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Its ability to persist for extended periods within host cells has led to increased research interest. This review examines the process of internalization of S. aureus, highlighting the impact of its toxins and adhesion factors on host cells. It elucidates the intricate interactions between them and the host cellular environment, thereby offering potential strategies for the treatment and prevention of S. aureus infections.<\/jats:p>","DOI":"10.3390\/ijms26020720","type":"journal-article","created":{"date-parts":[[2025,1,16]],"date-time":"2025-01-16T06:46:10Z","timestamp":1737009970000},"page":"720","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Strategies for Survival of Staphylococcus aureus in Host Cells"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5814-9989","authenticated-orcid":false,"given":"Huiling","family":"Xu","sequence":"first","affiliation":[{"name":"College of Veterinary Medicine, Shandong Agricultural University, Tai\u2019an 271018, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shengnan","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Shandong Agricultural University, Tai\u2019an 271018, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoting","family":"Liu","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Shandong Agricultural University, Tai\u2019an 271018, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muzi","family":"Li","sequence":"additional","affiliation":[{"name":"Shandong Provincial Key Laboratory of Zoonoses, Shandong Agricultural University, Tai\u2019an 271018, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaozhou","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Shandong Agricultural University, Tai\u2019an 271018, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huahua","family":"Chen","sequence":"additional","affiliation":[{"name":"Shandong Provincial Key Laboratory of Zoonoses, Shandong Agricultural University, Tai\u2019an 271018, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chaonan","family":"Qu","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Shandong Agricultural University, Tai\u2019an 271018, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yongxia","family":"Liu","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Shandong Agricultural University, Tai\u2019an 271018, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3634-0712","authenticated-orcid":false,"given":"Jianzhu","family":"Liu","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Shandong Agricultural University, Tai\u2019an 271018, China"},{"name":"Shandong Provincial Key Laboratory of Zoonoses, Shandong Agricultural University, Tai\u2019an 271018, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,1,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Oliveira, D., Borges, A., and Sim\u00f5es, M. (2018). Staphylococcus aureus Toxins and Their Molecular Activity in Infectious Diseases. Toxins, 10.","DOI":"10.3390\/toxins10060252"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Mayer, K., Kucklick, M., Marbach, H., Ehling-Schulz, M., Engelmann, S., and Grunert, T. (2021). Within-Host Adaptation of Staphylococcus aureus in a Bovine Mastitis Infection Is Associated with Increased Cytotoxicity. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22168840"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.1111\/jam.14706","article-title":"Staphylococcus aureus persistence properties associated with bovine mastitis and alternative therapeutic modalities","volume":"129","author":"Zaatout","year":"2020","journal-title":"J. Appl. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"18033","DOI":"10.1038\/nrdp.2018.33","article-title":"Methicillin-resistant Staphylococcus aureus","volume":"4","author":"Lee","year":"2018","journal-title":"Nat. Rev. Dis. Primers"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Tuchscherr, L., L\u00f6ffler, B., and Proctor, R.A. (2020). Persistence of Staphylococcus aureus: Multiple Metabolic Pathways Impact the Expression of Virulence Factors in Small-Colony Variants (SCVs). Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.01028"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Laabei, M., Uhlemann, A.C., Lowy, F.D., Austin, E.D., Yokoyama, M., Ouadi, K., Feil, E., Thorpe, H.A., Williams, B., and Perkins, M. (2015). Evolutionary Trade-Offs Underlie the Multi-faceted Virulence of Staphylococcus aureus. PLoS Biol., 13.","DOI":"10.1371\/journal.pbio.1002229"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.micpath.2019.03.030","article-title":"Immunomodulatory molecules regulate adhesin gene expression in Staphylococcus aureus: Effect on bacterial internalization into bovine mammary epithelial cells","volume":"131","year":"2019","journal-title":"Microb. Pathog."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Niemann, S., Nguyen, M.T., Eble, J.A., Chasan, A.I., Mrakovcic, M., B\u00f6ttcher, R.T., Preissner, K.T., Ro\u00dflenbroich, S., Peters, G., and Herrmann, M. (2021). More Is Not Always Better-the Double-Headed Role of Fibronectin in Staphylococcus aureus Host Cell Invasion. mBio, 12.","DOI":"10.1128\/mBio.01062-21"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Meng, M., Wang, J., Li, H., Wang, J., Wang, X., Li, M., Gao, X., Li, W., Ma, C., and Wei, L. (2023). Eliminating the invading extracellular and intracellular FnBp(+) bacteria from respiratory epithelial cells by autophagy mediated through FnBp-Fn-Integrin \u03b15\u03b21 axis. Front. Cell. Infect. Microbiol., 13.","DOI":"10.3389\/fcimb.2023.1324727"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Schlesier, T., Siegmund, A., Rescher, U., and Heilmann, C. (2020). Characterization of the Atl-mediated staphylococcal internalization mechanism. Int. J. Med. Microbiol. IJMM, 310.","DOI":"10.1016\/j.ijmm.2020.151463"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Ying, Y.T., Ren, W.J., Tan, X., Yang, J., Liu, R., and Du, A.F. (2021). Annexin A2-Mediated Internalization of Staphylococcus aureus into Bovine Mammary Epithelial Cells Requires Its Interaction with Clumping Factor B. Microorganisms, 9.","DOI":"10.3390\/microorganisms9102090"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Tribelli, P.M., Luqman, A., Nguyen, M.T., Madlung, J., Fan, S.H., Macek, B., Sass, P., Bitschar, K., Schittek, B., and Kretschmer, D. (2020). Staphylococcus aureus Lpl protein triggers human host cell invasion via activation of Hsp90 receptor. Cell. Microbiol., 22.","DOI":"10.1111\/cmi.13111"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e00194-19","DOI":"10.1128\/IAI.00194-19","article-title":"Tet38 of Staphylococcus aureus Binds to Host Cell Receptor Complex CD36-Toll-Like Receptor 2 and Protects from Teichoic Acid Synthesis Inhibitors Tunicamycin and Congo Red","volume":"87","author":"Wang","year":"2019","journal-title":"Infect. Immun."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1310","DOI":"10.1038\/nm.2451","article-title":"A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice","volume":"17","author":"Inoshima","year":"2011","journal-title":"Nat. Med."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.semcdb.2017.04.003","article-title":"Staphylococcus aureus pore-forming toxins: The interface of pathogen and host complexity","volume":"72","author":"Seilie","year":"2017","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1809","DOI":"10.1111\/j.1462-5822.2007.00917.x","article-title":"Involvement of alpha5beta1-integrin and TNF-alpha in Staphylococcus aureus alpha-toxin-induced death of epithelial cells","volume":"9","author":"Liang","year":"2007","journal-title":"Cell. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Virreira Winter, S., Zychlinsky, A., and Bardoel, B.W. (2016). Genome-wide CRISPR screen reveals novel host factors required for Staphylococcus aureus \u03b1-hemolysin-mediated toxicity. Sci. Rep., 6.","DOI":"10.1038\/srep24242"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"14337","DOI":"10.1073\/pnas.1510265112","article-title":"The adherens junctions control susceptibility to Staphylococcus aureus \u03b1-toxin","volume":"112","author":"Popov","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2132","DOI":"10.1016\/j.celrep.2018.10.088","article-title":"A Dock-and-Lock Mechanism Clusters ADAM10 at Cell-Cell Junctions to Promote \u03b1-Toxin Cytotoxicity","volume":"25","author":"Shah","year":"2018","journal-title":"Cell Rep."