Arginine-specific gingipains (RgpA/RgpB) knockdown modulates neutrophil machinery

References

• Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: Consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. [2018 Jun 1];89(S1):S173–9. doi: 10.1002/JPER.17-0721
   PubMedGoogle Scholar
• Van Winkelhoff AJ, Loos BG, Van Der Reijden WA, et al. Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. J Clinic Periodontology. 2002 Nov;29(11):1023–1028. doi: 10.1034/j.1600-051X.2002.291107.x
   PubMed Web of Science ®Google Scholar
• Holt SC, Ebersole JL. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the ‘red complex’, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000. 2005;38(1):72–122. doi: 10.1111/j.1600-0757.2005.00113.x
   PubMedGoogle Scholar
• Andrian E, Grenier D, Rouabhia M. In vitro models of tissue penetration and destruction by Porphyromonas gingivalis. Infect Immun. 2004 Aug;72(8):4689–4698. doi: 10.1128/IAI.72.8.4689-4698.2004
   PubMed Web of Science ®Google Scholar
• Abusleme L, Dupuy AK, Dutzan N, et al. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J. 2013 May;7(5):1016–1025. doi: 10.1038/ismej.2012.174
   PubMed Web of Science ®Google Scholar
• Hajishengallis G. Immune evasion strategies of Porphyromonas gingivalis. J Oral Biosci. 2011;53(3):233–240. doi: 10.1016/S1349-0079(11)80006-X
   PubMedGoogle Scholar
• Mysak J, Podzimek S, Sommerova P, et al. Porphyromonas gingivalis: Major periodontopathic pathogen overview. J Immunol Res [Internet]. 2014 [cited 2021 Mar 12]; Available from 2014:1–8. Available from: https://pubmed.ncbi.nlm.nih.gov/24741603/
   Web of Science ®Google Scholar
• Berker E, Kantarci A, Hasturk H, et al. Blocking proinflammatory cytokine release modulates peripheral blood mononuclear cell response to porphyromonas gingivalis. J Periodontol. 2013 Sep;84(9):1337–1345. doi: 10.1902/jop.2012.120422
   PubMed Web of Science ®Google Scholar
• Euzebio Alves VT, da Silva HAB, de França BN, et al. Periodontal treatment downregulates protease-activated receptor 2 in human gingival crevicular fluid cells. Infect Immun. 2013 Dec;81(12):4399–4407. doi: 10.1128/IAI.01107-13
   PubMed Web of Science ®Google Scholar
• Grenier D. Inactivation of human serum bactericidal activity by a trypsinlike protease isolated from Porphyromonas gingivalis. Infect Immun. 1992;60(5):1854–1857. doi: 10.1128/iai.60.5.1854-1857.1992
   PubMed Web of Science ®Google Scholar
• Mikolajczyk-Pawlinska J, Travis J, Potempa J. Modulation of interleukin-8 activity by gingipains from porphyromonas gingivalis: Implications for pathogenicity of periodontal disease. FEBS Lett. [1998 Dec 4];440(3):282–286. doi: 10.1016/S0014-5793(98)01461-6
   PubMed Web of Science ®Google Scholar
• Mȩzyk-Kopeć R, Bzowska M, Potempa J, et al. Inactivation of membrane tumor necrosis factor alpha by gingipains from Porphyromonas gingivalis. Infect Immun. 2005 Mar;73(3):1506–1514. doi: 10.1128/IAI.73.3.1506-1514.2005
   PubMed Web of Science ®Google Scholar
• Belibasakis GN, Bostanci N, Hashim A, et al. Regulation of RANKL and OPG gene expression in human gingival fibroblasts and periodontal ligament cells by porphyromonas gingivalis: A putative role of the arg-gingipains. Microb Pathog. 2007 Jul;43(1):46–53. doi: 10.1016/j.micpath.2007.03.001
   PubMed Web of Science ®Google Scholar
• Lourbakos A, Yuan YP, Jenkins AL, et al. Activation of protease-activated receptors by gingipains from porphyromonas gingivalis leads to platelet aggregation: A new trait in microbial pathogenicity. Blood. [2001 Jun 15];97(12):3790–3797. doi: 10.1182/blood.V97.12.3790
   PubMed Web of Science ®Google Scholar
• Bostanci N, Thurnheer T, Aduse-Opoku J, et al. Porphyromonas gingivalis regulates TREM-1 in human polymorphonuclear neutrophils via its gingipains. PLOS ONE. [2013 Oct 4];8(10):75784. doi: 10.1371/journal.pone.0075784
   Web of Science ®Google Scholar
