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Competition/antagonism associations of biofilm formation among Staphylococcus epidermidis Agr groups I, II, and III
Sergio Martínez-García , César I. Ortiz-García , Marisa Cruz-Aguilar , Juan Carlos Zenteno , José Martin Murrieta-Coxca , Sonia Mayra Pérez-Tapia , Sandra Rodríguez-Martínez , Mario E. Cancino-Diaz , Juan C. Cancino-Diaz
J. Microbiol. 2019;57(2):143-153.   Published online January 31, 2019
DOI: https://doi.org/10.1007/s12275-019-8322-5
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AbstractAbstract
Staphylococci have quorum-sensing (QS) systems that enable cell-to-cell communication, as well as the regulation of numerous colonization and virulence factors. The accessory gene regulator (Agr) operon is one of the Staphylococcus genus QS systems. Three groups (I, II, and III) are present in Staphylococcus epidermidis Agr operon. To date, it is unknown whether Agr groups can interact symbiotically during biofilm development. This study analyzed a symbiotic association among Agr groups during biofilm formation in clinical and commensal isolates. Different combinations among Agr group isolates was used to study biofilm formation in vitro and in vivo (using a mouse catheter-infection model). The analysis of Agr groups were also performed from samples of human skin (head, armpits, and nostrils). Different predominant coexistence was found within biofilms, suggesting symbiosis type. In vitro, Agr I had a competition with Agr II and Agr III. Agr II had a competition with Agr III, and Agr II was an antagonist to Agr I and III when the three strains were combined. In vivo, Agr II had a competition to Agr I, but Agr I and II were antagonists to Agr III. The associations found in vitro and in vivo were also found in different sites of the skin. Besides, other associations were observed: Agr III antagonized Agr I and II, and Agr III competed with Agr I and Agr II. These results suggest that, in S. epidermidis, a symbiotic association of competition and antagonism occurs among different Agr groups during biofilm formation.

