Accessible Requires Authentication Published by De Gruyter July 25, 2019

Terminalia ferdinandiana, a traditional medicinal plant of Australia, alleviates hydrogen peroxide induced oxidative stress and inflammation, in vitro

Mridusmita Chaliha and Yasmina Sultanbawa

Abstract

Background

Oxidative stress and inflammation are the underlying factors in many chronic debilitating diseases and commonly intertwined. Terminalia ferdinandiana is a traditional medicinal plant, endemic to Australia and is a rich source of many bioactive phytochemicals such as ellagic acid (EA) with known antioxidant capacity.

Methods

We investigated the in vitro antioxidant and anti-inflammatory activity of an aqueous food grade EA enriched (EAE) extract of T. ferdinandiana. Caco-2 and KERTr cell lines were treated with EAE or pure EA (used as reference control), followed by the exposure to hydrogen peroxide (H2O2). Levels of reactive oxygen species (ROS) production and gene expression of molecular markers associated with oxidative stress and inflammation were monitored.

Results

Significant reduction in ROS production was observed in both cell types treated with 100 or 200 µg/mL EA or EAE. Treatment of cells with EAE or EA showed upregulation of mRNA expression of the antioxidative gene superoxide dismutase (SOD)-2 and downregulated the expression of inducible nitric oxide synthase (iNOS), soluble cell adhesion molecule (sICAM), and cyclooxygenase (COX)-2. Neither EAE nor EA had any effect on the constitutively expressed COX1.

Conclusions

The antioxidant and anti-inflammatory activity of T. ferdinandiana extract on mammalian cells exposed to H2O2 suggests the potential of using this traditional medicinal plant in preventing oxidative damage and inflammation related diseases.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This project supported by RIRDC Grant (2014-2018-PRJ 2014000161). M. Chaliha’s PhD supported by the Research Training Program (RTP) Scholarship.

  3. Employment or leadership: None declared.

  4. Honorarium: None declared.

  5. Competing interests: We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. The funding organizations played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

References

[1] Klaunig JE, Kamendulis LM. The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 2004;44:239–67. Search in Google Scholar

[2] Gamaley IA, Klyubin IV. Roles of reactive oxygen species: signaling and regulation of cellular functions. Int Rev Cytol 1999;188:203–55. Search in Google Scholar

[3] He Y, Yue Y, Zheng X, Zhang K, Chen S, Du Z. Curcumin, inflammation, and chronic diseases: how are they linked? Molecules 2015;20:9183–213. Search in Google Scholar

[4] Stankovic M, Topuzovic M, Solujic S, Mihailovic V. Antioxidant activity and concentration of phenols and flavonoids in the whole plant and plant parts of Teucrium chamaerdys L. var. Glanduliferum Haussk. J Med Plants Res 2010;4:2092–8. Search in Google Scholar

[5] Organization WH. Noncommunicable diseases: World Health Organization. Available from: http://www.who.int/mediacentre/factsheets/fs355/en/. 2017. Search in Google Scholar

[6] DeVol R, Bedroussian A, Charuworn A, Chatterjee A, Kim IK, Kim S, et al. An Unhealthy America: The Economic Burden of Chronic Disease. Charting a New Course to Save Lives and Increase Productivity and Economic Growth USA: The Milken Institute. Available from: http://www.milkeninstitute.org/publications/view/321. 2007. Search in Google Scholar

[7] Kok JL, Williams A, Zhao L. Psychosocial interventions for people with diabetes and co-morbid depression. A systematic review. Int J Nurs Stud 2015;52:1625–39. Search in Google Scholar

[8] Lim TK. Terminalia ferdinandiana. Edible medicinal and non-medicinal plants. Netherlands: Springer, 2012:158–60. Search in Google Scholar

[9] Wiynjorrotj P, Flora S, Brown ND, Jatbula P, Galmur J, Katherine M, et al. Jawoyn plants and animals. In: J Galmur, editor. Northern territory. Australia: Jawoyn Association, Northern Territory Government, 2005:234. Search in Google Scholar

[10] Conservation Commission of the Northern Territory. Traditional Aboriginal medicines in the Northern Territory of Australia Darwin: Conservation Commission of the Northern Territory of Australia, 1993. Search in Google Scholar

