Role of Curcumin on Tumor Angiogenesis in Hepatocellular Carcinoma

Authors

  • Pornphrom Chintana

Keywords:

Curcumin, Angiogenesis, Hepatocellular carcinoma, VEGF, COX-2

Abstract

Hepatocellular carcinoma (HCC) is a malignant tumor characterized by active neovascularization. Vascular endothelial growth factor (VEGF) is the most important angiogenic factor that regulates the HCC development. Overexpression of VEGF enhances the HCC tumor growth associated with increase of angiogenesis in the tumor, whereas suppression of VEGF attenuates the tumor growth. Similarly, the cyclooxygenase-2 (COX-2) expression stepwisely increases during hepatocarcinogenesis. Curcurmin has been shown to inhibit several angiogenic biomarkers including, VEGF and COX-2 expression. Therefore, curcumin could be used as a candidate for the combined drug treatment for HCC in the future.

References

Aggarwal, B. B., Bhatt, I. D., Ichikawa, H., Ahn,

K. S., Sethi, G., Sandur, S. K., et al. (2007). Curcumin - biological and medicine properties. New York: CRC Press.

Aggarwal, S., Ichikawa, H., Takada, Y., Sandur,

S. K., Shishodia, S., & Aggarwal, B. B. (2006). Curcumin (diferuloylmethane) down-regulates expression of cell proliferation and antiapoptotic and metastatic gene products through suppression of IkappaBalpha kinase and Akt activation. Molecular Pharmacology, 69, 195-206.

Aggarwal, B. B., Kumar, A., & Bharti, A. C. (2003). Anticancer potential of curcumin: Preclinical and clinical studies. Anticancer Research, 23, 363-398.

Aggarwal, B. B., Shishodia, S., Takada, Y., Banerjee, S., Newman, R. A., Bueso-Ramos, C. E., et al. (2005). Curcumin suppresses the paclitaxel-induced nuclear factor-kappaB pathway in breast cancer cells and inhibits lung metastasis of human breast cancer in nude mice. Clinical Cancer Research, 11, 7490-7498.

An, F. Q., Matsuda, M., Fujii, H., & Matsumoto, Y. (2000). Expression of vascular endothelial growth factor in surgical specimens of hepatocellular carcinoma. Journal of Cancer Research and Clinical Oncology, 126, 153-160.

Anto, R. J., Maliekal, T. T., & Karunagaran, D. (2000). L-929 cells harboring ectopically expressed RelA resist curcumin-induced apoptosis. The Journal of Biological Chemistry, 275, 15601-15604.

Arbiser, J. L. (1997). Antiangiogenic therapy and dermatology: A review. Drugs Today, 33, 687-696.

Arbiser, J. L., Klauber, N., Rohan, R., van Leeuwen, R., Huang, M. T., Fisher, C., et al. (1998). Curcumin is an in vivo inhibitor of angiogenesis. Molecular Medicine, 4, 376-383.

Bae, S. H., Jung, E. S., Park, Y. M., Kim, B. S.,

Kim, B. K., Kim, D. G., et al. (2001). Expression of cyclooxygenase-2 (COX-2) in hepatocellular carcinoma and growth inhibition of hepatoma cell lines by a COX-2 inhibitor, NS-398. Clinical Cancer Research, 7, 1410-1418.

Bae, M. K., Kim, S. H., Jeong, J. W., Lee, Y. M., Kim, H.

S., Kim, S. R., et al. (2006). Curcumin inhibits hypoxia-induced angiogenesis via down-regulation of HIF-1. Oncology Report, 15, 1557-15562.

Bancroft, C. C., Chen, Z., Yeh, J., Sunwoo, J. B., Yeh, N. T., Jackson, S., et al. (2002). Effects of pharmacologic antagonists of epidermal growth factor receptor, PI3K and MEK signal kinases on NF-kappaB and AP-1 activation and IL-8 and VEGF expression in human head and neck squamous cell carcinoma lines. International Journal of Cancer, 99, 538-548.

Cao, J., Liu, Y., Jia, L., Zhou, H. M., Kong, Y., Yang, G., et al. (2007). Curcumin induces apoptosis through mitochondrial hyperpolarization and mtDNA damage in human hepatoma G2 cells. Free Radical Biology & Medicine, 43, 968-975.

