Structure of a Complex of Human Lactoferrin N-lobe with Pneumococcal Surface Protein A Provides Insight into Microbial Defense Mechanism

Journal of Molecular Biology

Volumn 370, Issue 4, 2007, Pages 701-713

  Senkovich, Olga ^a   Cook, William J ^b   Mirza, Shaper ^c   Hollingshead, Susan K ^c   Protasevich, Irina I ^a   Briles, David E ^c   Chattopadhyay, Debasish ^a,d  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

host pathogen interaction; immunity; lactoferricin; lactoferrin

Indexed keywords

BACTERIAL PROTEIN; LACTOFERRIN; MEMBRANE PROTEIN; PNEUMOCOCCAL SURFACE PROTEIN A; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; CRYSTAL STRUCTURE; HOST PATHOGEN INTERACTION; HOST RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PNEUMONIAE; STRUCTURE ANALYSIS; SURFACE CHARGE;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STREPTOCOCCUS PNEUMONIAE;

EID: 34249929901     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.04.075     Document Type: Article

References (60)

1. Valenti P., and Antonini G. Lactoferrin: an important host defence against microbial and viral attack. Cell. Mol. Life Sci. 62 (2005) 2576-2587
2. Farnaud S., and Evans R.W. Lactoferrin - a multifunctional protein with antimicrobial properties. Mol. Immunol. 40 (2003) 395-405
3. 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
4. Ward P.P., Paz E., and Conneely O.M. Multifunctional roles of lactoferrin: a critical overview. Cell. Mol. Life Sci. 62 (2005) 2540-2548
5. Ling J.M.L., and Schryvers A.B. Perspectives on interactions between lactoferrin and bacteria. Biochem. Cell. Biol. 84 (2006) 275-281
6. Yu R.H., and Schryvers A.B. Bacterial lactoferrin receptors: insights from characterizing the Moraxella bovis receptors. Biochem. Cell. Biol. 80 (2002) 81-90
7. Hammerschmidt S., Bethe G., Remane P.H., and Chhatwal G.S. Identification of pneumococcal surface protein A as a lactoferrin-binding protein of Streptococcus pneumoniae. Infect. Immun. 67 (1999) 1683-1687
8. Hakansson A., Roche H., Mirza S., McDaniel L.S., Brooks-Walter A., and Briles D.E. Characterization of the binding of human lactoferrin to pneumococcal surface protein A (PspA). Infect. Immun. 69 (2001) 3372-3381
9. Crain M.J., Waltman II W.D., Turner J.S., Yother J., Talkington D.F., McDaniel L.S., et al. Pneumococcal surface protein A (PspA) is serologically highly variable and is expressed by all clinically important capsular serotypes of Streptococcus pneumoniae. Infect. Immun. 58 (1990) 3293-3299
10. Shaper M., Hollingshead S.K., Benjamin Jr. W.H., and Briles D.E. PspA protects Streptococcus pneumoniae from killing by apolactoferrin, and antibody to PspA enhances killing of pneumococci by apolactoferrin. Infect. Immun. 72 (2004) 5031-5040
11. Baker E.N., and Baker H.M. Molecular structure, binding properties and dynamics of lactoferrin. Cell. Mol. Life Sci. 62 (2005) 2531-2539
12. Bullen J.J., Rogers H.J., and Leigh L. Iron-binding proteins in milk and resistance to Escherichia coli infection in infants. Brit. Med. J. 1 (1972) 69-75
13. Rainard P. Bacteriostatic activity of bovine milk lactoferrin against mastitic bacteria. Vet. Microbiol. 11 (1986) 387-392
14. Levay P.F., and Viljoen M. Lactoferrin: a general review. Haematologica 80 (1995) 252-267
15. Arnold R.R., Russel J.E., Champion W.J., Brewer M., and Gauthier J.J. Bactericidal activity of human lactoferrin: differentiation from the status of iron deprivation. Infect. Immun. 35 (1982) 792-799
16. Ellison III R.T., Giehl T.J., and LaForce F.M. Damage of outer membrane of enteric gram-negative bacteria by lactoferrin and transferrin. Infect. Immun. 56 (1988) 2774-2781
17. Bellamy W., Takase M., Yamauchi H., Wakabayashi H., Kawase K., and Tomita M. Identification of the bactericidal domain of lactoferrin. Biochim. Biophys. Acta 1121 (1992) 130-136
