Login Register Cart 0
Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Letter Article

Bovine Lactoferrin can Decrease the In Vitro Biofilm Production and Show Synergy with Antibiotics Against Listeria and Escherichia coli Isolates

Author(s): Karla Alejandra García-Borjas, Ivonne Ceballos-Olvera, Sarahí Luna-Castro* and Yosahandy Peña-Avelino

Volume 28, Issue 1, 2021

Published on: 03 April, 2020

Page: [101 - 107] Pages: 7

DOI: 10.2174/0929866527666200403111743

Price: $65

Abstract

Background: Bovine Lactoferrin (bLf) has been reported as antimicrobial, antiviral, immunomodulatory and anticancer protein. Escherichia coli and Listeria spp. are food-borne bacteria that can produce illness in human being and mammals, the emergent antimicrobial drug resistance has been reported in these pathogens.

Objective: The aim for this study was to evaluate the bLf effect on in vitro biofilm production and the synergic effect of antibiotics on E. coli and Listeria isolates.

Methods: E. coli and Listeria specimens were isolated from bovine carcasses and slaughterhouses surfaces, respectively. Biofilm formation was analyzed with or without bLf, incubated for 48 h and spectrophotometry, cell viability was analyzed by colony-forming unit (CFU) and the synergistic effect of bLf with ampicillin, oxytetracycline, and streptomycin was evaluated through the fractional concentration index (FCI).

Results: Our results show that a low bLf concentration (0.8 μM) can diminish the in vitro biofilm production in Listeria isolates; also improves the in vitro oxytetracycline and streptomycin activity against E. coli, and ampicillin activity against Listeria isolates.

Conclusion: bLf can affect the biofilm production in Listeria isolates from slaughterhouses surfaces and shown synergic effect with ampicillin. Also has a synergic effect with oxytetracycline and streptomycin against E. coli isolates from bovine carcasses.

Keywords: Bovine Lactoferrin, Escherichia coli, Listeria, biofilm production, synergy, antibiotics.

