Human milk lactoferrin is a serine protease that cleaves Haemophilus surface proteins at arginine-rich sites

Molecular Microbiology

Volumn 47, Issue 3, 2003, Pages 607-617

  Hendrixson, D R ^a   Qiu, J ^b   Shewry, S C ^c   Fink, D L ^a   Petty, S ^a   Baker, E N ^c   Plaut, A G ^b,c   St Geme III, J W ^a,d  

^a ST LOUIS CHILDREN S HOSPITAL   (United States)

^b TUFTS MEDICAL CENTER   (United States)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ARGININE; IMMUNOGLOBULIN A1; LACTOFERRIN; MEMBRANE PROTEIN; POLYPEPTIDE; SERINE PROTEINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HAEMOPHILUS INFLUENZAE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FAMILY; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ARGININE; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; CELL LINE; HAEMOPHILUS INFLUENZAE; HUMANS; LACTOFERRIN; MILK, HUMAN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SERINE ENDOPEPTIDASES;

BACTERIA (MICROORGANISMS); HAEMOPHILUS; HAEMOPHILUS INFLUENZAE; NEGIBACTERIA;

EID: 0037241594     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03327.x     Document Type: Article

References (48)

1. Aniansson, G., Alm, B., Andersson, B., Hakansson, A., Larsson, P., Nylen, O., et al. (1994) A prospective cohort study on breast-feeding and otitis media in Sweden. Pediatr Infect Dis J 13: 183-188.
2. Arnold, C., Makintube, S., and Istre, G.R. (1993) Day care attendance and other risk factors for invasive Haemophilus influenzae type b disease. Am J Epidemiol 138: 333-340.
3. Bellamy, W., Takase, M., Yamauchi, K., Wakabayashi, H., Kawase, K., and Tomita, M. (1992) Identification of the bactericidal domain of lactoferrin. Biochim Biophys Acta 1121: 130-136.
4. Carter, P., and Wells, J. (1988) Dissecting the catalytic triad of a serine protease. Nature 332: 564-568.
5. Cochi, S.L., Fleming, D.W., Hightower, A.W., Limpakarnjanarat, K., Facklam, R.R., Smith, J.D., et al. (1986) Primary invasive Haemophilus influenzae type b disease: a population-based assessment of risk factors. J Pediatr 108: 887-896.
6. Corey, D.R., and Craik, C.S. (1992) An investigation into the minimum requirements for peptide hydrolysis by mutation of the catalytic triad of trypsin. J Am Chem Soc 114: 1784-1790.
7. Craik, C.S., Roczniak, S., Largman, C., and Rutter, W.J. (1987) The catalytic role of the active site aspartic acid in serine proteases. Science 237: 909-913.
8. Cunningham, A.S. (1977) Morbidity in breast-fed and artificially fed infants. J Pediatr 90: 726-729.
9. Day, C.L., Stowell, K.M., Baker, E.N., and Tweedie, J.W. (1992) Studies of the N-terminal half of human lactoferrin produced from the cloned cDNA demonstrate that interlobe interactions modulate iron release. J Biol Chem 267: 13857-13862.
10. Duncan, B., Ey, J., Holberg, C.J., Wright, A.L., Martinez, F.D., and Taussig, L.M. (1993) Exclusive breast-feeding for at least 4 months protects against otitis media. Pediatrics 91: 867-872.
11. Fleishmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., et al. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512.
12. Gensberg, K., Jan, S., and Matthews, G.M. (1998) Subtilisin-related serine proteases in the mammalian constitutive secretory pathway. Sem Cell Devel Biol 9: 11-17.
13. Grundy, F.J., Plaut, A., and Wright, A. (1987) Haemophilus influenzae immunoglobulin A1 protease genes: cloning by plasmid integration-excision, comparative analysis, and localization of secretion determinants. J Bacteriol 169: 4442-4450.
14. Grundy, F.J., Plaut, A.G., and Wright, A. (1990) Localization of the cleavage site specificity determinant of Haemophilus influenzae immunoglobulin A1 protease genes. Infect Immun 58: 320-331.
15. He, J., and Furmanski, P. (1995) Sequence specificity and transcriptional activation in the binding of lactoferrin to DNA. Nature 373: 721-724.
16. Henderson, I.R., Navarro-Garcia, F., and Nataro, J.P. (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6: 370-377.
17. Hendrixson, D.R., and St. Geme, J.W., III (1998) The Haemophilus influenzae Hap serine protease promotes adherence and microcolony formation, potentiated by a soluble host protein. Mol Cell 2: 841-850.
18. Hendrixson, D.R., de la Morena, M.L., Stathopoulos, C., and St. Geme, J.W., III (1997) Structural determinants of processing and secretion of the Haemophilus influenzae Hap protein. Mol Microbiol 26: 505-518.
19. Jose, J., Jahnig, F., and Meyer, T.F. (1995) Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol Microbiol 18: 378-380.
20. Julius, D., Brake, A., Blair, L., Kunisawa, R., and Thorner, J. (1984) Isolation of the putative structural gene for the lysine-arginine-cleaving endopeptidase required for processing of the yeast prepro-alpha-factor. Cell 37: 1075-1089.
