GL-V9, a new synthetic flavonoid derivative, ameliorates DSSinduced colitis against oxidative stress by up-regulating Trx-1 expression via activation of AMPK/FOXO3a pathway

Oncotarget

Volumn 6, Issue 28, 2015, Pages 26291-26307

  Zhao, Yue ^a   Sun, Yang ^a   Ding, Youxiang ^a   Wang, Xiaoping ^a   Zhou, Yuxin ^a   Li, Wenjun ^a   Huang, Shaoliang ^a   Li, Zhiyu ^b   Kong, Lingyi ^c   Guo, Qinglong ^a   Lu, Na ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b Pharmaceutical University   (China)

^c China Pharmaceutical University   (China)

Author keywords

AMPK; Colitis; GL V9; ROS; Trx 1

Indexed keywords

5 HYDROXY 8 METHOXY 2 PHENYL 7 [4 (PYRROLIDIN 1 YL)BUTOXY] 4H CHROMEN 4 ONE; DEXTRAN SULFATE; FLAVONOID; GAMMA INTERFERON; GLUTATHIONE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MALONALDEHYDE; MESALAZINE; MYELOPEROXIDASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; THIOREDOXIN 1; TRANSCRIPTION FACTOR FKHRL1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 5-HYDROXY-8-METHOXY-2-PHENYL-7-(4-(PYRROLIDIN-1-YL)BUTOXY)4H-CHROMEN-4-ONE; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; AUTACOID; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, MOUSE; GASTROINTESTINAL AGENT; THIOREDOXIN; TXN1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; COLON INJURY; COLON LENGTH SHORTENING; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEXTRAN SODIUM SULFATE-INDUCED COLITIS; DIGESTIVE TRACT PARAMETERS; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MECHANISM; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNOHISTOCHEMISTRY; INFLAMMATORY INFILTRATE; MACROPHAGE; METABOLIC PARAMETERS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTECTION; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SYNTHESIS INHIBITION; RAW264.7 CELL LINE; TOTAL ANTIOXIDANT CAPACITY; UPREGULATION; WEIGHT REDUCTION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COLITIS; COLON; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; METABOLISM; PATHOLOGY; RAW 264.7 CELL LINE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTOR;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; COLITIS; COLON; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; FEMALE; FLAVONOIDS; FORKHEAD BOX PROTEIN O3; FORKHEAD TRANSCRIPTION FACTORS; GASTROINTESTINAL AGENTS; INFLAMMATION MEDIATORS; MACROPHAGES; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; RAW 264.7 CELLS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; THIOREDOXINS; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 84944463499     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4657     Document Type: Article

References (66)

