Low-Abundance Biofilm Species Orchestrates Inflammatory Periodontal Disease through the Commensal Microbiota and Complement
Open accessAbstract
Porphyromonas gingivalis is a low-abundance oral anaerobic bacterium implicated in periodontitis, a polymicrobial inflammatory disease, and the associated systemic conditions. However, the mechanism by which P. gingivalis contributes to inflammation and disease has remained elusive. Here we show that P. gingivalis, at very low colonization levels, triggers changes to the amount and composition of the oral commensal microbiota leading to inflammatory periodontal bone loss. The commensal microbiota and complement were both required for P. gingivalis-induced bone loss, as germ-free mice or conventionally raised C3a and C5a receptor-deficient mice did not develop bone loss after inoculation with P. gingivalis. These findings demonstrate that a single, low-abundance species can disrupt host-microbial homeostasis to cause inflammatory disease. The identification and targeting of similar low-abundance pathogens with community-wide impact may be important for treating inflammatory diseases of polymicrobial etiology.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Studies using germ-free mice have demonstrated the role of diabetes in disrupting the equilibrium of the oral microbiota and confirmed the role of the oral microbiota in periodontal disease pathogenesis.
“Studies using germ‐free mice have also been employed in the context of the oral microbiome, demonstrating the role of diabetes in disrupting the equilibrium of the oral microbiota50 and confirming the role of the oral microbiota in periodontal disease pathogenesis.51, 52”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [51]
Diseased periodontal tissues additionally store pro-inflammatory mediators associated with periodontitis.
“Diseased periodontal tissues additionally stores pro‐inflammatory mediators associated with periodontitis.51, 183, 202”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [51]
The importance of commensal species to pathogenesis is further demonstrated by the requirement for commensal microbial communities in the instigation of disease by periodontal pathogens.
“The importance of commensal species to pathogenesis is further demonstrated by the requirement for commensal microbial communities in the instigation of disease by periodontal pathogens.51, 52”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [51]
The integration of periodontal pathogens, even at low abundance, is able to alter the composition of the microbiota and results in destruction of periodontal tissues by inflammatory processes that they induce.
“The integration of periodontal pathogens, even at low abundance, is able to alter the composition of the microbiota and results in destruction of periodontal tissues by inflammatory processes that they induce.51”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [51]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Pihlstrom, B. L., Michalowicz, B. S., & Johnson, N. W. (2005) · The Lancet · doi:10.1016/s0140-6736(05)67728-8 · Cited by 3,718 · see citing works
Complement: a key system for immune surveillance and homeostasis
Ricklin, D., Hajishengallis, G., Yang, K., & Lambris, J. D. (2010) · Nature Immunology · doi:10.1038/ni.1923 · Cited by 3,654 · cited 7× · see citing works
“The C3aR requirement for the P. gingivalis effect on the oral microbiota and bone loss may be related to its synergistic interactions with C5aR that include reciprocal augmentation of receptor expression (Ricklin et al., 2010).”
