Protocatechuic acid inhibits cancer cell metastasis involving the down-regulation of Ras/Akt/NF-κB pathway and MMP-2 production by targeting RhoB activation

British Journal of Pharmacology

Volumn 162, Issue 1, 2011, Pages 237-254

  Lin, Hui Hsuan ^a,b   Chen, Jing Hsien ^c   Chou, Fen Pi ^a   Wang, Chau Jong ^a,b  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHUNG HWA UNIVERSITY OF MEDICAL TECHNOLOGY   (Taiwan)

Author keywords

invasion; metastasis; MMP 2; PCA; Ras Akt NF B; RhoB PKC

Indexed keywords

GELATINASE A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE B; PROTEIN KINASE C EPSILON; PROTOCATECHUIC ACID; RAS PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; TISSUE INHIBITOR OF METALLOPROTEINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CANCER INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER METASTASIS; MELANOMA B16; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; WOUND HEALING;

ANIMALS; ANTICARCINOGENIC AGENTS; BLOTTING, WESTERN; DOWN-REGULATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HYDROXYBENZOIC ACIDS; IMMUNOPRECIPITATION; MATRIX METALLOPROTEINASE 2; MELANOMA, EXPERIMENTAL; MICE; NEOPLASM METASTASIS; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-AKT; RAS PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHOB GTP-BINDING PROTEIN;

EID: 78650095235     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.01022.x     Document Type: Article

References (48)

