Inhibition of invasion and migration by newly synthesized quinazolinone MJ-29 in human oral cancer CAL 27 cells through suppression of MMP-2/9 expression and combined down-regulation of MAPK and AKT signaling

Anticancer Research

Volumn 32, Issue 7, 2012, Pages 2895-2903

  Lu, Chi Cheng ^a   Yang, Jai Sing ^b   Chiang, Jo Hua ^a   Hour, Mann Jen ^b   Amagaya, Sakae ^b,c   Lu, Kung Wen ^b   Lin, Jing Pin ^b   Tang, Nou Ying ^b   Lee, Tsung Han ^a,b   Chung, Jing Gung ^b,d  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c NIHON PHARMACEUTICAL UNIVERSITY   (Japan)

^d ASIA UNIVERSITY   (Taiwan)

Author keywords

CAL 27 human oral squamous cell carcinoma cells; Invasion; MAPK signaling; Migration; MJ 29; MMP 2 9

Indexed keywords

6 PYRROLIDINYL 2 (2 HYDROXYPHENYL) 4 QUINAZOLINONE; ANTINEOPLASTIC AGENT; GELATINASE A; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; MJ 29; PROTEIN KINASE B; QUINAZOLINONE DERIVATIVE; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CANCER INHIBITION; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; METASTASIS INHIBITION; MOUTH CANCER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ZYMOGRAPHY;

CARCINOMA, SQUAMOUS CELL; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; HEAD AND NECK NEOPLASMS; HUMANS; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MITOGEN-ACTIVATED PROTEIN KINASES; MOUTH NEOPLASMS; NEOPLASM INVASIVENESS; PROTO-ONCOGENE PROTEINS C-AKT; PYRROLIDINES; QUINAZOLINONES;

