Kinetics of <i>Candida albicans</i> and <i>Staphylococcus aureus</i> Biofilm Initiation on Herpes Simplex Virus (HSV-1 and HSV-2) Infected Cells — Oak Academic Publishing
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Kinetics of <i>Candida albicans</i> and <i>Staphylococcus aureus</i> Biofilm Initiation on Herpes Simplex Virus (HSV-1 and HSV-2) Infected Cells
Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
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Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
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Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
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Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
,
Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
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Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
1 Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
2 Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
3 Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
4 Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
5 Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
6 Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA
This study examines the kinetics of S. aureus and C. albicans adherence as it relates to HSV replication and corresponding dynamic display of shared receptors. HeLa cells infected for various times with HSV-1 gL86 or HSV-2 333gJ-(MOI 50) were incubated with S. aureus ATCC 25923 or C. albicans yeast and CFU measured. Over time, S. aureus adherence to HSV-1 infected cells was relatively stable for 45 min then decreased to 0.8 of virus-free control, before cycling at 15-to-30 min intervals. In contrast, staphylococcal adherence to HSV-2 infected cells proceeded at a more gradual rate, increasing to control levels at ~105 min before decreasing to a nadir at 165 min. Yeast adherence to HSV-1 infected cells remained relatively unchanged for the first 75 min then increased 2-fold before returning to its original level. This pattern is repeated over the next 90 min. While a similar pattern with C. albicans and HSV-2 was measured, it occurred more rapidly. Our model shows that while the interaction of both HSV-1 and HSV-2 with S. aureus is both dynamic and inhibitory, C. albicans interaction with HSV-2 is more permissive than HSV-1. However, the interaction of both microbes with HSV-infected cells in this model system appears to be independent of α5B1, CD36 and HSP60 viral-regulated receptor expression. These findings indicate that microbiome interactions across taxonomic kingdoms are more complex than previously thought.
Bradley, H., Markowitz, L.E., Gibson, T. and McQuillan, G.M. (2014) Seroprevalence of Herpes Simplex Virus Types 1 and 2-United States, 1999-2010. The Journal of Infectious Diseases, 209, 325-333. https://doi.org/10.1093/infdis/jit458
Szpara, M.L., Gatherer, D., Ochoa, A., Greenbaum, B., Dolan, A., Bowden, R.J., Enquist, L.W., Legendre, M. and Davison, A.J. (2014) Evolution and Diversity in Human Herpes Simplex Virus Genomes. Journal of Virology, 88, 1209-1227. https://doi.org/10.1128/JVI.01987-13
Palu, G., Biasolo, M.A., Sartor, G., Masotti, L., Papini, E., Floreani, M. and Palatini, P. (1994) Effects of Herpes-Simplex Virus Type-1 Infection on the Plasma-Membrane and Related Functions of HeLa S3 Cells. Journal of General Virology, 75, 3337-3344. https://doi.org/10.1099/0022-1317-75-12-3337