Citations

Citations to this article as recorded by  
  • The pathogenicity and virulence of the opportunistic pathogen Staphylococcus epidermidis
    Órla Burke, Merve S. Zeden, James P. O’Gara
    Virulence.2024;[Epub]     CrossRef
  • Synthetic Peptides Capable of Potent Multigroup Staphylococcal Quorum Sensing Activation and Inhibition in Both Cultures and Biofilm Communities
    Emma L. Eisenbraun, Troy D. Vulpis, Brendan N. Prosser, Alexander R. Horswill, Helen E. Blackwell
    Journal of the American Chemical Society.2024; 146(23): 15941.     CrossRef
  • Biofilm formation, occurrence, microbial communication, impact and characterization methods in natural and anthropic systems: a review
    Punniyakotti Elumalai, Xuke Gao, Jinjie Cui, Arunagiri Santhosh Kumar, Perumal Dhandapani, Punniyakotti Parthipan, Obulisamy Parthiba Karthikeyan, Jayaraman Theerthagiri, Soorathep Kheawhom, Myong Yong Choi
    Environmental Chemistry Letters.2024; 22(3): 1297.     CrossRef
  • Analysis of the Presence of the Virulence and Regulation Genes from Staphylococcus aureus (S. aureus) in Coagulase Negative Staphylococci and the Influence of the Staphylococcal Cross-Talk on Their Functions
    Magdalena Grazul, Ewa Balcerczak, Monika Sienkiewicz
    International Journal of Environmental Research and Public Health.2023; 20(6): 5155.     CrossRef
  • Staphylococcus epidermidis Controls Opportunistic Pathogens in the Nose, Could It Help to Regulate SARS-CoV-2 (COVID-19) Infection?
    Silvestre Ortega-Peña, Sandra Rodríguez-Martínez, Mario E. Cancino-Diaz, Juan C. Cancino-Diaz
    Life.2022; 12(3): 341.     CrossRef
  • Direct Quantitative Immunochemical Analysis of Autoinducer Peptide IV for Diagnosing and Stratifying Staphylococcus aureus Infections
    Enrique-J. Montagut, Gerardo Acosta, Fernando Albericio, Miriam Royo, Gerard Godoy-Tena, Alicia Lacoma, Cristina Prat, Juan-Pablo Salvador, María-Pilar Marco
    ACS Infectious Diseases.2022; 8(3): 645.     CrossRef
  • Non-Native Peptides Capable of Pan-Activating the agr Quorum Sensing System across Multiple Specificity Groups of Staphylococcus epidermidis
    Korbin H. J. West, Wenqi Shen, Emma L. Eisenbraun, Tian Yang, Joseph K. Vasquez, Alexander R. Horswill, Helen E. Blackwell
    ACS Chemical Biology.2021; 16(6): 1070.     CrossRef
  • Clinical and molecular characteristics of Staphylococcus aureus isolated from Chinese children: association among the agr groups and genotypes, virulence genes and disease types
    Yan Xu, Su-Yun Qian, Kai-Hu Yao, Fang Dong, Wen-Qi Song, Chen Sun, Xin Yang, Jing- Hui Zhen, Xi-Qing Liu, Zhi -Yong Lv, Xi Yang
    World Journal of Pediatrics.2021; 17(2): 180.     CrossRef
  • Non‐biofilm‐forming commensal Staphylococcus epidermidis isolates produce biofilm in the presence of trypsin
    Sergio Martínez‐García, Silvestre Ortega‐Peña, María De Jesús De Haro‐Cruz, Ma. Guadalupe Aguilera‐Arreola, María Dolores Alcántar‐Curiel, Gabriel Betanzos‐Cabrera, Janet Jan‐Roblero, Sonia Mayra Pérez‐Tapia, Sandra Rodríguez‐Martínez, Mario E. Cancino‐Di
    MicrobiologyOpen.2019;[Epub]     CrossRef
The role of programmed death ligand 1 pathway in persistent biomaterial-associated infections
Agnieszka Magrys , Jolanta Paluch-Oles , Agnieszka Bogut , Michal Kielbus , Dorota Plewik , Maria Koziol-Montewka
J. Microbiol. 2015;53(8):544-552.   Published online July 31, 2015
DOI: https://doi.org/10.1007/s12275-015-5022-7
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  • 10 Crossref
AbstractAbstract
Staphylococcus epidermidis is commonly involved in biomaterial- associated infections. Bacterial small colony variants (SCV) seem to be well adapted to persist intracellularly in professional phagocytes evading the host immune response. We studied the expression of PD-L1/L2 on macrophages infected with clinical isolates of S. epidermidis SCV and their parent wild type (WT) strains. The cytokine pattern which is triggered by the examined strains was also analysed. In the study, we infected macrophages with S. epidermidis WT and SCV strains. Persistence and release from macrophages were monitored via lysostaphin protection assays. Moreover, the effect of IFN-γ pre-treatment on bacterial internalisation was investigated. Expression of PD-L1/L2 molecules was analysed with the use of FACS. Inflammatory reaction was measured by IL-10, TNF-α ELISAs, and transcriptional induction of TNF-α. Our study revealed that clinical SCV isolates were able to persist and survive in macrophages for at least 3 days with a low cytotoxic effect and a reduced proinflammatory response as compared to WT strains. Bacteria upregulated PD-L1/L2 expression on macrophages as compared to non-stimulated cells. The results demonstrated that the ability of S. epidermidis SCVs to induce elevated levels of anti-inflammatory cytokine, IL-10, and reduced transcriptional induction of TNF-α, together with expression of PD-L1 on macrophages and the ability to persist intracellularly without damaging the host cell could be the key factor contributing to chronicity of SCV infections.

