DOI QR코드

DOI QR Code

Fimbristylis ovata and Artemisia vulgaris extracts inhibited AGE-mediated RAGE expression, ROS generation, and inflammation in THP-1 cells

  • Sukjamnong, Suporn (Department of Clinical Chemistry, Faculty of Allied Health Sciences, Chulalongkorn University) ;
  • Chen, Hui (School of Life Sciences, Faculty of Science, University of Technology Sydney) ;
  • Saad, Sonia (Kolling Institute of Medical Research, University of Sydney) ;
  • Santiyanont, Rachana (Department of Clinical Chemistry, Faculty of Allied Health Sciences, Chulalongkorn University)
  • Received : 2021.02.03
  • Accepted : 2021.11.15
  • Published : 2022.07.15

Abstract

Advanced glycation end products (AGEs) can induce inflammatory signaling pathways through the receptor for AGEs (RAGE). Targeting RAGE could be a therapeutic strategy for treating chronic inflammation mediated by the AGE-RAGE axis. This study aimed to investigate the effects of Fimbristylis ovata and Artemisia vulgaris extracts on AGE-RAGE signaling and AGE-mediated oxidative stress and inflammation in THP-1 cells. F. ovata and A. vulgaris were extracted by a Soxhlet extraction, and antioxidant capacity was evaluated using DPPH and ABTS assays. The human monocytic cell line THP-1 was treated with AGE (600 ㎍/ml) with and without F. ovata and A. vulgaris extracts (100 ㎍/ml). The mitochondria-targeting antioxidant MitoQ (2 ㎍/ml) was used as a positive control. Cell viability, ROS generation, RAGE, AGE-RAGE signaling pathway components, and inflammatory cytokine levels were analyzed. F. ovata and A. vulgaris extracts showed antioxidative effects in non-cell-based assays. Treatment of THP-1 cells with AGE significantly increased the protein levels of RAGE and significantly increased the mRNA expression of cytokines, including TNF-α, IL-1β, and IL-6. AGEs induced the generation of ROS and levels of signaling molecules downstream of RAGE, including phosphorylated and total Erk1/2, JNK, and p38 MAPK, although not significantly. F. ovata and A. vulgaris extracts significantly decreased the protein levels of RAGE and significantly decreased the mRNA levels of cytokines. In conclusion, this study revealed that F. ovata and A. vulgaris extracts exert anti-inflammatory effects through the AGE-RAGE axis. However, details on this anti-inflammatory effect through AGE-RAGE signaling should be further investigated.

Keywords

Acknowledgement

This work was financially supported by the 90th Anniversary of Chulalongkorn University Fund (Ratchadaphiseksomphot Endowment Fund) and National Research University Project, Office of Higher Education Commission (WCU-58-032-AS). MitoQ was provided by Greg Macpherson from MitoQ Limited, New Zealand. We thank the Center for Excellence in Omics-Nano Medical Technology Development Project Chulalongkorn University for allowing us to use various facilities.