Carmeliet, P. (2005). Angiogenesis in life, disease and medicine. Nature, 438, 932-936.

Cervello, M., & Montalto, G. (2006). Cyclooxygenases in hepatocellular carcinoma. World Journal of Gastroenterology, 12, 5113-5121.

Chen, Y. N., Cheng, C. C., Chen, J. C., Tsauer, W., & Hsu, S. L. (2003). Norcantharidin-induced apoptosis is via the extracellular signal-regulated kinase and c-Jun-NH2-terminal kinase signaling pathways in human hepatoma HepG2 cells. British Journal of Pharmacology, 140, 461-470.

Chen, A., & Xu, J. (2005). Activation of PPAR

{gamma} by curcumin inhibits Moser cell growth and mediates suppression of gene expression of cyclin D1 and EGFR. American Journal of Physiology - Gastrointestinal and Liver Physiology, 288, 447-456.

Chendil, D., Ranga, R. S., Meigooni, S., & Sathishkumar,

M. M. (2004). Curcumin confers radiosensitizing effect in prostate cancer cell line PC-3. Oncogene, 23, 1599-1607.

Cheng, A. S., Chan, H. L., To, K. F., Leung, W. K., Chan,

K. K., Liew, C. T., et al. (2004). Cyclooxygenase-2 pathway correlates with vascular endothelial growth factor expression and tumor angiogenesis in hepatitis B virus-associated hepatocellular carcinoma. International Journal of Oncology, 24, 853-860.

Cheng, A. L., Hsu, C. H., Lin, J. K., Hsu, M. M., Ho,

Y. F., Shen, T. S., et al. (2001). Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Research, 21, 2895-2900.

Choi, H., Chun, Y. S., Kim, S. W., Kim, M. S., & Park,

J. W. (2006). Curcumin inhibits hypoxia-inducible

Naresuan University Journal 2008; 16(3)

factor-1 by degrading aryl hydrocarbon receptor nuclear translocator: A mechanism of tumor growth in- hibition. Molecular Pharmacology, 70, 1664-1671.

Choudhuri, T., Pal, S., Das, T., & Sa, G. (2005). Curcumin selectively induces apoptosis in deregulated cyclin D1-expressed cells at G2 phase of cell cycle in a p53-dependent manner. Journal of Biological Chemistry, 280, 20059-20068.

Chuang, S. E., Cheng, A. L., Lin, J. K., & Kuo, M. L. (2000). Inhibition by curcumin of diethylnitrosamine-induced hepatic hyperplasia, inflammation, cellular gene products and cell-cycle- related proteins in rats. Food and Chemical Toxicology, 38, 991-995.

Cianchi, F., Cortesini, C., Bechi, P., Fantappie, O., Messerini, L., Vannacci, A., et al. (2001). Up-regulation of cyclooxygenase 2 gene expression correlates with tumor angiogenesis in human colorectal cancer. Gastroenterology, 121, 1339-1347.

Costa, C., Soares, R., Reis-Filho, J. S., Leitao, D., Amendoeira, I., & Schmitt, F. C. (2002). Cyclo- oxygenase 2 expression is associated with angiogenesis and lymph node metastasis in human breast cancer. Journal of Clinical Pathology, 55, 429-434.

Cui, S. X., Qu, X. J., Xie, Y. Y., Zhou, L., Nakata, M.,

Makuuchi, M., et al. (2006). Curcumin inhibits telomerase activity in human cancer cell lines. International Journal of Molecular Medicine, 18, 227-231

Deshpande, S. S., & Maru, G. B. (1995). Effects of curcumin on the formation of benzo[a]pyrene derived DNA adducts in vitro. Cancer Letters, 96, 71-80.

Dhillon, N., Aggarwal, B. B., Newman, R. A., Wolff,

R. A., Kunnumakkara, A. B., Abbruzzese, J. L., et al. (2008). Phase II trial of curcumin in patients with advanced pancreatic cancer. Clinical Cancer Research, 14, 4491-4499.

Dormond, O., Foletti, A., Paroz, C., & Ruegg, C. (2001). NSAIDs inhibit alpha V beta 3 integrin-mediated and Cdc42/Rac-dependent endothelial-cell spreading, migration and angiogenesis. Nature Medicine, 7, 1041-1047.

