Gallium(III), cobalt(III) and copper(II) protoporphyrin IX exhibit antimicrobial activity against Porphyromonas gingivalis by reducing planktonic and bioWlm growth and invasion of host epithelial cells

Archives of Microbiology

Volumn 194, Issue 8, 2012, Pages 719-724

  Olczak, Teresa ^a   Maszczak Seneczko, Dorota ^a   Smalley, John W ^b   Olczak, Mariusz ^a  

^a UNIVERSITY OF WROC AW   (Poland)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

BioWlm; Epithelial cell invasion; Heme; HmuY; Non iron metalloporphyrins; Porphyromonas gingivalis

Indexed keywords

BACTERIAL PROTEIN; COBALT; CUPRIC ION; DEUTEROPORPHYRIN IX; FERRIC ION; GALLIUM; HEME; MESOPORPHYRIN; METALLOPORPHYRIN; PROTEIN HMUR; PROTEIN HMUY; PROTOPORPHYRIN; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIUM MUTANT; BIOACCUMULATION; BIOFILM; CELL ADHESION; CELL GROWTH; CELL INVASION; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; DRUG TARGETING; EPITHELIUM CELL; HELA CELL; HOST CELL; HUMAN; HUMAN CELL; NONHUMAN; PLANKTON; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANTI-INFECTIVE AGENTS; BIOFILMS; COBALT; COPPER; EPITHELIAL CELLS; FERRIC COMPOUNDS; GALLIUM; HELA CELLS; HUMANS; MESOPORPHYRINS; METALLOPORPHYRINS; PORPHYROMONAS GINGIVALIS;

BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS;

EID: 84865968828     PISSN: 03028933     EISSN: 1432072X     Source Type: Journal    
DOI: 10.1007/s00203-012-0804-3     Document Type: Article

References (31)