BackgroundInfluentialSelf-citationGrice, E. A., & Segre, J. A. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2537 · Cited by 3,143 · see citing works
Challenges in the Quest for Keystones
Power, M. E., Tilman, D., Estes, J. A., Menge, B. A., Bond, W. J., Mills, L. S., Daily, G., Castilla, J. C., Lubchenco, J., & Paine, R. T. (1996) · BioScience · doi:10.2307/1312990 · Cited by 2,018 · see citing works
Periodontitis: a polymicrobial disruption of host homeostasis
Darveau, R. P. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2337 · Cited by 1,688 · see citing works
Self-citationImmune adaptations that maintain homeostasis with the intestinal microbiota
Hooper, L. V., & Macpherson, A. J. (2010) · Nature reviews. Immunology · doi:10.1038/nri2710 · Cited by 1,455 · see citing works
Treatment of periodontitis and endothelial function
Tonetti, M. S., D'Aiuto, F., Nibali, L., Donald, A., Storry, C., Parkar, M., Suvan, J., Hingorani, A. D., Vallance, P., & Deanfield, J. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa063186 · Cited by 1,326 · see citing works
Lupp, C., Robertson, M. L., Wickham, M. E., Sekirov, I., Champion, O. L., Gaynor, E. C., & Finlay, B. B. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.06.010 · Cited by 1,310 · see citing works
Complement regulators and inhibitory proteins
Zipfel, P. F., & Skerka, C. (2009) · Nature reviews. Immunology · doi:10.1038/nri2620 · Cited by 1,268 · see citing works
Stecher, B., Robbiani, R., Walker, A. W., Westendorf, A. M., Barthel, M., Kremer, M., Chaffron, S., Macpherson, A. J., Buer, J., Parkhill, J., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050244 · Cited by 1,048 · see citing works
Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice
Daley, J. M., Thomay, A. A., Connolly, M. D., Reichner, J. S., & Albina, J. E. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.0407247 · Cited by 1,047 · see citing works
Garrett, W. S., Gallini, C. A., Yatsunenko, T., Michaud, M., DuBois, A., Delaney, M. L., Punit, S., Karlsson, M., Bry, L., Glickman, J. N., et al. (2010) · Cell Host & Microbe · doi:10.1016/j.chom.2010.08.004 · Cited by 788 · see citing works
Modulation of the antitumor immune response by complement
Markiewski, M. M., DeAngelis, R. A., Benencia, F., Ricklin-Lichtsteiner, S. K., Koutoulaki, A., Gerard, C. J., Coukos, G., & Lambris, J. D. (2008) · Nature Immunology · doi:10.1038/ni.1655 · Cited by 770 · see citing works
Self-citationGut microbiome-host interactions in health and disease
Kinross, J. K., Darzi, A. W., & Nicholson, J. K. (2011) · Genome Medicine · doi:10.1186/gm228 · Cited by 685 · see citing works
Innate and Adaptive Immunity Cooperate Flexibly to Maintain Host-Microbiota Mutualism
Slack, E. M. C., Hapfelmeier, S., Stecher, B., Velykoredko, Y., Stoel, M., Lawson, M. A., Geuking, M. B., Beutler, B., Tedder, T. F., Hardt, W., et al. (2009) · Science · doi:10.1126/science.1172747 · Cited by 503 · see citing works
Periodontal Microbiota and Carotid Intima-Media Thickness
Desvarieux, M., Demmer, R. T., Rundek, T., Boden-Albala, B. M., Jacobs, D. R., Sacco, R. L., & Papapanou, P. N. (2005) · Circulation · doi:10.1161/01.cir.0000154582.37101.15 · Cited by 489 · see citing works
Bloom, S. M., Bijanki, V. N., Nava, G. M., Sun, L., Malvin, N. P., Donermeyer, D. L., Dunne, W. M., Allen, P. M., & Stappenbeck, T. S. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.04.009 · Cited by 488 · see citing works
Implantation of Bacteroides gingivalis in Nonhuman Primates Initiates Progression of Periodontitis
Holt, S. C., Ebersole, J. L., Felton, J. R., Brunsvold, M. A., & Kornman, K. S. (1988) · Science · doi:10.1126/science.3336774 · Cited by 464 · see citing works
Relative Contribution of LFA-1 and Mac-1 to Neutrophil Adhesion and Migration
Ding, Z., Babensee, J. E., Simon, S. I., Lu, H., Perrard, J. L., Bullard, D. C., Dai, X. Y., Bromley, S. K., Dustin, M. L., Entman, M. L., et al. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.9.5029 · Cited by 407 · see citing works
