Dietary Njavara (Oryza Sativa Linn.) Rice Bran Oil Regulates Immune Response by Regulating Th1/Th2 Lineage Balance in High Fat Diet Induced Atherosclerosis
Life Sciences-Immunology and Atherosclerosis
DOI:
https://doi.org/10.22376/ijlpr.2023.13.5.L118-L131Keywords:
Atherosclerosis, Njavara rice bran oil, CD4 T cell, T helper cells, High-fat dietAbstract
When considering inflammation, CD4+ T cells play a crucial role in the pathogenesis of atherosclerosis. The hypocholesterolemic effects of Njavara (Oryza sativa Linn.) rice bran oil (NjRBO) in the treatment of atherosclerosis has been previously explored. However, no evidence regarding understanding Th1/Th2-cell lineage differentiation in atherosclerotic rats has been studied. Hence the objective of this study was to investigate the regulatory effects of Njavara rice bran oil in modulating CD4+ T cell imbalance in the Sprague–Dawley rat model. Following in-vivo research for two months, splenocytes isolated were cultured ex-vivo and treated with Concanavalin A (1.5-3μg/ml medium), followed by incubation with anti-CD3e/CD28 platebound antibodies. Initially, body weight and biochemical parameters, including serum and hepatic lipid profile, were analyzed, and the results revealed suppression of the pro-inflammatory biochemical markers upon supplementation of NjRBO. Further evaluation of the effects of Njavara rice bran oil on Th1/Th2 lineage development of CD4+ T cells under anti-CD3/anti-CD28 antibody stimulation was studied. Results revealed that NjRBO significantly suppressed the amount of Th1 cytokines demonstrating its broad suppressive effect on Th1-related pro-inflammation, while an upregulation in the production of Th2 cytokines was noticed. Furthermore, significant attenuation in the mRNA expression pattern of Th1/Th2-related transcription factors and co-stimulatory expression in splenic CD4+ T cells were further examined. Hence these data indicate that NjRBO incorporation selectively alters Th1/Th2 Cell-mediated inflammation patterns and provides the pharmacological basis for its applications.
References
Wu L, Wei Q, Brzostek J, Gascoigne NRJ. Signalling from T cell receptors (TCRs) and chimeric antigen receptors (CARs) on T cells. Cell Mol Immunol. 2020;17(6):600-12. doi: 10.1038/s41423-020-0470-3, PMID 32451454.
Fowler DH. Rapamycin-resistant effector T-cell therapy. Immunol Rev. 2014;257(1):210-25. doi: 10.1111/in.12127, PMID 24329799.
Phillips T, Devata S, Wilcox RA. Challenges and opportunities for checkpoint blockade in T-cell lymphoproliferative disorders. J Immunother Cancer. 2016;4:95. doi: 10.1186/s40425-016-0201-6, PMID 28031823.
Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell. 2000;100(6):655-69. doi: 10.1016/S0092-8674(00)80702-3.
Wan YY. GATA3: a master of many trades in immune regulation. Trends Immunol. 2014;35(6):233-42. doi: 10.1016/j.it.2014.04.002, PMID 24786134.
Imig JD, Ryan MJ. Immune and inflammatory role in renal disease. Compr Physiol. 2013;3(2):957-76. doi: 10.1002/cosy.c120028, PMID 23720336.
Peter J, Sabu V, Aswathy IS, Krishnan S, Lal Preethi SS, Simon M et al. Dietary amaranths modulate the immune response via balancing Th1/Th2 and Th17/Treg response in collagen-induced arthritis. Mol Cell Biochem. 2020;472(1-2):57-66. doi: 10.1007/s11010-020-03783-x, PMID 32529499.
Costagliola G, Nuzzi G, Spada E, Comberiati P, Verduci E, Peroni DG. Nutraceuticals in viral infections: an overview of the immunomodulating properties. Nutrients. 2021;13(7):2410. doi: 10.3390/nu13072410, PMID 34371920.
Calpe-Berdiel L, Escolà-Gil JC, Benítez S, Bancells C, González-Sastre F, Palomer X et al. Dietary phytosterols modulate T-helper immune response but do not induce apparent anti-inflammatory effects in a mouse model of acute, aseptic inflammation. Life Sci. 2007;80(21):1951-6. doi: 10.1016/j.lfs.2007.02.032, PMID 17382351.
Hao Y, Cook MC. Inborn errors of immunity and their phenocopies: CTLA4 and PD-1. Front Immunol. 2021;12:806043. doi: 10.3389/fimmu.2021.806043, PMID 35154081.
