Journal Articles
- Competition/antagonism associations of biofilm formation among Staphylococcus epidermidis Agr groups I, II, and III
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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
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J. Microbiol. 2019;57(2):143-153. Published online January 31, 2019
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DOI: https://doi.org/10.1007/s12275-019-8322-5
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Abstract
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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.
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Citations
Citations to this article as recorded by

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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
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Agnieszka Magrys , Jolanta Paluch-Oles , Agnieszka Bogut , Michal Kielbus , Dorota Plewik , Maria Koziol-Montewka
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J. Microbiol. 2015;53(8):544-552. Published online July 31, 2015
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DOI: https://doi.org/10.1007/s12275-015-5022-7
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55
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Abstract
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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.
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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
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Mi-Sun Kang , Jong-Suk Oh , Seok-Woo Lee , Hoi-Soon Lim , Nam-Ki Choi , Seon-Mi Kim
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J. Microbiol. 2012;50(1):137-142. Published online February 27, 2012
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DOI: https://doi.org/10.1007/s12275-012-1286-3
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40
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Abstract
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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.
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Citations
Citations to this article as recorded by

- 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 - Probiotics and prebiotics in dermatology
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
Rosanna Capparelli, Francesco De Chiara, Nunzia Nocerino, Rosa Chiara Montella, Marco Iannaccone, Andrea Fulgione, Alessandra Romanelli, Concetta Avitabile, Giuseppe Blaiotta, Federico Capuano
BMC Immunology.2012;[Epub] CrossRef
- Binding Sites for Lead Ion in Staphylococcus epidermidis
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Kim, Mal Nam , Sung, Hye Yoon
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J. Microbiol. 1995;33(3):228-233.
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Abstract
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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.