Lactoferrin and lactoferrin chimera inhibit damage caused by enteropathogenic Escherichia coli in HEp-2 cells

Biochimie

Volumn 94, Issue 9, 2012, Pages 1935-1942

  Flores Villaseñor, Héctor ^a   Canizalez Román, Adrian ^a   De La Garza, Mireya ^b   Nazmi, Kamran ^c   Bolscher, Jan G M ^c   Leon Sicairos, Nidia ^a,d  

^a UNIVERSIDAD AUTÓNOMA DE SINALOA   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d Servicio de Hematología Y Oncología Hospital Pediátrico de Sinaloa Dr Rigoberto Aguilar Pico   (Mexico)

Author keywords

Adhesion; EPEC; Inhibition; Lactoferrin; LFchimera

Indexed keywords

LACTOFERRAMPIN; LACTOFERRICIN; LACTOFERRIN; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ARTICLE; CELL ADHESION; CHIMERA; DOSE RESPONSE; ENTEROPATHOGENIC ESCHERICHIA COLI; GENE EXPRESSION; HEMOLYSIS; HEP 2 CELL; HOST CELL; NONHUMAN;

ACTINS; ANIMALS; BACTERIAL ADHESION; CATTLE; CELL LINE; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEMOLYSIS; HUMANS; LACTOFERRIN; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT FUSION PROTEINS;

BOVINAE; ESCHERICHIA COLI;

EID: 84864283977     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.05.011     Document Type: Article

References (43)

