Mammalian target of rapamycin pathway promotes tumor-induced angiogenesis in adenoid cystic carcinoma: Its suppression by isoliquiritigenin through dual activation of c-Jun NH2-terminal kinase and inhibition of extracellular signal-regulated kinase

Journal of Pharmacology and Experimental Therapeutics

Volumn 334, Issue 2, 2010, Pages 500-512

  Sun, Zhi Jun ^a   Chen, Gang ^a   Zhang, Wei ^a   Hu, Xiang ^a   Huang, Cong Fa ^a   Wang, Yu Fan ^a   Jia, Jun ^a   Zhao, Yi Fang ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ISOLIQUIRITIGENIN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; VASCULOTROPIN;

ADENOID CYSTIC CARCINOMA; ANGIOGENESIS; ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CLINICAL ARTICLE; CLUSTER ANALYSIS; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO SELECTION; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR ANGIOGENESIS; TUMOR XENOGRAFT; XENOGRAFT;

ANGIOGENESIS INHIBITORS; ANIMALS; CARCINOMA, ADENOID CYSTIC; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CHALCONES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN-SERINE-THREONINE KINASES; SALIVARY GLAND NEOPLASMS; TRANSPLANTATION, HETEROLOGOUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77954942475     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.110.167692     Document Type: Article

References (40)