• Popadiak K, Potempa J, Riesbeck K, et al. Biphasic effect of gingipains from porphyromonas gingivalis on the human complement system. The J Immunol. [2007 Jun 1];178(11):7242–7250. doi: 10.4049/jimmunol.178.11.7242
   PubMed Web of Science ®Google Scholar
• Nakayama K. Domain-specific rearrangement between the two arg-gingipain-encoding genes in Porphyromonas gingivalis: possible involvement of nonreciprocal recombination. Microbiol Immunol. 1997;41(3):185–196. doi: 10.1111/j.1348-0421.1997.tb01189.x
   PubMed Web of Science ®Google Scholar
• Curtis MA, Kuramitsu HK, Lantz M, et al. Molecular genetics and nomenclature of proteases of porphyromonas gingivalis. J Periodontal Res. 1999;34(8):464–472. doi: 10.1111/j.1600-0765.1999.tb02282.x
   PubMed Web of Science ®Google Scholar
• Li N, Collyer CA. Gingipains from porphyromonas gingivalis – complex domain structures confer diverse functions. Eur J Microbiol Immunol (Bp). 2011 Mar;1(1):41–58. doi: 10.1556/EuJMI.1.2011.1.7
   PubMedGoogle Scholar
• Chow YC, Yam HC, Gunasekaran B, et al. Implications of porphyromonas gingivalis peptidyl arginine deiminase and gingipain R in human health and diseases. Front Cell Infect Microbiol. 2022;12:987683. doi: 10.3389/fcimb.2022.987683
   PubMed Web of Science ®Google Scholar
• Grenier D, Roy S, Chandad F, et al. Effect of inactivation of the arg- and/or lys-gingipain gene on selected virulence and physiological properties of Porphyromonas gingivalis. Infect Immun. 2003 Aug;71(8):4742–4748. doi: 10.1128/IAI.71.8.4742-4748.2003
   PubMed Web of Science ®Google Scholar
• Tokuda M, Karunakaran T, Duncan M, et al. Role of arg-gingipain a in virulence of porphyromonas gingivalis. Infect Immun. 1998;66(3):1159–1166. doi: 10.1128/IAI.66.3.1159-1166.1998
   PubMed Web of Science ®Google Scholar
• Houle MA, Grenier D, Plamondon P, et al. The collagenase activity of porphyromonas gingivalis is due to arg-gingipain. FEMS Microbiol Lett. [2003 Apr 25];221(2):181–185. doi: 10.1016/S0378-1097(03)00178-2
   PubMed Web of Science ®Google Scholar
• Grayson R, Douglas CWI, Heath J, et al. Activation of human matrix metalloproteinase 2 by gingival crevicular fluid and Porphyromonas gingivalis. J Clin Periodontol. 2003 Jun;30(6):542–550. doi: 10.1034/j.1600-051X.2003.00301.x
   PubMed Web of Science ®Google Scholar
• Gibson FC, Genco CA, Tuomanen EI. Prevention of porphyromonas gingivalis-induced oral bone loss following immunization with gingipain R1. Infect Immun. 2001;69(12):7959–7963. doi: 10.1128/IAI.69.12.7959-7963.2001
   PubMed Web of Science ®Google Scholar
• Wilensky A, Polak D, Houri-Haddad Y, et al. The role of RgpA in the pathogenicity of porphyromonas gingivalis in the murine periodontitis model. J Clin Periodontol. 2013 Oct;40(10):924–932. doi: 10.1111/jcpe.12139
   PubMed Web of Science ®Google Scholar
• Potempa J, Banbula A, Travis J. Role of bacterial proteinases in matrix destruction and modulation of host responses. Periodontol 2000. 2000;24(1):153–192. doi: 10.1034/j.1600-0757.2000.2240108.x
   PubMedGoogle Scholar
• Delima AJ, Van Dyke TE. Origin and function of the cellular components in gingival crevice fluid. Periodontol 2000. 2003;31(1):55–76. doi: 10.1034/j.1600-0757.2003.03105.x
   PubMedGoogle Scholar
• Takeuchi H, Hirano T, Whitmore SE, et al. The serine phosphatase serb of porphyromonas gingivalis suppresses il-8 production by dephosphorylation of NF-κB RelA/p65. PLOS Pathog [Internet]. 2013 Apr [cited 2021 Mar 12];9(4). Available from e1003326. https://pubmed.ncbi.nlm.nih.gov/23637609/
   PubMed Web of Science ®Google Scholar
• Tada H, Sugawara S, Nemoto E, et al. Proteolysis of ICAM-1 on human oral epithelial cells by gingipains. J Dent Res. [2003 Oct 12];82(10):796–801. doi: 10.1177/154405910308201007
   PubMed Web of Science ®Google Scholar
• Kantarci A, Van Dyke TE. Neutrophil-mediated host response to porphyromonas gingivalis. J Int Acad Periodontol. [2002 Oct 1];4(4):119–125.
