Analysis of Haptoglobin and Hemoglobin-Haptoglobin Interactions with the Neisseria meningitidis TonB-Dependent Receptor HpuAB by Flow Cytometry

Infection and Immunity

Volumn 72, Issue 5, 2004, Pages 2494-2506

  Rohde, Kyle H ^a,b   Dyer, David W ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b Animal Health Diagnostic Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HAPTOGLOBIN; HEMOGLOBIN; PROTEIN HPUAB; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BINDING AFFINITY; FLOW CYTOMETRY; HOST RESISTANCE; HUMAN; NEISSERIA MENINGITIDIS; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN POLYMORPHISM; PROTEIN PROTEIN INTERACTION;

APOPROTEINS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; FLOW CYTOMETRY; GENES, BACTERIAL; HAPTOGLOBINS; HEMOGLOBINS; HUMANS; IRON; KINETICS; LIGANDS; MEMBRANE PROTEINS; NEISSERIA MENINGITIDIS; PHENOTYPE; PROTEIN BINDING; PROTON-MOTIVE FORCE; RECEPTORS, CELL SURFACE;

EID: 2142761603     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.5.2494-2506.2004     Document Type: Article

References (88)

1. Bell, P. E., C. D. Nau, J. T. Brown, J. Konisky, and R. J. Kadner. 1990. Genetic suppression demonstrates interaction of TonB protein with outer membrane transport proteins in Escherichia coli. J. Bacteriol. 172:3826-3829.
2. Bradbeer, C. 1993. The proton motive force drives the outer membrane transport of cobalamin in Escherichia coli. J. Bacteriol. 175:3146-3150.
3. Bradbeer, C., and M. L. Woodrow. 1976. Transport of vitamin B12 in Escherichia coli: energy dependence. J. Bacteriol. 128:99-104.
4. Braun, V., S. Gaisser, C. Herrmann, K. Kampfenkel, H. Killmann, and I. Traub. 1996. Energy-coupled transport across the outer membrane of Escherichia coli: ExbB binds ExbD and TonB in vitro, and leucine 132 in the periplasmic region and aspartate 25 in the transmembrane region are important for ExbD activity. J. Bacteriol. 178:2836-2845.
5. Brener, D., I. W. De Voe, and B. E. Holbein. 1981. Increased virulence of Neisseria meningitidis after in vitro iron-limited growth at low pH. Infect. Immun. 33:59-66.
6. Buchanan, S. K., B. S. Smith, L Venkatramani, D. Xia, L. Esser, M. Palnitkar, R. Chakraborty, D. van der Helm, and J. Deisenhofer. 1999. Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat. Struct. Biol. 6:56-63.
7. Bünn, H. F. 1987. Subunit assembly of hemoglobin: an important determinant of hematologic phenotype. Blood 69:1-6.
8. Cadieux, N., C. Bradbeer, and R. J. Kadner. 2000. Sequence changes in the ton box region of BtuB affect its transport activities and interaction with TonB protein. J. Bacteriol. 182:5954-5961.
9. Centers for Disease Control and Prevention. 2000. Prevention and control of meningococcal disease. Recommendations of the Advisory Committee on Immunization Practices (ACIP). Morb. Mortal Wkly. Rep. 49:1-10.
10. Chang, C., A. Mooser, A. Pluckthun, and A. Wlodawer. 2001. Crystal structure of the dimeric C-terminal domain of TonB reveals a novel fold. J. Biol. Chem. 276:27535-27540.
11. Chen, C. J., C. Elkins, and P. F. Sparling. 1998. Phase variation of hemoglobin utilization in Neisseria gonorrhoeae. Infect. Immun. 66:987-993.
12. Chem C. J., D. McLean, C. E. Thomas, J. E. Anderson, and P. F. Sparling. 2002. Point mutations in HpuB enable gonococcal HpuA deletion mutants to grow on hemoglobin. J. Bacteriol. 184:420-426.
13. Chen, C. J., P. F. Sparling, L. A. Lewis, D. W. Dyer, and C. Elkins. 1996. Identification and purification of a hemoglobin-binding outer membrane protein from Neisseria gonorrhoeae. Infect. Immun. 64:5009-5014.
14. Cornelissen, C. N., J. E. Anderson, and P. F. Sparling. 1997. Energy-dependent changes in the gonococcal transferrin receptor. Mol. Microbiol. 26:25-35.
