Multilocus sequence type-dependent activity of human and animal cathelicidins against community-, hospital-, and livestock-associated methicillin-resistant Staphylococcus aureus isolates
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Sequence type (ST) 5 methicillin-resistant Staphylococcus aureus (MRSA) with staphylococcal cassette chromosome mec (SCCmec) type II (ST5-MRSA-II) and ST72-MRSA-IV represent the most significant genotypes for healthcare- (HA) and community-associated (CA) MRSA in Korea, respectively. In addition to the human-type MRSA strains, the prevalence of livestock-associated (LA) MRSA clonal lineages, such as ST541 and ST398 LA-MRSA-V in pigs and ST692 LA-MRSA-V and ST188 LA-MRSA-IV in chickens, has recently been found. In this study, clonotype- specific resistance profiles to cathelicidins derived from humans (LL-37), pigs (PMAP- 36), and chickens (CATH-2) were examined using six different ST groups of MRSA strains: ST5 HA-MRSA-II, ST72 CA-MRSA-IV, ST398 LA-MRSA-V, ST541 LA-MRSA-V, ST188 LA-MRSAIV, and ST692 LA-MRSA-V. Phenotypic characteristics often involved in cathelicidin resistance, such as net surface positive charge, carotenoid production, and hydrogen peroxide susceptibility were also determined in the MRSA strains. Human- and animal-type MRSA strains exhibited clonotype-specific resistance profiles to LL-37, PMAP-36, or CATH-2, indicating the potential role of cathelicidin resistance in the adaptation and colonization of human and animal hosts. The ST5 HA-MRSA isolates showed enhanced resistance to all three cathelicidins and hydrogen peroxide than ST72 CA-MRSA isolates by implementing increased surface positive charge and carotenoid production. In contrast, LA-MRSA strains employed mechanisms independent of surface charge regulation and carotenoid production for cathelicidin resistance. These results suggest that human- and livestock-derived MRSA strains use different strategies to counteract the bactericidal action of cathelicidins during the colonization of their respective host species.
Abstract
Sequence type (ST) 5 methicillin-resistant Staphylococcus aureus (MRSA) with staphylococcal cassette chromosome mec (SCCmec) type II (ST5-MRSA-II) and ST72-MRSA-IV represent the most significant genotypes for healthcare- (HA) and community-associated (CA) MRSA in Korea, respectively. In addition to the human-type MRSA strains, the prevalence of livestock-associated (LA) MRSA clonal lineages, such as ST541 and ST398 LA-MRSA-V in pigs and ST692 LA-MRSA-V and ST188 LA-MRSA-IV in chickens, has recently been found. In this study, clonotype- specific resistance profiles to cathelicidins derived from humans (LL-37), pigs (PMAP- 36), and chickens (CATH-2) were examined using six different ST groups of MRSA strains: ST5 HA-MRSA-II, ST72 CA-MRSA-IV, ST398 LA-MRSA-V, ST541 LA-MRSA-V, ST188 LA-MRSAIV, and ST692 LA-MRSA-V. Phenotypic characteristics often involved in cathelicidin resistance, such as net surface positive charge, carotenoid production, and hydrogen peroxide susceptibility were also determined in the MRSA strains. Human- and animal-type MRSA strains exhibited clonotype-specific resistance profiles to LL-37, PMAP-36, or CATH-2, indicating the potential role of cathelicidin resistance in the adaptation and colonization of human and animal hosts. The ST5 HA-MRSA isolates showed enhanced resistance to all three cathelicidins and hydrogen peroxide than ST72 CA-MRSA isolates by implementing increased surface positive charge and carotenoid production. In contrast, LA-MRSA strains employed mechanisms independent of surface charge regulation and carotenoid production for cathelicidin resistance. These results suggest that human- and livestock-derived MRSA strains use different strategies to counteract the bactericidal action of cathelicidins during the colonization of their respective host species.