Vitiello, G., Falanga, A., Galdiero, M., Marsh, D., Galdiero, S. and D’Errico, G. (2011) Lipid Composition Modulates the Interaction of Peptides Deriving from Herpes Simplex Virus Type I Glycoproteins B and H with Biomembranes. Biochimica et Biophysica Acta-Biomembranes, 1808, 2517-2526. https://doi.org/10.1016/j.bbamem.2011.07.012
Massey Ruth, C., Kantzanou Maria, N., Fowler, T., Day Nicholas, P.J., Schofield, K., Elisabeth, R.W., Anthony, R.B., Höök, M. and Peacock Sharon, J. (2001) Fibronectin-Binding Protein A of Staphylococcus aureus Has Multiple, Substituting, Binding Regions That Mediate Adherence to Fibronectin and Invasion of Endothelial Cells. Cellular Microbiology, 3, 839-851. https://doi.org/10.1046/j.1462-5822.2001.00157.x
Mayer, F.L., Wilson, D. and Hube, B. (2013) Candida albicans Pathogenicity Mechanisms. Virulence, 4, 119-128. https://doi.org/10.4161/viru.22913
Arduino, P.G. and Porter, S.R. (2008) Herpes Simplex Virus Type I infection: Overview on Relevant Clinico-Pathological Features. Journal of Oral Pathology & Medicine, 37, 107-121. https://doi.org/10.1111/j.1600-0714.2007.00586.x
Looker, K.J. and Garnett, G.P. (2005) A Systematic Review of the Epidemiology and Interaction of Herpes Simplex Virus Types 1 and 2. Sexually Transmitted Infections, 81, 103-107. https://doi.org/10.1136/sti.2004.012039
Taylor, T.J., Brockman, M.A., McNamee, E.E. and Knipe, D.M. (2002) Herpes Simplex Virus. Frontiers in Bioscience, 7, D752-D764. https://doi.org/10.2741/A809
Bernstein, D.I., Bellamy, A.R., Hook, E.W., Levin, M.J., Wald, A., Ewell, M.G., Wolff, P.A., Deal, C.D., Heineman, T.C., Dubin, G. and Belshe, R.B. (2013) Epidemiology, Clinical Presentation, and Antibody Response to Primary Infection with Herpes Simplex Virus Type 1 and Type 2 in Young Women. Clinical Infectious Diseases, 56, 344-351. https://doi.org/10.1093/cid/cis891
Plotkin, B.J., Sigar, I.M., Tiwari, V. and Halkyard, S. (2016) Herpes Simplex Virus (HSV) Modulation of Staphylococcus aureus and Candida albicans Initiation of HeLa 299 Cell-Associated Biofilm. Current Microbiology, 72, 529-537. https://doi.org/10.1007/s00284-015-0975-7
Cermelli, C., Orsi, C.F., Ardizzoni, A., Lugli, E., Cenacchi, V., Cossarizza, A. and Blasi, E. (2008) Herpes Simplex Virus Type 1 Dysregulates Anti-Fungal Defenses Preventing Monocyte Activation and Downregulating Toll-Like Receptor-2. Microbiology and Immunology, 52, 575-584. https://doi.org/10.1111/j.1348-0421.2008.00074.x
Bjarnsholt, T., Alhede, M., Alhede, M., Eickhardt-Sorensen, S.R., Moser, C., Kuhl, M., Jensen, P.O. and Hoiby, N. (2013) The in Vivo Biofilm. Trends in Microbiology, 21, 466-474. https://doi.org/10.1016/j.tim.2013.06.002
Baur, S., Rautenberg, M., Faulstich, M., Grau, T., Severin, Y., Unger, C., Hoffmann, W.H., Rudel, T., Autenrieth, I.B. and Weidenmaier, C. (2014) A Nasal Epithelial Receptor for Staphylococcus aureus WTA Governs Adhesion to Epithelial Cells and Modulates Nasal Colonization. PLoS Pathogens, 10, e1004247. https://doi.org/10.1371/journal.ppat.1004089
Colombo, A.V., Barbosa, G.M., Higashi, D., di Micheli, G., Rodrigues, P.H. and Simionato, M.R.L. (2013) Quantitative Detection of Staphylococcus aureus, Enterococcus faecalis and Pseudomonas aeruginosa in Human Oral Epithelial Cells from Subjects with Periodontitis and Periodontal Health. Journal of Medical Microbiology, 62, 1592-1600. https://doi.org/10.1099/jmm.0.055830-0
