Links between Insulin Resistance and Periodontal Bacteria: Insights on Molecular Players and Therapeutic Potential of Polyphenols
Abstract
:1. Introduction
2. Molecular Events Related to Insulin Signaling Pathway and Insulin Resistance
2.1. Insulin
2.2. Insulin-Stimulated Glucose Uptake Signaling Pathway
2.3. Insulin Resistance
2.4. Mechanisms of Insulin Signaling Disruption
2.4.1. Inflammation
2.4.2. Oxidative Stress
3. Molecular Players Linking Insulin Resistance and Periodontal Bacteria
3.1. Periodontitis and Associated Main Periodontal Bacteria
3.2. Impact of Periodontal Bacteria on Insulin Sensitivity and Secretion
3.2.1. Adipose Tissue
3.2.2. Skeletal Muscle
3.2.3. The Liver
3.2.4. Pancreatic β-Cells
4. Current Management of Periodontal Infection and Diabetes
5. Polyphenol-Based Therapies
5.1. Structures and Sources of Polyphenols
5.2. Bioavailability of Polyphenols
5.3. Biological Effects of Polyphenols
5.3.1. Anti-Inflammatory Properties of Polyphenols
5.3.2. Antioxidant Properties of Polyphenols
5.3.3. Insulin-Sensitizing Properties of Polyphenols
5.3.4. Anti-Bacterial Properties of Polyphenols
5.4. Polyphenol-Based Therapy for Periodontitis Management
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- IDF Diabetes Atlas 2021|IDF Diabetes Atlas. Available online: https://diabetesatlas.org/atlas/tenth-edition/ (accessed on 26 January 2022).
- World Health Organization. Global Report on Diabetes; World Health Organization: Geneva, Switzerland, 2016; ISBN 978-92-4-156525-7. [Google Scholar]
- Lamont, R.J.; Koo, H.; Hajishengallis, G. The oral microbiota: Dynamic communities and host interactions. Nat. Rev. Microbiol. 2018, 16, 745–759. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.-Y.; Kuan, Y.-H.; Tsai, Y.-F.; Tai, C.-J.; Tsai, T.-H.; Huang, K.-H. Correlation between diabetes mellitus and periodontitis in Taiwan: A nationwide cohort study. Diabetes Res. Clin. Pract. 2019, 150, 245–252. [Google Scholar] [CrossRef] [PubMed]
- Dhir, S.; Wangnoo, S.; Kumar, V. Impact of glycemic levels in Type 2 diabetes on periodontitis. Indian J. Endocrinol. Metab. 2018, 22, 672–677. [Google Scholar] [CrossRef]
- Takeda, K.; Mizutani, K.; Minami, I.; Kido, D.; Mikami, R.; Konuma, K.; Saito, N.; Kominato, H.; Takemura, S.; Nakagawa, K.; et al. Association of periodontal pocket area with type 2 diabetes and obesity: A cross-sectional study. BMJ Open Diabetes Res. Care 2021, 9, e002139. [Google Scholar] [CrossRef] [PubMed]
- Lin, S.-Y.; Lin, C.-L.; Liu, J.-H.; Wang, I.-K.; Hsu, W.-H.; Chen, C.-J.; Ting, I.-W.; Wu, I.-T.; Sung, F.-C.; Huang, C.-C.; et al. Association Between Periodontitis Needing Surgical Treatment and Subsequent Diabetes Risk: A Population-Based Cohort Study. J. Periodontol. 2014, 85, 779–786. [Google Scholar] [CrossRef] [PubMed]
- Graziani, F.; Gennai, S.; Solini, A.; Petrini, M. A systematic review and meta-analysis of epidemiologic observational evidence on the effect of periodontitis on diabetes An update of the EFP-AAP review. J. Clin. Periodontol. 2018, 45, 167–187. [Google Scholar] [CrossRef] [PubMed]
- Ziukaite, L.; Slot, D.E.; Van Der Weijden, F.A. Prevalence of diabetes mellitus in people clinically diagnosed with periodontitis: A systematic review and meta-analysis of epidemiologic studies. J. Clin. Periodontol. 2018, 45, 650–662. [Google Scholar] [CrossRef]
- Stöhr, J.; Barbaresko, J.; Neuenschwander, M.; Schlesinger, S. Bidirectional association between periodontal disease and diabetes mellitus: A systematic review and meta-analysis of cohort studies. Sci. Rep. 2021, 11, 1–9. [Google Scholar] [CrossRef]
- Arimatsu, K.; Yamada, H.; Miyazawa, H.; Minagawa, T.; Nakajima, M.; Ryder, M.I.; Gotoh, K.; Motooka, D.; Nakamura, S.; Iida, T.; et al. Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota. Sci. Rep. 2015, 4, 4828. [Google Scholar] [CrossRef] [Green Version]
- Blasco-Baque, V.; Garidou, L.; Pomié, C.; Escoula, Q.; Loubieres, P.; Le Gall-David, S.; Lemaitre, M.; Nicolas, S.; Klopp, P.; Waget, A.; et al. Periodontitis induced byPorphyromonas gingivalisdrives periodontal microbiota dysbiosis and insulin resistance via an impaired adaptive immune response. Gut 2017, 66, 872–885. [Google Scholar] [CrossRef] [Green Version]
- Watanabe, K.; Katagiri, S.; Takahashi, H.; Sasaki, N.; Maekawa, S.; Komazaki, R.; Hatasa, M.; Kitajima, Y.; Maruyama, Y.; Shiba, T.; et al. Porphyromonas gingivalis impairs glucose uptake in skeletal muscle associated with altering gut microbiota. FASEB J. 2021, 35, 35. [Google Scholar] [CrossRef]
- Teshome, A.; Yitayeh, A. The effect of periodontal therapy on glycemic control and fasting plasma glucose level in type 2 diabetic patients: Systematic review and meta-analysis. BMC Oral Health 2017, 17, 31. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baeza, M.; Morales, A.; Cisterna, C.; Cavalla, F.; Jara, G.; Isamitt, Y.; Pino, P.; Gamonal, J. Effect of periodontal treatment in patients with periodontitis and diabetes: Systematic review and meta-analysis. J. Appl. Oral Sci. 2020, 28, e20190248. [Google Scholar] [CrossRef] [PubMed]
- Supplement, D.; Oberti, L.; Gabrione, F.; Nardone, M.; Di Girolamo, M. Two-way relationship between diabetes and periodontal disease: A reality or a paradigm? J. Biol. Regul. Homeost. Agents 2019, 33, 153–159. [Google Scholar]
- Takeuchi, H.; Yamaga, S.; Sasaki, N.; Kuboniwa, M.; Matsusaki, M.; Amano, A. Porphyromonas gingivalis induces penetration of lipopolysaccharide and peptidoglycan through the gingival epithelium via degradation of coxsackievirus and adenovirus receptor. Cell. Microbiol. 2021, 23, e13388. [Google Scholar] [CrossRef]
- Seyama, M.; Yoshida, K.; Fujiwara, N.; Ono, K.; Eguchi, T.; Kawai, H.; Guo, J.; Weng, Y.; Haoze, Y.; Uchibe, K.; et al. Outer membrane vesicles of Porphyromonas gingivalis attenuate insulin sensitivity by delivering gingipains to the liver. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 2020, 1866, 165731. [Google Scholar] [CrossRef]
- Lin, D.; Xiao, M.; Zhao, J.; Li, Z.; Xing, B.; Li, X.; Kong, M.; Li, L.; Zhang, Q.; Liu, Y.; et al. An Overview of Plant Phenolic Compounds and Their Importance in Human Nutrition and Management of Type 2 Diabetes. Molecules 2016, 21, 1374. [Google Scholar] [CrossRef]
- Weiss, M.; Steiner, D.F.; Philipson, L.H. Insulin Biosynthesis, Secretion, Structure, and Structure-Activity Relationship. Available online: https://www.ncbi.nlm.nih.gov/books/NBK279029/.2000 (accessed on 23 February 2022).