15. Cornelissen, C. N., and P. F. Sparling. 1996. Binding and surface exposure characteristics of the gonococcal transferrin receptor are dependent on both transferrin-binding proteins. J. Bacteriol. 178:1437-1444.
16. Dahlqvist, S. R., G. Beckman, and L. Beckman. 1988. Serum protein markers in systemic lupus erythematosus. Hum. Hered. 38:44-47.
17. Dahlqvist, S. R., and N. Frohlander. 1985. Haptoglobin groups and rheumatoid arthritis. Hum. Hered. 35:207-211.
18. Dobryszycka, W. 1997. Biological functions of haptoglobin-new pieces to an old puzzle. Eur. J. Clin. Chem. Clin. Biochem. 35:647-654.
19. Dobryszycka, W., and I. Bec-Katnik. 1975. Effect of modification on physicochemical and biological properties of haptoglobin. Acetylation, iodination and nitration. Acta Biochim. Pol. 22:143-153.
20. Dyer, D. W., E. P. West, and P. F. Sparling. 1987. Effects of serum carrier proteins on the growth of pathogenic neisseriae with heme-bound iron. Infect. Immun. 55:2171-2175.
21. Eaton, J. W., P. Brandt, J. R. Mahoney, and J. T. Lee, Jr. 1982. Haptoglobin: a natural bacteriostat. Science 215:691-693.
22. El Ghmati, S. M., E. M. Van Hoeyveld, J. G. Van Strip, J. L. Ceuppens, and E. A. Stevens. 1996. Identification of haptoglobin as an alternative ligand for CD11b/CD18. J. Immunol. 156:2542-2552.
23. Ferguson, A. D., V. Braun, H. P. Fiedler, J. W. Coulton, K. Diederichs, and W. Welte. 2000. Crystal structure of the antibiotic albomycin in complex with the outer membrane transporter FhuA. Protein Sci. 9:956-963.
24. Ferguson, A. D., R. Chakraborty, B. S. Smith, L. Esser, D. van der Hehn, and J. Deisenhofer. 2002. Structural basis of gating by the outer membrane transporter FecA. Science 295:1715-1719.
25. Ferguson, A. D., E. Hofmann, J. W. Coulton, K. Diederichs, and W. Welte. 1998. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215-2220.
26. Francis, R. T., Jr., J. W. Booth, and R. R. Becker. 1985. Uptake of iron from hemoglobin and the haptoglobin-hemoglobin complex by hemolytic bacteria. Int. J. Biochem. 17:767-773.
27. Gauduchon, V., S. Werner, G. Prevost, H. Mouteil, and D. A. Colin. 2001. Flow cytometric determination of Panton-Valentine leucocidin S component binding. Infect. Immun. 69:2390-2395.
28. Hamaguchi, H. 1969. Purification and some properties of the three common genetic types of haptoglobins and the hemoglobin-haptoglobin complexes. Am. J. Hum. Genet. 21:440-456.
29. Hancock, R. W., and V. Braun. 1976. Nature of the energy requirement for the irreversible adsorption of bacteriophages T1 and phi80 to Escherichia coli. J. Bacteriol. 125:409-415.
30. Hargrove, M. S., T. Whitaker, J. S. Olson, R. J. Vali, and A. J. Mathews. 1997. Quaternary structure regulates hemin dissociation from human hemoglobin. J. Biol. Chem. 272:17385-17389.
31. Haugland, R. P. 2002. Handbook of fluorescent probes and research products, 9th ed. Molecular Probes, Inc., Eugene, Orag.
32. Heller, K. J., R. J. Kadner, and K. Gunther. 1988. Suppression of the btuB451 mutation by mutations in the tonB gene suggests a direct interaction between TonB and TonB-dependent receptor proteins in the outer membrane of Escherichia coli. Gene 64:147-153.
33. Hershko, C. 1975. The fate of circulating haemoglobin. Br. J. Haematol. 29:199-204.
34. Higgs, P. I., P. S. Myers, and K. Postle. 1998. Interactions in the TonB-dependent energy transduction complex: ExbB and ExbD form homomultimers. J. Bacteriol. 180:6031-6038.
