HcpR of Porphyromonas gingivalis is required for growth under nitrosative stress and survival within host cells

Infection and Immunity

Volumn 80, Issue 9, 2012, Pages 3319-3331

  Lewis, Janina P ^a   Yanamandra, Sai S ^a   Anaya Bergman, Cecilia ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL ENZYME; HEMIN; HYBRID CLUSTER PROTEIN R; HYBRID PROTEIN; NITRIC OXIDE; NITRITE; OXIDOREDUCTASE; RECOMBINANT DNA; REGULATOR PROTEIN; S NITROSOGLUTATHIONE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CELL SURVIVAL; CONTROLLED STUDY; ESCHERICHIA COLI; GENE INSERTION; HOST CELL; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; NITROSATIVE STRESS; NONHUMAN; NUCLEOTIDE SEQUENCE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATOR GENE; REGULATORY MECHANISM; UPREGULATION; WILD TYPE;

CELLS, CULTURED; CYTOPLASM; DNA-BINDING PROTEINS; ENDOTHELIAL CELLS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; IRON-SULFUR PROTEINS; MICROARRAY ANALYSIS; MICROBIAL VIABILITY; MUTAGENESIS, INSERTIONAL; NITROSATION; NITROSO COMPOUNDS; OXIDOREDUCTASES; PORPHYROMONAS GINGIVALIS; STRESS, PHYSIOLOGICAL; TRANS-ACTIVATORS;

EID: 84867609567     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00561-12     Document Type: Article

References (62)

