Curcumin inhibits the invasion of lung cancer cells by modulating the PKCα/Nox-2/ROS/ATF-2/MMP-9 signaling pathway

Oncology Reports

Volumn 34, Issue 2, 2015, Pages 691-698

  Fan, Zhigang ^a   Duan, Xiaoyi ^a   Cai, Hui ^a   Wang, Li ^a,b   Li, Min ^a   Qu, Jingkun ^a   Li, Wanjun ^a   Wang, Yongheng ^a   Wang, Jiansheng ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b CHANG'AN UNIVERSITY   (China)

Author keywords

Curcumin; Invasion; Lung cancer; Signaling pathway

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; CURCUMIN; GELATINASE B; PROTEIN KINASE C ALPHA; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMALL INTERFERING RNA; ANTINEOPLASTIC AGENT; ATF2 PROTEIN, HUMAN; CYBB PROTEIN, HUMAN; MEMBRANE PROTEIN; MMP9 PROTEIN, HUMAN; ONCOPROTEIN; PRKCA PROTEIN, HUMAN; PROTEIN TYROSINE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROS1 PROTEIN, HUMAN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INHIBITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LUNG CANCER; MITOSIS INHIBITION; MTT ASSAY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LUNG NEOPLASMS; METABOLISM; TUMOR CELL LINE;

ACTIVATING TRANSCRIPTION FACTOR 2; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CURCUMIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 9; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; PROTEIN KINASE C-ALPHA; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION;

EID: 84931318940     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2015.4044     Document Type: Article

References (41)

