Anti-inflammatory and antioxidant effects of polyphenols extracted from Antirhea borbonica medicinal plant on adipocytes exposed to Porphyromonas gingivalis and Escherichia coli lipopolysaccharides

Pharmacological Research

Volumn 119, Issue , 2017, Pages 303-312

  Le Sage, Fanny ^a,b   Meilhac, Olivier ^a,b,c   Gonthier, Marie Paule ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE LA RÉUNION   (France)

^c Centre d'Investigations Cliniques   (France)

Author keywords

Adipocytes; antioxidants; inflammation; LPS; oxidative stress; plant polyphenols

Indexed keywords

ADIPONECTIN; ANTIRHEA BORBONICA EXTRACT; CAFFEIC ACID; CHLOROGENIC ACID; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; KAEMPFEROL; MANGANESE SUPEROXIDE DISMUTASE; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PLANT EXTRACT; PLASMINOGEN ACTIVATOR INHIBITOR 1; POLYPHENOL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; RESISTIN; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; LIPOPOLYSACCHARIDE;

3T3 CELL LINE; ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ANTIRHEA BORBONICA; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DRUG SCREENING; GENE EXPRESSION REGULATION; INSULIN RESISTANCE; MOUSE; NONHUMAN; OBESITY; PORPHYROMONAS GINGIVALIS; RUBIACEAE; SIGNAL TRANSDUCTION; UPREGULATION; 3T3-L1 CELL LINE; ANIMAL; BACTEROIDACEAE INFECTIONS; CHEMISTRY; DRUG EFFECTS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; IMMUNOLOGY; INFLAMMATION; ISOLATION AND PURIFICATION; MEDICINAL PLANT; MICROBIOLOGY; OXIDATIVE STRESS;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; BACTEROIDACEAE INFECTIONS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; OXIDATIVE STRESS; PLANTS, MEDICINAL; POLYPHENOLS; PORPHYROMONAS GINGIVALIS; RUBIACEAE;

EID: 85014324330     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2017.02.020     Document Type: Article

References (59)