Citations

Citations to this article as recorded by  
  • The mononuclear phagocyte system obscures the accurate diagnosis of infected joint replacements
    Robert Manasherob, Shay I. Warren, Prerna Arora, Lyong Heo, Naomi L. Haddock, Ievgen Koliesnik, Diasuke Furukawa, Z. Ngalo Otieno-Ayayo, William J. Maloney, David W. Lowenberg, Stuart B. Goodman, Derek F. Amanatullah
    Journal of Translational Medicine.2024;[Epub]     CrossRef
  • Periprosthetic joint infection and immunity: Current understanding of host–microbe interplay
    Nicolas S. Piuzzi, Alison K. Klika, Qiuhe Lu, Carlos A. Higuera‐Rueda, Thaddeus Stappenbeck, Anabelle Visperas
    Journal of Orthopaedic Research.2024; 42(1): 7.     CrossRef
  • The first genomic characterization of a stable, hemin-dependent small colony variant strain of Staphylococcus epidermidis isolated from a prosthetic-joint infection
    Agnieszka Bogut, Piotr Koper, Małgorzata Marczak, Paulina Całka
    Frontiers in Microbiology.2023;[Epub]     CrossRef
  • Immune checkpoint upregulation in periprosthetic joint infection
    Shay I. Warren, Gregory W. Charville, Robert Manasherob, Derek F. Amanatullah
    Journal of Orthopaedic Research.2022; 40(11): 2663.     CrossRef
  • The road to success of coagulase-negative staphylococci: clinical significance of small colony variants and their pathogenic role in persistent infections
    Agnieszka Bogut, Agnieszka Magryś
    European Journal of Clinical Microbiology & Infectious Diseases.2021; 40(11): 2249.     CrossRef
  • Chronic Implant-Related Bone Infections—Can Immune Modulation be a Therapeutic Strategy?
    Elisabeth Seebach, Katharina F. Kubatzky
    Frontiers in Immunology.2019;[Epub]     CrossRef
  • Expression of programmed death ligand‐1 on bladder tissues is detected in a clinically and histologically well‐defined interstitial cystitis cohort
    Yuke Chen, Wei Yu, Yang Yang, Yunxiang Xiao, Yun Cui, Jihong Duan, Qun He, Jie Jin, Shiliang Wu
    Neurourology and Urodynamics.2018; 37(4): 1396.     CrossRef
  • The role of the PI3K/mTOR signaling pathway in Staphylococcus epidermidis small colony variants intracellular survival
    Agnieszka Magryś, Agnieszka Bogut, Michał Kiełbus, Alina Olender
    Immunological Investigations.2018; 47(3): 251.     CrossRef
  • Intraphagolysosomal conditions predispose to Staphylococcus epidermidis small colony variants persistence in macrophages
    Agnieszka Magryś, Kamil Deryło, Agnieszka Bogut, Alina Olender, Marek Tchórzewski, Holger Rohde
    PLOS ONE.2018; 13(11): e0207312.     CrossRef
  • Pathogenic Mechanisms and Host Interactions in Staphylococcus epidermidis Device-Related Infection
    Marina Sabaté Brescó, Llinos G. Harris, Keith Thompson, Barbara Stanic, Mario Morgenstern, Liam O'Mahony, R. Geoff Richards, T. Fintan Moriarty
    Frontiers in Microbiology.2017;[Epub]     CrossRef
Research Support, Non-U.S. Gov't
Effect of Lactobacillus reuteri on the Proliferation of Propionibacterium acnes and Staphylococcus epidermidis
Mi-Sun Kang , Jong-Suk Oh , Seok-Woo Lee , Hoi-Soon Lim , Nam-Ki Choi , Seon-Mi Kim
J. Microbiol. 2012;50(1):137-142.   Published online February 27, 2012
DOI: https://doi.org/10.1007/s12275-012-1286-3
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  • 14 Crossref
AbstractAbstract
While it is generally accepted that Propionibacterium acnes is involved in the development of acne, other bacteria including Staphylococcus epidermidis have also been isolated from the acne lesion. The interaction between Lactobacillus reuteri, a probiotic bacterium, and acnegenic bacteria is unclear. This study examined the effects of L. reuteri on the proliferation of P. acnes and S. epidermidis. Human-derived L. reuteri strains (KCTC 3594 and KCTC 3678) and rat-derived L. reuteri KCTC 3679 were used. All strains exhibited significant inhibitory effects on the growth of P. acnes and S. epidermidis. The proliferation of P. acnes was decreased by 2-log scales after incubation with L. reuteri for 24 h. In addition, the proliferation of S. epidermidis was decreased by 3-log scales after incubation with L. reuteri for 24 h, whereas the growth of L. reuteri was unaffected by P. acnes or S. epidermidis. Among the L. reuteri strains examined, L. reuteri KCTC 3679 had the strongest inhibitory effect on the growth of P. acnes and S. epidermidis, followed by L. reuteri KCTC 3594 and L. reuteri KCTC 3678. Interestingly, reuterin, an antimicrobial factor, was produced only by L. reuteri KCTC 3594. The most pronounced the antibacterial activities of L. reuteri were attributed to the production of organic acids. Overall, these results suggest that L. reuteri may be a useful probiotic agent to control the growth of bacteria involved in acne inflammation and prevent acne.