18. Kuwata H., Yip T., Tomita M., and Hutchens T.W. Direct evidence of the generation in human stomach of an antimicrobial peptide domain (lactoferricin) from ingested lactoferrin. Biochim. Biophys. Acta 1429 (1998) 129-141
19. Britigan B.E., Hayek M.B., Doebbeling B.N., and Fick Jr. R.B. Transferrin and lactoferrin undergo proteolytic cleavage in the Pseudomonas aeruginosa-infected lungs of patients with cystic fibrosis. Infect. Immun. 61 (1993) 5049-5055
20. Farnaud S., Spiller C., Moriarty L.C., Patel A., Gant V., Odell E.W., and Evans R.W. Interactions of lactoferricin-derived peptides with LPS and antimicrobial activity. FEMS Microbiol. Letters 233 (2004) 193-199
21. Geerts M.E.J., van Heen H.A., Mericskay M., de Boer H.A., and Nuijens J.H. N-terminal stretch Arg2, Arg3, Arg4 and Arg5 of human lactoferrin is essential for binding to heparin, bacterial lipopolysaccharide, human lysozyme and DNA. Biochem. J. 328 (1997) 145-151
22. Gifford J.L., Hunter H.N., and Vogel H.J. Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell. Mol. Life Sci. 62 (2005) 2588-2598
23. Wakabayashi H., Takase M., and Tomita M. Lactoferricin derived from milk protein lactoferrin. Curr. Pharm. Des. 9 (2003) 1277-1287
24. Yother J., and White J.M. Novel surface attachment mechanism of the Streptococcus pneumoniae protein PspA. J. Bacteriol. 176 (1994) 2976-2985
25. Yother J., and Briles D.E. Structural properties and evolutionary relationships of PspA, a surface protein of Streptococcus pneumoniae, as revealed by sequence analysis. J. Bacteriol. 174 (1992) 601-609
26. Jedrzejas M.J. Unveiling molecular mechanism of pneumococcal surface protein A interactions with antibodies and lactoferrin. Clin. Chim. Acta 367 (2006) 1-10
27. Day C.L., Anderson B.F., Tweedie J.W., and Baker E.N. Structure of the recombinant N-terminal lobe of human lactoferrin at 2.0 Å resolution. J. Mol. Biol. 232 (1993) 1084-1100
28. Baker H.M., Baker C.J., Smith C.A., and Baker E.N. Metal substitution in transferrins: specific binding of cerium (IV) revealed by the crystal structure of cerium-substituted human lactoferrin. J. Biol. Inorg. Chem. 5 (2000) 692-698
29. Sun X.L., Baker H.M., Shewry S.C., Jameson G.B., and Baker E.N. Structure of recombinant human lactoferrin expressed in Aspergillus awamori. Acta Crystallog. sect. D 55 (1999) 403-407
30. Thomassen E.A.J., Van Veen H.A., Van Berkel P.H.C., Nuijens J.H., and Abrahams J.P. The protein structure of recombinant human lactoferrin produced in the milk of transgenic cows closely matches the structure of human milk-derived lactoferrin. Transgen. Res. 14 (2005) 397-405
31. Peterson N., Arcus V., Anderson B., Tweedie J., Jameson G., and Baker E. "Dilysine trigger" in transferrins probed by mutagenesis of lactoferrin: crystal structures of the R210G, R210E, and R210L mutants of human lactoferrin. Biochemistry 41 (2002) 14167-14175
32. Holm L., and Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233 (1993) 123-138
33. Murzin A.G., Brenner S.E., Hubbard T., and Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247 (1995) 536-540
34. Vegarud G.E., Langsrud T., and Svenning C. Mineral-binding milk proteins and peptides; occurrence, biochemical and technological characteristics. Brit. J. Nutr. 84 (2000) S91-S98
35. Jabeen T., Sharma S., Singh N., Bhushan A., and Singh T.P. Structure of the zinc-saturated C-terminal lobe of bovine lactoferrin at 2.0 Å resolution. Acta Crystallog. sect. D 61 (2005) 1107-1115
36. Anderson B.F., Norris G.E., Rumball S.V., Thomas D.H., and Baker E.N. A comparison of the three-dimensional structures of human lactoferrin in its iron free and iron saturated forms. Adv. Exp. Med. Biol. 357 (1994) 227-230
37. Jameson G.B., Anderson B.F., Norris G.E., Thomas D.H., and Baker E.N. Structure of human apolactoferrin at 2.0 Å resolution. Refinement and analysis of ligand-induced conformational change. Acta Crystallog. sect. D 54 (1998) 1319-1335