Krummel MF, Sullivan TJ, Allison JP. Superantigen responses and co-stimulation: CD28 and CTLA-4 have opposing effects on T cell expansion in vitro and in vivo. Int Immunol. 1996;8(4):519-23. doi: 10.1093/intimm/8.4.519, PMID 8671638.
Lai YP, Kuo LC, Lin BR, Lin HJ, Lin CY, Chen YT et al. CD28 engagement inhibits CD73-mediated regulatory activity of CD8+ T cells. Commun Biol. 2021;4(1):595. doi: 10.1038/s42003-021-02119-9, PMID 34011962.
Loo K, Smithy JW, Postow MA, Betof Warner A. Factors determining long-term antitumor responses to immune checkpoint blockade therapy in melanoma. Front Immunol. 2021;12:810388. doi: 10.3389/fimmu.2021.810388, PMID 35087529.
Reis N, Castanho A, Lageiro M, Pereira C, Brites CM, Vaz-Velho M. Rice bran stabilization and oil extraction using the microwave-assisted method and its effects on GABA and gamma-oryzanol compounds. Foods. 2022;11(7):912. doi: 10.3390/foods11070912, PMID 35406999.
Mahdavi-Roshan M, Salari A, Vakilpour A, Savar Rakhsh A, Ghorbani Z. Rice bran oil could favourably ameliorate atherogenicity and insulin resistance indices among men with coronary artery disease: post hoc analysis of a randomized controlled trial. Lipids Health Dis. 2021;20(1):153. doi: 10.1186/s12944-021-01584-9, PMID 34742318.
Ramezani-Jolfaie, Nahid and Rouhani, Mohammad & Surkan, Pamela and Siassi, Fereydoun, Azadbakht, Leila, Siassi F, Azadbakht LRice Bran Oil Decreases Total and LDL Cholesterol in Humans: a Systematic Review and Meta-Analysis of Randomized Controlled Clinical Trials. Horm Metab Res. 2016;48(7):417-26. doi: 10.1055/s-0042-105748, PMID 27311126.
Chithra PK, Sindhu G, Shalini V, Parvathy R, Jayalekshmy A, Helen A. Dietary Njavara rice bran oil reduces experimentally induced hypercholesterolaemia by regulating genes involved in lipid metabolism. Br J Nutr. 2015;113(8):1207-19. doi: 10.1017/S0007114515000513, PMID 25823019.
Pushpan CK, V S, G S, Rathnam P, A J, A H. Attenuating atherosclerotic complications by modulating inflammatory responses in hypercholesterolemic rats with dietary Njavara rice bran oil. Biomed Pharmacother. 2016;83:1387-97. doi: 10.1016/j.biopha.2016.08.001, PMID 27583979.
Wu CT, Huang KS, Yang CH, Chen YC, Liao JW, Kuo CL et al. Inhibitory effects of cultured Dendrobium to sense on atopic dermatitis murine model. Int J Pharm. 2014; 25;463(2):193-200. doi: 10.1016/j.ijpharm.2013.08.015, PMID 23958754.
Liao CH, Lin JY. Purification, partial characterization and anti-inflammatory characteristics of lotus (Nelumbo nucifera Gaertn) plumule polysaccharides. Food Chem. 2012;135(3):1818-27. doi: 10.1016/j.foodchem.2012.06.063, PMID 22953928.
Dwyer JM, Johnson C. The use of concanavalin A to study the immunoregulation of human T cells. Clin Exp Immunol. 1981;46(2):237-49. PMID 6461456.
Reeves PG, Rossow KL, Lindlauf J. Development and testing of the AIN-93 purified diets for rodents: results on growth, kidney calcification and bone mineralization in rats and mice. J Nutr. 1993;123(11):1923-31. doi: 10.1093/jn/123.11.1923, PMID 8229309.
Folch J, Lees M, Sloane Stanley GH. A simple method for isolating and purifying total lipids from animal tissues. J Biol Chem. 1957;226(1):497-509. doi: 10.1016/S0021-9258(18)64849-5, PMID 13428781.
Lengi AJ, Phillips RA, Karpuzoglu E, Ahmed SA. Estrogen selectively regulates chemokines in murine splenocytes. J Leukoc Biol. 2007;81(4):1065-74. doi: 10.1189/jlb.0606391, PMID 17185357.
Wang J, Zhang Q, Jin S, He D, Zhao S, Liu S. Genistein modulate immune responses in a collagen-induced rheumatoid arthritis model. Maturitas. 2008;59(4):405-12. doi: 10.1016/j.maturitas.2008.04.003, PMID 18499367.
Engvall E, Jonsson K, Perlmann P. Enzyme-linked immunosorbent assay. II. Quantitative assay of a protein antigen, immunoglobulin G, using enzyme-labelled antigen and antibody-coated tubes. Biochim Biophys Acta. 1971;251(3):427-34. doi: 10.1016/0005-2795(71)90132-2, PMID 11452886.