« Previous Next »
Graphical Abstract

[1]
Baker, H.M.; Baker, E.N. Lactoferrin and iron: structural and dynamic aspects of binding and release. Biometals, 2004, 17(3), 209-216.
[http://dx.doi.org/10.1023/B:BIOM.0000027694.40260.70] [PMID: 15222467]
[2]
Trybek, G.; Metlerski, M.; Szumilas, K.; Aniko-Wlodarczyk, M.; Preuss, O.; Grocholewicz, K.; Wiszniewska, B. The biological properties of Lactoferrin. Cent Eur J Sport Sci Med, 201, 15(3), 15-25.
[3]
Vogel, H.J. Lactoferrin, a bird’s eye view. Biochem. Cell Biol., 2012, 90(3), 233-244.
[http://dx.doi.org/10.1139/o2012-016] [PMID: 22540735]
[4]
Drago-Serrano, M.E.; Campos-Rodríguez, R.; Carrero, J.L.; de la Garza, M. Lactoferrin: Balancing ups and downs of inflammation due to microbial infections. Int. J. Mol. Sci., 2017, 18, 501-522.
[http://dx.doi.org/10.3390/ijms18030501]
[5]
Baker, E.N.; Baker, H.M. A structural framework for understanding the multifunctional character of lactoferrin. Biochimie, 2009, 91(1), 3-10.
[http://dx.doi.org/10.1016/j.biochi.2008.05.006] [PMID: 18541155]
[6]
Khan, J.A.; Kumar, P.; Paramasivam, M.; Yadav, R.S.; Sahani, M.S.; Sharma, S.; Srinivasan, A.; Singh, T.P. Camel lactoferrin, a transferrin-cum-lactoferrin: crystal structure of camel apolactoferrin at 2.6 A resolution and structural basis of its dual role. J. Mol. Biol., 2001, 309(3), 751-761.
[http://dx.doi.org/10.1006/jmbi.2001.4692] [PMID: 11397094]
[7]
Yamauchi, K.; Tomita, M.; Giehl, T.J.; Ellison, R.T., III Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect. Immun., 1993, 61(2), 719-728.
[http://dx.doi.org/10.1128/IAI.61.2.719-728.1993] [PMID: 8423097]
[8]
Tsuji, S.; Hirata, Y.; Mukai, F.; Ohtagaki, S. Comparison of lactoferrin content in colostrum between different cattle breeds. J. Dairy Sci., 1990, 73(1), 125-128.
[http://dx.doi.org/10.3168/jds.S0022-0302(90)78654-7] [PMID: 2107229]
[9]
Abd El-Gawad, I.A.; El-Sayed, E.M.; Mahfouz, M.B.; Abd El-Salam, A.M. Changes of Lactoferrin concentration in colostrum and milk from different species. Egypt. J Dairy Sci., 1996, 24, 297-308.
[10]
Murdock, C.A.; Cleveland, J.; Matthews, K.R.; Chikindas, M.L. The synergistic effect of nisin and lactoferrin on the inhibition of Listeria monocytogenes and Escherichia coli O157:H7. Lett. Appl. Microbiol., 2007, 44(3), 255-261.
[http://dx.doi.org/10.1111/j.1472-765X.2006.02076.x] [PMID: 17309501]
[11]
Leon-Sicairos, N.; Canizalez-Roman, A.; de la Garza, M.; Reyes-Lopez, M.; Zazueta-Beltran, J.; Nazmi, K.; Gomez-Gil, B.; Bolscher, J.G. Bactericidal effect of lactoferrin and lactoferrin chimera against halophilic Vibrio parahaemolyticus. Biochimie, 2009, 91(1), 133-140.
[http://dx.doi.org/10.1016/j.biochi.2008.06.009] [PMID: 18625283]
[12]
Flores-Villaseñor, H.; Canizalez-Román, A.; Reyes-Lopez, M.; Nazmi, K.; De La Garza, M. Zazueta- Beltrán, J; León-Sicairos, N.; Bolscher, J. G. M. Bactericidal effect of bovine Lactoferrin, LFcin, LFampin and LFchimera on antibiotic-resistant Staphylococcus aureus and Escherichia coli. Biometals, 2010, 23(3), 569-578.
[PMID: 20195887]
[13]
Mosquito, S.; Zegarra, G.; Villanueva, C.; Ruiz, J.; Ochoa, T.J. Effect of bovine lactoferrin on the minimum inhibitory concentrations of ampicillin and trimethoprim-sulfamethoxazole for clinical Shigella spp. strains. Biochem. Cell Biol., 2012, 90(3), 412-416.
[http://dx.doi.org/10.1139/o11-066] [PMID: 22397495]
[14]
Luna-Castro, S.; Aguilar-Romero, F. Samaniego- Barrón, L.; Godínez-Vargas, D.; De La Garza, M. Effect of bovine apo-lactoferrin on the growth and virulence of Actinobacillus pleuropneumoniae. Biometals, 2014, 27(5), 891-903.