Dvorak, H. F., Nagy, J. A., Berse, B., Brown, L. F.,

Yeo, K. T., Yeo, T. K., et al. (1992). Vascular permeability factor, fibrin, and the pathogenesis of tumor stroma formation. Annals of the New York Academy of Sciences, 667, 101-111.

Fosslien, E. (2001). Review: Molecular pathology of cyclooxygenase-2 in cancer-induced angiogenesis. Annals of Clinical and Laboratory Science, 31, 325-348.

Fox, S. B., Gasparini, G., & Harris, A. L. (2001). Angiogenesis: Pathological, prognostic, and growth-factor pathways and their link to trial design and anticancer drugs. Lancet Oncology, 2, 278-289.

Garcea, G., Berry, D. P., Jones, D. J., Singh, R., Dennison,

A. R., Farmer, P. B., et al. (2005). Consumption of the putative chemopreventive agent curcumin by cancer patients: Assessment of curcumin levels in the colorectum and their pharmacodynamic consequences. Cancer Epidemiology Biomarkers & Prevention, 14, 120-125.

Grau, R., Punzon, C., Fresno, M., & Iniguez, M. A. (2006). Peroxisome-proliferator-activated receptor alpha agonists inhibit cyclo-oxygenase 2 and vascular endothelial growth factor transcriptional activation in human colorectal carcinoma cells via inhibition of activator protein-1. Biochemical Journal, 395, 81-88.

Guo, L. Y., Cai, X. F., Lee, J. J., Kang, S. S.,

Shin, E. M., Zhou, H. Y., et al. (2008). Comparison of suppressive effects of demethoxycurcumin and bisdemethoxycurcumin on expressions of inflammatory mediators in vitro and in vivo. Archives of Pharmacal Research, 31, 490-496.

Gupta, M. K., & Qin, R. Y. (2003). Mechanism and its regulation of tumor-induced angiogenesis. World Journal of Gastroenterology, 9, 1144-1155.

Gururaj, A. E., Belakavadi, M., Venkatesh, D. A., Marme, D., & Salimath, B. P. (2002). Molecular mechanisms of anti-angiogenic effect of curcumin. Biochemical and Biophysical Research Communications, 297, 934-942.

Hahm, E. R., Gho, Y. S., Park, S., Park, C., Kim, K. W.,

& Yang, C. H. (2004). Synthetic curcumin analogs inhibit activator protein-1 transcription and tumor-induced angiogenesis. Biochemical and Biophysical Research Communications, 321, 337-344.

Hanahan, D., & Folkman, J. (1996). Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353-364.

Hanahan, D., & Weinberg, R. A. (2000). The hallmarks of cancer. Cell, 100, 57-70.

Harris, A. L. (2002). Hypoxia--a key regulatory factor in tumour growth. Nature Reviews Cancer, 2,

-47.

Hla, T., Bishop-Bailey, D., Liu, C. H., Schaefers,

H. J., & Trifan, O. C. (1999). Cyclooxygenase-1 and -2 isoenzymes. The International Journal of Biochemistry & Cell Biology, 31, 551-557.

Huang, M. T., Lou, Y. R., Xie, J. G., Ma, W., Lu, Y. P.,

Yen, P., et al. (1998). Effect of dietary curcumin and dibenzoylmethane on formation of 7, 12-dimethylbenz[a]anthracene-induced mammary tumors and lymphomas/leukemias in Sencar mice. Carcinogenesis, 19, 1697-1700.

Huang, M. T., Ma, W., Lu, Y. P., Chang,

R. L., Fisher, C., Manchand, P. S., et al. (1995). Effects of curcumin, demethoxycurcumin, bisdemethoxycurcumin and tetrahydrocurcumin on 12-O-tetradecanoylphorbol-13-acetate-induced tumor promotion. Carcinogenesis, 16, 2493-2497.

Huang, M. T., Ma, W., Yen, P., Xie, J. G., Han, J.,

Frenkel, K., et al. (1997). Inhibitory effects of topical application of low doses of curcumin on 12-O-tetradecanoylphorbol-13-acetate-induced tumor promotion and oxidized DNA bases in mouse epidermis. Carcinogenesis, 18, 83-88.

