Soyasaponins can blunt inflammation by inhibiting the reactive oxygen species-mediated activation of PI3K/Akt/NF-kB pathway

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Zha, Longying ^a,d   Chen, Jiading ^a   Sun, Suxia ^a   Mao, Limei ^a   Chu, Xinwei ^a   Deng, Hong ^a   Cai, Junwei ^b,d   Li, Xuefeng ^b   Liu, Zhenqi ^c   Cao, Wenhong ^b,d,e  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b HUBEI UNIVERSITY OF MEDICINE   (China)

^c UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^d University of North Carolina   (United States)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; ACETYLCYSTEINE; CYCLOOXYGENASE 2; GLUTATHIONE; GLUTATHIONE DISULFIDE; I KAPPA B ALPHA; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MALONALDEHYDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN E2; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SAPONIN DERIVATIVE; SOYASAPONIN A1; SOYASAPONIN A2; SOYASAPONIN I; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; 3-(4-METHYLPHENYLSULFONYL)-2-PROPENENITRILE; CHROMONE DERIVATIVE; CHUK PROTEIN, MOUSE; I KAPPA B KINASE; MORPHOLINE DERIVATIVE; NITRILE; OLEANOLIC ACID; PTGS2 PROTEIN, MOUSE; RELA PROTEIN, MOUSE; SAPONIN; SULFONE;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; INFLAMMATION; MACROPHAGE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; MOUSE; PHOSPHORYLATION; SECRETION (PROCESS); SIGNAL TRANSDUCTION; SOYBEAN;

ANIMALS; CELL LINE; CHROMONES; CYCLOOXYGENASE 2; DINOPROSTONE; I-KAPPA B KINASE; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MALONDIALDEHYDE; MICE; MORPHOLINES; NITRILES; OLEANOLIC ACID; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; SAPONINS; SIGNAL TRANSDUCTION; SOYBEANS; SULFONES; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR RELA;

EID: 84907224839     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107655     Document Type: Article

References (52)