Merghni, A., Ben Nejma, M., Hentati, H., Mahjoub, A. and Mastouri, M. (2014) Adhesive Properties and Extracellular Enzymatic Activity of Staphylococcus aureus Strains Isolated from Oral Cavity. Microbial Pathogenesis, 73, 7-12. https://doi.org/10.1016/j.micpath.2014.05.002
Pereira, C.A., Toledo, B.C., Santos, C.T., Pereira Costa, A.C.B., Back-Brito, G.N., Kaminagakura, E. and Jorge, A.O.C. (2013) Opportunistic Microorganisms in Individuals with Lesions of Denture Stomatitis. Diagnostic Microbiology and Infectious Disease, 76, 419-424. https://doi.org/10.1016/j.diagmicrobio.2013.05.001
Plotkin, B.J., Sigar, I.M., Tiwari, V. and Halkyard, S. (2016) Determination of Biofilm Initiation on Virus-Infected Cells by Bacteria and Fungi. Journal of Visualized Experiments, No. 113, e54162. https://doi.org/10.3791/54162
Gerber, S.I., Belval, B.J. and Herold, B.C. (1995) Differences in the Role of Glycoprotein C of HSV-1 and HSV-2 in Viral Binding May Contribute to Serotype Differences in Cell Tropism. Virology, 214, 29-39. https://doi.org/10.1006/viro.1995.9957
Herold, B.C., Visalli, R.J., Susmarski, N., Brandt, C.R. and Spear, P.G. (1994) Glycoprotein C-Independent Binding of Herpes Simplex Virus to Cells Requires Cell Surface Heparan Sulphate and Glycoprotein B. Journal of General Virology, 75, 1211-1222. https://doi.org/10.1099/0022-1317-75-6-1211
Atanasiu, D., Saw, W.T., Gallagher, J.R., Hannah, B.P., Matsuda, Z., Whitbeck, J.C., Cohen, G.H. and Eisenberg, R.J. (2013) Dual Split Protein-Based Fusion Assay Reveals that Mutations to Herpes Simplex Virus (HSV) Glycoprotein gB Alter the Kinetics of Cell-Cell Fusion Induced by HSV Entry Glycoproteins. Journal of Virology, 87, 11332-11345. https://doi.org/10.1128/JVI.01700-13
Montgomery, R.I., Warner, M.S., Lum, B.J. and Spear, P.G. (1996) Herpes Simplex Virus-1 Entry into Cells Mediated by a Novel Member of the TNF/NGF Receptor Family. Cell, 87, 427-436. https://doi.org/10.1016/S0092-8674(00)81363-X
Ren, Z.Y. and Silverberg, J.I. (2020) Association of Atopic Dermatitis with Bacterial, Fungal, Viral, and Sexually Transmitted Skin Infections. Dermatitis, 31, 157-164. https://doi.org/10.1097/DER.0000000000000526
Lacour, M. and Hauser, C. (1993) The Role of Microorganisms in Atopic-Dermatitis. Clinical Reviews in Allergy, 11, 491-522.
Damour, A., Garcia, M., Seneschal, J., Leveque, N. and Bodet, C. (2020) Eczema Herpeticum: Clinical and Pathophysiological Aspects. Clinical Reviews in Allergy & Immunology, 59, 1-18.
Clement, C., Tiwari, V., Scanlan, P.M., Valyi-Nagy, T., Yue, B. and Shukla, D. (2006) A Novel Role for Phagocytosis-Like Uptake in Herpes Simplex Virus Entry. Journal of Cell Biology, 174, 1009-1021. https://doi.org/10.1083/jcb.200509155
Akhtar, J. and Shukla, D. (2009) Viral Entry Mechanisms: Cellular and Viral Mediators of Herpes Simplex Virus Entry. FEBS Journal, 276, 7228-7236. https://doi.org/10.1111/j.1742-4658.2009.07402.x
Brandhorst, T.T., Roy, R., Wuthrich, M., Nanjappa, S., Filutowicz, H., Galles, K., Tonelli, M., McCaslin, D.R., Satyshur, K. and Klein, B. (2013) Structure and Function of a Fungal Adhesin That Binds Heparin and Mimics Thrombospondin-1 by Blocking T Cell Activation and Effector Function. PLoS Pathogens, 9, e1003464. https://doi.org/10.1371/journal.ppat.1003464
Green, J.V., Orsborn, K.I., Zhang, M., Tan, Q.K.G., Greis, K.D., Porollo, A., Andes, D.R., Lu, J.L. and Hostetter, M.K. (2013) Heparin-Binding Motifs and Biofilm Formation by Candida albicans. Journal of Infectious Diseases, 208, 1695-1704. https://doi.org/10.1093/infdis/jit391