[11] Clarke PA. Aboriginal people and their plants. Dural, NSW, Australia: Rosenberg Publishing, 2007. Search in Google Scholar

[12] Konczak I, Maillot F, Dalar A. Phytochemical divergence in 45 accessions of Terminalia ferdinandiana (Kakadu plum). Food Chem 2014;151:248–56. Search in Google Scholar

[13] Konczak I, Zabaras D, Dunstan M, Aguas P. Antioxidant capacity and hydrophilic phytochemicals in commercially grown native Australian fruits. Food Chem 2010;123:1048–54. Search in Google Scholar

[14] Netzel M, Netzel G, Tian Q, Schwartz S, Konczak I. Native Australian fruits – a novel source of antioxidants for food. Innov Food Sci Emerg 2007;8:339–46. Search in Google Scholar

[15] Soong -Y-Y, Barlow PJ. Antioxidant activity and phenolic content of selected fruit seeds. Food Chem 2004;88:411–17. Search in Google Scholar

[16] Soong Y-Y, Barlow PJ. Quantification of gallic acid and ellagic acid from longan (Dimocarpus longan Lour.) seed and mango (Mangifera indica L.) kernel and their effects on antioxidant activity. Food Chem 2006;97:524–30. Search in Google Scholar

[17] Wang RF, Xie WD, Zhang Z, Xing DM, Ding Y, Wang W, et al. Bioactive compounds from the seeds of Punica granatum (pomegranate). J Nat Prod 2004;67:2096–8. Search in Google Scholar

[18] Chaliha M, Williams D, Edwards D, Pun S, Smyth H, Sultanbawa Y. Bioactive rich extracts from Terminalia ferdinandiana by enzyme-assisted extraction: a simple food safe extraction method. J Med Plants Res 2017;11:96–106. Search in Google Scholar

[19] Williams DJ, Edwards D, Pun S, Chaliha M, Sultanbawa Y. Profiling ellagic acid content: the importance of form and ascorbic acid levels. Food Res Int 2014;66:100–6. Search in Google Scholar

[20] Tan AC, Hou D-X, Konczak I, Tanigawa S, Ramzan I, Sze DM. Native Australian fruit polyphenols inhibit COX-2 and iNOS expression in LPS-activated murine macrophages. Food Res Int 2011;44:2362–7. Search in Google Scholar

[21] Akolkar G, da Silva Dias D, Ayyappan P, Bagchi AK, Jassal DS, Salemi VM, et al. Vitamin C mitigates oxidative/nitrosative stress and inflammation in doxorubicin-induced cardiomyopathy. Am J Physiol Heart Circ Physiol 2017;313:H795–H809. Search in Google Scholar

[22] Soardo G, Donnini D, Domenis L, Catena C, De Silvestri D, Cappello D, et al. Oxidative stress is activated by free fatty acids in cultured human hepatocytes. Metab Syndr Relat Disord 2011;9:397–401. Search in Google Scholar

[23] LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2′, 7′-dichlorofluorescein as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992;5:227–31. Search in Google Scholar

[24] Roschek B Jr., Fink RC, Li D, McMichael M, Tower CM, Smith RD, et al. Pro-inflammatory enzymes, cyclooxygenase 1, cyclooxygenase 2, and 5-lipooxygenase, inhibited by stabilized rice bran extracts J Med Food 2009;12:615–23. Search in Google Scholar

[25] García-Redondo AB, Briones AM, Beltrán AE, Alonso MJ, Simonsen U, Salaices M. Hypertension increases contractile responses to hydrogen peroxide in resistance arteries through increased thromboxane A2, Ca2+, and superoxide anion levels. J Pharmacol Exp Ther 2009;328:19. Search in Google Scholar

[26] Virdis A, Colucci R, Fornai M, Duranti E, Giannarelli C, Bernardini N, et al. Cyclooxygenase-1 is involved in endothelial dysfunction of mesenteric small arteries from angiotensin II-infused mice. Hypertension 2007;49:679–86. Search in Google Scholar

[27] Karlsson S, Nanberg E, Fjaeraa C, Wijkander J. Ellagic acid inhibits lipopolysaccharide-induced expression of enzymes involved in the synthesis of prostaglandin E2 in human monocytes. Br J Nutr 2010;103:1102–9. Search in Google Scholar