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Chu, M., Zhou, M., Jiang, C., Chen, X., Guo, L., Zhang, M., Chu, Z., and Wang, Y. (2018). Staphylococcus aureus Phenol-Soluble Modulins \u03b11-\u03b13 Act as Novel Toll-Like Receptor (TLR) 4 Antagonists to Inhibit HMGB1\/TLR4\/NF-\u03baB Signaling Pathway. Front. Immunol., 9.","DOI":"10.3389\/fimmu.2018.00862"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Lebtig, M., Scheurer, J., Muenkel, M., Becker, J., Bastounis, E., Peschel, A., and Kretschmer, D. (2023). Keratinocytes use FPR2 to detect Staphylococcus aureus and initiate antimicrobial skin defense. Front. Immunol., 14.","DOI":"10.3389\/fimmu.2023.1188555"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Richardson, J.R., Armbruster, N.S., G\u00fcnter, M., Henes, J., and Autenrieth, S.E. (2018). Staphylococcus aureus PSM Peptides Modulate Human Monocyte-Derived Dendritic Cells to Prime Regulatory T Cells. Front. Immunol., 9.","DOI":"10.3389\/fimmu.2018.02603"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"5438","DOI":"10.1038\/ncomms6438","article-title":"The staphylococcal toxins \u03b3-haemolysin AB and CB differentially target phagocytes by employing specific chemokine receptors","volume":"5","author":"Spaan","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1038\/nature11724","article-title":"CCR5 is a receptor for Staphylococcus aureus leukotoxin ED","volume":"493","author":"Alonzo","year":"2013","journal-title":"Nature"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1016\/j.chom.2013.09.005","article-title":"Staphylococcus aureus leukotoxin ED targets the chemokine receptors CXCR1 and CXCR2 to kill leukocytes and promote infection","volume":"14","author":"Alonzo","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Vrieling, M., Koymans, K.J., Heesterbeek, D.A., Aerts, P.C., Rutten, V.P., de Haas, C.J., van Kessel, K.P., Koets, A.P., Nijland, R., and van Strijp, J.A. (2015). Bovine Staphylococcus aureus Secretes the Leukocidin LukMF\u2019 To Kill Migrating Neutrophils through CCR1. mBio, 6.","DOI":"10.1128\/mBio.00335-15"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1016\/j.chom.2013.04.006","article-title":"The staphylococcal toxin Panton-Valentine Leukocidin targets human C5a receptors","volume":"13","author":"Spaan","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"10794","DOI":"10.1073\/pnas.1305121110","article-title":"Staphylococcus aureus LukAB cytotoxin kills human neutrophils by targeting the CD11b subunit of the integrin Mac-1","volume":"110","author":"DuMont","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"42524","DOI":"10.1074\/jbc.M302096200","article-title":"Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases","volume":"278","author":"Agerer","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e00058-18","DOI":"10.1128\/MMBR.00058-18","article-title":"Taming the Triskelion: Bacterial Manipulation of Clathrin","volume":"83","author":"Latomanski","year":"2019","journal-title":"Microbiol. Mol. Biol. Rev. MMBR"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1148","DOI":"10.1111\/1346-8138.16546","article-title":"Uptake of Staphylococcus aureus by keratinocytes is reduced by interferon-fibronectin pathway and filaggrin expression","volume":"49","author":"Miyake","year":"2022","journal-title":"J. Dermatol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e28023","DOI":"10.7554\/eLife.28023","article-title":"Cell differentiation defines acute and chronic infection cell types in Staphylococcus aureus","volume":"6","author":"Horger","year":"2017","journal-title":"eLife"},{"key":"ref_33","first-page":"583","article-title":"Staphylococcus aureus toxins--their functions and genetics","volume":"21","author":"Grumann","year":"2014","journal-title":"Infect. Genet. Evol. J. Mol. Epidemiol. Evol. Genet. Infect. Dis."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Kubica, M., Guzik, K., Koziel, J., Zarebski, M., Richter, W., Gajkowska, B., Golda, A., Maciag-Gudowska, A., Brix, K., and Shaw, L. (2008). A potential new pathway for Staphylococcus aureus dissemination: The silent survival of S. aureus phagocytosed by human monocyte-derived macrophages. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0001409"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"329ra331","DOI":"10.1126\/scitranslmed.aad9922","article-title":"Staphylococcus aureus \u03b1 toxin potentiates opportunistic bacterial lung infections","volume":"8","author":"Cohen","year":"2016","journal-title":"Sci. Transl. Med."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Fernandez, J.S., Tuttobene, M.R., Monta\u00f1a, S., Subils, T., Cantera, V., Iriarte, A., Tuchscherr, L., and Ramirez, M.S. (2022). Staphylococcus aureus \u03b1-Toxin Effect on Acinetobacter baumannii Behavior. Biology, 11.","DOI":"10.3390\/biology11040570"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Hong, S.W., Choi, E.B., Min, T.K., Kim, J.H., Kim, M.H., Jeon, S.G., Lee, B.J., Gho, Y.S., Jee, Y.K., and Pyun, B.Y. (2014). An important role of \u03b1-hemolysin in extracellular vesicles on the development of atopic dermatitis induced by Staphylococcus aureus. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0100499"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e00059-21","DOI":"10.1128\/mSphere.00059-21","article-title":"Staphylococcus aureus Arsenal To Conquer the Lower Respiratory Tract","volume":"6","author":"Pivard","year":"2021","journal-title":"mSphere"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"e00606-17","DOI":"10.1128\/IAI.00606-17","article-title":"Staphylococcus aureus Alpha-Toxin Disrupts Endothelial-Cell Tight Junctions via Acid Sphingomyelinase and Ceramide","volume":"86","author":"Becker","year":"2018","journal-title":"Infect. Immun."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1515\/hsz-2018-0161","article-title":"Pulmonary infection of cystic fibrosis mice with Staphylococcus aureus requires expression of \u03b1-toxin","volume":"399","author":"Keitsch","year":"2018","journal-title":"Biol. Chem."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Monecke, S., M\u00fcller, E., B\u00fcchler, J., Stieber, B., and Ehricht, R. (2014). Staphylococcus aureus in vitro secretion of alpha toxin (hla) correlates with the affiliation to clonal complexes. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0100427"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Bonifacius, A., Goldmann, O., Floess, S., Holtfreter, S., Robert, P.A., Nordengr\u00fcn, M., Kruse, F., Lochner, M., Falk, C.S., and Schmitz, I. (2020). Staphylococcus aureus Alpha-Toxin Limits Type 1 While Fostering Type 3 Immune Responses. Front. Immunol., 11.","DOI":"10.3389\/fimmu.2020.01579"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1038\/s41541-022-00598-3","article-title":"Toxin expression during Staphylococcus aureus infection imprints host immunity to inhibit vaccine efficacy","volume":"8","author":"Teymournejad","year":"2023","journal-title":"NPJ Vaccines"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e129","DOI":"10.3346\/jkms.2023.38.e129","article-title":"Anti-Alpha-Toxin Antibody Responses and Clinical Outcomes of Staphylococcus aureus Bacteremia","volume":"38","author":"Kim","year":"2023","journal-title":"J. Korean Med. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Lade, H., Chung, S.H., Lee, Y., Joo, H.S., and Kim, J.S. (2022). Genotypes of Staphylococcus aureus Clinical Isolates Are Associated with Phenol-Soluble Modulin (PSM) Production. Toxins, 14.","DOI":"10.3390\/toxins14080556"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Kristoffersen, K., Hansen, K.H., and Andreasen, M. (2023). Differential Effects of Lipid Bilayers on \u03b1PSM Peptide Functional Amyloid Formation. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25010102"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.ijmm.2013.11.019","article-title":"Phenol-soluble modulins","volume":"304","author":"Otto","year":"2014","journal-title":"Int. J. Med. Microbiol. IJMM"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1186","DOI":"10.1080\/21505594.2021.1910455","article-title":"Intracellular persistence of Staphylococcus aureus in endothelial cells is promoted by the absence of phenol-soluble modulins","volume":"12","author":"Siegmund","year":"2021","journal-title":"Virulence"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"12304","DOI":"10.1038\/ncomms12304","article-title":"Toll-like