Human lactoferrin impairs virulence of Shigella flexneri

Journal of Infectious Diseases

Volumn 187, Issue 1, 2003, Pages 87-95

  Gomez, Henry F ^a   Ochoa, Theresa J ^a   Carlin, Lily G ^a   Cleary, Thomas G ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LACTOFERRIN; LIPID A; PROTEIN; PROTEIN IPAB; PROTEIN IPAC; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIOSTASIS; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SHIGELLA FLEXNERI;

ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; HELA CELLS; HUMANS; LACTOFERRIN; LIPID A; PLASMIDS; PROTEASE INHIBITORS; SHIGELLA FLEXNERI; VIRULENCE;

EID: 0037222127     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/345875     Document Type: Article

References (79)

1. Guerrero L, Calva JJ, Morrow AL, et al. Asymptomatic Shigella infections in a cohort of Mexican children younger than two years of age. Pediatr Infect Dis J 1994; 13:597-602.
2. Ahmed F, Clemens ID, Rao MR, Sack DA, Khan MR, Haque E. Community based evaluation of the effect of breast feeding on the risk of microbiologically confirmed or clinically presumptive shigellosis in Bangladeshi children. Pediatrics 1992; 90:406-11.
3. Clemens JD, Stanton B, Stoll B, Shahid NS, Banu H, Chowdhury AKM. Breast feeding as a determinant of severity in shigellosis: Evidence for protection throughout the first three years of life in Bangladeshi children. Am J Epidemiol 1986; 123:710-20.
4. Hayani KC, Guerrero ML, Morrow AL, et al. Concentration of milk secretory immunoglobulin A against Shigella virulence plasmid-associated antigens as a predictor of symptom status in Shigella-infected breast-fed infants. J Pediatr 1992; 121:852-6.
5. Stoll BJ, Glass RI, Huq MI, Khan MU, Banu H, Holt J. Epidemiologic and clinical features of patients infected with Shigella who attended a diarrheal disease hospital in Bangladesh. J Infect Dis 1982; 146:177-83.
6. Brines RD, Brock JH. The effect of trypsin and chymotrypsin on the in vitro antimicrobial and iron-binding properties of lactoferrin in human milk and bovine colostrum: Unusual resistance of human apolactoferrin to proteolytic digestion. Biochim Biophys Acta 1983; 759: 229-35.
7. Arnold RR, Cole MF, McGhee IR. A bactericidal effect for human lactoferrin. Science 1977; 197:263-5.
8. Arnold RR, Brewer M, Gauthier JJ. Bactericidal activity of human lactoferrin: Sensitivity of a variety of microorganisms. Infect Immun 1980; 28:893-8.
9. Brock JH, Pickering MG, McDowall MC, Deacon AG. Role of antibody and enterobactin in controlling growth of Escherichia coli in human milk and acquisition of lactoferrin- and transferrin-bound iron by Escherichia coli. Infect Immun 1983;40:453-9.
10. Dolby JM, Honour P. Bacteriostasis of Escherichia coli by milk. IV. The bacteriostatic antibody of human milk. J Hyg (London) 1979; 83: 255-65.
11. Reiter B, Brock JH, Steel ED. Inhibition of Escherichia coli by bovine colostrum and post-colostral milk. II. The bacteriostatic effect of lactoferrin on a serum susceptible and serum resistant strain of E. coli. Immunology, 1975; 28:83-95.
12. Samson RR, Mirtle C, McClelland DB. Secretory IgA does not enhance the bacteriostatic effects of iron-binding or vitamin B12-binding proteins in human colostrum. Immunology 1979; 38:367-73.
13. Samson RR, Mirtle C, McClelland DB. The effect of digestive enzymes on the binding and bacteriostatic properties of lactoferrin and vitamin B12 binder in human milk. Acta Paediatr Scand 1980;69:517-23.
14. Stuart J, Norrell S, Harrington JP. Kinetic effect of human lactoferrin on the growth of Escherichia coli O111. Int J Biochem 1984; 16:1043-7.
15. Visca P, Dalmastri C, Verzili D, Antonini G, Chiancone E, Valenti P. Interaction of lactoferrin with Escherichia coli cells and correlation with antibacterial activity. Med Microbiol Immunol 1990; 179:323-33.