참고문헌 (54)
- Boswihi SS, "Methicillin-resistant Staphylococcus aureus : an update on the epidemiology, treatment options and infection control", Curr Med Res Pract, 8, pp.18~24 (2018)[DOI]
- Kondo Y, "Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment : rapid identification system for mec, ccr, and major differences in junkyard regions", Antimicrob Agents Chemother, 51, pp.264~274 (2007)[DOI]
- Davis KA, "Methicillin-resistant Staphylococcus aureus(MRSA)nares colonization at hospital admission and its effect on subsequent MRSA infection", Clin Infect Dis, 39, pp.776~782 (2004)[DOI]
- Gould IM, "The clinical significance of methicillin-resistant Staphylococcus aureus", J Hosp Infect, 61, pp.277~282 (2005)[DOI]
- Lakhundi S, "Methicillin-resistant Staphylococcus aureus : molecular characterization, evolution, and epidemiology", Clin Microbiol Rev, 31, pp.e00020~18 (2018)[DOI]
- Stefani S, "Meticillinresistant Staphylococcus aureus(MRSA) : global epidemiology and harmonisation of typing methods", Int J Antimicrob Agents, 39, pp.273~282 (2012)[DOI]
- 강기수, "Prevalence of Major Methicillin-Resistant Staphylococcus aureus Clones in Korea Between 2001 and 2008", Annals of Laboratory Medicine, 36(6), pp.536~541 (2016), 대한진단검사의학회
- Park SY, "Sequence type 72 communityassociated meticillin-resistant Staphylococcus aureus emerged as a predominant clone of nasal colonization in newly admitted patients", J Hosp Infect, 93, pp.386~389 (2016)[DOI]
- Yang E, "Changing characteristics of S. aureus bacteremia caused by PVL-negative, MRSA strain over 11 years", Sci Rep, 11, pp.1567~ (2021)[DOI]
- Aires-de-Sousa M, "Methicillin-resistant Staphylococcus aureus among animals : current overview", Clin Microbiol Infect, 23, pp.373~380 (2017)[DOI]
- Back SH, "Livestock-associated methicillinresistant Staphylococcus aureus in Korea : antimicrobial resistance and molecular characteristics of LA-MRSA strains isolated from pigs, pig farmers, and farm environment", J Vet Sci, 21, pp.e2~ (2020)[DOI]
- Golding GR, "Livestockassociated methicillin-resistant Staphylococcus aureus sequence type 398 in humans, Canada", Emerg Infect Dis, 16, pp.587~ (2010)[DOI]
- Lim SK, "The first detection of methicillinresistant Staphylococcus aureus ST398 in pigs in Korea", Vet Microbiol, 155, pp.88~92 (2012)[DOI]
- Moon DC, "Prevalence and characteristics of methicillinresistant Staphylococcus aureus isolates in pigs and pig farmers in Korea", Foodborne Pathog Dis, 16, pp.256~261 (2019)[DOI]
- 임숙경, "Prevalence and Characterization of Methicillin-Resistant Staphylococcus aureus in Raw Meat in Korea", Journal of Microbiology and Biotechnology, 20(4), pp.775~778 (2010), 한국미생물·생명공학회
- Moon DC, "Identification of livestock-associated methicillin-resistant Staphylococcus aureus isolates in Korea and molecular comparison between isolates from animal carcasses and slaughterhouse workers", Foodborne Pathog Dis, 12, pp.327~334 (2015)[DOI]
- Hancock REW, "Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies", Nat Biotechnol, 24, pp.1551~1557 (2006)[DOI]
- Kubicek-Sutherland JZ, "Antimicrobial peptide exposure selects for Staphylococcus aureus resistance to human defence peptides", J Antimicrob Chemother, 72, pp.115~127 (2017)[DOI]
- Quinn GA, "Suppression of innate immunity by a nasal carriage strain of Staphylococcus aureus increases its colonization on nasal epithelium", Immunology, 122, pp.80~89 (2007)[DOI]
- Zanger P, "Persistent nasal carriage of Staphylococcus aureus is associated with deficient induction of human β-defensin 3 after sterile wounding of healthy skin in vivo", Infect Immun, 79, pp.2658~2662 (2011)[DOI]
- Agier J, "Cathelicidin impact on inflammatory cells", Cent Eur J Immunol, 40, pp.225~235 (2015)[DOI]
- Kang KM, "Potential role of host defense antimicrobial peptide resistance in increased virulence of health care-associated MRSA strains of sequence type(ST)5 versus livestock-associated and community-associated MRSA strains of ST72", Comp Immunol Microbiol Infect Dis, 62, pp.13~18 (2019)[DOI]
- Nam EY, "Emergence of daptomycinnonsusceptible methicillin-resistant Staphylococcus aureus clinical isolates among daptomycinnaive patients in Korea", Microb Drug Resist, 24, pp.534~541 (2018)[DOI]
- Geha DJ, "Multiplex PCR for identification of methicillin-resistant staphylococci in the clinical laboratory", J Clin Microbiol, 32, pp.1768~1772 (1994)[DOI]