References

  1. Cerami C, Founds H, Nicholl I, Mitsuhashi T, Giordano D, Vanpatten S, Lee A, Al-Abed Y, Vlassara H, Bucala R, Cerami A (1997) Tobacco smoke is a source of toxic reactive glycation products. Proc Natl Acad Sci U S A 94:13915-13920. https://doi.org/10.1073/pnas.94.25.13915
  2. Campos C, Guzman R, Lopez-Fernandez E, Casado A (2011) Urinary biomarkers of oxidative/nitrosative stress in healthy smokers. Inhal Toxicol 23:148-156. https://doi.org/10.3109/08958378.2011.554460
  3. Prasad K, Dhar I, Caspar-Bell G (2015) Role of advanced glycation end products and its receptors in the pathogenesis of cigarette smoke-induced cardiovascular disease. Int J Angiol 24:75-80. https://doi.org/10.1055/s-0034-1396413
  4. Goldberg T, Cai W, Peppa M, Dardaine V, Baliga BS, Uribarri J, Vlassara H (2004) Advanced glycoxidation end products in commonly consumed foods. J Am Diet Assoc 104:1287-1291. https://doi.org/10.1016/j.jada.2004.05.214
  5. King GL, Brownlee M (1996) The cellular and molecular mechanisms of diabetic complications. Endocrinol Metab Clin North Am 25:255-270. https://doi.org/10.1016/s0889-8529(05)70324-8
  6. Ramasamy R, Vannucci SJ, Yan SS, Herold K, Yan SF, Schmidt AM (2005) Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. Glycobiology 15:16r-28r. https://doi.org/10.1093/glycob/cwi053
  7. Lander HM, Tauras JM, Ogiste JS, Hori O, Moss RA, Schmidt AM (1997) Activation of the receptor for advanced glycation end products triggers a p21(ras)-dependent mitogen-activated protein kinase pathway regulated by oxidant stress. J Biol Chem 272:17810-17814. https://doi.org/10.1074/jbc.272.28.17810
  8. Lin L, Park S, Lakatta EG (2009) RAGE signaling in inflammation and arterial aging. Front Biosci (Landmark Ed) 14:1403-1413. https://doi.org/10.2741/3315
  9. Zhang SP, Wu YW, Wu ZZ, Liu HY, Nie JH, Tong J (2009) Upregulation of RAGE and S100A6 in rats exposed to cigarette smoke. Environ Toxicol Pharmacol 28:259-264. https://doi.org/10.1016/j.etap.2009.04.013
  10. Gassman JR, Lewis JB, Milner DC, Lewis AL, Bodine JS, Dunaway TM, Monson TD, Broberg DS, Arroyo JA, Reynolds PR (2016) Spatial expression of receptor for advanced glycation endproducts (RAGE) in diverse tissue and organ systems differs following exposure to secondhand cigarette smoke. FASEB J. https://doi.org/10.1096/fasebj.30.1_supplement.lb741
  11. Rahman I, Gilmour PS, Jimenez LA, MacNee W (2002) Oxidative stress and TNF-alpha induce histone acetylation and NF-kappaB/AP-1 activation in alveolar epithelial cells: potential mechanism in gene transcription in lung inflammation. Mol Cell Biochem 234-235:239-248. https://doi.org/10.1023/A:1015905010086
  12. Whitmarsh AJ, Davis RJ (1996) Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med (Berl) 74:589-607. https://doi.org/10.1007/s001090050063
  13. Moens U, Kostenko S, Sveinbjornsson B (2013) The role of mitogen-activated protein kinase-activated protein kinases (MAPKAPKs) in inflammation. Genes (Basel) 4:101-133. https://doi.org/10.3390/genes4020101
  14. Udenigwe CC, Ramprasath VR, Aluko RE, Jones PJ (2008) Potential of resveratrol in anticancer and anti-inflammatory therapy. Nutr Rev 66:445-454. https://doi.org/10.1111/j.1753-4887.2008.00076.x
  15. D'Amico R, Fusco R, Gugliandolo E, Cordaro M, Siracusa R, Impellizzeri D, Peritore AF, Crupi R, Cuzzocrea S, Di Paola R (2019) Effects of a new compound containing palmitoylethanolamide and baicalein in myocardial ischaemia/reperfusion injury in vivo. Phytomedicine 54:27-42. https://doi.org/10.1016/j.phymed.2018.09.191
  16. Huang SM, Wu CH, Yen GC (2006) Effects of flavonoids on the expression of the pro-inflammatory response in human monocytes induced by ligation of the receptor for AGEs. Mol Nutr Food Res 50:1129-1139. https://doi.org/10.1002/mnfr.200600075
  17. Tuchinda P, Reutrakul V, Claeson P, Pongprayoon U, Sematong T, Santisuk T, Taylor WC (2002) Anti-inflammatory cyclohexenyl chalcone derivatives in Boesenbergia pandurata. Phytochemistry 59:169-173. https://doi.org/10.1016/s0031-9422(01)00451-4
