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PMID: 8631722 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Binding and surface exposure characteristics of the gonococcal transferrin receptor are dependent on both transferrin-binding proteins.

Journal of bacteriology ·Vol. 178 ·No. 5 ·1996-03-00 ·Pages 1437-44

Cornelissen CN, Sparling PF

Abstract

Neisseria gonorrhoeae is capable of iron utilization from human transferrin in a receptor-mediated event. Transferrin-binding protein 1 (Tbp1) and Tbp2 have been implicated in transferrin receptor function, but their specific roles in transferrin binding and transferrin iron utilization have not yet been defined. We utilized specific gonococcal mutants lacking Tbp1 or Tbp2 to assess the relative transferrin-binding properties of each protein independently of the other. The apparent affinities of the wild-type transferrin receptor and of Tbp1 and Tbp2 individually were much higher than previously estimated for the gonococcal receptor and similar to the estimates for the mammalian transferrin receptor. The binding parameters of both of the mutants were distinct from those of the parent, which expressed two transferrin-binding sites. Tbp2 discriminated between ferrated transferrin and apotransferrin, while Tbp1 did not. Results of transferrin-binding affinity purification, and protease accessibility experiments were consistent with the hypothesis that Tbp1 and Tbp2 interact in the wild-type strain, although both proteins were capable of binding to transferrin independently when separated in the mutants. The presence of Tbp1 partially protected Tbp2 from trypsin proteolysis, and Tbp2 also protected Tbp1 from trypsin exposure. Addition of transferrin to wild-type but not mutant cells protected Tbp1 from trypsin but increased the trypsin susceptibility of Tbp2. These observations indicate that Tbp1 and Tbp2 function together in the wild-type strain to evoke binding conformations that are distinct from those expressed by the mutants lacking either protein.

