Outer Membrane Proteins of Salmonella as Potential Markers of Resistance to Serum, Antibiotics and Biocides

Author(s): Bożena Futoma-Kołoch, Gabriela Bugla-Płoskońska*, Bartłomiej Dudek, Agata Dorotkiewicz-Jach, Zuzanna Drulis-Kawa, Andrzej Gamian*.

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 11 , 2019

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Salmonellosis continues to be a significant worldwide health problem. Despite rapid progress in identifying mechanisms of Salmonella virulence and resistance to chemicals, our knowledge of these mechanisms remains limited. Furthermore, it appears that the resistance to antibiotics can be amplified by ubiquitous usage of the disinfectants (biocides), both by industry and by ordinary households. Salmonella, as other Gram-negative bacteria possess outer membrane proteins (OMPs), which participate in maintaining cell integrity, adapting to environment, and interacting with infected host. Moreover, the OMPs may also contribute to resistance to antibacterials. This review summarizes the role of OMPs in Salmonella serum resistance, antibiotics resistance and cross-resistance to biocides. Although collected data do not allow to assign OMPs as markers of the Salmonella susceptibility to the above-mentioned factors, some of these proteins retain a dominant presence in certain types of resistance.

Keywords: Antibiotics, disinfectants, molecular marker, outer membrane proteins, resistance, Salmonella, serum.

May, K.L.; Silhavy, T.J. Making a membrane on the other side of the wall. Biochim. Biophys. Acta, 2017, 1862, 1386-1393.
Chaturvedi, D.; Mahalakshmi, R. Transmembrane β-barrels: evolution, folding and energetics. Biochim. Biophys. Acta, 2017, 1859, 2467-2482.
Remaut, H.; Fronzes, R. Bacterial membranes; Horizon Scientific Press: Poole, 2014.
Zipfel, P.F.; Hallström, T.; Riesbeck, K. Human complement control and complement evasion by pathogenic microbes - tipping the balance. Mol. Immunol., 2013, 56, 152-160.
Narita, S-I.; Tokuda, H. Bacterial lipoproteins; biogenesis, sorting and quality control. Biochim. Biophys. Acta, 2017, 1862, 1414-1423.
Gondwe, E.N.; Molyneux, M.E.; Goodall, M.; Graham, S.M.; Mastroeni, P.; Drayson, M.T.; MacLennan, C.A. Importance of antibody and complement for oxidative burst and killing of invasive nontyphoidal Salmonella by blood cells in Africans. Proc. Natl. Acad. Sci. USA, 2010, 107, 3070-3075.
Gil-Cruz, C.; Bobat, S.; Marshall, J.L.; Kingsley, R.A.; Ross, E.A.; Henderson, I.R.; Leyton, D.L.; Coughlan, R.E.; Khan, M.; Jensen, K.T.; Buckley, C.D.; Dougan, G.; MacLennan, I.C.M.; López-Macías, C.; Cunningham, A.F. The porin OmpD from nontyphoidal Salmonella is a key target for a protective B1b cell antibody response. Proc. Natl. Acad. Sci. USA, 2009, 106, 9803-9808.
Cunningham, A.F.; Gaspal, F.; Serre, K.; Mohr, E.; Henderson, I.R.; Scott-Tucker, A.; Kenny, S.M.; Khan, M.; Toellner, K-M.; Lane, P.J.L.; MacLennan, I.C.M. Salmonella induces a switched antibody response without germinal centers that impedes the extracellular spread of infection. J. Immunol., 2007, 178, 6200-6207.
Widal, F.M. Serodiagnostic de la fiévre typhoide a-propos d'uve modification par MMC Nicolle et al. Halipie. Bull. Soc. Med. Hop, 1896, 13, 561-566.
Ismail, A.; Kader, Z.S.; Kok-Hai, O. Dot enzyme immunosorbent assay for the serodiagnosis of typhoid fever. Southeast Asian J. Trop. Med. Public Health, 1991, 22, 563-566.
Cho, Y.; Park, S.; Barate, A.K.; Truong, Q.L.; Han, J.H.; Jung, C-H.; Yoon, J.W.; Cho, S.; Hahn, T-W. Proteomic analysis of outer membrane proteins in Salmonella enterica Enteritidis. J. Microbiol. Biotechnol., 2015, 25, 288-295.
Bai, J.; Kim, S.I.; Ryu, S.; Yoon, H. Identification and characterization of outer membrane vesicle-associated proteins in Salmonella enterica serovar Typhimurium. Infect. Immun., 2014, 82, 4001-4010.
Cho, Y.; Sun, J.; Han, J.H.; Jang, J.H.; Kang, Z.W.; Hahn, T-W. An immunoproteomic approach for characterization of the outer membrane proteins of Salmonella gallinarum. Electrophoresis, 2014, 35, 888-894.