  18. Pradhan A (2007) Obesity, metabolic syndrome, and type 2 diabetes: inflammatory basis of glucose metabolic disorders. Nutr Rev 65:S152-156. https://doi.org/10.1111/j.1753-4887.2007.tb00354.x
  19. Golia E, Limongelli G, Natale F, Fimiani F, Maddaloni V, Pariggiano I, Bianchi R, Crisci M, D'Acierno L, Giordano R, Di Palma G, Conte M, Golino P, Russo MG, Calabro R, Calabro P (2014) Inflammation and cardiovascular disease: from pathogenesis to therapeutic target. Curr Atheroscler Rep 16:435. https://doi.org/10.1007/s11883-014-0435-z
  20. McInnes IB, Schett G (2017) Pathogenetic insights from the treatment of rheumatoid arthritis. Lancet 389:2328-2337. https://doi.org/10.1016/s0140-6736(17)31472-1
  21. Chan SMH, Selemidis S, Bozinovski S, Vlahos R (2019) Pathobiological mechanisms underlying metabolic syndrome (MetS) in chronic obstructive pulmonary disease (COPD): clinical significance and therapeutic strategies. Pharmacol Ther 198:160-188. https://doi.org/10.1016/j.pharmthera.2019.02.013
  22. Wieczfnska J, Sitarek P, Kowalczyk T, Skala E, Pawliczak R (2020) The anti-inflammatory potential of selected plant-derived compounds in respiratory diseases. Curr Pharm Des. https://doi.org/10.2174/1381612826666200406093257
  23. Kinney JW, Bemiller SM, Murtishaw AS, Leisgang AM, Salazar AM, Lamb BT (2018) Inflammation as a central mechanism in Alzheimer's disease. Alzheimers Dement (NY) 4:575-590. https://doi.org/10.1016/j.trci.2018.06.014
  24. Santisuk T, Larsen K (1998) Flora of Thailand, vol 6/4. The Forest Herbarium, Royal Forest Department, Bangkok
  25. Tungmunnithum D, Thongboonyou A, Pholboon A, Yangsabai A (2018) Flavonoids and other phenolic compounds from medicinal plants for pharmaceutical and medical aspects: an overview. Medicines (Basel). https://doi.org/10.3390/medicines5030093
  26. Souto AL, Tavares JF, da Silva MS, Diniz Mde F, de Athayde-Filho PF, Barbosa Filho JM (2011) Anti-inflammatory activity of alkaloids: an update from 2000 to 2010. Molecules 16:8515-8534. https://doi.org/10.3390/molecules16108515
  27. Guclu-Ustundag O, Mazza G (2007) Saponins: properties, applications and processing. Crit Rev Food Sci Nutr 47:231-258. https://doi.org/10.1080/10408390600698197
  28. Roy R, Ud Daula A, Akter A, Sultana S, Barek MA, Liya IJ, Basher MA (2019) Antipyretic and anti-nociceptive effects of methanol extract of leaves of Fimbristylis miliacea in mice model. J Ethnopharmacol 243:112080. https://doi.org/10.1016/j.jep.2019.112080
  29. Kamiabi F, Jaal Z, Keng CL (2013) Bioefficacy of crude extract of Cyperus aromaticus (Family: Cyperaceae) cultured cells, against Aedes aegypti and Aedes albopictus mosquitoes. Asian Pac J Trop Biomed 3:767-775. https://doi.org/10.1016/s2221-1691(13)60153-7
  30. Khare C (2007) Indian medicinal plants an illustrated dictionary. Springer, USA
  31. Burkill HM, Dalziel JM, Hutchinson J (1985) The useful plants of West tropical Africa, 2nd edn. Royal Botanic Gardens, Kew, UK
  32. Sukjamnong S, Santiyanont R (2015) Effect of Fimbristylis ovata on receptor for advanced glycation end-products, proinflammatory cytokines, and cell adhesion molecule level and gene expression in U937 and bEnd.3 cell lines. Genet Mol Res 14:3984-3994. https://doi.org/10.4238/2015.April.27.13
  33. Sirirattanakul S, Santiyanont R (2021) Fimbristylis ovata extract and its ability to encounter AGEs-induced neurotoxicity in SH-SY5Y. Toxicol Res 37:355-367. https://doi.org/10.1007/s43188-020-00072-z
  34. Marina Radovic J, Darko G, Jovana Tubic V, Aleksandra M, Milena M, Milan S, Nenad V, Milena V, Olivera M-D (2020) In vitro study of genotoxic and cytotoxic activities of methanol extracts of Artemisia vulgaris L. and Artemisia alba Turra. S Afr J Bot 132:117-126. https://doi.org/10.1016/j.sajb.2020.04.016
  35. Abiri R, Silva ALM, de Mesquita LSS, de Mesquita JWC, Atabaki N, de Almeida EB, Shaharuddin NA, Malik S (2018) Towards a better understanding of artemisia vulgaris: botany, phytochemistry, pharmacological and biotechnological potential. Food Res Int 109:403-415. https://doi.org/10.1016/j.foodres.2018.03.072