- Saltiel, A.R.; Kahn, C.R. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001, 414, 799–806. [Google Scholar] [CrossRef]
- Leto, D.; Saltiel, A.R. Regulation of glucose transport by insulin: Traffic control of GLUT4. Nat. Rev. Mol. Cell Biol. 2012, 13, 383–396. [Google Scholar] [CrossRef]
- Sun, X.J.; Rothenberg, P.; Kahn, C.R.; Backer, J.M.; Araki, E.; Wilden, P.A.; Cahill, D.A.; Goldstein, B.J.; White, M.F. Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 1991, 352, 73–77. [Google Scholar] [CrossRef]
- Mîinea, C.P.; Sano, H.; Kane, S.; Sano, E.; Fukuda, M.; Peränen, J.; Lane, W.S.; Lienhard, G.E. AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem. J. 2005, 391, 87–93. [Google Scholar] [CrossRef] [PubMed]
- Prentki, M.; Nolan, C.J. Islet beta cell failure in type 2 diabetes. J. Clin. Investig. 2006, 116, 1802–1812. [Google Scholar] [CrossRef] [Green Version]
- Czech, M.P. Insulin action and resistance in obesity and type 2 diabetes. Nat. Med. 2017, 23, 804–814. [Google Scholar] [CrossRef]
- Esser, N.; Utzschneider, K.M.; Kahn, S.E. Early beta cell dysfunction vs insulin hypersecretion as the primary event in the pathogenesis of dysglycaemia. Diabetologia 2020, 63, 2007–2021. [Google Scholar] [CrossRef] [PubMed]
- Gastaldelli, A.; Abdul Ghani, M.; DeFronzo, R.A. Adaptation of Insulin Clearance to Metabolic Demand Is a Key Determinant of Glucose Tolerance. Diabetes 2021, 70, 377–385. [Google Scholar] [CrossRef] [PubMed]
- van Vliet, S.; Koh, H.-C.E.; Patterson, B.W.; Yoshino, M.; LaForest, R.; Gropler, R.J.; Klein, S.; Mittendorfer, B. Obesity Is Associated with Increased Basal and Postprandial β-Cell Insulin Secretion Even in the Absence of Insulin Resistance. Diabetes 2020, 69, 2112–2119. [Google Scholar] [CrossRef]
- Mittendorfer, B.; Patterson, B.W.; Smith, G.I.; Yoshino, M.; Klein, S. β Cell function and plasma insulin clearance in people with obesity and different glycemic status. J. Clin. Investig. 2022, 132, 132. [Google Scholar] [CrossRef]
- Huang, T.; Ley, S.H.; Zheng, Y.; Wang, T.; Bray, G.A.; Sacks, F.M.; Qi, L. Genetic susceptibility to diabetes and long-term improvement of insulin resistance and β cell function during weight loss: The Preventing Overweight Using Novel Dietary Strategies (POUNDS LOST) trial. Am. J. Clin. Nutr. 2016, 104, 198–204. [Google Scholar] [CrossRef] [Green Version]
- Han, L.; Zhang, T.; You, D.; Chen, W.; Bray, G.; Sacks, F.; Qi, L. Temporal and mediation relations of weight loss, and changes in insulin resistance and blood pressure in response to 2-year weight-loss diet interventions: The POUNDS Lost trial. Eur. J. Nutr. 2021, 61, 269–275. [Google Scholar] [CrossRef]
- Bondonno, N.P.; Dalgaard, F.; Murray, K.; Davey, R.J.; Bondonno, C.P.; Cassidy, A.; Lewis, J.R.; Kyrø, C.; Gislason, G.; Scalbert, A.; et al. Higher Habitual Flavonoid Intakes Are Associated with a Lower Incidence of Diabetes. J. Nutr. 2021, 151, 3533–3542. [Google Scholar] [CrossRef]
- Salas-Salvadó, J.; Díaz-López, A.; Ruiz-Canela, M.; Basora, J.; Fitó, M.; Corella, D.; Serra-Majem, L.; Wärnberg, J.; Romaguera, D.; Estruch, R.; et al. Effect of a Lifestyle Intervention Program With Energy-Restricted Mediterranean Diet and Exercise on Weight Loss and Cardiovascular Risk Factors: One-Year Results of the PREDIMED-Plus Trial. Diabetes Care 2018, 42, 777–788. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barzin, M.; Aryannezhad, S.; Khalaj, A.; Mahdavi, M.; Valizadeh, M.; Ghareh, S.; Azizi, F.; Hosseinpanah, F. Effects of bariatric surgery in different obesity phenotypes: Tehran Obesity Treatment Study (TOTS). Obes. Surg. 2019, 30, 461–469. [Google Scholar] [CrossRef]
- Cotillard, A.; Poitou, C.; Torcivia, A.; Bouillot, J.-L.; Dietrich, A.; Klöting, N.; Grégoire, C.; Lolmede, K.; Blüher, M.; Clément, K. Adipocyte Size Threshold Matters: Link with Risk of Type 2 Diabetes and Improved Insulin Resistance After Gastric Bypass. J. Clin. Endocrinol. Metab. 2014, 99, E1466–E1470. [Google Scholar] [CrossRef] [PubMed]
- Seki, Y.; Kasama, K.; Yokoyama, R.; Maki, A.; Shimizu, H.; Park, H.; Kurokawa, Y. Bariatric surgery versus medical treatment in mildly obese patients with type 2 diabetes mellitus in Japan: Propensity score-matched analysis on real-world data. J. Diabetes Investig. 2021, 13, 74–84. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.H.; Giraud, J.; Davis, R.J.; White, M.F. c-Jun N-terminal Kinase (JNK) Mediates Feedback Inhibition of the Insulin Signaling Cascade. J. Biol. Chem. 2003, 278, 2896–2902. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jakobsen, S.N.; Hardie, D.G.; Morrice, N.; Tornqvist, H.E. 5′-AMP-activated Protein Kinase Phosphorylates IRS-1 on Ser-789 in Mouse C2C12 Myotubes in Response to 5-Aminoimidazole-4-carboxamide Riboside. J. Biol. Chem. 2001, 276, 46912–46916. [Google Scholar] [CrossRef] [Green Version]
- Morino, K.; Neschen, S.; Bilz, S.; Sono, S.; Tsirigotis, D.; Reznick, R.M.; Moore, I.; Nagai, Y.; Samuel, V.; Sebastian, D.; et al. Muscle-Specific IRS-1 Ser→Ala Transgenic Mice Are Protected From Fat-Induced Insulin Resistance in Skeletal Muscle. Diabetes 2008, 57, 2644–2651. [Google Scholar] [CrossRef] [Green Version]
- Yaribeygi, H.; Farrokhi, F.R.; Butler, A.E.; Sahebkar, A. Insulin resistance: Review of the underlying molecular mechanisms. J. Cell. Physiol. 2019, 234, 8152–8161. [Google Scholar] [CrossRef]
- Dandona, P.; Aljada, A.; Bandyopadhyay, A. Inflammation: The link between insulin resistance, obesity and diabetes. Trends Immunol. 2004, 25, 4–7. [Google Scholar] [CrossRef]
- Schultz, O.; Oberhäuser, F.; Saech, J.; Rubbert-Roth, A.; Hahn, M.; Krone, W.; Laudes, M. Effects of Inhibition of Interleukin-6 Signalling on Insulin Sensitivity and Lipoprotein (A) Levels in Human Subjects with Rheumatoid Diseases. PLoS ONE 2010, 5, e14328. [Google Scholar] [CrossRef]
- Hirosumi, J.; Tuncman, G.; Chang, L.; Görgün, C.Z.; Uysal, K.T.; Maeda, K.; Karin, M.; Hotamisligil, G.S. A central role for JNK in obesity and insulin resistance. Nature 2002, 420, 333–336. [Google Scholar] [CrossRef] [PubMed]
- Yuan, M.; Konstantopoulos, N.; Lee, J.; Hansen, L.; Li, Z.W.; Karin, M.; Shoelson, S.E. Reversal of obesity- and diet-induced insulin resistance with salicylates or tar-geted disruption of Ikkbeta. Science 2001, 293, 1673–1677. [Google Scholar] [CrossRef]
- Hotamisligil, G.S.; Peraldi, P.; Budavari, A.; Ellis, R.; White, M.F.; Spiegelman, B.M. IRS-1-Mediated Inhibition of Insulin Receptor Tyrosine Kinase Activity in TNF-α- and Obesity-Induced Insulin Resistance. Science 1996, 271, 665–670. [Google Scholar] [CrossRef] [PubMed]