EID: 84865677062     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Chen YJ, Lin SC, Kao T, Chang CS, Hong PS, Shieh TM and Chang KW: Genome-wide profiling of oral squamous cell carcinoma. J Pathol 204: 326-332, 2004. (Pubitemid 39430093)
2. Pentenero M, Gandolfo S and Carrozzo M: Importance of tumor thickness and depth of invasion in nodal involvement and prognosis of oral squamous cell carcinoma: a review of the literature. Head Neck 27: 1080-1091, 2005. (Pubitemid 41705587)
3. Sommer G, Rossa C, Chi AC, Neville BW and Heise T: Implication of RNA-binding protein La in proliferation, migration and invasion of lymph node-metastasized hypopharyngeal SCC cells. PLoS One 6: e25402, 2011.
4. Liu SY, Lu CL, Chiou CT, Yen CY, Liaw GA, Chen YC, Liu YC and Chiang WF: Surgical outcomes and prognostic factors of oral cancer associated with betel quid chewing and tobacco smoking in Taiwan. Oral Oncol 46: 276-282, 2010.
5. Sanjiv K, Su TL, Suman S, Kakadiya R, Lai TC, Wang HY, Hsiao M and Lee TC: The novel DNA alkylating agent BO-1090 suppresses the growth of human oral cavity cancer in xenografted and orthotopic mouse models. Int J Cancer 130: 1440-1450, 2012.
6. Yu FS, Yang JS, Yu CS, Lu CC, Chiang JH, Lin CW and Chung JG: Safrole induces apoptosis in human oral cancer HSC-3 cells. J Dent Res 90: 168-174, 2011.
7. Choi Y, Kim SY, Kim SH, Yang J, Park K and Byun Y: Inhibition of tumor growth by biodegradable microspheres containing all-trans-retinoic acid in a human head-and-neck cancer xenograft. Int J Cancer 107: 145-148, 2003. (Pubitemid 37100099)
8. Lo WL, Kao SY, Chi LY, Wong YK and Chang RC: Outcomes of oral squamous cell carcinoma in Taiwan after surgical therapy: factors affecting survival. J Oral Maxillofac Surg 61: 751-758, 2003.
9. Muir C and Weiland L: Upper aerodigestive tract cancers. Cancer 75: 147-153, 1995.
10. Funk GF, Karnell LH, Robinson RA, Zhen WK, Trask DK and Hoffman HT: Presentation, treatment, and outcome of oral cavity cancer: a National Cancer Data Base report. Head Neck 24: 165-180, 2002. (Pubitemid 34111514)
11. Sano D and Myers JN: Metastasis of squamous cell carcinoma of the oral tongue. Cancer Metastasis Rev 26: 645-662, 2007. (Pubitemid 350115112)
12. Jiang L, Liu X, Kolokythas A, Yu J, Wang A, Heidbreder CE, Shi F and Zhou X: Downregulation of the Rho GTPase signaling pathway is involved in the microRNA-138-mediated inhibition of cell migration and invasion in tongue squamous cell carcinoma. Int J Cancer 127: 505-512, 2010.
13. Lu Z, Lu N, Li C, Li F, Zhao K, Lin B and Guo Q: Oroxylin A inhibits matrix metalloproteinase-2/9 expression and activation by up-regulating tissue inhibitor of metalloproteinase-2 and suppressing the ERK1/2 signaling pathway. Toxicol Lett 209: 211-220, 2012.
14. Babykutty S, P SP, R JN, Kumar MA, Nair MS, Srinivas P and Gopala S: Nimbolide retards tumor cell migration, invasion, and angiogenesis by downregulating MMP-2/9 expression via inhibiting ERK1/2 and reducing DNA-binding activity of NF-kappaB in colon cancer cells. Mol Carcinog, 2011.
15. Ni L, Feng Y, Wan H, Ma Q, Fan L, Qian Y, Li Q, Xiang Y and Gao B: Angiotensin-(1-7) inhibits the migration and invasion of A549 human lung adenocarcinoma cells through inactivation of the PI3K/Akt and MAPK signaling pathways. Oncol Rep 27: 783-790, 2012.
16. Hidalgo M and Eckhardt SG: Development of matrix metalloproteinase inhibitors in cancer therapy. J Natl Cancer Inst 93: 178-193, 2001. (Pubitemid 32166488)
17. Kim SA, Kwon SM, Kim JA, Kang KW, Yoon JH and Ahn SG: 5′-Nitro-indirubinoxime, an indirubin derivative, suppresses metastatic ability of human head and neck cancer cells through the inhibition of Integrin beta1/FAK/Akt signaling. Cancer Lett 306: 197-204, 2011.
