Elucidating the anti-biofilm and anti-quorum sensing potential of selenocystine against respiratory tract infections causing bacteria: in vitro and in silico studies
Abstract
Bacteria are increasingly relying on biofilms to develop resistance to antibiotics thereby resulting in their failure in treating many infections. In spite of continuous research on many synthetic and natural compounds, ideal anti-biofilm molecule is still not found thereby warranting search for new class of molecules. The current study focuses on exploring anti-biofilm potential of selenocystine against respiratory tract infection (RTI)-causing bacteria. Anti-bacterial and anti-biofilm assays demonstrated that selenocystine inhibits the growth of bacteria in their planktonic state, and formation of biofilms while eradicating preformed-biofilm effectively. Selenocystine at a MIC50 as low as 42 and 28 μg/mL effectively inhibited the growth of Klebsiella pneumonia and Pseudomonas aeruginosa. The antibacterial effect is further reconfirmed by agar cup diffusion assay and growth-kill assay. Selenocystine showed 30–60% inhibition of biofilm formation in K. pneumonia, and 44–70% in P. aeruginosa respectively. It also distorted the preformed-biofilms by degrading the eDNA component of the Extracellular Polymeric Substance matrix. Molecular docking studies of selenocystine with quorum sensing specific proteins clearly showed that through the carboxylic acid moiety it interacts and inhibits the protein function, thereby confirming its anti-biofilm potential. With further validation selenocystine can be explored as a potential candidate for the treatment of RTIs.
Funding source: Department of Atomic Energy
Acknowledgments
This work is supported by Department of Atomic Energy, India. The authors are thankful to Dr V.K. Jain, Director, CEBS for constant support and encouragement.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: This work is supported by Department of Atomic Energy, India.
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Ahmad, A., Viljoen, A.M., and Chenia, H.F. (2014). The impact of plant volatiles on bacterial quorum sensing. Lett. Appl. Microbiol. 60: 8–19. https://doi.org/10.1111/lam.12343.Suche in Google Scholar
Alam, M.F., Safhi, M.M., Moni, S.S., and Jabeen, A. (2016). In vitro antibacterial spectrum of sodium selenite against selected human pathogenic bacterial strains. Scientifica 2016, https://doi.org/10.1155/2016/9176273.Suche in Google Scholar
Al-Haidari, R.A., Shaaban, M.I., Ibrahim, S., and Mohamed, G.A. (2016). Anti-quorum sensing activity of some medicinal plants. Afr. J. Tradit., Complementary Altern. Med. 13: 67–71.10.21010/ajtcam.v13i5.10Suche in Google Scholar
Álvarez-Pérez, M., Ali, W., Marć, M.A., Handzlik, J., and Domínguez-Álvarez, E. (2018). Selenides and diselenides: a review of their anticancer and chemopreventive activity. Molecules 23: 628. https://doi.org/10.3390/molecules23030628.Suche in Google Scholar
Asfour, H.Z. (2018). Anti-quorum sensing natural compounds. J. Microsc. Ultrastruct. 6: 1–10. https://doi.org/10.4103/jmau.jmau_10_18.Suche in Google Scholar
Ashurst, J.V. and Dawson, A. (2019). Klebsiella pneumonia. In: StatPearls. StatPearls Publishing, Treasure Island (FL), Available at: <https://www.ncbi.nlm.nih.gov/pubmed/30085546.Suche in Google Scholar
Bazargani, M.M. and Jens, R. (2015). Anti-biofilm activity of essential oils and plant extracts against Staphylococcus aureus and E. coli biofilms. Food Contr. 61: 156–164.10.1016/j.foodcont.2015.09.036Suche in Google Scholar