1. Fiocchi C. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology. 1998; 115:182-205.
2. Sartor RB. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol. 2006; 3:390-407.
3. Conner EM, Brand SJ, Davis JM, Kang DY, Grisham MB. Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease: toxins, mediators, and modulators of gene expression. Inflamm Bowel Dis. 1996; 2:133-147.
4. Grisham MB. Oxidants and free radicals in inflammatory bowel disease. Lancet. 1994; 344:859-861.
5. Harris ML, Schiller HJ, Reilly PM, Donowitz M, Grisham MB, Bulkley GB. Free radicals and other reactive oxygen metabolites in inflammatory bowel disease: cause, consequence or epiphenomenon? Pharmacol Ther. 1992; 53:375-408.
6. Kruidenier L, Verspaget HW. Review article: oxidative stress as a pathogenic factor in inflammatory bowel disease -radicals or ridiculous? Aliment Pharmacol Ther. 2002; 16:1997-2015.
7. Kemp BE, Stapleton D, Campbell DJ, Chen ZP, Murthy S, Walter M, Gupta A, Adams JJ, Katsis F, van Denderen B, Jennings IG, Iseli T, Michell BJ, Witters LA. AMPactivated protein kinase, super metabolic regulator. Biochem Soc Trans. 2003; 31:162-168.
8. Canto C, Auwerx J. AMP-activated protein kinase and its downstream transcriptional pathways. Cell Mol Life Sci. 2010; 67:3407-3423.
9. Steinberg GR, Kemp BE. AMPK in Health and Disease. Physiol Rev. 2009; 89:1025-1078.
10. Han Y, Wang Q, Song P, Zhu Y, Zou MH. Redox regulation of the AMP-activated protein kinase. PLoS One. 2010; 5:e15420.
11. Canto C, Auwerx J. Calorie restriction: is AMPK a key sensor and effector? Physiology (Bethesda). 2011; 26:214-224.
12. Colombo SL, Moncada S. AMPKalpha1 regulates the antioxidant status of vascular endothelial cells. Biochem J. 2009; 421:163-169.
13. Xie Z, He C, Zou MH. AMP-activated protein kinase modulates cardiac autophagy in diabetic cardiomyopathy. Autophagy. 2011; 7:1254-1255.
14. Katerelos M, Mudge SJ, Stapleton D, Auwardt RB, Fraser SA, Chen CG, Kemp BE, Power DA. 5-ami noimid azole-4-carboxamide ribonucleoside and AMP-activated protein kinase inhibit signalling through NF-kappaB. Immunol Cell Biol. 2010; 88:754-760.
15. Kukidome D, Nishikawa T, Sonoda K, Imoto K, Fujisawa K, Yano M, Motoshima H, Taguchi T, Matsumura T, Araki E. Activation of AMP-activated protein kinase reduces hyperglycemia-induced mitochondrial reactive oxygen species production and promotes mitochondrial biogenesis in human umbilical vein endothelial cells. Diabetes. 2006; 55:120-127.
16. Storz P. Forkhead homeobox type O transcription factors in the responses to oxidative stress. Antioxid Redox Signal. 2011; 14:593-605.
17. Sengupta A, Molkentin JD, Paik JH, DePinho RA, Yutzey KE. FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem. 2011; 286:7468-7478.
18. Maiese K, Chong ZZ, Hou J, Shang YC. Oxidative stress: Biomarkers and novel therapeutic pathways. Exp Gerontol. 2010; 45:217-234.
19. Ronnebaum SM, Patterson C. The FoxO family in cardiac function and dysfunction. Annu Rev Physiol. 2010; 72:81-94.
20. Zoccarato F, Cavallini L, Alexandre A. Respirationdependent removal of exogenous H2O2 in brain mitochondria: inhibition by Ca2+. J Biol Chem. 2004; 279:4166-4174.
21. Drechsel DA, Patel M. Respiration-dependent H2O2 removal in brain mitochondria via the thioredoxin/peroxiredoxin system. J Biol Chem. 2010; 285:27850-27858.
22. Yamawaki H, Haendeler J, Berk BC. Thioredoxin: a key regulator of cardiovascular homeostasis. Circ Res. 2003; 93:1029-1033.
23. Shioji K, Kishimoto C, Nakamura H, Masutani H, Yuan Z, Oka S, Yodoi J. Overexpression of thioredoxin-1 in transgenic mice attenuates adriamycin-induced cardiotoxicity. Circulation. 2002; 106:1403-1409.
24. Bai J, Nakamura H, Hattori I, Tanito M, Yodoi J. Thioredoxin suppresses 1-methyl-4-phenylpyridiniuminduced neurotoxicity in rat PC12 cells. Neurosci Lett. 2002; 321:81-84.
