Cleistocalyx nervosum var. paniala Fruit Extract Attenuates Interleukin-1β-Induced Inflammation in Human Retinal Pigment Epithelial Cells

Authors

  • Pranee Srimard Graduate student in Master of Science Program in Nutrition, Faculty of Medicine Ramathibodi Hospital and Institute of Nutrition, Mahidol University, Bangkok, Thailand.
  • Chawanphat Muangnoi Cell and Animal Model Unit, Institute of Nutrition, Mahidol University, Nakhon Pathom, Thailand
  • Siriporn Tuntipopipat Cell and Animal Model Unit, Institute of Nutrition, Mahidol University, Nakhon Pathom, Thailand
  • Somsri Charoenkiatkul Institute of Nutrition, Mahidol University, Nakhon Pathom, Thailand.
  • Monruedee Sukprasansap Food Toxicology Unit, Institute of Nutrition, Mahidol University

Keywords:

Cleistocalyx nervosum var. paniala, Anti-inflammation, Human retinal pigment epithelial ARPE-19 cells

Abstract

Inflammation in retinal pigment epithelial (RPE) cells is a crucial event in the initiation of age-related macular degeneration (AMD). Ripe fruit of Cleistocalyx nervosum var. paniala, or “Ma-kiang,” contains abundant phytochemicals, especially anthocyanin, which is a plentiful source of antioxidant and anti-inflammatory activities. However, the effects of this ripe fruit on RPE cells have not yet been studied. The present research investigated the inhibitory effect of C. nervosum var. paniala fruit extract on interleukin (IL)-1β-mediated inflammation in human retinal pigment epithelial cells (ARPE-19). The ripe fruits of C. nervosum var. paniala were extracted using ethanol (CEE). Total anthocyanin content of the extract was analyzed using spectrophotometry, which showed high total anthocyanin content (31.54 ± 0.53 mg cyanidin-3-glucoside [C3G] equivalent/100 g DW). For the cell-based investigation, ARPE-19 cells were pretreated with CEE (5-500 µg/ml) or C3G at 100 µM for 1 h prior to co-incubation with or without IL-1β (0.1 ng/ml) for 24 h, and cell viability measured by MTT assay. Thereafter, a culture medium was collected to detect inflammatory mediators, namely, IL-6, IL-8, and monocyte chemoattractant protein-1 using ELISA kit assays. Our results showed that CEE and C3G treatments at all concentrations were not toxic. They also exhibited good potential to significantly inhibit IL-1β-induced inflammatory cytokines and chemokine in ARPE-19 cells. Consequently, our findings suggest that CEE and its major anthocyanin C3G have good anti-inflammatory potential. This fruit might be utilized as a natural alternative product to prevent inflammation-related AMD.

References

Brooks P. Inflammation as an important feature of osteoarthritis. Bulletin of the World Health Organization. 2003;81(9):689-90.

Sun K, Tordjman J, Clément K, Scherer PE. Fibrosis and adipose tissue dysfunction. Cell metabolism. 2013;18(4):470-7.

Zou M, Zhang Y, Chen A, Young CA, Li Y, Zheng D, et al. Variations and trends in global disease burden of age‐related macular degeneration: 1990‐2017. Acta Ophthalmol. 2021;99(3):e330-e5.

Mitchell P, Liew G, Gopinath B, Wong TY. Age-related macular degeneration. The Lancet. 2018;392(10153):1147-59.

Nowak JZ. Age-related macular degeneration (AMD): pathogenesis and therapy. Pharmacol Rep. 2006;58(3):353.

Arya M, Sabrosa AS, Duker JS, Waheed NK. Choriocapillaris changes in dry age-related macular degeneration and geographic atrophy: a review. Eye and Vision. 2018;5(1):1-7.

Juhn SK, Jung M-K, Hoffman MD, Drew BR, Preciado DA, Sausen NJ, et al. The role of inflammatory mediators in the pathogenesis of otitis media and sequelae. Clin Exp Otorhinolaryngol. 2008;1(3):117-38.