18. Liang X, Yang X, Tang Y, Zhou H, Liu X, Xiao L, Gao J and Mao Z: RNAi-mediated down-regulation of urokinase plasminogen activator receptor inhibits proliferation, adhesion, migration and invasion in oral cancer cells. Oral Oncol 44: 1172-1180, 2008.
19. Hour MJ, Yang JS, Lien JC, Kuo SC and Huang LJ: Synthesis and cytotoxicity of 6-pyrrolidinyl-2-(2-substituted phenyl)-4-quinazolinones. J Chin Chem Soc 54: 785-790, 2007.
20. Yang JS, Hour MJ, Huang WW, Lin KL, Kuo SC and Chung JG: MJ-29 inhibits tubulin polymerization, induces mitotic arrest, and triggers apoptosis via cyclin-dependent kinase 1-mediated Bcl-2 phosphorylation in human leukemia U937 cells. J Pharmacol Exp Ther 334: 477-488, 2010.
21. Hour MJ, Huang LJ, Kuo SC, Xia Y, Bastow K, Nakanishi Y, Hamel E and Lee KH: 6-Alkylamino- and 2,3-dihydro-3′-methoxy-2-phenyl-4-quinazolinones and related compounds: their synthesis, cytotoxicity, and inhibition of tubulin polymerization. J Med Chem 43: 4479-4487, 2000. (Pubitemid 32046872)
22. Yang JS, Hour MJ, Kuo SC, Huang LJ and Lee MR: Selective induction of G2/M arrest and apoptosis in HL-60 by a potent anticancer agent, HMJ-38. Anticancer Res 24: 1769-1778, 2004.
23. Jiang L, Ji N, Zhou Y, Li J, Liu X, Wang Z, Chen Q and Zeng X: CAL 27 is an oral adenosquamous carcinoma cell line. Oral Oncol 45: e204-207, 2009.
24. Fan MJ, Lin YC, Shih HD, Yang JS, Liu KC, Yang ST, Lin CY, Wu RS, Yu CS, Ko YC and Chung JG: Crude extracts of Agaricus brasiliensis induce apoptosis in human oral cancer CAL 27 cells through a mitochondria-dependent pathway. In Vivo 25: 355-366, 2011.
25. Chien MH, Ying TH, Hsieh YS, Chang YC, Yeh CM, Ko JL, Lee WS, Chang JH and Yang SF: Dioscorea nipponica Makino inhibits migration and invasion of human oral cancer HSC-3 cells by transcriptional inhibition of matrix metalloproteinase-2 through modulation of CREB and AP-1 activity. Food Chem Toxicol 50: 558-566, 2012.
26. Wang TP, Shu CH, Fang SC and Huang RF: Folate deprivation enhanced invasiveness of human colon cancer cells mediated by activation of sonic hedgehog signaling through promoter hypomethylation and cross-action with transcription nuclear factor-kappa B pathway. Carcinogenesis, 2012.
27. Wang JH, Manning BJ, Wu QD, Blankson S, Bouchier-Hayes D and Redmond HP: Endotoxin/lipopolysaccharide activates NF-kappa B and enhances tumor cell adhesion and invasion through a beta 1 integrin-dependent mechanism. J Immunol 170: 795-804, 2003. (Pubitemid 36070531)
28. Wu PP, Liu KC, Huang WW, Ma CY, Lin H, Yang JS and Chung JG: Triptolide induces apoptosis in human adrenal cancer NCI-H295 cells through a mitochondrial-dependent pathway. Oncol Rep 25: 551-557, 2011.
29. Chen YY, Chiang SY, Lin JG, Ma YS, Liao CL, Weng SW, Lai TY and Chung JG: Emodin, aloe-emodin and rhein inhibit migration and invasion in human tongue cancer SCC-4 cells through the inhibition of gene expression of matrix metalloproteinase-9. Int J Oncol 36: 1113-1120, 2010.
30. Lai KC, Huang AC, Hsu SC, Kuo CL, Yang JS, Wu SH and Chung JG: Benzyl isothiocyanate (BITC) inhibits migration and invasion of human colon cancer HT29 cells by inhibiting matrix metalloproteinase-2/-9 and urokinase plasminogen (uPA) through PKC and MAPK signaling pathway. J Agric Food Chem 58: 2935-2942, 2010.
31. Lin HJ, Su CC, Lu HF, Yang JS, Hsu SC, Ip SW, Wu JJ, Li YC, Ho CC, Wu CC and Chung JG: Curcumin blocks migration and invasion of mouse-rat hybrid retina ganglion cells (N18) through the inhibition of MMP-2, -9, FAK, Rho A and Rock-1 gene expression. Oncol Rep 23: 665-670, 2010.