25. Hoshino T, Nakamura H, Okamoto M, Kato S, Araya S, Nomiyama K, Oizumi K, Young HA, Aizawa H, Yodoi J. Redox-active protein thioredoxin prevents proinflammatory cytokine- or bleomycin-induced lung injury. Am J Respir Crit Care Med. 2003; 168:1075-1083.
26. Tan A, Nakamura H, Kondo N, Tanito M, Kwon YW, Ahsan MK, Matsui H, Narita M, Yodoi J. Thioredoxin-1 attenuates indomethacin-induced gastric mucosal injury in mice. Free Radic Res. 2007; 41:861-869.
27. Takagi Y, Mitsui A, Nishiyama A, Nozaki K, Sono H, Gon Y, Hashimoto N, Yodoi J. Overexpression of thioredoxin in transgenic mice attenuates focal ischemic brain damage. Proc Natl Acad Sci U S A. 1999; 96:4131-4136.
28. Tanito M, Masutani H, Nakamura H, Oka S, Ohira A, Yodoi J. Attenuation of retinal photooxidative damage in thioredoxin transgenic mice. Neurosci Lett. 2002; 326:142-146.
29. Kasuno K, Nakamura H, Ono T, Muso E, Yodoi J. Protective roles of thioredoxin, a redox-regulating protein, in renal ischemia/reperfusion injury. Kidney Int. 2003; 64:1273-1282.
30. Tamaki H, Nakamura H, Nishio A, Nakase H, Ueno S, Uza N, Kido M, Inoue S, Mikami S, Asada M, Kiriya K, Kitamura H, Ohashi S, Fukui T, Kawasaki K, Matsuura M, et al. Human thioredoxin-1 ameliorates experimental murine colitis in association with suppressed macrophage inhibitory factor production. Gastroenterology. 2006; 131:1110-1121.
31. Li L, Lu N, Dai Q, Wei L, Zhao Q, Li Z, He Q, Dai Y, Guo Q. GL-V9, a newly synthetic flavonoid derivative, induces mitochondrial-mediated apoptosis and G2/M cell cycle arrest in human hepatocellular carcinoma HepG2 cells. Eur J Pharmacol. 2011; 670:13-21.
32. Li L, Chen P, Ling Y, Song X, Lu Z, He Q, Li Z, Lu N, Guo Q. Inhibitory effects of GL-V9 on the invasion of human breast carcinoma cells by downregulating the expression and activity of matrix metalloproteinase-2/9. Eur J Pharm Sci. 2011; 43:393-399.
33. Huang WH, Lee AR, Yang CH. Antioxidative and antiinflammatory activities of polyhydroxyflavonoids of Scutellaria baicalensis GEORGI. Biosci Biotechnol Biochem. 2006; 70:2371-2380.
34. Yao J, Pan D, Zhao Y, Zhao L, Sun J, Wang Y, You QD, Xi T, Guo QL, Lu N. Wogonin prevents lipopolysaccharide- induced acute lung injury and inflammation in mice via peroxisome proliferator-activated receptor gammamediated attenuation of the nuclear factor-kappaB pathway. Immunology. 2014; 143:241-257.
35. Yao J, Zhao L, Zhao Q, Zhao Y, Sun Y, Zhang Y, Miao H, You QD, Hu R, Guo QL. NF-kappaB and Nrf2 signaling pathways contribute to wogonin-mediated inhibition of inflammation-associated colorectal carcinogenesis. Cell Death Dis. 2014; 5:e1283.
36. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990; 98:694-702.
37. Serra AM, Waddell J, Manivannan A, Xu H, Cotter M, Forrester JV. CD11b+ bone marrow-derived monocytes are the major leukocyte subset responsible for retinal capillary leukostasis in experimental diabetes in mouse and express high levels of CCR5 in the circulation. Am J Pathol. 2012; 181:719-727.
38. Garside P. Cytokines in experimental colitis. Clin Exp Immunol. 1999; 118:337-339.
39. Banks C, Bateman A, Payne R, Johnson P, Sheron N. Chemokine expression in IBD. Mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn's disease. J Pathol. 2003; 199:28-35.
40. Araki Y, Andoh A, Fujiyama Y. The free radical scavenger edaravone suppresses experimental dextran sulfate sodiuminduced colitis in rats. Int J Mol Med. 2003; 12:125-129.
41. Li XN, Song J, Zhang L, LeMaire SA, Hou X, Zhang C, Coselli JS, Chen L, Wang XL, Zhang Y, Shen YH. Activation of the AMPK-FOXO3 pathway reduces fatty acid-induced increase in intracellular reactive oxygen species by upregulating thioredoxin. Diabetes. 2009; 58:2246-2257.
42. Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental influences. Gastroenterology. 2004; 126:1504-1517.
43. Mohamadzadeh M, Pfeiler EA, Brown JB, Zadeh M, Gramarossa M, Managlia E, Bere P, Sarraj B, Khan MW, Pakanati KC, Ansari MJ, O'Flaherty S, Barrett T, Klaenhammer TR. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci U S A. 2011; 108:4623-4630.