38. Petrey D., and Honig B. GRASP2: visualization, surface properties, and electrostatics of macromolecular structure and sequences. Methods Enzymol. 374 (2003) 492-509
39. McDaniel L.S., Scott G., Kearney J.F., and Briles D.E. Monoclonal antibodies against protease-sensitive pneumococcal antigens can protect mice from fatal infection with Streptococcus pneumoniae. J. Exp. Med. 160 (1984) 386-397
40. Lopez R. Pneumococcus: the sugar-coated bacteria. Int. Microbiol. 9 (2006) 179-190
41. Schmidt-Ioanas M., and Lode H. Treatment of pneumonia in elderly patients. Expert Opin. Pharmacother. 7 (2006) 499-507
42. Jacobs M.R. Streptococcus pneumoniae: epidemiology and patterns of resistance. Am. J. Med. 117 Suppl. 3A (2004) 3S-15S
43. Bogaert D., Hermans P.W.M., Adrian P.V., Rumke H.C., and de Groot R. Pneumococcal vaccines: an update on current strategies. Vaccine 22 (2004) 2209-2220
44. Pelton S.I., Dagan R., Gaines B.M., Klugman K.P., Laufer D., O'Brien K., and Schmitt H.J. Pneumococcal conjugate vaccines: Proceedings from an interactive symposium at the 41st Interscience Conference on Antimicrobial Agents and Chemotherapy. Vaccine 21 (2003) 1562-1571
45. Ogunniyi A.D., Grabowicz M., Briles D.E., Cook J., and Paton J.C. Development of a vaccine against invasive pneumococcal disease based on combination of proteins of Streptococcus pneumoniae. Infec. Immun. 75 (2007) 350-357
46. Tai S.S. Streptococcus pneumoniae protein vaccine candidates: properties, activities and animal studies. Crit. Rev. Microbiol. 32 (2006) 139-153
47. Briles D.E., Hollingshead S.K., King J., Swift A., Braun P.A., Park M.K., et al. Immunization of humans with recombinant pneumococcal surface protein A (rPspA) elicits antibodies that passively protect mice from fatal infection with Streptococcus pneumoniae bearing heterologous PspA. J. Infect. Dis. 182 (2000) 1694-1701
48. Briles D.E., Tart R.C., Swiatlo E., Dillard J.P., Smith P., Benton K.A., et al. Pneumococcal diversity: considerations for new vaccine strategies with emphasis on pneumococcal surface protein A (PspA). Clin. Microbiol. Rev. 11 (1998) 645-657
49. Ren B., McCrory M.A., Pass C., Bullard D.C., Ballantyne C.M., Xu Y., et al. The virulence function of Streptococcus pneumoniae surface protein A involves inhibition of complement activation and impairment of complement receptor-mediated protection. J. Immunol. 173 (2004) 7506-7512
50. Hunter H.N., Demcoe A.R., Jenssen H., Gutteberg T.J., and Vogel H.J. Human lactoferricin is partially folded in aqueous solution and is better stabilized in a membrane mimetic solvent. Antimicrob. Agents Chemother. 49 (2005) 3387-3395
51. Yamauchi K., Tomita M., Giehl T.J., and Ellison III R.T. Antimicrobial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect. Immun. 61 (1993) 719-728
52. Berg T. Modulation of protein-protein interactions with small organic molecules. Angew. Chem. Int. Ed. Engl. 42 (2003) 2462-2481
53. Toogood P.L. Inhibition of protein-protein association by small molecules: approaches and progress. J. Med. Chem. 45 (2002) 1543-1558
54. Roche H., Hakansson A., Hollingshead S.K., and Briles D.E. Regions of PspA/EF3296 best able to elicit protection against Streptococcus pneumoniae in a murine infection model. Infect. Immiun. 71 (2003) 1033-1041
55. McDaniel L.S., Ralph B.A., McDaniel D.O., and Briles D.E. Localization of protection-eliciting epitopes on PspA of Streptococcus pneumoniae between amino acid residues 192 and 260. Microbial. Pathogenesis 17 (1994) 323-337
56. Wiseman T., Williston S., Brandts J.F., and Lin L.N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179 (1989) 131-137
57. Riboldi-Tunnicliffe A., and Hilgenfeld R. Cryocrystallography with oil - an old idea revived. J. Appl. Crystallog. 32 (1999) 1003-1005
58. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallog. sect. D 60 (2004) 2126-2132
59. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
60. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763