Effect of lactoferrin on enteric pathogens

Biochimie

Volumn 91, Issue 1, 2009, Pages 30-34

  Ochoa, Theresa J ^a,b   Cleary, Thomas G ^b  

^a UNIVERSIDAD PERUANA CAYETANO HEREDIA   (Peru)

^b UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Diarrhea; Enteric bacteria; Enteric parasites; Enteric viruses; Lactoferrin

Indexed keywords

LACTOFERRIN; LYSOZYME; VIRULENCE FACTOR;

CLINICAL TRIAL; DIARRHEA; DIET SUPPLEMENTATION; DRUG ACTIVITY; DRUG EFFECT; DRUG INHIBITION; ENTEROAGGREGATIVE ESCHERICHIA COLI; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ENTEROTOXIGENIC ESCHERICHIA COLI; GASTROENTERITIS; GASTROINTESTINAL INFECTION; HUMAN; ORAL REHYDRATION THERAPY; REVIEW; SALMONELLA; SHIGELLA;

DIARRHEA, INFANTILE; ENTEROBACTERIACEAE; ENTEROVIRUS; HUMANS; INFANT; INFANT, NEWBORN; INTESTINAL DISEASES, PARASITIC; LACTOFERRIN;

ANIMALIA; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GIARDIA; MAMMALIA; ROTAVIRUS; SALMONELLA; SHIGELLA;

EID: 58149121478     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2008.04.006     Document Type: Review

References (55)