Ferrer-Navarro, M.; Ballesté-Delpierre, C.; Vila, J.; Fàbrega, A. Characterization of the outer membrane subproteome of the virulent strain Salmonella typhimurium SL1344. J. Proteomics, 2016, 146, 141-147.
Dudek, B.; Krzyżewska, E.; Kapczyńska, K.; Rybka, J.; Pawlak, A.; Korzekwa, K.; Klausa, E.; Bugla-Płoskońska, G. Proteomic analysis of outer membrane proteins from Salmonella enteritidis strains with different sensitivity to human serum. PLoS One, 2016, 11e0164069
Chooneea, D.; Karlsson, R.; Encheva, V.; Arnold, C.; Appleton, H.; Shah, H. Elucidation of the outer membrane proteome of Salmonella enterica serovar Typhimurium utilising a lipid-based protein immobilization technique. BMC Microbiol., 2010, 10, 44.
Majowicz, S.E.; Musto, J.; Scallan, E.; Angulo, F.J.; Kirk, M.; O’Brien, S.J.; Jones, T.F.; Fazil, A.; Hoekstra, R.M. International collaboration on enteric disease ‘Burden of Illness’ studies. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis., 2010, 50, 882-889.
Popoff, M.Y.; Le Minor, L. Antigenic formulas of the Salmonella serovars, 9th ed.; World Health Organization Collaborating Centre for Reference and Research on Salmonella, Pasteur Institute, Paris, 2007.
Shelobolina, E.S.; Sullivan, S.A.; O’Neill, K.R.; Nevin, K.P.; Lovley, D.R. Isolation, characterization, and U(VI)-reducing potential of a facultatively anaerobic, acid-resistant bacterium from low-pH, nitrate- and U(VI)-contaminated subsurface sediment and description of Salmonella subterranea sp. nov. Appl. Environ. Microbiol., 2004, 70, 2959-2965.
Centers for Disease Control and Prevention (CDC). National Enteric Disease Surveillance: Salmonella surveillance overview. Available at: www.cdc.gov/nationalsurveillance/ pdfs/NationalSalmSurveillOverview_508.pdf (Accessed April 9, 2019).
Parker, C.T.; Tindall, B.J.; Garrity, G.M. International code of nomenclature of prokaryotes. Int. J. Syst. Evol. Microbiol., 2016, 69(1A), S1-S111.
World Health Organization State of the art report health risks in aquifer recharge using reclaimer water., Available at: www.euro.who.int/__data/assets/pdf_file/0018/240228/E78995.pdf (Accessed April 9, 2019).
Kenneth, J.; Ryan, M.D.C.; George Ray, M.D. Sherris Medical Microbiology. An Introduction to Infectious Diseases. Medical Publishing Division, 4th ed; McGraw-Hill, 2004.
World Health Organization. Available at: www.who.int/en/news-room/fact-sheets/detail/salmonella-(non-typhoidal) (Accessed April 9, 2019).
Darwin, K.H.; Miller, V.L. Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clin. Microbiol. Rev., 1999, 12, 405-428.
European Food Safety Authority. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2016. Available at:, www.efsa.europa.eu/en/efsajournal/pub/5182 (Accessed April 9, 2019).
Kariuki, S.; Gordon, M.A.; Feasey, N.; Parry, C.M. Antimicrobial resistance and management of invasive Salmonella disease. Vaccine, 2015, 33, C21-C29.
Boyd, D.; Cloeckaert, A.; Chaslus-Dancla, E.; Mulvey, M.R. Characterization of variant Salmonella genomic island 1 multidrug resistance regions from serovars Typhimurium DT104 and Agona. Antimicrob. Agents Chemother., 2002, 46, 1714-1722.
Kempf, I.; Jouy, E.; Chauvin, C. Colistin use and colistin resistance in bacteria from animals. Int. J. Antimicrob. Agents, 2016, 48, 598-606.
Directive 98/8/EC of the European Parliament and of the Council of 16 February 1998 concerning the placing of biocidal products on the market. J. Eur. Commun., 1998, Vol. 41.
European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC).European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J., 2018, 16(12)e5500
Yu, C-Y.; Chou, S-J.; Yeh, C-M.; Chao, M-R.; Huang, K-C.; Chang, Y-F.; Chiou, C-S.; Weill, F-X.; Chiu, C-H.; Chu, C-H.; Chu, C. Prevalence and characterization of multidrug-resistant (type ACSSuT) Salmonella enterica serovar Typhimurium strains in isolates from four gosling farms and a hatchery farm. J. Clin. Microbiol., 2008, 46, 522-526.