1. P. Gerner-Smidt, C. Jensen, K.E. Olsen, F. Scheutz, K. Molbak, and B. Olesen Diarrheagenic potential of Escherichia coli in children in a developed country J. Clin. Microbiol. 41 2003 5836 5837 author reply (Pubitemid 37543303)
2. J.E. Vidal, A. Canizalez-Roman, J. Gutierrez-Jimenez, and F. Navarro-Garcia Molecular pathogenesis, epidemiology and diagnosis of enteropathogenic Escherichia coli Salud Publica Mex. 49 2007 376 386
3. A.E. Jerse, J. Yu, B.D. Tall, and J.B. Kaper A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells Proc. Natl. Acad. Sci. U S A 87 1990 7839 7843
4. J.P. Nataro, and J.B. Kaper Diarrheagenic Escherichia coli Clin. Microbiol. Rev. 11 1998 142 201 (Pubitemid 28046019)
5. M.S. Donnenberg, J.A. Giron, J.P. Nataro, and J.B. Kaper A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence Mol. Microbiol. 6 1992 3427 3437
6. T.K. McDaniel, K.G. Jarvis, M.S. Donnenberg, and J.B. Kaper A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens Proc. Natl. Acad. Sci. U S A 92 1995 1664 1668
7. G. Frankel, A.D. Phillips, I. Rosenshine, G. Dougan, J.B. Kaper, and S. Knutton Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements Mol. Microbiol. 30 1998 911 921 (Pubitemid 28550116)
8. S.J. Daniell, N. Takahashi, R. Wilson, D. Friedberg, I. Rosenshine, F.P. Booy, R.K. Shaw, S. Knutton, G. Frankel, and S. Aizawa The filamentous type III secretion translocon of enteropathogenic Escherichia coli Cell Microbiol. 3 2001 865 871 (Pubitemid 33133481)
9. S. Knutton, I. Rosenshine, M.J. Pallen, I. Nisan, B.C. Neves, C. Bain, C. Wolff, G. Dougan, and G. Frankel A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells EMBO J. 17 1998 2166 2176 (Pubitemid 28171902)
10. J.B. Kaper, T.K. McDaniel, K.G. Jarvis, and O. Gomez-Duarte Genetics of virulence of enteropathogenic E. coli Adv. Exp. Med. Biol. 412 1997 279 287 (Pubitemid 27263567)
11. J.B. Kaper, J.P. Nataro, and H.L. Mobley Pathogenic Escherichia coli Nat. Rev. Microbiol. 2 2004 123 140 (Pubitemid 39490066)
12. S. Farnaud, and R.W. Evans Lactoferrin: a multifunctional protein with antimicrobial properties Mol. Immunol. 40 2003 395 405 (Pubitemid 37244032)
13. S.Y. Arslan, K.P. Leung, and C.D. Wu The effect of lactoferrin on oral bacterial attachment Oral Microbiol. Immunol. 24 2009 411 416
14. T.J. Ochoa, M. Noguera-Obenza, and T.G. Cleary Lactoferrin blocks the initial host cell attachment mechanism of Enteropathogenic E. coli (EPEC) Adv. Exp. Med. Biol. 554 2004 463 466 (Pubitemid 39304560)
15. Y. Kawasaki, S. Tazume, K. Shimizu, H. Matsuzawa, S. Dosako, H. Isoda, M. Tsukiji, R. Fujimura, Y. Muranaka, and H. Isihida Inhibitory effects of bovine lactoferrin on the adherence of enterotoxigenic Escherichia coli to host cells Biosci. Biotechnol. Biochem. 64 2000 348 354
16. W. Fang, R.A. Almeida, and S.P. Oliver Effects of lactoferrin and milk on adherence of Streptococcus uberis to bovine mammary epithelial cells Am. J. Vet. Res. 61 2000 275 279
17. M. Ikeda, K. Sugiyama, T. Tanaka, K. Tanaka, H. Sekihara, K. Shimotohno, and N. Kato Lactoferrin markedly inhibits hepatitis C virus infection in cultured human hepatocytes Biochem. Biophys. Res. Commun. 245 1998 549 553 (Pubitemid 28418543)
18. K.R. Alugupalli, and S. Kalfas Inhibitory effect of lactoferrin on the adhesion of Actinobacillus actinomycetemcomitans and Prevotella intermedia to fibroblasts and epithelial cells APMIS 103 1995 154 160
19. K.R. Alugupalli, and S. Kalfas Characterization of the lactoferrin-dependent inhibition of the adhesion of Actinobacillus actinomycetemcomitans, Prevotella intermedia and Prevotella nigrescens to fibroblasts and to a reconstituted basement membrane Apmis 105 1997 680 688 (Pubitemid 27417887)
20. J.H. Brock The physiology of lactoferrin Biochem. Cell Biol. 80 2002 1 6 (Pubitemid 34194221)
21. H.F. Gomez, T.J. Ochoa, L.G. Carlin, and T.G. Cleary Human lactoferrin impairs virulence of Shigella flexneri J. Infect. Dis. 187 2003 87 95 (Pubitemid 36034475)
22. T.J. Ochoa, M. Noguera-Obenza, F. Ebel, C.A. Guzman, H.F. Gomez, and T.G. Cleary Lactoferrin impairs type III secretory system function in enteropathogenic Escherichia coli Infect. Immun. 71 2003 5149 5155 (Pubitemid 37070758)
23. W. Bellamy, M. Takase, H. Wakabayashi, K. Kawase, and M. Tomita Antibacterial spectrum of lactoferricin B, a potent bactericidal peptide derived from the N-terminal region of bovine lactoferrin J. Appl. Bacteriol. 73 1992 472 479
24. M.I. van der Kraan, J. Groenink, K. Nazmi, E.C. Veerman, J.G. Bolscher, and A.V. Nieuw Amerongen Lactoferrampin: a novel antimicrobial peptide in the N1-domain of bovine lactoferrin Peptides 25 2004 177 183 (Pubitemid 38520047)