   PubMedGoogle Scholar
• Teng TS, Ji AL, Ji XY, et al. Neutrophils and immunity: From bactericidal action to being conquered. J Immunol Res [Internet]. 2017 [cited 2021 Mar 12];2017. Available from: https://pubmed.ncbi.nlm.nih.gov/28299345/1–1410.1155/2017/9671604
   PubMed Web of Science ®Google Scholar
• Wingrove JA, DiScipio RG, Chen Z, et al. Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from porphyromonas (bacteroides) gingivalis. J Biol Chem. [1992 Sep 15];267(26):18902–18907. doi: 10.1016/S0021-9258(19)37046-2
   PubMed Web of Science ®Google Scholar
• Guzik K, Potempa J. Friendly fire against neutrophils: Proteolytic enzymes confuse the recognition of apoptotic cells by macrophages. Biochimie. 2008 Feb;90(2):405–415. doi: 10.1016/j.biochi.2007.09.008
   PubMed Web of Science ®Google Scholar
• Guzik K, Bzowska M, Smagur J, et al. A new insight into phagocytosis of apoptotic cells: Proteolytic enzymes divert the recognition and clearance of polymorphonuclear leukocytes by macrophages. Cell Death Differ. 2007 Jan;14(1):171–182. doi: 10.1038/sj.cdd.4401927
   PubMed Web of Science ®Google Scholar
• Kalmar JR, Arnold RR, Warbington ML, et al. Superior leukocyte separation with a discontinuous one-step ficoll-hypaque gradient for the isolation of human neutrophils. J Immunol Methods. [1988 Jun 13];110(2):275–281. doi: 10.1016/0022-1759(88)90115-9
   PubMed Web of Science ®Google Scholar
• Browne RW, Kantarci A, LaMonte MJ, et al. Performance of multiplex cytokine assays in serum and saliva among community-dwelling postmenopausal women. Glogauer M, editor. PLOS ONE. 2013 Apr 5;8(4):e59498. doi: 10.1371/journal.pone.0059498
   PubMed Web of Science ®Google Scholar
• Sochalska M, Potempa J. Manipulation of neutrophils by porphyromonas gingivalis in the development of periodontitis. Front Cell Infect Microbiol. 2017 May 23;7(MAY):197. doi: 10.3389/fcimb.2017.00197
   PubMedGoogle Scholar
• Gibson FC, Savelli J, Van Dyke TE, et al. Gingipain-specific igg in the sera of patients with periodontal disease is necessary for opsonophagocytosis of Porphyromonas gingivalis. J Periodontol. 2005 Oct;76(10):1629–1636. doi: 10.1902/jop.2005.76.10.1629
   PubMed Web of Science ®Google Scholar
• Bryzek D, Ciaston I, Dobosz E, et al. Triggering NETosis via protease-activated receptor (PAR)-2 signaling as a mechanism of hijacking neutrophils function for pathogen benefits. PLOS Pathog [Internet]. 2019 May 1 [cited 2021 Mar 12];15(5). Available from e1007773. https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1007773
   PubMed Web of Science ®Google Scholar
• Potempa J, Pike RN. Corruption of innate immunity by bacterial proteases. J Innate Immun. 2009;1(2):70–87. doi: 10.1159/000181144
   PubMed Web of Science ®Google Scholar
• Wang M, Krauss JL, Domon H, et al. Microbial hijacking of complement-toll-like receptor crosstalk. Sci Signal [Internet]. 2010 Feb 16 [cited 2021 Mar 12];3(109). Available from: https://pubmed.ncbi.nlm.nih.gov/20159852/
   Web of Science ®Google Scholar
• Zeng MY, Miralda I, Armstrong CL, et al. The roles of NADPH oxidase in modulating neutrophil effector responses. Mol Oral Microbiol. 2019 Apr 1;34(2):27–38. doi: 10.1111/omi.12252
   PubMed Web of Science ®Google Scholar
• Jäättela M, Candé C, Kroemer G. Lysosomes and mitochondria in the commitment to apoptosis: A potential role for cathepsin D and AIF. Cell Death Differ. 2004 Feb;11(2):135–136. doi: 10.1038/sj.cdd.4401333
   PubMed Web of Science ®Google Scholar
• Yagi M, Kantarci A, Iwata T, et al. PDK1 regulates chemotaxis in human neutrophils. J Dent Res. 2009 Dec;88(12):1119–1124. doi: 10.1177/0022034509349402
   PubMed Web of Science ®Google Scholar
• Gamonal J, Sanz M, O’Connor A, et al. Delayed neutrophil apoptosis in chronic periodontitis patients. J Clin Periodontol. 2003 Jul;30(7):616–623. doi: 10.1034/j.1600-051X.2003.00350.x
   PubMed Web of Science ®Google Scholar
• Murray DA, Wilton JMA. Lipopolysaccharide from the periodontal pathogen porphyromonas gingivalis prevents apoptosis of hl60-derived neutrophils in vitro. Infect Immun. 2003 Dec;71(12):7232–7235. doi: 10.1128/IAI.71.12.7232-7235.2003
   PubMed Web of Science ®Google Scholar
• Zaric S, Shelburne C, Darveau R, et al. Impaired immune tolerance to porphyromonas gingivalis lipopolysaccharide promotes neutrophil migration and decreased apoptosis. Infect Immun. 2010 Oct;78(10):4151–4156. doi: 10.1128/IAI.00600-10
   PubMed Web of Science ®Google Scholar
• Makkawi H, Hoch S, Burns E, et al. Porphyromonas gingivalis stimulates TLR2-PI3K signaling to escape immune clearance and induce bone resorption independently of MyD88. Front Cell Infect Microbiol [Internet]. 2017 Aug 8 [cited 2021 Mar 12];7(AUG). Available from: https://pubmed.ncbi.nlm.nih.gov/28848717/10.3389/fcimb.2017.00359
   PubMedGoogle Scholar
• Smalley JW, Olczak T. Heme acquisition mechanisms of porphyromonas gingivalis – strategies used in a polymicrobial community in a heme-limited host environment. Mol Oral Microbiol. 2017 Feb 1;32(1):1–23. doi: 10.1111/omi.12149
   PubMed Web of Science ®Google Scholar
• Abdi K, Chen T, Klein BA, et al. Mechanisms by which porphyromonas gingivalis evades innate immunity. PLoS One [Internet]. 2017 Aug 1 [cited 2021 Mar 12];12(8). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5542538/
   Web of Science ®Google Scholar
• Zhang J, Dong H, Kashket S, et al. IL-8 degradation by porphyromonas gingivalis proteases. Microb Pathog. 1999;26(5):275–280. doi: 10.1006/mpat.1998.0277
   PubMed Web of Science ®Google Scholar
• Stathopoulou PG, Benakanakere MR, Galicia JC, et al. The host cytokine response to porphyromonas gingivalis is modified by gingipains. Oral Microbiol And Immunol. 2009 Feb;24(1):11–17. doi: 10.1111/j.1399-302X.2008.00467.x
   PubMedGoogle Scholar
• Calkins CC, Platt K, Potempa J, et al. Inactivation of tumor necrosis factor-α by proteinases (gingipains) from the periodontal pathogen, porphyromonas gingivalis. Implications of immune evasion. J Biol Chem. 1998 Mar 20;273(12):6611–6614. doi: 10.1074/jbc.273.12.6611
   PubMed Web of Science ®Google Scholar