16. Yamauchi K, Tomita M, Giehl TJ, Ellison RT 3rd. Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect Immun 1993; 61:719-28.
17. Dolby JM, Stephens S. Antibodies to Escherichia coli O antigens and the in-vitro bacteriostatic properties of human milk and its IgA. Acta Paediatr Scand 1983; 72:577-82.
18. Rainard P. Activation of the classical pathway of complement by binding of bovine lactoferrin to unencapsulated Streptococcus agalactiae. Immunology 1993; 79:648-52.
19. Ellison RT 3rd, Giehl TJ. Killing of gram-negative bacteria by lactoferrin and lysozyme. J Clin Invest 1991; 88:1080-91.
20. Tigyi Z, Kishore AR, Maeland JA, Forsgren A, Naidu AS. Lactoferrin-binding proteins in Shigella flexneri. Infect Immun 1992; 60:2619-26.
21. High N, Mounier J, Prevost MC, Sansonetti PJ. IpaB of Shigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole. EMBO J 1992; 11:1991-9.
22. Menard R, Sansonetti PJ, Parsot C. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 1993; 175:5899-06.
23. Oaks EV, Hale TL, Formal SB. Serum immune response to Shigella protein antigens in rhesus monkeys and humans infected with Shigella spp. Infect Immun 1986;53:57-63.
24. Gomez HF, Herrera-Insua I, Siddiqui MM, et al. Protective role of human lactoferrin against invasion of Shigella flexneri M90T. Adv Exp Med Biol 2001;501:457-67.
25. Ward PP, Piddington CS, Cunningham GA, Zhou X, Wyatt RD, Conneely OM. A system for production of commercial quantities of human lactoferrin: A broad spectrum natural antibiotic. Biotechnology 1995; 13:498-503.
26. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Biotechnology 1992; 24:145-9.
27. Mills JA, Buysse JM, Oaks EV. Shigella flexneri invasion plasmid antigens B and C: Epitope location and characterization with monoclonal antibodies. Infect Immun 1988; 56:2933-41.
28. Turbyfill KR, Mertz JA, Mallett CP, Oaks EV. Identification of epitope and surface-exposed domains of Shigella flexneri invasion plasmid antigen D (IpaD). Infect Immun 1998;66:1999-2006.
29. Menard R, Sansonetti PJ, Parsot C. The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD. EMBO J 1994; 13:5293-302.
30. Menard R, Prevost MC, Gounon P, Sansonetti PJ, Dehio C. The secreted Ipa complex of Shigella flexneri promotes entry into mammalian cells. Proc Natl Acad Sci USA 1996;93:1254-8.
31. Menard R, Sansonetti PJ, Parsot C, Vasselon T. Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of S. flexneri. Cell 1994; 79:515-25.
32. Bahrani FK, Sansonetti PJ, Parsot C. Secretion of Ipa proteins by Shigella flexneri: Inducer molecules and kinetics of activation. Infect Immun 1997; 65:4005-10.
33. Adler B, Sasakawa C, Tobe T, Makino S, Komatsu K, Yoshikawa M. A dual transcriptional activation system for the 230 kb plasmid genes coding for virulence-associated antigens of Shigella flexneri. Mol Microbiol 1989; 3:627-35.
34. Chosa H, Makino S, Sasakawa C, et al. Loss of virulence in Shigella strains preserved in culture collections due to molecular alteration of the invasion plasmid. Microb Pathog 1989;6:337-42.
35. Andrews GP, Hromockyj AE, Coker C, Maurelli AT. Two novel virulence loci, mxiA and mxiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigens. Infect Immun 1991; 59:1997-2005.
36. Parsot C, Menard R, Gounon P, Sansonetti PJ. Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol Microbiol 1995; 16:291-300.
37. Venkatesan MM, Buysse JM, Oaks EV. Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus. J Bacteriol 1992; 174:1990-2001.
38. Li A, Zhao CR, Ekwall E, Lindberg AA. Serum IgG antibody responses to Shigella invasion plasmid-coded antigens detected by immunoblot. Scand J Infect Dis 1994;26:435-45.
39. Oaks EV, Picking WD, Picking WL. Antibody response of monkeys to invasion plasmid antigen D after infection with Shigella spp. Clin Diagn Lab Immunol 1996; 3:242-5.