Chen, T. and Wong, Y.S. (2008). Selenocystine induces apoptosis of A375 human melanoma cells by activating ROS-mediated mitochondrial pathway and p53 phosphorylation. Cell. Mol. Life Sci. 65: 2763–2775. https://doi.org/10.1007/s00018-008-8329-2.Suche in Google Scholar
Chen, T. and Wong, Y.S. (2009). Selenocystine induces caspase-independent apoptosis in MCF-7 human breast carcinoma cells with involvement of p53 phosphorylation and reactive oxygen species generation. Int. J. Biochem. Cell Biol. 41: 666–676. https://doi.org/10.1016/j.biocel.2008.07.014.Suche in Google Scholar
Di Martino, P. (2018). Extracellular polymeric substances, a key element in understanding biofilm phenotype. AIMS Microbiol. 4: 274–288. https://doi.org/10.3934/microbiol.2018.2.274.Suche in Google Scholar
Di Martino, P., Cafferini, N., Joly, B., and Darfeuille-Michaud, A. (2003). Klebsiella pneumoniae type 3 pili facilitate adherence and biofilm formation on abiotic surfaces. Res. Microbiol. 154: 9–16.10.1016/S0923-2508(02)00004-9Suche in Google Scholar
Dong, C., Zhou, J., Wang, P., Li, T., Zhao, Y., Ren, X., Lu, J., Wang, J., Holmgren, A., and Zou, L. (2020). Topical therapeutic efficacy of Ebselen against multidrug-resistant Staphylococcus aureus LT-1 targeting thioredoxin reductase. Front. Microbiol. 10: 3016. https://doi.org/10.3389/fmicb.2019.03016.Suche in Google Scholar
Flohe, L., Günzler, W.A., and Schock, H.H. (1973). Glutathione peroxidase: a selenoenzyme. FEBS Lett. 32: 132–134.10.1016/0014-5793(73)80755-0Suche in Google Scholar
Geier, H., Mostowy, S., Cangelosi, G.A., Behr, M.A., and Timothy, E.F. (2008). Autoinducer-2 triggers the oxidative stress response in Mycobacterium avium, leading to biofilm formation. Appl. Environ. Microbiol. 74: 1798–1804. https://doi.org/10.1128/aem.02066-07.Suche in Google Scholar
Getahun, A., Abraham, A., Alemayehu, S., Solomon, G., Bekele, F., Dawit, W., and Håkan, M. (2004). Evaluation of direct colorimetric assay for rapid detection of Rifampicin resistant Mycobacterium tuberculosis. J. Clin. Microbiol. 42: 871–873.10.1128/JCM.42.2.871-873.2004Suche in Google Scholar PubMed PubMed Central
Gómez-Gómez, B., Arregui, L., Serrano, S., Santos, A., Pérez-Corona, T., and Madrid, Y. (2019). Selenium and tellurium-based nanoparticles as interfering factors in quorum sensing-regulated processes: violacein production and bacterial biofilm formation. Metallomics 11: 1104–1114. https://doi.org/10.1039/c9mt00044e.Suche in Google Scholar
González, J.E. and Keshavan, N.D. (2006). Messing with bacterial quorum sensing. Microbiol. Mol. Biol. Rev. 70: 859–875.10.1128/MMBR.00002-06Suche in Google Scholar PubMed PubMed Central
Graziano, T.S., Cuzzullin, M.C., Franco, G.C., Schwartz-Filho, H.O., de Andrade, E.D., Groppo, F.C., and Cogo-Müller, K. (2015). Statins and antimicrobial effects: simvastatin as a potential drug against Staphylococcus aureus bioflm. PloS One 10: e0128098. https://doi.org/10.1371/journal.pone.0128098.Suche in Google Scholar
Heatley, N.G. (1944). A method for the assay of pencillin. Biochem. J. 38: 62–65. https://doi.org/10.1042/bj0380061.Suche in Google Scholar
Hesketh, J. (2008). Nutrigenomics and selenium: gene expression patterns, physiological targets, and genetics. Ann. Rev. Nutri. 28: 157–177.10.1146/annurev.nutr.28.061807.155446Suche in Google Scholar PubMed
Ho Sui, S.J., Lo, R., Fernandes, A.R., Caulfield, M.D.G., Lerman, J.A., Xie, L., Bourne, P.E., Baillie, D.L., and Brinkman, F.S.L. (2012). Raloxifene attenuates Pseudomonas aeruginosa pyocyanin production and virulence. Int. J. Antimicrob. Agents 40: 246–251. https://doi.org/10.1016/j.ijantimicag.2012.05.009.Suche in Google Scholar
