Molecular characterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization

Infection and Immunity

Volumn 67, Issue 8, 1999, Pages 3879-3892

  Thompson, Jan M ^a   Jones, Heather A ^a   Perry, Robert D ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; HAPTOGLOBIN; HEMIN; HEMOPROTEIN; MYOGLOBIN;

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; GENE DELETION; IRON METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGEN TRANSPORT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; YERSINIA PESTIS;

YERSINIA PESTIS;

EID: 0032765125     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.8.3879-3892.1999     Document Type: Article

References (71)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1987. Current protocols in molecular biology. John Wiley & Sons, New York, N.Y.
4. Bearden, S. W., J. D. Fetherston, and R. D. Perry. 1997. Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis. Infect. Immun. 65:1659-1668.
5. Bearden, S. W., and R. D. Perry. 1999. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32:403-414.
6. Bearden, S. W., T. M. Staggs, and R. D. Perry. 1998. An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J. Bacteriol. 180:1135-1147.
7. Braun, V., K. Hantke, and W. Köster. 1998. Bacterial iron transport: mechanisms, genetics, and regulation. Met. Ions Biol. Syst. 35:67-145.
8. Cope, L. D., S. E. Thomas, Z. Hrkal, and E. J. Hansen. 1998. Binding of heme-hemopexin complexes by soluble HxuA protein allows utilization of this complexed heme by Haemophilus influenzae. Infect. Immun. 66:4511- 4516.
9. Cope, L. D., R. Yogev, U. Müller-Eberhard, and E. J. Hansen. 1995. A gene cluster involved in the utilization of both free heme and heme:hemopexin by Haemophilus influenzae type b. J. Bacteriol. 177:2644-2653.
10. Crosa, J. H. 1997. Signal transduction and transcriptional and posttranscriptional control of iron-regulated genes in bacteria. Microbiol. Mol. Biol. Rev. 61:319-336.
11. Daskaleros, P. A., J. A. Stoebner, and S. M. Payne. 1991. Iron uptake in Plesiomonas shigelloides: cloning of the genes for the heme-iron uptake system. Infect. Immun. 59:2706-2711.
12. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
13. Donnenberg, M. S., and J. H. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
14. Elkins, C., P. A. Totten, B. Olsen, and C. E. Thomas. 1998. Role of the Haemophilus ducreyi Ton system in internalization of heme from hemoglobin. Infect. Immun. 66:151-160.
15. Fetherston, J. D., S. W. Bearden, and R. D. Perry. 1996. YbtA, an AraC-type regulator of the Yersinia pestis pesticin/yersiniabactin receptor. Mol. Microbiol. 22:315-325.
16. Fetherston, J. D., J. W. Lillard, Jr., and R. D. Perry. 1995. Analysis of the pesticin receptor from Yersinia pestis: role in iron-deficient growth and possible regulation by its siderophore. J. Bacteriol. 177:1824-1833.
17. Froehlich, B., L. Husmann, J. Caron, and J. R. Scott. 1994. Regulation of rns, a positive regulatory factor for pili of enterotoxigenic Escherichia coli. J. Bacteriol. 176:5385-5392.
18. Gehring, A. M., E. DeMoll, J. D. Fetherston, I. Mori, G. F. Mayhew, F. R. Blattner, C. T. Walsh, and R. D. Perry. 1998. Iron acquisition in plague: modular logic in enzymatic biogenesis of yersiniabactin by Yersinia pestis. Chem. Biol. 5:555-568.
19. Ghigo, J.-M., S. Létoffé, and C. Wandersman. 1997. A new type of hemophore-dependent heme acquisition system of Serratia marcescens reconstituted in Escherichia coli. J. Bacteriol. 179:3572-3579.
20. Henderson, D. P., and S. M. Payne. 1994. Characterization of the Vibrio cholerae outer membrane heme transport protein HutA: sequence of the gene, regulation of expression, and homology to the family of TonB-dependent proteins. J. Bacteriol. 176:3269-3277.