1. [1] Backhed, F., Ding, H., Wang, T., Hooper, L.V., Koh, G.Y., Nagy, A., Semenkovich, C.F., Gordon, J.I., The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U. S. A. 101:44 (2004), 15718–15723.
2. [2] Cani, P.D., Amar, J., Iglesias, M.A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A.M., Fava, F., Tuohy, K.M., Chabo, C., Waget, A., Delmee, E., Cousin, B., Sulpice, T., Chamontin, B., Ferrieres, J., Tanti, J.F., Gibson, G.R., Casteilla, L., Delzenne, N.M., Alessi, M.C., Burcelin, R., Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:7 (2007), 1761–1772.
3. [3] Hersoug, L.G., Moller, P., Loft, S., Gut microbiota-derived lipopolysaccharide uptake and trafficking to adipose tissue: implications for inflammation and obesity. Obes. Rev.: Off. J. Int. Assoc. Study Obes. 17:4 (2016), 297–312.
4. [4] Akira, S., Takeda, K., Toll-like receptor signalling. Nat. Rev. Immunol. 4:7 (2004), 499–511.
5. [5] Bes-Houtmann, S., Roche, R., Hoareau, L., Gonthier, M.P., Festy, F., Caillens, H., Gasque, P., Lefebvre d'Hellencourt, C., Cesari, M., Presence of functional TLR2 and TLR4 on human adipocytes. Histochem. Cell Biol. 127:2 (2007), 131–137.
6. [6] Kang, Y.E., Kim, J.M., Joung, K.H., Lee, J.H., You, B.R., Choi, M.J., Ryu, M.J., Ko, Y.B., Lee, M.A., Lee, J., Ku, B.J., Shong, M., Lee, K.H., Kim, H.J., The roles of adipokines, proinflammatory cytokines, and adipose tissue macrophages in obesity-associated insulin resistance in modest obesity and early metabolic dysfunction. PLOS ONE, 11(4), 2016, e0154003.
7. [7] Bullon, P., Roman-Malo, L., Marin-Aguilar, F., Alvarez-Suarez, J.M., Giampieri, F., Battino, M., Cordero, M.D., Lipophilic antioxidants prevent lipopolysaccharide-induced mitochondrial dysfunction through mitochondrial biogenesis improvement. Pharmacol. Res. 91 (2015), 1–8.
8. 2, TNFalpha and LPS inflammatory mediators by regulating the expression of superoxide dismutase and NF-kappaB genes. J. Inflamm. (London, England), 12, 2015, 10.
9. [9] de Ferranti, S., Mozaffarian, D., The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clin. Chem. 54:6 (2008), 945–955.
10. [10] Houstis, N., Rosen, E.D., Lander, E.S., Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440:7086 (2006), 944–948.
11. [11] Taira, R., Yamaguchi, S., Shimizu, K., Nakamura, K., Ayabe, T., Taira, T., Bacterial cell wall components regulate adipokine secretion from visceral adipocytes. J. Clin. Biochem. Nutr. 56:2 (2015), 149–154.
12. [12] Astapova, O., Leff, T., Adiponectin and PPARgamma: cooperative and interdependent actions of two key regulators of metabolism. Vitam. Horm. 90 (2012), 143–162.
13. [13] Ouchi, N., Parker, J.L., Lugus, J.J., Walsh, K., Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 11:2 (2011), 85–97.
14. [14] Amar, S., Leeman, S., Periodontal innate immune mechanisms relevant to obesity. Mol. Oral Microbiol. 28:5 (2013), 331–341.
15. [15] Gurav, A., Jadhav, V., Periodontitis and risk of diabetes mellitus. J. Diabetes 3:1 (2011), 21–28.
16. [16] Arimatsu, K., Yamada, H., Miyazawa, H., Minagawa, T., Nakajima, M., Ryder, M.I., Gotoh, K., Motooka, D., Nakamura, S., Iida, T., Yamazaki, K., Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota. Scient. Rep., 4, 2014, 4828.
17. [17] Blasco-Baque, V., Garidou, L., Pomie, C., Escoula, Q., Loubieres, P., Le Gall-David, S., Lemaitre, M., Nicolas, S., Klopp, P., Waget, A., Azalbert, V., Colom, A., Bonnaure-Mallet, M., Kemoun, P., Serino, M., Burcelin, R., Periodontitis induced by Porphyromonas gingivalis drives periodontal microbiota dysbiosis and insulin resistance via an impaired adaptive immune response. Gut, 2016.
18. [18] Artese, H.P., Foz, A.M., Rabelo, M.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, 10(5), 2015, e0128344.
19. [19] Delzenne, N.M., Cani, P.D., Everard, A., Neyrinck, A.M., Bindels, L.B., Gut microorganisms as promising targets for the management of type 2 diabetes. Diabetologia 58:10 (2015), 2206–2217.
20. [20] Etxeberria, U., Hijona, E., Aguirre, L., Milagro, F.I., Bujanda, L., Rimando, A.M., Martinez, J.A., Portillo, M.P., Pterostilbene-induced changes in gut microbiota composition in relation to obesity. Mol. Nutr. Food Res., 2016.