Cheng S-C, Huang W-C, S. Pang J-H, Wu Y-H, Cheng C-Y. Quercetin inhibits the production of IL-1β-induced inflammatory cytokines and chemokines in ARPE-19 cells via the MAPK and NF-κB signaling pathways. Int J Mol Sci. 2019;20(12):2957.

Škrovánková S, Mišurcová L, Machů L. Antioxidant activity and protecting health effects of common medicinal plants. Adv Food Nutr Res. 2012;67:75-139.

Diniz do Nascimento L, Moraes AABd, Costa KSd, Pereira Galúcio JM, Taube PS, Costa CML, et al. Bioactive natural compounds and antioxidant activity of essential oils from spice plants: New findings and potential applications. Biomolecules. 2020;10(7):988.

Dzoyem JP, Eloff JN. Anti-inflammatory, anticholinesterase and antioxidant activity of leaf extracts of twelve plants used traditionally to alleviate pain and inflammation in South Africa. J Ethnopharmacol. 2015;160:194-201.

Azarpazhooh E, Sharayei P, Zomorodi S, Ramaswamy HS. Physicochemical and phytochemical characterization and storage stability of freeze-dried encapsulated pomegranate peel anthocyanin and in vitro evaluation of its antioxidant activity. Food Bioproc Tech. 2019;12(2):199-210.

Jezek M, Zörb C, Merkt N, Geilfus C-M. Anthocyanin management in fruits by fertilization. J Agr Food Chem. 2018;66(4):753-64.

Meydan I, Kizil G, Demir H, Ceken Toptanci B, Kizil M. In vitro DNA damage, protein oxidation protective activity and antioxidant potentials of almond fruit (Amygdalus trichamygdalus) parts (hull and drupe) using soxhlet ethanol extraction. Adv Trad Med. 2020;20(4):571-9.

Shahreza FD. Oxidative stress, free radicals, kidney disease and plant antioxidants. Immunopathologia Persa. 2016;3(2):e11.

Engwa GA. Free radicals and the role of plant phytochemicals as antioxidants against oxidative stress-related diseases. Phytochemicals: Source of Antioxidants and Role in Disease Prevention. BoD–Books on Demand. 2018.

Kizawa Y, Sekikawa T, Kageyama M, Tomobe H, Kobashi R, Yamada T. Effects of anthocyanin, astaxanthin, and lutein on eye functions: a randomized, double-blind, placebo-controlled study. J Clin Biochem Nutr. 2021:20-149.

Cherlet A. The disease-fighting power of berries. Life Extension magazine. 2008;9:1-2.

Yang J, Cui J, Chen J, Yao J, Hao Y, Fan Y, et al. Evaluation of physicochemical properties in three raspberries (Rubus idaeus) at five ripening stages in northern China. Scientia Horticulturae. 2020;263:109146.

Tantratian S, Balmuang N, Krusong W. Phenolic enrichment of Ma-Kieng seed extract using absorbent and this enriched extract application for safety control of fresh-cut cantaloupe. LWT. 2019;106:105-12.

Prasansuklab A, Brimson JM, Tencomnao T. Potential Thai medicinal plants for neurodegenerative diseases: A review focusing on the anti-glutamate toxicity effect. J Tradi Compl Med. 2020;10(3):301-8.

Prasanth MI, Brimson JM, Chuchawankul S, Sukprasansap M, Tencomnao T. Antiaging, stress resistance, and neuroprotective efficacies of Cleistocalyx nervosum var. paniala fruit extracts using Caenorhabditis elegans model. Oxidative Med Cell Long. 2019;2019.

Brimson JM, Prasanth MI, Isidoro C, Sukprasansap M, Tencomnao T. Cleistocalyx nervosum var. paniala seed extracts exhibit sigma-1 antagonist sensitive neuroprotective effects in PC12 cells and protects C. elegans from stress via the SKN-1/NRF-2 pathway. Nutr Healthy Aging. 2021;6(2):131-46.

Sukprasansap M, Chanvorachote P, Tencomnao T. Cleistocalyx nervosum var. paniala berry fruit protects neurotoxicity against endoplasmic reticulum stress-induced apoptosis. Food Chem Tox. 2017;103:279-88.