Threlfall, E.J.; Frost, J.A.; Ward, L.R.; Rowe, B. Increasing spectrum of resistance in multiresistant Salmonella Typhimurium. Lancet, 1996, 347, 1053-1054.
Cavaco, L.M.; Hasman, H.; Xia, S.; Aarestrup, F.M. qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob. Agents Chemother., 2009, 53, 603-608.
Ellington, M.J.; Ekelund, O.; Aarestrup, F.M.; Canton, R.; Doumith, M.; Giske, C.; Grundman, H.; Hasman, H.; Holden, M.T.G.; Hopkins, K.L.; Iredell, J.; Kahlmeter, G.; Köser, C.U.; MacGowan, A.; Mevius, D.; Mulvey, M.; Naas, T.; Peto, T.; Rolain, J-M.; Samuelsen, Ø.; Woodford, N. The role of whole genome sequencing in antimicrobial susceptibility testing of bacteria: Report from the EUCAST Subcommittee. Clin. Microbiol. Infect., 2017, 23, 2-22.
Hendriksen, R.S.; Leekitcharoenphon, P.; Mikoleit, M.; Jensen, J.D.; Kaas, R.S.; Roer, L.; Joshi, H.B.; Pornruangmong, S.; Pulsrikarn, C.; Gonzalez-Aviles, G.D.; Reuland, E.A. Naiemi, Al, N.; Wester, A.L.; Aarestrup, F.M.; Hasman, H. Genomic dissection of travel-associated extended-spectrum-beta-lactamase-producing Salmonella enterica serovar Typhi isolates originating from the Philippines: a one-off occurrence or a threat to effective treatment of typhoid fever? J. Clin. Microbiol., 2015, 53, 677-680.
Hopkins, K.L.; Wootton, L.; Day, M.R.; Threlfall, E.J. Plasmid-mediated quinolone resistance determinant qnrS1 found in Salmonella enterica strains isolated in the UK. J. Antimicrob. Chemother., 2007, 59, 1071-1075.
Moskowitz, S.M.; Brannon, M.K.; Dasgupta, N.; Pier, M.; Sgambati, N.; Miller, A.K.; Selgrade, S.E.; Miller, S.I.; Denton, M.; Conway, S.P.; Johansen, H.K.; Høiby, N. PmrB mutations promote polymyxin resistance of Pseudomonas aeruginosa isolated from colistin-treated cystic fibrosis patients. Antimicrob. Agents Chemother., 2012, 56, 1019-1030.
Guo, L.; Lim, K.B.; Gunn, J.S.; Bainbridge, B.; Darveau, R.P.; Hackett, M.; Miller, S.I. Regulation of lipid a modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science, 1997, 276, 250-253.
Anjum, M.F.; Duggett, N.A.; AbuOun, M.; Randall, L.; Nunez-Garcia, J.; Ellis, R.J.; Rogers, J.; Horton, R.; Brena, C.; Williamson, S.; Martelli, F.; Davies, R.; Teale, C. Colistin resistance in Salmonella and Escherichia coli isolates from a pig farm in Great Britain. J. Antimicrob. Chemother., 2016, 71, 2306-2313.
Liu, Y-Y.; Wang, Y.; Walsh, T.R.; Yi, L-X.; Zhang, R.; Spencer, J.; Doi, Y.; Tian, G.; Dong, B.; Huang, X.; Yu, L.F.; Gu, D.; Ren, H.; Chen, X.; Lv, L.; He, D.; Zhou, H.; Liang, Z.; Liu, J.H.; Shen, J. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: A microbiological and molecular biological study. Lancet Infect. Dis., 2016, 16, 161-168.
Thanh, D.P.; Tuyen, H.T.; Nguyen, T.N.T.; Wick, R.R.; Thwaites, G.; Baker, S.; Holt, K.E. Inducible colistin resistance via a disrupted plasmid-borne mcr-1 gene in a 2008 Vietnamese Shigella sonnei isolate. J. Antimicrob. Chemother., 2016, 71, 2314-2317.
Tse, H.; Yuen, K-Y. Dissemination of the mcr-1 colistin resistance gene. Lancet Infect. Dis., 2016, 2, 145-146.
European Medicines Agency. Updated advice on the use of colistin products in animals within the European Union: development of resistance and possible impact on human and animal health.EMA/CVMP/CHMP/231573/2016, 27 July, 2016.
Herrero-Fresno, A.; Wallrodt, I.; Leekitcharoenphon, P.; Olsen, J.E.; Aarestrup, F.M.; Hendriksen, R.S. The role of the St313-Td gene in virulence of Salmonella typhimurium ST313. PLoS One, 2014, 9e84566
Parsons, B.N.; Humphrey, S.; Salisbury, A.M.; Mikoleit, J.; Hinton, J.C.D.; Gordon, M.A.; Wigley, P. Invasive non-typhoidal Salmonella typhimurium ST313 are not host-restricted and have an invasive phenotype in experimentally infected chickens. PLoS Negl. Trop. Dis., 2013, 7e2487
Futoma-Kołoch, B. Bacterial outer membrane proteins - dependent complement activation. J. Mol. Immunol., 2016, 1, 1000e104.
Bennett, K.M.; Rooijakkers, S.H.M.; Gorham, R.D. Let’s tie the knot: marriage of complement and adaptive immunity in pathogen evasion, for better or worse. Front. Microbiol., 2017, 8, 944.
Haas, P-J.; van Strijp, J. Anaphylatoxins: their role in bacterial infection and inflammation. Immunol. Res., 2007, 37, 161-175.
Garcia, B.L.; Zwarthoff, S.A.; Rooijakkers, S.H.M.; Geisbrecht, B.V. Novel evasion mechanisms of the classical complement pathway. J. Immunol., 2016, 197, 2051-2060.
Merle, N.S.; Noe, R.; Halbwachs-Mecarelli, L.; Fremeaux-Bacchi, V.; Roumenina, L.T. Complement system part II: role in immunity. Front. Immunol., 2015, 6, 257.
Rosbjerg, A.; Genster, N.; Pilely, K.; Garred, P. Evasion mechanisms used by pathogens to escape the lectin complement pathway. Front. Microbiol., 2017, 8, 1212.
Fernández, F.J.; Gómez, S.; Vega, M.C. Pathogens’ toolbox to manipulate human complement. Sem. Cell Develop. Biol., 2017, S1084-9521(17), 30138-30146.
Nicod, C.; Banaei-Esfahani, A.; Collins, B.C. Elucidation of host-pathogen protein–protein interactions to uncover mechanisms of host cell rewiring. Curr. Opin. Microbiol., 2017, 39, 7-15.
Heffernan, E.J.; Reed, S.; Hackett, J.; Fierer, J.; Roudier, C.; Guiney, D. Mechanism of resistance to complement-mediated killing of bacteria encoded by the Salmonella Typhimurium virulence plasmid gene Rck. J. Clin. Invest., 1992, 90, 953-964.
Mambu, J.; Virlogeux-Payant, I.; Holbert, S.; Grépinet, O.; Velge, P.; Wiedemann, A. An updated view on the Rck invasin of Salmonella: still much to discover. Front. Cell. Infect. Microbiol., 2017, 7, 500.
Gunn, J.S.; Alpuche-Aranda, C.M.; Loomis, W.P.; Belden, W.J.; Miller, S.I. Characterization of the Salmonella typhimurium pagC/pagD chromosomal region. J. Bacteriol., 1995, 177, 5040-5047.
Pulkkinen, W.S.; Miller, S.I. A Salmonella typhimurium virulence protein is similar to a Yersinia enterocolitica invasion protein and a bacteriophage lambda outer membrane protein. J. Bacteriol., 1991, 173, 86-93.
Miller, V.L.; Falkow, S. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect. Immun., 1988, 56, 1242-1248.
Heffernan, E.J.; Harwood, J.; Fierer, J.; Guiney, D. The Salmonella Typhimurium virulence plasmid complement resistance gene Rck is homologous to a family of virulence-related outer membrane protein genes, including pagC and Ail. J. Bacteriol., 1992, 174, 84-91.
Haneda, T.; Okada, N.; Nakazawa, N.; Kawakami, T.; Danbara, H. Complete DNA sequence and comparative analysis of the 50-kilobase virulence plasmid of Salmonella enterica serovar Choleraesuis. Infect. Immun., 2001, 69, 2612-2620.
Nishio, M.; Okada, N.; Miki, T.; Haneda, T.; Danbara, H. Identification of the outer-membrane protein PagC required for the serum resistance phenotype in Salmonella enterica serovar Choleraesuis. Microbiol., 2005, 151, 863-873.
Mecsas, J.; Welch, R.; Erickson, J.W.; Gross, C.A. Identification and characterization of an outer membrane protein, OmpX, in Escherichia coli that is homologous to a family of outer membrane proteins including Ail of Yersinia enterocolitica. J. Bacteriol., 1995, 177, 799-804.
Ho, D.K.; Tissari, J.; Järvinen, H.M.; Blom, A.M.; Meri, S.; Jarva, H. Functional recruitment of human complement inhibitor C4B-binding protein to outer membrane protein Rck of Salmonella. PLoS One, 2011, 6e27546
Abed, N.; Grépinet, O.; Canepa, S.; Hurtado-Escobar, G.A.; Guichard, N.; Wiedemann, A.; Velge, P.; Virlogeux-Payant, I. Direct regulation of the pefI-srgC operon encoding the Rck invasin by the quorum-sensing regulator SdiA in Salmonella Typhimurium. Mol. Microbiol., 2014, 94, 254-271.