  36. Soon L, Ng PQ, Chellian J, Madheswaran T, Panneerselvam J, Gupta G, Nammi S, Hansbro NG, Hsu A, Dureja H, Mehta M, Satija S, Hansbro PM, Dua K, Collet T, Chellappan DK (2019) Therapeutic potential of artemisia vulgaris: an insight into underlying immunological mechanisms. J Environ Pathol Toxicol Oncol 38:205-216. https://doi.org/10.1615/JEnvironPatholToxicolOncol.2019029397
  37. Manczak M, Mao P, Calkins MJ, Cornea A, Reddy AP, Murphy MP, Szeto HH, Park B, Reddy PH (2010) Mitochondria-targeted antioxidants protect against amyloid-beta toxicity in Alzheimer's disease neurons. J Alzheimers Dis 20:S609-S631. https://doi.org/10.3233/jad-2010-100564
  38. Gane EJ, Weilert F, Orr DW, Keogh GF, Gibson M, Lockhart MM, Frampton CM, Taylor KM, Smith RA, Murphy MP (2010) The mitochondria-targeted anti-oxidant mitoquinone decreases liver damage in a phase II study of hepatitis C patients. Liver Int 30:1019-1026. https://doi.org/10.1111/j.1478-3231.2010.02250.x
  39. Dashdorj A, Jyothi KR, Lim S, Jo A, Nguyen MN, Ha J, Yoon KS, Kim HJ, Park JH, Murphy MP, Kim SS (2013) Mitochondria-targeted antioxidant MitoQ ameliorates experimental mouse colitis by suppressing NLRP3 inflammasome-mediated inflammatory cytokines. BMC Med 11:178. https://doi.org/10.1186/1741-7015-11-178
  40. Xiao L, Xu X, Zhang F, Wang M, Xu Y, Tang D, Wang J, Qin Y, Liu Y, Tang C, He L, Greka A, Zhou Z, Liu F, Dong Z, Sun L (2017) The mitochondria-targeted antioxidant MitoQ ameliorated tubular injury mediated by mitophagy in diabetic kidney disease via Nrf2/PINK1. Redox Biol 11:297-311. https://doi.org/10.1016/j.redox.2016.12.022
  41. Mao P, Manczak M, Shirendeb UP (2013) MitoQ, a mitochondria-targeted antioxidant, delays disease progression and alleviates pathogenesis in an experimental autoimmune encephalomyelitis mouse model of multiple sclerosis. Biochim Biophys Acta 1832 12:2322-2331. https://doi.org/10.1016/j.bbadis.2013.09.005
  42. Li G, Chan YL, Sukjamnong S, Anwer AG, Vindin H, Padula M, Zakarya R, George J, Oliver BG, Saad S, Chen H (2019) A mitochondrial specific antioxidant reverses metabolic dysfunction and fatty liver induced by maternal cigarette smoke in mice. Nutrients. https://doi.org/10.3390/nu11071669
  43. Sukjamnong S, Chan YL, Zakarya R, Saad S, Sharma P, Santiyanont R, Chen H, Oliver BG (2017) Effect of long-term maternal smoking on the offspring's lung health. Am J Physiol Lung Cell Mol Physiol 313:L416-L423. https://doi.org/10.1152/ajplung.00134.2017
  44. Sukjamnong S, Chan YL, Zakarya R, Nguyen LT, Anwer AG, Zaky AA, Santiyanont R, Oliver BG, Goldys E, Pollock CA, Chen H, Saad S (2018) MitoQ supplementation prevent long-term impact of maternal smoking on renal development, oxidative stress and mitochondrial density in male mice offspring. Sci Rep 8:6631. https://doi.org/10.1038/s41598-018-24949-0
  45. Castaneda-Arriaga R, Perez-Gonzalez A, Reina M, AlvarezIdaboy JR, Galano A (2018) Comprehensive investigation of the antioxidant and pro-oxidant effects of phenolic compounds: a double-edged sword in the context of oxidative stress? J Phys Chem B 122:6198-6214. https://doi.org/10.1021/acs.jpcb.8b03500
  46. Baiano A, Del Nobile MA (2016) Antioxidant compounds from vegetable matrices: biosynthesis, occurrence, and extraction systems. Crit Rev Food Sci Nutr 56:2053-2068. https://doi.org/10.1080/10408398.2013.812059
  47. Lee KJ, Oh YC, Cho WK, Ma JY (2015) Antioxidant and anti-inflammatory activity determination of one hundred kinds of pure chemical compounds using offline and online screening HPLC assay. Evid Based Complement Alternat Med 2015:165457. https://doi.org/10.1155/2015/165457
  48. Dawidowicz AL, Olszowy M (2013) The importance of solvent type in estimating antioxidant properties of phenolic compounds by ABTS assay. Eur Food Res Technol 236:1099-1105. https://doi.org/10.1007/s00217-013-1982-1