1. Bryce J., Boschi-Pinto C., Shibuya K., and Black R.E. WHO Child Health Epidemiology Reference Group. WHO estimates of the causes of death in children. Lancet 365 (2005) 1147-1152
2. Lima A.A., Moore S.R., Barboza Jr. M.S., Soares A.M., Schleupner M.A., Newman R.D., Sears C.L., Nataro J.P., Fedorko D.P., Wuhib T., Schorling J.B., and Guerrant R.L. Persistent diarrhea signals a critical period of increased diarrhea burdens and nutritional shortfalls: a prospective cohort study among children in northeastern Brazil. J. Infect. Dis. 182 (2000) 1643-1651
3. Guerrant D.I., Moore S.R., Lima A.A., Patrick P.D., Schorling J.B., and Guerrant R.L. Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in northeast Brazil. Am. J. Trop. Med. Hyg. 61 (1999) 707-713
4. Berkman D.S., Lescano A.G., Gilman R.H., Lopez S.L., and Black M.M. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 359 (2002) 564-571
5. Jones G., Steketee R.W., Black R.E., Bhutta Z.A., and Morris S.S. Bellagio Child Survival Study Group. How many child deaths can we prevent this year?. Lancet 362 (2003) 65-71
6. Hamosh M. Bioactive factors in human milk. Pediatr. Clin. North Am. 48 (2001) 69-86
7. Lonnerdal B. Nutritional and physiologic significance of human milk proteins. Am. J. Clin. Nutr. 77 (2003) 537S-1543S
8. Brock J.H. The physiology of lactoferrin. Biochem. Cell Biol. 80 (2002) 1-6
9. Farnaud S., and Evans R.W. Lactoferrin-a multifunctional protein with antimicrobial properties. Mol. Immunol. 40 (2003) 395-405
10. Pierce A., Colavizza D., Benaissa M., Maes P., Tartar A., Montreuil J., and Spik G. Molecular cloning and sequence analysis of bovine lactotransferrin. Eur. J. Biochem. 196 (1991) 177-184
11. Steijns J.M., and van Hooijdonk A.C. Occurrence, structure, biochemical properties and technological characteristics of lactoferrin. Br. J. Nutr. 84 (2000) S11-S17
12. Superti F., Ammendolia M.G., Valenti P., and Seganti L. Antirotaviral activity of milk proteins: lactoferrin prevents rotavirus infection in the enterocyte-like cell line HT-29. Med. Microbiol. Immunol. (Berl.) 186 (1997) 83-91
13. Superti F., Siciliano R., Rega B., Giansanti F., Valenti P., and Antonini G. Involvement of bovine lactoferrin metal saturation, sialic acid and protein fragments in the inhibition of rotavirus infection. Biochim. Biophys. Acta. 1528 (2001) 107-115
14. Seganti L., DiBiase A.M., Marchetti M., Pietrantoni A., Tinari A., and Superti F. Biometals antiviral activity of lactoferrin towards naked viruses. Biometals 17 (2004) 295-299
15. Kvistgaard A.S., Pallesen L.T., Arias C.F., Lopez S., Peetersen T.E., Heegaard C.W., and Rqasmussen J.T. Inhibitory effects of human and bovine milk constituents on rotavirus infections. J. Dairy Sci. 87 (2004) 4088-4096
16. McCann K.B., Lee A., Wan J., Roginski H., and Coventry M.J. 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
17. Arnold R.R., Brewer M., and Gauthier J.J. Bactericidal activity of human lactoferrin: sensitivity of a variety of microorganisms. Infect. Immun. 28 (1980) 893-898
18. Di Biase A.M., Pietrantoni A., Tinari A., Sicianiano R., Valenti P., Antonini G., Seganti L., and Superti F. Heparin-interacting sites of bovine lactoferrin are involved in anti-adenovirus activity. J. Med. Virol. 69 (2003) 495-502
19. Pietrantoni A., Di Biase A.M., Tinari A., Marchetti M., Valenti P., Seganti L., and Superti F. Bovine lactoferrin inhibits adenovirus infection by interacting with viral structural polypeptides. Antimicrob. Agents Chemother. 47 (2003) 2688-2691
20. Turchany J.M., Aley S.B., and Gillin F.D. Giardicidal activity of lactoferrin and N-terminal peptides. Infect. Immun. 63 (1995) 4550-4552
21. Turchany J.M., McCaffery J.M., Aley S.B., and Gillin F.D. Ultrastructural effects of lactoferrin binding on Giardia lamblia trophozoites. J. Eukaryot. Microbiol. 44 (1997) 68-72
22. Leon-Sicairos N., Reyes-Lopez M., Canizalez-Roman A., Bermudez-Cruz R.M., Serrano-Luna J., Arroyo R., and de la Garza M. Human hololactoferrin: endocytosis and use as an iron source by the parasite Entamoeba histolytica. Microbiology 151 (2005) 3859-3871
23. Leon-Sicairos N., Lopez-Soto F., Reyes-Lopez M., Godinez-Vargas D., Ordaz-Pichardo C., and de la Garza M. Amoebicidal activity of milk, apo-lactoferrin, slgA and lysozyme. Clin. Med. Res. 4 (2006) 106-113
24. Appelmelk B.J., An Y.Q., Geerts M., Thijs B.G., de Boer H.A., MacLaren D.M., de Graaff J., and Nuijens J.H. Lactoferrin is a lipid A-binding protein. Infect. Immun. 62 (1994) 2628-2632
25. Brandenburg K., Jurgens G., Muller M., Fukuoka S., and Koch M.H. Biophysical characterization of lipopolysaccharide and lipid A inactivation by lactoferrin. Biol. Chem. 382 (2001) 1215-1225
26. Di Biase A.M., Tinari A., Pietrantoni A., Antonini G., Valenti P., Conte M.P., and Superti F. Effect of bovine lactoferricin on enteropathogenic Yersinia adhesion and invasion in HEp-2 cells. J. Med. Microbiol. 53 (2004) 407-412
27. Superti F., Pietrantoni A., Di Biase A.M., Longhi C., Valenti P., and Tinari A. Inv-mediated apoptosis of epithelial cells infected with enteropathogenic Yersinia: a protective effect of lactoferrin. Res. Microbiol. 156 (2005) 728-737
28. Tigyi Z., Kishore A.R., Maeland J.A., Forsgren A., and Naidu A.S. Lactoferrin-binding proteins in Shigella flexneri. Infect. Immun. 60 (1992) 2619-2626
29. Gomez H.F., Herrera-lnsua I., Siddiqui M.M., Diaz-Gonzalez V.A., Caceres E., Newburg D.S., and Cleary T.G. Protective role of human lactoferrin against invasion of Shigella flexneri M90T. Adv. Exp. Med. Biol. 501 (2001) 457-467
