Transition metals at the host-pathogen interface: How Neisseria exploit human metalloproteins for acquiring iron and zinc

Essays in Biochemistry

Volumn 61, Issue 2, 2017, Pages 211-223

  Neumann, Wilma ^a   Hadley, Rose C ^a   Nolan, Elizabeth M ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CALGRANULIN; IRON; LACTOFERRIN; METALLOPROTEIN; TRANSFERRIN; ZINC;

HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; NEISSERIA;

BACTERIAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; IRON; LACTOFERRIN; LEUKOCYTE L1 ANTIGEN COMPLEX; METALLOPROTEINS; NEISSERIA; TRANSFERRIN; ZINC;

EID: 85019430407     PISSN: 00711365     EISSN: None     Source Type: Journal    
DOI: 10.1042/EBC20160084     Document Type: Review

References (106)

1. Waldron, K.J. and Robinson, N.J. (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nat. Rev. Microbiol. 7, 25-35
2. Weinberg, E.D. (1975) Nutritional immunity. Host's attempt to withold iron from microbial invaders. J. Am. Med. Assoc. 231, 39-41
3. Hood, M.I. and Skaar, E.P. (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10, 525-537
4. Becker, K.W. and Skaar, E.P. (2014) Metal limitation and toxicity at the interface between host and pathogen. FEMS Microbiol. Rev. 38, 1235-1249
5. Palmer, L.D. and Skaar, E.P. (2016) Transition metals and virulence in bacteria. Annu. Rev. Genet. 50, 67-91
6. Rohde, K.H. and Dyer, D.W. (2003) Mechanisms of iron acquisition by the human pathogens Neisseria meningitidis and Neisseria gonorrhoeae. Front. Biosci. 8, d1186-d1218
7. Stork, M., Grijpstra, J., Bos, M.P., Mañas Torres, C., Devos, N., Poolman, J.T. et al. (2013) Zinc piracy as a mechanism of Neisseria meningitidis for evasion of nutritional immunity. PLoS Pathog. 9, e1003733
8. Jean, S., Juneau, R.A., Criss, A.K. and Cornelissen, C.N. (2016) Neisseria gonorrhoeae evades calprotectin-mediated nutritional immunity and survives neutrophil extracellular traps by production of TdfH. Infect. Immun. 84, 2982-2994
9. Cassat, J.E. and Skaar, E.P. (2012) Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity. Semin. Immunopathol. 34, 215-235
10. Virji, M. (2009) Pathogenic Neisseriae: surface modulation, pathogenesis and infection control. Nat. Rev. Microbiol. 7, 274-286
11. Unemo, M. and Shafer, W.M. (2014) Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin. Microbiol. Rev. 27, 587-613
12. Zhu, W., Chen, C.-J., Thomas, C.E., Anderson, J.E., Jerse, A.E. and Sparling, P.F. (2011) Vaccines for gonorrhea: can we rise to the challenge? Front. Microbiol 2, 124
13. Cash, D.R., Noinaj, N., Buchanan, S.K. and Cornelissen, C.N. (2015) Beyond the crystal structure: insight into the function and vaccine potential of TbpA expressed by Neisseria gonorrhoeae. Infect. Immun. 83, 4438-4449
14. Schauer, K., Rodionov, D.A. and de Reuse, H. (2008) New substrates for TonB-dependent transport: do we only see the 'tip of the iceberg'? Trends Biochem. Sci. 33, 330-338
15. Noinaj, N., Guillier, M., Barnard, T.J. and Buchanan, S.K. (2010) TonB-dependent transporters: regulation, structure, and function. Annu. Rev. Microbiol. 64, 43-60
16. Buchanan, S.K., Smith, B.S., Venkatramani, L., Xia, D., Esser, L., Palnitkar, M. et al. (1999) Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat. Struct. Biol. 6, 56-63
17. Braun, V. (1995) Energy-coupled transport and signal transduction through the Gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol. Rev. 16, 295-307
18. Braun, V. and Endriss, F. (2007) Energy-coupled outer membrane transport proteins and regulatory proteins. Biometals 20, 219-231
19. Postle, K. and Larsen, R.A. (2007) TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20, 453-465
20. Celia, H., Noinaj, N., Zakharov, S.D., Bordignon, E., Botos, I., Santamaria, M. et al. (2016) Structural insight into the role of the Ton complex in energy transduction. Nature 538, 60-65