1. Ali MA, Choy H, Habib AA, and Saha D (2007) SNS-032 prevents tumor cell-induced angiogenesis by inhibiting vascular endothelial growth factor. Neoplasia 9:370-381.
2. Benvenuto G, Li S, Brown SJ, Braverman R, Vass WC, Cheadle JP, Halley DJ, Sampson JR, Wienecke R, and DeClue JE (2000) The tuberous sclerosis-1 (TSC1) gene product hamartin suppresses cell growth and augments the expression of the TSC2 product tuberin by inhibiting its ubiquitination. Oncogene 19:6306-6316.
3. Buller CL, Loberg RD, Fan MH, Zhu Q, Park JL, Vesely E, Inoki K, Guan KL, and Brosius FC 3rd (2008) A GSK-3/TSC2/mTOR pathway regulates glucose uptake and GLUT1 glucose transporter expression. Am J Physiol Cell Physiol 295:C836-C843.
4. Bussolino F, Mantovani A, and Persico G (1997) Molecular mechanisms of blood vessel formation. Trends Biochem Sci 22:251-256. (Pubitemid 27310945)
5. Chang HL, Wu YC, Su JH, Yeh YT, and Yuan SS (2008) Protoapigenone, a novel flavonoid, induces apoptosis in human prostate cancer cells through activation of p38 mitogen-activated protein kinase and c-Jun NH2-terminal kinase 1/2. J Pharmacol Exp Ther 325:841-849.
6. Chen G, Zhu L, Liu Y, Zhou Q, Chen H, and Yang J (2009) Isoliquiritigenin, a flavonoid from licorice, plays a dual role in regulating gastrointestinal motility in vitro and in vivo. Phytother Res 23:498-506.
7. De Smet F, Carmeliet P, and Autiero M (2006) Fishing and frogging for antiangiogenic drugs. Nat Chem Biol 2:228-229.
8. Dhanabal M, Jeffers M, and Larochelle WJ (2005) Anti-angiogenic therapy as a cancer treatment paradigm. Curr Med Chem Anticancer Agents 5:115-130.
9. Eisen MB, Spellman PT, Brown PO, and Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863-14868.
10. Folkman J (1990) What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 82:4-6.
11. Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1:27-31.
12. Guan XF, Qiu WL, He RG, and Zhou XJ (1997) Selection of adenoid cystic carcinoma cell clone highly metastatic to the lung: an experimental study. Int J Oral Maxillofac Surg 26:116-119.
13. Hanahan D and Folkman J (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86:353-364.
14. Hsu YL, Kuo PL, Lin LT, and Lin CC (2005) Isoliquiritigenin inhibits cell proliferation and induces apoptosis in human hepatoma cells. Planta Med 71:130-134.
15. Inoki K, Corradetti MN, and Guan KL (2005) Dysregulation of the TSC-mTOR pathway in human disease. Nat Genet 37:19-24. (Pubitemid 40070934)
16. Jośko J and Mazurek M (2004) Transcription factors having impact on vascular endothelial growth factor (VEGF) gene expression in angiogenesis. Med Sci Monit 10:RA89-RA98.
17. Jung JI, Lim SS, Choi HJ, Cho HJ, Shin HK, Kim EJ, Chung WY, Park KK, and Park JH (2006) Isoliquiritigenin induces apoptosis by depolarizing mitochondrial membranes in prostate cancer cells. J Nutr Biochem 17:689-696.
18. Kang SW, Choi JS, Choi YJ, Bae JY, Li J, Kim DS, Kim JL, Shin SY, Lee YJ, Kwun IS, et al. (2010) Licorice isoliquiritigenin dampens angiogenic activity via inhibition of MAPK-responsive signaling pathways leading to induction of matrix metalloproteinases. J Nutr Biochem 21:55-65.
19. Kim YM, Kim YM, Lee YM, Kim HS, Kim JD, Choi Y, Kim KW, Lee SY, and Kwon YG (2002) TNF-related activation-induced cytokine (TRANCE) induces angiogenesis through the activation of Src and phospholipase C (PLC) in human endothelial cells. J Biol Chem 277:6799-6805.
20. Klos KS, Wyszomierski SL, Sun M, Tan M, Zhou X, Li P, Yang W, Yin G, Hittelman WN, and Yu D (2006) ErbB2 increases vascular endothelial growth factor protein synthesis via activation of mammalian target of rapamycin/p70S6K leading to increased angiogenesis and spontaneous metastasis of human breast cancer cells. Cancer Res 66:2028-2037.
21. Korkolopoulou P, Levidou G, Saetta AA, El-Habr E, Eftichiadis C, Demenagas P, Thymara I, Xiromeritis K, Boviatsis E, Thomas-Tsagli E, et al. (2008) Expression of nuclear factor-κB in human astrocytomas: relation to pIκBa, vascular endothelial growth factor, Cox-2, microvascular characteristics, and survival. Hum Pathol 39:1143-1152.
22. Kwiatkowski DJ, Zhang H, Bandura JL, Heiberger KM, Glogauer M, el-Hashemite N, and Onda H (2002) A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells. Hum Mol Genet 11:525-534.
23. Kwon HM, Choi YJ, Choi JS, Kang SW, Bae JY, Kang IJ, Jun JG, Lee SS, Lim SS, and Kang YH (2007) Blockade of cytokine-induced endothelial cell adhesion molecule expression by licorice isoliquiritigenin through NF-κB signal disruption. Exp Biol Med (Maywood) 232:235-245.
24. Lee DF, Kuo HP, Chen CT, Hsu JM, Chou CK, Wei Y, Sun HL, Li LY, Ping B, Huang WC, et al. (2007) IKKβ suppression of TSC1 links inflammation and tumor angiogenesis via the mTOR pathway. Cell 130:440-455.
25. Lin HL, Chiou SH, Wu CW, Lin WB, Chen LH, Yang YP, Tsai ML, Uen YH, Liou JP, and Chi CW (2007) Combretastatin A4-induced differential cytotoxicity and reduced metastatic ability by inhibition of AKT function in human gastric cancer cells. J Pharmacol Exp Ther 323:365-373.
26. Ma L, Chen Z, Erdjument-Bromage H, Tempst P, and Pandolfi PP (2005) Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 121:179-193.
27. Ma L, Teruya-Feldstein J, Bonner P, Bernardi R, Franz DN, Witte D, Cordon-Cardo C, and Pandolfi PP (2007) Identification of S664 TSC2 phosphorylation as a marker for extracellular signal-regulated kinase-mediated mTOR activation in tuberous sclerosis and human cancer. Cancer Res 67:7106-7112.
28. Onda H, Lueck A, Marks PW, Warren HB, and Kwiatkowski DJ (1999) Tsc2(+/-) mice develop tumors in multiple sites that express gelsolin and are influenced by genetic background. J Clin Invest 104:687-695. (Pubitemid 29536354)
29. Passam FH, Sfiridaki A, Pappa C, Kyriakou D, Petreli E, Roussou PA, and Alexandrakis MG (2008) Angiogenesis-related growth factors and cytokines in the serum of patients with B non-Hodgkin lymphoma; relation to clinical features and response to treatment. Int J Lab Hematol 30:17-25.
30. Passaniti A (1992) Extracellular matrix-cell interactions: Matrigel and complex cellular pattern formation. Lab Invest 67:804.
31. Saldanha AJ (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20:3246-3248.
32. Slomiany MG and Rosenzweig SA (2006) Hypoxia-inducible factor-1-dependent and -independent regulation of insulin-like growth factor-1-stimulated vascular endothelial growth factor secretion. J Pharmacol Exp Ther 318:666-675.
33. Spiro RH (1997) Distant metastasis in adenoid cystic carcinoma of salivary origin. Am J Surg 174:495-498.
34. Sun ZJ, Chen G, Hu X, Zhang W, Liu Y, Zhu LX, Zhou Q, and Zhao YF (2010) Activation of PI3K/Akt/IKK-α/NF-κB signaling pathway is required for the apoptosis-evasion in human salivary adenoid cystic carcinoma: its inhibition by quercetin. Apoptosis doi: 10.1007/s10495-010-0497-5.
35. Weidner N, Semple JP, Welch WR, and Folkman J (1991) Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. N Engl J Med 324:1-8.
36. Yamazaki S, Morita T, Endo H, Hamamoto T, Baba M, Joichi Y, Kaneko S, Okada Y, Okuyama T, Nishino H, et al. (2002) Isoliquiritigenin suppresses pulmonary metastasis of mouse renal cell carcinoma. Cancer Lett 183:23-30.
37. Ye L, Gho WM, Chan FL, Chen S, and Leung LK (2009) Dietary administration of the licorice flavonoid isoliquiritigenin deters the growth of MCF-7 cells overexpressing aromatase. Int J Cancer 124:1028-1036.
38. Yoshida T, Horinaka M, Takara M, Tsuchihashi M, Mukai N, Wakada M, and Sakai T (2008) Combination of isoliquiritigenin and tumor necrosis factor-related apoptosis-inducing ligand induces apoptosis in colon cancer HT29 cells. Environ Health Prev Med 13:281-287.
39. Zhang J and Peng B (2009) NF-κB promotes iNOS and VEGF expression in salivary gland adenoid cystic carcinoma cells and enhances endothelial cell motility in vitro. Cell Prolif 42:150-161.
40. Zhang J, Peng B, and Chen X (2005) Expressions of nuclear factor κB, inducible nitric oxide synthase, and vascular endothelial growth factor in adenoid cystic carcinoma of salivary glands: correlations with the angiogenesis and clinical outcome. Clin Cancer Res 11:7334-7343.