35. Holbein, B. E. 1981. Enhancement of Neisseria meningitidis infection in mice by addition of iron bound to transferrin. Infect. Immun. 34:120-125.
36. Holbein, B. E. 1980. Iron-controlled infection with Neisseria meningitidis in mice. Infect. Immun. 29:886-891.
37. Holbein, B. E., K. W. Jericho, and G. C. Likes. 1979 Neisseria meningitidis infection in mice: influence of iron, variations in virulence among strains, and pathology. Infect. Immun. 24:545-551.
38. Jaskula, J. C., T. E. Letain, S. K. Roof, J. T. Skare, and K. Postle. 1994. Role of the TonB amino terminus in energy transduction between membranes. J. Bacteriol. 176:2326-2338.
39. Jin, H., Z. Ren, P. W. Whitby, D. J. Morton, and T. L. Stull. 1999. Characterization of hgpA, a gene encoding a haemoglobin/haemoglobin-haptoglobin-binding protein of Haemophilus influenzae. Microbiology 145:905-914.
40. Karlsson, M., K. Hannavy, and C. F. Higgins. 1993. A sequence-specific function for the N-teminal signal-like sequence of the TonB protein. Mol. Microbiol. 8:379-388.
41. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
42. Lammler, C., and H. Blobel. 1986. Binding of human haptoglobin to streptococci of serological group A. Zentbl. Bakteriol. Mikrobiol. Hyg. Ser. A 261:161-166.
43. Lammler, C., T. Guszezynski, and W. Dobryszycka. 1988. Further characterization of haptoglobin binding to streptococci of serological group A. Zentbl. Bakteriol. Mikrobiol. Hyg. Ser. A 269:454-459.
44. Langlois, M. R., and J. R. Delangbe 1996. Biological and clinical significance of haptoglobin polymorphism in humans. Clin. Chem. 42:1589-1600.
45. Larsen, R. A., D. Foster-Hartnett, M. A. McIntosh, and K. Postle. 1997. Regions of Escherichia coli TonB and FepA proteins essential for in vivo physical interactions. J. Bacteriol. 179:3213-3221.
46. Letain, T. E., and K. Postle. 1997. TonB protein appears to transduce energy by shuttling between the cytoplasmic membrane and the outer membrane in Escherichia coli. Mol. Microbiol. 24:271-283. (Erratum, 25:617, 1997.)
47. Lewis, L. A., and D. W. Dyer. 1995. Identification of an iron-regulated outer membrane protein of Neisseria meningitidis involved in the utilization of hemoglobin complexed to haptoglobin. J. Bacteriol. 177:1299-1306.
48. Lewis, L. A., M. Gipson, K. Hartman, T. Ownbey, J. Vaughn, and D. W. Dyer. 1999. Phase variation of HpuAB and HmbR, two distinct haemoglobin receptors of Neisseria meningitidis DNM2. Mol. Microbiol. 32:977-989.
49. Lewis, L. A., E. Gray, Y. P. Wang, B. A. Roe, and D. W. Dyer. 1997. Molecular characterization of hpuAB, the haemoglobin-haptoglobin-utilization operon of Neisseria meningitidis. Mol. Microbiol. 23:737-749.
50. Lewis, L. A., K. Rohde, M. Gipson, B. Behrens, E. Gray, S. I. Toth, B. A. Roe, and D. W. Dyer. 1998. Identification and molecular analysis of lbpBA, which encodes the two-component meningococcal lactoferrin receptor. Infect. Immun. 66:3017-3023.
51. Lewis, L. A., M. H. Sung, M. Gipson, K. Hartman, and D. W. Dyer. 1998. Transport of intact porphyrin by HpuAB, the hemoglobin-haptoglobin utilization system of Neisseria meningitidis. J. Bacteriol. 180:6043-6047.
52. Locher, K. P., B. Rees, R. Koebnik, A. Mitschler, L. Moulinier, J. P. Rosenbusch, and D. Moras. 1998. Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell. 95:771-779.
53. Maeda, N., F. Yang, D. R. Barnett, B. H. Bowman, and O. Smithies. 1984. Duplication within the haptoglobin Hp2 gene. Nature 309:131-135.
54. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1989. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
55. Mickelsen, P. A., E. Blackman, and P. F. Sparling. 1982. Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from lactoferrin. Infect. Immun. 35:915-920.