30. Gomez H.F., Ochoa T.J., Herrera-lnsua I., Cariin L.G., and Cleary T.G. Lactoferrin protects rabbits from Shigella flexneri-induced inflammatory enteritis. Infect. Immun. 70 (2002) 7050-7053
31. Gomez H.F., Ochoa T.J., Carilin L.G., and Cleary T.G. Human lactoferrin impairs virulence of Shigella flexneri. J. Infect. Dis. 187 (2003) 87-95
32. Naidu S.S., Svensson U., Kishore A.R., and Naidu A.S. Relationship between antibacterial activity and porin binding of lactoferrin in Escherichia coli and Salmonella typhimurium. Antimicrob. Agents Chemother 37 (1993) 240-245
33. Ochoa T.J., Nakamatsu C., Cabello M., Prada A., and Cleary T.G. Efecto de lactoferrina bovina en el crecimiento, adherencia e invasividad de Salmonella typhimurium. XVI Jornadas Científicas (September 2007), Universidad Peruana Cayetano Heredia, Lima, Peru Abstract
34. Bessler H.C., de Oliveira I.R., and Giugliano L.G. Human milk glycoproteins inhibit the adherence of Salmonella typhimurium to HeLa cells. Microbiol. Immunol. 50 (2006) 877-882
35. Naidu S.S., Erdei J., Czirok E., Kalfas S., Gado I., Thoren A., Forsgren A., and Naidu A.S. Specific binding of lactoferrin to Escherichia coli isolated from human intestinal infections. APMIS 99 (1991) 1142-1150
36. de Oliveira I.R., de Araujo A.N., Bao S.N., and Giugliano L.G. Binding of lactoferrin and free secretory component to enterotoxigenic Escherichia coli. FEMS Microbiol. Lett. 203 (2001) 29-33
37. Giugliano L.G., Ribeiro S.T., Vainstein M.H., and Ulhoa C.J. Free secretory component and lactoferrin of human milk inhibit the adhesion of enterotoxigenic Escherichia coli. J. Med. Microbiol. 42 (1995) 3-9
38. Kawasaki Y., Tazume S., Shimizu K., Matsuzawa H., Oosako S., Ssoda H., Tsukiji M., Fujimura R., Muranaka Y., and Isihida H. Inhibitory effects of bovine lactoferrin on the adherence of enterotoxigenic Escherichia coli to host cells. Biosci. Biotechnol. Biochem. 64 (2000) 348-354
39. de Araujo A.N., and Giugliano L.G. Lactoferrin and free secretory component of human milk inhibit the adhesion of enteropathogenic Escherichia coli in HeLa cells. BMC Microbiol. 1 (2001) 25
40. Ochoa T.J., Noguera-Obenza M., Ebel F., Guzman C.A., Gomez H.F., and Cleary T.G. Lactoferrin impairs type III secretory system function in enteropathogenic E. coli. Infect. Immun. 71 (2003) 5149-5155
41. Ochoa T.J., Noguera-Obenza M., and Cleary T.G. Lactoferrin blocks the initial host cell attachment mechanism of Enteropathogenic E. coli (EPEC). Adv. Exp. Med. Biol. 554 (2004) 463-466
42. Iizumi Y., Sagara H., Kabe Y., Azuma M., Kume K., Ogawa M., Nagai T., Gillespie P.G., Sasakawa C., and Handa H. The enteropathogenic E. coli effector EspB facilitates microvillus effacing and antiphagocytosis by inhibiting myosin function. Cell Host Microbe 2 (2007) 383-392
43. Ochoa T.J., and Cleary T.G. Lactoferrin disruption of bacterial type III secretion systems. BioMetals 17 (2004) 257-260
44. T.J. Ochoa, T.J. Cleary, The Effects of Lactoferrin on type III secretory system and toxin/phage induction virulence mechanisms in Shiga toxin producing E. coli. VII International Lactoferrin Conference. Hawaii, U.S.A. October 16-19, 2005.
45. de Araujo A., and Giugliano L.G. Human milk fractions inhibit the adherence of diffusely adherent Escherichia coli (DAEC) and enteroaggregative E. coli (EAEC) to HeLa cells. FEMS Microbiol. Lett. 184 (2000) 91-94
46. Ochoa T.J., Brown E.L., Guion C.E., Chen J.Z., McMahon R.J., and Cleary T.G. Effect of lactoferrin on Enteroaggregative E. coli (EAEC). Biochem. Cell Biol. 84 (2006) 369-376
47. Schulz-Lell G., Dorner K., Oldigs H.D., Sievers E., and Schaub J. Iron availability from an infant formula supplemented with bovine lactoferrin. Acta Paediatr. Scand 80 (1991) 155-158
48. Chierici R., Sawatzki G., Tamisari L., Volpato S., and Vigi V. Supplementation of an adapted formula with bovine lactoferrin. 2. Effects on serum iron, ferritin and zinc levels. Acta Paediatr. 81 (1992) 475-479
49. Lonnerdal B., and Hemell O. Iron, zinc, copper and selenium status of breast-fed infants and infants fed trace element fortified milk-based infant formula. Acta Paediatr. 83 (1994) 367-373
50. Hernell O., and Lonnerdal B. Iron status of infants fed low-iron formula: no effect of added bovine lactoferrin or nucleotides. Am. J. Clin. Nutr. 76 (2002) 858-864
51. Egashira M., Takayanagi T., Moriuchi M., and Moriuchi H. Does daily intake of bovine lactoferrin-containing products ameliorate rotaviral gastroenteritis?. Acta Paediatr. 96 (2007) 1242-1244
52. King Jr. J.C., Cummings G.E., Guo N., Trivedi L., Readmond B.X., Keane V., Feigelman S., and de Waard R. A double-blind, placebo-controlled, pilot study of bovine lactoferrin supplementation in bottle-fed infants. J. Pediatr. Gastroenterol. Nutr. 44 (2007) 245-251
53. Zavaleta N., Figueroa D., Rivera J., Sanchez J., Alfaro S., and Lonnerdal B. Efficacy of rice-based oral rehydration solution containing recombinant human lactoferrin and lysozyme in Peruvian children with acute diarrhea. J. Pediatr. Gastroenterol. Nutr. 44 (2007) 258-264
54. Ochoa, T.J., Chea-Woo, E., Campos, M., Pecho, I., Prada, A., McMahon, R.J., Cleary, T.G. Impact of lactoferrin supplementation on Giardia burden and growth in children. Clin. Infect. Dis. (2008) In press, June 15.
55. Omata Y., Satake M., Maeda R., Saito A., Shimazaki K., Yamauchi K., Uzuka Y., Tanabe S., Sarashina T., and Mikami T. Reduction of the infectivity of Toxoplasma gondii and Eimeria stiedai sporozoites by treatment with bovine lactoferricin. J. Vet. Med. Sci. 63 (2001) 187-190