Hochbaum, A.I., Kolodkly-Gal, L., Foulston, L., Kolter, R., Aizenberg, J., and Losick, R. (2011). Inhibitory effects of D-amino acids on Staphylococcus aureus biofilm development. J. Bactreiol. 193: 5616–5622. https://doi.org/10.1128/jb.05534-11.Suche in Google Scholar
Hotterbeekx, A., Xavier, B., Bielen, K., Lammens, C., Moons, P., Schepens, T., Ieven, M., Jorens, P.G., Goossens, H., Singh, S.K., et al.. (2016). The endotracheal tube microbiome associated with Pseudomonas aeruginosa or Staphylococcus epidermidis. Sci. Rep. 6: 36507. https://doi.org/10.1038/srep36507.Suche in Google Scholar
Huang, T., Holden, J.A., Heath, D.E., O’Brien-Simpsonb, N.M., and O’Connor, A.J. (2019). Engineering highly effective antimicrobial selenium nanoparticles through control of particle size. Nanoscale 11: 14937–14951. https://doi.org/10.1039/c9nr04424h.Suche in Google Scholar
Ibrahim, M., Hassan, W., Anwar, J., Deobald, A.M., Kamdem, J.P., Souza, D.O., and Rocha, J.B. (2014). 1-(2-(2-(2-(1-Aminoethyl)phenyl)diselanyl)phenyl) ethanamine: an amino organoselenium compound with interesting antioxidant profile. Toxicol. Vitro 28: 524–530. https://doi.org/10.1016/j.tiv.2013.12.010.Suche in Google Scholar
Jasim, S.T., Noori, A.M., Sadiq, S.T., and Flayyih, M.T. (2020). Antimicrobial and antibiofilm activity of D-amino acids combined with nanoparticles against Candida albicans. Sys. Rev. Pharm. 11: 274–280.10.31838/srp.2020.5.40Suche in Google Scholar
Johansson, L., Gafvelin, G., and Arnér, E.S.J. (2005). Selenocysteine in proteins properties and biotechnological use. Biochim. Biophys. Acta Gen. Subj. 1726: 1–13. https://doi.org/10.1016/j.bbagen.2005.05.010.Suche in Google Scholar
Kamal, A., Nazari, V.M., Yaseen, M., Iqbal, M.A., Ahamed, M.B.K., Majid, A.S.A., and Bhatti, H.N. (2019). Green synthesis of selenium-N-heterocyclic carbene compounds: evaluation of antimicrobial and anticancer potential. Bioorg. Chem. 90: 103042, https://doi.org/10.1016/j.bioorg.2019.103042.Suche in Google Scholar
Kim, H.S., Lee, S.H., Byun, Y., and Park, H.D. (2015). 6-gingerol reduces Pseudomonas aeruginosa biofilm formation and virulence via quorum sensing inhibition. Sci. Rep. 5: 8656. https://doi.org/10.1038/srep08656.Suche in Google Scholar
Maryland, H. (1994). Selenium in plant and animal nutrition. In: Frankenberger, W.T., Benson, S., and Dekker, M. (Eds.), Selenium in the environment. Marcel Dekker Inc., New York, NY, USA, pp. 29–45.Suche in Google Scholar
Meng, X.Y., Zhang, H.X., Mezei, M., and Cui, M. (2011). Molecular docking: a powerful approach for structure-based drug discovery. Curr. Comput. Aided Drug Des. 7: 146–157. https://doi.org/10.2174/157340911795677602.Suche in Google Scholar
Munita, J.M., and Arias, C.A. (2015). Mechanisms of antibiotic resistance. Microbiol. Spectr. 4: 481–511, https://doi.org/10.1128/microbiolspec.VMBF-0016-2015.Suche in Google Scholar
Narajj, C., Karvekar, M.D., and Das, A.K. (2007). Biological importance of organoselenium compounds. Indian J. Pharmaceut. Sci. 69: 344–351.10.4103/0250-474X.34541Suche in Google Scholar
Nie, Y., Zhong, M., Li, S., Li, X., Zhang, Y., Zhang, Y., and He, X. (2020). Synthesis and potential anticancer activity of some novel selenocyanates and diselenides. Chem. Biodivers. 17: e1900603. https://doi.org/10.1002/cbdv.201900603.Suche in Google Scholar
Nithya, C., Lewis Oscar, F., Kanaga, S., Kavitha, R., Dhamodharan, B., Kumar, A., Alharbi, N., Chinnathambi, A., Alharbi, S., and Thajuddin, N. (2014). Biofilm inhibitory potential of Chlamydomonas sp. extract against Pseudomonas aeruginosa. J. Algal Biomass Util. 5: 74–81.Suche in Google Scholar
