Passiflora edulis leaf extract inhibits inflammatory response and preserves intestinal barrier function in Caco-2 and RAW264.7 co-culture model

Autores

DOI:

https://doi.org/10.5327/fst.109422

Palavras-chave:

gut inflammation, Passiflora edulis leaf extract, intestinal bowel disease, intestinal barrier

Resumo

Inflammatory bowel disease (IBD) is a chronic and incurable illness that affects people all over the world. Conventional therapies usually cause adverse side effects that may affect patients’ quality of life. This study assessed the effect of the aqueous extract of Passiflora edulis leaves (PELE) in co-culture of Caco-2 and RAW264.7 cells, simulating an in vitro model of IBD. After being stimulated with bacterial-derived lipopolysaccharides (LPS), PELE’s treatment inhibited the release of the pro-inflammatory cytokines interleukin (IL) 6 and 8, although was not able to reduce nitric oxide (NO) production. In the co-culture system, PELE was also able to preserve the intestinal barrier function by decreasing paracellular permeability and increasing transepithelial electrical resistance (TEER) values, compromised after the LPS stimulus. The beneficial activity seen in this in vitro study may suggest that PELE has a possible anti-inflammatory role in IBD and can alleviate inflammatory events.

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Referências

Albuquerque, M. A. C., Levit, R., Beres, C., Bedani, R., LeBlanc, A. de M. de, Saad, S. M. I., & LeBlanc, J. G. (2019). Tropical fruit by-products water extracts as sources of soluble fibres and phenolic compounds with potential antioxidant, anti-inflammatory, and functional properties. Journal of Functional Foods, 52, 724-733. https://doi.org/10.1016/j.jff.2018.12.002

Anilkumar, K., Reddy, G. V., Azad, R., Yarla, N. S., Dharmapuri, G., Srivastava, A., Kamal, M. A., & Pallu, R. (2017). Evaluation of anti-inflammatory properties of isoorientin isolated from tubers of Pueraria tuberosa. Oxidative Medicine and Cellular Longevity, 2017, 5498054. https://doi.org/10.1155/2017/5498054

Barbosa, P. P. M., Ruviaro, A. R., Martins, I. M., Macedo, J. A., LaPointe, G., & Macedo, G. A. (2020). Effect of enzymatic treatment of citrus by-products on bacterial growth, adhesion and cytokine production by Caco-2 cells. Food and Function, 11(10), 8996. https://doi.org/10.1039/d0fo01963a

Carmo, M. C. L., Martins, I. M., Barbosa, P. de P. M., Macedo, G. A., & Macedo, J. A. (2020a). Passiflora edulis extract effects on probiotic and pathogenic modulation for healthier microbiota. Nutrire, 45, 15. https://doi.org/10.1186/s41110-020-00117-1

Carmo, M. C. L., Martins, I. M., Magalhães, A. E. R., Maróstica Júnior, M. R., & Macedo, J. A. (2020b). Passion fruit (Passiflora edulis) leaf aqueous extract ameliorates intestinal epithelial barrier dysfunction and reverts inflammatory parameters in Caco-2 cells monolayer. Food Research International, 133, 109162. https://doi.org/10.1016/j.foodres.2020.109162

Cazarin, C. B. B., da Silva, J. K., Colomeu, T. C., Batista, Â. G., Meletti, L. M. M., Paschoal, J. A. R., Bogusz Junior, S., de Campos Braga, P. A., Reyes, F. G. R., Augusto, F., de Meirelles, L. R., de Lima Zollner, R., & Maróstica Júnior, M. R. (2015). Intake of Passiflora edulis leaf extract improves antioxidant and anti-inflammatory status in rats with 2,4,6-trinitrobenzenesulphonic acid induced colitis. Journal of Functional Foods, 17, 575-586. https://doi.org/10.1016/j.jff.2015.05.034

Colomeu, T. C., Figueiredo, D., Cazarin, C. B. B., Schumacher, N. S. G., Maróstica, M. R., Meletti, L. M. M., & Zollner, R. L. (2014). Antioxidant and anti-diabetic potential of Passiflora alata Curtis aqueous leaves extract in type 1 diabetes mellitus (NOD-mice). International Immunopharmacology, 18(1), 106-115. https://doi.org/10.1016/j.intimp.2013.11.005

Cross, R. K., & Wilson, K. T. (2003). Nitric oxide in inflammatory bowel disease. Inflammatory Bowel Diseases, 9(3), 179-189. https://doi.org/10.1097/00054725-200305000-00006

Ding, X., Hu, X., Chen, Y., Xie, J., Ying, M., Wang, Y., & Yu, Q. (2021). Differentiated Caco-2 cell models in food-intestine interaction study: Current applications and future trends. Trends in Food Science & Technology, 107, 455-465. https://doi.org/10.1016/j.tifs.2020.11.015