The use of rodent models to investigate host–bacteria interactions related to periodontal diseases
Graves, D. T., Fine, D. H., Teng, Y. A., Dyke, T. E. V., & Hajishengallis, G. (2008) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2007.01172.x · Cited by 406 · see citing works
Self-citationInnate immune mechanisms of colitis and colitis-associated colorectal cancer
Saleh, M., & Trinchieri, G. (2010) · Nature reviews. Immunology · doi:10.1038/nri2891 · Cited by 402 · see citing works
Complex Species Interactions and the Dynamics of Ecological Systems: Long-Term Experiments
Brown, J. H., Whitham, T. G., Ernest, S. K. M., & Gehring, C. A. (2001) · Science · doi:10.1126/science.293.5530.643 · Cited by 393 · see citing works
Periodontitis in RA—the citrullinated enolase connection
Lundberg, K., Wegner, N., Yucel‐Lindberg, T., & Venables, P. J. (2010) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2010.139 · Cited by 344 · see citing works
Local Chemokine Paralysis, a Novel Pathogenic Mechanism forPorphyromonas gingivalis
Darveau, R. P., Belton, C. M., Reife, R. A., & Lamont, R. J. (1998) · Infection and Immunity · doi:10.1128/iai.66.4.1660-1665.1998 · Cited by 343 · see citing works
Self-citationKumar, P., Leys, E. J., Bryk, J., Martinez, F. J., Moeschberger, M. L., & Griffen, A. L. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.00317-06 · Cited by 318 · see citing works
Microbial manipulation of receptor crosstalk in innate immunity
Hajishengallis, G., & Lambris, J. D. (2011) · Nature reviews. Immunology · doi:10.1038/nri2918 · Cited by 307 · see citing works
Self-citationCrosstalk pathways between Toll-like receptors and the complement system
Hajishengallis, G., & Lambris, J. D. (2010) · Trends in Immunology · doi:10.1016/j.it.2010.01.002 · Cited by 277 · see citing works
Self-citationNaito, M., Hirakawa, H., Yamashita, A., Ohara, N., Shoji, M., Yukitake, H., Nakayama, K., Toh, H., Yoshimura, F., Kuhara, S., et al. (2008) · DNA Research · doi:10.1093/dnares/dsn013 · Cited by 277 · see citing works
Low-Molecular-Weight Peptidic and Cyclic Antagonists of the Receptor for the Complement Factor C5a
Finch, A. M., Wong, A. K., Paczkowski, N. J., Wadi, S. K., Craik, D. J., Fairlie, D. P., & Taylor, S. M. (1999) · Journal of Medicinal Chemistry · doi:10.1021/jm9806594 · Cited by 247 · see citing works
Microbial Hijacking of Complement–Toll-Like Receptor Crosstalk
Wang, M., Krauss, J. L., Domon, H., Hosur, K. B., Liang, S., Magotti, P., Triantafilou, M., Triantafilou, K., Lambris, J. D., & Hajishengallis, G. (2010) · Science Signaling · doi:10.1126/scisignal.2000697 · Cited by 229 · see citing works
Self-citationUsing community viability analysis to identify fragile systems and keystone species
Ebenman, B., & Jönsson, T. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.06.011 · Cited by 211 · see citing works
Tonetti, M. S., Imboden, M. A., & Lang, N. P. (1998) · Journal of Periodontology · doi:10.1902/jop.1998.69.10.1139 · Cited by 196 · see citing works
Wang, M., Shakhatreh, M.-A. K., James, D., Liang, S., Nishiyama, S.-I., Yoshimura, F., Demuth, D. R., & Hajishengallis, G. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.4.2349 · Cited by 191 · see citing works
Self-citationInactivation of the Porphyromonas gingivalis fimA gene blocks periodontal damage in gnotobiotic rats
Malek, R. L., Fisher, J. G., Caleca, A., Stinson, M. W., van Oss, C. J., Lee, J. Y., Cho, M. I., Genco, R. J., Evans, R. T., & Dyer, D. W. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.4.1052-1059.1994 · Cited by 186 · see citing works
Reducing the risk of CVD in patients with periodontitis
Genco, R. J., & Van Dyke, T. E. (2010) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2010.120 · Cited by 182 · see citing works
Liang, S., Krauss, J. L., Domon, H., McIntosh, M. L., Hosur, K. B., Qu, H., Li, F., Τζέκου, Α., Lambris, J. D., & Hajishengallis, G. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1003252 · Cited by 173 · see citing works
Self-citationPorphyromonas gingivalis–host interactions: open war or intelligent guerilla tactics?
