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Structure determination and analysis of a haemolytic gingipain adhesin domain from Porphyromonas gingivalis.

Li N, Yun P, Nadkarni MA, Ghadikolaee NB, Nguyen KA, Lee M, Hunter N, Collyer CA
Mol Microbiol 76 861-73 (2010)
Cited: 22 times
EuropePMC logo PMID: 20233299

Abstract

Porphyromonas gingivalis is an obligately anaerobic bacterium recognized as an aetiological agent of adult periodontitis. P. gingivalis produces cysteine proteinases, the gingipains. The crystal structure of a domain within the haemagglutinin region of the lysine gingipain (Kgp) is reported here. The domain was named K2 as it is the second of three homologous structural modules in Kgp. The K2 domain structure is a 'jelly-roll' fold with two anti-parallel beta-sheets. This fold topology is shared with adhesive domains from functionally diverse receptors such as MAM domains, ephrin receptor ligand binding domains and a number of carbohydrate binding modules. Possible functions of K2 were investigated. K2 induced haemolysis of erythrocytes in a dose-dependent manner that was augmented by the blocking of anion transport. Further, cysteine-activated arginine gingipain RgpB, which degrades glycophorin A, sensitized erythrocytes to the haemolytic effect of K2. Cleaved K2, similar to that found in extracted Kgp, lacks the haemolytic activity indicating that autolysis of Kgp may be a staged process which is artificially enhanced by extraction of the protein. The data indicate a functional role for K2 in the integrated capacity conferred by Kgp to enable the porphyrin auxotroph P. gingivalis to capture essential haem from erythrocytes.

Reviews - 3km5 mentioned but not cited (1)

  1. Gingipains from Porphyromonas gingivalis - Complex domain structures confer diverse functions. Li N, Collyer CA. Eur J Microbiol Immunol (Bp) 1 41-58 (2011)

Articles - 3km5 mentioned but not cited (2)

  1. New structural and functional contexts of the Dx[DN]xDG linear motif: insights into evolution of calcium-binding proteins. Rigden DJ, Woodhead DD, Wong PW, Galperin MY. PLoS One 6 e21507 (2011)
  2. The lysine gingipain adhesin domains from Porphyromonas gingivalis interact with erythrocytes and albumin: Structures correlate to function. Ganuelas LA, Li N, Yun P, Hunter N, Collyer CA. Eur J Microbiol Immunol (Bp) 3 152-162 (2013)


Reviews citing this publication (4)

  1. Dichotomy of gingipains action as virulence factors: from cleaving substrates with the precision of a surgeon's knife to a meat chopper-like brutal degradation of proteins. Guo Y, Nguyen KA, Potempa J. Periodontol 2000 54 15-44 (2010)
  2. Calcium binding proteins and calcium signaling in prokaryotes. Domínguez DC, Guragain M, Patrauchan M. Cell Calcium 57 151-165 (2015)
  3. Type IX secretion: the generation of bacterial cell surface coatings involved in virulence, gliding motility and the degradation of complex biopolymers. Veith PD, Glew MD, Gorasia DG, Reynolds EC. Mol Microbiol 106 35-53 (2017)
  4. Heme acquisition mechanisms of Porphyromonas gingivalis - strategies used in a polymicrobial community in a heme-limited host environment. Smalley JW, Olczak T. Mol Oral Microbiol 32 1-23 (2017)

Articles citing this publication (15)

  1. Structure and mechanism of cysteine peptidase gingipain K (Kgp), a major virulence factor of Porphyromonas gingivalis in periodontitis. de Diego I, Veillard F, Sztukowska MN, Guevara T, Potempa B, Pomowski A, Huntington JA, Potempa J, Gomis-Rüth FX. J Biol Chem 289 32291-32302 (2014)
  2. Both the unique and repeat regions of the Porphyromonas gingivalis hemagglutin A are involved in adhesion and invasion of host cells. Bélanger M, Kozarov E, Song H, Whitlock J, Progulske-Fox A. Anaerobe 18 128-134 (2012)
  3. Porphyromonas gingivalis Uses Specific Domain Rearrangements and Allelic Exchange to Generate Diversity in Surface Virulence Factors. Dashper SG, Mitchell HL, Seers CA, Gladman SL, Seemann T, Bulach DM, Chandry PS, Cross KJ, Cleal SM, Reynolds EC. Front Microbiol 8 48 (2017)
  4. Pyocyanina contributory factor in haem acquisition and virulence enhancement of Porphyromonas gingivalis in the lung [corrected]. Benedyk M, Byrne DP, Glowczyk I, Potempa J, Olczak M, Olczak T, Smalley JW. PLoS One 10 e0118319 (2015)
  5. Neutrophils alter epithelial response to Porphyromonas gingivalis in a gingival crevice model. Bondy-Carey JL, Galicia J, Bagaitkar J, Potempa JS, Potempa B, Kinane DF, Veillard F, Scott DA. Mol Oral Microbiol 28 102-113 (2013)
  6. The modular structure of haemagglutinin/adhesin regions in gingipains of Porphyromonas gingivalis. Li N, Yun P, Jeffries CM, Langley D, Gamsjaeger R, Church WB, Hunter N, Collyer CA. Mol Microbiol 81 1358-1373 (2011)
  7. An early report: a modified porphyrin-linked metronidazole targeting intracellular Porphyromonas gingivalis in cultured oral epithelial cells. Ye P, Chang J, Foo LF, Yap BC. Int J Oral Sci 9 167-173 (2017)
  8. Isolation of a variant Porphyromonas sp. from polymicrobial infections in central bearded dragons (Pogona vitticeps). Bemis DA, Greenacre CB, Bryant MJ, Jones RD, Kania SA. J Vet Diagn Invest 23 99-104 (2011)
  9. The association between clinical periodontal parameters and free haem concentration within the gingival crevicular fluid: a pilot study. Liu LY, McGregor N, Wong BK, Butt H, Darby IB. J Periodontal Res 51 86-94 (2016)
  10. Three/four-dimensional (3D/4D) microscopic imaging and processing in clinical dental research. Ye P, Yu H, Houshmandi M. BMC Oral Health 16 84 (2016)
  11. In Situ Raman Study of Neurodegenerated Human Neuroblastoma Cells Exposed to Outer-Membrane Vesicles Isolated from Porphyromonas gingivalis. Pezzotti G, Adachi T, Imamura H, Bristol DR, Adachi K, Yamamoto T, Kanamura N, Marin E, Zhu W, Kawai T, Mazda O, Kariu T, Waku T, Nichols FC, Riello P, Rizzolio F, Limongi T, Okuma K. Int J Mol Sci 24 13351 (2023)
  12. Structural characterization of a prolyl aminodipeptidase (PepX) from Lactobacillus helveticus. Ojennus DD, Bratt NJ, Jones KL, Juers DH. Acta Crystallogr F Struct Biol Commun 75 625-633 (2019)
  13. Prediction of virulence factors using bioinformatics approaches. Chaudhuri R, Ramachandran S. Methods Mol Biol 1184 389-400 (2014)
  14. The K1K2 region of Lys-gingipain of Porphyromonas gingivalis blocks induction of HLA expression by gamma interferon. Yun PL, Li N, Collyer CA, Hunter N. Infect Immun 80 3733-3741 (2012)
  15. TrkA serves as a virulence modulator in Porphyromonas gingivalis by maintaining heme acquisition and pathogenesis. Zou R, Zhao L, Shen D, Wu Y. Front Cell Infect Microbiol 12 1012316 (2022)


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