Abstract
Pro-inflammatory mediators produced during inflammatory response have been demonstrated to initiate and aggravate pathological development of several chronic diseases. Plant bioactive constituents have been reported to exert anti-inflammatory activities. Various parts of Moringa oleifera have long been used as habitual diets and traditional remedy along the tropical region. Anti-inflammatory activity of boiled M. oleifera pod extract was assessed by measuring pro-inflammatory mediator expression in the lipopolysaccharide-induced murine RAW264.7 macrophage cells. Prior treatment with 31–250 μg/mL M. oleifera extract for 1 h inhibited elevation of mRNA and protein level of interleukine-6, tumor necrosis factor-alpha, inducible nitric oxide synthase, and cyclooxygenease-2, induced by lipopolysaccharide for 24 h in a dose-dependent manner. The suppressive effect was mediated partly by inhibiting phosphorylation of inhibitor kappa B protein and mitogen-activated protein kinases. These results indicate that the anti-inflammatory activity from bioactive compounds present in the M. oleifera pod constituents may contribute to ameliorate the pathogenesis of inflammatory-associated chronic diseases.
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Guha, M., and N. Mackman. 2001. LPS induction of gene expression in human monocytes. Cellular Signalling 13: 85–94.
Ahn, K., and B. Aggrawal. 2005. Transcription factor NF-{kappa}B: a sensor for smoke and stress signals. Annals of the New York Academy of Science 1056: 218–233.
Medzhitov, R. 2008. Origin and physiological roles of inflammation. Nature 454: 428–435.
Aggarwal, B.B. 2004. Nuclear factor-[kappa]B: the enemy within. Cancer Cell 6: 203–208.
Bengmark, S. 2004. Acute and "chronic" phase reaction—a mother of disease. Clinical Nutrition 23: 1256–1266.
FitzGerald, G. 2004. Coxibs and cardiovascular disease. The New England Journal of Medicine 351: 1709–1711.
Gilani, A.H., and R. Atta-ur. 2005. Trends in ethnopharmacology. Journal of Ethnopharmacology 100: 43–49.
Block, G., B. Patterson, and A. Subar. 1992. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutrition and Cancer 18: 1–29.
Reddy, L., B. Odhav, and K.D. Bhoola. 2003. Natural products for cancer prevention: a global perspective. Pharmacology & Therapeutics 99: 1–13.
Steinmetz, K., and J. Potter. 1996. Vegetables, fruit, and cancer prevention: a review. Journal of the American Dietetic Association 96: 1027–1039.
Kris-Etherton, P.M., K.D. Hecker, A. Bonanome, S.M. Coval, A.E. Binkoski, K.F. Hilpert, A.E. Griel, and T.D. Etherton. 2002. Bioactive compounds in foods: their role in the prevention of cardiovascular disease and cancer. The American Journal of Medicine 113: 71–88.
Havsteen, B.H. 2002. The biochemistry and medical significance of the flavonoids. Pharmacology & Therapeutics 96: 67–202.
Prasad, S., K. Phromnoi, V.R. Yadav, M.M. Chaturvedi, and B.B. Aggarwal. 2010. Targeting inflammatory pathways by flavonoids for prevention and treatment of cancer. Planta Medica 76: 1044–1063.
Punturee, K., C. Wild, and U. Vinitketkumneun. 2004. Thai medicinal plants modulate nitric oxide and tumor necrosis factor-[alpha] in J774.2 mouse macrophages. Journal of Ethnopharmacology 95: 183–189.
Tuntipopipat, S., C. Muangnoi, and M.L. Failla. 2009. Anti-inflammatory activities of extracts of Thai spices and herbs with lipopolysaccharide-activated RAW 264.7 murine macrophages. Journal of Medicinal Food 12: 1213–1220.
Sae-wong, C., P. Tansakul, and S. Tewtrakul. 2009. Anti-inflammatory mechanism of Kaempferia parviflora in murine macrophage cells (RAW 264.7) and in experimental animals. Journal of Ethnopharmacology 124: 576–580.