21. Kaleida, P.H., Nativio, D.G., Chao, H.P., and Cowden, S.N. (1993) Prevalence of bacterial respiratory pathogens in the nasopharynx in breast-fed versus formula-fed infants. J Clin Microbiol 31: 2674-2678.
22. Klauser, T., Pohlner, J., and Meyer, T.F. (1993) The secretion pathway of IgA protease-type proteins in gram negative bacteria. Bioessays 15: 799-805.
23. Krysan, D.J., Rockwell, N.C., and Fuller, R.S. (1999) Quantitative characterization of furin specificity. J Biol Chem 274: 23229-23234.
24. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage. Nature 227: 680-685.
25. Levay, P.F., and Viljoen, M. (1995) Lactoferrin: a general review. Haematologica 80: 252-267.
26. Lomholt, H. (1996) Molecular biology and vaccine aspects of bacterial immunoglobulin A1 proteases. APMIS 104 (Suppl. 62): 5-28.
27. Murphy, T.F., Bernstein, J.M., Dryja, D.M., Campagnari, A.A., and Apicella, M.A. (1987) Outer membrane protein and lipooligosaccharide analysis of paired nasopharyngeal and middle ear isolates in otitis media due to nontypeable Haemophilus influenzae: pathogenic and epidemiologic observations. J Infect Dis 5: 723-731.
28. Nicholson, H., Anderson, B.F., Bland, T., Shewry, S.C., Tweedie, J.W., and Baker, E.N. (1997) Mutagenesis of the histidine ligand in human lactoferrin: iron binding properties and crystal structure of the histidine-253 methionine mutant. Biochemistry 36: 341-346.
29. van den Ouweland, A.M., van Duinhoven, H.L., Keizer, G.D., Dorssers, L.C., and van de Ven, W.J. (1990) Structural homology between the human fur gene product and the subtilisin-like portease encoded by yeast KEX2. Nucleic Acids Res 18: 664.
30. Paetzel, M., and Dalbey, R.E. (1997) Catalytic hydroxyl/amine dyads with serine proteases. Trends Biochem Sci 22: 28-31.
31. Paetzel, M., and Strynadka, N.C.J. (1999) Common protein architecture and binding sites in proteases utilizing a Ser/Lys dyad mechanism. Protein Sci 8: 2533-2536.
32. Palmiter, R.D., Behringer, R.R., Quaife, C.J., Maxwell, F., Maxwell, I.H., and Brinster, R.L. (1987) Cell lineage ablation in transgenic mice by cell-specific expression of a toxin gene. Cell 50: 435-443.
33. Plaut, A.G., Qiu, J., Grundy, F., and Wright, A. (1992) Growth of Haemophilus influenzae. human milk: synthesis, distribution, and activity of IgA protease as determined by study of iga+ and mutant iga- cells. J Infect Dis 166: 43-52.
34. Qiu, J., Hendrixson, D.R., Baker, E.N., Murphy, T.F., St. Geme, J.W., III, and Plaut, A.G. (1998) Human milk lactoferrin inactivates two putative colonization factors expressed by Haemophilus influenzae. Proc Natl Acad Sci USA 95: 12641-12646.
35. Rawlings, N.D., and Barretts, A.J. (1994) Families of serine proteases. Methods Enzymol 244: 19-61.
36. Saarinen, U.M. (1982) Prolonged breast feeding as prophylaxis for recurrent otitis media. Acta Pediatr Scand 71: 567-571.
37. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
38. Setlow, J.K., Brown, D.C., Boling, M.E., Mattingly, A., and Gordon, M.P. (1968) Repair of deoxyribonucleic acid in Haemophilus influenzae. I. X-ray sensitivity of ultraviolet-sensitive mutants and their behavior as hosts to ultraviolet-irradiated bacteriophage and transforming deoxyribonucleic acid. J Bacteriol 95: 546-558.
39. St. Geme, J.W., III, and Falkow, S. (1990) Haemophilus influenzae adheres to and enters cultured human epithelial cells. Infect Immun 58: 4036-4044.
40. St. Geme, J.W., III, Falkow, S., and Barenkamp, S.J. (1993) High-molecular-weight proteins of nontypable Haemophilus influenzae mediate attachment to human epithelial cells. Proc Natl Acad Sci USA 90: 2875-2879.
41. St. Geme, J.W., III, de al Morena, M.L., and Falkow, S. (1994) A Haemophilus influenzae IgA protease-like protein promotes intimate interaction with human epithelial cells. Mol Microbiol 14: 217-233.
42. Steineke-Grober, A., Vey, M., Angliker, H., Shaw, E., Thomas, G., Roberts, C., Klenk, H.D., and Garten, W. (1992) Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J 11: 2407-2714.
43. Takala, A.K., Eskola, J., Palmgren, J., Ronnberg, P.-R., Kela, E., Rekola, P., and Makela, P.H. (1989) Risk factors of invasive Haemophilus influenzae type b disease among children in Finland. J Pediatr 115: 694-701.
44. Teele, D.W., Klein, J.O., Rosner, B., and the Greater Boston Otitis Media Study Group. (1989) Epidemiology of otitis media during the first seven years of life in children in greater Boston: a prospective cohort study. J Infect Dis 160: 83-94.
45. Tomb, J.-F., Barcak, G.J., Chandler, M.S., Redfield, R.J., and Smith, H.O. (1989) Transposon mutagenesis, characterization, and cloning of transformation genes of Haemophilus influenzae Rd. J Bacteriol 171: 3796-3802.
46. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354.
47. Turk, D.C. (1984) The pathogenicity of Haemophilus influenzae. J Med Microbiol 18: 1-16.
48. Vorland, L.H. (1999) Lactoferrin: a multifunctional glycoprotein. APMIS 107: 971-981.