000000000115 · Cited by 18
Udaondo, Z., Jenjaroenpun, P., Wongsurawat, T., Meyers, E., Anderson, C., Lopez, J., Mohan, M., Tytarenko, R. G., Walker, B. A., Ussery, D. W., et al. (2020) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofaa180 · Cited by 17
“Our data therefore support previous studies that argue that DAP exposure is a key driver of resistance development [19, 20] and that DAP-NS genotypes can be present in VREfm strains exhibiting DAP MICs <4 μg/ mL [19, 21].”
ResultWang, G., Kamalakaran, S., Dhand, A., Huang, W., Ojaimi, C., Zhuge, J., Yee, L. L., Mayigowda, P., Surendraiah, P. K. M., Dimitrova, N., et al. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02683-14 · Cited by 18
Carvalhaes, C. G., Sader, H. S., Flamm, R. K., Streit, J. M., & Mendes, R. E. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00175-20 · Cited by 16
“Based on these findings and other evidence (26, 27), CLSI revisited the interpretive breakpoint for daptomycin against E.”
ResultChilambi, G. S., Gao, I. H., Yoon, B. K., Park, S.-H., Kawakami, L. M., Ravikumar, V., Chan‐Park, M. B. E., Cho, N., Bazan, G. C., Kline, K. A., et al. (2018) · RSC Advances · doi:10.1039/c7ra11823f · Cited by 16
[Resistance to "last resort" antibiotics in Gram-positive cocci: The post-vancomycin era].
Rincón, S., Panesso, D., Díaz, L., Carvajal, L. P., Reyes, J., Munita, J. M., & Arias, C. A. (2014) · PubMed · doi:10.1590/s0120-41572014000500022 · Cited by 16
Self-citationBacterial Stress Responses as Determinants of Antimicrobial Resistance
Fruci, M., & Poole, K. (2016) · Wiley eBooks · doi:10.1002/9781119004813.ch10 · Cited by 17
Cusumano, J. A., Khan, R., Shah, Z., Philogene, C., Harrichand, A., & Huang, V. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.00621-22 · Cited by 14
“Experiments were performed using cation adjusted (calcium, 25 mg/mL; magnesium, 12.5 mg/mL) Mueller-Hinton broth (MHB; BD Difco, Sparks, MD).”
MethodInfluentialBelley, A. C., Arhin, F. F., & Moeck, G. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01873-17 · Cited by 14
“Mutant 1527-140-4 (daptomycin MIC, 16 g/ml) contains a single nucleotide polymorphism that encodes an amino acid change (Val129Glu) in LiaS, which is part of the LiaFSR three-component system that has been implicated in reduced susceptibility to daptomycin (12).”
BackgroundTreatment of Vancomycin-Resistant Enterococci: Focus on Daptomycin
Kohinke, R. M., & Pakyz, A. L. (2017) · Current Infectious Disease Reports · doi:10.1007/s11908-017-0589-2 · Cited by 13
Wan, T., Yeo, H., Lee, T.-F., Huang, Y., Hsueh, P., & Chiu, H. (2022) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkac414 · Cited by 13
Kaushik, S., Yadav, J., Das, S., Karthikeyan, D., Chug, R., Jyoti, A., Srivastava, V. K., Jain, A., Kumar, S., & Sharma, V. (2022) · Current Protein and Peptide Science · doi:10.2174/1389203723666220526155644 · Cited by 12
Cusumano, J. A., Daffinee, K. E., Ugalde‐Silva, P., Peti, W., Arthur, M., Desbonnet, C. R., Rice, L. B., LaPlante, K. L., & Garcia-Solache, M. A. (2023) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00871-22 · Cited by 12
“Streaks and colonies were plated onto brain heart infusion agar (BHA; Difco, Becton, Dickinson) due to better growth (1, 14, 42).”