56. Mickelsen, P. A., and P. F. Sparling. 1981. Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from transferrin and iron compounds. Infect. Immun. 33:555-564.
57. Moore, P. S. 1992. Meningococcal meningitis in sub-Saharan Africa: a model for the epidemic process. Clin. Infect. Dis. 14:515-525.
58. Morton, D. J., P. W. Whitby, H. Jin, Z. Ren, and T. L. Stull. 1999. Effect of multiple mutations in the hemoglobin- and hemoglobin-haptoglobin-binding proteins, HgpA, HgpB, and HgpC, of Haemophilus influenzae type b. Infect. Immun. 67:2729-2739.
59. Muller-Eberhard, U., J. Javid, H. H. Liem, A. Hanstein, and M. Hanna. 1968. Plasma concentrations of hemopexin, haptoglobin and heme in patients with various hemolytic disease. Blood. 32:811-815.
60. Nagel, R. L., and Q. H. Gibson. 1971. The binding of hemoglobin to haptoglobin and its relation to subunit dissociation of hemoglobin. J. Biol. Chem. 246:69-73.
61. Nishina, Y., S. Miyoshi, A. Nagase, and S. Shinoda. 1992. Significant role of an exocellular protease in utilization of heme by Vibrio vulnificus. Infect. Immun. 60:2128-2132.
62. Otto, B. R., M. Sparrius, D. J. Wors, F. K. de Graaf, and D. M. MacLaren. 1994. Utilization of haem from the haptoglobin-haemoglobin complex by Bacteroides fragilis. Microb. Pathog. 17:137-147.
63. Parkhill, J., M. Achtman, K. D. James, S. D. Bentley, C. Churcher, S. R. Klee, G, Morelli, D. Basham, D. Brown, T. Chillingworth, R. M. Davies, P. Davis, K. Devlin, T. Feltwell, N. Hamlin, S. Holroyd, K. Jagels, S. Leather, S. Moule, K. Mungall, M. A. Quail, M. A. Rajandream, K. M. Rutherford, M. Simmonds, J. Skelton, S. Whitehead, B. G. Spratt, and B. G. Barrell. 2000. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404:502-506.
64. Ren, Z., H. Jin, D. J. Morton, and T. L. Stull. 1998. hgpB, a gene encoding a second Haemophilus influenzae hemoglobin- and hemoglobin-haptoglobin-binding protein. Infect. Immun. 66:4733-4741.
65. Ren, Z., H. Jin, P. W. Whitby, D. J. Morton, and T. L. Stull. 1999. Role of CCAA nucleotide repeats in regulation of hemoglobin and hemoglobin-haptoglobin binding protein genes of Haemophilus influenzae. J. Bacteriol. 181:5865-5870.
66. Riedo, F. X., B. D. Plikaytis, and C. V. Broome. 1995. Epidemiology and prevention of meningococcal disease. Pediatr. Infect. Dis. J. 14:643-657.
67. Riggs, A. F. 1998. Self-association, cooperativity and supercooperativity of oxygen binding by hemoglobins. J. Exp. Biol. 201:1073-1084.
68. Rohde, K. H., and D. W. Dyer. 2003. Mechanisms of iron acquisition by the human pathogens Neisseria meningitidis and Neisseria gonorrhoeae. Front. Biosci. 8:1186-1218.
69. Rohde, K. H., A. F. Gillaspy, M. D. Hatfield, L. A. Lewis, and D. W. Dyer. 2002. Interactions of haemeglobin with the Neisseria meningitidis receptor HpuAB: the role of TonB and an intact proton motive force. Mol. Microbiol. 43:335-354.
70. Schryvers, A. B., and G. C. Gonzalez. 1989. Comparison of the abilities of different protein sources of iron to enhance Neisseria meningitidis infection in mice. Infect. Immun. 57:2425-2429.
71. Schryvers, A. B., and L. J. Morris. 1988. Identification and characterization of the human lactoferrin-binding protein from Neisseria meningitidis. Infect. Immun. 56:1144-1149.
72. Schryvers, A. B., and L. J. Morris. 1988. Identification and characterization of the transferrin receptor from Neisseria meningitidis. Mol. Microbiol. 2:281-288.
73. Schryvers, A. B., and I. Stojiljkovic. 1999. Iron acquisition systems in the pathogenic Neisseria. Mol. Microbiol. 32:1117-1123.