Nanasombat, S., and N. Teckchuen. 2009. Antimicrobial, antioxidant and anticancer activities of Thai local vegetables. Journal of Medicinal Plants Research 3: 443–449.
Ramachandran, C., K.V. Peter, and P.K. Gopalakrishnan. 1980. Drumstick (Moringa oleifera): a multipurpose Indian vegetable. Economic Botany 34: 276–283.
Soliman, K.F., and E.A. Mazzio. 1998. In vitro attenuation of nitric oxide production in C6 astrocyte cell culture by various dietary compounds. Proceedings of the Society for Experimental Biology and Medicine 218: 390–397.
Morton, J.F. 1991. The horseradish tree, Moringa pterigosperma (Moringaceae). A boon to arid lands. Economic Botany 45: 318–333.
Anwar, F., S. Latif, M. Ashraf, and A. Gilani. 2007. Moringa oleifera: a food plant with multiple medicinal uses. Phytotherapy Research 21: 17–25.
Amaglo, N.K., R.N. Bennett, R.B. Lo Curto, E.A.S. Rosa, V. Lo Turco, A. Giuffrida, A.L. Curto, F. Crea, and G.M. Timpo. 2010. Profiling selected phytochemicals and nutrients in different tissues of the multipurpose tree Moringa oleifera L., grown in Ghana. Food Chemistry 122: 1047–1054.
Padmarao, P., B.M. Acharya, and T.J. Dennis. 1996. Pharmacognostic study on stembark of Moringa oleifera Lam. Bulletin Medico-Ethno-Botanical Research 17: 141–151.
Faizi, S., B.S. Siddiqui, R. Saleem, K. Aftab, F. Shaheen, and A.H. Gilani. 1998. Hypotensive constituents from the pods of Moringa oleifera. Planta Medica 64: 225–228.
Mahajan, S.G., R.G. Mali, and A.A. Mehta. 2007. Protective effect of ethanolic extract of seeds of Moringa oleifera Lam. against inflammation associated with development of arthritis in rats. Journal of Immunotoxicology 4: 39–47.
Chumark, P., P. Khunawat, Y. Sanvarinda, S. Phornchirasilp, N.P. Morales, L. Phivthong-ngam, P. Ratanachamnong, S. Srisawat, and KuS Pongrapeeporn. 2008. The in vitro and ex vivo antioxidant properties, hypolipidaemic and antiatherosclerotic activities of water extract of Moringa oleifera Lam. leaves. Journal of Ethnopharmacology 116: 439–446.
Mokkhasmit, M., K. Swasdimongkol, W. Ngarmwathana, and U. Permphiphat. 1971. Pharmacological evaluation of Thai medicinal plants. Journal of the Medical Association of Thailand 54: 490–504.
MaAaC, T.N.B.o.A.C.a.F.S. 2006. The amount of food consumption at 95 percentile per capita and eater only. In: Food Consumption Data of Thailand. The Agricultural Co-operative Federation of Thailand Bangkok, Thailand, p 173
Mughal, M.H., G. Ali, P.S. Srivastava, and M. Iqbal. 1999. Improvement of drumstick (Moringa pterygosperma Gaertn.)—a unique source of food and medicine through tissue culture. Hamdard medicus 42: 37–42.
Vichai, V., and K. Kirtikara. 2006. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nature Protocol 1: 1112–1116.
Green, L.C., D.A. Wagner, J. Glogowski, P.L. Skipper, J.S. Wishnok, and S.R. Tannenbaum. 1982. Analysis of nitrate, nitrite, and [15 N]nitrate in biological fluids. Analytical Biochemistry 126: 131–138.
Tuntipopipat, S., C. Muangnoi, P. Chingsuwanrote, M. Parengam, P. Chantravisut, S. Charoenkiatkul and S. Svasti. 2011. Anti-inflammatory activities of red curry paste extract on lipopolysaccharide-activated murine macrophage cell line. Nutrition (in press)
Hommes, D.W., M.P. Peppelenbosch, and S.J.H. van Deventer. 2003. Mitogen activated protein (MAP) kinase signal transduction pathways and novel anti-inflammatory targets. Gut 52: 144–151.