Frontela-Saseta, C., López-Nicolás, R., González-Bermúdez, C. A., Martínez-Graciá, C., & Ros-Berruezo, G. (2013). Anti-inflammatory properties of fruit juices enriched with pine bark extract in an in vitro model of inflamed human intestinal epithelium: The effect of gastrointestinal digestion. Food and Chemical Toxicology, 53, 94-99. https://doi.org/10.1016/j.fct.2012.11.024

García-Lafuente, A., Guillamón, E., Villares, A., Rostagno, M. A., & Martínez, J. A. (2009). Flavonoids as anti-inflammatory agents: implications in cancer and cardiovascular disease. Inflammation Research, 58, 537-552. https://doi.org/10.1007/s00011-009-0037-3

Green, L. C., Wagner, D. A., Glogowski, J., Skipper, P. L., Wishnok, J. S., & Tannenbaum, S. R. (1982). Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Analytical Biochemistry, 126(1), 131-138. https://doi.org/10.1016/0003-2697(82)90118-X

He, S., Li, X., Li, C., Deng, H., Shao, Y., & Yuan, L. (2019). Isoorientin attenuates benzo[a]pyrene-induced colonic injury and gut microbiota disorders in mice. Food Research International, 126, 108599. https://doi.org/10.1016/j.foodres.2019.108599

He, X., Luan, F., Yang, Y., Wang, Z., Zhao, Z., Fang, J., Wang, M., Zuo, M., & Li, Y. (2020). Passiflora edulis: an insight into current researches on phytochemistry and pharmacology. Frontiers in Pharmacology, 11, 617. https://doi.org/10.3389/fphar.2020.00617

Huang, B. P., Lin, C. H., Chen, Y. C., & Kao, S. H. (2014). Anti-inflammatory effects of Perilla frutescens leaf extract on lipopolysaccharide-stimulated RAW264.7 cells. Molecular Medicine Reports, 10(2), 1077-1083. https://doi.org/10.3892/mmr.2014.2298

Kaplan, G. G. (2015). The global burden of IBD: from 2015 to 2025. Nature Reviews Gastroenterology and Hepatology, 12, 720-727. https://doi.org/10.1038/nrgastro.2015.150

Katsanos, K. H., Papamichael, K., Feuerstein, J. D., Christodoulou, D. K., & Cheifetz, A. S. (2019). Biological therapies in inflammatory bowel disease: Beyond anti-TNF therapies. Clinical Immunology, 206, 9-14. https://doi.org/10.1016/j.clim.2018.03.004

Kim, K. J., Kim, Y., Jin, S. G., & Kim, J. Y. (2021). Acai berry extract as a regulator of intestinal inflammation pathways in a Caco-2 and RAW 264.7 co-culture model. Journal of Food Biochemistry, 45(8), e13848. https://doi.org/10.1111/jfbc.13848

Kim, K. M., Kim, Y. S., Lim, J. Y., Min, S. J., Ko, H. C., Kim, S. J., & Kim, Y. (2014). Intestinal anti-inflammatory activity of Sasa quelpaertensis leaf extract by suppressing lipopolysaccharide-stimulated inflammatory mediators in intestinal epithelial Caco-2 cells co-cultured with RAW 264.7 macrophage cells. Nutrition Research and Practice, 9(1), 3-10. https://doi.org/10.4162/nrp.2015.9.1.3

Kubes, P., & McCafferty, D. M. (2000). Nitric oxide and intestinal inflammation. The American Journal of Medicine, 109(2), 150-158. https://doi.org/10.1016/S0002-9343(00)00480-0

León-Rodríguez, M. C. P., Guyot, J.-P., & Laurent-Babot, C. (2019). Intestinal in vitro cell culture models and their potential to study the effect of food components on intestinal inflammation. Critical Reviews in Food Science and Nutrition, 59(22), 3648-3666. https://doi.org/10.1080/10408398.2018.1506734

Leonard, F., Collnot, E. M., & Lehr, C. M. (2010). A three-dimensional coculture of enterocytes, monocytes and dendritic cells to model inflamed intestinal mucosa in vitro. Molecular Pharmaceutics, 7(6), 2103-2119. https://doi.org/10.1021/mp1000795

Li, H., Christman, L.M., Li, R., Gu, L. (2020). Synergic interactions between polyphenols and gut microbiota in mitigating inflammatory bowel diseases. Food & Function, 11(6), 4878-4891. https://doi.org/10.1039/D0FO00713G

Liu, F., Li, D., Wang, X., Cui, Y., & Li, X. (2020). Polyphenols intervention is an effective strategy to ameliorate inflammatory bowel disease: a systematic review and meta-analysis. International Journal of Food Sciences and Nutrition, 72(1), 14-25. https://doi.org/10.1080/09637486.2020.1760220