Nantacharoen W, Baek SJ, Plaingam W, Charoenkiatkul S, Tencomnao T, Sukprasansap M. Cleistocalyx nervosum var. paniala Berry Promotes Antioxidant Response and Suppresses Glutamate-Induced Cell Death via SIRT1/Nrf2 Survival Pathway in Hippocampal HT22 Neuronal Cells. Molecules. 2022;27(18):5813.

Abdel‐Aal ES, Hucl P. A rapid method for quantifying total anthocyanins in blue aleurone and purple pericarp wheats. Cereal Chem. 1999;76(3):350-4.

Da Cunha A, Zhang Q, Prentiss M, Wu X, Kainz V, Xu Y, et al. The hierarchy of proinflammatory cytokines in ocular inflammation. Curr Eye Res. 2018;43(4):553-65.

Beaudry-Richard A, Nadeau-Vallée M, Prairie É, Maurice N, Heckel É, Nezhady M, et al. Antenatal IL-1-dependent inflammation persists postnatally and causes retinal and sub-retinal vasculopathy in progeny. Sci Rep. 2018;8(1):1-13.

Jansom C, Bhamarapravati S, Itharat A. Major anthocyanin from ripe berries of Cleistocalyx nervosum var. paniala. Thammasat Med J. 2008;8(3):364-70.

Charoensin S, Taya S, Wongpornchai S, Wongpoomchai R. Assessment of genotoxicity and antigenotoxicity of an aqueous extract of Cleistocalyx nervosum var. paniala in in vitro and in vivo models. Interdiscip Toxicol. 2012;5(4):201.

Pipattanamomgkol P, Lourith N, Kanlayavattanakul M. The natural approach to hair dyeing product with Cleistocalyx nervosum var. paniala. Sustain Chem Pharm. 2018;8:88-93.

Chariyakornkul A, Juengwiroj W, Ruangsuriya J, Wongpoomchai R. Antioxidant Extract from Cleistocalyx nervosum var. paniala Pulp Ameliorates Acetaminophen-Induced Acute Hepatotoxicity in Rats. Molecules. 2022;27(2):553.

Prasanth MI, Sivamaruthi BS, Sukprasansap M, Chuchawankul S, Tencomnao T, Chaiyasut C. Functional properties and bioactivities of Cleistocalyx nervosum var. paniala berry plant: a review. Food Sci Technol. 2020;40:369-73.

Jonas JB, Wei WB, Xu L, Wang YX. Systemic inflammation and eye diseases. The Beijing Eye Study. PLoS One. 2018;13(10):e0204263.

Hu W-W, Huang Y-K, Huang X-G. Comparison of peripheral blood inflammatory indices in patients with neovascular age-related macular degeneration and haemorrhagic polypoidal choroidal vasculopathy. Ocul Immunol Inflamm. 2022:1-5.

Pan M, Zhou P, Liu Z, Guo J, Du L, Jin X. Peripheral complete blood cell count indices and serum lipid levels in polypoidal choroidal vasculopathy. Clin Exp Optom. 2022:1-6.

Yoshimura T. The production of monocyte chemoattractant protein-1 (MCP-1)/CCL2 in tumor microenvironments. Cytokine. 2017;98:71-8.

Osuka K, Ohmichi Y, Ohmichi M, Nakura T, Iwami K, Watanabe Y, et al. Sequential Expression of Chemokines in Chronic Subdural Hematoma Fluids after Trepanation Surgery. J Neurotrauma. 2021;38(14):1979-87.

Sato T, Takeuchi M, Karasawa Y, Enoki T, Ito M. Intraocular inflammatory cytokines in patients with neovascular age-related macular degeneration before and after initiation of intravitreal injection of anti-VEGF inhibitor. Sci Rep. 2018;8(1):1-10.

Terao N, Koizumi H, Kojima K, Yamagishi T, Yamamoto Y, Yoshii K, et al. Distinct aqueous humour cytokine profiles of patients with pachychoroid neovasculopathy and neovascular age-related macular degeneration. Sci Rep. 2018;8(1):1-10.