Khalil, M.A. and Sonbol, F.I. (2014) Investigation of Biofilm Formation on Contact Eye Lenses Caused by Methicillin Resistant Staphylococcus aureus. Nigerian Journal of Clinical Practice, 17, 776-784. https://doi.org/10.4103/1119-3077.144398
Shanks, R.M.Q., Donegan, N.P., Graber, M.L., Buckingham, S.E., Zegans, M.E., Cheung, A.L. and O'Toole, G.A. (2005) Heparin Stimulates Staphylococcus aureus Biofilm Formation. Infection and Immunity, 73, 4596-4606. https://doi.org/10.1128/IAI.73.8.4596-4606.2005
Tiwari, V., Clement, C., Xu, D., Valyi-Nagy, T., Yue, B., Liu, J. and Shukla, D. (2006) Role for 3-O-Sulfated Heparan Sulfate as the Receptor for Herpes Simplex Virus Type 1 Entry into Primary Human Corneal Fibroblasts. Journal of Virology, 80, 8970-8980. https://doi.org/10.1128/JVI.00296-06
Delboy, M.G., Patterson, J.L., Hollander, A.M. and Nicola, A.V. (2006) Nectin-2-Mediated Entry of a Syncytial Strain of Herpes Simplex Virus via pH-Independent Fusion with the Plasma Membrane of Chinese Hamster Ovary Cells. Virology Journal, 3, Article No. 105. https://doi.org/10.1186/1743-422x-3-105
Di Giovine, P., Settembre, E.C., Bhargava, A.K., Luftig, M.A., Lou, H., Cohen, G.H., Eisenberg, R.J., Krummenacher, C. and Carfi, A. (2011) Structure of Herpes Simplex Virus Glycoprotein D Bound to the Human Receptor Nectin-1. PLoS Pathogens, 7, e1002277. https://doi.org/10.1371/journal.ppat.1002277
Hauck, C.R. (2002) Cell Adhesion Receptors—Signaling Capacity and Exploitation by Bacterial Pathogens. Medical Microbiology and Immunology, 191, 55-62. https://doi.org/10.1007/s00430-002-0119-0
Kramko, N., Sinitski, D., Seebach, J., Loffler, B., Dieterich, P., Hellmann, C., Peters, G. and Schnittler, H.J. (2013) Early Staphylococcus aureus-Induced Changes in Endothelial Barrier Function Are Strain-Specific and Unrelated to Bacterial Translocation. International Journal of Medical Microbiology, 303, 635-644. https://doi.org/10.1016/j.ijmm.2013.09.006
Roy, S., Nasser, S., Yee, M., Graves, D.T. and Roy, S. (2011) A Long-Term siRNA Strategy Regulates Fibronectin Overexpression and Improves Vascular Lesions in Retinas of Diabetic Rats. Molecular Vision, 17, 3166-3174.
Sato, R., Iiizumi, S., Kim, E.S., Honda, F., Lee, S.K., Adachi, N., Koyama, H., Mizutani, S. and Morio, T. (2012) Impaired Cell Adhesion, Apoptosis, and Signaling in WASP Gene-Disrupted Nalm-6 Pre-B Cells and Recovery of Cell Adhesion Using a Transducible form of WASp. Interna-tional Journal of Hematology, 95, 299-310. https://doi.org/10.1007/s12185-012-1013-1
Shukla, S.Y., Singh, Y.K. and Shukla, D. (2009) Role of Nectin-1, HVEM, and PILR-alpha in HSV-2 Entry into Human Retinal Pigment Epithelial Cells. Investigative Ophthalmology & Visual Science, 50, 2878-2887. https://doi.org/10.1167/iovs.08-2981
Stump, J.D. and Sticht, H. (2014) Mutations in Herpes Simplex Virus gD Protein Affect Receptor Binding by Different Molecular Mechanisms. Journal of Molecular Modeling, 20, Article No. 2192. https://doi.org/10.1007/s00894-014-2192-x
Zelano, J., Wallquist, W., Hailer, N.P. and Cullheim, S. (2006) Expression of Nectin-1, Nectin-3, N-Cadherin, and NCAM in Spinal Motoneurons after Sciatic Nerve Transection. Ex-perimental Neurology, 201, 461-469. https://doi.org/10.1016/j.expneurol.2006.04.026
Akhtar, J., Tiwari, V., Oh, M.J., Kovacs, M., Jani, A., Kovacs, S.K., Valyi-Nagy, T. and Shukla, D. (2008) HVEM and Nectin-1 Are the Major Mediators of Herpes Simplex Virus 1 (HSV-1) Entry into Human Conjunctival Epithelium. Investigative Ophthalmology & Visual Science, 49, 4026-4035. https://doi.org/10.1167/iovs.08-1807