MeSH Terms
Bacterial Proteins/genetics,metabolism Binding, Competitive Carrier Proteins/genetics,metabolism Chromatography, Affinity Cytidine Monophosphate N-Acetylneuraminic Acid/metabolism Iron-Binding Proteins Mutation Neisseria gonorrhoeae/metabolism Protein Binding Protein Conformation Receptors, Transferrin/genetics,metabolism Transferrin/metabolism Transferrin-Binding Proteins
Chemicals
Bacterial Proteins Carrier Proteins Iron-Binding Proteins Receptors, Transferrin Transferrin Transferrin-Binding Proteins Cytidine Monophosphate N-Acetylneuraminic Acid
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Cornelissen C N
Department of Medicine, School of Medicine, University of North Carolina at Chapel Hill, 27599, USA.
Sparling P F
References (54)
54 references, click to expand
  1. Expression of gonococcal transferrin-binding protein 1 causes Escherichia coli to bind human transferrin.
    J Bacteriol. 1993 Apr;175(8):2448-50 PMID: 8468302
  2. Identification of the transferrin- and lactoferrin-binding proteins in Haemophilus influenzae.
    J Med Microbiol. 1989 Jun;29(2):121-30 PMID: 2543820
  3. Conversion of the FhuA transport protein into a diffusion channel through the outer membrane of Escherichia coli.
    EMBO J. 1993 Aug;12(8):3007-16 PMID: 7688295
  4. Cloning and characterization of Neisseria meningitidis genes encoding the transferrin-binding proteins Tbp1 and Tbp2.
    Gene. 1993 Aug 16;130(1):73-80 PMID: 8344530
  5. Preparation and analysis of isogenic mutants in the transferrin receptor protein genes, tbpA and tbpB, from Neisseria meningitidis.
    Mol Microbiol. 1993 Jun;8(6):1125-33 PMID: 8361357
  6. Permeability properties of a large gated channel within the ferric enterobactin receptor, FepA.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10653-7 PMID: 7504275
  7. TonB protein and energy transduction between membranes.
    J Bioenerg Biomembr. 1993 Dec;25(6):591-601 PMID: 8144488
  8. Mechanisms of TonB-catalyzed iron transport through the enteric bacterial cell envelope.
    J Bioenerg Biomembr. 1993 Dec;25(6):603-11 PMID: 8144489
  9. Gonococcal transferrin-binding protein 2 facilitates but is not essential for transferrin utilization.
    J Bacteriol. 1994 Jun;176(11):3162-70 PMID: 8195069
  10. The ferric iron-binding protein of pathogenic Neisseria spp. functions as a periplasmic transport protein in iron acquisition from human transferrin.
    Mol Microbiol. 1993 Oct;10(2):311-8 PMID: 7934822
  11. Iron piracy: acquisition of transferrin-bound iron by bacterial pathogens.
    Mol Microbiol. 1994 Dec;14(5):843-50 PMID: 7715446
  12. NEISSERIA GONORRHOEAE. I. VIRULENCE GENETICALLY LINKED TO CLONAL VARIATION.
    J Bacteriol. 1963 Jun;85:1274-9 PMID: 14047217
  13. Gonococcal transferrin-binding protein 1 is required for transferrin utilization and is homologous to TonB-dependent outer membrane receptors.
    J Bacteriol. 1992 Sep;174(18):5788-97 PMID: 1325963
  14. A graphic method for the determination and presentation of binding parameters in a complex system.
    Anal Biochem. 1967 Sep;20(3):525-32 PMID: 6048188
  15. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  16. Proteins of human vaginal fluid.
    Fertil Steril. 1977 Dec;28(12):1345-8 PMID: 590545
  17. Iron and infection.
    Microbiol Rev. 1978 Mar;42(1):45-66 PMID: 379572
  18. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  19. Iron acquisition by Neisseria meningitidis in vitro.
    Infect Immun. 1980 Feb;27(2):322-34 PMID: 6445876
  20. Responses of Haemophilus pleuropneumoniae to iron restriction: changes in the outer membrane protein profile and the removal of iron from porcine transferrin.
    Mol Microbiol. 1989 Aug;3(8):1083-9 PMID: 2532702
  21. Utilization of transferrin-bound iron by Haemophilus species of human and porcine origins.
    FEMS Microbiol Lett. 1989 Nov;53(1-2):123-7 PMID: 2533128
  22. Molecular cloning and characterization of the structural gene for the major iron-regulated protein expressed by Neisseria gonorrhoeae.
    J Exp Med. 1990 May 1;171(5):1535-46 PMID: 2110241
  23. Siderophore-independent acquisition of transferrin-bound iron by Haemophilus influenzae type b.
    J Gen Microbiol. 1990 May;136(5):927-33 PMID: 2143216
  24. Genetic evidence that Neisseria gonorrhoeae produces specific receptors for transferrin and lactoferrin.
    J Bacteriol. 1990 Sep;172(9):5225-35 PMID: 2168377
  25. Identification and characterization of a porcine-specific transferrin receptor in Actinobacillus pleuropneumoniae.
    Mol Microbiol. 1990 Jul;4(7):1173-9 PMID: 2233254