receptor 2 activation depends on lipopeptide shedding by bacterial surfactants","volume":"7","author":"Hanzelmann","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/j.chom.2017.10.006","article-title":"Staphylococcus aureus Epicutaneous Exposure Drives Skin Inflammation via IL-36-Mediated T Cell Responses","volume":"22","author":"Liu","year":"2017","journal-title":"Cell Host Microbe"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"105237","DOI":"10.1016\/j.micinf.2023.105237","article-title":"Staphylococcus aureus-derived virulent phenol-soluble modulin \u03b1 triggers alarmin release to drive IL-36-dependent corneal inflammation","volume":"26","author":"Nakajima","year":"2024","journal-title":"Microbes Infect."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2474","DOI":"10.1080\/21505594.2021.1975909","article-title":"Phenol-soluble modulins \u03b1 are major virulence factors of Staphylococcus aureus secretome promoting inflammatory response in human epidermis","volume":"12","author":"Damour","year":"2021","journal-title":"Virulence"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Ventura, C.L., Malachowa, N., Hammer, C.H., Nardone, G.A., Robinson, M.A., Kobayashi, S.D., and DeLeo, F.R. (2010). Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0011634"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1172","DOI":"10.1111\/cmi.12577","article-title":"Influence of Sae-regulated and Agr-regulated factors on the escape of Staphylococcus aureus from human macrophages","volume":"18","author":"Geiger","year":"2016","journal-title":"Cell. Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1093\/infdis\/jit445","article-title":"Panton-Valentine leukocidin facilitates the escape of Staphylococcus aureus from human keratinocyte endosomes and induces apoptosis","volume":"209","author":"Chi","year":"2014","journal-title":"J. Infect. Dis."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"3117","DOI":"10.1172\/JCI22684","article-title":"Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils","volume":"115","author":"Genestier","year":"2005","journal-title":"J. Clin. Investig."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2150","DOI":"10.1111\/ced.15392","article-title":"Panton-Valentine leucocidin-producing Staphylococcus aureus: A clinical review","volume":"47","author":"Hussain","year":"2022","journal-title":"Clin. Exp. Dermatol."},{"key":"ref_58","first-page":"775","article-title":"Skin Infections Due to Panton-Valentine Leukocidin-Producing S. Aureus","volume":"119","author":"Leistner","year":"2022","journal-title":"Dtsch. Arztebl. Int."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1939","DOI":"10.3201\/eid2608.201413","article-title":"Panton-Valentine Leukocidin-Secreting Staphylococcus aureus Pneumonia Complicating COVID-19","volume":"26","author":"Duployez","year":"2020","journal-title":"Emerg. Infect. Dis."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Liu, Z.H., Wu, Q.Y., Xu, F., Zhang, X., and Liao, X.B. (2023). Biofunction and clinical potential of extracellular vesicles from methicillin-resistant Staphylococcus aureus. Microbiol. Res., 266.","DOI":"10.1016\/j.micres.2022.127238"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Wang, X., Koffi, P.F., English, O.F., and Lee, J.C. (2021). Staphylococcus aureus Extracellular Vesicles: A Story of Toxicity and the Stress of 2020. Toxins, 13.","DOI":"10.3390\/toxins13020075"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Wang, X., Uppu, D.S., Dickey, S.W., Burgin, D.J., Otto, M., and Lee, J.C. (2023). Staphylococcus aureus delta toxin modulates both extracellular membrane vesicle biogenesis and amyloid formation. mBio, 14.","DOI":"10.1128\/mbio.01748-23"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"2000","DOI":"10.1080\/22221751.2021.1991239","article-title":"Extracellular vesicles from methicillin resistant Staphylococcus aureus stimulate proinflammatory cytokine production and trigger IgE-mediated hypersensitivity","volume":"10","author":"Asano","year":"2021","journal-title":"Emerg. Microbes Infect."