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Cloning and characterization of a novel periplasmic heme-transport protein from the human pathogen Pseudomonas aeruginosa
Abstract
Successful iron acquisition plays a crucial role in bacterial virulence. Numerous Gram-negative pathogenic bacteria have developed a novel heme-acquisition system to steal iron from hosts. This system involves a cell-surface heme receptor, a periplasmic heme-transport protein (HTP) and inner-membrane proteins typical for ATP binding cassette transporters. We have cloned the gene encoding a periplasmic HTP from Pseudomonas aeruginosa, overexpressed it in Escherichia coli and purified it as a 33-kDa His-tagged protein. Heme-staining and heme-content assays reveal that the isolated HTP contains approximately 50% heme-bound and apo forms. The heme is noncovalently attached and can be transferred to apomyoglobin in vitro. Electron paramagnetic resonance and UV-vis spectroscopies indicate a five-coordinate, high-spin, ferric heme in HTP. HTP is reduced by dithionite but not by either dithiothreitol or ascorbate. Fluorescence and circular dichroism spectroscopies indicate a well-ordered structure for the HTP and a conformational change upon heme binding to apo-HTP. This was confirmed by limited proteolysis assays. Apo-HTP binds heme or protoporphyrin IX at 1:1 ratio with high affinity (K (d) approximately 1.2 and 14 nM, respectively). A BLASTP search revealed approximately 52 putative bacterial periplasmic heme transporters, which can be grouped into six classes, most of which are associated with pathogenic bacteria. Multiple sequence alignment reveals that these HTPs share low sequ…
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“A specific example of a direct heme-binding uptake system is Pseudomonas aeruginosa phuR-phuSTUVW , where PhuR is the outer membrane receptor, PhuT is the HTP, PhuUVW is the ABC transporter, and PhuS is the cytoplasmic protein (53, 79, 117).”
From Overcoming the Heme Paradox: Heme Toxicity and Tolerance in Bacterial Pathogens (2010) · cites this paper as [117]
Citations
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
LAEMMLI, U. K. (1970) · Nature · doi:10.1038/227680a0 · Cited by 249,961
Raza, H., John, A., & Nemmar, A. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350087 · Cited by 47,221
Thompson, J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.24.4876 · Cited by 38,993
MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment
Kumar, S. (2004) · Briefings in Bioinformatics · doi:10.1093/bib/5.2.150 · Cited by 11,756
The PSIPRED protein structure prediction server
McGuffin, L. J., Bryson, K., & Jones, D. T. (2000) · Bioinformatics · doi:10.1093/bioinformatics/16.4.404 · Cited by 3,887
Whitmore, L., & Wallace, B. A. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh371 · Cited by 2,338
Iron Metabolism in Pathogenic Bacteria
Ratledge, C., & Dover, L. G. (2000) · Annual Review of Microbiology · doi:10.1146/annurev.micro.54.1.881 · Cited by 1,539
Thomas, P. E., Ryan, D. E., & Levin, W. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90067-1 · Cited by 1,065
Enterobactin: an archetype for microbial iron transport.
Raymond, K. N., Dertz, E. A., & Kim, S. S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0630018100 · Cited by 933
Bacterial Iron Sources: From Siderophores to Hemophores
Wandersman, C., & Delepelaire, P. (2004) · Annual Review of Microbiology · doi:10.1146/annurev.micro.58.030603.123811 · Cited by 930
Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra
Berry, E. A., & Trumpower, B. L. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90643-9 · Cited by 914
Mineralization in ferritin: an efficient means of iron storage
Chasteen, N. D., & Harrison, P. M. (1999) · Journal of Structural Biology · doi:10.1006/jsbi.1999.4118 · Cited by 815
Identification of an Intestinal Heme Transporter
Shayeghi, M., Latunde-Dada, G. O., Oakhill, J. S., Laftah, A. H., Takeuchi, K., Halliday, N., Khan, Y., Warley, A., McCann, F. E., Hider, R. C., et al. (2005) · Cell · doi:10.1016/j.cell.2005.06.025 · Cited by 755
Lobley, A., Whitmore, L., & Wallace, B. A. (2002) · Bioinformatics · doi:10.1093/bioinformatics/18.1.211 · Cited by 726
Todar's Online Textbook of Bacteriology
Darmani, H. (2006) · Cited by 522
The Molar Light Absorption of Pyridine Ferroprotoporphrin (Pyridine Haemochromogen).