21. Krewulak, K.D. and Vogel, H.J. (2008) Structural biology of bacterial iron uptake. Biochim. Biophys. Acta 1778, 1781-1804
22. Cornelissen, C.N. and Hollander, A. (2011) TonB-dependent transporters expressed by Neisseria gonorrhoeae. Front. Microbiol. 2, 117
23. Mickelsen, P.A. and Sparling, P.F. (1981) Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from transferrin and iron compounds. Infect. Immun. 33, 555-564
24. Mickelsen, P.A., Blackman, E. and Sparling, P.F. (1982) Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from lactoferrin. Infect. Immun. 35, 915-920
25. Lee, B.C. (1992) Isolation of haemin-binding proteins of Neisseria gonorrhoeae. J. Med. Microbiol. 36, 121-127
26. Schryvers, A.B. and Stojiljkovic, I. (1999) Iron acquisition systems in the pathogenic Neisseria. Mol. Microbiol. 32, 1117-1123
27. Perkins-Balding, D., Ratliff-Griffin, M. and Stojiljkovic, I. (2004) Iron transport systems in Neisseria meningitidis. Microbiol. Mol. Biol. Rev. 68, 154-171
28. Caza, M. and Kronstad, J.W. (2013) Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front. Cell. Infect. Microbiol. 3, 80
29. Raymond, K.N., Dertz, E.A. and Kim, S.S. (2003) Enterobactin: an archetype for microbial iron transport. Proc. Natl. Acad. Sci. U.S.A. 100, 3584-3588
30. Dlouhy, A.C. and Outten, C.E. (2013) The iron metallome in eukaryotic organisms. Met. Ions Life Sci. 12, 241-278
31. Cassat, J.E. and Skaar, E.P. (2013) Iron in infection and immunity. Cell Host Microbe 13, 509-519
32. Drabkin, D.L. (1951) Metabolism of the hemin chromoproteins. Physiol. Rev. 31, 345-431
33. Cabantchik, Z.I. (2014) Labile iron in cells and body fluids: physiology, pathology, and pharmacology. Front. Pharmacol. 5, 45
34. Sánchez, L., Calvo, M. and Brock, J.H. (1992) Biological role of lactoferrin. Arch. Dis. Child. 67, 657-661
35. Flo, T.H., Smith, K.D., Sato, S., Rodriguez, D.J., Holmes, M.A., Strong, R.K. et al. (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432, 917-921
36. Nemeth, E. and Ganz, T. (2006) Regulation of iron metabolism by hepcidin. Annu. Rev. Nutr. 26, 323-342
37. Schryvers, A.B. and Gonzalez, G.C. (1989) Comparison of the abilities of different protein sources of iron to enhance Neisseria meningitidis infection in mice. Infect. Immun. 57, 2425-2429
38. Zarantonelli, M.-L., Szatanik, M., Giorgini, D., Hong, E., Huerre, M., Guillou, F. et al. (2007) Transgenic mice expressing human transferrin as a model for meningococcal infection. Infect. Immun. 75, 5609-5614
39. Cornelissen, C.N., Kelley, M., Hobbs, M.M., Anderson, J.E., Cannon, J.G., Cohen, M.S. et al. (1998) The transferrin receptor expressed by gonococcal strain FA1090 is required for the experimental infection of human male volunteers. Mol. Microbiol. 27, 611-616
40. Anderson, J.E., Hobbs, M.M., Biswas, G.D. and Sparling, P.F. (2003) Opposing selective forces for expression of the gonococcal lactoferrin receptor. Mol. Microbiol. 48, 1325-1337
41. Lin, L., Pantapalangkoor, P., Tan, B., Bruhn, K.W., Ho, T., Nielsen, T. et al. (2014) Transferrin iron starvation therapy for lethal bacterial and fungal infections. J. Infect. Dis. 210, 254-264
42. Klausner, R.D., Ashwell, G., van Renswoude, J., Harford, J.B. and Bridges, K.R. (1983) Binding of apotransferrin to K562 cells: explanation of the transferrin cycle. Proc. Natl. Acad. Sci. U.S.A. 80, 2263-2266
43. Wally, J. and Buchanan, S.K. (2007) A structural comparison of human serum transferrin and human lactoferrin. Biometals 20, 249-262
44. Lambert, L.A., Perri, H., Halbrooks, P.J. and Mason, A.B. (2005) Evolution of the transferrin family: conservation of residues associated with iron and anion binding. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 142, 129-141
45. Wally, J., Halbrooks, P.J., Vonrhein, C., Rould, M.A., Everse, S.J., Mason, A.B. et al. (2006) The crystal structure of iron-free human serum transferrin provides insight into inter-lobe communication and receptor binding. J. Biol. Chem. 281, 24934-24944
46. Aisen, P., Leibman, A. and Zweier, J. (1978) Stoichiometric and site characteristics of the binding of iron to human transferrin. J. Biol. Chem. 253, 1930-1937
47. MacGillivray, R.T.A., Moore, S.A., Chen, J., Anderson, B.F., Baker, H., Luo, Y. et al. (1998) Two high resolution structures of the recombinant N-lobe of human transferrin reveal a structural change implicated in iron release. Biochemistry 37, 7919-7928
48. Cornelissen, C.N., Biswas, G.D., Tsai, J., Paruchuri, D.K., Thompson, S.A. and Sparling, P.F. (1992) Gonococcal transferrin-binding protein 1 is required for transferrin utilization and is homologous to TonB-dependent outer membrane receptors. J. Bacteriol. 174, 5788-5797
49. Gray-Owen, S.D. and Schryvers, A.B. (1996) Bacterial transferrin and lactoferrin receptors. Trends Microbiol. 4, 185-191
50. Morgenthau, A., Pogoutse, A., Adamiak, P., Moraes, T.F. and Schryvers, A.B. (2013) Bacterial receptors for host transferrin and lactoferrin: molecular mechanisms and role in host-microbe interactions. Future Microbiol. 8, 1575-1585
51. Anderson, J.E., Sparling, P.F. and Cornelissen, C.N. (1994) Gonococcal transferrin-binding protein 2 facilitates but is not essential for transferrin utilization. J. Bacteriol. 176, 3162-3170
52. DeRocco, A.J., Yost-Daljev, M.K., Kenney, C.D. and Cornelissen, C.N. (2009) Kinetic analysis of ligand interaction with the gonococcal transferrin-iron acquisition system. Biometals 22, 439-451
53. Cornelissen, C.N. and Sparling, P.F. (1996) Binding and surface exposure characteristics of the gonococcal transferrin receptor are dependent on both transferrin-binding proteins. J. Bacteriol. 178, 1437-1444
54. Boulton, I.C., Gorringe, A.R., Allison, N., Robinson, A., Gorinsky, B., Joannou, C.L. et al. (1998) Transferrin-binding protein B isolated from Neisseria meningitidis discriminates between apo and diferric human transferrin. Biochem. J. 334, 269-273
55. Noinaj, N., Easley, N.C., Oke, M., Mizuno, N., Gumbart, J., Boura, E. et al. (2012) Structural basis for iron piracy by pathogenic Neisseria. Nature 483, 53-58
56. Calmettes, C., Alcantara, J., Yu, R.-H., Schryvers, A.B. and Moraes, T.F. (2012) The structural basis of transferrin sequestration by transferrin-binding protein B. Nat. Struct. Mol. Biol. 19, 358-360
57. Noinaj, N., Buchanan, S.K. and Cornelissen, C.N. (2012) The transferrin-iron import system from pathogenic Neisseria species. Mol. Microbiol. 86, 246-257
58. Siburt, C.J., Roulhac, P.L., Weaver, K.D., Noto, J.M., Mietzner, T.A., Cornelissen, C.N. et al. (2009) Hijacking transferrin bound iron: protein-receptor interactions involved in iron transport in N. gonorrhoeae. Metallomics 1, 249-255
59. Adhikari, P., Berish, S.A., Nowalk, A.J., Veraldi, K.L., Morse, S.A. and Mietzner, T.A. (1996) The fbpABC locus of Neisseria gonorrhoeae functions in the periplasm-to-cytosol transport of iron. J. Bacteriol. 178, 2145-2149
60. Parker Siburt, C.J., Mietzner, T.A. and Crumbliss, A.L. (2012) FbpA - a bacterial transferrin with more to offer. Biochim. Biophys. Acta 1820, 379-392
61. Khun, H.H., Kirby, S.D. and Lee, B.C. (1998) A Neisseria meningitidis fbpABC mutant is incapable of using nonheme iron for growth. Infect. Immun. 66, 2330-2336
62. Ling, J.M. and Schryvers, A.B. (2006) Perspectives on interactions between lactoferrin and bacteria. Biochem. Cell Biol. 84, 275-281
63. Sun, X.L., Baker, H.M., Shewry, S.C., Jameson, G.B. and Baker, E.N. (1999) Structure of recombinant human lactoferrin expressed in Aspergillus awamori. Acta Crystallogr. D Biol. Crystallogr. 55, 403-407