Jacob, A., Wu, R., Zhou, M., & Wang, P. (2007). Mechanism of the anti-inflammatory effect of curcumin: PPAR-gamma activation. PPAR Research, 2007, 1-5.

Jinno, K., Tanimizu, M., Hyodo, I., Nishikawa, Y., Hosokawa, Y., Doi, T., et al. (1998). Circulating vascular endothelial growth factor (VEGF) is a possible tumor marker for metastasis in human hepatocellular carcinoma. Journal of Gastroenterology, 33, 376-382.

Jung, J. O., Gwak, G. Y., Lim, Y. S., Kim, C. Y., & Lee,

H. S. (2003). [Role of hepatic stellate cells in the angiogenesis of hepatoma]. Korean Journal of Gastroenterology, 42, 142-148.

Kamat, A. M., Sethi, G., & Aggarwal, B. B. (2007). Curcumin potentiates the apoptotic effects of chemotherapeutic agents and cytokines through down-regulation of nuclear factor-kappaB and nuclear factor-kappaB-regulated gene products in IFN-alpha-sensitive and IFN-alpha-resistant human bladder cancer cells. Molecular Cancer Therapeutics, 6, 1022-1030.

Kambayashi, T., Alexander, H. R., Fong, M., & Strassmann, G. (1995). Potential involvement of IL-10 in suppressing tumor-associated macrophages. Colon-26-derived prostaglandin E2 inhibits

TNF-alpha release via a mechanism involving IL-10. The Journal of Immunology, 154, 3383-3390.

Kim, K. J., Li, B., Winer, J., Armanini, M., Gillett, N., Phillips, H. S., et al. (1993). Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature, 362, 841-844.

Konturek, P. C., Kania, J., Burnat, G., Hahn, E. G., & Konturek, S. J. (2005). Prostaglandins as mediators of COX-2 derived carcinogenesis in gastrointestinal tract. Canadian Journal of Physiology and Pharmacology, 56, 57-73.

Kunnumakkara, A. B., Anand, P., & Aggarwal, B. B. (2008). Curcumin inhibits proliferation, invasion, angiogenesis and metastasis of different cancers through interaction with multiple cell signaling proteins. Cancer Letters, 269, 199-225.

Kunnumakkara, A. B., Guha, S., Diagaradjane, P., Gelovani, J., & Aggarwal, B. B. (2007). Curcumin potentiates antitumor activity of gemcitabine in an orthotopic model of pancreatic cancer through suppression of proliferation, angiogenesis, and inhibition of nuclear factor-kappaB-regulated gene products. Cancer Research, 67, 3853-3861.

Kuttan, R., Sudheeran, P. C., & Josph, C. D. (1987). Turmeric and curcumin as topical agents in cancer therapy. Tumori, 73, 29-31.

Labbozzetta, M., Notarbartolo, M., Poma, P., Giannitrapani, L., Cervello, M., Montalto, G., et al. (2006). Significance of autologous interleukin-6 production in the HA22T/VGH cell model of hepatocellular carcinoma. Annals of the New York Academy of Sciences, 1089, 268-275.

Lee, C. C., Chen, S. C., Tsai, S. C., Wang, B. W., Liu,

Y. C., Lee, H. M., et al. (2006). Hyperbaric oxygen induces VEGF expression through ERK, JNK and c-Jun/AP-1 activation in human umbilical vein endothelial cells. Journal of Biomedical Science, 13, 143-156.

Lee, J., Im, Y. H., Jung, H. H., Kim, J. H., Park, J. O., Kim,

K., et al. (2005). Curcumin inhibits interferon-alpha induced NF-kappaB and COX-2 in human A549 non-small cell lung cancer cells. Biochemical and Biophysical Research Communications, 334, 313-318.

Lee, E. O., Lee, H. J., Hwang, H. S., Ahn, K. S., Chae, C., Kang, K. S., et al. (2006). Potent inhibition of Lewis lung cancer growth by heyneanol A from the roots of Vitis amurensis through apoptotic and anti-angiogenic activities. Carcinogenesis, 27,

-2069.