Parente, R.; Clark, S.J.; Inforzato, A.; Day, A.J. Complement factor H in host defense and immune evasion. Cell. Mol. Life Sci., 2017, 74, 1605-1624.
Rawal, N.; Rajagopalan, R.; Salvi, V.P. Stringent regulation of complement lectin pathway C3/C5 convertase by C4b-binding protein (C4BP). Mol. Immunol., 2009, 46, 2902-2910.
Hovingh, E.S.; van den Broek, B.; Jongerius, I. Hijacking complement regulatory proteins for bacterial immune evasion. Front. Microbiol., 2016, 7, 325.
Ho, D.K.; Jarva, H.; Meri, S. Human complement factor H binds to outer membrane protein Rck of Salmonella. J. Immunol., 2010, 185, 1763-1769.
Miller, V.L.; Beer, K.B.; Loomis, W.P.; Olson, J.A.; Miller, S.I. An unusual pagC:TnphoA mutation leads to an invasion- and virulence-defective phenotype in Salmonellae. Infect. Immun., 1992, 60, 3763-3770.
Guina, T.; Yi, E.C.; Wang, H.; Hackett, M.; Miller, S.I. A PhoP-regulated outer membrane protease of Salmonella enterica serovar Typhimurium promotes resistance to alpha-helical antimicrobial peptides. J. Bacteriol., 2000, 182, 4077-4086.
Ramu, P.; Lobo, L.A.; Kukkonen, M.; Bjur, E.; Suomalainen, M.; Raukola, H.; Miettinen, M.; Julkunen, I.; Holst, O.; Rhen, M.; Korhonen, T.K.; Lähteenmäki, K. Activation of pro-matrix metalloproteinase-9 and degradation of gelatin by the surface protease PgtE of Salmonella enterica serovar Typhimurium. Int. J. Med. Microbiol., 2008, 298, 263-278.
Haiko, J.; Laakkonen, L.; Juuti, K.; Kalkkinen, N.; Korhonen, T.K. The omptins of Yersinia pestis and Salmonella Enterica cleave the reactive center loop of plasminogen activator inhibitor 1. J. Bacteriol., 2010, 192, 4553-4561.
Järvinen, H.M.; Laakkonen, L.; Haiko, J.; Johansson, T.; Juuti, K.; Suomalainen, M.; Buchrieser, C.; Kalkkinen, N.; Korhonen, T.K. Human single-chain urokinase is activated by the omptins PgtE of Salmonella enterica and Pla of Yersinia pestis despite mutations of active site residues. Mol. Microbiol., 2013, 89, 507-517.
Ramu, P.; Tanskanen, R.; Holmberg, M.; Lähteenmäki, K.; Korhonen, T.K.; Meri, S. The surface protease PgtE of Salmonella enterica affects complement activity by proteolytically cleaving C3b, C4b and C5. FEBS Lett., 2007, 581, 1716-1720.
Zhou, Y.; Zhou, J.; Wang, D.; Gao, Q.; Mu, X.; Gao, S.; Liu, X. Evaluation of ompA and pgtE genes in determining pathogenicity in Salmonella enterica serovar Enteritidis. Vet. J., 2016, 218, 19-26.
Riva, R.; Korhonen, T.K.; Meri, S. The outer membrane protease PgtE of Salmonella enterica interferes with the alternative complement pathway by cleaving factors B and H. Front. Microbiol., 2015, 6, 63.
Schaller, J.; Gerber, S.; Kaempfer, U.; Lejon, S.; Trachsel, C. Human Blood Plasma Proteins; John Wiley & Sons: Chichester, UK, 2008.
Sukupolvi, S.; Vuorio, R.; Qi, S.Y.; O’Connor, D.; Rhen, M. Characterization of the traT gene and mutants that increase outer membrane permeability from the Salmonella typhimurium virulence plasmid. Mol. Microbiol., 1990, 4, 49-57.
Sukupolvi, S.; O’Connor, C.D. TraT lipoprotein, a plasmid-specified mediator of interactions between gram-negative bacteria and their environment. Microbiol. Rev., 1990, 54, 331-341.
Pramoonjago, P.; Kaneko, M.; Kinoshita, T.; Ohtsubo, E.; Takeda, J.; Hong, K.S.; Inagi, R.; Inoue, K. Role of TraT protein, an anticomplementary protein produced in Escherichia coli by R100 factor, in serum resistance. J. Immunol., 1992, 148, 827-836.