Citations

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  • Modulations of the skin microbiome in skin disorders: A narrative review from a wound care perspective
    Antonia Piazzesi, Matteo Scanu, Guido Ciprandi, Lorenza Putignani
    International Wound Journal.2024;[Epub]     CrossRef
  • 15 % Azelaic acid gel modify the skin microbiota of acne vulgaris
    Wenxin Yu, Huchi Shen, Beilei Cai, Yuanruo Xie, Yue Wang, Jing Wang
    Journal of Dermatologic Science and Cosmetic Technology.2024; 1(4): 100041.     CrossRef
  • Potential of Bifidobacteriumlactis IDCC 4301 isolated from breast milk‐fed infant feces as a probiotic and functional ingredient
    O‐Hyun Ban, Won Yeong Bang, Hyeon Ji Jeon, Young Hoon Jung, Jungwoo Yang, Dong Hyun Kim
    Food Science & Nutrition.2023; 11(4): 1952.     CrossRef
  • Explore the Anti-Acne Mechanism of Licorice Flavonoids Based on Metabonomics and Microbiome
    Shi-Fa Ruan, Yi Hu, Wen-Feng Wu, Qun-Qun Du, Zhu-Xian Wang, Ting-Ting Chen, Qun Shen, Li Liu, Cui-Ping Jiang, Hui Li, Yankui Yi, Chun-Yan Shen, Hong-Xia Zhu, Qiang Liu
    Frontiers in Pharmacology.2022;[Epub]     CrossRef
  • Probiyotiklerin Akne Vulgaris’e Etkisi
    Nedime GÜNDÜZ, Reyhan İRKİN
    Sağlık Akademisi Kastamonu.2022; 7(2): 364.     CrossRef
  • Host Microbiota Balance in Teenagers with Gum Hypertrophy Concomitant with Acne Vulgaris: Role of Oral Hygiene Associated with Topical Probiotics
    Giovanna Mosaico, Giulia Artuso, Mara Pinna, Gloria Denotti, Germano Orrù, Cinzia Casu
    Microorganisms.2022; 10(7): 1344.     CrossRef
  • An approach to extend the shelf life of ribbonfish fillet using lactic acid bacteria cell-free culture supernatant
    Du-Min Jo, Seul-Ki Park, Fazlurrahman Khan, Min-Gyun Kang, Jae-Hwa Lee, Young-Mog Kim
    Food Control.2021; 123: 107731.     CrossRef
  • Microbiome Modulation as a Therapeutic Approach in Chronic Skin Diseases
    Karina Polak, Antal Jobbágy, Tomasz Muszyński, Kamila Wojciechowska, Aleksandra Frątczak, András Bánvölgyi, Beata Bergler-Czop, Norbert Kiss
    Biomedicines.2021; 9(10): 1436.     CrossRef
  • Lactobacillus reuteri DSM 17938 as a Novel Topical Cosmetic Ingredient: A Proof of Concept Clinical Study in Adults with Atopic Dermatitis
    Éile Butler, Christoffer Lundqvist, Jakob Axelsson
    Microorganisms.2020; 8(7): 1026.     CrossRef
  • Invitro synergistic activity of lactic acid bacteria against multi-drug resistant staphylococci
    Jinal Bhola, Rama Bhadekar
    BMC Complementary and Alternative Medicine.2019;[Epub]     CrossRef
  • Antimicrobial activity of Lactobacillus salivarius and Lactobacillus fermentum against Staphylococcus aureus
    Mi-Sun Kang, Hae-Soon Lim, Jong-Suk Oh, You-jin Lim, Karin Wuertz-Kozak, Janette M. Harro, Mark E. Shirtliff, Yvonne Achermann
    Pathogens and Disease.2017;[Epub]     CrossRef
  • Acne vulgaris, probiotics and the gut-brain-skin axis: from anecdote to translational medicine
    W. Bowe, N.B. Patel, A.C. Logan
    Beneficial Microbes.2014; 5(2): 185.     CrossRef
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    Katherine L. Baquerizo Nole, Elizabeth Yim, Jonette E. Keri
    Journal of the American Academy of Dermatology.2014; 71(4): 814.     CrossRef
  • New perspectives for natural antimicrobial peptides: application as antinflammatory drugs in a murine model
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    BMC Immunology.2012;[Epub]     CrossRef
Binding Sites for Lead Ion in Staphylococcus epidermidis
Kim, Mal Nam , Sung, Hye Yoon
J. Microbiol. 1995;33(3):228-233.
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AbstractAbstract
As S. epidermidis cell was fractionated into cell wall, cell membrane, and cytoplasm, the cell membrane proved to be the most efficient absorbent for lead ion. Ultrasonication was effective, when the cells were treated during their exponential growth. The amount of the lead ion adsorbed in cell membrane decreased as hydrogen ion concentration of solution increased. Protein purified from the cell membrane showed higher adsorption capacity for the lead ion than peptidoglycan, teichoic acid from cell wall, or cell membrane lipid. Modification of carboxyl groups in the membrane protein with ethylenediamine and 1-ethyl-3-carbodiimide hydrochloride resulted in a considerable decrease of lead ion adsorption capability, suggesting that the main binding site for lead ion was the carboxyl groups of protein in cell membrane.

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