1. Allaker RP, Silva Mendez LS, Hardie JM, Benjamin N. 2001. Antimicrobial effect of acidified nitrite on periodontal bacteria. Oral Microbiol. Immunol. 16:253-256.
2. Altschul SF, et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Aragao D, Mitchell EP, Frazao CF, Carrondo MA, Lindley PF. 2008. Structural and functional relationships in the hybrid cluster protein family: structure of the anaerobically purified hybrid cluster protein from Desulfovibrio vulgaris at 1.35 A resolution. Acta Crystallogr. D Biol. Crystallogr. 64:665-674.
4. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201.
5. Beck JD, Offenbacher S, Williams R, Gibbs P, Garcia R. 1998. Periodontitis: a risk factor for coronary heart disease? Ann. Periodontol. 3:127-141.
6. Bordoli L, et al. 2009. Protein structure homology modeling using SWISS-MODEL workspace. Nat. Protoc. 4:1-13.
7. Boutrin MC, Wang C, Aruni W, Li X, Fletcher HM. 2012. Nitric oxide stress resistance in Porphyromonas gingivalis is mediated by a putative hydroxylamine reductase. J. Bacteriol. 194:1582-1592.
8. Cabello P, et al. 2004. Hydroxylamine assimilation by Rhodobacter capsulatus E1F1. requirement of the hcp gene (hybrid cluster protein) located in the nitrate assimilation nas gene region for hydroxylamine reduction. J. Biol. Chem. 279:45485-45494.
9. Cadby IT, Busby SJ, Cole JA. 2011. An HcpR homologue from Desulfovibrio desulfuricans and its possible role in nitrate reduction and nitrosative stress. Biochem. Soc. Trans. 39:224-229.
10. Castiglione N, Rinaldo S, Giardina G, Cutruzzola F. 2009. The transcription factor DNR from Pseudomonas aeruginosa specifically requires nitric oxide and haem for the activation of a target promoter in Escherichia coli. Microbiology 155:2838-2844.
11. Cooper SJ, Garner CD, Hagen WR, Lindley PF, Bailey S. 2000. Hybridcluster protein (HCP) from Desulfiovibrio vulgaris (Hildenborough) at 1.6 A resolution. Biochemistry 39:15044-15054.
12. Das Gupta T, Bandyopadhyay B, Das Gupta SK. 2008. Modulation of DNA-binding activity of Mycobacterium tuberculosis HspR by chaperones. Microbiology 154:484-490.
13. Dorn BR, Burks JN, Seifert KN, Progulske-Fox A. 2000. Invasion of endothelial and epithelial cells by strains of Porphyromonas gingivalis. FEMS Microbiol. Lett. 187:139-144.
14. Dorn BR, Dunn WA, Jr, Progulske-Fox A. 2001. Porphyromonas gingivalis traffics to autophagosomes in human coronary artery endothelial cells. Infect. Immun. 69:5698-5708.
15. Ezzo PJ, Cutler CW. 2003. Microorganisms as risk indicators for periodontal disease. Periodontol. 2000 32:24-35.
16. Fang FC. 1997. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 99: 2818-2825.
17. Filenko N, et al. 2007. The NsrR regulon of Escherichia coli K-12 includes genes encoding the hybrid cluster protein and the periplasmic, respiratory nitrite reductase. J. Bacteriol. 189:4410-4417.
18. Filenko NA, Browning DF, Cole JA. 2005. Transcriptional regulation of a hybrid cluster (prismane) protein. Biochem. Soc. Trans. 33:195-197.
19. Fletcher HM, et al. 1995. Virulence of a Porphyromonas gingivalis W83 mutant defective in the prtH gene. Infect. Immun. 63:1521-1528.
20. Giardina G, Rinaldo S, Castiglione N, Caruso M, Cutruzzola F. 2009. A dramatic conformational rearrangement is necessary for the activation of DNR from Pseudomonas aeruginosa. Crystal structure of wild-type DNR. Proteins 77:174-180.
21. Giardina G, et al. 2008. NO sensing in Pseudomonas aeruginosa: structure of the transcriptional regulator DNR. J. Mol. Biol. 378:1002-1015.
22. Gostick DO, et al. 1999. Two operons that encode FNR-like proteins in Lactococcus lactis. Mol. Microbiol. 31:1523-1535.
23. Green J, Scott C, Guest JR. 2001. Functional versatility in the CRP-FNR superfamily of transcription factors: FNR and FLP. Adv. Microb. Physiol. 44:1-34.
24. Hajishengallis G, et al. 2011. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 10:497-506.
25. Hammes WP. 2012. Metabolism of nitrate in fermented meats: the characteristic feature of a specific group of fermented foods. Food Microbiol. 29:151-156.
26. Haveman SA, Greene EA, Stilwell CP, Voordouw JK, Voordouw G. 2004. Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris Hildenborough by nitrite. J. Bacteriol. 186:7944-7950.
27. He J, et al. 2006. Role of Porphyromonas gingivalis FeoB2 in metal uptake and oxidative stress protection. Infect. Immun. 74:4214-4223.
28. Huber R, et al. 1986. Thermatoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90oC. Arch. Microbiol. 144:324-333.
29. Kern M, Volz J, Simon J. 2011. The oxidative and nitrosative stress defence network of Wolinella succinogenes: cytochrome c nitrite reductase mediates the stress response to nitrite, nitric oxide, hydroxylamine and hydrogen peroxide. Environ. Microbiol. 13:2478-2494.
30. Kiley PJ, Beinert H. 1998. Oxygen sensing by the global regulator, FNR: the role of the iron-sulfur cluster. FEMS Microbiol. Rev. 22:341-352.
31. Lamont RJ, Jenkinson HF. 1998. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62: 1244-1263.