- CLSI, , 2018
- "Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals: approved standard-2nd ed", NCCLS, ~ (2002)
- CLSI [Clinical, "Performance standards for antimicrobial susceptibility testing", CLSI, ~ (2011)
- Enright MC, "Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus", J Clin Microbiol, 38, pp.1008~1015 (2000)[DOI]
- Gilot P, "Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis", J Clin Microbiol, 40, pp.4060~4067 (2002)[DOI]
- Vandamme D, "A comprehensive summary of LL-37, the factotum human cathelicidin peptide", Cell Immunol, 280, pp.22~35 (2012)[DOI]
- Zhang G, "Porcine antimicrobial peptides : new prospects for ancient molecules of host defense", Vet Res, 31, pp.277~296 (2000)[DOI]
- Cuperus T, "Avian host defense peptides", Dev Comp Immunol, 41, pp.352~369 (2013)[DOI]
- Xiong YQ, "Functional interrelationships between cell membrane and cell wall in antimicrobial peptide-mediated killing of Staphylococcus aureus", Antimicrob Agents Chemother, 49, pp.3114~3121 (2005)[DOI]
- Meehl M, "Interaction of the GraRS two-component system with the VraFG ABC transporter to support vancomycin-intermediate resistance in Staphylococcus aureus", Antimicrob Agents Chemother, 51, pp.2679~2689 (2007)[DOI]
- Peschel A, "Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides", J Biol Chem, 274, pp.8405~8410 (1999)[DOI]
- Hamilton A, "Penicillin-binding protein 1a promotes resistance of group B streptococcus to antimicrobial peptides", Infect Immun, 74, pp.6179~6187 (2006)[DOI]
- Yang Y, "Protective effect of the golden staphyloxanthin biosynthesis pathway on Staphylococcus aureus under cold atmospheric plasma treatment", Appl Environ Microbiol, 86, pp.e01998~19 (2020)[DOI]
- Liu GY, "Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity", J Exp Med, 202, pp.209~215 (2005)[DOI]
- Kim ES, "A survey of communityassociated methicillin-resistant Staphylococcus aureus in Korea", J Antimicrob Chemother, 60, pp.1108~1114 (2007)[DOI]
- Kong EF, "Community-associated methicillin-resistant Staphylococcus aureus : an enemy amidst us", PLoS Pathog, 12, pp.e1005837~ (2016)[DOI]
- van Dijk A, "Avian cathelicidins : paradigms for the development of anti-infectives", Vet Microbiol, 153, pp.27~36 (2011)[DOI]
- Zanetti M, "Cathelicidins, multifunctional peptides of the innate immunity", J Leukoc Biol, 75, pp.39~48 (2004)[DOI]
- ZasloffM, "Antimicrobial peptides of multicellular organisms", Nature, 415, pp.389~395 (2002)[DOI]
- Muder RR, "Methicillinresistant staphylococcal colonization and infection in a long-term care facility", Ann Intern Med, 114, pp.107~112 (1991)[DOI]
- Zhu S, "Positive selection in cathelicidin host defense peptides : adaptation to exogenous pathogens or endogenous receptors?", Heredity, 118, pp.453~465 (2017)[DOI]
- Nimmo GR, "Community-associated methicillin-resistant Staphylococcus aureus(MRSA)in Australia", Int J Antimicrob Agents, 31, pp.401~410 (2008)[DOI]
- Wang Y, "Phylogenetic analysis and virulence determinant of the host-adapted Staphylococcus aureus lineage ST188 in China", Emerg Microbes Infect, 7, pp.1~11 (2018)[DOI]
- Bayer AS, "Frequency and distribution of single-nucleotide polymorphisms within mprF in methicillin-resistant Staphylococcus aureus clinical isolates and their role in cross-resistance to daptomycin and host defense antimicrobial peptides", Antimicrob Agents Chemother, 59, pp.4930~4937 (2015)[DOI]
- Joo HS, "Bacterial strategies of resistance to antimicrobial peptides", Philos Trans R Soc Lond B Biol Sci, 371, pp.20150292~ (2016)[DOI]
- Kraus D, "Molecular mechanisms of bacterial resistance to antimicrobial peptides", Curr Top Microbiol Immunol, 306, pp.231~250 (2006)[DOI]
- Mishra NN, "Carotenoidrelated alteration of cell membrane fluidity impacts Staphylococcus aureus susceptibility to host defense peptides", Antimicrob Agents Chemother, 55, pp.526~531 (2011)[DOI]
- Clauditz A, "Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress", Infect Immun, 74, pp.4950~4953 (2006)[DOI]
- Liu CI, "A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence", Science, 319, pp.1391~1394 (2008)[DOI]
- Park KH, "Community-associated MRSA strain ST72-SCCmecIV causing bloodstream infections : clinical outcomes and bacterial virulence factors", J Antimicrob Chemother, 70, pp.1185~1192 (2015)[DOI]