[http://dx.doi.org/10.1007/s10534-014-9752-5] [PMID: 24878848]
[15]
Acosta-Smith, E.; Viveros-Jiménez, K.; Canizalez-Román, A.; Reyes-Lopez, M.; Bolscher, J.G.M.; Nazmi, K.; Flores-Villaseñor, H.; Alapizco-Castro, G.; de la Garza, M.; Martínez-Garcia, J.J. Velazquez- Roman, J.; Leon-Sicairos, N. Bovine Lactoferrin and Lactoferrin-derived peptides inhibit the growth of Vibrio cholerae and other Vibrio species. Front. Microbiol., 2018, 8(JAN), 2633.
[16]
Sijbrandij, T.; Ligtenberg, A.J.; Nazmi, K.; van den Keijbus, P.A.M.; Veerman, E.C.I.; Bolscher, J.G.M.; Bikker, F.J. LFchimera protects HeLa cells from invasion by Yersinia spp. in vitro. Biometals, 2018, 31(6), 941-950.
[http://dx.doi.org/10.1007/s10534-018-0136-0] [PMID: 30136243]
[17]
Vargas, C.Y.V.; Rodríguez, G.J.A.; Umaña, P.Y.A.; Leal, C.A.L.; Almanzar, R.G.; García, C.J.E.; Rivera, M.Z.J. Antibacterial synthetic peptides derived from bovine lactoferricin exhibit cytotoxic effect against MDA-MB-468 and MDA-MB-231 breast cancer cell lines. Molecules, 2017, 22, 1641.
[http://dx.doi.org/10.3390/molecules22101641]
[18]
Ritter, G. D.; Acuff, G. R.; Bergeron, G.; Bourassa, M. W.; Chapman, B. J.; Dickson, J. S.; Opengart, K.; Salois, M.J.; Singer, R.S.; Storrs, C. Antimicrobial-resistant bacterial infections from foods of animal origin: Understanding and effectively communicating to consumers. Ann. N. Y. Acad. Sci., 2019, 1441(1), 40-49.
[http://dx.doi.org/10.1111/nyas.14091] [PMID: 30924543]
[19]
Heredia, N.; García, S. Animals as sources of food-borne pathogens: A review. Anim Nutr, 2018, 4(3), 250-255.
[http://dx.doi.org/10.1016/j.aninu.2018.04.006] [PMID: 30175252]
[20]
Sarowska, J.; Futoma-Koloch, B.; Jama-Kmiecik, A.; Frej-Madrzak, M.; Ksiazczyk, M.; Bugla-Ploskonska, G.; Choroszy-Krol, I. I. Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: Recent reports. Gut Pathog., 2019, 11(1), 1-17.
[http://dx.doi.org/10.1186/s13099-019-0290-0] [PMID: 30675188]
[21]
Nyachuba, D.G. Foodborne illness: is it on the rise? Nutr. Rev., 2010, 68(5), 257-269.
[http://dx.doi.org/10.1111/j.1753-4887.2010.00286.x] [PMID: 20500787]
[22]
Moreno, L.Z.; Paixão, R.; de Gobbi, D.D.; Raimundo, D.C.; Porfida Ferreira, T.S.P.; Micke Moreno, M.A.; Hofer, E.; dos Reis, C.M.F.; Matté, G.R.; Matté, M.H. Phenotypic and genotypic characterization of atypical Listeria monocytogenes and Listeria innocua isolated from swine slaughterhouses and meat markets. BioMed Res. Int., 2014, 1-12.
[http://dx.doi.org/10.1155/2014/742032]
[23]
Zapata-Leyva, L. Estudios de drogosensibilidad y detección de genes de resistencia en Escherichia coli y Salmonella spp., aisladas de canales de bovino Master Thesis, 2015.
[24]
Estrada-García, T.; Perez-Martinez, I. Bernal- Reynaga, R.; Zaidi, M.B. Enteroaggregative coli: A pathogen bridging the North and South. Curr. Trop. Med. Rep., 2014, 1(2), 88-96.
[PMID: 24892007]
[25]
Coyle, M.B. Manual of Antimicrobial Susceptibility Testing. American Society for Microbiology, 2005. Available from: https://www.nu.edu.sd/docs/lecture/lab/Manual%20o
[26]
Ochoa, T.J.; Brown, E.L.; Guion, C.E.; Chen, J.Z.; McMahon, R.J.; Cleary, T.G. Effect of lactoferrin on enteroaggregative E. coli (EAEC). Biochem. Cell Biol., 2006, 84(3), 369-376.
[http://dx.doi.org/10.1139/o06-053] [PMID: 16936809]
[27]
Wakabayashi, H.; Yamauchi, K.; Kobayashi, T.; Yaeshima, T.; Iwatsuki, K.; Yoshie, H. Inhibitory effects of lactoferrin on growth and biofilm formation of Porphyromonas gingivalis and Prevotella intermedia. Antimicrob. Agents Chemother., 2009, 53(8), 3308-3316.
[http://dx.doi.org/10.1128/AAC.01688-08] [PMID: 19451301]
[28]
