Rice bran oil ameliorates inflammatory responses by enhancing mitochondrial respiration in murine macrophages
Autoři:
Sojung Lee aff001; Seungmin Yu aff001; Hye Jeong Park aff001; Jiyeon Jung aff002; Gwang-woong Go aff002; Wooki Kim aff001
Působiště autorů:
Department of Food Science and Biotechnology, Graduate School of Biotechnology, Kyung Hee University, Yongin-si, Gyeonggi-do, Korea
aff001; Department of Food and Nutrition, Hanyang University, Seongdong-gu, Seoul, Korea
aff002
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0222857
Souhrn
Previous studies have revealed the anti-inflammatory properties of rice bran oil (RBO), but the detailed mechanisms are poorly understood. Recent studies on the molecular/cellular anti-inflammatory mechanisms of dietary components have demonstrated that mitochondrial respiration plays a key role in macrophage functioning. Since dietary lipids are major substrates for mitochondrial respiration through β-oxidation, the current study examined whether RBO regulates inflammatory responses by modulating mitochondrial energy metabolism. Palm oil (PO), enriched with palmitic acid which are known to be effectively taken up by cells and used for oxidative phosphorylation, served as a positive control. In the in vitro model of LPS-stimulated RAW 264.7 murine cells, the levels of pro-inflammatory cytokines (IL-6 and TNF-α) in the culture supernatant were significantly reduced by RBO treatment. In contrast, secretion of the anti-inflammatory cytokine IL-10 was upregulated by RBO. Transcription of genes encoding inflammatory mediator molecules (COX-2 and iNOS) and expression of activation markers (CD80, CD86, and MHC-II) in LPS-stimulated RAW 264.7 cells were suppressed by RBO. Mitochondrial respiration (as assessed by an extracellular flux analyzer) increased upon RBO treatment, as the basal respiration, maximal respiration, ATP production, and spare respiratory capacity were upregulated. In an in vivo study, C57BL/6 mice were fed a negative control diet containing corn oil (CO), PO, or RBO for 4 weeks, and bone marrow-derived macrophages (BMDM) were isolated from their tibias and femurs. In pro-inflammatory M1-polarized BMDM (M1-BMDM), the RBO-induced suppression of IL-6 and TNF-α was recapitulated in vivo. Mitochondrial respiration in M1-BMDM also increased following the RBO intervention and the PO control treatment as compared to CO fed negative control. Overall, the current study for the first time demonstrates that RBO regulates inflammatory responses in murine macrophages by upregulating mitochondrial respiration. Further clinical studies are required to validate the animal study.
Klíčová slova:
Cytokines – Fatty acids – Inflammation – Macrophages – Mitochondria – Oils – Rice – Vegetable oils
Zdroje
1. Mills EL, O’Neill LA. Reprogramming mitochondrial metabolism in macrophages as an anti-inflammatory signal. Eur J Immunol. 2016;46: 13–21. doi: 10.1002/eji.201445427 26643360
2. Liberti M V., Locasale JW. The Warburg effect: How does it benefit cancer cells? Trends Biochem Sci. 2016;41: 211–218. doi: 10.1016/j.tibs.2015.12.001 26778478
3. Van den Bossche J, Baardman J, de Winther MPJ. Metabolic characterization of polarized M1 and M2 bone marrow-derived macrophages using real-time extracellular flux analysis. J Vis Exp. 2015;105: 1–7. doi: 10.3791/53424 26649578
4. Dunster JL. The macrophage and its role in inflammation and tissue repair: mathematical and systems biology approaches. Wiley Interdiscip Rev Syst Biol Med. 2016;8: 87–99. doi: 10.1002/wsbm.1320 26459225
5. Gordon S. The role of the macrophage in immune regulation. Res Immunol. 1998;149: 685–688. doi: 10.1016/S0923-2494(99)80039-X 9851524
6. Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014;6: 13. doi: 10.12703/P6-13 24669294
7. Ley K. M1 means kill; M2 means heal. J Immunol. 2017;199: 2191–2193. doi: 10.4049/jimmunol.1701135 28923980
8. Mehta MM, Weinberg SE, Chandel NS. Mitochondrial control of immunity: Beyond ATP. Nat Rev Immunol. 2017;17: 608–620. doi: 10.1038/nri.2017.66 28669986