1. Kaplan MJ (2009) Management of cardiovascular disease risk in chronic inflammatory disorders. Nature Reviews Rheumatology 5: 208-217.
2. Olefsky JM, Glass C.K. (2010) Macrophages, inflammation, and insulin resistance. Annual Review of Physiology 72: 219-246.
3. Coussens LM, Werb Z. (2002) Inflammation and cancer. Nature 420: 860-867.
4. Yoon JH, Baek S.J. (2005) Molecular targets of dietary polyphenols with anti-inflammatory properties. Yonsei Medical Journal 46: 585-596.
5. Yadav VR, Prasad S, Sung B., Kannappan R, Aggarwal B.B. (2010) Targeting inflammatory pathways by triterpenoids for prevention and treatment of cancer. Toxins 2: 2428-2466.
6. Hirai S, Takahashi N, Goto T., Lin S, Uemura T, et al (2010) Functional food targeting the regulation of obesity-induced inflammatory responses and pathologies. Mediators of Inflammation 2010: 367838.
7. Sakurai H (2012) Targeting of TAK1 in inflammatory disorders and cancer. Trends in Pharmacological Sciences 33: 522-530.
8. Azadbakht L, Kimiagar M, Mehrabi Y., Esmaillzadeh A, Hu FB, et al (2007) Soy consumption, markers of inflammation, and endothelial function: a crossover study in postmenopausal women with the metabolic syndrome. Diabetes Care 30: 967-973.
9. Azadbakht L, Atabak S, Esmaillzadeh A. (2008) Soy protein intake, cardiorenal indices, and C-reactive protein in type 2 diabetes with nephropathy: a longitudinal randomized clinical trial. Diabetes Care 31: 648-654.
10. Boyapati SM, Shu XO, Ruan Z.X., Dai Q., Cai Q, et al. (2005) Soyfood intake and breast cancer survival: a followup of the Shanghai Breast Cancer Study. Breast Cancer Research and Treatment 92: 11-17.
11. Toyomura K, Kono S. (2002) Soybeans, Soy Foods, Isoflavones and Risk of Colorectal Cancer: a Review of Experimental and Epidemiological Data. Asian Pacific Journal of Cancer Prevention: APJCP 3: 125-132.
12. Messina MJ (1999) Legumes and soybeans: overview of their nutritional profiles and health effects. The American Journal of Clinical Nutrition 70: 439S-450S.
13. Kang J, Badger TM, Ronis M.J., Wu X. (2010) Non-isoflavone phytochemicals in soy and their health effects. Journal of Agricultural and Food Chemistry 58: 8119-8133.
14. Isanga J, Zhang G.N. (2008) Soybean bioactive components and their implications to health: a review. Food Reviews Internatioal 24: 252-276.
15. Zhang W, Popovich D.G. (2008) Effect of soyasapogenol A and soyasapogenol B concentrated extracts on HEP-G2 cell proliferation and apoptosis. Journal of Agricultural and Food Chemistry 56: 2603-2608.
16. Zhang W, Popovich D.G. (2009) Chemical and biological characterization of oleanane triterpenoids from soy. Molecules 14: 2959-2975.
17. Berhow MA, Wagner ED, Vaughn S.F., Plewa M.J. (2000) Characterization and antimutagenic activity of soybean saponins. Mutation Research 448: 11-22.
18. Jun HS, Kim SE, Sung M.K. (2002) Protective effect of soybean saponins and major antioxidants against aflatoxin B1-induced mutagenicity and DNA-adduct formation. Journal of Medicinal Food 5: 235-240.
19. Xiao JX, Huang GQ, Zhang S.H. (2007) Soyasaponins inhibit the proliferation of Hela cells by inducing apoptosis. Experimental and Toxicologic Pathology: Official Journal of the Gesellschaft fur Toxikologische Pathologie 59: 35-42.
20. Hayashi K, Hayashi H, Hiraoka N., Ikeshiro Y. (1997) Inhibitory activity of soyasaponin II on virus replication in vitro. Planta Medica 63: 102-105.
21. Nakashima H, Okubo K, Honda Y., Tamura T, Matsuda S, et al (1989) Inhibitory effect of glycosides like saponin from soybean on the infectivity of HIV in vitro. AIDS 3: 655-658.
22. Kinjo J, Imagire M, Udayama M., Arao T, Nohara T. (1998) Structure-hepatoprotective relationships study of soyasaponins I - IV having soyasapogenol B as aglycone. Planta Medica 64: 233-236.
23. Kinjo J, Hirakawa T, Tsuchihashi R., Nagao T, Okawa M, et al (2003) Hepatoprotective constituents in plants. 14. Effects of soyasapogenol B, sophoradiol, and their glucuronides on the cytotoxicity of tert-butyl hydroperoxide to HepG2 cells. Biological & Pharmaceutical Bulletin 26: 1357-1360.
24. Ishii Y, Tanizawa H. (2006) Effects of soyasaponins on lipid peroxidation through the secretion of thyroid hormones. Biological & Pharmaceutical Bulletin 29: 1759-1763.
25. Lee SO, Simons AL, Murphy P.A., Hendrich S. (2005) Soyasaponins lowered plasma cholesterol and increased fecal bile acids in female golden Syrian hamsters. Experimental Biology and Medicine (Maywood) 230: 472-478.
26. Oakenfull D, Sidhu G.S. (1990) Could saponins be a useful treatment for hypercholesterolaemia? European Journal of Clinical Nutrition 44: 79-88.