Chomczynski P, Mackey K. Short technical reports. Modification of the TRI reagent procedure for isolating RNA from polysaccharide- and proteoglycan-rich sources. BioTechniques. 1995;19(6):942-5. PMID 8747660.
Bennet CA, Franklin NI. Statistical analysis of chemistry and the chemical Industry. London: John Wiley & Sons Inc; 1967. p. 208-27.
Weber C, Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med. 2011;17(11):1410-22. doi: 10.1038/nm.2538, PMID 22064431.
Ratheesh M, Shyni GL, Sindhu G, Helen A. Inhibitory effect of Ruta graveolens L. on oxidative damage, inflammation and aortic pathology in hypercholesterolemic rats. Exp Toxicol Pathol. 2011;63(3):285-90. doi: 10.1016/j.etp.2010.01.007, PMID 20163942.
Min B. Spontaneous T cell proliferation: A physiologic process to create and maintain homeostatic balance and diversity of the immune system. Front Immunol. 2018; 9;9:547.10.3389. doi: 10.3389/fimmu.2018.00547, PMID 29616038.
Uyemura, Koichi & Demer, L & castle. Steven Jullien Denis Berl J Gately M Warrier Rajeev Pharm, N & Fogelman, A. & Modlin, R. Cross-regulatory roles of interleukin (IL)-12 and IL-10 in atherosclerosis. The Journal of clinical investigation. 1996; 97: 2130-8. 10.1172/JCI118650.
Yuan L, Wang M, Liu T, Lei Y, Miao Q, Li Q et al.Carbonic Anhydrase 1-Mediated Calcification Is Associated With Atherosclerosis, and Methazolamide Alleviates Its Pathogenesis. Front Pharmacol. 2019;10:766. doi: 10.3389/fphar.2019.00766, PMID 31354482.
Larsberg F, Sprecher M, Hesse D, Brockmann GA, Kreuzer-Redmer S. Chicken immune cell assay to model adaptive immune responses in vitro. Animals (Basel). 2021;11(12):3600. doi: 10.3390/ani11123600, PMID 34944374.
Fasano R, Malerba E, Prete M, Solimando AG, Buonavoglia A, Silvestris N et al. Impact of antigen presentation mechanisms on immune response in autoimmune hepatitis. Front Immunol. 2021;12:814155. doi: 10.3389/fimmu.2021.814155, PMID 35116039.
Ando Y, Yasuoka C, Mishima T, Ikematsu T, Ueda T, Matsunaga T et al. Concanavalin A-mediated T cell proliferation is regulated by herpes virus entry mediator co-stimulatory molecule. In Vitro Cell Dev Biol Anim. 2014;50(4):313-20. doi: 10.1007/s11626-013-9705-2, PMID 24163161.
Wen YH, Lin WT, Wang WT, Chen DP. CD28 gene polymorphisms in the promoter region are associated with transfusion reactions: A functional study. J Clin Med. 2021;10(4):871. doi: 10.3390/jcm10040871, PMID 33672525.
LeBlanc R, Hideshima T, Catley LP, Shringarpure R, Burger R, Mitsiades N et al. Immunomodulatory drug costimulates T cells via the B7-CD28 pathway. Blood. 2004;103(5):1787-90. doi: 10.1182/blood-2003-02-0361, PMID 14512311.
Lee S, Yu S, Park HJ, Jung J, Go GW, Kim W. Rice bran oil ameliorates inflammatory responses by enhancing mitochondrial respiration in murine macrophages. PLOS ONE. 2019;14(10):e0222857. doi: 10.1371/journal.pone.0222857, PMID 31603952.
Fatkhullina AR, Peshkova IO, Koltsova EK. The role of cytokines in the development of atherosclerosis. Biochemistry (Mosc). 2016;81(11):1358-70. doi: 10.1134/S0006297916110134, PMID 27914461.
Yang R, Weisshaar M, Mele F, Benhsaien I, Dorgham K, Han J et al. High Th2 cytokine levels and upper airway inflammation in human inherited T-bet deficiency. J Exp Med. 2021;218(8):e20202726. doi: 10.1084/jem.20202726, PMID 34160550.
Buono C, Binder CJ, Stavrakis G, Witztum JL, Glimcher LH, Lichtman AH. T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses. Proc Natl Acad Sci U S A. 2005;102(5):1596-601. doi: 10.1073/pnas.0409015102, PMID 15665085.
Published
How to Cite
Issue
Section
Copyright (c) 2023 Lal Preethi Suja Sathyaseelan, Vidya Sabu, Dr. A. Helen
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.