MethodChuang, Y., Lin, H., Wang, J., Yang, J., Lin, C., Huang, S., Chen, Y., & Chang, S. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113710 · Cited by 11
Woods, R. J., Patel, T. S., Nagel, J. L., Newton, D. W., & Read, A. F. (2018) · Infection Control and Hospital Epidemiology · doi:10.1017/ice.2017.279 · Cited by 11
“Several groups have suggested lowering the daptomycin clinical breakpoint for Enterococcus from 4 to 2 μg/mL because patients who have an initial MIC of 3 or 4 μg/mL often have mutations associated with daptomycin nonsusceptibility and may have worse clinical outcomes.(5,10) In our study, only patients whose initial s…”
Antimicrobial tolerance and its role in the development of resistance: Lessons from enterococci
Darnell, R. L., Paxie, O., Rose, F. O. T., Morris, S. M., Krause, A. L., Monk, I. R., Smith, M. J. B., Stinear, T. P., Cook, G. M., & Gebhard, S. (2022) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/bs.ampbs.2022.06.004 · Cited by 11
Mutant prevention concentrations of daptomycin for Enterococcus faecium clinical isolates
Sinel, C., Jaussaud, C., Auzou, M., Giárd, J.-C., & Cattoir, V. (2016) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2016.07.006 · Cited by 11
“Indeed, it has been proposed that an MIC of 3–4 mg/L may be an indicator of possible treatment failure, likely corresponding to a first-step mutant predisposed to develop in vivo highlevel resistance [19].”
BackgroundMenon, V., Davis, R. J., Shackel, N. A., Espedido, B. A., Beukers, A. G., Jensen, S. O., & van Hal, S. J. (2017) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2017.10.017 · Cited by 10
Rossolini, G. M., Arena, F., & Pollini, S. (2013) · Springer eBooks · doi:10.1007/978-3-642-39968-8_2 · Cited by 11
“…system involved in the cell envelope response to antibiotics (liaFSR) or in genes encoding proteins involved in phospholipid metabolism have been associated with daptomycin resistance (Arias et al. 2011; Munita et al. 2012; see Baltz, this volume), but the mechanism of resistance remains unclear.”
BackgroundGodlewska, A., Pawlak, K., & Jańczewski, D. (2025) · Advances in Colloid and Interface Science · doi:10.1016/j.cis.2025.103738 · Cited by 9
Tymoszewska, A., Szylińska, M., & Aleksandrzak‐Piekarczyk, T. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.00343-23 · Cited by 9
Chow, A. L., Win, N.-N., Ng, P. Y., Lee, W., & Win, M.-K. (2016) · Epidemiology and Infection · doi:10.1017/s0950268816000923 · Cited by 8
“Enterococcal isolates with daptomycin MIC 3–4 μg/ml have been observed to harbour mutations in liaFSR, a threecomponent regulatory system controlling cell-envelope stress response, that have been linked with the emergence of daptomycin resistance in enterococci [19].”
BackgroundBelley, A. C., Séguin, D. L., Arhin, F. F., & Moeck, G. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01265-17 · Cited by 8
“Ontario, Canada) was performed using published primer sequences (20).”
MethodRincón, S., Panesso, D., Miller, W. R., Singh, K. V., Cruz, M. R., Khan, A., Dinh, A. Q., Díaz, L., Ríos, R., Shamoo, Y. E., et al. (2019) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiz131 · Cited by 8
“None of the genes have been previously associated with DAP resistance [12, 13, 16, 17], with the exception of those related to sugar phosphotransferase systems [36].”
BackgroundSelf-citationCard, K. J., Crozier, D., Durmaz, A., Gray, J., Creary, J., Stocks, A., Maltas, J., Bonomo, R. A., Burke, Z. D. C., & Scott, J. G. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2507962122 · Cited by 7
“Bacteria evolve thicker cell walls under vancomycin selection that hinder daptomycin entry ( 45 – 48 ), likely explaining this finding as well as clinical accounts of collateral resistance ( 49 ).”
Enterococcal Infections and Drug Resistance Mechanisms
Sarathy, M. V., Balaji, S., & Rao, T. J. M. (2020) · Springer eBooks · doi:10.1007/978-981-15-1695-5_9 · Cited by 7
Pinto, L., Torres, C., Gil, C., Santos, H. M., Capelo, J. L., Borges, V., Gomes, J. P., Silva, C., Vieira, L., Poeta, P. A. C. Q. D., et al. (2020) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2019.0164 · Cited by 5
“LiaFSR has been previously proven to coordinate the cell envelope response to antibiotics (such as to cell wall-interacting vancomycin) in Gram-positive bacteria (Klinzing et al., 2013; Munita et al., 2012).”