27. Zha LY, Mao LM, Lu X.C., Deng H., Ye JF, et al. (2011) Anti-inflammatory effect of soyasaponins through suppressing nitric oxide production in LPS-stimulated RAW 264.7 cells by attenuation of NF-kappaB-mediated nitric oxide synthase expression. Bioorganic & Medicinal Chemistry Letters 21: 2415-2418.
28. Kang JH, Sung MK, Kawada T, Yoo H., Kim YK, et al. (2005) Soybean saponins suppress the release of proinflammatory mediators by LPS-stimulated peritoneal macrophages. Cancer Letters 230: 219-227.
29. Lee IA, Park YJ, Yeo H.K., Han MJ, Kim D.H. (2010) Soyasaponin I Attenuates TNBS-Induced Colitis in Mice by Inhibiting NF-kappaB Pathway. Journal of Agricultural and Food Chemistry 58: 10929-10934.
30. Barnes PJ, Karin M. (1997) Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. The New England Journal of Medicine 336: 1066-1071.
31. Li Q, Withoff S, Verma I.M. (2005) Inflammation-associated cancer: NF-kappaB is the lynchpin. Trends in Immunology 26: 318-325.
32. Luo J.L. KH, Karin M. (2013) IKK/NF-kB signaling: balancing life and death - a new approach to cancer therapy. The Journal of Clinical Investigation 15: 2625-2632.
33. Hattori Y, Hattori S, Kasai K. (2003) Lipopolysaccharide activates Akt in vascular smooth muscle cells resulting in induction of inducible nitric oxide synthase through nuclear factor-kappa B activation. European Journal of Pharmacology 481: 153-158.
34. Venkatesan B, Valente AJ, Prabhu S.D., Shanmugam P., Delafontaine P, et al. (2010) EMMPRIN activates multiple transcription factors in cardiomyocytes, and induces interleukin-18 expression via Rac1-dependent PI3 K/Akt/IKK/NF-kappaB and MKK7/JNK/AP-1 signaling. Journal of Molecular and Cellular Cardiology 49: 655-663.
35. Murillo MM, Carmona-Cuenca I, Del Castillo G, Ortiz C, Roncero C., et al. (2007) Activation of NADPH oxidase by transforming growth factor-beta in hepatocytes mediates up-regulation of epidermal growth factor receptor ligands through a nuclear factor-kappaB-dependent mechanism. The Biochemical Journal 405: 251-259.
36. Bhattacharyya J, Biswas S, Datta A.G. (2004) Mode of action of endotoxin: role of free radicals and antioxidants. Current Medicinal Chemistry 11: 359-368.
37. Hennessy BT, Smith DL, Ram P.T., Lu Y., Mills G.B. (2005) Exploiting the PI3K/AKT pathway for cancer drug discovery. Nature Reviews Drug Discovery 4: 988-1004.
38. Liu HY, Hong T, Wen G.B., Han J., Zuo D, et al. (2009) Increased basal level of Akt-dependent insulin signaling may be responsible for the development of insulin resistance. American Journal of Physiology Endocrinology and Metabolism 297: E898-906.
39. Cao W, Ning J, Liu H.Y., Hong T., Liu Z. (2011) Excess Exposure to Insulin is the Primary Cause of Insulin Resistance and its Associated Atherosclerosis. Current Molecular Pharmacology 4: 154-166.
40. Accili D (2004) Lilly lecture 2003: the struggle for mastery in insulin action: from triumvirate to republic. Diabetes 53: 1633-1642.
41. Burns JM, Donnelly JE, Anderson H.S., Mayo MS, Spencer-Gardner L, et al. (2007) Peripheral insulin and brain structure in early Alzheimer disease. Neurology 69: 1094-1104.
42. Cole GM, Frautschy S.A. (2007) The role of insulin and neurotrophic factor signaling in brain aging and Alzheimer's Disease. Experimental Gerontology 42: 10-21.
43. Crowell JA, Steele VE, Fay J.R. (2007) Targeting the AKT protein kinase for cancer chemoprevention. Molecular Cancer and Therapy 6: 2139-2148.
44. Al-Shawwa B.A., Al-Huniti NH, DeMattia L., Gershan W. (2007) Asthma and insulin resistance in morbidly obese children and adolescents. Journal of Asthma 44: 469-473.
45. Sterry W, Strober BE, Menter A. (2007) Obesity in psoriasis: the metabolic, clinical and therapeutic implications. Report of an interdisciplinary conference and review. British Journal Dermatology 157: 649-655.
46. Popa C, Netea MG, van Riel PL, van der Meer JW, Stalenhoef AF (2007) The role of TNF-alpha in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. Journal of Lipid Research 48: 751-762.
47. Okazaki R (2008) [Links between osteoporosis and atherosclerosis; beyond insulin resistance]. Clinical Calcium 18: 638-643.
48. Kerwin SM (2004) Soy saponins and the anticancer effects of soybeans and soy-based foods. Current Medicinal Chemistry Anti-Cancer Agents 4: 263-272.
49. Messina MJ, Persky V, Setchell K.D., Barnes S. (1994) Soy intake and cancer risk: a review of the in vitro and in vivo data. Nutrition and Cancer 21: 113-131.
50. Scherz-Shouval R., Elazar Z. (2011) Regulation of autophagy by ROS: physiology and pathology. Trends in Biochemical Sciences 36: 30-38.
51. Yoshiki Y, Okubo K. (1995) Active oxygen scavenging activity of DDMP (2, 3-dihydroxyl-4H-pyran-4 one) saponin in soybean seed. Bioscience, Biotechnology, and Biochemistry 59: 1556-1557.
52. Ray PD, Huang BW, Tsuji Y. (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cellular Signalling 24: 981-990.