Pietka-Ottlik, M., Wójtowicz-Młochowska, H., Kołodziejczyk, K., Piasecki, E., and Młochowski, J. (2008). New organoselenium compounds active against pathogenic bacteria, fungi and viruses. Chem. Pharm. Bull. 56: 1423–1427. https://doi.org/10.1248/cpb.56.1423.Suche in Google Scholar
Pinto, N.C.C., Silva, J.B., Menegati, L.M., Guedes, M.C.M.R., Marques, L.B., Silva, T.P.D., Melo, R.C.N., Souza-Fagundes, E.M., Salvador, M.J., Scio, E., et al.. (2017). Cytotoxicity and bacterial membrane destabilization induced by Annona squamosa L. extracts. An Acad. Bras Ciências 89: 2053–2073. https://doi.org/10.1590/0001-3765201720150702.Suche in Google Scholar
Pinzi, L. and Rastelli, G. (2019). Molecular docking: shifting paradigms in drug discovery. Int. J. Mol. Sci. 20: 4331. https://doi.org/10.3390/ijms20184331.Suche in Google Scholar
Pirushi, R. and Zavalani, F. (2014). Management of nosocomial respiratory infections. Int. J. Sci. Res. 3: 2562–2564.Suche in Google Scholar
Prateeksha, Singh, B.R., Shoeb, M., Sharma, S., Naqvi, A.H., Gupta, V.K., and Singh, B.N. (2017). Scaffold of selenium nanovectors and honey phytochemicals for inhibition of Pseudomonas aeruginosa quorum sensing and biofilm formation. Front. Cell. Infect. Microbiol. 7: 93. https://doi.org/10.3389/fcimb.2017.00093.Suche in Google Scholar
Qifeng, B., Li, L., Shanhui, L., Shujun, X., and Yu, G. (2018). Drug design progress of in silico, in vitro and in vivo researches. In-vitro In-vivo In-silico J. 1: 16–37.Suche in Google Scholar
Radhakrishna, P., Sharada, K.C., Vagdevi, M., Abhilekha, M., Mubeen, R., and Nischal, K. (2010). Synthesis and antibacterial activity of novel organoselenium compounds. Int. J. Chem. 2: 149–154, https://doi.org/10.5539/ijc.v2n2p149.Suche in Google Scholar
Ramon-Perez, M.L., Diaz-Cedillo, F., Ibarra, J.A., Torales-Cardeña, A., Rodríguez-Martínez, S., Jan-Roblero, J., Cancino-Diaz, M.E., and Cancino-Diaz, J.C. (2014). D-amino acids inhibit bioflm formation in Staphylococcus epidermidisstrains from ocular infections. J. Med. Microbiol. 63: 1369–1376. https://doi.org/10.1099/jmm.0.075796-0.Suche in Google Scholar
Riquelme, S.A., Ahn, D., and Prince, A. (2018). Pseudomonas aeruginosa and Klebsiella pneumoniae adaptation to innate immune clearance mechanisms in the lung. J. Innate Immun. 10: 442–454. https://doi.org/10.1159/000487515.Suche in Google Scholar
Rode, D.K.H., Singh, P.K., and Drescher, K. (2020). Multicellular and unicellular responses of microbial biofilms to stress. Biol. Chem. 401: 1365–1374. https://doi.org/10.1515/hsz-2020-0213.Suche in Google Scholar
Romero, D., Vlamakis, H., Losick, R., and Kolter, R. (2011). An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol. Microbiol. 80: 1155–1168. https://doi.org/10.1111/j.1365-2958.2011.07653.x.Suche in Google Scholar
Rotruck, J.T., Pope, A.L., Ganther, H.E., Swanson, A.B., Hafeman, D.G., and Hoekstra, W.G. (1973). Selenium: biochemical role as a component of glatathione peroxidase. Science 179: 588–590.10.1126/science.179.4073.588Suche in Google Scholar PubMed
Sadikot, R.T., Blackwell, T.S., Christman, J.W., and Prince, A.S. (2005). Pathogen–host interactions in Pseudomonas aeruginosa pneumonia. Am. J. Respir. Crit. Care Med. 171: 1209–1223. https://doi.org/10.1164/rccm.200408-1044so.Suche in Google Scholar