25. E.F. Haney, F. Lau, and H.J. Vogel Solution structures and model membrane interactions of lactoferrampin, an antimicrobial peptide derived from bovine lactoferrin Biochim. Biophys. Acta 1768 2007 2355 2364 (Pubitemid 47532018)
26. J.G. Bolscher, R. Adao, K. Nazmi, P.A. van den Keybus, W. van 't Hof, A.V. Nieuw Amerongen, M. Bastos, and E.C. Veerman Bactericidal activity of LFchimera is stronger and less sensitive to ionic strength than its constituent lactoferricin and lactoferrampin peptides Biochimie 91 2009 123 132
27. N. Leon-Sicairos, A. Canizalez-Roman, M. de la Garza, M. Reyes-Lopez, J. Zazueta-Beltran, K. Nazmi, B. Gomez-Gil, and J.G. Bolscher Bactericidal effect of lactoferrin and lactoferrin chimera against halophilic Vibrio parahaemolyticus Biochimie 91 2009 133 140
28. H. Flores-Villasenor, A. Canizalez-Roman, M. Reyes-Lopez, K. Nazmi, M. de la Garza, J. Zazueta-Beltran, N. Leon-Sicairos, and J.G. Bolscher Bactericidal effect of bovine lactoferrin, LFcin, LFampin and LFchimera on antibiotic-resistant Staphylococcus aureus and Escherichia coli Biometals 23 2010 569 578
29. A. Cravioto, R.J. Gross, S.M. Scotland, and B. Rowe An adhesive factor found in strains of Escherichia belonging to the traditional infantile enteropathogenic serotype Curr. Microbiol. 3 1979 95 99 (Pubitemid 10125777)
30. K. Tanaka, Y. Takayanagi, N. Fujita, A. Ishihama, and H. Takahashi Heterogeneity of the principal sigma factor in Escherichia coli: the rpoS gene product, sigma 38, is a second principal sigma factor of RNA polymerase in stationary-phase Escherichia coli Proc. Natl. Acad. Sci. U S A 90 1993 8303 (Pubitemid 23260908)
31. T. Dong, and H.E. Schellhorn Control of RpoS in global gene expression of Escherichia coli in minimal media Mol. Genet. Genomics 281 2009 19 33
32. A.N. de Araujo, and L.G. Giugliano Lactoferrin and free secretory component of human milk inhibit the adhesion of enteropathogenic Escherichia coli to HeLa cells BMC Microbiol. 1 2001 25
33. A.M. Di Biase, A. Tinari, A. Pietrantoni, G. Antonini, P. Valenti, M.P. Conte, and F. Superti Effect of bovine lactoferricin on enteropathogenic Yersinia adhesion and invasion in HEp-2 cells J. Med. Microbiol. 53 2004 407 412 (Pubitemid 38586507)
34. P. Palmeira, S.B. Carbonare, M.L. Silva, L.R. Trabulsi, and M.M. Carneiro-Sampaio Inhibition of enteropathogenic Escherichia coli (EPEC) adherence to HEp-2 cells by bovine colostrum and milk Allergol. Immunopathol. (Madr) 29 2001 229 237 (Pubitemid 33636524)
35. K.B. McCann, A. Lee, J. Wan, H. Roginski, and M.J. Coventry The effect of bovine lactoferrin and lactoferricin B on the ability of feline calicivirus (a norovirus surrogate) and poliovirus to infect cell cultures J. Appl. Microbiol. 95 2003 1026 1033 (Pubitemid 37357385)
36. J.H. Andersen, H. Jenssen, K. Sandvik, and T.J. Gutteberg Anti-HSV activity of lactoferrin and lactoferricin is dependent on the presence of heparan sulphate at the cell surface J. Med. Virol. 74 2004 262 271 (Pubitemid 39150393)
37. H. Jenssen, K. Sandvik, J.H. Andersen, R.E. Hancock, and T.J. Gutteberg Inhibition of HSV cell-to-cell spread by lactoferrin and lactoferricin Antiviral. Res. 79 2008 192 198
38. R.A. Rashid, T.A. Tabata, M.J. Oatley, T.E. Besser, P.I. Tarr, and S.L. Moseley Expression of putative virulence factors of Escherichia coli O157:H7 differs in bovine and human infections Infect. Immun. 74 2006 4142 4148 (Pubitemid 43993347)
39. L. Huo, K. Zhang, J. Ling, Z. Peng, X. Huang, H. Liu, and L. Gu Antimicrobial and DNA-binding activities of the peptide fragments of human lactoferrin and histatin 5 against Streptococcus mutans Arch. Oral Biol. 2011
40. J. Warawa, B.B. Finlay, and B. Kenny Type III secretion-dependent hemolytic activity of enteropathogenic Escherichia coli Infect. Immun. 67 1999 5538 5540 (Pubitemid 29455342)
41. T. Ide, S. Laarmann, L. Greune, H. Schillers, H. Oberleithner, and M.A. Schmidt Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli Cell Microbiol. 3 2001 669 679 (Pubitemid 32976338)
42. R.K. Shaw, S. Daniell, F. Ebel, G. Frankel, and S. Knutton EspA filament-mediated protein translocation into red blood cells Cell Microbiol. 3 2001 213 222 (Pubitemid 32303355)
43. F. Lopez-Soto, N. Leon-Sicairos, K. Nazmi, J.G. Bolscher, and M. de la Garza Microbicidal effect of the lactoferrin peptides Lactoferricin17-30, Lactoferrampin265-284, and Lactoferrin chimera on the parasite Entamoeba histolytica Biometals 23 2010 563 668