Sarowska, J.; Bugla-Płoskońska, G.; Futoma-Kołoch, B.; Drulis-Kawa, Z. The sensitivity level of Salmonella enterica ESBL+ transconjugants to normal human serum correlated with OMP band patterns obtained by SDS-PAGE. Adv. Clin. Exp. Med., 2010, 6, 669-677.
Futoma-Kołoch, B.; Bugla-Płoskońska, G.; Sarowska, J. In:Salmonella - distribution, adaptation, control measures and molecular technologies., Bassam A. Annous; Joshua B. ; Gurtler,; Ed.;. InTech, 2012, pp. 265-290.
Futoma-Kołoch, B.; Dudek, B.; Kapczyńska, K.; Krzyżewska, E.; Wańczyk, M.; Korzekwa, K.; Rybka, J.; Klausa, E.; Bugla-Płoskońska, G. Relationship of triamine-biocide tolerance of Salmonella enterica serovar Senftenberg to antimicrobial susceptibility, serum resistance and outer membrane proteins. Int. J. Mol. Sci., 2017, 18, 1459.
Bugla-Płoskońska, G.; Korzeniowska-Kowal, A.; Guz-Regner, K. Reptiles as a source of Salmonella O48-clinically important bacteria for children: the relationship between resistance to normal cord serum and outer membrane protein patterns. Microb. Ecol., 2011, 61, 41-51.
Parry, C.M. Antimicrobial drug resistance in Salmonella enterica. Curr. Opin. Infect. Dis., 2003, 16, 467-472.
Nishino, K.; Latifi, T.; Groisman, E.A. Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol. Microbiol., 2006, 59, 126-141.
Miller, S.I. Antibiotic resistance and regulation of the gram-negative bacterial outer membrane barrier by host innate immune molecules. MBio, 2016, 7, e01541-e16.
Quinn, T.; O’Mahony, R.; Baird, A.W.; Drudy, D.; Whyte, P.; Fanning, S. Multi-drug resistance in Salmonella enterica: Efflux mechanisms and their relationships with the development of chromosomal resistance gene clusters. Curr. Drug Targets, 2006, 7, 849-860.
Nikaido, H. Multidrug efflux pumps of gram-negative bacteria. J. Bacteriol., 1996, 178, 5853-5859.
Horiyama, T.; Yamaguchi, A.; Nishino, K. TolC dependency of multidrug efflux systems in Salmonella enterica serovar Typhimurium. J. Antimicrob. Chemother., 2010, 65, 1372-1376.
Andersen, J.L.; He, G-X.; Kakarla, P. K C, R.; Kumar, S.; Lakra, W.S.; Mukherjee, M.M.; Ranaweera, I.; Shrestha, U.; Tran, T.; Varela, M.F. Multidrug efflux pumps from Enterobacteriaceae, Vibrio cholerae and Staphylococcus aureus bacterial food pathogens. Int. J. Environ. Res. Public Health, 2015, 12, 1487-1547.
Baucheron, S.; Chaslus-Dancla, E.; Cloeckaert, A. Role of TolC and parC mutation in high-level fluoroquinolone resistance in Salmonella enterica serotype Typhimurium DT204. J. Antimicrob. Chemother., 2004, 53, 657-659.
Tal, N.; Schuldiner, S. A Coordinated network of transporters with overlapping specificities provides a robust survival strategy. Proc. Natl. Acad. Sci. USA, 2009, 106, 9051-9056.
Murakami, S.; Nakashima, R.; Yamashita, E.; Matsumoto, T.; Yamaguchi, A. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature, 2006, 443, 173-179.
Koronakis, V.; Li, J.; Koronakis, E.; Stauffer, K. Structure of TolC, the outer membrane component of the bacterial type I efflux system, derived from two-dimensional crystals. Mol. Microbiol., 1997, 23, 617-626.
Koronakis, V.; Sharff, A.; Koronakis, E.; Luisi, B.; Hughes, C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature, 2000, 405, 914-919.
Morona, R.; Manning, P.A.; Reeves, P. Identification and characterization of the TolC protein, an outer membrane protein from Escherichia coli. J. Bacteriol., 1983, 153, 693-699.
Higgins, M.K.; Bokma, E.; Koronakis, E.; Hughes, C.; Koronakis, V. Structure of the periplasmic component of a bacterial drug efflux pump. Proc. Natl. Acad. Sci. USA, 2004, 101, 9994-9999.
Wang, Z.; Fan, G.; Hryc, C.F.; Blaza, J.N.; Serysheva, I.I.; Schmid, M.F.; Chiu, W.; Luisi, B.F.; Du, D. An allosteric transport mechanism for the AcrAB-TolC multidrug efflux pump. eLife, 2017, 6, 11103.