Li, M., Zhang, Z., Hill, D.L., Wang, H., & Zhang, R. (2007). Curcumin, a dietary component, has anticancer, chemosensitization, and radiosensitization effects by down-regulating the MDM2 oncogene through the PI3K/mTOR/ETS2 pathway. Cancer Research, 67, 1988-1996.

Lin, L. I., Ke, Y. F., Ko, Y. C., & Lin, J. K. (1998).

Curcumin inhibits SK-Hep-1 hepatocellular carcinoma cell invasion in vitro and suppresses matrix metalloproteinase-9 secretion. Oncology, 55, 349-353.

Lin, Y. G., Kunnumakkara, A. B., Nair, A., Merritt,

W. M., Han, L. Y., Armaiz-Pena, G. N., et al. (2007). Curcumin inhibits tumor growth and angiogenesis in ovarian carcinoma by targeting the nuclear factor-kappaB pathway. Clinical Cancer Research, 13, 3423-3430.

Longo, R., Sarmiento, R., Fanelli, M., Capaccetti, B., Gattuso, D., & Gasparini, G. (2002). Anti-angiogenic therapy: Rationale, challenges and clinical studies. Angiogenesis, 5, 237-256.

Masood, R., Cai, J., Zheng, T., Smith, D. L., Hinton, D. R., & Gill, P. S. (2001). Vascular endothelial growth factor (VEGF) is an autocrine growth factor for VEGF receptor-positive human tumors. Blood, 98, 1904-1913.

Mise, M., Arii, S., Higashituji, H., Furutani, M., Niwano, M., Harada, T., et al. (1996). Clinical significance of vascular endothelial growth factor and basic fibroblast growth factor gene expression in liver tumor. Hepatology, 23, 455-464.

Mohan, R., Sivak, J., Ashton, P., Russo, L. A., Pham,

B. Q., Kasahara, N., et al. (2000). Curcuminoids inhibit the angiogenic response stimulated by fibroblast growth factor-2, including expression of matrix metalloproteinase gelatinase B. Journal of Biological Chemistry, 275, 10405-10412.

Moon, E. J., Jeong, C. H., Jeong, J. W., Kim, K. R., Yu, D. Y., Murakami, S., et al. (2004). Hepatitis B virus X protein induces angiogenesis by stabilizing hypoxia-inducible factor-1alpha. Journal of the Federation of American Societies for Experimental Biology, 18, 382-384.

Morita, I. (2002). Distinct functions of COX-1 and COX-2. Prostaglandins & Other Lipid Mediators, 68-69, 165-175.

Mukhopadhyay, A., Banerjee, S., Stafford, L. J., Xia, C.,

Liu, M., & Aggarwal, B. B. (2002). Curcumin-induced suppression of cell proliferation correlates with down-regulation of cyclin D1 expression and CDK4- mediated retinoblastoma protein phosphorylation. Oncogene, 21, 8852-8861.

Pang, R., & Poon, R. T. (2006). Angiogenesis and antiangiogenic therapy in hepatocellular carcinoma. Cancer Letters, 242, 151-167.

Park, M. J., Kim, E. H., Park, I. C., Lee, H. C., Woo, S. H.,

Lee, J. Y., et al. (2002). Curcumin inhibits cell cycle progression of immortalized human umbilical vein endothelial (ECV304) cells by up-regulating cyclin-dependent kinase inhibitor, p21WAF1/CIP1, p27KIP1 and p53. International Journal of Oncology, 21, 379-383.

Park, Y. N., Kim, Y. B., Yang, K. M., & Park, C. (2000).

Increased expression of vascular endothelial growth factor and angiogenesis in the early stage of multistep hepatocarcinogenesis. Archives of Pathology and Laboratory Medicine, 124, 1061-1065.

Parkin, D. M., Bray, F., Ferlay, J., & Pisani, P. (2001). Estimating the world cancer burden: Globocan 2000. International Journal of Cancer, 94, 153-156.

Plummer, S. M., Hill, K. A., Festing, M. F., Steward, W. P., Gescher, A. J., & Sharma, R. A. (2001). Clinical development of leukocyte cyclooxygenase-2 activity as a systemic biomarker for cancer chemopreventive agents. Cancer Epidemiology, Biomarkers & Prevention, 10, 1295-1299.