Hajishengallis, G. (2009) · Microbes and Infection · doi:10.1016/j.micinf.2009.03.009 · Cited by 169 · see citing works
Self-citationGenetic Control of Susceptibility toPorphyromonas gingivalis-Induced Alveolar Bone Loss in Mice
Baker, P. J., Dixon, M., & Roopenian, D. C. (2000) · Infection and Immunity · doi:10.1128/iai.68.10.5864-5868.2000 · Cited by 162 · see citing works
Evans, R. T., Klausen, B., Sojar, H. T., et al. (1992) · Infection and Immunity · doi:10.1128/iai.60.7.2926-2935.1992 · Cited by 158 · see citing works
Paramonov, N. A., Rangarajan, M., Hashim, A., Gallagher, A., Aduse‐Opoku, J., Slaney, J. M., Hounsell, E. F., & Curtis, M. A. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04871.x · Cited by 128 · see citing works
Self-citationHajishengallis, G. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.06.017 · Cited by 116 · see citing works
Self-citationSchenkein, H. A., & Genco, R. J. (1977) · Journal of Periodontology · doi:10.1902/jop.1977.48.12.778 · Cited by 114 · see citing works
Chaves, E. S., Jeffcoat, M. K., Ryerson, C. C., & Snyder, B. (2000) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2000.027012897.x · Cited by 111 · see citing works
Pathirana, R. D., O’brien-simpson, N. M., Brammar, G. C., Slakeski, N., & Reynolds, E. C. (2007) · Infection and Immunity · doi:10.1128/iai.01627-06 · Cited by 88 · see citing works
Bainbridge, B. W., Verma, R. K., Eastman, C., Yehia, B., Rivera, M. F., Moffatt, C. E., Bhattacharyya, I., Lamont, R. J., & Kesavalu, L. N. (2010) · Infection and Immunity · doi:10.1128/iai.00703-10 · Cited by 69 · see citing works
Assessment of complement cleavage in gingival fluid during experimental gingivitis in man
Patters, M. R., Niekrash, C. E., & Lang, N. P. (1989) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.1989.tb01609.x · Cited by 68 · see citing works
Doungudomdacha, S., Rawlinson, Ā., & Douglas, C. W. I. (2000) · Journal of Medical Microbiology · doi:10.1099/0022-1317-49-10-861 · Cited by 62 · see citing works
Page, R. C., Lantz, M. S., Darveau, R. P., Jeffcoat, M. K., Mancl, L., Houston, L. S., Braham, P. H., & Persson, G. R. (2007) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.2007.00337.x · Cited by 51 · see citing works
Self-citationDeposits of immunoglobulins, complement, and immune complexes in inflamed human gingiva
Athina, A., Papaconstantinou, N., Johannessen, A. C., et al. (1987) · Acta Odontologica Scandinavica · doi:10.3109/00016358709098858 · Cited by 41 · see citing works
Integrative physiology of the aging bone: insights from animal and cellular models
Syed, F. A., & Hoey, K. A. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05813.x · Cited by 33 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Periodontitis: from microbial immune subversion to systemic inflammation
Hajishengallis, G. (2015) · Nature Reviews Immunology · doi:10.1038/nri3785 · Cited by 3,046 · see citing works
Self-citationThe Oral Microbiota: Dynamic Communities and Host Interactions
Lamont, R. J., Koo, H., & Hajishengallis, G. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0089-x · Cited by 2,217 · see citing works
Dysbiosis and the immune system
Levy, M., Kolodziejczyk, A. A., Thaiss, C. A., & Elinav, E. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.7 · Cited by 1,769 · see citing works
The keystone-pathogen hypothesis
Hajishengallis, G., Darveau, R. P., & Curtis, M. A. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2873 · Cited by 1,790 · see citing works
Self-citationTonetti, M. S., Jepsen, S., Jin, L., & Otomo‐Corgel, J. (2017) · Journal of Clinical Periodontology · doi:10.1111/jcpe.12732 · Cited by 1,329 · see citing works
Hajishengallis, G., & Lamont, R. J. (2012) · Molecular Oral Microbiology · doi:10.1111/j.2041-1014.2012.00663.x · Cited by 1,267 · see citing works
Self-citationImmunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response
Hajishengallis, G. (2014) · Trends in Immunology · doi:10.1016/j.it.2013.09.001 · Cited by 1,150 · see citing works
Self-citationAbed, J., Emgård, J. E. M., Zamir, G., Faroja, M., Almogy, G., Grenov, A., Sol, A., Naor, R., Pikarsky, E., Atlan, K. A., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.07.006 · Cited by 888 · see citing works
The human microbiome: Our second genome
Grice, E. A., & Segre, J. A. (2012) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-090711-163814 · Cited by 759 · see citing works
The oral microbiome: Role of key organisms and complex networks in oral health and disease
Sedghi, L., DiMassa, V., Harrington, A., Lynch, S. V., & Kapila, Y. L. (2021) · Periodontology 2000 · doi:10.1111/prd.12393 · Cited by 755 · see citing works
The role of the microbiota in periodontal disease
Curtis, M. A., Diaz, P. I., & Van Dyke, T. E. (2020) · Periodontology 2000 · doi:10.1111/prd.12296 · Cited by 698 · see citing works
Self-citationThe oral microbiome and the immunobiology of periodontal disease and caries
Costalonga, M., & Herzberg, M. C. (2014) · Immunology Letters · doi:10.1016/j.imlet.2014.08.017 · Cited by 645 · see citing works
Polymicrobial synergy and dysbiosis in inflammatory disease
Lamont, R. J., & Hajishengallis, G. (2015) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.11.004 · Cited by 585 · see citing works
Self-citationThe leukocyte integrin antagonist Del-1 inhibits IL-17-mediated inflammatory bone loss
Eskan, M. A., Jotwani, R., Abe, T., Chmelar, J., Lim, J.-H., Liang, S., Ciero, P. A., Krauss, J. L., Li, F., Rauner, M., et al. (2012) · Nature Immunology · doi:10.1038/ni.2260 · Cited by 429 · see citing works
Self-citationMicrobial signatures of health, gingivitis and periodontitis
Abusleme, L., Hoare, A., Hong, B., & Diaz, P. I. (2021) · Periodontology 2000 · doi:10.1111/prd.12362 · Cited by 400 · see citing works
Diabetes Enhances IL-17 Expression and Alters the Oral Microbiome to Increase Its Pathogenicity
Xiao, E., Mattos, M., Vieira, G. H. A., Chen, S., Corrêa, J. D., Wu, Y., Albiero, M. L., Bittinger, K., & Graves, D. T. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.06.014 · Cited by 396 · see citing works
Compartmentalized and systemic control of tissue immunity by commensals
Belkaid, Y., & Naik, S. (2013) · Nature Immunology · doi:10.1038/ni.2604 · Cited by 382 · see citing works
Metatranscriptomics of the Human Oral Microbiome during Health and Disease
Jorth, P., Turner, K. H., Gumus, P., Nizam, N., Buduneli, N., & Whiteley, M. (2014) · mBio · doi:10.1128/mbio.01012-14 · Cited by 386 · see citing works
Can oral bacteria affect the microbiome of the gut?