Cusumano, J. A., Daffinee, K. E., Piehl, E. C., Garcia-Solache, M. A., Desbonnet, C. R., Rice, L. B., & LaPlante, K. L. (2022) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00426-22 · Cited by 5
“Streaks and colony counts were plated on brain heart infusion agar (BHIA; Difco, Becton Dickinson) due to better growth (9, 34, 35).”
MethodMathpal, S., Panickar, A., Joshi, T., Ramaiah, S., & Anbarasu, A. (2025) · Current Genetics · doi:10.1007/s00294-025-01331-y · Cited by 3
“…resistance is largely associated with mutations in the liaFSR and yycFGHIJ gene clusters, which mediate envelope stress responses, as well as genes related to phospholipid metabolism, such as gdpD (glycerophosphoryl diester phosphodiesterase) and cls (cardiolipin synthetase) (Munita et al. 2012).”
Recent Epidemiological Changes in Infectious Diseases
Pucci, M. J., Callebaut, C., Cathcart, A. L., & Bush, K. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-409547-2.12405-9 · Cited by 4
Morley, V. J., Sim, D. G., Penkevich, A., Woods, R. J., & Read, A. F. (2022) · Evolution Medicine and Public Health · doi:10.1093/emph/eoac035 · Cited by 4
“The three-component LiaFSR system regulates the cellular envelope stress response, which impacts daptomycin susceptibility [25].”
BackgroundNigo, M., Hasbun, R., & Vigil, K. J. (2018) · OBM Transplantation · doi:10.21926/obm.transplant.1804023 · Cited by 3
Paz, D. L., & Tattevin, P. (2026) · Critical Care · doi:10.1186/s13054-026-06011-y · Cited by 3
“Interestingly, higher daptomycin minimal inhibitory concentrations (MIC) are correlated with de novo liaF mutations in E. faecium [7].”
Development of VRE meningitis due to haematogenous spread while on high-dose daptomycin therapy
Sanikommu, S., Lusardi, K. T., Burdine, L. J., & Dare, R. K. (2023) · JAC-Antimicrobial Resistance · doi:10.1093/jacamr/dlad118 · Cited by 2
Metadata
- Authors
- Munita, J. M., Panesso, D., Diaz, L., Tran, T. T., Reyes, J., Wanger, A., Murray, B. E., & Arias, C. A.
- Affiliations
- Universidad del Desarrollo (CL)
- Universidad El Bosque (CO)
- Laboratory for Antimicrobial Research, University of Texas Medical School at Houston, Houston, Texas, USA
- University of Houston (US)
- The University of Texas Health Science Center at Houston (US)
- Venue
- Antimicrobial Agents and Chemotherapy
- Publisher
- American Society for Microbiology
- Published
- 2012-08
- Volume
- 56
- Issue
- 8
- Pages
- 4354-4359
- ISSN
- 0066-4804 (ISSN-L)
- 1098-6596
- PMC
- PMC3421602
- OpenAlex
- W2107978429
- Cited by
- 118
- References
- 37
- Citations by year
- 2026: 8 · 2025: 3 · 2023: 6 · 2022: 12 · 2021: 2 · 2020: 12 · 2019: 4 · 2018: 12 · 2017: 8 · 2016: 17 · 2015: 12 · 2014: 13 · 2013: 7 · 2012: 2
- FWCI
- 4.99
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Antimicrobial Agents and Chemotherapy (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Repositorio Institucional Universidad El Bosque (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (R01AI093749, R00AI072961, R01 AI72961, K99AI072961)
- Topics
- Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
- Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- daptomycin resistance, Enterococcus faecium, minimum inhibitory concentration, envelope stress response, bloodstream isolates, antimicrobial susceptibility testing
- MeSH terms
- Anti-Bacterial Agents, Bacterial Proteins, Base Sequence, Cell Wall, DNA, Bacterial, Microbial Sensitivity Tests, Mutation, Vancomycin, Enterococcus faecium, Sequence Analysis, DNA, Daptomycin, Vancomycin Resistance, Drug Resistance, Bacterial
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