Webber, M.A.; Bailey, A.M.; Blair, J.M.A.; Morgan, E.; Stevens, M.P.; Hinton, J.C.D.; Ivens, A.; Wain, J.; Piddock, L.J.V. The global consequence of disruption of the AcrAB-TolC efflux pump in Salmonella enterica includes reduced expression of SPI-1 and other attributes required to infect the host. J. Bacteriol., 2009, 191, 4276-4285.
Pagès, J-M.; James, C.E.; Winterhalter, M. The porin and the permeating antibiotic: a selective diffusion barrier in gram-negative bacteria. Nat. Rev. Microbiol., 2008, 6, 893-903.
Hu, W.S.; Lin, J-F.; Lin, Y-H.; Chang, H-Y. Outer membrane protein STM3031 (Ail/OmpX-Like Protein) plays a key role in the ceftriaxone resistance of Salmonella enterica serovar Typhimurium. Antimicrob. Agents Chemother., 2009, 53, 3248-3255.
Santiviago, C.A.; Fuentes, J.A.; Bueno, S.M.; Trombert, A.N.; Hildago, A.A.; Socias, L.T.; Youderian, P.; Mora, G.C. The Salmonella enterica sv. Typhimurium smvA, yddG and ompD (porin) genes are required for the efficient efflux of methyl viologen. Mol. Microbiol., 2002, 46, 687-698.
Pilonieta, M.C.; Erickson, K.D.; Ernst, R.K.; Detweiler, C.S. A protein important for antimicrobial peptide resistance, YdeI/OmdA, is in the periplasm and interacts with OmpD/NmpC. J. Bacteriol., 2009, 191, 7243-7252.
Zgurskaya, H.I.; Krishnamoorthy, G.; Ntreh, A.; Lu, S. Mechanism and function of the outer membrane channel TolC in multidrug resistance and physiology of Enterobacteria. Front. Microbiol., 2011, 2, 189.
Li, Q.; Hu, Y.; Wu, Y.; Wang, X.; Xie, X.; Tao, M.; Yin, J.; Lin, Z.; Jiao, Y.; Xu, L.; Jiao, X. Complete genome sequence of Salmonella enterica serovar Pullorum multidrug resistance strain S06004 from China. J. Microbiol. Biotechnol., 2015, 25, 606-611.
Usui, M.; Nagai, H.; Hiki, M.; Tamura, Y.; Asai, T. Effect of antimicrobial exposure on AcrAB expression in Salmonella enterica subspecies enterica serovar Choleraesuis. Front. Microbiol., 2013, 4, 53.
Feuerriegel, S.; Heisig, P. Role of global regulator rma for multidrug efflux-mediated fluoroquinolone resistance in Salmonella. Microb. Drug Resist., 2008, 14, 259-263.
Kalily, E.; Hollander, A.; Korin, B.; Cymerman, I.; Yaron, S. Mechanisms of resistance to linalool in Salmonella Senftenberg and their role in survival on Basil. Environ. Microbiol., 2016, 18, 3673-3688.
Solnik-Isaac, H.; Weinberger, M.; Tabak, M.; Ben-David, A.; Shachar, D.; Yaron, S. Quinolone resistance of Salmonella enterica serovar Virchow isolates from humans and poultry in Israel: evidence for clonal expansion. J. Clin. Microbiol., 2007, 45, 2575-2579.
Santiviago, C.A.; Toro, C.S.; Bucarey, S.A.; Mora, G.C. A Chromosomal Region Surrounding the ompD porin gene marks a genetic difference between Salmonella typhi and the majority of Salmonella serovars. Microbiol., 2001, 147, 1897-1907.
Toro, C.S.; Lobos, S.R.; Calderón, I.; Rodríguez, M.; Mora, G.C. Clinical isolate of a porinless Salmonella typhi resistant to high levels of chloramphenicol. Antimicrob. Agents Chemother., 1990, 34, 1715-1719.
Muriel Masi, J-M.P. Suppl 1: Structure, function and regulation of outer membrane proteins involved in drug transport in Enterobactericeae: the OmpF/C - TolC case. Open Microbiol. J., 2013, 7, 22-33.
Long, M.; Lai, H.; Deng, W.; Zhou, K.; Li, B.; Liu, S.; Fan, L.; Wang, H.; Zou, L. Disinfectant susceptibility of different Salmonella serotypes isolated from chicken and egg production chains. J. Appl. Microbiol., 2016, 121, 672-681.
Książczyk, M.; Krzyżewska, E.; Futoma-Kołoch, B.; Bugla-Płoskońska, G. Disinfectants - bacterial cells interactions in the view of hygiene and public health. Postepy Hig. Med. Dosw., 2015, 69, 1042-1055.
Futoma-Kołoch, B.; Książczyk, M. The risk of Salmonella resistance following exposure to common disinfectants: an emerging problem. Biol. Internat., 2013, 53, 54-66.