- Solinas, G.; Karin, M. JNK1 and IKKβ: Molecular links between obesity and metabolic dysfunction. FASEB J. 2010, 24, 2596–2611. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, A.; Medzhitov, R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004, 5, 987–995. [Google Scholar] [CrossRef]
- Le Sage, F.; Meilhac, O.; Gonthier, M.-P. Porphyromonas gingivalis lipopolysaccharide induces pro-inflammatory adipokine secretion and oxidative stress by regulating Toll-like receptor-mediated signaling pathways and redox enzymes in adipocytes. Mol. Cell. Endocrinol. 2017, 446, 102–110. [Google Scholar] [CrossRef]
- Rui, L.; Yuan, M.; Frantz, D.; Shoelson, S.; White, M.F. SOCS-1 and SOCS-3 Block Insulin Signaling by Ubiquitin-mediated Degradation of IRS1 and IRS2. J. Biol. Chem. 2002, 277, 42394–42398. [Google Scholar] [CrossRef] [Green Version]
- Jager, J.; Grémeaux, T.; Cormont, M.; Le Marchand-Brustel, Y.; Tanti, J.-F. Interleukin-1β-Induced Insulin Resistance in Adipocytes through Down-Regulation of Insulin Receptor Substrate-1 Expression. Endocrinology 2007, 148, 241–251. [Google Scholar] [CrossRef]
- Yasukawa, T.; Tokunaga, E.; Ota, H.; Sugita, H.; Martyn, J.A.J.; Kaneki, M. S-Nitrosylation-dependent Inactivation of Akt/Protein Kinase B in Insulin Resistance. J. Biol. Chem. 2005, 280, 7511–7518. [Google Scholar] [CrossRef] [Green Version]
- Ouchi, N.; Parker, J.L.; Lugus, J.J.; Walsh, K. Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 2011, 11, 85–97. [Google Scholar] [CrossRef]
- Phaniendra, A.; Jestadi, D.B.; Periyasamy, L. Free Radicals: Properties, Sources, Targets, and Their Implication in Various Diseases. Indian J. Clin. Biochem. 2015, 30, 11–26. [Google Scholar] [CrossRef] [Green Version]
- Pizzino, G.; Irrera, N.; Cucinotta, M.; Pallio, G.; Mannino, F.; Arcoraci, V.; Squadrito, F.; Altavilla, D.; Bitto, A. Oxidative Stress: Harms and Benefits for Human Health. Oxid. Med. Cell. Longev. 2017, 2017, 8416763. [Google Scholar] [CrossRef] [PubMed]
- Rajendran, P.; Nandakumar, N.; Rengarajan, T.; Palaniswami, R.; Gnanadhas, E.N.; Lakshminarasaiah, U.; Gopas, J.; Nishigaki, I. Antioxidants and human diseases. Clin. Chim. Acta 2014, 436, 332–347. [Google Scholar] [CrossRef] [PubMed]
- Li, N.; Alam, J.; Venkatesan, M.I.; Eiguren-Fernandez, A.; Schmitz, D.; Di Stefano, E.; Slaughter, N.; Killeen, E.; Wang, X.; Huang, A.; et al. Nrf2 Is a Key Transcription Factor That Regulates Antioxidant Defense in Macrophages and Epithelial Cells: Protecting against the Proinflammatory and Oxidizing Effects of Diesel Exhaust Chemicals. J. Immunol. 2004, 173, 3467–3481. [Google Scholar] [CrossRef]
- Furukawa, S.; Fujita, T.; Shimabukuro, M.; Iwaki, M.; Yamada, Y.; Nakajima, Y.; Nakayama, O.; Makishima, M.; Matsuda, M.; Shimomura, I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Investig. 2004, 114, 1752–1761. [Google Scholar] [CrossRef] [PubMed]
- Houstis, N.; Rosen, E.D.; Lander, E.S. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006, 440, 944–948. [Google Scholar] [CrossRef] [PubMed]
- Hajishengallis, G.; Chavakis, T. Local and systemic mechanisms linking periodontal disease and inflammatory comorbidities. Nat. Rev. Immunol. 2021, 21, 426–440. [Google Scholar] [CrossRef] [PubMed]
- Minty, M.; Canceill, T.; Serino, M.; Burcelin, R.; Tercé, F.; Blasco-Baque, V. Oral microbiota-induced periodontitis: A new risk factor of metabolic diseases. Rev. Endocr. Metab. Disord. 2019, 20, 449–459. [Google Scholar] [CrossRef]
- Dahlen, G.; Basic, A.; Bylund, J. Importance of Virulence Factors for the Persistence of Oral Bacteria in the Inflamed Gingival Crevice and in the Pathogenesis of Periodontal Disease. J. Clin. Med. 2019, 8, 1339. [Google Scholar] [CrossRef] [Green Version]
- Lu, Y.-C.; Yeh, W.-C.; Ohashi, P.S. LPS/TLR4 signal transduction pathway. Cytokine 2008, 42, 145–151. [Google Scholar] [CrossRef]
- Bès-Houtmann, S.; Roche, R.; Hoareau, L.; Gonthier, M.-P.; Festy, F.; Caillens, H.; Gasque, P.; D’Hellencourt, C.L.; Cesari, M. Presence of functional TLR2 and TLR4 on human adipocytes. Histochem. Cell Biol. 2007, 127, 131–137. [Google Scholar] [CrossRef] [PubMed]
- Liang, H.; Hussey, S.E.; Sanchez-Avila, A.; Tantiwong, P.; Musi, N. Effect of Lipopolysaccharide on Inflammation and Insulin Action in Human Muscle. PLoS ONE 2013, 8, e63983. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.-S.; Kim, Y.-H.; Jung, Y.S.; Kim, K.-S.; Kim, N.-K.; Na, S.-Y.; Lee, J.-M.; Lee, C.-H.; Choi, H.-S. Hepatocyte toll-like receptor 4 mediates lipopolysaccharide-induced hepcidin expression. Exp. Mol. Med. 2017, 49, e408. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- He, W.; Rebello, O.; Savino, R.; Terracciano, R.; Schuster-Klein, C.; Guardiola, B.; Maedler, K. TLR4 triggered complex inflammation in human pancreatic islets. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 2019, 1865, 86–97. [Google Scholar] [CrossRef] [PubMed]
- Kuboniwa, M.; Lamont, R.J. Subgingival biofilm formation. Periodontology 2000 2009, 52, 38–52. [Google Scholar] [CrossRef] [PubMed]
- Maeda, K.; Nagata, H.; Nonaka, A.; Kataoka, K.; Tanaka, M.; Shizukuishi, S. Oral streptococcal glyceraldehyde-3-phosphate dehydrogenase mediates interaction with Porphyromonas gingivalis fimbriae. Microbes Infect. 2004, 6, 1163–1170. [Google Scholar] [CrossRef] [PubMed]
- Rudney, J.; Chen, R.; Zhang, G. Streptococci Dominate the Diverse Flora within Buccal Cells. J. Dent. Res. 2005, 84, 1165–1171. [Google Scholar] [CrossRef]
- Jan, A.T. Outer Membrane Vesicles (OMVs) of Gram-negative Bacteria: A Perspective Update. Front. Microbiol. 2017, 8, 1053. [Google Scholar] [CrossRef]
- Xu, W.; Zhou, W.; Wang, H.; Liang, S. Roles of Porphyromonas gingivalis and its virulence factors in periodontitis. Adv. Protein Chem. Struct. Biol. 2020, 120, 45–84. [Google Scholar] [CrossRef] [PubMed]
- Abdi, K.; Chen, T.; Klein, B.A.; Tai, A.K.; Coursen, J.; Liu, X.; Skinner, J.; Periasamy, S.; Choi, Y.; Kessler, B.M.; et al. Mechanisms by which Porphyromonas gingivalis evades innate immunity. PLoS ONE 2017, 12, e0182164. [Google Scholar] [CrossRef] [Green Version]
- Kadowaki, T.; Baba, A.; Abe, N.; Takii, R.; Hashimoto, M.; Tsukuba, T.; Okazaki, S.; Suda, Y.; Asao, T.; Yamamoto, K. Suppression of Pathogenicity ofPorphyromonas gingivalisby Newly Developed Gingipain Inhibitors. Mol. Pharmacol. 2004, 66, 1599–1606. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benakanakere, M.; Kinane, D.F. Innate Cellular Responses to the Periodontal Biofilm. Front. Oral Biol. 2012, 15, 41–55. [Google Scholar] [CrossRef] [PubMed]