Paul, K. G., Theorell, H., Åkeson, Å., Virtanen, A. I., & Sörensen, N. A. (1953) · Acta Chemica Scandinavica · doi:10.3891/acta.chem.scand.07-1284 · Cited by 507
Relative helix-forming tendencies of nonpolar amino acids
Padmanabhan, S., Marqusee, S., Ridgeway, T., Laue, T. M., & Baldwin, R. L. (1990) · Nature · doi:10.1038/344268a0 · Cited by 462
Iron-Source Preference of Staphylococcus aureus Infections
Skaar, E. P., Humayun, M., Bae, T., DeBord, K. L., & Schneewind, O. (2004) · Science · doi:10.1126/science.1099930 · Cited by 440
Kurz, C. L. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg159 · Cited by 371
Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores
Wandersman, C., & Stojiljkovic, I. (2000) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00078-3 · Cited by 318
Ochsner, U. A., Johnson, Z., & Vasil, M. L. (2000) · Microbiology · doi:10.1099/00221287-146-1-185 · Cited by 310
Stojiljkovic, I., & Hantke, K. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05535.x · Cited by 258
Peisach, J., Blumberg, W. E., Ogawa, S., Rachmilewitz, E. A., & Oltzik, R. (1971) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)62232-x · Cited by 251
The role of the proximal ligand in heme enzymes
Poulos, T. L. (1996) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s007750050064 · Cited by 250
Iron uptake mechanisms and their regulation in pathogenic bacteria
Braun, V. (2001) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00103 · Cited by 249
[4] Preparation of derivatives of ferrous and ferric hemoglobin
Iorio, E. E. D. (1981) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(81)76114-7 · Cited by 246
Emerging strategies in microbial haem capture
Genco, C. A., & Dixon, D. W. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02231.x · Cited by 245
Dealing with iron: Common structural principles in proteins that transport iron and heme
Baker, H. M., Anderson, B. F., & Baker, E. N. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0637295100 · Cited by 243
Lack of heme synthesis in a free-living eukaryote
Rao, A. U., Carta, L. K., Lesuisse, E., & Hamza, I. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500877102 · Cited by 241
Guo, M., Sun, H., McArdle, H. J., Gambling, L., & Sadler, P. J. (2000) · Biochemistry · doi:10.1021/bi000798z · Cited by 228
Self-citationStructure of the CO sensing transcription activator CooA.
Poulos, T. L., Lanzilotta, W. N., Schuller, D. J., Thorsteinsson, M. V., Kerby, R. L., & Roberts, G. P. (2000) · Nature Structural Biology · doi:10.1038/82820 · Cited by 227
The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter
Borths, E. L., Locher, K. P., Lee, A. T., & Rees, D. C. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.262659699 · Cited by 226
The Association Rate Constant for Heme Binding to Globin Is Independent of Protein Structure
Hargrove, M. S., Barrick, D., & Olson, J. S. (1996) · Biochemistry · doi:10.1021/bi960371l · Cited by 210
Iron-regulated surface determinants (Isd) of Staphylococcus aureus: stealing iron from heme
P. Skaar, E., & Schneewind, O. (2004) · Microbes and Infection · doi:10.1016/j.micinf.2003.12.008 · Cited by 209
The crystal structure of HasA, a hemophore secreted by Serratia marcescens.
Czjzek, M., Arnoux, P., Haser, R., Izadi‐Pruneyre, N., Lecroisey, A., Delepierre, M., & Wandersman, C. (1999) · Nature Structural Biology · doi:10.1038/9281 · Cited by 200
Occhino, D. A., Wyckoff, E. E., Henderson, D. P., Wrona, T. J., & Payne, S. M. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.01034.x · Cited by 175
Iron transport and signaling in Escherichia coli
Braun, V., & Braun, M. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)03185-x · Cited by 170
Karpowich, N. K., Huang, H. H., Smith, P., & Hunt, J. F. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212239200 · Cited by 169
Thompson, J. M., Jones, H. A., & Perry, R. D. (1999) · Infection and Immunity · doi:10.1128/iai.67.8.3879-3892.1999 · Cited by 154
Purification, characterization, and cloning of a heme-binding protein (23 kDa) in rat liver cytosol
Iwahara, S.-I., Satoh, H., Song, D.-X., Webb, J., Burlingame, A. L., Nagae, Y., & Müller‐Eberhard, U. (1995) · Biochemistry · doi:10.1021/bi00041a017 · Cited by 140
Processing of Heme and Heme-Containing Proteins by Bacteria