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"e12080","DOI":"10.1002\/jev2.12080","article-title":"Staphylococcus aureus membrane vesicles contain immunostimulatory DNA, RNA and peptidoglycan that activate innate immune receptors and induce autophagy","volume":"10","author":"Bitto","year":"2021","journal-title":"J. Extracell. Vesicles"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Wang, X., Li, H., Wang, J., Xu, H., Xue, K., Liu, X., Zhang, Z., Liu, J., and Liu, Y. (2023). Staphylococcus aureus extracellular vesicles induce apoptosis and restrain mitophagy-mediated degradation of damaged mitochondria. Microbiol. Res., 273.","DOI":"10.1016\/j.micres.2023.127421"},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Lister, J.L., and Horswill, A.R. (2014). Staphylococcus aureus biofilms: Recent developments in biofilm dispersal. Front. Cell. Infect. Microbiol., 4.","DOI":"10.3389\/fcimb.2014.00178"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"e00026-19","DOI":"10.1128\/MMBR.00026-19","article-title":"Staphylococcal Biofilm Development: Structure, Regulation, and Treatment Strategies","volume":"84","author":"Schilcher","year":"2020","journal-title":"Microbiol. Mol. Biol. Rev. MMBR"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1146\/annurev-med-042711-140023","article-title":"Staphylococcal infections: Mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity","volume":"64","author":"Otto","year":"2013","journal-title":"Annu. Rev. Med."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Grando, K., Nicastro, L.K., Tursi, S.A., De Anda, J., Lee, E.Y., Wong, G.C.L., and T\u00fckel, \u00c7. (2022). Phenol-Soluble Modulins From Staphylococcus aureus Biofilms Form Complexes With DNA to Drive Autoimmunity. Front. Cell. Infect. Microbiol., 12.","DOI":"10.3389\/fcimb.2022.884065"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"e01021-15","DOI":"10.1128\/mBio.01021-15","article-title":"Staphylococcus aureus Biofilms Induce Macrophage Dysfunction Through Leukocidin AB and Alpha-Toxin","volume":"6","author":"Scherr","year":"2015","journal-title":"mBio"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"2704","DOI":"10.1039\/C7MB00365J","article-title":"Staphylococcus aureus extracellular vesicles (EVs): Surface-binding antagonists of biofilm formation","volume":"13","author":"Im","year":"2017","journal-title":"Mol. Biosyst."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1038\/nrmicro3480","article-title":"Through the wall: Extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi","volume":"13","author":"Brown","year":"2015","journal-title":"Nat. Reviews. Microbiol."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Sabino, Y.N.V., Ara\u00fajo Domingues, K.C., Mathur, H., G\u00f3mez-Mascaraque, L.G., Drouin, G., Mart\u00ednez-Abad, A., T\u00f3tola, M.R., Abreu, L.M., Cotter, P.D., and Mantovani, H.C. (2023). Exopolysaccharides produced by Bacillus spp. inhibit biofilm formation by Staphylococcus aureus strains associated with bovine mastitis. Int. J. Biol. Macromol., 253.","DOI":"10.1016\/j.ijbiomac.2023.126689"},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Guo, H., Tong, Y., Cheng, J., Abbas, Z., Li, Z., Wang, J., Zhou, Y., Si, D., and Zhang, R. (2022). Biofilm and Small Colony Variants-An Update on Staphylococcus aureus Strategies toward Drug Resistance. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23031241"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Zhou, S., Rao, Y., Li, J., Huang, Q., and Rao, X. (2022). Staphylococcus aureus small-colony variants: Formation, infection, and treatment. Microbiol. Res., 260.","DOI":"10.1016\/j.micres.2022.127040"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/s00294-015-0503-0","article-title":"Staphylococcus aureus dynamically adapts global regulators and virulence factor expression in the course from acute to chronic infection","volume":"62","author":"Tuchscherr","year":"2016","journal-title":"Curr. Genet."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Tuchscherr, L., Geraci, J., and L\u00f6ffler, B. (2017). Staphylococcus aureus Regulator Sigma B is Important to Develop Chronic Infections in Hematogenous Murine Osteomyelitis Model. Pathogens, 6.","DOI":"10.3390\/pathogens6030031"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1302\/2046-3758.1112.BJR-2021-0590.R1","article-title":"The role of Staphylococcus aureus small colony variants in intraosseous invasion and colonization in periprosthetic joint infection","volume":"11","author":"Cai","year":"2022","journal-title":"Bone Jt. Res."