1. Alakus H, Grass G, Hennecken JK, Bollschweiler E, Schulte C, Drebber U, et al. (2008). Clinicopathological significance of MMP-2 and its specific inhibitor TIMP-2 in gastric cancer. Histol Histopathol 23: 917-923.
2. Barbacid M, (1987). Ras genes. Annu Rev Biochem 56: 779-827.
3. Bergman MR, Cheng S, Honbo N, Piacentini L, Karliner JS, Lovett DH, (2003). A functional activating protein 1 (AP-1) site regulates matrix metalloproteinase 2 (MMP-2) transcription by cardiac cells through interactions with JunB-Fra1 and JunB-FosB heterodimers. Biochem J 369: 485-496.
4. Chan FL, Choi HL, Chen ZY, Chan PS, Huang Y, (2000). Induction of apoptosis in prostate cancer cell lines by a flavonoid, baicalin. Cancer Lett 160: 219-228.
5. Chen YX, Li BZ, Diao F, Cao DM, Fu CC, Lu J, (2006). Up-regulation of RhoB by glucocorticoids and its effects on the cell proliferation and NF-κB transcriptional activity. J Steroid Biochem Mol Biol 101: 179-187.
6. Chen JH, Lin HH, Chiang TA, Ho HH, Lee YC, Wang CJ, (2008). Gaseous nitrogen oxide promotes human lung cancer cell line A549 migration, invasion, and metastasis via iNOS-mediated MMP-2 Production. Toxicol Sci 106: 364-375.
7. Chiu LC, Wan JM, (1999). Induction of apoptosis in HL-60 cells by eicosapentaenoic acid (EPA) is associated with downregulation of bcl-2 expression. Cancer Lett 145: 17-27.
8. Chu SC, Chiou HL, Chen PN, Yang SF, Hsieh YS, (2004). Silibinin inhibits the invasion of human lung cancer cells via decreased productions of urokinase-plasminogen activator and matrix metalloproteinase-2. Mol Carcinog 40: 143-149.
9. Delarue FL, Adnane J, Joshi B, Blaskovich MA, Wang DA, Hawker J, et al. (2007). Farnesyltransferase and geranylgeranyltransferase I inhibitors upregulate RhoB expression by HDAC1 dissociation, HAT association and histone acetylation of the RhoB promoter. Oncogene 26: 633-640.
10. Du J, Jiang B, Coffey RJ, Barnard J, (2004). Raf and RhoA cooperate to transform intestinal epithelial cells and induce growth resistance to transforming growth factor beta. Mol Cancer Res 2: 233-241.
11. Fidler IJ, (2005). The organ microenvironment and cancer metastasis. Differentiation 70: 498-505.
12. Fritz G, Kaina B, Aktories K, (1995). The ras-related small GTP-binding protein RhoB is immediate-early inducible by DNA damaging treatments. J Biol Chem 270: 25172-25177.
13. Gong M, Meng L, Jiang B, Zhang J, Yang H, Wu J, et al. (2008). p37 from Mycoplasma hyorhinis promotes cancer cell invasiveness and metastasis through activation of MMP-2 and followed by phosphorylation of EGFR. Mol Cancer Ther 7: 530-537.
14. Hudson EA, Dinh PA, Kokubun T, Simmonds MS, Gescher A, (2000). Characterization of potentially chemopreventive phenols in extracts of brown rice that inhibit the growth of human breast and colon cancer cells. Cancer Epidemiol Biomarkers Prev 9: 1163-1170.
15. Hwang ES, Lee HJ, (2008). Benzyl isothiocyanate inhibits metalloproteinase-2/-9 expression by suppressing the mitogen-activated protein kinase in SK-Hep1 human hepatoma cells. Food Chem Toxicol 46: 2358-2364.
16. Jiang K, Sun J, Cheng J, Djeu JY, Wei S, Sebti S, (2004). Akt mediates Ras downregulation of RhoB, a suppressor of transformation, invasion, and metastasis. Mol Cell Biol 24: 5565-5576.
17. Kampa M, Alexaki VI, Notas G, Nifli AP, Nistikaki A, Hatzoglou A, et al. (2004). Antiproliferative and apoptotic effects of selective phenolic acids on T47D human breast cancer cells: potential mechanisms of action. Breast Cancer Res 6: R63-R74.
18. Karlsson R, Pedersen ED, Wang Z, Brakebusch C, (2009). Rho GTPase function in tumorigenesis. Biochim Biophys Acta 1796: 91-98.
19. Kawamori T, Tanaka T, Kojima T, Suzui M, Ohnishi M, Mori H, (1994). Suppression of azoxymethane-induced rat colon aberrant crypt foci by dietary protocatechuic acid. Jpn J Cancer Res 85: 686-691.
20. Kim CH, Won M, Choi CH, Ahn J, Kim BK, Song KB, et al. (2010). Increase of RhoB in gamma-radiation-induced apoptosis is regulated by c-Jun N-terminal kinase in Jurkat T cells. Biochem Biophys Res Commun 391: 1182-1186.
21. Lee IR, Yang MY, (1994). Phenolic compounds from Duchesnea chrysantha and their cytotoxic activities in human cancer cell. Arch Pharm Res 17: 476-479.
22. Li P, Wang XQ, Wang HZ, Wu YN, (1993). High performance liquid chromatographic determination of phenolic acids in fruits and vegetables. Biomed Environ Sci 6: 389-398.
23. Lin HH, Chen JH, Huang CC, Wang CJ, (2007). Apoptotic effect of 3,4-dihydroxybenzoic acid on human gastric carcinoma cells involving JNK/p38 MAPK signaling activation. Int J Cancer 120: 2306-2316.