40. Phalipon A, Arondel J, Nato F, Rouyre S, Mazie JC, Sansonetti PJ. Identification and characterization of B-cell epitopes of IpaC, an invasion-associated protein of Shigella flexneri. Infect Immun 1992;60: 1919-26.
41. Watarai M, Tobe T, Yoshikawa M, Sasakawa C. Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness. EMBO J 1995; 14:2461-70.
42. Clerc PL, Sansonetti PJ. Evidence for clathrin mobilization during directed phagocytosis of Shigella flexneri by HEp2 cells. Microb Pathog 1989; 7:329-36.
43. Tran Van Nhieu G, Ben-Ze'ev A, Sansonetti PJ. Modulation of bacterial entry into epithelial cells by association between vinculin and the Shigella IpaA invasin. EMBO J 1997; 16:2717-2729.
44. Goldberg MB, Barzu O, Parsot C, Sansonetti PJ. Unipolar localization and ATPase activity, of IcsA, a Shigella flexneri protein involved in intracellular movement. J Bacteriol 1993; 175:2189-96.
45. Goldberg MB, Theriot JA, Sansonetti PJ. Regulation of surface presentation of IcsA, a Shigella protein essential to intracellular movement and spread, is growth phase dependent. Infect Immun 1994; 62:5664-8.
46. Sansonetti PJ, Mounier J, Prevost MC, Mege RM. Cadherin expression is required for the spread of Shigella flexneri between epithelial cells. Cell 1994; 76:829-39.
47. Suzuki T, Saga S, Sasakawa C. Functional analysis of Shigella VirG domains essential for interaction with vinculin and actin-based motility. J Biol Chem 1996; 271:21878-85.
48. Sansonetti PJ, Arondel J, Fontaine A, d'Hauteville H, Bernardini ML. OmpB (osmo-regulation) and icsA (cell to cell spread) mutants of Shigella flexneri: Vaccine candidates and probes to study the pathogenesis of shigellosis. Vaccine 1991; 9:416-22.
49. Ito K, Nakajima T, Sasaki T, Watanabe H. Localization of IpaB protein in Escherichia coli K-12 MC 1061 strain carrying Shigella sonnei form I plasmid pSS120. Microbiol Immunol 1991;35:335-41.
50. Barzu S, Benjelloun-Touimi Z, Phalipon A, Sansonetti PJ, Parsot C. Functional analysis of the Shigella flexneri IpaC invasin by insertional mutagenesis. Infect Immun 1997; 65:1599-605.
51. Blocker A, Gounon P, Larquet E, et al. The tripartite type III secretion of S. flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 1999; 147:683-93.
52. Headley VL, Payne SM. Differential protein expression by Shigella flexneri in intracellular and extracellular environments. Proc Natl Acad Sci USA 1990; 87:4179-83.
53. Erdei J, Forsgren A, Naidu AS. Lactoferrin binds to porins OmpF and OmpC in Escherichia coli. Infect Immun 1994; 62:1236-40.
54. Naidu SS, Svensson U, Kishore AR, Naidu AS. Relationship between antibacterial activity, and porin binding of lactoferrin in Escherichia coli and Salmonella typhimurium. Antimicrob Agents Chemother 1993; 37: 240-5.
55. Dalmastri C, Valenti P, Visca P, Vittorioso P, Orsi N. Enhanced anti-microbial activity of lactoferrin by binding to the bacterial surface. Microbiologica 1988; 11:225-30.
56. Ellison RT 3rd, Giehl TJ, LaForce FM. Damage of the outer membrane of enteric gram-negative bacteria by lactoferrin and transferrin. Infect Immun 1988; 56:2774-81.
57. Ellison RT 3rd, Giehl TJ, LaForce FM. Damage of the outer membrane of enteric gram-negative bacteria by lactoferrin and transferrin. Infect Immun 1988; 56:2774-81.
58. Elass-Rochard E, Roseanu A, Legrand D, et al. Lactoferrin-lipopolysaccharide interaction: Involvement of the 28-34 loop region of human lactoferrin in the high-affinity binding to Escherichia coli O55B5 lipopolysaccharide. Biochem J 1995; 312:839-45.
59. Bellamy W, Takase M, Yamauchi K, Wakabayashi H, Kawase K, Tomita M. Identification of the bactericidal domain of lactoferrin. Biochim Biophys Acta 1992; 1121:130-6.