32. Lewis JP, Iyer D, Anaya-Bergman C. 2009. Adaptation of Porphyromonas gingivalis to microaerophilic conditions involves increased consumption of formate and reduced utilization of lactate. Microbiology 155:3758-3774.
33. Lewis JP, Plata K, Yu F, Rosato A, Anaya C. 2006. Transcriptional organization, regulation and role of the Porphyromonas gingivalis W83 hmu haemin-uptake locus. Microbiology 152:3367-3382.
34. Lundberg JO, Weitzberg E, Cole JA, Benjamin N. 2004. Nitrate, bacteria and human health. Nat. Rev. Microbiol. 2:593-602.
35. MacMicking JD, et al. 1995. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81: 641-650.
36. Mazoch J, Kucera I. 2002. Control of gene expression by FNR-like proteins in facultatively anaerobic bacteria. Folia Microbiol. (Praha) 47: 95-103.
37. Meuric V, Rouillon A, Chandad F, Bonnaure-Mallet M. 2010. Putative respiratory chain of Porphyromonas gingivalis. Future Microbiol. 5:717-734.
38. Munch R, et al. 2005. Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21: 4187-4189.
39. Mydel P, et al. 2006. Roles of the host oxidative immune response and bacterial antioxidant rubrerythrin during Porphyromonas gingivalis infection. PLoS Pathog. 2:e76. doi:10.1371/journal.ppat.0020076.
40. Nathan C. 1995. Natural resistance and nitric oxide. Cell 82:873-876.
41. Nelson KE, et al. 1999. Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399: 323-329.
42. Nelson KE, et al. 2003. Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J. Bacteriol. 185:5591-5601.
43. Olczak T, Sroka A, Potempa J, Olczak M. 2008. Porphyromonas gingivalis HmuY and HmuR: further characterization of a novel mechanism of heme utilization. Arch. Microbiol. 189:197-210.
44. Palmerini CA, Palombari R, Perito S, Arienti G. 2003. NO synthesis in human saliva. Free Radic. Res. 37:29-31.
45. Rinaldo S, Giardina G, Brunori M, Cutruzzola F. 2006. N-oxide sensing and denitrification: the DNR transcription factors. Biochem. Soc. Trans. 34:185-187.
46. Rodionov DA, Dubchak IL, Arkin AP, Alm EJ, Gelfand MS. 2005. Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLoS Comput. Biol. 1:e55. doi: 10.1371/journal.pcbi.0010055.
47. Schwede T, Kopp J, Guex N, Peitsch MC. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31: 3381-3385.
48. Seth D, Hausladen A, Wang YJ, Stamler JS. 2012. Endogenous protein S-Nitrosylation in E. coli: regulation by OxyR. Science 336:470-473.
49. Singh A, et al. 2011. The capsule of Porphyromonas gingivalis leads to a reduction in the host inflammatory response, evasion of phagocytosis, and increase in virulence. Infect. Immun. 79:4533-4542.
50. Smalley JW, et al. 2011. HmuY haemophore and gingipain proteases constitute a unique syntrophic system of haem acquisition by Porphyromonas gingivalis. PLoS One 6:e17182. doi:10.1371/journal-pone.0017182.
51. Spiro S. 2006. Nitric oxide-sensing mechanisms in Escherichia coli. Biochem. Soc. Trans. 34:200-202.
52. Spraggon G, et al. 2004. On the use of DXMS to produce more crystallizable proteins: structures of the T. maritima proteins TM0160 and TM1171. Protein Sci. 13:3187-3199.
53. Stewart GR, et al. 2002. Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 148: 3129-3138.
54. Sztukowska M, Bugno M, Potempa J, Travis J, Kurtz DM, Jr. 2002. Role of rubrerythrin in the oxidative stress response of Porphyromonas gingivalis. Mol. Microbiol. 44:479-488.
55. Ueshima J, et al. 2003. Purification, gene cloning, gene expression, and mutants of Dps from the obligate anaerobe Porphyromonas gingivalis. Infect. Immun. 71:1170-1178.
56. van den Berg WA, Hagen WR, van Dongen WM. 2000. The hybridcluster protein ('prismane protein') from Escherichia coli. Characterization of the hybrid-cluster protein, redox properties of the [2Fe-2S] and [4Fe-2S-2O] clusters and identification of an associated NADH oxidoreductase containing FAD and [2Fe-2S]. Eur. J. Biochem. 267:666-676.
57. Vollack KU, Hartig E, Korner H, Zumft WG. 1999. Multiple transcription factors of the FNR family in denitrifying Pseudomonas stutzeri: characterization of four fnr-like genes, regulatory responses and cognate metabolic processes. Mol. Microbiol. 31:1681-1694.
58. Wolfe MT, Heo J, Garavelli JS, Ludden PW. 2002. Hydroxylamine reductase activity of the hybrid cluster protein from Escherichia coli. J. Bacteriol. 184:5898-5902.
59. Xia DS, Liu Y, Zhang CM, Yang SH, Wang SL. 2006. Antimicrobial effect of acidified nitrate and nitrite on six common oral pathogens in vitro. Chin Med. J. (Engl.) 119:1904-1909.
60. Xu J, Verstraete W. 2001. Evaluation of nitric oxide production by lactobacilli. Appl. Microbiol. Biotechnol. 56:504-507.
61. Yanamandra SS, Sarrafee SS, Anaya-Bergman C, Jones K, Lewis JP. 2012. Role of the Porphyromonas gingivalis extracytoplasmic function sigma factor, SigH. Mol. Oral Microbiol. 27:202-219.
62. Yilmaz O. 2008. The chronicles of Porphyromonas gingivalis: the microbium, the human oral epithelium and their interplay. Microbiology 154: 2897-2903.