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/j.ijmm.2013.11.011","article-title":"Staphylococcus aureus persistence in non-professional phagocytes","volume":"304","author":"Tuchscherr","year":"2014","journal-title":"Int. J. Med. Microbiol. IJMM"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1623","DOI":"10.1080\/21505594.2020.1844418","article-title":"Time-resolved analysis of Staphylococcus aureus invading the endothelial barrier","volume":"11","author":"Raineri","year":"2020","journal-title":"Virulence"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Pidwill, G.R., Gibson, J.F., Cole, J., Renshaw, S.A., and Foster, S.J. (2020). The Role of Macrophages in Staphylococcus aureus Infection. Front. Immunol., 11.","DOI":"10.3389\/fimmu.2020.620339"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"e02288-20","DOI":"10.1128\/mBio.02288-20","article-title":"Staphylococcal DNA Repair Is Required for Infection","volume":"11","author":"Ha","year":"2020","journal-title":"mBio"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1525","DOI":"10.1038\/s41467-022-29206-7","article-title":"The induction of natural competence adapts staphylococcal metabolism to infection","volume":"13","author":"Cordero","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"e01224-17","DOI":"10.1128\/mBio.01224-17","article-title":"Dehydrosqualene Desaturase as a Novel Target for Anti-Virulence Therapy against Staphylococcus aureus","volume":"8","author":"Gao","year":"2017","journal-title":"mBio"},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Lushchak, V.I., and Lushchak, O. (2021). Interplay between reactive oxygen and nitrogen species in living organisms. Chem. -Biol. Interact., 349.","DOI":"10.1016\/j.cbi.2021.109680"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"e00344-19","DOI":"10.1128\/IAI.00344-19","article-title":"Staphylococcus aureus Lipoic Acid Synthesis Limits Macrophage Reactive Oxygen and Nitrogen Species Production To Promote Survival during Infection","volume":"87","author":"Grayczyk","year":"2019","journal-title":"Infect. Immun."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/S0076-6879(08)36011-X","article-title":"Flavohemoglobin of Staphylococcus aureus","volume":"436","author":"Nobre","year":"2008","journal-title":"Methods Enzymol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"8753","DOI":"10.3390\/ijms15058753","article-title":"Colonization and infection of the skin by S. aureus: Immune system evasion and the response to cationic antimicrobial peptides","volume":"15","author":"Ryu","year":"2014","journal-title":"Int. J. Mol. Sci."},{"key":"ref_89","first-page":"162","article-title":"The endolysosomal cysteine cathepsins L and K are involved in macrophage-mediated clearance of Staphylococcus aureus and the concomitant cytokine induction","volume":"28","author":"Faulhaber","year":"2014","journal-title":"FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1111\/mmi.15184","article-title":"Differential survival of Staphylococcal species in macrophages","volume":"121","author":"Bayer","year":"2024","journal-title":"Mol. Microbiol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"e01143-18","DOI":"10.1128\/mBio.01143-18","article-title":"Staphylococcus aureus Uses the GraXRS Regulatory System To Sense and Adapt to the Acidified Phagolysosome in Macrophages","volume":"9","author":"Flannagan","year":"2018","journal-title":"mBio"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"3460","DOI":"10.1111\/jcmm.15027","article-title":"Staphylococcus aureus facilitates its survival in bovine macrophages by blocking autophagic flux","volume":"24","author":"Cai","year":"2020","journal-title":"J. Cell. Mol. Med."