Lloyd-Price, J., Arze, C., Ananthakrishnan, A. N., Schirmer, M., Avila-Pacheco, J., Poon, T. W., Andrews, E., Ajami, N. J., Bonham, K. S., Brislawn, colin J., Casero, D., Courtney, H., Gonzalez, A., Graeber, thomas G., Brantley Hall, A., Lake, K., Landers, carol J., Mallick, H., Plichta, D., … Huttenhower, C. (2019). Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature, 569, 655-662. https://doi.org/10.1038/s41586-019-1237-9

Machado, A. P. F., Geraldi, M. V., Nascimento, R. P., Moya, A. M. T. M., Vezza, T., Diez-Echave, P., Gálvez, J. J., Cazarin, C. B. B., & Maróstica Júnior, M. R. (2021). Polyphenols from food by-products: An alternative or complementary therapy to IBD conventional treatments. Food Research International, 140, 110018. https://doi.org/10.1016/j.foodres.2020.110018

Montanher, A. B., Zucolotto, S. M., Schenkel, E. P., & Fröde, T. S. (2007). Evidence of anti-inflammatory effects of Passiflora edulis in an inflammation model. Journal of Ethnopharmacology, 109(2), 281-288. https://doi.org/10.1016/j.jep.2006.07.031

Mu, K., Yu, S., & Kitts, D. D. (2019). The role of nitric oxide in regulating intestinal redox status and intestinal epithelial cell functionality. International Journal of Molecular Sciences, 20(7), 1755. https://doi.org/10.3390/ijms20071755

Neurath, M. F. (2014). Cytokines in inflammatory bowel disease. Nature Reviews Immunology, 14, 329-342. https://doi.org/10.1038/nri3661

Olejnik, A., Kowalska, K., Olkowicz, M., Juzwa, W., Dembczyński, R. D., & Schmidt, M. (2016). A gastrointestinally digested Ribes nigrum L. fruit extract inhibits inflammatory response in a co-culture model of intestinal Caco-2 cells and RAW264.7 macrophages. Journal of Agriculture and Food Chemistry, 64(41), 7710-7721. https://doi.org/10.1021/acs.jafc.6b02776

Silva, F. A. R., Rodrigues, B. L., Ayrizono, M. L. S., & Leal, R. F. (2016). The immunological basis of inflammatory bowel disease. Gastroenterology Research and Practice, 2097274. https://doi.org/10.1155/2016/2097274

Silva, J. K., Cazarin, C. B. B., Colomeu, T. C., Batista, Â. G., Meletti, L. M. M., Paschoal, J. A. R., Bogusz Júnior, S., Furlan, M. F., Reyes, F. G. R., Augusto, F., Maróstica Júnior, M. R., & de Lima Zollner, R. (2013). Antioxidant activity of aqueous extract of passion fruit (Passiflora edulis) leaves: In vitro and in vivo study. Food Research International, 53(2), 882-890. https://doi.org/10.1016/j.foodres.2012.12.043

Tanoue, T., Nishitani, Y., Kanazawa, K., Hashimoto, T., & Mizuno, M. (2008). In vitro model to estimate gut inflammation using co-cultured Caco-2 and RAW264.7 cells. Biochemical and Biophysical Research Communications, 374(3), 565-569. https://doi.org/10.1016/j.bbrc.2008.07.063

Valdez, J. C., Cho, J., & Bolling, B. W. (2020). Aronia berry inhibits disruption of Caco-2 intestinal barrier function. Archives of Biochemistry and Biophysics, 688, 108409. https://doi.org/10.1016/j.abb.2020.108409

Van De Walle, J., Hendrickx, A., Romier, B., Larondelle, Y., & Schneider, Y. J. (2010). Inflammatory parameters in Caco-2 cells: Effect of stimuli nature, concentration, combination and cell differentiation. Toxicology in Vitro, 24(5), 1441-1449. https://doi.org/10.1016/j.tiv.2010.04.002

Wedler, J., Daubitz, T., Schlotterbeck, G., & Butterweck, V. (2014). In vitro anti-inflammatory and wound-healing potential of a Phyllostachys edulis leaf extract – identification of isoorientin as an active compound. Planta Medica, 80(18), 1678-1684. https://doi.org/10.1055/s-0034-1383195

Yuan, L., Han, X., Li, W., Ren, D., & Yang, X. (2016). Isoorientin prevents hyperlipidemia and liver injury by regulating lipid metabolism, antioxidant capability, and inflammatory cytokine release in high-fructose-fed mice. Journal of Agricultural and Food Chemistry, 64(13), 2682-2689. https://doi.org/10.1021/acs.jafc.6b00290

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Publicado

2023-10-09

Como Citar

CARMO, M. C. L. do, MARTINS, I. M., MAGALHÃES, A. E. R., CHIOCCHETTI, G. de M. e, MARÓSTICA JÚNIOR, M. R. M. J., & MACEDO, J. A. (2023). Passiflora edulis leaf extract inhibits inflammatory response and preserves intestinal barrier function in Caco-2 and RAW264.7 co-culture model. Food Science and Technology, 43. https://doi.org/10.5327/fst.109422

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