Stojiljkovic, I., & Perkins-Balding, D. (2002) · DNA and Cell Biology · doi:10.1089/104454902753759708 · Cited by 134
Wyckoff, E. E., Duncan, D., Torres, A. G., Mills, M., Maase, K., & Payne, S. M. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00873.x · Cited by 132
Friedman, J., Lad, L., Li, H., Wilks, A., & Poulos, T. L. (2004) · Biochemistry · doi:10.1021/bi049687g · Cited by 112
Izadi‐Pruneyre, N., Henry, Y. A., Haladjian, J., Goldberg, M., Wandersman, C., Delepierre, M., & Lecroisey, A. (1997) · Biochemistry · doi:10.1021/bi962577s · Cited by 111
Octaheme tetrathionate reductase is a respiratory enzyme with novel heme ligation
Mowat, C. G., Rothery, E. L., Miles, C. S., McIver, L., Doherty, M. K., Drewette, K. J., Taylor, P., Walkinshaw, M. D., Chapman, S. K., & Reid, G. A. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb827 · Cited by 110
Eakanunkul, S., Lukat-Rodgers, G. S., Sumithran, S., Ghosh, A., Rodgers, K. R., Dawson, J. H., & Wilks, A. (2005) · Biochemistry · doi:10.1021/bi050422r · Cited by 110
Liu, Y., Moënne‐Loccoz, P., Hildebrand, D. P., et al. (1999) · Biochemistry · doi:10.1021/bi982707s · Cited by 106
Morton, D. J., Whitby, P. W., Jin, H., Ren, Z., & Stull, T. L. (1999) · Infection and Immunity · doi:10.1128/iai.67.6.2729-2739.1999 · Cited by 97
Deniau, C., Gilli, R. M., Izadi‐Pruneyre, N., Létoffé, S., Delepierre, M., Wandersman, C., Briand, C. M., & Lecroisey, A. (2003) · Biochemistry · doi:10.1021/bi030015k · Cited by 92
Discovery of a haem uptake system in the soil bacterium Bradyrhizobium japonicum
Nienaber, A., Hennecke, H., & Fischer, H. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02555.x · Cited by 92
Lansky, I. B., Lukat-Rodgers, G. S., Block, D., Rodgers, K. R., Ratliff, M., & Wilks, A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m600824200 · Cited by 92
Phase Variation of Hemoglobin Utilization in Neisseria gonorrhoeae
Chen, C.-J., Elkins, C., & Sparling, P. F. (1998) · Infection and Immunity · doi:10.1128/iai.66.3.987-993.1998 · Cited by 84
Guo, M., Sulc, F., Ribbe, M. W., Farmer, P. J., & Burgess, B. K. (2002) · Journal of the American Chemical Society · doi:10.1021/ja026478f · Cited by 79
Self-citationPathogenic bacteria prefer heme.
Rouault, T. A. (2004) · Science · doi:10.1126/science.1102975 · Cited by 76
Heme binding to murine erythroleukemia cells. Evidence for a heme receptor.
Galbraith, R. A., Sassa, S., & Kappas, A. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)39008-7 · Cited by 72
Iron transport: emerging roles in health and disease
Goswami, T., Rolfs, A., & Hediger, M. A. (2002) · Biochemistry and Cell Biology · doi:10.1139/o02-159 · Cited by 71
Bullen, J. J., Griffiths, E., & Edmiston, C. E. (1999) · Shock · doi:10.1097/00024382-199911000-00013 · Cited by 70
Fluorimetric study of the binding of protoporphyrin to haemopexin and albumin
Lamola, A. A., Asher, I. M., Müller‐Eberhard, U., & Poh‐Fitzpatrick, M. B. (1981) · Biochemical Journal · doi:10.1042/bj1960693 · Cited by 68
Synergistic Anion and Metal Binding to the Ferric Ion-binding Protein from Neisseria gonorrhoeae
Guo, M., Harvey, I., Yang, W., Coghill, L. S., Campopiano, D. J., Parkinson, J. A., MacGillivray, R. T. A., Harris, W. R., & Sadler, P. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m208776200 · Cited by 67
Self-citationSpectroscopic and Biochemical Characterization of Heme Binding to Yeast Dap1p and Mouse PGRMC1p
Ghosh, K., Thompson, A. M., Goldbeck, R. A., Shi, X., Whitman, S., Oh, E., Zhu, Z., Vulpe, C. D., & Holman, T. R. (2005) · Biochemistry · doi:10.1021/bi0511585 · Cited by 63
Resonance Raman studies on protocatechuate 3,4-dioxygenase inhibitor complexes
QUE, L. J., & Epstein, R. (1981) · Biochemistry · doi:10.1021/bi00512a028 · Cited by 57
Characterization of a human and mouse tetrapyrrole-binding protein
Blackmon, B. J., Dailey, T. A., Lianchun, X., et al. (2002) · Archives of Biochemistry and Biophysics · doi:10.1016/s0003-9861(02)00471-x · Cited by 57
Guo, M., Bhaskar, B., Li, H., Barrows, T. P., & Poulos, T. L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306708101 · Cited by 56
Self-citationAndrews, N. C. (2005) · New England Journal of Medicine · doi:10.1056/nejmcibr053987 · Cited by 55
Heme coordination of prostaglandin H synthase.