- Takeuchi, H.; Sasaki, N.; Yamaga, S.; Kuboniwa, M.; Matsusaki, M.; Amano, A. Porphyromonas gingivalis induces penetration of lipopolysaccharide and peptidoglycan through the gingival epithelium via degradation of junctional adhesion molecule 1. PLOS Pathog. 2019, 15, e1008124. [Google Scholar] [CrossRef] [PubMed]
- Katz, J.; Yang, Q.-B.; Zhang, P.; Potempa, J.; Travis, J.; Michalek, S.M.; Balkovetz, D.F. Hydrolysis of Epithelial Junctional Proteins by Porphyromonas gingivalis Gingipains. Infect. Immun. 2002, 70, 2512–2518. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Delbosc, S.; Alsac, J.-M.; Journé, C.; Louedec, L.; Castier, Y.; Bonnaure-Mallet, M.; Ruimy, R.; Rossignol, P.; Bouchard, P.; Michel, J.-B.; et al. Porphyromonas gingivalis Participates in Pathogenesis of Human Abdominal Aortic Aneurysm by Neutrophil Activation. Proof of Concept in Rats. PLoS ONE 2011, 6, e18679. [Google Scholar] [CrossRef] [Green Version]
- Figuero, E.; Sánchez-Beltrán, M.; Cuesta-Frechoso, S.; Tejerina, J.M.; del Castro, J.A.; Gutiérrez, J.M.; Herrera, D.; Sanz, M. Detection of Periodontal Bacteria in Atheromatous Plaque by Nested Polymerase Chain Reaction. J. Periodontol. 2011, 82, 1469–1477. [Google Scholar] [CrossRef] [Green Version]
- Stelzel, M.; Conrads, G.; Pankuweit, S.; Maisch, B.; Vogt, S.; Moosdorf, R.; Flores-De-Jacoby, L. Detection of Porphyromonas gingivalisDNA in Aortic Tissue by PCR. J. Periodontol. 2002, 73, 868–870. [Google Scholar] [CrossRef]
- Ilievski, V.; Zuchowska, P.K.; Green, S.J.; Toth, P.; Ragozzino, M.E.; Le, K.; Aljewari, H.W.; O’Brien-Simpson, N.; Reynolds, E.C.; Watanabe, K. Chronic oral application of a periodontal pathogen results in brain inflammation, neurodegeneration and amyloid beta production in wild type mice. PLoS ONE 2018, 13, e0204941. [Google Scholar] [CrossRef] [Green Version]
- Ilievski, V.; Toth, P.; Valyi-Nagy, K.; Valyi-Nagy, T.; Green, S.J.; Marattil, R.S.; Aljewari, H.W.; Wicksteed, B.; O’Brien-Simpson, N.M.; Reynolds, E.C.; et al. Identification of a periodontal pathogen and bihormonal cells in pancreatic islets of humans and a mouse model of periodontitis. Sci. Rep. 2020, 10, 9976. [Google Scholar] [CrossRef]
- Loos, B.G.; Craandijk, J.; Hoek, F.J.; Dillen, P.M.W.-V.; Van Der Velden, U. Elevation of Systemic Markers Related to Cardiovascular Diseases in the Peripheral Blood of Periodontitis Patients. J. Periodontol. 2000, 71, 1528–1534. [Google Scholar] [CrossRef]
- Noack, B.; Genco, R.J.; Trevisan, M.; Grossi, S.; Zambon, J.J.; De Nardin, E. Periodontal Infections Contribute to Elevated Systemic C-Reactive Protein Level. J. Periodontol. 2001, 72, 1221–1227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Demmer, R.T.; Squillaro, A.; Papapanou, P.N.; Rosenbaum, M.; Friedewald, W.T.; Jacobs, D.R.; Desvarieux, M. Periodontal Infection, Systemic Inflammation, and Insulin Resistance. Diabetes Care 2012, 35, 2235–2242. [Google Scholar] [CrossRef] [Green Version]
- Allen, E.M.; Matthews, J.B.; Halloran, D.J.O.; Griffiths, H.R.; Chapple, I.L. Oxidative and inflammatory status in Type 2 diabetes patients with periodontitis: Periodontitis and Diabetes Inflammatory Status. J. Clin. Periodontol. 2011, 38, 894–901. [Google Scholar] [CrossRef] [PubMed]
- D’Aiuto, F.; Gkranias, N.; Bhowruth, D.; Khan, T.; Orlandi, M.; Suvan, J.; Masi, S.; Tsakos, G.; Hurel, S.; Hingorani, A.; et al. Systemic effects of periodontitis treatment in patients with type 2 diabetes: A 12 month, single-centre, investigator-masked, randomised trial. Lancet Diabetes Endocrinol. 2018, 6, 954–965. [Google Scholar] [CrossRef]
- Tsobgny-Tsague, N.-F.; Lontchi-Yimagou, E.; Nana, A.R.N.; Tankeu, A.T.; Katte, J.C.; Dehayem, M.Y.; Bengondo, C.M.; Sobngwi, E. Effects of nonsurgical periodontal treatment on glycated haemoglobin on type 2 diabetes patients (PARODIA 1 study): A randomized controlled trial in a sub-Saharan Africa population. BMC Oral Health 2018, 18, 1–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Artese, H.P.C.; Foz, A.M.; Rabelo, M.D.S.; Gomes, G.H.; Orlandi, M.; Suvan, J.; D’Aiuto, F.; Romito, G.A. Periodontal Therapy and Systemic Inflammation in Type 2 Diabetes Mellitus: A Meta-Analysis. PLoS ONE 2015, 10, e0128344. [Google Scholar] [CrossRef] [Green Version]
- Ilievski, V.; Kinchen, J.M.; Prabhu, R.; Rim, F.; Leoni, L.; Unterman, T.G.; Watanabe, K. Experimental Periodontitis Results in Prediabetes and Metabolic Alterations in Brain, Liver and Heart: Global Untargeted Metabolomic Analyses. J. Oral Biol. (Northborough) 2016, 3. [Google Scholar] [CrossRef] [Green Version]
- Ilievski, V.; Cho, Y.; Katwala, P.; Rodríguez, H.; Tulowiecka, M.; Kurian, D.; Leoni, L.; Christman, J.W.; Unterman, T.G.; Watanabe, K. TLR4 Expression by Liver Resident Cells Mediates the Development of Glucose Intolerance and Insulin Resistance in Experimental Periodontitis. PLoS ONE 2015, 10, e0136502. [Google Scholar] [CrossRef]
- Watanabe, K.; Iizuka, T.; Adeleke, A.; Pham, L.; Shlimon, A.E.; Yasin, M.; Horvath, P.; Unterman, T.G. Involvement of toll-like receptor 4 in alveolar bone loss and glucose homeostasis in experimental periodontitis. J. Periodontal Res. 2010, 46, 21–30. [Google Scholar] [CrossRef] [Green Version]
- Watanabe, K.; Petro, B.J.; Shlimon, A.E.; Unterman, T.G. Effect of Periodontitis on Insulin Resistance and the Onset of Type 2 Diabetes Mellitus in Zucker Diabetic Fatty Rats. J. Periodontol. 2008, 79, 1208–1216. [Google Scholar] [CrossRef]
- Ni, J.; Chen, L.; Zhong, S.; Chai, Q.; Zhang, L.; Wang, D.; Li, S.; Zhang, J. Influence of periodontitis and scaling and root planing on insulin resistance and hepatic CD36 in obese rats. J. Periodontol. 2018, 89, 476–485. [Google Scholar] [CrossRef] [PubMed]
- Colombo, N.H.; Shirakashi, D.J.; Chiba, F.Y.; Coutinho, M.S.D.L.; Ervolino, E.; Garbin, C.A.S.; Machado, U.F.; Sumida, D.H. Periodontal Disease Decreases Insulin Sensitivity and Insulin Signaling. J. Periodontol. 2012, 83, 864–870. [Google Scholar] [CrossRef]
- Sasaki, N.; Katagiri, S.; Komazaki, R.; Watanabe, K.; Maekawa, S.; Shiba, T.; Udagawa, S.; Takeuchi, Y.; Ohtsu, A.; Kohda, T.; et al. Endotoxemia by Porphyromonas gingivalis Injection Aggravates Non-alcoholic Fatty Liver Disease, Disrupts Glucose/Lipid Metabolism, and Alters Gut Microbiota in Mice. Front. Microbiol. 2018, 9, 2470. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chaffee, B.W.; Weston, S.J. Association Between Chronic Periodontal Disease and Obesity: A Systematic Review and Meta-Analysis. J. Periodontol. 2010, 81, 1708–1724. [Google Scholar] [CrossRef] [PubMed]