32. Pitchakarn P, Suzuki S, Ogawa K, Pompimon W, Takahashi S, Asamoto M, Limtrakul P and Shirai T: Kuguacin J, a triterpeniod from Momordica charantia leaf, modulates the progression of androgen-independent human prostate cancer cell line, PC3. Food Chem Toxicol 50: 840-847, 2012.
33. Troeberg L and Nagase H: Zymography of metalloproteinases. Curr Protoc Protein Sci Chapter 21: Unit 21 15, 2004.
34. Lu CC, Yang JS, Huang AC, Hsia TC, Chou ST, Kuo CL, Lu HF, Lee TH, Wood WG and Chung JG: Chrysophanol induces necrosis through the production of ROS and alteration of ATP levels in J5 human liver cancer cells. Mol Nutr Food Res 54: 967-976, 2010.
35. Chiang JH, Yang JS, Ma CY, Yang MD, Huang HY, Hsia TC, Kuo HM, Wu PP, Lee TH and Chung JG: Danthron, an anthraquinone derivative, induces DNA damage and caspase cascades-mediated apoptosis in SNU-1 human gastric cancer cells through mitochondrial permeability transition pores and Bax-triggered pathways. Chem Res Toxicol 24: 20-29, 2011.
36. Lu CC, Yang JS, Chiang JH, Hour MJ, Lin KL, Lin JJ, Huang WW, Tsuzuki M, Lee TH and Chung JG: Novel quinazolinone MJ-29 triggers endoplasmic reticulum stress and intrinsic apoptosis in murine leukemia WEHI-3 cells and inhibits leukemic mice. PLoS One, 2012.
37. Yang HL, Kuo YH, Tsai CT, Huang YT, Chen SC, Chang HW, Lin E, Lin WH and Hseu YC: Anti-metastatic activities of Antrodia camphorata against human breast cancer cells mediated through suppression of the MAPK signaling pathway. Food Chem Toxicol 49: 290-298, 2011.
38. Deng YT and Lin JK: EGCG inhibits the invasion of highly invasive CL1-5 lung cancer cells through suppressing MMP-2 expression via JNK signaling and induces G2/M arrest. J Agric Food Chem 59: 13318-13327, 2011.
39. Tseng MY, Liu SY, Chen HR, Wu YJ, Chiu CC, Chan PT, Chiang WF, Liu YC, Lu CY, Jou YS and Chen JY: Serine protease inhibitor (SERPIN) B1 promotes oral cancer cell motility and is over-expressed in invasive oral squamous cell carcinoma. Oral Oncol 45: 771-776, 2009.
40. Christiansen JJ and Rajasekaran AK: Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 66: 8319-8326, 2006. (Pubitemid 44449137)
41. Rosenthal EL and Matrisian LM: Matrix metalloproteases in head and neck cancer. Head Neck 28: 639-648, 2006. (Pubitemid 44025114)
42. Liabakk NB, Talbot I, Smith RA, Wilkinson K and Balkwill F: Matrix metalloprotease 2 (MMP-2) and matrix metalloprotease 9 (MMP-9) type IV collagenases in colorectal cancer. Cancer Res 56: 190-196, 1996. (Pubitemid 26010399)
43. Kumar S, Bryant CS, Chamala S, Qazi A, Seward S, Pal J, Steffes CP, Weaver DW, Morris R, Malone JM, Shammas MA, Prasad M and Batchu RB: Ritonavir blocks AKT signaling, activates apoptosis and inhibits migration and invasion in ovarian cancer cells. Mol Cancer 8: 26, 2009.
44. Wagner EF and Nebreda AR: Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9: 537-549, 2009.
45. Zucker S and Cao J: Measurement of matrix metalloproteinases in serum of patients with melanoma: snarled in technical pitfalls. Clin Cancer Res 11: 5069-5070, 2005. (Pubitemid 41003688)
46. Zhou HY and Wong AS: Activation of p70S6K induces expression of matrix metalloproteinase 9 associated with hepatocyte growth factor-mediated invasion in human ovarian cancer cells. Endocrinology 147: 2557-2566, 2006.
47. Lee EJ, Kim DI, Kim WJ and Moon SK: Naringin inhibits matrix metalloproteinase-9 expression and AKT phosphorylation in tumor necrosis factor-alpha-induced vascular smooth muscle cells. Mol Nutr Food Res 53: 1582-1591, 2009.
48. Wang SW, Pan SL, Peng CY, Huang DY, Tsai AC, Chang YL, Guh JH, Kuo SC, Lee KH and Teng CM: CHM-1 inhibits hepatocyte growth factor-induced invasion of SK-Hep-1 human hepatocellular carcinoma cells by suppressing matrix metalloproteinase-9 expression. Cancer Lett 257: 87-96, 2007.