64. Baker, H.M. and Baker, E.N. (2004) Lactoferrin and iron: structural and dynamic aspects of binding and release. Biometals 17, 209-216
65. Aisen, P. and Leibman, A. (1972) Lactoferrin and transferrin: a comparative study. Biochim. Biophys. Acta 257, 314-323
66. Brooks, C.L., Arutyunova, E. and Lemieux, M.J. (2014) The structure of lactoferrin-binding protein B from Neisseria meningitidis suggests roles in iron acquisition and neutralization of host defences. Acta Crystallogr. F Struct. Biol. Commun. 70, 1312-1317
67. Noinaj, N., Cornelissen, C.N. and Buchanan, S.K. (2013) Structural insight into the lactoferrin receptors from pathogenic Neisseria. J. Struct. Biol. 184, 83-92
68. Morgenthau, A., Livingstone, M., Adamiak, P. and Schryvers, A.B. (2012) The role of lactoferrin binding protein B in mediating protection against human lactoferricin. Biochem. Cell Biol. 90, 417-423
69. 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
70. Stojiljkovic, I., Hwa, V., de Saint Martin, L., O'Gaora, P., Nassif, X., Heffron, F. et al. (1995) The Neisseria meningitidis haemoglobin receptor: its role in iron utilization and virulence. Mol. Microbiol. 15, 531-541
71. Chen, C.J., Sparling, P.F., Lewis, L.A., Dyer, D.W. and Elkins, C. (1996) Identification and purification of a hemoglobin-binding outer membrane protein from Neisseria gonorrhoeae. Infect. Immun. 64, 5008-5014
72. Lewis, L.A. and Dyer, D.W. (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
73. Stojiljkovic, I., Larson, J., Hwa, V., Anic, S. and So, M. (1996) HmbR outer membrane proteins of pathogenic Neisseriae: iron-regulated, hemoglobin binding proteins with high degree of primary structure conservation. J. Bacteriol. 178, 4670-4678
74. Zhu, W., Hunt, D.J., Richardson, A.R. and Stojiljkovic, I. (2000) Use of heme compounds as iron sources by pathogenic Neisseriae requires the product of the hemO gene. J. Bacteriol. 182, 439-447
75. Zhu, W., Wilks, A. and Stojiljkovic, I. (2000) Degradation of heme in Gram-negative bacteria: the product of the hemO gene of Neisseriae is a heme oxygenase. J. Bacteriol. 182, 6783-6790
76. Wong, C.T., Xu, Y., Gupta, A., Garnett, J.A., Matthews, S.J. and Hare, S.A. (2015) Structural analysis of haemoglobin binding by HpuA from the Neisseriaceae family. Nat. Commun. 6, 10172
77. Maret, W. (2013) Zinc biochemistry: from a single zinc enzyme to a key element of life. Adv. Nutr. 4, 82-91
78. Maret, W. (2013) Zinc and the zinc proteome. Met. Ions Life Sci. 12, 479-501
79. Krèżl, A. and Maret, W. (2016) The biological inorganic chemistry of zinc ions. Arch. Biochem. Biophys. 611, 3-19
80. Subramanian Vignesh, K. and Deepe, Jr, G.S. (2016) Immunological orchestration of zinc homeostasis: the battle between host mechanisms and pathogen defenses. Arch. Biochem. Biophys. 611, 66-78
81. Zackular, J.P., Chazin, W.J. and Skaar, E.P. (2015) Nutritional immunity: S100 proteins at the host-pathogen interface. J. Biol. Chem. 290, 18991-18998
82. Stríz, I. and Trebichavský, I. (2004) Calprotectin - a pleiotropic molecule in acute and chronic inflammation. Physiol. Res. 53, 245-253
83. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D.S. et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535
84. Urban, C.F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W. et al. (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5, e1000639
85. Hunter, M.J. and Chazin, W.J. (1998) High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factor-related proteins 8 and 14. J. Biol. Chem. 273, 12427-12435
86. Korndoörfer, I.P., Brueckner, F. and Skerra, A. (2007) The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotectin, illustrates how conformational changes of interacting α-helices can determine specific association of two EF-hand proteins. J. Mol. Biol. 370, 887-898
87. Donato, R. (2001) S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int. J. Biochem. Cell Biol. 33, 637-668
88. Brophy, M.B., Hayden, J.A. and Nolan, E.M. (2012) Calcium ion gradients modulate the zinc affinity and antibacterial activity of human calprotectin. J. Am. Chem. Soc. 134, 18089-18100
89. Hayden, J.A., Brophy, M.B., Cunden, L.S. and Nolan, E.M. (2013) High-affinity manganese coordination by human calprotectin is calcium-dependent and requires the histidine-rich site formed at the dimer interface. J. Am. Chem. Soc. 135, 775-787
90. Nakashige, T.G., Zhang, B., Krebs, C. and Nolan, E.M. (2015) Human calprotectin is an iron-sequestering host-defense protein. Nat. Chem. Biol. 11, 765-771
91. Brini, M., Ottolini, D., Calì, T. and Carafoli, E. (2013) Calcium in health and disease. Met. Ions Life Sci. 13, 81-137
92. Williams, R.J.P. (1996) Calcium binding proteins in normal and transformed cells. Cell Calcium 20, 87-93
93. Kehl-Fie, T.E., Chitayat, S., Hood, M.I., Damo, S., Restrepo, N., Garcia, C. et al. (2011) Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10, 158-164
94. Damo, S.M., Kehl-Fie, T.E., Sugitani, N., Holt, M.E., Rathi, S., Murphy, W.J. et al. (2013) Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc. Natl. Acad. Sci. U.S.A. 110, 3841-3846
95. Gagnon, D.M., Brophy, M.B., Bowman, S.E.J., Stich, T.A., Drennan, C.L., Britt, R.D. et al. (2015) Manganese binding properties of human calprotectin under conditions of high and low calcium: X-ray crystallographic and advanced electron paramagnetic resonance spectroscopic analysis. J. Am. Chem. Soc. 137, 3004-3016
96. Nakashige, T.G., Stephan, J.R., Cunden, L.S., Brophy, M.B., Wommack, A.J., Keegan, B.C. et al. (2016) The hexahistidine motif of host-defense protein human calprotectin contributes to zinc withholding and its functional versatility. J. Am. Chem. Soc. 138, 12243-12251
97. Chen, C.Y. and Morse, S.A. (2001) Identification and characterization of a high-affinity zinc uptake system in Neisseria gonorrhoeae. FEMS Microbiol. Lett. 202, 67-71
98. Stork, M., Bos, M.P., Jongerius, I., de Kok, N., Schilders, I., Weyants, V.E. et al. (2010) An outer membrane receptor of Neisseria meningitidis involved in zinc acquisition with vaccine potential. PLoS Pathog. 6, e1000969
99. Calmettes, C., Ing, C., Buckwalter, C.M., El Bakkouri, M., Chieh-Lin Lai, C., Pogoutse, A. et al. (2015) The molecular mechanism of zinc acquisition by the neisserial outer-membrane transporter ZnuD. Nat. Commun. 6, 7996
100. Larson, J.A., Howie, H.L. and So, M. (2004) Neisseria meningitidis accelerates ferritin degradation in host epithelial cells to yield an essential iron source. Mol. Microbiol. 53, 807-820
101. West, S.E. and Sparling, P.F. (1985) Response of Neisseria gonorrhoeae to iron limitation: alterations in expression of membrane proteins without apparent siderophore production. Infect. Immun. 47, 388-394
102. Biegel Carson, S.D., Klebba, P.E., Newton, S.M.C. and Sparling, P.F. (1999) Ferric enterobactin binding and utilization by Neisseria gonorrhoeae. J. Bacteriol. 181, 2895-2901
103. Strange, H.R., Zola, T.A. and Cornelissen, C.N. (2011) The fbpABC operon is required for Ton-independent utilization of xenosiderophores by Neisseria gonorrhoeae strain FA19. Infect. Immun. 79, 267-278
104. Jordan, P.W. and Saundersm, N.J. (2009) Host iron binding proteins acting as niche indicators for Neisseria meningitidis. PLoS ONE 4, e5198
105. Barber, M.F. and Elde, N.C. (2014) Escape from bacterial iron piracy through rapid evolution of transferrin. Science 346, 1362-1366
106. Armitage, A.E. and Drakesmith, H. (2014) The battle for iron. Science 346, 1299-1300