Sanchez, C.J., Akers, K.S., Romano, D.R., Woodbury, R.L., Hardy, S.K., Murray, C.K., and Wenkea, J.C. (2014). D-amino acids enhance the activity of antimicrobials against biofilms of clinical wound isolates of Staphylococcus aureus and Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 58: 4353–4361. https://doi.org/10.1128/aac.02468-14.Suche in Google Scholar
Sancineto, L., Fabro de Bem, A., Tew, K.D., Santi, C., Radi, R., Toquato, P., and Galli, F. (2017). Selenocompounds in cancer therapy: an overview. Adv. Canc. Res. 5: 14186–14193.Suche in Google Scholar
Sancineto, L., Piccioni, M., De Marco, S., Pagiotti, R., Nascimento, V., Luiz Braga, A., Santi, C., and Pietrella, D. (2016). Diphenyl diselenide derivatives inhibit microbial biofilm formation involved in wound infection. BMC Microbiol. 16: 220. https://doi.org/10.1186/s12866-016-0837-x.Suche in Google Scholar
Sasirekha, B., Megha, D.M., Sharath Chandra, M.S., and Soujanya, R. (2015). Study on effect of different plant extracts on microbial biofilms. Asian J. Biotechnol. 7: 1–12. https://doi.org/10.3923/ajbkr.2015.Suche in Google Scholar
Schmidt, R.L. and Simonović, M. (2012). Synthesis and decoding of selenocysteine and human health. Croat. Med. J. 53: 535–550. https://doi.org/10.3325/cmj.2012.53.535.Suche in Google Scholar
Schwarz, K. and Foltz, C.M. (1957). Selenium as an integral part of factor-3 against dietary necrotic liver degeneration. J. Am. Chem. Soc. 79: 3292–3293. https://doi.org/10.1021/ja01569a087.Suche in Google Scholar
Shaaban, S., Negm, A., Sobh, M.A., and Wessjohann, L.A. (2015). Organoselenocyanates and symmetrical diselenides redox modulators: design, synthesis and biological evaluation. Eur. J. Med. Chem. 97: 190–201. https://doi.org/10.1016/j.ejmech.2015.05.002.Suche in Google Scholar
Shrift, A. (1958). Biological activities of selenium compounds. Bot. Rev. 24: 550–583. https://doi.org/10.1007/bf02872594.Suche in Google Scholar
Singh, B.G., and Kunwar, A. (2020). In silico screening of organo-selenium compounds for anti-viral activity against SARS-CoV2. BARC News Letter, Mumbai, India.Suche in Google Scholar
Singh, F.V. and Wirth, T. (2018). Synthesis of organoselenium compounds with potential biological activities. In: Jain, V.K. and Priyadarsini, K.I. (Eds.). Organoselenium compounds in biology and medicine: synthesis, biological and therapeutic treatments, 1st ed. Royal. Soc. Chem, Cambridge, UK, pp. 77–121.10.1039/9781788011907-00077Suche in Google Scholar
Spallholz, J.E. (1994). On the nature of selenium toxicity and carcinostatic activity. Free Radical Biol. Med. 17: 45–64.10.1016/0891-5849(94)90007-8Suche in Google Scholar
Spengler, G., Kincses, A., Mosolygó, T., Marć, M.A., Nové, M., Gajdács, M., Sanmartín, C., McNeil, H.E., Blair, J., and Domínguez-Álvarez, E. (2019). Antiviral, antimicrobial and antibiofilm activity of selenoesters and selenoanhydrides. Molecules 24: 4264. https://doi.org/10.3390/molecules24234264.Suche in Google Scholar
Tabassum, R., Shafique, M., Khawaja, K.A., Alvi, I.A., Rehman, Y., Sheik, C.S., Abbas, Z., and Rehman, S. (2018). Complete genome analysis of a Siphoviridae phage TSK1 showing biofilm removal potential against Klebsiella pneumonia. Sci. Rep. 8: 17904. https://doi.org/10.1038/s41598-018-36229-y.Suche in Google Scholar
Talas, Z.S., Gok, Y., Ozdemir, I., Ates, B., Gunal, S., and Yilmaz, I. (2015). Synthesis, antioxidant and anti-microbial properties of two organoselenium compounds. Pak. J. Pharm. Sci. 28: 611–616.Suche in Google Scholar
Thuluz, M.-M., Claudia, J.-P., and Zepeda, R.C. (2020). Past, present, and future of molecular docking. IntechOpen, London.Suche in Google Scholar
