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Original Article

Inflammatory response of gut, spleen, and liver in mice induced by orally administered Porphyromonas gingivalis

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Article: 2088936 | Received 24 Mar 2022, Accepted 09 Jun 2022, Published online: 16 Jun 2022

References

  • Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases[J]. Lancet. 2005;366(9499):1809–14.
  • Nassar H, Kantarci A, Van Dyke TE. Diabetic periodontitis: a model for activated innate immunity and impaired resolution of inflammation[J]. Periodontol 2000. 2007;43:233–244.
  • Bale BF, Doneen AL, Vigerust DJ. High-risk periodontal pathogens contribute to the pathogenesis of atherosclerosis[J]. Postgrad Med J. 2017;93(1098):215–220.
  • González-Febles J, Sanz M. Periodontitis and rheumatoid arthritis: what have we learned about their connection and their treatment?[J]. Periodontol 2000. 2021;87(1):181–203.
  • Nagasaki A, Sakamoto S, Arai T, et al. Elimination of Porphyromonas gingivalis inhibits liver fibrosis and inflammation in NASH[J]. J Clin Periodontol. 2021;48(10):1367–1378.
  • Elwishahy A, Antia K, Bhusari S, et al. Porphyromonas gingivalis as a risk factor to alzheimer’s disease: a systematic review[J]. J Alzheimers Dis Rep. 2021;5(1):721–732.
  • Mulhall H, Huck O, Amar S. Porphyromonas gingivalis, a Long-Range Pathogen: systemic Impact and Therapeutic Implications[J]. Microorganisms. 2020;8:6.
  • Schmidt TS, Hayward MR, Coelho LP, et al. Extensive transmission of microbes along the gastrointestinal tract[J]. Elife. 20198:e42693 doi:10.7554/eLife.42693.
  • Lira-Junior R, Boström EA. Oral-gut connection: one step closer to an integrated view of the gastrointestinal tract?[J]. Mucosal Immunol. 2018;11(2):316–318.
  • Lorenzo D, GianVincenzo Z, Carlo Luca R, et al. Oral-gut microbiota and arthritis: is there an evidence-based axis?[J]. J Clin Med. 2019;8:10.
  • Byrd KM, Gulati AS. The “Gum-Gut” axis in inflammatory bowel diseases: a hypothesis-driven review of associations and advances[J]. Front Immunol. 2021;12:620124.
  • Shi C, Cai L, Xun Z, et al. Metagenomic analysis of the salivary microbiota in patients with caries, periodontitis and comorbid diseases[J]. J Dent Sci. 2021;16(4):1264–1273.
  • He J, Huang W, Pan Z, et al. Quantitative analysis of microbiota in saliva, supragingival, and subgingival plaque of Chinese adults with chronic periodontitis[J]. Clin Oral Investig. 2012;16(6):1579–1588.
  • Boutaga K, Savelkoul PH, Winkel EG, et al. Comparison of subgingival bacterial sampling with oral lavage for detection and quantification of periodontal pathogens by real-time polymerase chain reaction[J]. J Periodontol. 2007;78(1):79–86.
  • Saygun I, Nizam N, Keskiner I, et al. Salivary infectious agents and periodontal disease status[J]. J Periodontal Res. 2011;46(2):235–239.
  • Arimatsu K, Yamada H, Miyazawa H, et al. Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota[J]. Sci Rep. 2014;4:4828.
  • Nakajima M, Arimatsu K, Kato T, et al. Oral Administration of P. gingivalis Induces Dysbiosis of Gut Microbiota and Impaired Barrier Function Leading to Dissemination of Enterobacteria to the Liver[J]. PLoS One. 2015;10(7):e0134234.
  • Lewis SM, Williams A, Eisenbarth SC. Structure and function of the immune system in the spleen[J]. Sci Immunol. 2019;4:33.
  • Zha XQ, Zhao HW, Bansal V, et al. Immunoregulatory activities of dendrobium huoshanense polysaccharides in mouse intestine, spleen and liver[J]. Int J Biol Macromol. 2014;64:377–382.
  • Liu Y, Huang W, Wang J, et al. Multifaceted impacts of periodontal pathogens in disorders of the intestinal barrier[J]. Front Immunol. 2021;12:693479.
  • Takebayashi K, Koboziev I, Ostanin DV, et al. Role of the gut-associated and secondary lymphoid tissue in the induction of chronic colitis[J]. Inflamm Bowel Dis. 2011;17(1):268–278.
  • Weiberg D, Basic M, Smoczek M, et al. Participation of the spleen in the IgA immune response in the gut[J]. PLoS One. 2018;13(10):e0205247.
  • Spencer J, Dogan A. A common migratory highway between human spleen and mucosa-associated lymphoid tissues; data from nature’s own experiments[J]. Mucosal Immunol. 2009;2(5):380–382.
  • Spadoni I, Zagato E, Bertocchi A, et al. A gut-vascular barrier controls the systemic dissemination of bacteria[J]. Science. 2015;350(6262):830–834.
  • Fonseca MT, Moretti EH, Marques LMM, et al. A leukotriene-dependent spleen-liver axis drives TNF production in systemic inflammation[J]. Sci Signal. 2021;14:679.
  • Tripathi A, Debelius J, Brenner DA, et al. The gut-liver axis and the intersection with the microbiome[J]. Nat Rev Gastroenterol Hepatol. 2018;15(7):397–411.
  • Sun J, Zhang J, Wang X, et al. Gut-liver crosstalk in sepsis-induced liver injury[J]. Crit Care. 2020;24(1):614.
  • Fujita M, Kuraji R, Ito H, et al. Histological effects and pharmacokinetics of lipopolysaccharide derived from Porphyromonas gingivalis on rat maxilla and liver concerning with progression into non-alcoholic steatohepatitis[J]. J Periodontol. 2018;89(9):1101–1111.
  • Kuraji R, Ito H, Fujita M, et al. Porphyromonas gingivalis induced periodontitis exacerbates progression of non-alcoholic steatohepatitis in rats[J]. Clin Exp Dent Res. 2016;2(3):216–225.
  • Nakahara T, Hyogo H, Ono A, et al. Involvement of Porphyromonas gingivalis in the progression of non-alcoholic fatty liver disease[J]. J Gastroenterol. 2018;53(2):269–280.
  • Ding LY, Liang LZ, Zhao YX, et al. Porphyromonas gingivalis-derived lipopolysaccharide causes excessive hepatic lipid accumulation via activating NF-κB and JNK signaling pathways[J]. Oral Dis. 2019;25(7):1789–1797.
  • Gemmell E, Winning T A, Bird P S, et al. Cytokine profiles of lesional and splenic T cells in Porphyromonas gingivalis infection in a murine model[J]. J Periodontol. 1998;69(10):1131–1138.
  • Cai Y, Kobayashi R, Hashizume-Takizawa T, et al. Porphyromonas gingivalis infection enhances Th17 responses for development of atherosclerosis[J]. Arch Oral Biol. 2014;59(11):1183–1191.
  • Mandato C, Delli Bovi AP, Vajro P. The gut-liver axis as a target of liver disease management[J]. Hepatobiliary Surg Nutr. 2021;10(1):100–102.
  • Liang Q, Zhang M, Hu Y, et al. Gut microbiome contributes to liver fibrosis impact on t cell receptor immune repertoire[J]. Front Microbiol. 2020;11:571847.
  • Tap J, Mondot S, Levenez F, et al. Towards the human intestinal microbiota phylogenetic core[J]. Environ Microbiol. 2009;11(10):2574–2584.
  • Kramer CD, Simas AM, He X, et al. Distinct roles for dietary lipids and Porphyromonas gingivalis infection on atherosclerosis progression and the gut microbiota[J]. Anaerobe. 2017;45:19–30.
  • Philips CA, Augustine P, Yerol PK, et al. Modulating the intestinal microbiota: therapeutic opportunities in liver disease[J]. J Clin Transl Hepatol. 2020;8(1):87–99.
  • Schnabl B, Brenner DA. Interactions between the intestinal microbiome and liver diseases[J]. Gastroenterology. 2014;146(6):1513–1524.
  • Lo BC, Chen GY, Núñez G, et al. Gut microbiota and systemic immunity in health and disease[J]. Int Immunol. 2021;33(4):197–209.
  • Jia W, Rajani C, Xu H, et al. Gut microbiota alterations are distinct for primary colorectal cancer and hepatocellular carcinoma[J]. Protein Cell . 2020.12:374–93.
  • Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota[J]. Environ Microbiol. 2017;19(1):29–41.
  • Baxter NT, Schmidt AW, Venkataraman A, et al. Dynamics of human gut microbiota and short-chain fatty acids in response to dietary interventions with three fermentable Fibers[J]. mBio. 2019;10:1.
  • Li X, Li Z, He Y, et al. Regional distribution of Christensenellaceae and its associations with metabolic syndrome based on a population-level analysis[J]. PeerJ. 2020;8:e9591.
  • Marafini I, Monteleone I, Di Fusco D, et al. TNF-α producing innate lymphoid cells (ILCs) are increased in active celiac disease and contribute to promote intestinal atrophy in mice[J]. PLoS One. 2015;10(5):e0126291.
  • Kalliolias GD, Ivashkiv LB. TNF biology, pathogenic mechanisms and emerging therapeutic strategies[J]. Nat Rev Rheumatol. 2016;12(1):49–62.
  • Paredes JM, Moreno N, Latorre P, et al. Clinical impact of sonographic transmural healing after anti-TNF antibody treatment in patients with Crohn’s disease[J]. Dig Dis Sci. 2019;64(9):2600–2606.
  • Braegger CP, Nicholls S, Murch SH, et al. Tumour necrosis factor alpha in stool as a marker of intestinal inflammation[J]. Lancet. 1992;339(8785):89–91.
  • Murch SH, Braegger CP, Walker-Smith JA, et al. Location of tumour necrosis factor alpha by immunohistochemistry in chronic inflammatory bowel disease[J]. Gut. 1993;34(12):1705–1709.
  • Monaco C, Nanchahal J, Taylor P, et al. Anti-TNF therapy: past, present and future[J]. Int Immunol. 2015;27(1):55–62.
  • Reibetanz J, Germer CT. [Anti-TNF antibodies in prevention and treatment of postoperative recurrence of Crohn’s disease][J]. Chirurg. 2015;86(5):498.
  • Langer V, Vivi E, Regensburger D, et al. IFN-γ drives inflammatory bowel disease pathogenesis through VE-cadherin-directed vascular barrier disruption[J]. J Clin Invest. 2019;129(11):4691–4707.
  • Beaurepaire C, Smyth D, McKay DM. Interferon-gamma regulation of intestinal epithelial permeability[J]. J Interferon Cytokine Res. 2009;29(3):133–144.
  • Dou L, Liang HF, Geller DA, et al. The regulation role of interferon regulatory factor-1 gene and clinical relevance[J]. Hum Immunol. 2014;75(11):1110–1114.
  • Meghil MM, Ghaly M, Cutler CW. A tale of two fimbriae: how invasion of dendritic cells by porphyromonas gingivalis disrupts DC maturation and depolarizes the T-cell-mediated immune response[J]. Pathogens. 2022;11:3.
  • Tarantino G, Savastano S, Capone D, et al. Spleen: a new role for an old player?[J]. World J Gastroenterol. 2011;17(33):3776–3784.
  • Papa MZ, Shiloni E, Vetto JT, et al. Surgical morbidity in patients with systemic lupus erythematosus[J]. Am J Surg. 1989;157(3):295–298.
  • Curovic Rotbain E, Lund Hansen D, Schaffalitzky de Muckadell O; Schaffalitzky de Muckadell O, et al. Splenomegaly - Diagnostic validity, work-up and underlying causes[J]. PLoS One. 2017;12(11):e0186674.
  • Keramida G, Dunford A, Kaya G, et al. Hepato-splenic axis: hepatic and splenic metabolic activities are linked[J]. Am J Nucl Med Mol Imaging. 2018;8(3):228–238.
  • Ma B, Chen K, Liu P, et al. Dichotomal functions of phosphorylated and unphosphorylated STAT1 in hepatocellular carcinoma[J]. J Mol Med (Berl). 2019;97(1):77–88.
  • Gambin A, Charzyńska A, Ellert-Miklaszewska A, et al. Computational models of the JAK1/2-STAT1 signaling[J]. Jakstat. 2013;2(3):e24672.
  • Bousoik E, Montazeri Aliabadi H. “Do we know Jack” about JAK? A closer look at JAK/STAT signaling pathway[J]. Front Oncol. 2018;8:287.
  • Buccione C, Fragale A, Polverino F, et al. Role of interferon regulatory factor 1 in governing Treg depletion, Th1 polarization, inflammasome activation and antitumor efficacy of cyclophosphamide[J]. Int J Cancer. 2018;142(5):976–987.
  • Shevyrev D, Treg Heterogeneity TV. Function, and Homeostasis[J]. Front Immunol. 2019;10:3100.
  • Huang H, Chen S, Li H, et al. The association between markers of liver injury and clinical outcomes in patients with COVID-19 in Wuhan[J]. Aliment Pharmacol Ther. 2020;52(6):1051–1059.
  • Samuel VT, Shulman GI. The pathogenesis of insulin resistance: integrating signaling pathways and substrate flux[J]. J Clin Invest. 2016;126(1):12–22.
  • Saito T, Shimazaki Y, Koga T, et al. Relationship between periodontitis and hepatic condition in Japanese women[J]. J Int Acad Periodontol. 2006;8(3): 89–95
  • Takamisawa K, Sugita N, Komatsu S, et al. Association between serum IgG antibody titers against Porphyromonas gingivalis and liver enzyme levels: a cross-sectional study in Sado Island[J]. Heliyon. 2020;6(11):e05531.
  • Yoneda M, Naka S, Nakano K, et al. Involvement of a periodontal pathogen, Porphyromonas gingivalis on the pathogenesis of non-alcoholic fatty liver disease[J]. BMC Gastroenterol. 2012;12:16.
  • Gerges SH, Wahdan SA, Elsherbiny DA, et al. Non-alcoholic fatty liver disease: an overview of risk factors, pathophysiological mechanisms, diagnostic procedures, and therapeutic interventions[J]. Life Sci. 2021;271:119220.
  • Liu C, Yang H, Shi W, et al. MicroRNA-mediated regulation of T helper type 17/regulatory T-cell balance in autoimmune disease[J]. Immunology. 2018;155(4):427–434.
  • Mo C, Zeng Z, Deng Q, et al. Imbalance between T helper 17 and regulatory T cell subsets plays a significant role in the pathogenesis of systemic sclerosis[J]. Biomed Pharmacother. 2018;108:177–183.
  • Beringer A, Miossec P. IL-17 and IL-17-producing cells and liver diseases, with focus on autoimmune liver diseases[J]. Autoimmun Rev. 2018;17(12):1176–1185.
  • Harley IT, Stankiewicz TE, Giles DA, et al. IL-17 signaling accelerates the progression of nonalcoholic fatty liver disease in mice[J]. Hepatology. 2014;59(5):1830–1839.
  • Gomes AL, Teijeiro A, Burén S, et al. Metabolic Inflammation-Associated IL-17A causes non-alcoholic steatohepatitis and hepatocellular carcinoma[J]. Cancer Cell. 2016;30(1):161–175.
  • Zhao L, Qiu DK, Ma X. Th17 cells: the emerging reciprocal partner of regulatory T cells in the liver[J]. J Dig Dis. 2010;11(3):126–133.
  • Kimura A, Kishimoto TIL-6. regulator of Treg/Th17 balance[J]. Eur J Immunol. 2010;40(7):1830–1835.
  • Ogobuiro I, Gonzales J, Tuma F. Physiology, Gastrointestinal [M]. StatPearls. Treasure Island (FL); StatPearls Publishing Copyright ©2021. StatPearls Publishing LLC; 2021.
  • Gelberg HB. Comparative anatomy, physiology, and mechanisms of disease production of the esophagus, stomach, and small intestine[J]. Toxicol Pathol. 2014;42(1):54–66.