  26. C reactive protein and immunoglobulin G in synovial fluid and serum in joint disease.
    Ann Rheum Dis. 1991 Jan;50(1):32-5 PMID: 1704698
  27. TonB and the gram-negative dilemma.
    Mol Microbiol. 1990 Dec;4(12):2019-25 PMID: 2150975
  28. Transport of iron across the outer membrane.
    Biol Met. 1991;4(1):14-22 PMID: 1854585
  29. Characterization of a soluble ferric reductase from Neisseria gonorrhoeae.
    Biol Met. 1991;4(2):126-31 PMID: 1908693
  30. Pseudomonas and neutrophil products modify transferrin and lactoferrin to create conditions that favor hydroxyl radical formation.
    J Clin Invest. 1991 Oct;88(4):1092-102 PMID: 1655825
  31. Cloning and expression of a transferrin-binding protein from Actinobacillus pleuropneumoniae.
    Infect Immun. 1992 Mar;60(3):892-8 PMID: 1541562
  32. Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from transferrin and iron compounds.
    Infect Immun. 1981 Aug;33(2):555-64 PMID: 6792081
  33. Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from lactoferrin.
    Infect Immun. 1982 Mar;35(3):915-20 PMID: 6121757
  34. Mechanism and regulation of synthesis of aerobactin in Escherichia coli K12 (pColV-K30).
    Can J Microbiol. 1992 Jul;38(7):728-33 PMID: 1393837
  35. Formation of a gated channel by a ligand-specific transport protein in the bacterial outer membrane.
    Science. 1992 Oct 16;258(5081):471-5 PMID: 1411544
  36. Antibodies to N-terminal peptides of gonococcal porin are bactericidal when gonococcal lipopolysaccharide is not sialylated.
    Mol Microbiol. 1992 Sep;6(18):2617-28 PMID: 1280317
  37. Iron assimilation and storage in prokaryotes.
    J Gen Microbiol. 1992 Dec;138(12):2475-83 PMID: 1487719
  38. Expression of a high-affinity mechanism for acquisition of transferrin iron by Neisseria meningitidis.
    Infect Immun. 1982 Apr;36(1):107-13 PMID: 6210635
  39. Amino terminus of outer membrane PhoE protein: localization by use of a bla-phoE hybrid gene.
    J Bacteriol. 1984 Jan;157(1):327-9 PMID: 6361002
  40. Ceruloplasmin and transferrin in human seminal plasma: are they an index of seminiferous tubular function?
    Fertil Steril. 1985 Feb;43(2):290-4 PMID: 3917951
  41. Response of Neisseria gonorrhoeae to iron limitation: alterations in expression of membrane proteins without apparent siderophore production.
    Infect Immun. 1985 Feb;47(2):388-94 PMID: 3155708
  42. Differential effects of iron on the growth of Listeria monocytogenes: minimum requirements and mechanism of acquisition.
    J Infect Dis. 1985 Apr;151(4):721-30 PMID: 3919119
  43. Haemophilus influenzae can use human transferrin as a sole source for required iron.
    Infect Immun. 1985 Apr;48(1):248-51 PMID: 3872264
  44. Bacterial periplasmic transport systems: structure, mechanism, and evolution.
    Annu Rev Biochem. 1986;55:397-425 PMID: 3527048
  45. Surface-exposed antigenic cleavage fragments of Neisseria gonorrhoeae proteins 1A and IB.
    Infect Immun. 1986 Dec;54(3):841-5 PMID: 3096894
  46. The structure, function, and regulation of transferrin receptors.
    Invest Radiol. 1987 Jan;22(1):74-83 PMID: 3546186
  47. Phenotypic variation in epitope expression of the Neisseria gonorrhoeae lipooligosaccharide.
    Infect Immun. 1987 Aug;55(8):1755-61 PMID: 2440807
  48. Aerobactin utilization by Neisseria gonorrhoeae and cloning of a genomic DNA fragment that complements Escherichia coli fhuB mutations.
    J Bacteriol. 1987 Aug;169(8):3414-21 PMID: 3112120
  49. Molecular mechanism of regulation of siderophore-mediated iron assimilation.
    Microbiol Rev. 1987 Dec;51(4):509-18 PMID: 2963952
  50. Iron uptake from lactoferrin and transferrin by Neisseria gonorrhoeae.
    Infect Immun. 1988 Apr;56(4):785-91 PMID: 3126143
  51. Identification and characterization of the transferrin receptor from Neisseria meningitidis.
    Mol Microbiol. 1988 Mar;2(2):281-8 PMID: 3132585
  52. Loss of transferrin receptor activity in Neisseria meningitidis correlates with inability to use transferrin as an iron source.
    Infect Immun. 1988 Dec;56(12):3132-8 PMID: 3141281
  53. Specificity of the lactoferrin and transferrin receptors in Neisseria gonorrhoeae.
    Mol Microbiol. 1988 Nov;2(6):827-9 PMID: 2850444
  54. Reduction of ferric iron by Listeria monocytogenes and other species of Listeria.
    Can J Microbiol. 1993 May;39(5):480-5 PMID: 8330259
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1996-03-00
Pages
1437-44
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC177819
Subset
IM
Grants
NIAID NIH HHS · AI26837 · United States
NIAID NIH HHS · AI31496 · United States
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