24. Liu H, Qiu Y, Xiao L, Dong F, (2006). Involvement of protein kinase Cepsilon in the negative regulation of Akt activation stimulated by granulocyte colony-stimulating factor. J Immunol 176: 2407-2413.
25. Liu GT, Zhang TM, Wang BE, Wang YW, (1992). Protective action of seven natural phenolic compounds against peroxidative damage to biomembranes. Biochem Pharmacol 43: 147-152.
26. Masella R, Cantafora A, Modesti D, Cardilli A, Gennaro L, Bocca A, et al. (1999). Antioxidant activity of 3,4-DHPEA-EA and protocatechuic acid: a comparative assessment with other olive oil biophenols. Redox Rep 4: 113-121.
27. Matsumoto M, Ogawa W, Hino Y, Furukawa K, Ono Y, Takahashi M, et al. (2001). Inhibition of insulin-induced activation of Akt by a kinase-deficient mutant of the isozyme of protein kinase C. J Biol Chem 276: 14400-14406.
28. Nakamura H, Nishikawa A, Furukawa F, Kasahara K, Miyauchi M, Son HY, et al. (2000). Inhibitory effects of protocatechuic acid on the post-initiation phase of hamster pancreatic carcinogenesis induced by N-nitrosobis(2-oxopropyl) amine. Anticancer Res 20: 3423-3427.
29. Parks WC, Shapiro SD, (2001). Matrix metalloproteinases in lung biology. Respir Res 2: 10-19.
30. Philip S, Kundu GC, (2003). Osteopontin induces nuclear factor kappa B mediated promatrix metalloproteinase-2 activation through I kappa B alpha/ IKK signaling pathways, and curcumin (diferulolylmethane) down-regulates these pathways. J Biol Chem 278: 14487-14497.
31. Rao JS, (2003). Molecular mechanisms of glioma invasiveness: the role of proteases. Nat Rev Cancer 3: 489-501.
32. Reischer D, Heyfets A, Shimony S, Nordenberg J, Kashman Y, Flescher E, (2007). Effects of natural and novel synthetic jasmonates in experimental metastatic melanoma. Br J Pharmacol 150: 738-749.
33. Ren XD, Kiosses WB, Schwartz MA, (1999). Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18: 578-585.
34. Siddiqui IA, Adhami VM, Afaq F, Ahmad N, Mukhtar H, (2004). Modulation of phosphatidylinositol-3-kinase/protein kinase B- and mitogen-activated protein kinase-pathways by tea polyphenols in human prostate cancer cells. J Cell Biochem 91: 232-242.
35. Stich HF, (1991). The beneficial and hazardous effects of simple phenolic compounds. Mutat Res 259: 307-324.
36. Tanaka T, Kojima T, Kawamori T, Yoshimi N, Mori H, (1993). Chemoprevention of diethylnitrosamine-induced hepatocarcinogenesis by a simple phenolic acid protocatechuic acid in rats. Cancer Res 53: 2775-2779.
37. Tanaka T, Kojima T, Kawamori T, Mori H, (1995). Chemoprevention of digestive organs carcinogenesis by natural product protocatechuic acid. Cancer 75: 1433-1439.
38. Tanno S, Tanno S, Mitsuuchi Y, Altomare DA, Xiao GH, Testa JR, (2001). AKT activation up-regulates insulin-like growth factor I receptor expression and promotes invasiveness of human pancreatic cancer cells. Cancer Res 61: 589-593.
39. Tseng TH, Wang CJ, Kao ES, Chu HY, (1996). Hibiscus protocatechuic acid protects against oxidative damage induced by tert-butylhydroperoxide in rat primary hepatocytes. Chem Biol Interact 101: 137-148.
40. Tseng TH, Kao TW, Chu CY, Chou FP, Lin WL, Wang CJ, (2000). Induction of apoptosis by hibiscus protocatechuic acid in human leukemia cells via reduction of retinoblastoma (RB) phosphorylation and Bcl-2 expression. Biochem Pharmacol 60: 07-15.
41. Ueda J, Saito N, Shimazu Y, Ozawa T, (1996). A comparison of scavenging abilities of antioxidants against hydroxyl radicals. Arch Biochem Biophys 333: 77-84.
42. Vivanco I, Sawyers CL, (2002). The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2: 489-501.
43. Weng MW, Lai JC, Hsu CP, Yu KY, Chen CY, Lin TS, et al. (2005). Alternative splicing of MDM2 mRNA in lung carcinomas and lung cell lines. Environ Mol Mutagen 46: 1-11.
44. Westermarck J, Kähäri VM, (1999). Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J 13: 781-792.
45. Woo MS, Jung SH, Kim SY, Hyun JW, Ko KH, Kim WK, et al. (2005). Curcumin suppresses phorbol ester-induced matrix metalloproteinase-9 expression by inhibiting the PKC to MAPK signaling pathways in human astroglioma cells. Biochem Biophys Res Commun 335: 1017-1025.
46. Yen GC, Hsieh CL, (2000). Reactive oxygen species scavenging activity of Du-zhong (Eucommia ulmoides Oliv.) and its active compounds. J Agric Food Chem 48: 3431-3436.
47. Yin MC, Lin CC, Wu HC, Tsao SM, Hsu CK, (2009). Apoptotic effects of protocatechuic acid in human breast, lung, liver, cervix, and prostate cancer cells: potential mechanisms of action. J Agric Food Chem 57: 6468-6473.
48. Zhen MC, Huang XH, Wang Q, Sun K, Liu YJ, Li W, et al. (2006). Green tea polyphenol epigallocatechin-3-gallate suppresses rat hepatic stellate cell invasion by inhibition of MMP-2 expression and its activation. Acta Pharmacol Sin 27: 1600-1607.