- Singh, S.P.; Huck, O.; Abraham, N.G.; Amar, S. Kavain Reduces Porphyromonas Gingivalis–Induced Adipocyte Inflammation: Role of PGC-1α Signaling. J. Immunol. 2018, 201, 1491–1499. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamaguchi, M.; Nishimura, F.; Naruishi, H.; Soga, Y.; Kokeguchi, S.; Takashiba, S. Thiazolidinedione (Pioglitazone) Blocks P. gingivalis- and F. nucleatum, but not E. coli, Lipopolysaccharide (LPS)-induced Interleukin-6 (IL-6) Production in Adipocytes. J. Dent. Res. 2005, 84, 240–244. [Google Scholar] [CrossRef]
- Singh, S.P.; Grant, I.; Meissner, A.; Kappas, A.; Abraham, N.G. Ablation of adipose-HO-1 expression increases white fat over beige fat through inhibition of mitochondrial fusion and of PGC1α in female mice. Horm. Mol. Biol. Clin. Investig. 2017, 31, 31. [Google Scholar] [CrossRef]
- Kuraji, R.; Sekino, S.; Kapila, Y.; Numabe, Y. Periodontal disease–related nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: An emerging concept of oral-liver axis. Periodontology 2000 2021, 87, 204–240. [Google Scholar] [CrossRef]
- Alazawi, W.; Bernabe, E.; Tai, D.; Janicki, T.; Kemos, P.; Samsuddin, S.; Syn, W.-K.; Gillam, D.; Turner, W. Periodontitis is associated with significant hepatic fibrosis in patients with non-alcoholic fatty liver disease. PLoS ONE 2017, 12, e0185902. [Google Scholar] [CrossRef] [Green Version]
- Wilson, C.G.; Tran, J.L.; Erion, D.M.; Vera, N.B.; Febbraio, M.; Weiss, E.J. Hepatocyte-Specific Disruption of CD36 Attenuates Fatty Liver and Improves Insulin Sensitivity in HFD-Fed Mice. Endocrinology 2016, 157, 570–585. [Google Scholar] [CrossRef] [Green Version]
- Ahn, J.-S.; Yang, J.W.; Oh, S.-J.; Shin, Y.Y.; Kang, M.-J.; Park, H.R.; Seo, Y.; Kim, H.-S. Porphyromonas gingivalis exacerbates the progression of fatty liver disease via CD36-PPARγ pathway. BMB Rep. 2021, 54, 323–328. [Google Scholar] [CrossRef]
- Ishikawa, M.; Yoshida, K.; Okamura, H.; Ochiai, K.; Takamura, H.; Fujiwara, N.; Ozaki, K. Oral Porphyromonas gingivalis translocates to the liver and regulates hepatic glycogen synthesis through the Akt/GSK-3β signaling pathway. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 2013, 1832, 2035–2043. [Google Scholar] [CrossRef] [Green Version]
- Takano, M.; Sugano, N.; Mochizuki, S.; Koshi, R.N.; Narukawa, T.S.; Sawamoto, Y.; Ito, K. Hepatocytes produce tumor necrosis factor-α and interleukin-6 in response to Porphyromonas gingivalis. J. Periodontal Res. 2011, 47, 89–94. [Google Scholar] [CrossRef]
- Mitsuhashi, K.; Nosho, K.; Sukawa, Y.; Matsunaga, Y.; Ito, M.; Kurihara, H.; Kanno, S.; Igarashi, H.; Naito, T.; Adachi, Y.; et al. Association ofFusobacteriumspecies in pancreatic cancer tissues with molecular features and prognosis. Oncotarget 2015, 6, 7209–7220. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bhat, U.G.; Ilievski, V.; Unterman, T.G.; Watanabe, K. Porphyromonas gingivalisLipopolysaccharide Upregulates Insulin Secretion From Pancreatic β Cell Line MIN6. J. Periodontol. 2014, 85, 1629–1636. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bhat, U.G.; Watanabe, K. Serpine1 Mediates Porphyromonas gingivalis Induced Insulin Secretion in the Pancreatic Beta Cell Line MIN6. J. Oral Biol. (Northborough) 2015, 2, 2. [Google Scholar] [CrossRef] [Green Version]
- Bastard, J.-P.; Hainque, B. Relationship between plasma plasminogen activator inhibitor 1 and insulin resistance. Diabetes/Metab. Res. Rev. 2000, 16, 192–201. [Google Scholar] [CrossRef]
- Ilievski, V.; Bhat, U.G.; Suleiman-Ata, S.; Bauer, B.A.; Toth, P.; Olson, S.T.; Unterman, T.G.; Watanabe, K. Oral application of a periodontal pathogen impacts SerpinE1 expression and pancreatic islet architecture in prediabetes. J. Periodontal Res. 2017, 52, 1032–1041. [Google Scholar] [CrossRef]
- Chakravarthy, H.; Gu, X.; Enge, M.; Dai, X.; Wang, Y.; Damond, N.; Downie, C.; Liu, K.; Wang, J.; Xing, Y.; et al. Converting Adult Pancreatic Islet α Cells into β Cells by Targeting Both Dnmt1 and Arx. Cell Metab. 2017, 25, 622–634. [Google Scholar] [CrossRef] [Green Version]
- Thorel, F.; Népote, V.; Avril, I.; Kohno, K.; Desgraz, R.; Chera, S.; Herrera, P.L. Conversion of adult pancreatic α-cells to β-cells after extreme β-cell loss. Nature 2010, 464, 1149–1154. [Google Scholar] [CrossRef] [Green Version]
- Mezza, T.; Sorice, G.P.; Conte, C.; Sun, V.A.; Cefalo, C.M.A.; Moffa, S.; Pontecorvi, A.; Mari, A.; Kulkarni, R.N.; Giaccari, A. β-Cell Glucose Sensitivity Is Linked to Insulin/Glucagon Bihormonal Cells in Nondiabetic Humans. J. Clin. Endocrinol. Metab. 2016, 101, 470–475. [Google Scholar] [CrossRef] [Green Version]
- Kwon, T.; Lamster, I.B.; Levin, L. Current Concepts in the Management of Periodontitis. Int. Dent. J. 2021, 71, 462–476. [Google Scholar] [CrossRef]
- Teughels, W.; Feres, M.; Oud, V.; Martín, C.; Matesanz, P.; Herrera, D. Adjunctive effect of systemic antimicrobials in periodontitis therapy: A systematic review and meta-analysis. J. Clin. Periodontol. 2020, 47, 257–281. [Google Scholar] [CrossRef] [PubMed]
- Palaiologou, A.A.; Schiavo, J.H.; Maney, P. Surgical Treatment of Periodontal Diseases—A Review of Current Clinical Research. Curr. Oral Health Rep. 2019, 6, 198–208. [Google Scholar] [CrossRef]
- Koop, R.; Merheb, J.; Quirynen, M. Periodontal Regeneration with Enamel Matrix Derivative in Reconstructive Periodontal Therapy: A Systematic Review. J. Periodontol. 2012, 83, 707–720. [Google Scholar] [CrossRef]
- Khoshkam, V.; Chan, H.-L.; Lin, G.-H.; Mailoa, J.; Giannobile, W.V.; Wang, H.-L.; Oh, T.-J. Outcomes of regenerative treatment with rhPDGF-BB and rhFGF-2 for periodontal intra-bony defects: A systematic review and meta-analysis. J. Clin. Periodontol. 2015, 42, 272–280. [Google Scholar] [CrossRef] [PubMed]
- Doyle-Delgado, D.K.; Chamberlain, J.J.; Shubrook, D.J.H.; Skolnik, N.; Trujillo, J. Pharmacologic Approaches to Glycemic Treatment of Type 2 Diabetes: Synopsis of the 2020 American Diabetes Association’s Standards of Medical Care in Diabetes Clinical Guideline. Ann. Intern. Med. 2020, 173, 813–821. [Google Scholar] [CrossRef]
- Bailey, C.J.; Day, C. Treatment of type 2 diabetes: Future approaches. Br. Med. Bull. 2018, 126, 123–137. [Google Scholar] [CrossRef] [Green Version]