1. Minami-Shimmyo Y, Ohe Y, Yamamoto S, Sumi M, Nokihara H, Horinouchi H, Yamamoto N, Sekine I, Kubota K and Tamura T: Risk factors for treatment-related death associated with chemotherapy and thoracic radiotherapy for lung cancer. J Thorac Oncol 7: 177-182, 2012.
2. Hung JJ, Jeng WJ, Hsu WH, Chou TY, Huang BS and Wu YC: Predictors of death, local recurrence, and distant metastasis in completely resected pathological stage-I non-small-cell lung cancer. J Thorac Oncol 7: 1115-1123, 2012.
3. Schiavina R, Borghesi M, Brunocilla E, Manferrari F, Fiorentino M, Vagnoni V, Baccos A, Pultrone CV, Rocca GC, Rizzi S, et al: Differing risk of cancer death among patients with lymph node metastasis after radical prostatectomy and pelvic lymph node dissection: Identification of risk categories according to number of positive nodes and Gleason score. BJU Int 111: 1237-1244, 2013.
4. Mizutani K, Kofuji K and Shirouzu K: The significance of MMP-1 and MMP-2 in peritoneal disseminated metastasis of gastric cancer. Surg Today 30: 614-621, 2000.
5. Zhang HM, Han YJ, Zhao WB, Hu LJ, Fei YT and Tu Y: Effects of scalp acupuncture on expression of hippocampal MMP-9 in cerebral ischemia injury rats. Zhen Ci Yan Jiu 36: 193-198, 2011 (In Chinese).
6. Kim HJ, Fillmore HL, Reeves TM and Phillips LL: Elevation of hippocampal MMP-3 expression and activity during trauma-induced synaptogenesis. Exp Neurol 192: 60-72, 2005.
7. Sun C, Wang Q, Zhou H, Yu S, Simard AR, Kang C, Li Y, Kong Y, An T, Wen Y, et al: Antisense MMP-9 RNA inhibits malignant glioma cell growth in vitro and in vivo. Neurosci Bull 29: 83-93, 2013.
8. Lin ZM, Zhao JX, Duan XN, Zhang LB, Ye JM, Xu L and Liu YH: Effects of tissue factor, PAR-2 and MMP-9 expression on human breast cancer cell line MCF-7 invasion. Asian Pac J Cancer Prev 15: 643-646, 2014.
9. Oshima T, Kunisaki C, Yoshihara K, Yamada R, Yamamoto N, Sato T, Makino H, Yamagishi S, Nagano Y, Fujii S, et al: Clinicopathological significance of the gene expression of matrix metalloproteinases and reversion-inducing cysteine-rich protein with Kazal motifs in patients with colorectal cancer: MMP-2 gene expression is a useful predictor of liver metastasis from colorectal cancer. Oncol Rep 19: 1285-1291, 2008.
10. Lee LY, Wu CM, Wang CC, Yu JS, Liang Y, Huang KH, Lo CH and Hwang TL: Expression of matrix metalloproteinases MMP-2 and MMP-9 in gastric cancer and their relation to claudin-4 expression. Histol Histopathol 23: 515-521, 2008.
11. Park SY, Kim YH, Kim Y and Lee SJ: Frondoside A has an anti-invasive effect by inhibiting TPA-induced MMP-9 activation via NF-κB and AP-1 signaling in human breast cancer cells. Int J Oncol 41: 933-940, 2012.
12. Kim ES, Sohn YW and Moon A: TGF-beta-induced transcriptional activation of MMP-2 is mediated by activating transcription factor (ATF)2 in human breast epithelial cells. Cancer Lett 252: 147-156, 2007.
13. Hsieh HL, Lin CC, Shih RH, Hsiao LD and Yang CM: NADPH oxidase-mediated redox signal contributes to lipoteichoic acid-induced MMP-9 upregulation in brain astrocytes. J Neuroinflammation 9: 110, 2012.
14. 2+/ROS-mediated suppression of ERK/c-Fos pathway and activation of p38 MAPK/ATF-2 pathway. Toxicol Lett 191: 140-148, 2009.
15. Ji JL, Huang XF and Zhu HL: Curcumin and its formulations: Potential anti-cancer agents. Anticancer Agents Med Chem 12: 210-218, 2012.
16. Chen CC, Sureshbabul M, Chen HW, Lin YS, Lee JY, Hong QS, Yang YC and Yu SL: Curcumin suppresses metastasis via Sp-1, FAK inhibition, and E-cadherin upregulation in colorectal cancer. Evid Based Complement Alternat Med 2013: 541695, 2013.
17. Chen HW, Lee JY, Huang JY, Wang CC, Chen WJ, Su SF, Huang CW, Ho CC, Chen JJ, Tsai MF, et al: Curcumin inhibits lung cancer cell invasion and metastasis through the tumor suppressor HLJ1. Cancer Res 68: 7428-7438, 2008.
18. Chan WH, Wu HJ and Hsuuw YD: Curcumin inhibits ROS formation and apoptosis in methylglyoxal-treated human hepatoma G2 cells. Ann NY Acad Sci 1042: 372-378, 2005.
19. Carbone F, Camillo Teixeira P, Braunersreuther V, Mach F, Vuilleumier N and Montecucco F: Pathophysiology and treatments of oxidative injury in ischemic stroke: Focus on the phagocytic NADPH oxidase 2. Antioxid Redox Signal: Apr 22, 2014 (Epub ahead of print). doi:10.1089/ars.2013.5778.
20. Makino J, Kamiya T, Hara H and Adachi T: TPA induces the expression of EC-SOD in human monocytic THP-1 cells: Involvement of PKC, MEK/ERK and NOX-derived ROS. Free Radic Res 46: 637-644, 2012.