74. Schuchat, A., K. Robinson, J. D. Wenger, L. H. Harrison, M. Farley, A. L. Reingold, L. Lefkowitz, B. A. Perkins, and the Active Surveillance Team. 1997. Bacterial meningitis in the United States in 1995. N. Engl. J. Med. 337:970-976.
75. Schwartz, B., P. S. Moore, and C. V. Broome. 1989. Global epidemiology of meningococcal disease. Clin. Microbiol. Rev. 2(Suppl):S118-S124.
76. Smith, M. J., and W. S. Beck. 1967. Peroxidase activity of hemoglobin and its subunits: effects thereupon of haptoglobin. Biochim. Biophys. Acta 147:324-333.
77. Smithies, O. 1955. Zone electrophoresis in starch gels: group variations in the serum proteins of normal human adults. Biochem. J. 61:629-641.
78. Stojiljkovic, I., V. Hwa, L. de Saint Martin, P. O'Gaora, X. Nassif, F. Heffron, and M. So. 1995. The Neisseria meningitidis haemoglobin receptor: its role in iron utilization and virulence. Mol. Microbiol. 15:531-541.
79. Stojiljkovic, I., J. Larson, V. Rwa, S. Anic, and M. So. 1996. HmbR outer membrane receptor of pathogenic Neisseria spp.: iron-regulated, hemoglobin-binding proteins with a high level of primary structure conservation. J. Bacteriol. 178:4670-4678.
80. Stojiljkovic, I., and N. Srinivasan. 1997. Neisseria meningitidis tonB, exbB, and exbD genes: Ton-dependent utilization of protein-bound iron in neisseriae. J. Bacteriol. 179:805-812.
81. Sun, Y. H., S. Bakshi, R. Chalmers, and C. M. Tang. 2000. Functional genomics of Neisseria meningitidis pathogenesis. Nat. Med. 6:1269-1273.
82. Tettelin, H., N. J. Saunders, J. Heidelberg, A. C. Jeffries, K. E. Nelson, J. A. Eisen, K. A. Ketchum, D. W. Hood, J. F. Peden, R. J. Dodson, W. C. Nelson, M. L. Gwinn, R. DeBoy, J. D. Peterson, E. K. Hickey, D. H. Haft, S. L. Salzberg, O. White, R. D. Fleischmann, B. A. Dougherty, T. Mason, A. Ciecko, D. S. Parksey, E. Blair, H. Cittone, E. B. Clark, M. D. Cotton, T. R. Utterback, H. Khouri, H. Qin, J. Vamathevan, J. Gill, V. Scarlato, V. Masignani, M. Pizza, G. Grandi, L. Sun, H. O. Smith, C. M. Fraser, E. R. Moxon, R. Rappuoli, and J. C. Venter. 2000. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287:1809-1815.
83. Tuckman, M., and M. S. Osburne. 1992. In vivo inhibition of TonB-dependent processes by a TonB box consensus pentapeptide. J. Bacteriol. 174:320-323.
84. Turner, P. C., C. E. Thomas, I. Stojiljkovic, C. Elkins, G. Kizel, D. A. Ala'Aldeen, and P. F. Sparling. 2001. Neisserial TonB-dependent outer-membrane proteins: detection, regulation and distribution of three putative candidates identified from the genome sequences. Microbiology 147:1277-1290.
85. Weinberg, E. D. 1975. Nutritional immunity. Host's attempt to withold iron from microbial invaders. JAMA 231:39-41.
86. Wejman, J. C., D. Hovsepian, J. S. Wall, J. F. Hainfeld, and J. Greer. 1994. Structure and assembly of haptoglobin polymers by electron microscopy. J. Mol. Biol. 174:343-368.
87. Wejman, J. C., D. Hovsepian, J. S. Wall, J. F. Hainfeld, and J. Greer. 1984. Structure of haptoglobin and the haptoglobin-hemoglobin complex by electron microscopy. J. Mol. Biol. 174:319-341.
88. Zakaria-Meehan, Z., G. Massad, L. M. Simpson, J. C. Travis, and J. D. Oliver. 1988. Ability of Vibrio vulnificus to obtain iron from hemoglobin-haptoglobin complexes. Infect. Immun. 56:275-277.