Tsai, A., Kulmacz, R. J., Wang, J. S., Wang, Y., Wart, H. E. V., & Palmer, G. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)52911-2 · Cited by 50
Sato, E., Sagami, I., Uchida, T., Sato, A., Kitagawa, T., Igarashi, J., & Shimizu, T. (2004) · Biochemistry · doi:10.1021/bi048742i · Cited by 50
A novel protein–mineral interface
Alexeev, D. G., Zhu, H., Guo, M., Zhong, W., Hunter, D. J. B., Yang, W., Campopiano, D. J., & Sadler, P. J. (2003) · Nature Structural & Molecular Biology · doi:10.1038/nsb903 · Cited by 47
Self-citationThe Intestinal Heme Transporter Revealed
Rouault, T. A. (2005) · Cell · doi:10.1016/j.cell.2005.08.027 · Cited by 47
Structure, Properties and Reactivity of the FeIIFeIII and ZnIIFeIII Purple Acid Phosphatases
Twitchett, M. B., & Sykes, A. G. (1999) · European Journal of Inorganic Chemistry · doi:10.1002/(sici)1099-0682(199912)1999:12<2105::aid-ejic2105>3.0.co;2-2 · Cited by 47
Migita, C. T., Zhang, X., & Yoshida, T. (2003) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2003.03421.x · Cited by 44
Haem-globin equilibrium studies by fluorimetry
Teale, F. W. J. (1959) · Biochimica et Biophysica Acta · doi:10.1016/0006-3002(59)90376-2 · Cited by 33
Juíz-Río, S., Osorio, C. R., & Lemos, M. L. (2005) · Archives of Microbiology · doi:10.1007/s00203-005-0779-4 · Cited by 28
Short Oxo–Titanium( IV ) Bond in Bacterial Transferrin: A Protein Target for Metalloantibiotics
Guo, M., Harvey, I., Campopiano, D. J., & Sadler, P. J. (2006) · Angewandte Chemie International Edition · doi:10.1002/anie.200600260 · Cited by 26
Self-citationZelent, B., Kaposi, A. D., Nucci, N. V., Sharp, K. A., Dalosto, S. D., Wright, W. W., & Vanderkooi, J. M. (2004) · The Journal of Physical Chemistry B · doi:10.1021/jp037664q · Cited by 21
Iron acquisition: straight up and on the rocks?
Butler, A. (2003) · Nature Structural & Molecular Biology · doi:10.1038/nsb0403-240 · Cited by 16
Manipulation of Iron to Determine Survival: Competition Between Host and Pathogen
Laham-Karam, N., & Ehrlich, R. L. (2004) · Immunologic Research · doi:10.1385/ir:30:1:015 · Cited by 16
Worrall, J. A. R., van Roon, A. M., Ubbink, M., & Canters, G. W. (2005) · FEBS Journal · doi:10.1111/j.1742-4658.2005.04664.x · Cited by 15
Metal-Dependent Conformers of the Periplasmic Ferric Ion Binding Protein
Nowalk, A. J., Vaughan, K. G., Day, B. W., Tencza, S. B., & Mietzner, T. A. (1997) · Biochemistry · doi:10.1021/bi971413o · Cited by 12
(1999)
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Overcoming the Heme Paradox: Heme Toxicity and Tolerance in Bacterial Pathogens
Anzaldi, L. L., & Skaar, E. P. (2010) · Infection and Immunity · doi:10.1128/iai.00613-10 · Cited by 295
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Tong, Y., & Guo, M. (2009) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2008.10.013 · Cited by 162
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Xiao, Q., Jiang, X., Moore, K. J., Shao, Y., Pi, H., Dubail, I., Charbit, A., Newton, S. M., & Klebba, P. E. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07667.x · Cited by 51
Metadata
- Authors
- Tong, Y., & Guo, M.
- Venue
- JBIC Journal of Biological Inorganic Chemistry
- Published
- 2007-03-27
- Volume
- 12
- Issue
- 6
- Pages
- 735-750
- ISSN
- 0949-8257
- 1432-1327
- Cited by
- 32
- References
- 80
- Language
- en
- Licence
- www.springer.com/tdm (tdm)
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