Olsen, I., & Yamazaki, K. (2019) · Journal of Oral Microbiology · doi:10.1080/20002297.2019.1586422 · Cited by 328 · see citing works
Airway microbiome dynamics in exacerbations of chronic obstructive pulmonary disease
Huang, Y. J., Sethi, S., Murphy, T., Nariya, S., Boushey, H. A., & Lynch, S. V. (2014) · Journal of Clinical Microbiology · doi:10.1128/jcm.00035-14 · Cited by 323 · see citing works
The Role of the Microbiota in Inflammation, Carcinogenesis, and Cancer Therapy
Dzutsev, A., Goldszmid, R. S., Viaud, S., Zitvogel, L., & Trinchieri, G. (2015) · European Journal of Immunology · doi:10.1002/eji.201444972 · Cited by 300 · see citing works
Hajishengallis, G., & Lamont, R. J. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.02.010 · Cited by 275 · see citing works
“In stark contrast, in conventional (specific-pathogen-free) mice, the same bacterium transforms the periodontal microbiota into a dysbiotic, periodontitis-causing community, as long as complement and Toll-like receptor signaling pathways remain intact [38, 39].”
BackgroundSelf-citationInflammatory osteolysis: A conspiracy against bone
Mbalaviele, G., Novack, D. V., Schett, G., & Teitelbaum, S. L. (2017) · Journal of Clinical Investigation · doi:10.1172/jci93356 · Cited by 251 · see citing works
Dutzan, N., Abusleme, L., Bridgeman, H., Greenwell-Wild, T., Zangerle-Murray, T., Fife, M. E., Bouladoux, N., Linley, H., Brenchley, L., Wemyss, K., et al. (2017) · Immunity · doi:10.1016/j.immuni.2016.12.010 · Cited by 252 · see citing works
“, 2014) are causative in periodontitis, as are dysbioticmicrobial communities that stimulate aberrant inflammatory responses promoting the disease in mouse models (Hajishengallis et al., 2011) and in susceptible patients (Darveau, 2010; Lamont and Hajishengallis, 2015).”
BackgroundOral microbiota and cancer development
Tuominen, H., & Rautava, J. (2021) · Pathobiology · doi:10.1159/000510979 · Cited by 238 · see citing works
Changes in cystic fibrosis airway microbiota at pulmonary exacerbation
Carmody, L. A., Zhao, J., Schloss, P. D., Petrosino, J. F., Murray, S., Young, V. B., Li, J. Z., & LiPuma, J. J. (2013) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201211-107oc · Cited by 239 · see citing works
Xu, H., Sobue, T., Thompson, A., Xie, Z., Poon, K., Ricker, A., Cervantes, J., Diaz, P. I., & Dongari‐Bagtzoglou, A. (2014) · Cellular Microbiology · doi:10.1111/cmi.12216 · Cited by 179 · see citing works
Distinct Oral Neutrophil Subsets Define Health and Periodontal Disease States
Fine, N., Hassanpour, S., Borenstein, A., Sima, C., Oveisi, M., Scholey, J., Cherney, D., & Glogauer, M. (2016) · Journal of Dental Research · doi:10.1177/0022034516645564 · Cited by 163 · see citing works
Microbial involvement in Alzheimer disease development and progression
Bulgart, H. R., Neczypor, E. W., Wold, L. E., & Mackos, A. R. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00378-4 · Cited by 116 · see citing works
Torrungruang, K., Jitpakdeebordin, S., Charatkulangkun, O., & Gleebbua, Y. (2015) · PLOS ONE · doi:10.1371/journal.pone.0136646 · Cited by 102 · see citing works
Carberry, C. A., Waters, S. M., Kenny, D. A., & Creevey, C. J. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.03131-13 · Cited by 100 · see citing works
Lynch, S. V., Goldfarb, K. C., Wild, Y. K., Kong, W., De Lisle, R. C., & Brodie, E. L. (2013) · Gut Microbes · doi:10.4161/gmic.22430 · Cited by 87 · see citing works