- Brown, D.X.; Evans, M. Choosing between GLP-1 Receptor Agonists and DPP-4 Inhibitors: A Pharmacological Perspective. J. Nutr. Metab. 2012, 2012, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Joshi, S.R.; Standl, E.; Tong, N.; Shah, P.; Kalra, S.; Rathod, R. Therapeutic potential of α-glucosidase inhibitors in type 2 diabetes mellitus: An evidence-based review. Expert Opin. Pharmacother. 2015, 16, 1959–1981. [Google Scholar] [CrossRef]
- Reddy, R.P.M.; Inzucchi, S.E. SGLT2 inhibitors in the management of type 2 diabetes. Endocrine 2016, 53, 364–372. [Google Scholar] [CrossRef] [PubMed]
- Sands, A.T.; Zambrowicz, B.P.; Rosenstock, J.; Lapuerta, P.; Bode, B.W.; Garg, S.K.; Buse, J.B.; Banks, P.; Heptulla, R.; Rendell, M.; et al. Sotagliflozin, a Dual SGLT1 and SGLT2 Inhibitor, as Adjunct Therapy to Insulin in Type 1 Diabetes. Diabetes Care 2015, 38, 1181–1188. [Google Scholar] [CrossRef] [Green Version]
- Scalbert, A.; Williamson, G. Dietary Intake and Bioavailability of Polyphenols. J. Nutr. 2000, 130, 2073S–2085S. [Google Scholar] [CrossRef]
- Kawabata, K.; Yoshioka, Y.; Terao, J. Role of Intestinal Microbiota in the Bioavailability and Physiological Functions of Dietary Polyphenols. Molecules 2019, 24, 370. [Google Scholar] [CrossRef] [Green Version]
- Rice-Evans, C.A.; Miller, N.J.; Paganga, G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 1996, 20, 933–956. [Google Scholar] [CrossRef]
- Manach, C.; Scalbert, A.; Morand, C.; Rémésy, C.; Jiménez, L. Polyphenols: Food sources and bioavailability. Am. J. Clin. Nutr. 2004, 79, 727–747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Clifford, M.N.; Scalbert, A. Ellagitannins—Nature, Occurrence and Dietary Burden. J. Sci. Food Agric. 2000, 80, 1118–1125. [Google Scholar] [CrossRef]
- Woodward, K.A.; Draijer, R.; Thijssen, D.H.J.; Low, D.A. Polyphenols and Microvascular Function in Humans: A Systematic Review. Curr. Pharm. Des. 2018, 24, 203–226. [Google Scholar] [CrossRef] [Green Version]
- Weiskirchen, S.; Weiskirchen, R. Resveratrol: How Much Wine Do You Have to Drink to Stay Healthy? Adv. Nutr. 2016, 7, 706–718. [Google Scholar] [CrossRef] [Green Version]
- Adlercreutz, H.; Mazur, W. Phyto-oestrogens and Western Diseases. Ann. Med. 1997, 29, 95–120. [Google Scholar] [CrossRef]
- Septembre-Malaterre, A.; Stanislas, G.; Douraguia, E.; Gonthier, M.-P. Evaluation of nutritional and antioxidant properties of the tropical fruits banana, litchi, mango, papaya, passion fruit and pineapple cultivated in Réunion French Island. Food Chem. 2016, 212, 225–233. [Google Scholar] [CrossRef]
- Taïlé, J.; Arcambal, A.; Clerc, P.; Gauvin-Bialecki, A.; Gonthier, M.-P. Medicinal Plant Polyphenols Attenuate Oxidative Stress and Improve Inflammatory and Vasoactive Markers in Cerebral Endothelial Cells during Hyperglycemic Condition. Antioxidants 2020, 9, 573. [Google Scholar] [CrossRef] [PubMed]
- Septembre-Malaterre, A.; Le Sage, F.; Hatia, S.; Catan, A.; Janci, L.; Gonthier, M.-P. Curcuma longapolyphenols improve insulin-mediated lipid accumulation and attenuate proinflammatory response of 3T3-L1 adipose cells during oxidative stress through regulation of key adipokines and antioxidant enzymes. BioFactors 2016, 42, 418–430. [Google Scholar] [CrossRef] [PubMed]
- D’Archivio, M.; Filesi, C.; Di Benedetto, R.; Gargiulo, R.; Giovannini, C.; Masella, R. Polyphenols, dietary sources and bioavailability. Ann. Ist. Super. Sanita 2007, 43, 348. [Google Scholar]
- Cardona, F.; Andrés-Lacueva, C.; Tulipani, S.; Tinahones, F.J.; Queipo-Ortuño, M.I. Benefits of polyphenols on gut microbiota and implications in human health. J. Nutr. Biochem. 2013, 24, 1415–1422. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Spencer, J.P.; El Mohsen, M.M.A.; Rice-Evans, C. Cellular uptake and metabolism of flavonoids and their metabolites: Implications for their bioactivity. Arch. Biochem. Biophys. 2004, 423, 148–161. [Google Scholar] [CrossRef]
- Danielsen, E.T. Glycol chitosan: A stabilizer of lipid rafts in the intestinal brush border. Biochim. Biophys. Acta (BBA) Biomembr. 2017, 1859, 360–367. [Google Scholar] [CrossRef]
- Williamson, G.; Clifford, M.N. Role of the small intestine, colon and microbiota in determining the metabolic fate of polyphenols. Biochem. Pharmacol. 2017, 139, 24–39. [Google Scholar] [CrossRef] [Green Version]
- Gonthier, M.-P.; Verny, M.-A.; Besson, C.; Rémésy, C.; Scalbert, A. Chlorogenic Acid Bioavailability Largely Depends on Its Metabolism by the Gut Microflora in Rats. J. Nutr. 2003, 133, 1853–1859. [Google Scholar] [CrossRef] [Green Version]
- Gonthier, M.-P.; Cheynier, V.; Donovan, J.L.; Manach, C.; Morand, C.; Mila, I.; Lapierre, C.; Rémésy, C.; Scalbert, A. Microbial Aromatic Acid Metabolites Formed in the Gut Account for a Major Fraction of the Polyphenols Excreted in Urine of Rats Fed Red Wine Polyphenols. J. Nutr. 2003, 133, 461–467. [Google Scholar] [CrossRef] [Green Version]
- Gonthier, M.-P.; Donovan, J.L.; Texier, O.; Felgines, C.; Remesy, C.; Scalbert, A. Metabolism of dietary procyanidins in rats. Free Radic. Biol. Med. 2003, 35, 837–844. [Google Scholar] [CrossRef]
- Brial, F.; Chilloux, J.; Nielsen, T.; Vieira-Silva, S.; Falony, G.; Andrikopoulos, P.; Olanipekun, M.; Hoyles, L.; Djouadi, F.; Neves, A.L.; et al. Human and preclinical studies of the host–gut microbiome co-metabolite hippurate as a marker and mediator of metabolic health. Gut 2021, 70, 2105–2114. [Google Scholar] [CrossRef] [PubMed]
- Zheng, W.; Ma, Y.; Zhao, A.; He, T.; Lyu, N.; Pan, Z.; Mao, G.; Liu, Y.; Li, J.; Wang, P.; et al. Compositional and functional differences in human gut microbiome with respect to equol production and its association with blood lipid level: A cross-sectional study. Gut Pathog. 2019, 11, 20. [Google Scholar] [CrossRef] [PubMed]
- González-Sarrías, A.; Núñez-Sánchez, M.Á.; Tomás-Barberán, F.A.; Espín, J.C. Neuroprotective Effects of Bioavailable Polyphenol-Derived Metabolites against Oxidative Stress-Induced Cytotoxicity in Human Neuroblastoma SH-SY5Y Cells. J. Agric. Food Chem. 2017, 65, 752–758. [Google Scholar] [CrossRef] [Green Version]
- Chang, H.C.; Churchwell, M.I.; Delclos, K.B.; Newbold, R.R.; Doerge, D.R. Mass Spectrometric Determination of Genistein Tissue Distribution in Diet-Exposed Sprague-Dawley Rats. J. Nutr. 2000, 130, 1963–1970. [Google Scholar] [CrossRef] [Green Version]
- Kim, S.; Lee, M.-J.; Hong, J.; Li, C.; Smith, T.J.; Yang, G.-Y.; Seril, D.N.; Yang, C.S. Plasma and Tissue Levels of Tea Catechins in Rats and Mice During Chronic Consumption of Green Tea Polyphenols. Nutr. Cancer 2000, 37, 41–48. [Google Scholar] [CrossRef]