21. [21] Anhe, F.F., Roy, D., Pilon, G., Dudonne, S., Matamoros, S., Varin, T.V., Garofalo, C., Moine, Q., Desjardins, Y., Levy, E., Marette, A., A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice. Gut 64:6 (2015), 872–883.
22. [22] Palaska, I., Papathanasiou, E., Theoharides, T.C., Use of polyphenols in periodontal inflammation. Eur. J. Pharmacol. 720:1–3 (2013), 77–83.
23. [23] 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. 24:4 (2013), 613–623.
24. [24] Scalbert, A., Williamson, G., Dietary intake and bioavailability of polyphenols. J. Nutr. 130:8S Suppl (2000), 2073S–2085S.
25. [25] Poullain, C., Girard-Valenciennes, E., Smadja, J., Plants from reunion island: evaluation of their free radical scavenging and antioxidant activities. J. Ethnopharmacol. 95:1 (2004), 19–26.
26. [26] Marques, V., Farah, A., Chlorogenic acids and related compounds in medicinal plants and infusions. Food Chem. 113 (2009), 1370–1376.
27. [27] Lavergne, R., Tisaneurs et plantes médicinales indigènes de la Réunion. Orphie, 2001, 521.
28. [28] Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976), 248–254.
29. [29] Hatia, S., Septembre-Malaterre, A., Le Sage, F., Badiou-Beneteau, A., Baret, P., Payet, B., Lefebvre d'hellencourt, C., 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. 48:4 (2014), 387–401.
30. [30] Hirschfeld, M., Ma, Y., Weis, J.H., Vogel, S.N., Weis, J.J., Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J. Immunol. (Baltimore, Md.: 1950) 165:2 (2000), 618–622.
31. [31] Berezow, A.B., Ernst, R.K., Coats, S.R., Braham, P.H., Karimi-Naser, L.M., Darveau, R.P., The structurally similar, penta-acylated lipopolysaccharides of Porphyromonas gingivalis and Bacteroides elicit strikingly different innate immune responses. Microb. Pathog. 47:2 (2009), 68–77.
32. [32] Dixon, D.R., Darveau, R.P., Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid a structure. J. Dent. Res. 84:7 (2005), 584–595.
33. [33] Hashimoto, M., Asai, Y., Ogawa, T., Separation and structural analysis of lipoprotein in a lipopolysaccharide preparation from Porphyromonas gingivalis. Int. Immunol. 16:10 (2004), 1431–1437.
34. [34] Yen, G.C., Chen, Y.C., Chang, W.T., Hsu, C.L., Effects of polyphenolic compounds on tumor necrosis factor-alpha (TNF-alpha)-induced changes of adipokines and oxidative stress in 3T3-L1 adipocytes. J. Agric. Food Chem. 59:2 (2011), 546–551.
35. [35] Park, M.Y., Mun, S.T., Carnosic acid inhibits TLR4-MyD88 signaling pathway in LPS-stimulated 3T3-L1 adipocytes. Nutr. Res. Pract. 8:5 (2014), 516–520.
36. [36] Everard, A., Geurts, L., Caesar, R., Van Hul, M., Matamoros, S., Duparc, T., Denis, R.G., Cochez, P., Pierard, F., Castel, J., Bindels, L.B., Plovier, H., Robine, S., Muccioli, G.G., Renauld, J.C., Dumoutier, L., Delzenne, N.M., Luquet, S., Backhed, F., Cani, P.D., Intestinal epithelial MyD88 is a sensor switching host metabolism towards obesity according to nutritional status. Nature Commun., 5, 2014, 5648.
37. [37] Hwang, S.J., Kim, Y.W., Park, Y., Lee, H.J., Kim, K.W., Anti-inflammatory effects of chlorogenic acid in lipopolysaccharide-stimulated RAW 264.7 cells. Inflamm. Res.: Off. J. Eur. Histamine Res. Soc. [et al.] 63:1 (2014), 81–90.
38. [38] Ruifeng, G., Yunhe, F., Zhengkai, W., Ershun, Z., Yimeng, L., Minjun, Y., Xiaojing, S., Zhengtao, Y., Naisheng, Z., Chlorogenic acid attenuates lipopolysaccharide-induced mice mastitis by suppressing TLR4-mediated NF-kappaB signaling pathway. Eur. J. Pharmacol. 729 (2014), 54–58.
39. [39] Juman, S., Yasui, N., Okuda, H., Ueda, A., Negishi, H., Miki, T., Ikeda, K., Caffeic acid phenethyl ester suppresses the production of adipocytokines, leptin, tumor necrosis factor – alpha and resistin, during differentiation to adipocytes in 3T3-L1 cells. Biol. Pharmaceut. Bull. 34:4 (2011), 490–494.
40. [40] Kim, S.H., Park, J.G., Lee, J., Yang, W.S., Park, G.W., Kim, H.G., Yi, Y.S., Baek, K.S., Sung, N.Y., Hossen, M.J., Lee, M.N., Kim, J.H., Cho, J.Y., The dietary flavonoid Kaempferol mediates anti-inflammatory responses via the Src, Syk, IRAK1, and IRAK4 molecular targets. Mediators Inflamm., 2015, 2015, 904142.