The role of the host—Neutrophil biology
Chapple, I. L. C., Hirschfeld, J., Kantarci, A., Wilensky, A., & Shapira, L. (2023) · Periodontology 2000 · doi:10.1111/prd.12490 · Cited by 83 · see citing works
Interactions Between Neutrophils and Periodontal Pathogens in Late-Onset Periodontitis
Jiang, Q., Zhao, Y., Shui, Y., Zhou, X., Cheng, L., Ren, B., Chen, Z., & Li, M. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.627328 · Cited by 76 · see citing works
Costa, R. C., Souza, J. G. S., Bertolini, M., Retamal‐Valdes, B., Feres, M., & Barão, V. A. R. (2020) · Clinical Oral Implants Research · doi:10.1111/clr.13663 · Cited by 48 · see citing works
Microbiome: paediatricians’ perspective
Arora, S., Dewan, P., & Gupta, P. (2015) · Indian Journal of Medical Research · doi:10.4103/0971-5916.171275 · Cited by 39 · see citing works
Connolly, E., Millhouse, E., Doyle, R., Culshaw, S., Ramage, G., & Moran, G. P. (2017) · Molecular Oral Microbiology · doi:10.1111/omi.12151 · Cited by 35 · see citing works
Esparbès, P., Legrand, A., Bandiaky, O. N., Chéraud-Carpentier, M., Martin, H., Montassier, E., & Soueidan, A. (2021) · Microorganisms · doi:10.3390/microorganisms9112364 · Cited by 24 · see citing works
Aptamer Based SPREETA Sensor for the Detection of <i>Porphyromonas gingivalis</i> G-Protein
Park, S.-G., Lee, H. J., Ji, T., Kim, K., & Ohk, S.-H. (2024) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.2310.10042 · Cited by 2 · see citing works
- Authors
- Hajishengallis, G., Liang, S., Payne, M. A., Hashim, A., Jotwani, R., Eskan, M. A., McIntosh, M. L., Alsam, A., Kirkwood, K. L., Lambris, J. D., Darveau, R. P., & Curtis, M. A.
- Affiliations
- University of Louisville (US)
- Queen Mary University of London (GB)
- Medical University of South Carolina (US)
- University of Pennsylvania (US)
- University of Washington (US)
- Corresponding author
- Hajishengallis, George
- Darveau, Richard P.
- Curtis, Michael A.
- ORCID
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2011-11
- Volume
- 10
- Issue
- 5
- Pages
- 497-506
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC3221781
- OpenAlex
- W2090443712
- Cited by
- 1,154
- References
- 50
- Citations by year
- 2026: 56 · 2025: 75 · 2024: 95 · 2023: 85 · 2022: 84 · 2021: 99 · 2020: 112 · 2019: 80 · 2018: 80 · 2017: 80 · 2016: 61 · 2015: 71 · 2014: 71 · 2013: 59 · 2012: 41
- FWCI
- 69.00
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 660 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell Host & Microbe (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (GM062134, R01GM062134)
- National Institute of Allergy and Infectious Diseases (AI 068730, P01AI068730)
- National Institute of Dental and Craniofacial Research (R01DE018292, DE-015254, R01DE015254, DE021580, R01DE018274, DE018274, DE018292, RC4DE021580, R01DE021423)
- National Center for Research Resources (P20RR017696)
- Topics
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Keywords
- Porphyromonas gingivalis, periodontitis, periodontal bone loss, complement system, C3a receptor, C5a receptor, host-microbe homeostasis, germ-free mice, dental plaque
- MeSH terms
- Animals, Complement System Proteins, Humans, Mice, Inbred BALB C, Mice, Inbred C3H, Periodontitis, Periodontium, Bacteroidaceae Infections, Porphyromonas gingivalis, Mice, Knockout, Biofilms, Mice, Metagenome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