Tran, P.L., Hammond, A.A., Mosley, T., Cortez, J., Gray, T., Colmer-Hamood, J.A., Shashtri, M., Spallholz, J.E., Hamood, A.N., and Reid, T.W. (2009). Organoselenium coating on cellulose inhibits the formation of biofilms by Pseudomonas aeruginosa and Staphylococcus aureus. Appl. Environ. Microbiol. 75: 3586–3592. https://doi.org/10.1128/aem.02683-08.Suche in Google Scholar
Tran, P.L., Lowry, N., Campbell, T., Reid, T.W., Webster, D.R., Tobin, E., Aslani, A., Mosley, T., Dertien, J., Colmer-Hamood, J.A., et al.. (2012). An organoselenium compound inhibits Staphylococcus aureus biofilms on hemodialysis catheters in vivo. Antimicrob. Agents Chemother. 56: 972–978. https://doi.org/10.1128/aac.05680-11.Suche in Google Scholar
Tran, P.A., O’Brien-Simpson, N., Palmer, J.A., Bock, N., Reynolds, E.C., Webster, T.J., Deva, A., Morrison, W.A., and O’Connor, A.J. (2019). Selenium nanoparticles as anti-infective implant coatings for trauma orthopedics against methicillin-resistant Staphylococcus aureus and epidermidis: in vitro and in vivo assessment. Int. J. Nanomed. 14: 4613–4624. https://doi.org/10.2147/IJN.S197737.Suche in Google Scholar
Trentin Dda, S., Giordani, R.B., Zimmer, K.R., da Silva, A.G., da Silva, M.V., Correia, M.T., Baumvol, I.J., and Macedo, A.J. (2011). Potential of medicinal plants from the Brazilian semi-arid region (Caatinga) against Staphylococcus epidermidis planktonic and biofilm lifestyles. J. Ethnopharmacol. 137: 327–35. https://doi.org/10.1016/j.jep.2011.05.030.Suche in Google Scholar
Troeger, C., Blacker, B., Khalil, I.A., Rao, P.C., Cao, J., Zimsen, S.R.M., Albertson, S.B., Deshpande, A., Farag, T., Abebe, Z., et al.. (2018). Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory infections in 195 countries, 1990–2016: a systematic analysis for the Global Burden of Disease Study. Lancet Infect. Dis. 18: 1191–1210. https://doi.org/10.1016/S1473-3099(18)30310-4.Suche in Google Scholar
Vasić, S., Radojević, I., Pešić, N., and Čomić, L. (2011). Influence of sodium selenite on the growth of selected bacteria species and their sensitivity to antibiotics. Kragujevac J. Sci. 33: 55–61.Suche in Google Scholar
Verbeke, F., De Craemer, S., Debunne, N., Janssens, Y., Wynendaele, E., Van de Wiele, C., and De Spiegeleer, B. (2017). Peptides as quorum sensing molecules: measurement techniques and obtained levels in vitro and in vivo. Front. Neurosci. 11: 183. https://doi.org/10.3389/fnins.2017.00183.Suche in Google Scholar
Vishwakarma, J. and Vavilala, S.L. (2019). Evaluating the antibacterial and antibiofilm potential of sulfated polysaccharides extracted from green algae Chlamydomonas reinhardtii. J. Appl. Microbiol. 127: 1004–1017. https://doi.org/10.1111/jam.14364.Suche in Google Scholar
Vishwakarma, J. and Vavilala, S.L. (2020). Unraveling the anti-biofilm potential of green algal sulfated polysaccharides against Salmonella enterica and Vibrio harveyi. Appl. Microbiol. Biotechnol. 104: 6299–6314. https://doi.org/10.1007/s00253-020-10653-5.Suche in Google Scholar
Vishwanath, S., Chawla, K., and Gopinathan, A. (2013). Multidrug resistant gram-negative bacilli in lower respiratory tract infections. Iran. J. Microbiol. 5: 323–327. https://doi.org/10.4103/0974-777x.121996.Suche in Google Scholar
Warraich, A.A., Mohammed, A.R., Perrie, Y., Hussain, M., Gibson, H., and Rahman, A. (2020). Evaluation of anti-biofilm activity of acidic amino acids and synergy with ciprofloxacin on Staphylococcus aureus biofilms. Sci. Rep. 10: 9021. https://doi.org/10.1038/s41598-020-66082-x.Suche in Google Scholar