44. Coskun M, Nielsen OH. Tumor necrosis factor inhibitors for inflammatory bowel disease. N Engl J Med. 2013; 369:2561-2562.
45. Meier J, Sturm A. Current treatment of ulcerative colitis. World J Gastroenterol. 2011; 17:3204-3212.
46. Perse M, Cerar A. Dextran sodium sulphate colitis mouse model: traps and tricks. J Biomed Biotechnol. 2012; 2012:718617.
47. Nakashima T, Maeda T, Nagamoto H, Kumakura T, Takai M, Mori T. Rebamipide enema is effective for treatment of experimental dextran sulfate sodium induced colitis in rats. Dig Dis Sci. 2005; 50:S124-131.
48. Zheng L, Gao ZQ, Wang SX. A chronic ulcerative colitis model in rats. World J Gastroenterol. 2000; 6:150-152.
49. Kannan N, Guruvayoorappan C. Protective effect of Bauhinia tomentosa on acetic acid induced ulcerative colitis by regulating antioxidant and inflammatory mediators. Int Immunopharmacol. 2013; 16:57-66.
50. Oz HS, Chen TS, McClain CJ, de Villiers WJ. Antioxidants as novel therapy in a murine model of colitis. J Nutr Biochem. 2005; 16:297-304.
51. Kruidenier L, Kuiper I, Van Duijn W, Mieremet-Ooms MA, van Hogezand RA, Lamers CB, Verspaget HW. Imbalanced secondary mucosal antioxidant response in inflammatory bowel disease. J Pathol. 2003; 201:17-27.
52. Martensson J, Jain A, Meister A. Glutathione is required for intestinal function. Proc Natl Acad Sci U S A. 1990; 87:1715-1719.
53. Chapuis N, Tamburini J, Green AS, Willems L, Bardet V, Park S, Lacombe C, Mayeux P, Bouscary D. Perspectives on inhibiting mTOR as a future treatment strategy for hematological malignancies. Leukemia. 2010; 24:1686-1699.
54. Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell. 2006; 124:471-484.
55. Holz MK, Ballif BA, Gygi SP, Blenis J. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell. 2005; 123:569-580.
56. Sun SY. Impact of genetic alterations on mTOR-targeted cancer therapy. Chin J Cancer. 2013; 32:270-274.
57. van der Horst A, Burgering BM. Stressing the role of FoxO proteins in lifespan and disease. Nat Rev Mol Cell Biol. 2007; 8:440-450.
58. van der Horst A, de Vries-Smits AM, Brenkman AB, van Triest MH, van den Broek N, Colland F, Maurice MM, Burgering BM. FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat Cell Biol. 2006; 8:1064-1073.
59. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 2004; 303:2011-2015.
60. van der Horst A, Tertoolen LG, de Vries-Smits LM, Frye RA, Medema RH, Burgering BM. FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J Biol Chem. 2004; 279:28873-28879.
61. Zhao Y, Yao J, Wu XP, Zhao L, Zhou YX, Zhang Y, You QD, Guo QL, Lu N. Wogonin suppresses human alveolar adenocarcinoma cell A549 migration in inflammatory microenvironment by modulating the IL-6/STAT3 signaling pathway. Mol Carcinog. 2014.
62. Wu X, Yang Y, Dou Y, Ye J, Bian D, Wei Z, Tong B, Kong L, Xia Y, Dai Y. Arctigenin but not arctiin acts as the major effective constituent of Arctium lappa L. fruit for attenuating colonic inflammatory response induced by dextran sulfate sodium in mice. Int Immunopharmacol. 2014; 23:505-515.
63. Yao J, Hu R, Sun J, Lin B, Zhao L, Sha Y, Zhu B, You QD, Yan T, Guo QL. Oroxylin A prevents inflammationrelated tumor through down-regulation of inflammatory gene expression by inhibiting NF-kappaB signaling. Mol Carcinog. 2014; 53:145-158.
64. Qiang L, Yang Y, You QD, Ma YJ, Yang L, Nie FF, Gu HY, Zhao L, Lu N, Qi Q, Liu W, Wang XT, Guo QL. Inhibition of glioblastoma growth and angiogenesis by gambogic acid: an in vitro and in vivo study. Biochem Pharmacol. 2008; 75:1083-1092.
65. Mu R, Qi Q, Gu H, Wang J, Yang Y, Rong J, Liu W, Lu N, You Q, Guo Q. Involvement of p53 in oroxylin A-induced apoptosis in cancer cells. Mol Carcinog. 2009; 48:1159-1169.
66. Dan HC, Cooper MJ, Cogswell PC, Duncan JA, Ting JP, Baldwin AS. Akt-dependent regulation of NF-{kappa}B is controlled by mTOR and Raptor in association with IKK. Genes Dev. 2008; 22:1490-1500.