Valledor, A., M. Comalada, L. Santamaría-Babi, J. Lloberas, and A. Celada. 2010. Macrophage proinflammatory activation and deactivation: a question of balance. Advance Immunology 108: 1–20.
Moncada, S., R.M. Palmer, and E.A. Higgs. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmocological Review 43: 109–142.
Kolb, J., N. Paul-Eugene, C. Damais, K. Yamaoka, J. Drapier, and B. Dugas. 1994. Interleukin-4 stimulates cGMP production by IFN-gamma-activated human monocytes. Involvement of the nitric oxide synthase pathway. The Journal of Biological Chemistry 269: 9811–9816.
Coleman, J.W. 2001. Nitric oxide in immunity and inflammation. International Immunopharmacology 1: 1397–1406.
Yang, G.-Y., S. Taboada, and J. Liao. 2009. Inflammatory bowel disease: a model of chronic inflammation-induced cancer. Methods in Molecular Biology 511: 193–233.
Chun, O.K., S.J. Chung, and W.O. Song. 2007. Estimated dietary flavonoid intake and major food sources of U.S. adults. The Journal of Nutrition 137: 1244–1252.
Vane, J.R., Y.S. Bakhle, and R.M. Botting. 1998. Cyclooxygenases 1 and 2. Annual Review of Pharmacology and Toxicology 38: 97–120.
Krakauer, T. 2004. Molecular therapeutic targets in inflammation: cyclooxygenase and NF-kappaB. Current Drug Targets. Inflammation and Allergy 3: 317–324.
Pistoia, F., F. Cipollone, C. Ferri, M. Sarà, I. Sudano, and G.B. Desideri. 2010. Cyclooxygenase and atherosclerosis: a smoking area. Current Pharmaceutical Design 16: 2567–2571.
Cerella, C., C. Sobolewski, M. Dicato, and M. Diederich. 2010. Targeting COX-2 expression by natural compounds: a promising alternative strategy to synthetic COX-2 inhibitors for cancer chemoprevention and therapy. Biochemical Pharmacology 80: 1801–1815.
Mikuls, T.R., and K. Saag. 2001. Comorbidity in rheumatoid arthritis. Rheumatic Diseases Clinics of North America 27: 283–303.
Kang, R.Y., J. Freire-Moar, E. Sigal, and C.Q. Chu. 1996. Expression of cyclooxygenase-2 in human and an animal model of rheumatoid arthritis. British Journal of Rheumatology 35: 711–778.
Amin, A.R., M. Attur, R.N. Patel, G.D. Thakker, P.J. Marshall, J. Rediske, S.A. Stuchin, I.R. Patel, and S.B. Abramson. 1997. Superinduction of cyclooxygenase-2 activity in human osteoarthritis-affected cartilage. Influence of nitric oxide. The Journal of Clinical Investigation 99: 1231–1237.
Sano, H., Y. Kawahito, R.L. Wilder, A. Hashiramoto, S. Mukai, K. Asai, S. Kimura, H. Kato, M. Kondo, and T. Hla. 1995. Expression of cyclooxygenase-1 and -2 in human colorectal cancer. Cancer Research 55: 3785–3789.
Tsujii, M., S. Kawano, and R.N. DuBois. 1997. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proceedings of the National Academy of Sciences of the United States of America 94: 3336–3340.
Tsujii, M., S. Kawano, S. Tsuji, H. Sawaoka, M. Hori, and R.N. DuBois. 1998. Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 93: 705–716.
Feghali, C.A., and T.M. Wright. 1997. Cytokines in acute and chronic inflammation. Frontiers in Bioscience 1: 12–26.