McDonnell, G.; Russell, A.D. Antiseptics and disinfectants: activity, action, and resistance. Clin. Microbiol. Rev., 1999, 12, 147-179.
McLaren, I.; Wales, A.; Breslin, M.; Davies, R. Evaluation of commonly-used farm disinfectants in wet and dry models of Salmonella farm contamination. Avian Pathol., 2011, 40, 33-42.
Dann, A.B.; Hontela, A. Triclosan: environmental exposure, toxicity and mechanisms of action. J. Appl. Toxicol., 2011, 31, 285-311.
Condell, O.; Power, K.A.; Händler, K.; Finn, S.; Sheridan, A.; Sergeant, K.; Renaut, J.; Burgess, C.M.; Hinton, J.C.D.; Nally, J.E.; Fanning, S. Comparative analysis of Salmonella susceptibility and tolerance to the biocide chlorhexidine identifies a complex cellular defense network. Front. Microbiol., 2014, 5, 373.
Shah, N.; Naseby, D.C. Efficacy of benzalkonium chloride against bioluminescent P. aeruginosa ATCC9027 constructs. Biosens. Bioelectron., 2017, 97, 8-15.
Carrique-Mas, J.J.; Marin, C.; Breslin, M.; McLaren, I.; Davies, R. A Comparison of the efficacy of cleaning and disinfection methods in eliminating Salmonella spp. from commercial egg laying houses. Avian Pathol., 2009, 38, 419-424.
Lin, W.; Guan, X.; Cao, J.; Niu, B.; Chen, Q. Bactericidal mechanism of glutaraldehyde-didecyldimethylammonium bromide as a disinfectant against Escherichia coli. J. Appl. Microbiol., 2017, 122, 676-685.
Endo, Y.; Tani, T.; Kodama, M. Antimicrobial activity of tertiary amine covalently bonded to a polystyrene fiber. Appl. Environ. Microbiol., 1987, 53, 2050-2055.
Linley, E.; Denyer, S.P.; McDonnell, G.; Simons, C.; Maillard, J-Y. Use of hydrogen peroxide as a biocide: new consideration of its mechanisms of biocidal Action. J. Antimicrob. Chemother., 2012, 67, 1589-1596.
Curiao, T.; Marchi, E.; Grandgirard, D.; León-Sampedro, R.; Viti, C.; Leib, S.L.; Baquero, F.; Oggioni, M.R.; Martinez, J.L.; Coque, T.M. Multiple adaptive routes of Salmonella enterica Typhimurium to biocide and antibiotic exposure. BMC Genomics, 2016, 17, 491.
Karatzas, K.A.G.; Randall, L.P.; Webber, M.; Piddock, L.J.V.; Humphrey, T.J.; Woodward, M.J.; Coldham, N.G. Phenotypic and proteomic characterization of multiply antibiotic-resistant variants of Salmonella enterica serovar Typhimurium selected following exposure to disinfectants. Appl. Environ. Microbiol., 2008, 74, 1508-1516.
Futoma-Kołoch, B.; Książczyk, M.; Korzekwa, K.; Migdał, I.; Pawlak, A.; Jankowska, M.; Kędziora, A.; Dorotkiewicz-Jach, A.; Bugla-Płoskońska, G. Selection and electrophoretic characterization of Salmonella enterica subsp. enterica biocide variants resistant to antibiotics. Pol. J. Vet. Sci., 2015, 18, 725-732.
Zhang, C.-Z.; Chen, P.-X.; Yang, L.; Li, W.; Chang, M.-X.; Jiang, H.-X. Coordinated expression of acrAB-tolC and eight other functional efflux pumps through activating ramA and marA in Salmonella enterica serovar Typhimurium. Microb. Drug Resist., 2017. mdr.2017.0086.
Bailey, A.M.; Constantinidou, C.; Ivens, A.; Garvey, M.I.; Webber, M.A.; Coldham, N.; Hobman, J.L.; Wain, J.; Woodward, M.J.; Piddock, L.J.V. Exposure of Escherichia coli and Salmonella enterica serovar Typhimurium to triclosan induces a species-specific response, including drug detoxification. J. Antimicrob. Chemother., 2009, 64, 973-985.
Whitehead, R.N.; Overton, T.W.; Kemp, C.L.; Webber, M.A. Exposure of Salmonella enterica serovar Typhimurium to high level biocide challenge can select multidrug resistant mutants in a single step. PLoS One, 2011, 6e22833
Rifai, N.; Gillette, M.A.; Carr, S.A. Protein biomarker discovery and validation: The long and uncertain path to clinical utility. Nat. Biotechnol., 2006, 24, 971-983.

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Year: 2019
Page: [1960 - 1978]
Pages: 19
DOI: 10.2174/0929867325666181031130851
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