60. Odell EW, Sarra R, Foxworthy M, Chapple DS, Evans RW. Antibacterial activity of peptides homologous to a loop region in human lactoferrin. FEBS Lett 1996;382:175-8.
61. Chapple DS, Mason DJ, Joannou CL, Odell EW, Gant V, Evans RW. Structure function relationship of antibacterial synthetic peptides homologous to a helical surface region on human lactoferrin against E. coli serotype O111. Infect Immun 1998; 66:2434-40.
62. Brandenburg K, Jurgens G, Muller M, Fukuoaka S, Koch MHJ. Biophysical characterization of lipopolysaccharide and lipid A inactivation by lactoferrin. Biol Chem 2001; 382:1215-25.
63. van Berkel PH, Geerts ME, van Veen HA, Mericskay M, de Boer HA, Nuijens JH. N-terminal stretch Arg2, Arg4 and Arg5 of human lactoferrin is essential for binding to heparin, bacterial lipopolysaccharide, human lysozyme and DNA. Biochem J 1997; 328:145-51.
64. Zhang G, Mann DM, Tsai C. Neutralization of endotoxin in vitro and in vivo by a human lactoferrin derived peptide. Infect Immun 1999; 67:1353-8.
65. Mounier J, Bahrani FK, Sansonetti PJ. Secretion of Shigella flexneri Ipa invasins on contact with epithelial cells and subsequent entry of the bacterium into cells are growth stage dependent. Infect Immun 1997; 65:774-82.
66. Altschul SF, Madden TL, Schaffer AA, et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acid Res 1997; 25:3389-402.
67. Steinhauer J, Agha R, Pham T, Varga AW, Goldberg MB. The unipolar Shigella surface protein IcsA is targeted directly to the bacterial old pole: IcsP cleavage of IcsA occurs over the entire bacterial surface. Mol Microbiol 1999; 32:367-77.
68. Robbins JR, Monack D, McCallum SJ, et al. The making of a gradient: IcsA (VirG) polarity in Shigella flexneri. Mol Microbiol 2001; 41:861-72.
69. Plaut AG, Qiu J, St Geme JW 3rd. Human lactoferrin proteolytic activity: Analysis of the cleaved region in the IgA protease of Haemophilus influenzae. Vaccine 2000; 19(Suppl 1):S148-52.
70. Qui J, Hendrixson DR, Baker EN, Murphy TF, St Geme JW 3rd, Plaut AG. Human milk lactoferrin inactivates two putative colonization factors expressed by Haemophilus influenzae. Proc Natl Acad Sci USA 1998; 95:12641-6.
71. Hsia RC, Small PL, Bavoil PM. Characterization of virulence genes of enteroinvasive Escherichia coli by TnphoA mutagenesis: Identification of invX, a gene required for entry into HEp-2 cells. J Bacteriol 1993;175: 4817-23.
72. Rosqvist R, Hakansson S, Forsberg A, Wolf-Watz H. Functional conservation of the secretion and translocation machinery for virulence proteins of yersiniae, salmonellae and shigellae. EMBO J 1995; 14: 4187-95.
73. Hueck CJ, Hantman MJ, Bajaj V, Johnston C, Lee CA, Miller SI. Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins. Mol Microbiol 1995; 18:479-90.
74. Kaniga K, Tucker S, Trollinger D, Galan JE. Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J Bacteriol 1995; 177:3965-71.
75. Kaniga K, Trollinger D, Galan JE. Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. J Bacteriol 1995; 177:7078-85.
76. Hermant D, Menard R, Arricau N, Parsot C, Popoff MY. Functional conservation of the Salmonella and Shigella effectors of entry into epithelial cells. Mol Microblol 1995; 17:781-9.
77. Allaoui A, Sansonetti PJ, Parsot C. MxiJ, a lipoprotein involved in secretion of Shigella Ipa invasins, is homologous to YscJ, a secretion factor of the Yersinia Yop proteins. J Bacteriol 1992; 174:7661-9.
78. Andrews GP, Maurelli AT. mxiA of Shigella flexneri 2a, which facilitates export of invasion plasmid antigens, encodes a homolog of the low-calcium-response protein, LcrD, of Yersinia pestis. Infect Immun 1992; 60:3287-95.
79. Jarvis KG, Giron JA, Jerse AE, McDaniel TK, Donnenberg MS, Kaper JB. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc Natl Acad Sci USA 1995;92: 7996-8000.