Ammons, M.C.B.; Ward, L.S.; Dowd, S.; James, G.A. Combined treatment of Pseudomonas aeruginosa biofilm with lactoferrin and xylitol inhibits the ability of bacteria to respond to damage resulting from lactoferrin iron chelation. Int. J. Antimicrob. Agents, 2011, 37(4), 316-323.
[http://dx.doi.org/10.1016/j.ijantimicag.2010.12.019] [PMID: 21377840]
[29]
Drago-Serrano, M.E. Actividades antibacterianas de la lactoferrina. Enf Inf Microbiol., 2006, 26(2), 58-63.
[30]
Min, S.; Harris, L. Krochta. Antimicrobial effects of lactoferrin, lysozyme, and the lactoperoxidase system and edible whey protein films incorporating the lactoperoxidase system against Salmonella enterica and Escherichia coli O157:H7. J. Food Sci., 2005, 70(7), 332-338.
[http://dx.doi.org/10.1111/j.1365-2621.2005.tb11476.x]
[31]
Gandhi, M.; Chikindas, M.L. Listeria: A foodborne pathogen that knows how to survive. Int. J. Food Microbiol., 2007, 113(1), 1-15.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2006.07.008] [PMID: 17010463]
[32]
Longhi, C.; Conte, M.P.; Penta, M.; Cossu, A.; Antonini, G.; Superti, F.; Seganti, L. Lactoferricin influences early events of Listeria monocytogenes infection in THP-1 human macrophages. J. Med. Microbiol., 2004, 53(Pt 2), 87-91.
[http://dx.doi.org/10.1099/jmm.0.05367-0] [PMID: 14729926]
[33]
Payne, K.D.; Davidson, P.M.; Oliver, S.P.; Christen, G.L. Influence of bovine lactoferrin on the growth of Listeria monocytogenes. J. Food Prot., 1990, 53(6), 468-472.
[http://dx.doi.org/10.4315/0362-028X-53.6.468] [PMID: 31018344]
[34]
Branen, J.K.; Davidson, P.M. Enhancement of nisin, lysozyme, and monolaurin antimicrobial activities by ethylenediaminetetraacetic acid and lactoferrin. Int. J. Food Microbiol., 2004, 90(1), 63-74.
[http://dx.doi.org/10.1016/S0168-1605(03)00172-7] [PMID: 14672831]
[35]
Walsh, C. Microbiology AS Antibiotics: actions, origins, resistance., 2003,
[http://dx.doi.org/10.1128/9781555817886]
[36]
Tadesse, D.A.; Zhao, S.; Tong, E.; Ayers, S.; Singh, A.; Bartholomew, M.J.; McDermott, P.F. Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002. Emerg. Infect. Dis., 2012, 18(5), 741-749.
[http://dx.doi.org/10.3201/eid1805.111153] [PMID: 22515968]
[37]
Van Der Kraan, M. I. A.; Van Marle, J.; Nazmi, K.; Groenink, J.; Van, T.; Hof, W.; Veerman, E.C.I.; Bolscher, J.G.; Nieuw Amerongen, A.V. Ultrastructural effects of antimicrobial peptides from bovine lactoferrin on the membranes of Candida albicans and Escherichia coli. Peptides, 2005, 26(9), 1537-1542.
[http://dx.doi.org/10.1016/j.peptides.2005.02.011] [PMID: 16112390]
[38]
Zimmermann, R.A.; Moellering, R.C.Jr., ; Weinberg, A.N. Mechanism of resistance to antibiotic synergism in enterococci. J. Bacteriol., 1971, 105(3), 873-879.
[http://dx.doi.org/10.1128/JB.105.3.873-879.1971] [PMID: 4994038]
[39]
Walsh, D.; Duffy, G.; Sheridan, J.J.; Blair, I.S.; McDowell, D.A. Antibiotic resistance among Listeria, including Listeria monocytogenes, in retail foods. J. Appl. Microbiol., 2001, 90(4), 517-522.
[http://dx.doi.org/10.1046/j.1365-2672.2001.01273.x] [PMID: 11309061]
[40]
Meletiadis, J.; Pournaras, S.; Roilides, E.; Walsh, T.J. Defining fractional inhibitory concentration index cutoffs for additive interactions based on self-drug additive combinations, Monte Carlo simulation analysis, and in vitro-in vivo correlation data for antifungal drug combinations against Aspergillus fumigatus. Antimicrob. Agents Chemother., 2010, 54(2), 602-609.
[http://dx.doi.org/10.1128/AAC.00999-09] [PMID: 19995928]

Rights & Permissions Print Cite
Article Metrics
13
5
© 2024 Bentham Science Publishers | Privacy Policy