1. Bozja J, Yi K, Shafer WM, Stojiljkovic I (2004) Porphyrin-based compounds exert antibacterial action against the sexually transmitted pathogens Neisseria gonorrhoeae and Haemophilus ducreyi. Int J Antimicrob Agents 24:578-584
2. Bramanti TE, Holt SC (1991) Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50. J Bacteriol 173:7330-7339
3. Craig RG, Yip YK, So MK, Boylan RJ, Socransky SS, HaVajee AD (2003) Relationship of destructive periodontal disease to the acute-phase response. J Periodontol 74:1007-1016
4. Curtis MA, GriYths GS, Price SJ, Coulthurst SK, Johnson NW (1988) Detection of high-risk groups and individuals for periodontal diseases. Clinical assessment of the periodontium. J Clin Periodontol 15:628-632
5. Fuller MD, Caldwell DR (1982) Tetrapyrrole utilization by Bacteroides fragilis. Can J Microbiol 28:1304-1310
6. Gao JL, Nguyen KA, Hunter N (2010) Characterization of a hemophore- like protein from Porphyromonas gingivalis. J Biol Chem 285:40028-40038
7. Graves DT, Jiang Y, Genco CA (2000) Periodontal disease: bacterial virulence factors, host response and impact on systemic health. Curr Opin Infect Dis 13:227-232
8. Krewulak KD, Vogel HJ (2008) Structural biology of bacterial iron uptake. Biochim Biophys Acta 1778:1781-1804
9. Kuboniwa M, Hendrickson EL, Xia Q, Wang T, Xie H, Hackett M, Lamont RJ (2009) Proteomics of Porphyromonas gingivalis within a model oral microbial community. BMC Microbiol 9:98
10. Lamont RJ, Chan A, Belton CM, Izutsu KT, Vasel D, Weinberg A (1995) Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 63:3878-3885
11. Leon R, Silva N, Ovalle A, Chaparro A, Ahumada A, Gajardo M, Martinez M, Gamonal J (2007) Detection of Porphyromonas gingivalis in the amniotic Xuid in pregnant women with a diagnosis of threatened premature labor. J Periodontol 78:1249-1255
12. Marsh PD (2004) Dental plaque as a microbial bioWlm. Caries Res 38:204-211
13. McCall DR, Caldwell DR (1977) Tetrapyrrole utilization by Bacteroides ruminicola. J Bacteriol 131:809-814
14. Meurman JH, Sanz M, Janket SJ (2004) Oral health, atherosclerosis, and cardiovascular disease. Crit Rev Oral Biol Med 15:403-413
15. Nakagawa I, Inaba H, Yamamura T, Kato T, Kawai S, Ooshima T, Amano A (2006) Invasion of epithelial cells and proteolysis of cellular focal adhesion components by distinct types of Porphyromonas gingivalis Wmbriae. Infect Immun 74:3773-3782
16. Olczak T, Dixon DW, Genco CA (2001) Binding speciWcity of the Porphyromonas gingivalis heme and hemoglobin receptor HmuR, gingipain K, and gingipain R1 for heme, porphyrins, and metalloporphyrins. J Bacteriol 183:5599-5608
17. Olczak T, Simpson W, Liu X, Genco CA (2005) Iron and heme utilization in Porphyromonas gingivalis. FEMS Microbiol Rev 29:119-144
18. 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 183:197-210
19. Olczak T, Wojtowicz H, Ciuraszkiewicz J, Olczak M (2010) Species speciWcity, surface exposure, protein expression, immunogenicity, and participation in bioWlm formation of Porphyromonas gingivalis HmuY. BMC Microbiol 10:134
20. Paramaesvaran M, Nguyen KA, Caldon E, McDonald JA, Najdi S, Gonzaga G, Langley DB, DeCarlo A, Crossley MJ, Hunter N, Collyer CA (2003) Porphyrin-mediated cell surface heme capture from hemoglobin by Porphyromonas gingivalis. J Bacteriol 185:2528-2537
21. Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G (2004) Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. InXammation 28:311-318
22. Roth GA, Ankersmit HJ, Brown VB, Papapanou PN, Schmidt AM, Lalla E (2007) Porphyromonas gingivalis infection and cell death in human aortic endothelial cells. FEMS Microbiol Lett 272:106-113
23. Smalley JW, Birss AJ, Silver J (2000) The periodontal pathogen Porphyromonas gingivalis harnesses the chemistry of the μ-oxo bishaem of iron protoporphyrin IX to protect against hydrogen peroxide. FEMS Microbiol Lett 183:159-164
24. Smalley JW, Silver J, Birss AJ, Withnall R, Titler PJ (2003) The heam pigment of the oral anaerobes Prevotella nigrescens and Prevotella intermedia is composed of iron(III) protoporphyrin IX in the monomeric form. Microbiology 149:1711-1718
25. Smalley JW, Byrne DP, Birss AJ, Wojtowicz H, Sroka A, Potempa J, Olczak T (2011) HmuY haemophore and gingipain proteases constitute a unique syntrophic system of haem acquisition by Porphyromonas gingivalis. PLoS ONE 6(2):e17182
26. Stojiljkovic I, Kumar V, Srinivasan N (1999) Non-iron metalloporphyrins: potent antibacterial compounds that exploit haem/Hb uptake systems of pathogenic bacteria. Mol Microbiol 31:429-442
27. Wojaczynski J, Wojtowicz H, Bielecki M, Olczak M, Smalley JW, Latos- Grazynski L, Olczak T (2011) Iron(III) mesoporphyrin IX and iron(III) deuteroporphyrin IX bind to the Porphyromonas gingivalis HmuY hemophore. Biochem Biophys Res Commun 411:299-304
28. Wojtowicz H, Guevara T, Tallant C, Olczak M, Sroka A, Potempa J, Sola M, Olczak T, Gomis-Ruth FX (2009a) Unique structure and stability of HmuY, a novel heme-binding protein of Porphyromonas gingivalis. PLoS Pathog 5(5):e100041
29. Wojtowicz H, Wojaczynski J, Olczak M, Kroliczewski J, Latos-Grazynski L, Olczak T (2009b) Heme environment in HmuY, theheme-binding protein of Porphyromonas gingivalis. Biochem Biophys Res Commun 383:178-182
30. Yilmaz O, Verbeke P, Lamont RJ, Ojcius DM (2006) Intercellular spreading of Porphyromonas gingivalis infection in primary gingival epithelial cells. Infect Immun 74:703-710
31. Yukitake H, Naito M, Sato K, Shoji M, Ohara N, Yoshimura M, Sakai E, Nakayama K (2011) EVects of non-iron metalloporphyrins on growth and gene expression of Porphyromonas gingivalis. Microbiol Immunol 55:141-153