21. Henderson, D. P., and S. M. Payne. 1993. Cloning and characterization of the Vibrio choleras genes encoding the utilization of the iron from haemin and haemoglobin. Mol. Microbiol. 7:461-469.
22. Higgins, C. F. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67-113.
23. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
24. Hornung, J. M., H. A. Jones, and R. D. Perry. 1996. The hmu locus of Yersinia pestis is essential for utilization of free haemin and haem-protein complexes as iron sources. Mol. Microbiol. 20:725-739.
25. 12 transport in Escherichia coli: energy coupling between membranes. Mol. Microbiol. 4:2027-2033.
26. Lee, B. C. 1995. Quelling the red menace: haem capture by bacteria. Mol. Microbiol. 18:383-390.
27. Lee, B. C., and S. Levesque. 1997. A monoclonal antibody directed against the 97-kilodalton gonococcal hemin-binding protein inhibits hemin utilization by Neisseria gonorrhoeae. Infect. Immun. 65:2970-2974.
28. 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.
29. Lewis, L. A., E. Gray, V.-P. Wang, B. A. Roe, and D. W. Dyer. 1997. Molecular characterization of hpuAB, the haemoglobulin-haptoglobin-utilization operon of Neisseria meningitidis. Mol. Microbiol. 23:737-749.
30. Lillard, J. W., Jr., S. W. Bearden, J. D. Fetherston, and R. D. Perry. 1999. The haemin storage (Hms+) phenotype of Yersinia pestis is not essential for the pathogenesis of bubonic plague in mammals. Microbiology 145:197-209.
31. Litwin, C. M., and B. L. Byrne. 1998. Cloning and characterization of an outer membrane protein of Vibrio vulnificus required for heme utilization: regulation of expression and determination of the gene sequence. Infect. Immun. 66:3134-3141.
32. Lucier, T. S., J. D. Fetherston, R. R. Brubaker, and R. D. Perry. 1996. Iron uptake and iron-repressible polypeptides in Yersinia pestis. Infect. Immun. 64:3023-3031.
33. Maciver, I., J. L. Latimer, H. H. Liem, U. Muller-Eberhard, Z. Hrkal, and E. J. Hansen. 1996. Identification of an outer membrane protein involved in utilization of hemoglobin-haptoglobin complexes by nontypeable Haemophilus influenzae. Infect. Immun. 64:3703-3712.
34. Mietzner, T. A., and S. A. Morse. 1994. The role of iron-binding proteins in the survival of pathogenic bacteria. Annu. Rev. Nutr. 14:471-493.
35. Miller, J. H. 1992. A short course in bacterial genetics. A laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
36. Miller, V. L., and J. J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
37. Mills, M., and S. M. Payne. 1995. Genetics and regulation of heme iron transport in Shigella dysenteriae and detection of an analogous system in Escherichia coli O157:H7. J. Bacteriol. 177:3004-3009.
38. Mills, M., and S. M. Payne. 1997. Identification of shuA, the gene encoding the heme receptor of Shigella dysenteriae, and analysis of invasion and intracellular multiplication of a shuA mutant. Infect. Immun. 65:5358-5363.
39. Muller-Eberhard, U., and H. Nikkilä. 1989. Transport of tetrapyrroles by proteins. Semin. Hematol. 26:86-104.
40. Nakai, K., and M. Kanehisa. 1991. Expert system for predicting protein localization sites in Gram-negative bacteria. Proteins 11:95-110.
41. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Heijni. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
42. Oechino, D. A., E. E. Wyckoff, D. P. Henderson, T. J. Wrona, and S. M. Payne. 1998. Vibrio cholerae iron transport: haem transport genes are linked to one of two sets of tonB, exbB, exbD genes. Mol. Microbiol. 29: 1493-1507.
43. Ochsner, U. A., Z. Johnson, Z. Vasil, and M. L. Vasil. 1998. DNA sequence and expression of a Pseudomonas aeruginosa receptor and ABC transporter locus homologous to haemin iron uptake systems of bacterial pathogens, abstr. B258, p. 98. In Abstracts of the 98th General Meeting of the American Society for Microbiology 1998. American Society for Microbiology, Washington, D.C.
44. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
45. Perry, R. D., T. S. Lucier, D. J. Sikkema, and R. R. Brubaker. 1993. Storage reservoirs of hemin and inorganic iron in Yersinia pestis. Infect. Immun. 61:32-39.
46. Perry, R. D., M. L. Pendrak, and P. Schuetze. 1990. Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis. J. Bacteriol. 172:5929-5937.
47. Perry, R. D., and R. R. Brubaker. 1979. Accumulation of iron by yersiniae. J. Bacteriol. 137:1290-1298.
48. 2+ response virulence genes. J. Bacteriol. 173:2649-2657.
49. Reece, K. S., and G. J. Phillips. 1995. New plasmids carrying antibiotic-resistance cassettes. Gene 165:141-142.
50. Reed, L. J., and H. Muench. 1938. A simple method for estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
51. 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.
52. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
53. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
54. Saurin, W., W. Köster, and E. Dassa. 1994. Bacterial binding protein-dependent permeases: characterization of distinctive signatures for functionally related integral cytoplasmic membrane proteins. Mol. Microbiol. 12:993-1004.
55. Sikkema, D. J., and R. R. Brubaker. 1989. Outer membrane peptides of Yersinia pestis mediating siderophore-independent assimilation of iron. Biol. Met. 2:174-184.
56. Sikkema, D. J., and R. R. Brubaker. 1987. Resistance to pesticin, storage of iron, and invasion of HeLa cells by yersiniae. Infect. Immun. 55:572-578.
57. Simon, E. H., and I. Tessman. 1963. Thymidine-requiring mutants of phage T4. Proc. Natl. Acad. Sci. USA 50:526-532.
58. Staggs, T. M., and R. D. Perry. 1991. Identification and cloning of a fur regulatory gene in Yersinia pestis. J. Bacteriol. 173:417-425.
59. Stojiljkovic, I., and K. Hantke. 1992. Hemin uptake system of Yersinia enterocolitica: similarities with other TonB-dependent systems in Gram-negative bacteria. EMBO J. 11:4359-4367.
60. Stojiljkovic, I., and K. Hantke. 1994. Transport of haemin across the cytoplasmic membrane through a haemin-specific periplasmic binding-protein-dependent transport system in Yersinia enterocolitica. Mol. Microbiol. 13: 719-732.
61. 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.
62. 2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect. Immun. 51:445-454.
63. Surgalla, M. J., and E. D. Beesley. 1969. Congo red-agar plating medium for detecting pigmentation in Pasteurella pestis. Appl. Microbiol. 18:834-837.
64. Tam, R., and M. H. Saier, Jr. 1993. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol. Rev. 57:320-346.
65. The Sanger Centre Yersinia pestis Genomic Project. 27 July 1998, revision date (sequence updated weekly). [Online.] Yersinia pestis CO92 genomic sequence database. The Sanger Centre, Hinxton, Cambridge, United Kingdom. ftp://ftp.sanger.ac.uk/pub/pathogens/yp/YP.dbs.
66. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
67. Torres, A. G., and S. M. Payne. 1997. Haem iron-transport system in enterohaemorrhagic Escherichia coli O157:H7. Mol. Microbiol. 23:825-833.
68. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
69. Villarejo, M. R., and I. Zabin. 1974. β-Galactosidase from termination and deletion mutant strains. J. Bacteriol. 120:466-474.
70. von Gabain, A., J. G. Belasco, J. L. Schottel, A. C. Chang, and S. N. Cohen. 1983. Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts. Proc. Natl. Acad. Sci. USA 80:653-657.
71. Wyckoff, E. E., D. Duncan, A. G. Torres, M. Mills, K. Maase, and S. M. Payne. 1998. Structure of the Shigella dysenteriae haem transport locus and its phylogenetic distribution in enteric bacteria. Mol. Microbiol. 28:1139-1152.