Tan W, Zou J, Yoshida S, Jiang B, Zhou Y. The role of inflammation in age-related macular degeneration. Int J Biol Sci. 2020;16(15):2989.

Shukla R, Pandey V, Vadnere GP, Lodhi S. Role of flavonoids in management of inflammatory disorders. Bioactive food as dietary interventions for arthritis and related inflammatory diseases: Elsevier; 2019. p. 293-322.

Valdez JC, Bolling BW. Anthocyanins and intestinal barrier function: A review. J Food Bioact. 2019;5:18-30.

Stromsnes K, Correas AG, Lehmann J, Gambini J, Olaso-Gonzalez G. Anti-inflammatory properties of diet: Role in healthy aging. Biomedicines. 2021;9(8):922.

Iwashima T, Kudome Y, Kishimoto Y, Saita E, Tanaka M, Taguchi C, et al. Aronia berry extract inhibits TNF-α-induced vascular endothelial inflammation through the regulation of STAT3. Food & Nutr Res. 2019;63.

Islam SU, Lee JH, Shehzad A, Ahn E-M, Lee YM, Lee YS. Decursinol angelate inhibits LPS-induced macrophage polarization through modulation of the NFκB and MAPK signaling pathways. Molecules. 2018;23(8):1880.

Jayasinghe AMK, Kirindage KGIS, Fernando IPS, Han EJ, Oh G-W, Jung W-K, et al. Fucoidan isolated from sargassum confusum suppresses inflammatory responses and oxidative stress in tnf-α/ifn-γ-stimulated hacat keratinocytes by activating nrf2/ho-1 signaling pathway. Mar Drugs. 2022;20(2):117.

Chen Y, Shou K, Gong C, Yang H, Yang Y, Bao T. Anti-inflammatory effect of geniposide on osteoarthritis by suppressing the activation of p38 MAPK signaling pathway. BioMed Rres Int. 2018;2018.

Qiu T, Sun Y, Wang X, Zheng L, Zhang H, Jiang L, et al. Drum drying-and extrusion-black rice anthocyanins exert anti-inflammatory effects via suppression of the NF-κB/MAPKs signaling pathways in LPS-induced RAW 264.7 cells. Food BioSci. 2021;41:100841.

Jung S, Lee M-S, Choi A-J, Kim C-T, Kim Y. Anti-inflammatory effects of high hydrostatic pressure extract of mulberry (Morus alba) fruit on LPS-stimulated RAW264. 7 cells. Molecules. 2019;24(7).

Amin FU, Shah SA, Badshah H, Khan M, Kim MO. Anthocyanins encapsulated by PLGA@ PEG nanoparticles potentially improved its free radical scavenging capabilities via p38/JNK pathway against Aβ1–42-induced oxidative stress. J Nanobiotechnol. 2017;15(1):1-16.

Aboonabi A, Aboonabi A. Anthocyanins reduce inflammation and improve glucose and lipid metabolism associated with inhibiting nuclear factor-kappaB activation and increasing PPAR-γ gene expression in metabolic syndrome subjects. Free Radical Biology and Medicine. 2020;150:30-9.

Khoo HE, Azlan A, Tang ST, Lim SM. Anthocyanidins and anthocyanins: Colored pigments as food, pharmaceutical ingredients, and the potential health benefits. Food Nutr Res. 2017;61(1):1361779.

Krga I, Tamaian R, Mercier S, Boby C, Monfoulet L-E, Glibetic M, et al. Anthocyanins and their gut metabolites attenuate monocyte adhesion and transendothelial migration through nutrigenomic mechanisms regulating endothelial cell permeability. Free Radic Biol Med. 2018;124:364-79.

Downloads

Published

2022-11-04

How to Cite

Srimard, P., Muangnoi, C., Tuntipopipat, S., Charoenkiatkul, S., & Sukprasansap, M. (2022). Cleistocalyx nervosum var. paniala Fruit Extract Attenuates Interleukin-1β-Induced Inflammation in Human Retinal Pigment Epithelial Cells. Journal of Nutrition Association of Thailand, 57(2), 18–31. Retrieved from https://he01.tci-thaijo.org/index.php/JNAT/article/view/259090

Issue

Section

Research article