41. [41] Devi, K.P., Malar, D.S., Nabavi, S.F., Sureda, A., Xiao, J., Nabavi, S.M., Daglia, M., Kaempferol and inflammation: from chemistry to medicine. Pharmacol. Res. 99 (2015), 1–10.
42. [42] Morange, P.E., Alessi, M.C., Verdier, M., Casanova, D., Magalon, G., Juhan-Vague, I., PAI-1 produced ex vivo by human adipose tissue is relevant to PAI-1 blood level. Arterioscler. Thromb. Vasc. Biol. 19:5 (1999), 1361–1365.
43. [43] Juhan-Vague, I., Alessi, M.C., Mavri, A., Morange, P.E., Plasminogen activator inhibitor-1, inflammation, obesity, insulin resistance and vascular risk. J. Thromb. Haemost. 1:7 (2003), 1575–1579.
44. [44] Hiroshima, Y., Bando, M., Inagaki, Y., Mihara, C., Kataoka, M., Murata, H., Shinohara, Y., Nagata, T., Kido, J., Resistin in gingival crevicular fluid and induction of resistin release by Porphyromonas gingivalis lipopolysaccharide in human neutrophils. J. Periodontal Res. 47:5 (2012), 554–562.
45. [45] Furugen, R., Hayashida, H., Saito, T., Porphyromonas gingivalis and Escherichia coli lipopolysaccharide causes resistin release from neutrophils. Oral Dis. 19:5 (2013), 479–483.
46. [46] Jin, S., Chang, C., Zhang, L., Liu, Y., Huang, X., Chen, Z., Chlorogenic acid improves late diabetes through adiponectin receptor signaling pathways in db/db mice. PLOS ONE, 10(4), 2015, e0120842.
47. [47] Ong, K.W., Hsu, A., Tan, B.K., Anti-diabetic and anti-lipidemic effects of chlorogenic acid are mediated by ampk activation. Biochem. Pharmacol. 85:9 (2013), 1341–1351.
48. [48] Sharma, A.M., Staels, B., Review: peroxisome proliferator-activated receptor gamma and adipose tissue–understanding obesity-related changes in regulation of lipid and glucose metabolism. J. Clin. Endocrinol. Metab. 92:2 (2007), 386–395.
49. [49] Berger, J., Moller, D.E., The mechanisms of action of PPARs. Annu. Rev. Med. 53 (2002), 409–435.
50. [50] Ricote, M., Glass, C.K., PPARs and molecular mechanisms of transrepression. Biochim. Biophys. Acta 1771:8 (2007), 926–935.
51. [51] Zoechling, A., Liebner, F., Jungbauer, A., Red wine: a source of potent ligands for peroxisome proliferator-activated receptor gamma. Food Funct. 2:1 (2011), 28–38.
52. [52] Hempel, S.L., Buettner, G.R., O'Malley, Y.Q., Wessels, D.A., Flaherty, D.M., Dihydrofluorescein diacetate is superior for detecting intracellular oxidants: comparison with 2′,7′-dichlorodihydrofluorescein diacetate, 5(and 6)-carboxy-2′,7′-dichlorodihydrofluorescein diacetate, and dihydrorhodamine 123. Free Rad. Biol. Med. 27:1–2 (1999), 146–159.
53. [53] Jung, U.J., Lee, M.K., Park, Y.B., Jeon, S.M., Choi, M.S., Antihyperglycemic and antioxidant properties of caffeic acid in db/db mice. J. Pharmacol. Exp. Ther. 318:2 (2006), 476–483.
54. [54] Bedard, K., Krause, K.H., The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87:1 (2007), 245–313.
55. [55] Lee, J.W., Bae, C.J., Choi, Y.J., Kim, S.I., Kwon, Y.S., Lee, H.J., Kim, S.S., Chun, W., 3,4,5-Trihydroxycinnamic acid inhibits lipopolysaccharide (LPS)-induced inflammation by Nrf2 activation in vitro and improves survival of mice in LPS-induced endotoxemia model in vivo. Mol. Cell. Biochem. 390:1–2 (2014), 143–153.
56. [56] Pilon, G., Charbonneau, A., White, P.J., Dallaire, P., Perreault, M., Kapur, S., Marette, A., Endotoxin mediated-iNOS induction causes insulin resistance via ONOO(−) induced tyrosine nitration of IRS-1 in skeletal muscle. PLoS One, 5(12), 2010, e15912.
57. [57] Choi, I.S., Choi, E.Y., Jin, J.Y., Park, H.R., Choi, J.I., Kim, S.J., Kaempferol inhibits P. intermedia lipopolysaccharide-induced production of nitric oxide through translational regulation in murine macrophages: critical role of heme oxygenase-1-mediated ROS reduction. J. Periodontol. 84:4 (2013), 545–555.
58. [58] Aggarwal, B.B., Sung, B., Pharmacological basis for the role of curcumin in chronic diseases: an age-old spice with modern targets. Trends Pharmacol. Sci. 30:2 (2009), 85–94.
59. [59] Septembre-Malaterre, A., Le Sage, F., Hatia, S., Catan, A., Janci, L., Gonthier, M.P., Curcuma longa polyphenols 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 (Oxford, England) 42:4 (2016), 418–430.