},{"key":"ref_93","doi-asserted-by":"crossref","unstructured":"Vozza, E.G., Mulcahy, M.E., and McLoughlin, R.M. (2021). Making the Most of the Host; Targeting the Autophagy Pathway Facilitates Staphylococcus aureus Intracellular Survival in Neutrophils. Front. Immunol., 12.","DOI":"10.3389\/fimmu.2021.667387"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"15569","DOI":"10.1074\/jbc.RA118.003555","article-title":"PtpA, a secreted tyrosine phosphatase from Staphylococcus aureus, contributes to virulence and interacts with coronin-1A during infection","volume":"293","author":"Baronian","year":"2018","journal-title":"J. Biol. Chem."},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Youssouf, N., Martin, M., Bischoff, M., Soubeyran, P., Gannoun-Zaki, L., and Molle, V. (2023). The secreted tyrosine phosphatase PtpA promotes Staphylococcus aureus survival in RAW 264.7 macrophages through decrease of the SUMOylation host response. Microbiol. Spectr., 11.","DOI":"10.1128\/spectrum.02813-23"},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Elhawy, M.I., Huc-Brandt, S., P\u00e4tzold, L., Gannoun-Zaki, L., Abdrabou, A.M.M., Bischoff, M., and Molle, V. (2021). The Phosphoarginine Phosphatase PtpB from Staphylococcus aureus Is Involved in Bacterial Stress Adaptation during Infection. Cells, 10.","DOI":"10.3390\/cells10030645"},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Elhawy, M.I., Molle, V., Becker, S.L., and Bischoff, M. (2021). The Low-Molecular Weight Protein Arginine Phosphatase PtpB Affects Nuclease Production, Cell Wall Integrity, and Uptake Rates of Staphylococcus aureus by Polymorphonuclear Leukocytes. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22105342"},{"key":"ref_98","doi-asserted-by":"crossref","unstructured":"Ahmad-Mansour, N., Elhawy, M.I., Huc-Brandt, S., Youssouf, N., P\u00e4tzold, L., Martin, M., Abdel-Wadood, N., Aljohmani, A., Morsli, M., and Krasteva-Christ, G. (2022). Characterization of the Secreted Acid Phosphatase SapS Reveals a Novel Virulence Factor of Staphylococcus aureus That Contributes to Survival and Virulence in Mice. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms232214031"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"6995","DOI":"10.1038\/s41467-022-34432-0","article-title":"YAP promotes cell-autonomous immune responses to tackle intracellular Staphylococcus aureus in vitro","volume":"13","author":"Caire","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_100","doi-asserted-by":"crossref","unstructured":"Geng, N., Wang, X., Yu, X., Wang, R., Zhu, Y., Zhang, M., Liu, J., and Liu, Y. (2020). Staphylococcus aureus Avoids Autophagy Clearance of Bovine Mammary Epithelial Cells by Impairing Lysosomal Function. Front. Immunol., 11.","DOI":"10.3389\/fimmu.2020.00746"},{"key":"ref_101","doi-asserted-by":"crossref","unstructured":"Gauron, M.C., Newton, A.C., and Colombo, M.I. (2021). PKC\u03b1 Is Recruited to Staphylococcus aureus-Containing Phagosomes and Impairs Bacterial Replication by Inhibition of Autophagy. Front. Immunol., 12.","DOI":"10.3389\/fimmu.2021.662987"},{"key":"ref_102","first-page":"e131","article-title":"Lysosomal alkalization to potentiate eradication of intra-osteoblastic Staphylococcus aureus in the bone and joint infection setting","volume":"28","author":"Abad","year":"2022","journal-title":"Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1007\/s00430-006-0015-0","article-title":"Live cell imaging of phagosome maturation in Staphylococcus aureus infected human endothelial cells: Small colony variants are able to survive in lysosomes","volume":"195","author":"Kland","year":"2006","journal-title":"Med. Microbiol. Immunol."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"6040","DOI":"10.1038\/s41467-023-41721-9","article-title":"AlphaFold-Multimer predicts cross-kingdom interactions at the plant-pathogen interface","volume":"14","author":"Homma","year":"2023","journal-title":"Nat. Commun."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/2\/720\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T10:29:39Z","timestamp":1759919379000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/2\/720"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,16]]},"references-count":104,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2025,1]]}},"alternative-id":["ijms26020720"],"URL":"https:\/\/doi.org\/10.3390\/ijms26020720","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,16]]}}}