9. Huang SCCC-C, Everts B, Ivanova Y, O’Sullivan D, Nascimento M, Smith AMM, et al. Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages. Nat Immunol. 2014;15: 846–855. doi: 10.1038/ni.2956 25086775
10. Schönfeld P, Wojtczak L. Short- and medium-chain fatty acids in energy metabolism: the cellular perspective. J Lipid Res. 2016;57: 943–954. doi: 10.1194/jlr.R067629 27080715
11. Kwon Y, Yu S, Choi GS, Kim JH, Baik M, Su ST, et al. Puffing of Rehmannia glutinosa enhances anti-oxidant capacity and down-regulates IL-6 production in RAW 264.7 cells. Food Sci Biotechnol. 2019;28: 1235–1240. doi: 10.1007/s10068-019-00566-z 31275724
12. Governa P, Carullo G, Biagi M, Rago V, Aiello F. Evaluation of the In Vitro Wound-Healing Activity of Calabrian Honeys. Antioxidants. 2019; doi: 10.3390/antiox8020036 30736314
13. Frattaruolo L, Carullo G, Brindisi M, Mazzotta S, Bellissimo L, Rago V, et al. Antioxidant and Anti-Inflammatory Activities of Flavanones from Glycyrrhiza glabra L. (licorice) Leaf Phytocomplexes: Identification of Licoflavanone as a Modulator of NF-kB/MAPK Pathway. Antioxidants. 2019;8: 186. doi: 10.3390/antiox8060186 31226797
14. Che DN, Kang HJ, Cho BO, Shin JY, Jang S Il. Combined effects of Diospyros lotus leaf and grape stalk extract in high-fat-diet-induced obesity in mice. Food Sci Biotechnol. 2019; doi: 10.1007/s10068-018-00551-y 31275721
15. Tundis R, Frattaruolo L, Carullo G, Armentano B, Badolato M, Loizzo MR, et al. An ancient remedial repurposing: synthesis of new pinocembrin fatty acid acyl derivatives as potential antimicrobial/anti-inflammatory agents. Nat Prod Res. 2019;33: 162–168. doi: 10.1080/14786419.2018.1440224 29463111
16. Carullo G, Galligano F, Aiello F. Structure-activity relationships for the synthesis of selective cyclooxygenase 2 inhibitors: an overview (2009–2016). MedChemComm. 2017. doi: 10.1039/c6md00569a 30108767
17. Aiello F, Carullo G, Badolato M, Brizzi A. TRPV1–FAAH–COX: The Couples Game in Pain Treatment. ChemMedChem. 2016. doi: 10.1002/cmdc.201600111 27240888
18. Pestana-Bauer VR, Zambiazi RC, Mendonça CRB, Beneito-Cambra M, Ramis-Ramos G. γ-Oryzanol and tocopherol contents in residues of rice bran oil refining. Food Chem. 2012; doi: 10.1016/j.foodchem.2012.03.059 25005970
19. Poorna Chandra Rao Y, Sugasini D, Lokesh B. Dietary gamma oryzanol plays a significant role in the anti-inflammatory activity of rice bran oil by decreasing pro-inflammatory mediators secreted by peritoneal macrophages of rats. Biochem Biophys Res Commun. 2016;479: 747–752. doi: 10.1016/j.bbrc.2016.09.140 27693794
20. Nagendra Prasad M, Sanjay K, Shravya Khatokar M, Vismaya M, Nanjunda Swamy S. Health benefits of rice bran—A review. J Nutr Food Sci. 2011;01: 108. doi: 10.4172/2155-9600.1000108
21. Park HY, Lee KW, Choi HD. Rice bran constituents: immunomodulatory and therapeutic activities. Food Funct. 2017;8: 935–943. doi: 10.1039/c6fo01763k 28224159
22. Ergönül PG, Köseoǧlu O. Changes in α-, β-, γ- And δ-tocopherol contents of mostly consumed vegetable oils during refining process. CYTA—J Food. 2014; doi: 10.1080/19476337.2013.821672
23. Ying W, Cheruku PS, Bazer FW, Safe SH, Zhou B. Investigation of macrophage polarization using bone marrow derived macrophages. J Vis Exp. 2013;76: e50323. doi: 10.3791/50323 23851980
24. Nicholas D, Proctor EA, Raval FM, Ip BC, Habib C, Ritou E, et al. Advances in the quantification of mitochondrial function in primary human immune cells through extracellular flux analysis. PLoS One. 2017;12: e0170975. doi: 10.1371/journal.pone.0170975 28178278
25. Shapiro H, Lutaty A, Ariel A. Macrophages, meta-inflammation, and immuno-metabolism. Sci World J. 2011;11: 2509–2529. doi: 10.1100/2011/397971 22235182
26. Shanura Fernando IP, Asanka Sanjeewa KK, Samarakoon KW, Lee WW, Kim HS, Ranasinghe P, et al. Antioxidant and anti-inflammatory functionality of ten Sri Lankan seaweed extracts obtained by carbohydrase assisted extraction. Food Sci Biotechnol. 2018; doi: 10.1007/s10068-018-0406-1 30483441
27. Schulz H. Beta oxidation of fatty acids. Biochimica et Biophysica Acta (BBA)/Lipids and Lipid Metabolism. 1991. doi: 10.1016/0005-2760(91)90015-A