Poon, R. T., Lau, C. P., Cheung, S. T., Yu, W. C., & Fan, S. T. (2003). Quantitative correlation of serum levels and tumor expression of vascular endothelial growth factor in patients with hepatocellular carcinoma. Cancer Research, 63, 3121-3126.

Rahman, M. A., Dhar, D. K., Yamaguchi, E.,

Maruyama, S., Sato, T., Hayashi, H., et al. (2001). Coexpression of inducible nitric oxide synthase and COX-2 in hepatocellular carcinoma and surrounding liver: possible involvement of COX-2 in the angiogenesis of hepatitis C virus-positive cases. Clinical Cancer Research, 7, 1325-1332.

Ruby, A. J., Kuttan, G., Babu, K. D., Rajasekharan,

K. N., & Kuttan, R. (1995). Anti-tumour and antioxidant activity of natural curcuminoids. Cancer Letters, 94, 79-83.

Sandur, S. K., Ichikawa, H., Pandey, M. K., Kunnumakkara, A. B., Sung, B., Sethi, G., et al. (2007). Role of pro-oxidants and antioxidants in the anti-inflammatory and apoptotic effects of curcumin

(diferuloylmethane). Free Radical Biology & Medicine, 43, 568-580.

Semela, D., & Dufour, J. F. (2004). Angiogenesis and hepatocellular carcinoma. Journal of Hepatology, 41, 864-880.

Shankar, S., Chen, Q., Sarva, K., Siddiqui, I., & Srivastava, R. K. (2007). Curcumin enhances the apoptosis-inducing potential of TRAIL in prostate cancer cells: molecular mechanisms of apoptosis, migration and angiogenesis. Journal of Molecular Signaling, 2, 10.

Shao, Z. M., Wu, J., Shen, Z. Z., & Barsky, S. H. (1998).

Genistein exerts multiple suppressive effects on human breast carcinoma cells. Cancer Reasearch, 58, 4851-4857.

Sharma, R. A., McLelland, H. R., Hill, K. A., Ireson,

C. R., Euden, S. A., Manson, M. M., et al. (2001). Pharmacodynamic and pharmacokinetic study of oral Curcuma extract in patients with colorectal cancer. Clinical Cancer Research, 7, 1894-1900.

Sharma, R. A., Euden, S. A., Platton, S. L., Cooke, D. N., Shafayat, A., Hewitt, H. R., et al. (2004). Phase I clinical trial of oral curcumin: Biomarkers of systemic activity and compliance. Clinical Cancer Research, 10, 6847-6854.

Sheng, H., Shao, J., Morrow, J. D., Beauchamp, R. D., & DuBois, R. N. (1998). Modulation of apoptosis and Bcl-2 expression by prostaglandin E2 in human colon cancer cells. Cancer Research, 58, 362-366.

Singh, A. K., Sidhu, G. S., Deepa, T., & Maheshwari,

R. K. (1996). Curcumin inhibits the proliferation and cell cycle progression of human umbilical vein endothelial cell. Cancer Letters, 107, 109-115.

Singletary, K., MacDonald, C., Wallig, M., & Fisher, C. (1996). Inhibition of 7,12-dimethylbenz[a]anthracene (DMBA)-induced mammary tumorigenesis and DMBA-DNA adduct formation by curcumin. Cancer Letters, 103, 137-141.

Suryanarayana, P., Satyanarayana, A., Balakrishna, N., Kumar, P. U., & Reddy, G. B. (2007). Effect of turmeric and curcumin on oxidative stress and antioxidant enzymes in streptozotocin-induced diabetic rat. Medical Science Monitor, 13, 286-292.

Tanaka, T., Makita, H., Ohnishi, M., Hirose, Y., Wang, A., Mori, H., et al. (1994). Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by dietary curcumin and hesperidin: Comparison with the protective effect of beta-carotene. Cancer

Research, 54, 4653-4659.

Tang, F. Y., Chiang, E. P., & Shih, C. J. (2006). Green tea catechin inhibits ephrin-A1-mediated cell migration and angiogenesis of human umbilical vein endothelial cells. The Journal of Nutritional Biochemistry, 18, 391-399.

Tang, T. C., Poon, R. T., Lau, C. P., Xie, D., & Fan, S. T.

(2005). Tumor cyclooxygenase-2 levels correlate with tumor invasiveness in human hepatocellular carcinoma. World Journal of Gastroenterology, 11, 1896-1902.

Thaloor, D., Singh, A. K., Sidhu, G. S., Prasad, P. V., Kleinman, H. K., & Maheshwari, R. K. (1998). Inhibition of angiogenic differentiation of human umbilical vein endothelial cells by curcumin. Cell Growth & Differentiation, 9, 305-312.

Tomita, M., Kawakami, H., Uchihara, J. N., Okudaira, T., Masuda, M., Takasu, N., et al. (2006). Curcumin suppresses constitutive activation of AP-1 by downregulation of JunD protein in HTLV-1-infected T-cell lines. Leukemia Research, 30, 313-321.

Tong, R. T., Boucher, Y., Kozin, S. V., Winkler, F., Hicklin, D. J., & Jain, R. K. (2004). Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Research, 64, 3731-3736.

Torimura, T., Sata, M., Ueno, T., Kin, M., Tsuji, R., Suzaku, K., et al. (1998). Increased expression of vascular endothelial growth factor is associated with tumor progression in hepatocellular carcinoma. Human Pathology, 29, 986-991.

Tsujii, M., Kawano, S., & DuBois, R. N. (1997). Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proceedings of the National Academy of Sciences of the United States of America, 94, 3336-3340.

Tsujii, M., Kawano, S., Tsuji, S., Sawaoka, H., Hori, M., & DuBois, R. N. (1998). Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell, 93, 705-716.

Vanisree, A.J., & Sudha, N. (2006). Curcumin combats against cigarette smoke and ethanol-induced lipid alterations in rat lung and liver. Molecular and Cellular Biochemistry, 288, 115-123.

Vatanasapt, V., Sriamporn, S., & Vatanasapt, P. (2002). Cancer control in Thailand. Japanese Journal of Clinical Oncology, 32, 82-91.

Naresuan University Journal 2008; 16(3)

Veikkola, T., Karkkainen, M., Claesson-Welsh, L., & Alitalo, K. (2000). Regulation of angiogenesis via vascular endothelial growth factor receptors. Cancer Research, 60, 203-212.

Wu, X. Z., Xie, G. R., & Chen, D. (2007). Hypoxia and hepatocellular carcinoma: The therapeutic target for hepatocellular carcinoma. Journal of Gastroenterology and Hepatology, 22, 1178-1182.

Yamaguchi, R., Yano, H., Nakashima, Y., Ogasawara, S., Higaki, K., Akiba, J., et al. (2000). Expression and localization of vascular endothelial growth factor receptors in human hepatocellular carcinoma and non-HCC tissues. Oncology Reports, 7, 725-729.

Yoo, Y. G., Oh, S. H., Park, E. S., Cho, H., Lee, N.,

Park, H., et al. (2003). Hepatitis B virus X protein enhances transcriptional activity of hypoxia-inducible factor-1alpha through activation of mitogen-activated protein kinase pathway. Journal of Biological Chemistry, 278, 39076-39084.

Yoysungnoen, P., Wirachwong, P., Bhattarakosol, P., Niimi, H., & Patumraj, S. (2006). Effects of curcumin on tumor angiogenesis and biomarkers, COX-2 and VEGF, in hepatocellular carcinoma cell-implanted nude mice. Clinical Hemorheology and Microcirculation, 34, 109-115.

Yoysungnoen, P., Wirachwong, P., Changtam, C., Suksamrarn, A., & Patumraj, S. (2008). Anti-cancer and anti-angiogenic effects of curcumin and tetrahydrocurcumin on implanted hepatocellular carcinoma in nude mice. World Journal of Gastroenterology, 14, 2003-2009.

Zhao, Q. T., Yue, S. Q., Cui, Z., Wang, Q., Cui, X.,

Zhai, H. H., et al. (2007). Potential involvement of the cyclooxygenase-2 pathway in hepatocellular carcinoma-associated angiogenesis. Life Sciences, 80, 484-492.

Zhou, J. R., Gugger, E. T., Tanaka, T., Guo, Y., Blackburn, G. L., & Clinton, S. K. (1999). Soybean phytochemicals inhibit the growth of transplantable human prostate carcinoma and tumor angiogenesis in mice. The Journal of Nutrition, 129, 1628-1635.

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