Wrobel, K.J., Power, R., and Toborek, M. (2015). Biological activity of selenium: revisited. IUBMB Life 68: 97–105. https://doi.org/10.1002/iub.1466.Suche in Google Scholar
Yang, J., Wang, J., Yang, K., Liu, M., Qi, Y., Zhang, T., Fan, M., Wei, X., Yang, J., Wang, J., et al.. (2018). Antibacterial activity of selenium-enriched lactic acid bacteria against common food-borne pathogens in vitro. J. Dairy Sci. 101: 1930–1942. https://doi.org/10.3168/jds.2017-13430.Suche in Google Scholar
Zhang, W. and Li, C. (2016). Exploiting quorum sensing interfering strategies in gram-negative bacteria for the enhancement of environmental applications. Front. Microbiol. 6: 1535. https://doi.org/10.3389/fmicb.2015.01535.Suche in Google Scholar
Zhao, K., Du, L., Lin, J., Yuan, Y., Wang, X., Yue, B., Wang, X., Guo, Y., Chu, Y., and Zhou, Y. (2018). Pseudomonas aeruginosa quorum-sensing and type VI secretion system can direct interspecific coexistence during evolution. Front. Microbiol. 9: 2287. https://doi.org/10.3389/fmicb.2018.02287.Suche in Google Scholar
© 2021 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Research Articles/Short Communications
- Protein Structure and Function
- Structural and kinetic characterization of Porphyromonas gingivalis glutaminyl cyclase
- Molecular Medicine
- Elucidating the anti-biofilm and anti-quorum sensing potential of selenocystine against respiratory tract infections causing bacteria: in vitro and in silico studies
- Carotenoids in Sporidiobolus pararoseus ameliorate diabetic nephropathy in mice through attenuating oxidative stress
- Cell Biology and Signaling
- Berberine improves dietary-induced cardiac remodeling by upregulating Kruppel-like factor 4-dependent mitochondrial function
- Decreased level of miR-1301 promotes colorectal cancer progression via activation of STAT3 pathway
- JMJD3-regulated expression of IL-6 is involved in the proliferation and chemosensitivity of acute myeloid leukemia cells
- Modulation of recombinant human alpha 1 glycine receptor by flavonoids and gingerols
- IL-24 inhibits the malignancy of human glioblastoma cells via destabilization of Zeb1
- Glycation of benign meningioma cells leads to increased invasion
- Proteolysis
- Marked difference in efficiency of the digestive enzymes pepsin, trypsin, chymotrypsin, and pancreatic elastase to cleave tightly folded proteins
Artikel in diesem Heft
- Frontmatter
- Research Articles/Short Communications
- Protein Structure and Function
- Structural and kinetic characterization of Porphyromonas gingivalis glutaminyl cyclase
- Molecular Medicine
- Elucidating the anti-biofilm and anti-quorum sensing potential of selenocystine against respiratory tract infections causing bacteria: in vitro and in silico studies
- Carotenoids in Sporidiobolus pararoseus ameliorate diabetic nephropathy in mice through attenuating oxidative stress
- Cell Biology and Signaling
- Berberine improves dietary-induced cardiac remodeling by upregulating Kruppel-like factor 4-dependent mitochondrial function
- Decreased level of miR-1301 promotes colorectal cancer progression via activation of STAT3 pathway
- JMJD3-regulated expression of IL-6 is involved in the proliferation and chemosensitivity of acute myeloid leukemia cells
- Modulation of recombinant human alpha 1 glycine receptor by flavonoids and gingerols
- IL-24 inhibits the malignancy of human glioblastoma cells via destabilization of Zeb1
- Glycation of benign meningioma cells leads to increased invasion
- Proteolysis
- Marked difference in efficiency of the digestive enzymes pepsin, trypsin, chymotrypsin, and pancreatic elastase to cleave tightly folded proteins