Chandel, N.S., W.C. Trzyna, D.S. McClintock, and P.T. Schumacker. 2000. Role of oxidants in NF–κB activation and TNF-α gene transcription induced by hypoxia and endotoxin. Journal of Immunology 165: 1013–1021.
Aggarwal, B.B., S. Shishodia, S.K. Sandur, M.K. Pandey, and G. Sethi. 2006. Inflammation and cancer: how hot is the link? Biochemical Pharmacology 72: 1605–1621.
Zhang, X., H. Li, H. Feng, H. Xiong, L. Zhang, Y. Song, L. Yu, and X. Deng. 2009. Valnemulin downregulates nitric oxide, prostaglandin E2, and cytokine production via inhibition of NF-[kappa]B and MAPK activity. International Immunopharmacology 9: 810–816.
Trayhurn, P., and I.S. Wood. 2005. Signaling role of adipose tissue: adipokines and inflammation in obesity. Biochemical Society Transactions 33: 1078–1081.
Choy, E.H., and G.S. Panayi. 2001. Cytokine pathways and joint inflammation in rheumatoid arthritis. The New England Journal of Medicine 344: 907–916.
Tilg, H., and A.R. Moschen. 2006. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nature Reviews Immunology 6: 772–783.
Kaplanski, G., V. Marin, F. Montero-Julian, A. Mantovani, and C. Farnarier. 2003. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends in Immunology 24: 25–29.
Cronstein, B. 2007. Interleukin-6: a key mediator of systemic and local symptoms in rheumatoid arthritis. Bulletin of the NYU Hospital for Joint Diseases 65: S11–S15.
Pradhan, A.D., J.E. Manson, N. Rifai, J.E. Buring, and P.M. Ridker. 2001. C-Reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. Journal of the American Medical Association 286: 327–334.
Hennigan, S., and A. Kavanaugh. 2008. Interleukin-6 inhibitors in the treatment of rheumatoid arthritis. Ther Clin Risk Manag 4: 767–775.
Hodge, D.R., E.M. Hurt, and W.L. Farrar. 2005. The role of IL-6 and STAT3 in inflammation and cancer. European Journal of Cancer 41: 2502–2512.
Drachenberg, D.E., A.-A.A. Elgamal, R. Rowbotham, M. Peterson, and G.P. Murphy. 1999. Circulating levels of interleukin-6 in patients with hormone refractory prostate cancer. The Prostate 41: 127–133.
Tak, P.P., and G.S. Firestein. 2001. NF–κB: a key role in inflammatory diseases. The Journal of Clinical Investigation 107: 7–11.
Epstein, F.H., P.J. Barnes, and M. Karin. 1997. Nuclear factor-κB—a pivotal transcription factor in chronic inflammatory diseases. The New England Journal of Medicine 336: 1066–1071.
Sethi, G., and V. Tergaonkar. 2009. Potential pharmacological control of the NF-[kappa]B pathway. Trends in Pharmacological Sciences 30: 313–321.
Chang, L., and M. Karin. 2001. Mammalian MAP kinase signalling cascades. Nature 410: 37–40.
Kaminska, B. 2005. MAPK signalling pathways as molecular targets for anti-inflammatory therapy–from molecular mechanisms to therapeutic benefits. Biochimica et Biophysica Acta 1754: 253–262.
Kim, E.K., and E.-J. Choi. 2010. Pathological roles of MAPK signaling pathways in human diseases. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease 1802: 396–405.
Acknowledgment
This study was supported by National Science and Technology Development Agency, Thailand. The authors thank Dr. Harold C. Furr for his helpful commentary during manuscript preparation.
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Muangnoi, C., Chingsuwanrote, P., Praengamthanachoti, P. et al. Moringa oleifera Pod Inhibits Inflammatory Mediator Production by Lipopolysaccharide-Stimulated RAW 264.7 Murine Macrophage Cell Lines. Inflammation 35, 445–455 (2012). https://doi.org/10.1007/s10753-011-9334-4
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DOI: https://doi.org/10.1007/s10753-011-9334-4