[28] Bjarnason I, Scarpignato C, Holmgren E, Olszewski M, Rainsford KD, Lanas A Mechanisms of damage to the gastrointestinal tract from non-steroidal anti-inflammatory drugs. Gastroenterology. 2017. Search in Google Scholar

[29] Morita I. Distinct functions of COX-1 and COX-2. Prostaglandins Other Lipid Mediat 2002;68–69:165–75. Search in Google Scholar

[30] Marrogi AJ, Travis WD, Welsh JA, Khan MA, Rahim H, Tazelaar H, et al. Nitric oxide synthase, cyclooxygenase 2, and vascular endothelial growth factor in the angiogenesis of non-small cell lung carcinoma. Clin Cancer Res 2000;6:4739–44. Search in Google Scholar

[31] Vakkala M, Kahlos K, Lakari E, Paakko P, Kinnula V, Soini Y. Inducible nitric oxide synthase expression, apoptosis, and angiogenesis in in situ and invasive breast carcinomas. Clin Cancer Res 2000;6:2408–16. Search in Google Scholar

[32] Santiago PG, Gasparotto FM, Gebara KS, Bacha FB, Livero F, Strapazon MA, et al. Mechanisms underlying antiatherosclerotic properties of an enriched fraction obtained from Ilex paraguariensis A. St-Hil Phytomed 2017;34:162–70. Search in Google Scholar

[33] Zhang J, Fan S, Mao Y, Ji Y, Jin L, Lu J, et al. Cardiovascular protective effect of polysaccharide from Ophiopogon japonicus in diabetic rats. Int J Biol Macromol 2016;82:505–13. Search in Google Scholar

[34] Manalil JJ, Baby M, Ramavarma SK, Suseela IM, Padikkala J, Raghavamenon A. Development of an anti-atherosclerotic polyherbal formulation: GSTC3. J Environ Pathol Toxicol Oncol 2015;34:237–48. Search in Google Scholar

[35] Zhao C, Sakaguchi T, Fujita K, Ito H, Nishida N, Nagatomo A, et al. Pomegranate-derived polyphenols reduce reactive oxygen species production via SIRT3-mediated SOD2 activation. Oxid Med Cell Longev 2016;2016:2927131. Search in Google Scholar

[36] Varma SR, Sivaprakasam TO, Mishra A, Kumar LM, Prakash NS, Prabhu S, et al. Protective effects of Triphala on dermal fibroblasts and human keratinocytes. PLoS One 2016;11:e0145921. Search in Google Scholar

[37] Tahan G, Aytac E, Aytekin H, Gunduz F, Dogusoy G, Aydin S, et al. Vitamin E has a dual effect of anti-inflammatory and antioxidant activities in acetic acid-induced ulcerative colitis in rats. Can J Surg 2011;54:333–8. Search in Google Scholar

[38] Hseu Y-C, Chou C-W, Senthil Kumar KJ, Fu K-T, Wang H-M, Hsu L-S, et al. Ellagic acid protects human keratinocyte (HaCaT) cells against UVA-induced oxidative stress and apoptosis through the upregulation of the HO-1 and Nrf-2 antioxidant genes. Food Chem Toxicol 2012;50:1245–55. Search in Google Scholar

[39] Kim Y-S, Zerin T, Song H-Y. Antioxidant action of ellagic acid ameliorates paraquat-induced A549 cytotoxicity. Biol Pharm Bull 2013;36:609–15. Search in Google Scholar

[40] Sarkar S, Siddiqui AA, Mazumder S, De R, Saha SJ, Banerjee C, et al. Ellagic acid, a Dietary polyphenol inhibits Tautomerase activity of human macrophage migration inhibitory factor and its pro-inflammatory responses in human peripheral blood mononuclear cells. J Agric Food Chem 2015;5:395–413. Search in Google Scholar

[41] Ahad A, Ganai AA, Mujeeb M, Siddiqui WA. Ellagic acid, an NF-kB inhibitor, ameliorates renal function in experimental diabetic nephropathy. Chem Biol Interact 2014;28:64–75. Search in Google Scholar

Supplementary Material

The online version of this article offers supplementary material (DOI:https://doi.org/10.1515/jcim-2019-0008).

Received: 2019-01-08
Accepted: 2019-04-11
Published Online: 2019-07-25

© 2019 Walter de Gruyter GmbH, Berlin/Boston