- Vitrac, X.; Desmoulière, A.; Brouillaud, B.; Krisa, S.; Deffieux, G.; Barthe, N.; Rosenbaum, J.; Mérillon, J.-M. Distribution of [14C]-trans-resveratrol, a cancer chemopreventive polyphenol, in mouse tissues after oral administration. Life Sci. 2003, 72, 2219–2233. [Google Scholar] [CrossRef]
- Arcambal, A.; Taïlé, J.; Couret, D.; Planesse, C.; Veeren, B.; Diotel, N.; Gauvin-Bialecki, A.; Meilhac, O.; Gonthier, M. Protective Effects of Antioxidant Polyphenols against Hyperglycemia-Mediated Alterations in Cerebral Endothelial Cells and a Mouse Stroke Model. Mol. Nutr. Food Res. 2020, 64, e1900779. [Google Scholar] [CrossRef]
- Margalef, M.; Pons, Z.; Carres, L.I.; Quiñones, M.; Bravo, F.I.; Arola-Arnal, A.; Muguerza, B. Rat health status affects bioavailability, target tissue levels, and bioactivity of grape seed flavanols. Mol. Nutr. Food Res. 2016, 61, 61. [Google Scholar] [CrossRef]
- Morand, C.; De Roos, B.; Garcia-Conesa, M.T.; Gibney, E.R.; Landberg, R.; Manach, C.; Milenkovic, D.; Rodriguez-Mateos, A.; Van de Wiele, T.; Tomas-Barberan, F. Why interindividual variation in response to consumption of plant food bioactives matters for future personalised nutrition. Proc. Nutr. Soc. 2020, 79, 225–235. [Google Scholar] [CrossRef]
- Morand, C.; Tomás Barberán, F.A. Contribution of plant food bioactives in promoting health effects of plant foods: Why look at interindividual variability? Eur. J. Nutr. 2019, 58, 13–19. [Google Scholar] [CrossRef] [Green Version]
- Ulaszewska, M.; Vázquez-Manjarrez, N.; Garcia-Aloy, M.; Llorach, R.; Mattivi, F.; Dragsted, L.O.; Praticò, G.; Manach, C. Food intake biomarkers for apple, pear, and stone fruit. Genes Nutr. 2018, 13, 1–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ulaszewska, M.M.; Weinert, C.H.; Trimigno, A.; Portmann, R.; Andres Lacueva, C.; Badertscher, R.; Brennan, L.; Brunius, C.; Bub, A.; Capozzi, F.; et al. Nutrimetabolomics: An Integrative Action for Metabolomic Analyses in Human Nutritional Studies. Mol. Nutr. Food Res. 2019, 63, e1800384. [Google Scholar] [CrossRef] [PubMed]
- Rahman, M.; Rahaman, S.; Islam, R.; Rahman, F.; Mithi, F.M.; Alqahtani, T.; Almikhlafi, M.A.; Alghamdi, S.Q.; Alruwaili, A.S.; Hossain, S.; et al. Role of Phenolic Compounds in Human Disease: Current Knowledge and Future Prospects. Molecules 2021, 27, 233. [Google Scholar] [CrossRef] [PubMed]
- Siriwardhana, N.; Kalupahana, N.S.; Cekanova, M.; LeMieux, M.; Greer, B.; Moustaid-Moussa, N. Modulation of adipose tissue inflammation by bioactive food compounds. J. Nutr. Biochem. 2013, 24, 613–623. [Google Scholar] [CrossRef]
- Hatia, S.; Septembre-Malaterre, A.; Le Sage, F.; Badiou-Bénéteau, A.; Baret, P.; Payet, B.; D’Hellencourt, C.L.; Gonthier, M.-P. Evaluation of antioxidant properties of major dietary polyphenols and their protective effect on 3T3-L1 preadipocytes and red blood cells exposed to oxidative stress. Free Radic. Res. 2014, 48, 387–401. [Google Scholar] [CrossRef]
- Marimoutou, M.; Le Sage, F.; Smadja, J.; D’Hellencourt, C.L.; Gonthier, M.-P.; Silva, C.R.-D. Antioxidant polyphenol-rich extracts from the medicinal plants Antirhea borbonica, Doratoxylon apetalum and Gouania mauritiana protect 3T3-L1 preadipocytes against H2O2, TNFα and LPS inflammatory mediators by regulating the expression of superoxide dismutase and NF-κB genes. J. Inflamm. 2015, 12, 1–15. [Google Scholar] [CrossRef] [Green Version]
- Weisberg, S.P.; Leibel, R.; Tortoriello, D.V. Dietary Curcumin Significantly Improves Obesity-Associated Inflammation and Diabetes in Mouse Models of Diabesity. Endocrinology 2008, 149, 3549–3558. [Google Scholar] [CrossRef] [Green Version]
- Kim, S.; Jin, Y.; Choi, Y.; Park, T. Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice. Biochem. Pharmacol. 2011, 81, 1343–1351. [Google Scholar] [CrossRef] [PubMed]
- Dhanya, R. Quercetin for managing type 2 diabetes and its complications, an insight into multitarget therapy. Biomed. Pharmacother. 2021, 146, 112560. [Google Scholar] [CrossRef]
- Khan, N.; Mukhtar, H. Tea Polyphenols in Promotion of Human Health. Nutrients 2018, 11, 39. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cheng, A.-S.; Cheng, Y.-H.; Chiou, C.-H.; Chang, T.-L. Resveratrol Upregulates Nrf2 Expression To Attenuate Methylglyoxal-Induced Insulin Resistance in Hep G2 Cells. J. Agric. Food Chem. 2012, 60, 9180–9187. [Google Scholar] [CrossRef] [PubMed]
- Daayf, F.; Lattanzio, V. Recent Advances in Polyphenol Research; Wiley-Blackwell: Oxford, UK, 2008; ISBN 978-1-4051-5837-4. [Google Scholar]
- Luna-Vital, D.A.; De Mejia, E.G. Anthocyanins from purple corn activate free fatty acid-receptor 1 and glucokinase enhancing in vitro insulin secretion and hepatic glucose uptake. PLoS ONE 2018, 13, e0200449. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Muscarà, C.; Molonia, M.S.; Speciale, A.; Bashllari, R.; Cimino, F.; Occhiuto, C.; Saija, A.; Cristani, M. Anthocyanins ameliorate palmitate-induced inflammation and insulin resistance in 3T3-L1 adipocytes. Phytother. Res. 2019, 33, 1888–1897. [Google Scholar] [CrossRef]
- Na, L.-X.; Zhang, Y.-L.; Li, Y.; Liu, L.-Y.; Li, R.; Kong, T.; Sun, C.-H. Curcumin improves insulin resistance in skeletal muscle of rats. Nutr. Metab. Cardiovasc. Dis. 2011, 21, 526–533. [Google Scholar] [CrossRef]
- Do, G.-M.; Jung, U.J.; Park, H.-J.; Kwon, E.-Y.; Jeon, S.-M.; McGregor, R.A.; Choi, M.-S. Resveratrol ameliorates diabetes-related metabolic changes via activation of AMP-activated protein kinase and its downstream targets in db/db mice. Mol. Nutr. Food Res. 2012, 56, 1282–1291. [Google Scholar] [CrossRef]
- Lee, Y.-E.; Kim, J.-W.; Lee, E.-M.; Ahn, Y.-B.; Song, K.-H.; Yoon, K.-H.; Kim, H.-W.; Park, C.-W.; Li, G.; Liu, Z.; et al. Chronic Resveratrol Treatment Protects Pancreatic Islets against Oxidative Stress in db/db Mice. PLoS ONE 2012, 7, e50412. [Google Scholar] [CrossRef]
- He, H.-J.; Wang, G.-Y.; Gao, Y.; Ling, W.-H.; Guo-Yu, W.; Jin, T.-R. Curcumin attenuates Nrf2 signaling defect, oxidative stress in muscle and glucose intolerance in high fat diet-fed mice. World J. Diabetes 2012, 3, 94–104. [Google Scholar] [CrossRef]
- Hartogh, D.J.D.; Vlavcheski, F.; Giacca, A.; Tsiani, E. Attenuation of Free Fatty Acid (FFA)-Induced Skeletal Muscle Cell Insulin Resistance by Resveratrol is Linked to Activation of AMPK and Inhibition of mTOR and p70 S6K. Int. J. Mol. Sci. 2020, 21, 4900. [Google Scholar] [CrossRef]
- Raimundo, A.F.; Félix, F.; Andrade, R.; García-Conesa, M.-T.; González-Sarrías, A.; Gilsa-Lopes, J.; do Ó, D.; Ribeiro, R.; Rodriguez-Mateos, A.; Santos, C.N.; et al. Combined effect of interventions with pure or enriched mixtures of (poly)phenols and anti-diabetic medication in type 2 diabetes management: A meta-analysis of randomized controlled human trials. Eur. J. Nutr. 2020, 59, 1329–1343. [Google Scholar] [CrossRef]