28. He C, Carter AB. The metabolic prospective and redox regulation of macrophage polarization. J Clin Cell Immunol. 2015;06: 371. doi: 10.4172/2155-9899.1000371 26962470
29. Hwang SJ, Kim YW, Park Y, Lee HJ, Kim KW. Anti-inflammatory effects of chlorogenic acid in lipopolysaccharide- stimulated RAW 264.7 cells. Inflamm Res. 2014; doi: 10.1007/s00011-013-0674-4 24127072
30. Islam MS, Ushio H, Hori M, Ozaki H. Cycloartenyl Ferulate downregulates lipopolysaccharide stimulated iNOS mRNA via NF-kB suppression in RAW 264.7 macrophages. Asian J Med Biol Res. 2017;2: 523. doi: 10.3329/ajmbr.v2i4.30992
31. Sierra S, Lara-Villoslada F, Olivares M, Jimenez J, Boza J, Xaus J. Increased immune response in mice consuming rice bran oil. Eur J Nutr. 2005;44: 509–516. doi: 10.1007/s00394-005-0554-y 15719157
32. Yadav NV, Sadashivaiah, Ramaiyan B, Acharya P, Belur L, Talahalli RR. Sesame oil and rice bran oil ameliorates adjuvant-induced arthritis in rats: Distinguishing the role of minor components and fatty acids. Lipids. 2016;51: 1385–1395. doi: 10.1007/s11745-016-4203-4 27747452
33. Fattore E, Fanelli R. Palm oil and palmitic acid: A review on cardiovascular effects and carcinogenicity. International Journal of Food Sciences and Nutrition. 2013. doi: 10.3109/09637486.2013.768213 23406428
34. Kim H, Choe JH, Choi JH, Kim HJ, Park SH, Lee MW, et al. Medium-Chain Enriched Diacylglycerol (MCE-DAG) Oil Decreases Body Fat Mass in Mice by Increasing Lipolysis and Thermogenesis in Adipose Tissue. Lipids. 2017;52: 665–673. doi: 10.1007/s11745-017-4277-7 28707153
35. Papamandjaris AA, Macdougall DE, Jones PJH. Medium chain fatty acid metabolism and energy expenditure: Obesity treatment implications. Life Sci. 1998;62: 1203–1215. doi: 10.1016/s0024-3205(97)01143-0 9570335
36. Imamura H, Huynh Nhat KP, Togawa H, Saito K, Iino R, Kato-Yamada Y, et al. Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc Natl Acad Sci. 2009;106: 15651–15656. doi: 10.1073/pnas.0904764106 19720993
37. Brennan J, Southworth R, Medina R, Davidson S, Duchenn M, Shattock M. Mitochondrial uncoupling, with low concentration FCCP, induces ROS-dependent cardioprotection independent of KATP channel activation. Cardiovasc Res. 2006;72: 313–321. doi: 10.1016/j.cardiores.2006.07.019 16950237
38. Eddie Ip WK, Hoshi N, Shouval DS, Snapper S, Medzhitov R. Anti-inflammatory effect of IL-10 mediated by metabolic reprogramming of macrophages. Science (80-). 2017;356: 513–519. doi: 10.1126/science.aal3535 28473584
39. Wynn TA, Chawla A, Pollard JW. Macrophage biology in development, homeostasis and disease. Nature. 2013. doi: 10.1038/nature12034 23619691
40. Rao YPC, Kumar PP, Lokesh BR. Molecular Mechanisms for the Modulation of Selected Inflammatory Markers by Dietary Rice Bran Oil in Rats Fed Partially Hydrogenated Vegetable Fat. Lipids. 2016;51: 451–467. doi: 10.1007/s11745-016-4132-2 26939679
41. Wang F, Zhang S, Vuckovic I, Jeon R, Lerman A, Folmes CD, et al. Glycolytic Stimulation Is Not a Requirement for M2 Macrophage Differentiation. Cell Metab. 2018;28: 463–475.e4. doi: 10.1016/j.cmet.2018.08.012 30184486
42. Meiser J, Krämer L, Sapcariu SC, Battello N, Ghelfi J, D’Herouel AF, et al. Pro-inflammatory macrophages sustain pyruvate oxidation through pyruvate dehydrogenase for the synthesis of itaconate and to enable cytokine expression. J Biol Chem. 2016;291: 3932–3946. doi: 10.1074/jbc.M115.676817 26679997
Článek vyšel v časopise
PLOS One
2019 Číslo 10
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Je libo čepici místo mozkového implantátu?
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
- AI může chirurgům poskytnout cenná data i zpětnou vazbu v reálném čase
- Nová metoda odlišení nádorové tkáně může zpřesnit resekci glioblastomů
Nejčtenější v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Experimentally validated simulation of coronary stents considering different dogboning ratios and asymmetric stent positioning
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy