Regulatory role of the MisR/S two-component system in hemoglobin utilization in Neisseria meningitidis

Infection and Immunity

Volumn 78, Issue 3, 2010, Pages 1109-1122

  Zhao, Shuming ^a,b   Montanez, Grisselle E ^a,c   Kumar, Pradeep ^a   Sannigrahi, Soma ^a   Tzeng, Yih Ling ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SOUTHWEST HOSPITAL   (China)

^c ROHM AND HAAS COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN; IRON;

ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIUM MUTANT; BINDING SITE; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSCRIPTION; HEMO GENE; HMBR HENE; MISR GENE; MISS GENE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR GENE; REPORTER GENE;

BACTERIAL PROTEINS; BASE SEQUENCE; DNA, BACTERIAL; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; HEME OXYGENASE (DECYCLIZING); HEMOGLOBINS; HUMANS; IRON; MOLECULAR SEQUENCE DATA; NEISSERIA MENINGITIDIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION INITIATION SITE;

EID: 77349118477     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00363-09     Document Type: Article

References (58)

1. Alifano, P., F. Rivellini, D. Limauro, C. B. Bruni, and M. S. Carlomagno. 1991. A consensus motif common to all Rho-dependent prokaryotic transcription terminators. Cell 64:553-563.
2. Al-Tawfiq, J. A., K. R. Fortney, B. P. Katz, A. F. Hood, C. Elkins, and S. M. Spinola. 2000. An isogenic hemoglobin receptor-deficient mutant of Haemophilus ducreyi is attenuated in the human model of experimental infection. J. Infect. Dis. 181:1049-1054.
3. Angerer, A., S. Enz, M. Ochs, and V. Braun. 1995. Transcriptional regulation of ferric citrate transport in Escherichia coli K-12. Fecl belongs to a new subfamily of sigma 70-type factors that respond to extracytoplasmic stimuli. Mol. Microbiol. 18:163-174.
4. Black, C. G., J. A. Fyfe, and J. K. Davies. 1995. A promoter associated with the neisserial repeat can be used to transcribe the uvrB gene from Neisseria gonorrhoeae. J. Bacteriol. 177:1952-1958.
5. Buisine, N., C. M. Tang, and R. Chalmers. 2002. Transposon-like Correia elements: structure, distribution and genetic exchange between pathogenic Neisseria sp. FEBS Lett. 522:52-58.
6. Correia, F. F., S. Inouye, and M. Inouye. 1986. A 26-base-pair repetitive sequence specific for Neisseria gonorrhoeae and Neisseria meningitidis genomic DNA. J. Bacteriol. 167:1009-1015.
7. Craig, N. L., and H. A. Nash. 1984. E. coli integration host factor binds to specific sites in DNA. Cell 39:707-716.
8. De Gregorio, E., C. Abrescia, M. S. Carlomagno, and P. P. Di Nocera. 2003. Asymmetrical distribution of Neisseria miniature insertion sequence DNA repeats among pathogenic and nonpathogenic Neisseria strains. Infect. Immun. 71:4217-4221.
9. De Gregorio, E., C. Abrescia, M. S. Carlomagno, and P. P. Di Nocera. 2003. Ribonuclease III-mediated processing of specific Neisseria meningitidis mRNAs. Biochem. J. 374:799-805.
10. Delany, I., R. Grifantini, E. Bartolini, R. Rappuoli, and V. Scarlato. 2006. Effect of Neisseria meningitidis fur mutations on global control of gene transcription. J. Bacteriol. 188:2483-2492.
11. Escolar, L., J. Perez-Martin, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229.
12. Goosen, N., and P. van de Putte. 1995. The regulation of transcription initiation by integration host factor. Mol. Microbiol. 16:1-7.
13. Gray-Owen, S. D., and A. B. Schryvers. 1996. Bacterial transferrin and lactoferrin receptors. Trends Microbiol. 4:185-191.
14. Grifantini, R., E. Frigimelica, I. Delany, E. Bartolini, S. Giovinazzi, S. Balloni, S. Agarwal, G. Galli, C. Genco, and G. Grandi. 2004. Characterization of a novel Neisseria meningitidis Fur and iron-regulated operon required for protection from oxidative stress: utility of DNA microarray in the assignment of the biological role of hypothetical genes. Mol. Microbiol. 54:962-979.
15. Grifantini, R., S. Sebastian, E. Frigimelica, M. Draghi, E. Bartolini, A. Muzzi, R. Rappuoli, G. Grandi, and C. A. Genco. 2003. Identification of iron-activated and -repressed Fur-dependent genes by transcriptome analysis of Neisseria meningitidis group B. Proc. Natl. Acad. Sci. U. S. A. 100:9542-9547.
16. Hammerschmidt, S., A. Muller, H. Sillmann, M. Muhlenhoff, R. Borrow, A. Fox, J. van Putten, W. D. Zollinger, R. Gerardy-Schahn, and M. Frosch. 1996. Capsule phase variation in Neisseria meningitidis serogroup B by slipped-strand mispairing in the polysialyltransferase gene (siaD): correlation with bacterial invasion and the outbreak of meningococcal disease. Mol. Microbiol. 20:1211-1220.
17. Harrison, O. B., N. J. Evans, J. M. Blair, H. S. Grimes, C. R. Tinsley, X. Nassif, P. Kriz, R. Ure, S. J. Gray, J. P. Derrick, M. C. Maiden, and I. M. Feavers. 2009. Epidemiological evidence for the role of the hemoglobin receptor, HmbR, in meningococcal virulence. J. Infect. Dis. 200:94-98.
18. Heinrichs, D. E., and K. Poole. 1996. PchR, a regulator of ferripyochelin receptor gene (fptA) expression in Pseudomonas aeruginosa, functions both as an activator and as a repressor. J. Bacteriol. 178:2586-2592.
19. Hoch, J. A., and T. J. Silhavy. 1995. Two-component signal transduction. American Society for Microbiology Press, Washington, DC.
20. Janik, A., E. Juni, and G. A. Heym. 1976. Genetic transformation as a tool for detection of Neisseria gonorrhoeae. J. Clin. Microbiol. 4:71-81.
21. Jerse, A. E., E. T. Crow, A. N. Bordner, I. Rahman, C. N. Cornelissen, T. R. Moench, and K. Mehrazar. 2002. Growth of Neisseria gonorrhoeae in the female mouse genital tract does not require the gonococcal transferrin or hemoglobin receptors and may be enhanced by commensal lactobacilli. Infect. Immun. 70:2549-2558.
22. Johnson, C. R., J. Newcombe, S. Thorne, H. A. Borde, L. J. Eales-Reynolds, A. R. Gorringe, S. G. Funnell, and J. J. McFadden. 2001. Generation and characterization of a PhoP homologue mutant of Neisseria meningitidis. Mol. Microbiol. 39:1345-1355.
23. Kahler, C. M., E. Blum, Y. K. Miller, D. Ryan, T. Popovic, and D. S. Stephens. 2001. exl, an exchangeable genetic island in Neisseria meningitidis. Infect. Immun. 69:1687-1696.
24. Koster, M., W. van Klompenburg, W. Bitter, J. Leong, and P. Weisbeek. 1994. Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope. EMBO J. 13:2805-2813.
25. Larson, J. A., D. L. Higashi, I. Stojiljkovic, and M. So. 2002. Replication of Neisseria meningitidis within epithelial cells requires TonB-dependent acquisition of host cell iron. Infect. Immun. 70:1461-1467.
26. Lavitola, A., C. Bucci, P. Salvatore, G. Maresca, C. B. Bruni, and P. Alifano. 1999. Intracistronic transcription termination in polysialyltransferase gene (siaD) affects phase variation in Neisseria meningitidis. Mol. Microbiol. 33: 119-127.
27. Lewis, L. A., M. Gipson, K. Hartman, T. Ownbey, J. Vaughn, and D. W. Dyer. 1999. Phase variation of HpuAB and HmbR, two distinct hemogobin receptors of Neisseria meningitidis DNM2. Mol. Microbiol. 32:977-989.
28. 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.
29. Liu, S. V., N. J. Saunders, A. Jeffries, and R. F. Rest. 2002. Genome analysis and strain comparison of correia repeats and correia repeat-enclosed elements in pathogenic Neisseria. J. Bacteriol. 184:6163-6173.
30. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
31. Mazzone, M., E. De Gregorio, A. Lavitola, C. Pagliarulo, P. Alifano, and P. P. Di Nocera. 2001. Whole-genome organization and functional properties of miniature DNA insertion sequences conserved in pathogenic Neisseriae. Gene 278:211-222.
32. Menard, R., P. J. Sansonetti, and C. Parsot. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5906.
33. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
34. Newcombe, J., L. J. Eales-Reynolds, L. Wootton, A. R. Gorringe, S. G. Funnell, S. C. Taylor, and J. J. McFadden. 2004. Infection with an avirulent phoP mutant of Neisseria meningitidis confers broad cross-reactive immunity. Infect. Immun. 72:338-344.
35. Otto, B. R., A. M. Verweij-van Vught, and D. M. MacLaren. 1992. Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit. Rev. Microbiol. 18:217-233.
36. Packiam, M., D. M. Shell, S. V. Liu, Y. B. Liu, D. J. McGee, R. Srivastava, S. Seal, and R. F. Rest. 2006. Differential expression and transcriptional analysis of the alpha-2,3-sialyltransferase gene in pathogenic Neisseria spp. Infect. Immun. 74:2637-2650.
37. Perkins-Balding, D., M. Ratliff-Griffin, and I. Stojiljkovic. 2004. Iron transport systems in Neisseria meningitidis. Microbiol. Mol. Biol. Rev. 68:154-171.
38. Richardson, A. R., and I. Stojiljkovic. 1999. HmbR, a hemoglobin-binding outer membrane protein of Neisseria meningitidis, undergoes phase variation. J. Bacteriol. 181:2067-2074.
39. Richardson, A. R., and I. Stojiljkovic. 1999. HmbR, a hemoglobin-binding outer membrane protein of Neisseria meningitidis, undergoes phase variation. J. Bacteriol. 181:2067-2074.
40. Rivellini, F., P. Alifano, C. Piscitelli, V. Blasi, C. B. Bruni, and M. S. Carlomagno. 1991. A cytosine- over guanosine-rich sequence in RNA activates rhodependent transcription termination. Mol. Microbiol. 5:3049-3054.
41. Rouquette-Loughlin, C. E., J. T. Balthazar, S. A. Hill, and W. M. Shafer. 2004. Modulation of the mtrCDE-encoded efflux pump gene complex of Neisseria meningitidis due to a Correia element insertion sequence. Mol. Microbiol. 54:731-741.
42. Rozen, S., and H. Skaletsky. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132:365-386.
43. Sannigrahi, S., X. Zhang, and Y. L. Tzeng. 2009. Regulation of the type I protein secretion system by the MisR/MisS two-component system in Neisseria meningitidis. Microbiology 155:1588-1601.
44. Schryvers, A. B., and I. Stojiljkovic. 1999. Iron acquisition systems in the pathogenic Neisseria. Mol. Microbiol. 32:1117-1123.
45. Sebastian, S., S. Agarwal, J. R. Murphy, and C. A. Genco. 2002. The gonococcal fur regulon: identification of additional genes involved in major catabolic, recombination, and secretory pathways. J. Bacteriol. 184:3965-3974.
46. Stephens, D. S., J. S. Swartley, S. Kathariou, and S. A. Morse. 1991. Insertion of Tn916 in Neisseria meningitidis resulting in loss of group B capsular polysaccharide. Infect. Immun. 59:4097-4102.
47. Stevens, M. K., S. Porcella, J. Klesney-Tait, S. Lumbley, S. E. Thomas, M. V. Norgard, J. D. Radolf, and E. J. Hansen. 1996. A hemoglobin-binding outer membrane protein is involved in virulence expression by Haemophilus ducreyi in an animal model. Infect. Immun. 64:1724-1735.
48. 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.
49. Stojiljkovic, I., J. Larson, V. Hwa, S. Anic, and M. So. 1996. HmbR outer membrane receptors of pathogenic Neisseria spp.: iron-regulated, hemoglobin-binding proteins with a high level of primary structure conservation. J. Bacteriol. 178:4670-4678.
50. Torres, V. J., G. Pishchany, M. Humayun, O. Schneewind, and E. P. Skaar. 2006. Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. J. Bacteriol. 188:8421-8429.
51. Tzeng, Y. L., A. Datta, K. D. Ambrose, J. K. Davies, R. W. Carlson, D. S. Stephens, and C. M. Kahler. 2004. The MisR/MisS two-component regulatory system influences inner core structure and immunotype of lipooligosaccharide in Neisseria meningitidis. J. Biol. Chem. 279:35053-35062.
52. Tzeng, Y. L., C. M. Kahler, X. Zhang, and D. S. Stephens. 2008. MisR/MisS two-component regulon in Neisseria meningitidis. Infect. Immun. 76:704-716.
53. Tzeng, Y. L., X. Zhou, S. Bao, S. Zhao, C. Noble, and D. S. Stephens. 2006. Autoregulation of the MisR/MisS two-component signal transduction system in Neisseria meningitidis. J. Bacteriol. 188:5055-5065.
54. Vanderpool, C. K., and S. K. Armstrong. 2003. Heme-responsive transcriptional activation of Bordetella bhu genes. J. Bacteriol. 185:909-917.
55. Venturi, V., C. Ottevanger, M. Bracke, and P. Weisbeek. 1995. Iron regulation of siderophore biosynthesis and transport in Pseudomonas putida WCS358: involvement of a transcriptional activator and of the Fur protein. Mol. Microbiol. 15:1081-1093.
56. Wandersman, C., and P. Delepelaire. 2004. Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 58:611-647.
57. Zhou, D., and M. A. Apicella. 1996. Plasmids with erythromycin resistance and catechol 2,3-dioxygenase- or beta-galactosidase-encoding gene cassettes for use in Neisseria spp. Gene 171:133-134.
58. Zhu, W., D. J. Hunt, A. R. Richardson, and I. Stojiljkovic. 2000. Use of heme compounds as iron sources by pathogenic neisseriae requires the product of the hemO gene. J. Bacteriol. 182:439-447.