  49. Figarola JL, Shanmugam N, Natarajan R, Rahbar S (2007) Anti-inflammatory effects of the advanced glycation end product inhibitor LR-90 in human monocytes. Diabetes 56:647-655. https://doi.org/10.2337/db06-0936
  50. Bucciarelli LG, Wendt T, Qu W, Lu Y, Lalla E, Rong LL, Goova MT, Moser B, Kislinger T, Lee DC, Kashyap Y, Stern DM, Schmidt AM (2002) RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation 106:2827-2835. https://doi.org/10.1161/01.cir.0000039325.03698.36
  51. Soro-Paavonen A, Watson AM, Li J, Paavonen K, Koitka A, Calkin AC, Barit D, Coughlan MT, Drew BG, Lancaster GI, Thomas M, Forbes JM, Nawroth PP, Bierhaus A, Cooper ME, Jandeleit-Dahm KA (2008) Receptor for advanced glycation end products (RAGE) deficiency attenuates the development of atherosclerosis in diabetes. Diabetes 57:2461-2469. https://doi.org/10.2337/db07-1808
  52. Kanda A, Dong Y, Noda K, Saito W, Ishida S (2017) Advanced glycation endproducts link inflammatory cues to upregulation of galectin-1 in diabetic retinopathy. Sci Rep 7:16168. https://doi.org/10.1038/s41598-017-16499-8
  53. Hodgkinson CP, Laxton RC, Patel K, Ye S (2008) Advanced glycation end-product of low density lipoprotein activates the toll-like 4 receptor pathway implications for diabetic atherosclerosis. Arterioscler Thromb Vasc Biol 28:2275-2281. https://doi.org/10.1161/atvbaha.108.175992
  54. Gasiorowski K, Brokos B, Echeverria V, Barreto GE, Leszek J (2018) RAGE-TLR crosstalk sustains chronic inflammation in neurodegeneration. Mol Neurobiol 55:1463-1476. https://doi.org/10.1007/s12035-017-0419-4
  55. Xu H, He Y, Yang X, Liang L, Zhan Z, Ye Y, Yang X, Lian F, Sun L (2007) Anti-malarial agent artesunate inhibits TNF-alpha-induced production of proinflammatory cytokines via inhibition of NF-kappaB and PI3 kinase/Akt signal pathway in human rheumatoid arthritis fibroblast-like synoviocytes. Rheumatology (Oxford) 46:920-926. https://doi.org/10.1093/rheumatology/kem014
  56. Lee C-W, Lin C-C, Lin W-N, Liang K-C, Luo S-F, Wu C-B, Wang S-W, Yang C-M (2007) TNF-alpha induces MMP-9 expression via activation of Src/EGFR, PDGFR/PI3K/Akt cascade and promotion of NF-kappaB/p300 binding in human tracheal smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 292:L799-L812. https://doi.org/10.1152/ajplung.00311.2006
  57. Kontny E, Ziolkowska M, Ryzewska A, Maslinski W (1999) Protein kinase c-dependent pathway is critical for the production of pro-inflammatory cytokines (TNF-alpha, IL-1beta, IL-6). Cytokine 11:839-848. https://doi.org/10.1006/cyto.1998.0496
  58. Huang JS, Guh JY, Chen HC, Hung WC, Lai YH, Chuang LY (2001) Role of receptor for advanced glycation end-product (RAGE) and the JAK/STAT-signaling pathway in AGE-induced collagen production in NRK-49F cells. J Cell Biochem 81:102-113. https://doi.org/10.1002/1097-4644(20010401)81:1%3c102::aid-jcb1027%3e3.0.co;2-y
  59. Huttunen HJ, Kuja-Panula J, Rauvala H (2002) Receptor for advanced glycation end products (RAGE) signaling induces CREB-dependent chromogranin expression during neuronal differentiation. J Biol Chem 277:38635-38646. https://doi.org/10.1074/jbc.M202515200
  60. Lee EJ, Kim JY, Oh SH (2016) Advanced glycation end products (AGEs) promote melanogenesis through receptor for AGEs. Sci Rep 6:27848. https://doi.org/10.1038/srep27848
  61. Xu Y, Toure F, Qu W, Lin L, Song F, Shen X, Rosario R, Garcia J, Schmidt AM, Yan SF (2010) Advanced glycation end product (AGE)-receptor for AGE (RAGE) signaling and up-regulation of Egr-1 in hypoxic macrophages. J Biol Chem 285:23233-23240. https://doi.org/10.1074/jbc.M110.117457
  62. Adamopoulos C, Piperi C, Gargalionis AN, Dalagiorgou G, Spilioti E, Korkolopoulou P, Diamanti-Kandarakis E, Papavassiliou AG (2016) Advanced glycation end products upregulate lysyl oxidase and endothelin-1 in human aortic endothelial cells via parallel activation of ERK1/2-NF-κB and JNK-AP-1 signaling pathways. Cell Mol Life Sci 73:1685-1698. https://doi.org/10.1007/s00018-015-2091-z