- Chuengsamarn, S.; Rattanamongkolgul, S.; Luechapudiporn, R.; Phisalaphong, C.; Jirawatnotai, S. Curcumin Extract for Prevention of Type 2 Diabetes. Diabetes Care 2012, 35, 2121–2127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Na, L.-X.; Li, Y.; Pan, H.-Z.; Zhou, X.-L.; Sun, D.-J.; Meng, M.; Li, X.-X.; Sun, C.-H. Curcuminoids exert glucose-lowering effect in type 2 diabetes by decreasing serum free fatty acids: A double-blind, placebo-controlled trial. Mol. Nutr. Food Res. 2012, 57, 1569–1577. [Google Scholar] [CrossRef] [PubMed]
- Karandish, M.; Mozaffari-Khosravi, H.; Mohammadi, S.M.; Cheraghian, B.; Azhdari, M. The effect of curcumin and zinc co-supplementation on glycemic parameters in overweight or obese prediabetic subjects: A phase 2 randomized, placebo-controlled trial with a multi-arm, parallel-group design. Phytother. Res. 2021, 35, 4377–4387. [Google Scholar] [CrossRef] [PubMed]
- Caricilli, A.M.; Saad, M.J.A. The Role of Gut Microbiota on Insulin Resistance. Nutrients 2013, 5, 829–851. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tzounis, X.; Vulevic, J.; Kuhnle, G.G.C.; George, T.; Leonczak, J.; Gibson, G.R.; Kwik-Uribe, C.; Spencer, J.P.E. Flavanol monomer-induced changes to the human faecal microflora. Br. J. Nutr. 2008, 99, 782–792. [Google Scholar] [CrossRef] [Green Version]
- Etxeberria, U.; Fernandez-Quintela, A.; Milagro, F.I.; Aguirre, L.; Martínez, J.A.; Portillo, M.P. Impact of Polyphenols and Polyphenol-Rich Dietary Sources on Gut Microbiota Composition. J. Agric. Food Chem. 2013, 61, 9517–9533. [Google Scholar] [CrossRef] [PubMed]
- Gibson, G.R.; Hutkins, R.; Sanders, M.E.; Prescott, S.L.; Reimer, R.A.; Salminen, S.J.; Scott, K.; Stanton, C.; Swanson, K.S.; Cani, P.D.; et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 2017, 14, 491–502. [Google Scholar] [CrossRef] [Green Version]
- Belda, E.; Voland, L.; Tremaroli, V.; Falony, G.; Adriouch, S.; Assmann, K.E.; Prifiti, E.; Aron-Wisnewsky, J.; Debédat, J.; Le Roy, T.; et al. Impairment of gut microbial biotin metabolism and host biotin status in severe obesity: Effect of biotin and prebiotic supplementation on improved metabolism. Gut 2022. [Google Scholar] [CrossRef]
- Blaut, M.; Clavel, T. Metabolic Diversity of the Intestinal Microbiota: Implications for Health and Disease. J. Nutr. 2007, 137, 751S–755S. [Google Scholar] [CrossRef]
- Rizzo, A.; Bevilacqua, N.; Guida, L.; Annunziata, M.; Carratelli, C.R.; Paolillo, R. Effect of resveratrol and modulation of cytokine production on human periodontal ligament cells. Cytokine 2012, 60, 197–204. [Google Scholar] [CrossRef]
- Le Sage, F.; Meilhac, O.; Gonthier, M.-P. Anti-inflammatory and antioxidant effects of polyphenols extracted from Antirhea borbonica medicinal plant on adipocytes exposed to Porphyromonas gingivalis and Escherichia coli lipopolysaccharides. Pharmacol. Res. 2017, 119, 303–312. [Google Scholar] [CrossRef] [PubMed]
- Kajiura, Y.; Nishikawa, Y.; Lew, J.H.; Kido, J.-I.; Nagata, T.; Naruishi, K. β-carotene suppresses Porphyromonas gingivalis lipopolysaccharide-mediated cytokine production in THP-1 monocytes cultured with high glucose condition: β-Carotene Suppresses Cytokine Production. Cell Biol. Int. 2018, 42, 105–111. [Google Scholar] [CrossRef] [PubMed]
- Nishigaki, M.; Yamamoto, T.; Ichioka, H.; Honjo, K.-I.; Yamamoto, K.; Oseko, F.; Kita, M.; Mazda, O.; Kanamura, N. β-cryptoxanthin regulates bone resorption related-cytokine production in human periodontal ligament cells. Arch. Oral Biol. 2013, 58, 880–886. [Google Scholar] [CrossRef]
- Kose, O.; Arabaci, T.; Yemenoglu, H.; Kara, A.; Ozkanlar, S.; Kayis, S.; Duymus, Z.Y. Influences of Fucoxanthin on Alveolar Bone Resorption in Induced Periodontitis in Rat Molars. Mar. Drugs 2016, 14, 70. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shadisvaaran, S.; Chin, K.-Y.; Shahida, M.-S.; Ima-Nirwana, S.; Leong, X.-F. Effect of vitamin E on periodontitis: Evidence and proposed mechanisms of action. J. Oral Biosci. 2021, 63, 97–103. [Google Scholar] [CrossRef]
- Aytekin, Z.; Arabacı, T.; Toraman, A.; Bayır, Y.; Albayrak, M.; Üstün, K. Immune modulatory and antioxidant effects of locally administrated vitamin C in experimental periodontitis in rats. Acta Odontol. Scand. 2020, 78, 425–432. [Google Scholar] [CrossRef]
- Nakajima, M.; Arimatsu, K.; Kato, T.; Matsuda, Y.; Minagawa, T.; Takahashi, N.; Ohno, H.; Yamazaki, K. Oral Administration of P. gingivalis Induces Dysbiosis of Gut Microbiota and Impaired Barrier Function Leading to Dissemination of Enterobacteria to the Liver. PLoS ONE 2015, 10, e0134234. [Google Scholar] [CrossRef] [Green Version]
- Iwamoto, Y.; Nishimura, F.; Nakagawa, M.; Sugimoto, H.; Shikata, K.; Makino, H.; Fukuda, T.; Tsuji, T.; Iwamoto, M.; Murayama, Y. The Effect of Antimicrobial Periodontal Treatment on Circulating Tumor Necrosis Factor-Alpha and Glycated Hemoglobin Level in Patients With Type 2 Diabetes. J. Periodontol. 2001, 72, 774–778. [Google Scholar] [CrossRef]
- Demmer, R.T.; Jacobs, D.R.; Desvarieux, M. Periodontal Disease and Incident Type 2 Diabetes: Results from the First National Health and Nutrition Examination Survey and Its Epidemiologic Follow-up Study. Diabetes Care 2008, 31, 1373–1379. [Google Scholar] [CrossRef] [Green Version]
- Borgnakke, W.S.; Poudel, P. Diabetes and Oral Health: Summary of Current Scientific Evidence for Why Transdisciplinary Collaboration Is Needed. Front. Dent. Med. 2021, 2, 2. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Thouvenot, K.; Turpin, T.; Taïlé, J.; Clément, K.; Meilhac, O.; Gonthier, M.-P. Links between Insulin Resistance and Periodontal Bacteria: Insights on Molecular Players and Therapeutic Potential of Polyphenols. Biomolecules 2022, 12, 378. https://doi.org/10.3390/biom12030378
Thouvenot K, Turpin T, Taïlé J, Clément K, Meilhac O, Gonthier M-P. Links between Insulin Resistance and Periodontal Bacteria: Insights on Molecular Players and Therapeutic Potential of Polyphenols. Biomolecules. 2022; 12(3):378. https://doi.org/10.3390/biom12030378
Chicago/Turabian StyleThouvenot, Katy, Teva Turpin, Janice Taïlé, Karine Clément, Olivier Meilhac, and Marie-Paule Gonthier. 2022. "Links between Insulin Resistance and Periodontal Bacteria: Insights on Molecular Players and Therapeutic Potential of Polyphenols" Biomolecules 12, no. 3: 378. https://doi.org/10.3390/biom12030378