Heo, S.-K., Ju, S.-A., Lee, S.-C., Park, S.-M., Choe, S.-Y., Kwon, B., Kwon, B.S. and Kim, B.-S. (2006) LIGHT Enhances the Bactericidal Activity of Human Monocytes and Neutrophils via HVEM. Journal of Leukocyte Biology, 79, 330-338. https://doi.org/10.1189/jlb.1104694
Weidenmaier, C., Kokai-Kun, J.F., Kristian, S.A., Chanturiya, T., Kalbacher, H., Gross, M., Nicholson, G., Neumeister, B., Mond, J.J. and Peschel, A. (2004) Role of Teichoic Acids in Staphylococcus aureus Nasal Colonization, a Major Risk Factor in Nosocomial Infections. Nature Medicine, 10, 243-245. https://doi.org/10.1038/nm991
Willis, A.M., Coulter, W.A., Fulton, C.R., Hayes, J.R., Bell, P.M. and Lamey, P.J. (1999) Oral Candidal Carriage and Infection in Insulin-Treated Diabetic Patients. Diabetic Medicine, 16, 675-679. https://doi.org/10.1046/j.1464-5491.1999.00134.x
Alva-Murillo, N., Lopez-Meza, J.E. and Ochoa-Zarzosa, A. (2014) Nonprofessional Phagocytic Cell Receptors Involved in Staphylococcus aureus Internalization. BioMed Research International, 2014, Article ID: 538546. https://doi.org/10.1155/2014/538546
Calderone, R.A. and Scheld, W.M. (1987) Role of Fibronectin in the Pathogenesis of Candidal Infections. Reviews of Infectious Diseases, 9, S400-S403. https://doi.org/10.1093/clinids/9.Supplement_4.S400
Fowler, T., Wann, E.R., Joh, D., Johansson, S., Foster, T.J. and Hook, M. (2000) Cellular Invasion by Staphylococcus aureus Involves a Fibronectin Bridge between the Bacterial Fibronectin-Binding MSCRAMMs and Host Cell Beta1 Integrins. European Journal of Cell Biology, 79, 672-679. https://doi.org/10.1078/0171-9335-00104
Christopher, R.A., Kowalczyk, A.P. and McKeown-Longo, P.J. (1997) Localization of Fibronectin Matrix Assembly Sites on Fibroblasts and Endothelial Cells. Journal of Cell Science, 110, 569-581.
Heino, J. and Kapyla, J. (2009) Cellular Receptors of Extracellular Matrix Molecules. Current Pharmaceutical Design, 15, 1309-1317. https://doi.org/10.2174/138161209787846720
Hynes, R.O., Ali, I.U., Destree, A.T., Mautner, V., Perkins, M.E., Senger, D.R., Wagner, D.D. and Smith, K.K. (1978) A Large Glycoprotein Lost from the Surfaces of Transformed Cells. Annals of the New York Academy of Sciences, 312, 317-342. https://doi.org/10.1111/j.1749-6632.1978.tb16811.x
Mao, Y. and Schwarzbauer, J.E. (2005) Fibronectin Fibrillogenesis, a Cell-Mediated Matrix Assembly Process. Matrix Biology, 24, 389-399. https://doi.org/10.1016/j.matbio.2005.06.008
Schwarzbauer, J.E. and DeSimone, D.W. (2011) Fibronectins, Their Fibrillogenesis, and in Vivo Functions. Cold Spring Harbor Perspectives in Biology, 3, a005041. https://doi.org/10.1101/cshperspect.a005041
Dziewanowska, K., Carson, A.R., Patti, J.M., Deobald, C.F., Bayles, K.W. and Bohach, G.A. (2000) Staphylococcal Fibronectin Binding Protein Interacts with Heat Shock Protein 60 and Integrins: Role in Internalization by Epithelial Cells. Infection and Immunity, 68, 6321-6328. https://doi.org/10.1128/IAI.68.11.6321-6328.2000
Means, T.K., Mylonakis, E., Tampakakis, E., Colvin, R.A., Seung, E., Puckett, L., Tai, M.F., Stewart, C.R., Pukkila-Worley, R., Hickman, S.E., Moore, K.J., Calderwood, S.B., Hacohen, N., Luster, A.D. and El Khoury, J. (2009) Evolutionarily Conserved Recognition and Innate Immunity to Fungal Pathogens by the Scavenger Receptors SCARF1 and CD36. The Journal of Experimental Medicine, 206, 637-653. https://doi.org/10.1084/jem.20082109