21. Soetikno V, Watanabe K, Sari FR, Harima M, Thandavarayan RA, Veeraveedu PT, Arozal W, Sukumaran V, Lakshmanan AP, Arumugam S, et al: Curcumin attenuates diabetic nephropathy by inhibiting PKC-α and PKC-β1 activity in streptozotocin-induced type I diabetic rats. Mol Nutr Food Res 55: 1655-1665, 2011.
22. Soh JW and Weinstein IB: Roles of specific isoforms of protein kinase C in the transcriptional control of cyclin D1 and related genes. J Biol Chem 278: 34709-34716, 2003.
23. Chen XP, Qian LL, Jiang H and Chen JH: Ginsenoside Rg3 inhibits CXCR4 expression and related migrations in a breast cancer cell line. Int J Clin Oncol 16: 519-523, 2011.
24. Chen J, Li Z, Chen AY, Ye X, Luo H, Rankin GO and Chen YC: Inhibitory effect of baicalin and baicalein on ovarian cancer cells. Int J Mol Sci 14: 6012-6025, 2013.
25. Li LQ, Li XL, Wang L, Du WJ, Guo R, Liang HH, Liu X, Liang DS, Lu YJ, Shan HL, et al: Matrine inhibits breast cancer growth via miR-21/PTEN/Akt pathway in MCF-7 cells. Cell Physiol Biochem 30: 631-641, 2012.
26. Saha SK and Khuda-Bukhsh AR: Molecular approaches towards development of purified natural products and their structurally known derivatives as efficient anti-cancer drugs: Current trends. Eur J Pharmacol 714: 239-248, 2013.
27. Schmalfeldt B, Prechtel D, Härting K, Späthe K, Rutke S, Konik E, Fridman R, Berger U, Schmitt M, Kuhn W, et al: Increased expression of matrix metalloproteinases (MMP)-2, MMP-9, and the urokinase-type plasminogen activator is associated with progression from benign to advanced ovarian cancer. Clin Cancer Res 7: 2396-2404, 2001.
28. Mehner C, Hockla A, Miller E, Ran S, Radisky DC and Radisky ES: Tumor cell-produced matrix metalloproteinase 9 (MMP-9) drives malignant progression and metastasis of basal-like triple negative breast cancer. Oncotarget 5: 2736-2749, 2014.
29. Kim HS, Kim MH, Jeong M, Hwang YS, Lim SH, Shin BA, Ahn BW and Jung YD: EGCG blocks tumor promoter-induced MMP-9 expression via suppression of MAPK and AP-1 activation in human gastric AGS cells. Anticancer Res 24: 747-753, 2004.
30. Yeh JH, Lecine P, Nunes JA, Spicuglia S, Ferrier P, Olive D and Imbert J: Novel CD28-responsive enhancer activated by CREB/ATF and AP-1 families in the human interleukin-2 receptor alpha-chain locus. Mol Cell Biol 21: 4515-4527, 2001.
31. Jendrysik MA, Vasilevsky S, Yi L, Wood A, Zhu N, Zhao Y, Koontz SM and Jackson SH: NADPH oxidase-2 derived ROS dictates murine DC cytokine-mediated cell fate decisions during CD4 T helper-cell commitment. PLoS One 6: e28198, 2011.
32. Kuo FC, Tseng YT, Wu SR, Wu MT and Lo YC: Melamine activates NF-κB/COX-2/PGE2 pathway and increases NADPH oxidase-dependent ROS production in macrophages and human embryonic kidney cells. Toxicol In Vitro 27: 1603-1611, 2013.
33. Jiang Q, Zhou C, Healey S, Chu W, Kouttab N, Bi Z and Wan Y: UV radiation down-regulates Dsg-2 via Rac/NADPH oxidase-mediated generation of ROS in human lens epithelial cells. Int J Mol Med 18: 381-387, 2006.
34. Remijsen QF, Fontayne A, Verdonck F, Clynen E, Schoofs L and Willems J: The antimicrobial peptide parabutoporin competes with p47(phox) as a PKC-substrate and inhibits NADPH oxidase in human neutrophils. FEBS Lett 580: 6206-6210, 2006.
35. Anstrom DM, Zhou X, Kalk CN, Song B and Lan Q: Mosquitocidal properties of natural product compounds isolated from Chinese herbs and synthetic analogs of curcumin. J Med Entomol 49: 350-355, 2012.
36. Yilmaz Savcun G, Ozkan E, Dulundu E, Topaloʇlu U, Sehirli AO, Tok OE, Ercan F and Sener G: Antioxidant and anti-inflammatory effects of curcumin against hepatorenal oxidative injury in an experimental sepsis model in rats. Ulus Travma Acil Cerrahi Derg 19: 507-515, 2013.
37. Meng B, Li J and Cao H: Antioxidant and antiinflammatory activities of curcumin on diabetes mellitus and its complications. Curr Pharm Des 19: 2101-2113, 2013.
38. Mo N, Li ZQ, Li J and Cao YD: Curcumin inhibits TGF-β1-induced MMP-9 and invasion through ERK and Smad signaling in breast cancer MDA-MB-231 cells. Asian Pac J Cancer Prev 13: 5709-5714, 2012.
39. Pan Y, Zhang X, Wang Y, Cai L, Ren L, Tang L, Wang J, Zhao Y, Wang Y, Liu Q, et al: Targeting JNK by a new curcumin analog to inhibit NF-κB-mediated expression of cell adhesion molecules attenuates renal macrophage infiltration and injury in diabetic mice. PLoS One 8: e79084, 2013.
40. Bimonte S, Barbieri A, Palma G, Luciano A, Rea D and Arra C: Curcumin inhibits tumor growth and angiogenesis in an orthotopic mouse model of human pancreatic cancer. Biomed Res Int 2013: 810423, 2013.
41. Vishvakarma NK, Kumar A and Singh SM: Role of curcumin-dependent modulation of tumor microenvironment of a murine T cell lymphoma in altered regulation of tumor cell survival. Toxicol Appl Pharmacol 252: 298-306, 2011.