Resveratrol Suppresses the Angiogenesis and Tumor Growth of Gliomas in Rats

Clinical Cancer Research

Volumn 10, Issue 6, 2004, Pages 2190-2202

  Tseng, Sheng Hong ^a   Lin, Swei Ming ^a   Chen, Jin Cherng ^b   Su, Yen Hao ^a   Huang, Hsin Yi ^a   Chen, Chia Kang ^a   Lin, Po Yin ^a   Chen, Yun ^a,c  

^a NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^b BUDDHIST TZU CHI GENERAL HOSPITAL   (Taiwan)

^c FAR EASTERN MEMORIAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

RESVERATROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CELL SORTER; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG ACTIVITY; DRUG EFFECT; FLOW CYTOMETRY; GLIOMA; GLIOMA CELL; GROWTH INHIBITION; GROWTH RATE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SURVIVAL RATE; TIME; TUMOR GROWTH; TUMOR VOLUME; UMBILICAL VEIN;

ANGIOGENESIS INHIBITORS; ANIMALS; APOPTOSIS; CELL DIVISION; CELL LINE; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; FLOW CYTOMETRY; GLIOMA; KINETICS; NEOVASCULARIZATION, PATHOLOGIC; RATS; STILBENES; UMBILICAL VEINS;

EID: 1642382931     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-03-0105     Document Type: Article

References (71)

1. Daumas-Duport C, Scheithauer B, O'Fallon J, Kelly P. Grading of astrocytomas: a simple and reproducible method. Cancer 1988;62: 2152-65.
2. Kim TS, Halliday AL, Hedley-Whyte ET, Convey K. Correlates of survival and the Daumas-Duport grading system for astrocytomas. J Neurosurg 1991;74:27-37.
3. Mahaley MS Jr, Mettlin C, Natarajan N, Laws ER Jr. National survey on patterns of care for brain-tumor patients. J Neurosurg 1989;71: 826-36.
4. Salazar OM, Rubin P, Feldstein ML, Pizzutiello R. High dose radiation therapy in the treatment of malignant gliomas: final report. Int J Radiat Oncol Biol Phys 1979;5:1733-40.
5. Shapiro WR, Green SB, Burger PC, et al. Randomized trial of three chemotherapy regimens and two radiotherapy regimens in postoperative treatment of malignant gliomas. J Neurosurg 1989;71:1-9.
6. Walker MD, Green SB, Byar DR, et al. Randomized comparisons of radiotherapy and nitrosoureas for the treatment of malignant glioma after surgery. N Engl J Med 1980;303:1323-9.
7. Soleas GJ, Diamandis EP, Goldberg DM. Resveratrol: a molecule whose time has come and gone? Clin Biochem 1997;30:91-113.
8. Belguendouz L, Fremont L, Linard A. Resveratrol inhibits metal ion-dependent and independent peroxidation of porcine low-density lipoproteins. Biochem Pharmacol 1997;53:1347-55.
9. Frankel EN, Waterhouse AL, Kinsella JE. Inhibition of human LDL oxidation by resveratrol. Lancet 1993;34:1103-4.
10. Arichi H, Kimura Y, Okuda H, Baba K, Kozawa M, Arichi S. Effects of stilbene components of the roots of polygonium on lipid metabolism. Chem Pharm Bull 1982;30:1766-70.
11. Jang M, Cai L, Udeani GO, et al. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 1997;275: 218-20.
12. Uenobe F, Nakamura S, Miyazawa M. Antimutagenic effect of resveratrol against Trp-P1. Mutat Res 1997;373:197-200.
13. Clement MV, Hirpara JL, Chawdhury SH, Hirpara JL, Chawdhury SH, Pervaiz S. Chemopreventive agent resveratrol, a natural product derived from grapes, triggers CD95 signaling-dependent apoptosis in human tumor cells. Blood 1998;92:996-1002.
14. Kuwajerwala N, Cifuentes E, Gautam S, Menon M, Barrack ER, Veer Reddy GP. Resveratrol induces prostate cancer cell line entry into S phase and inhibits DNA synthesis. Cancer Res 2002;62:2488-92.
15. Lu R, Serrero G. Resveratrol, a natural product derived from grapes, exhibits antiestrogenic activity and inhibits the growth of human breast cancer cells. J Cell Physiol 1999;179:297-304.
16. Schneider Y, Vincent F, Duranton B, et al. Anti-proliferative effect of resveratrol, a natural component of grapes and wine, on human colonic cancer cells. Cancer Lett 2000;158:85-91.
17. Surh YJ, Hurh YJ, Kang JY, Lee E, Kong G, Lee SJ. Resveratrol, an antioxidant present in red wine, induces apoptosis in human promyelocytic leukemia (HL-60) cells. Cancer Lett 1999;140:1-10.
18. Huang C, Ma WY, Goranson A, Dong Z. Resveratrol suppresses cell transformation and induces apoptosis through a p53-dependent pathway. Carcinogenesis 1999;20:237-42.
19. Miloso M, Bertelli AAE, Nicolini G, Tredici G. Resveratrol-induced activation of the mitogen-activated protein kinases, ERK1 and ERK2, in human neuroblastoma SH-SY5Y cells. Neurosci Lett 1999; 264:141-4.
20. She QB, Bode AM, Ma WY, Chen NY, Dong Z. Resveratrol-induced activation of p53 and apoptosis is mediated by extracellular-signal-regulated protein kinases and p38 kinase. Cancer Res 2001;61: 1604-10.
21. Chun YJ, Kim MY, Guengerich FP. Resveratrol is a selective human cytochrome P450 1A1 inhibitor. Biochem Biophys Res Commun 1999;262:20-4.
22. Fontecave M, Lepoivre M, Elleingand E, Gerez C, Guittet O. Resveratrol, a remarkable inhibitor of ribonucleotide reductase. FEBS Lett 1998;421:277-9.
23. Subbaramaiah K, Chung WJ, Michaluart P, et al. Resveratrol inhibits cyclooxjgenase-2 transcription and activity in phorbol ester-treated human mammary epithelial cells. J Biol Chem 1998;273: 21875-82.
24. Sun NJ, Woo SH, Cassady JM, Snapka RM. DNA polymerase and topoisomerase II inhibitors form Psoralea corylifolia. J Natl Prod 1998; 61:362-6.
25. Maccarrone M, Lorenzon T, Guerrieri P, Agro AF. Resveratrol prevents apoptosis in K562 cells by inhibiting lipoxygenase and cyclooxygenase activity. Eur J Biochem 1999;265:27-34.
26. Zou J, Huang Y, Chen Q, Wang N, Cao K, Hsieh TC, et al. Suppression of mitogenesis and regulation of cell cycle traverse by resveratrol in cultured smooth muscle cells. Int J Oncol 1999;15: 647-51.
27. Hsieh TC, Wu JM. Differential effects on growth, cell cycle arrest, and induction of apoptosis by resveratrol in human prostate cancer cell lines. Exp Cell Res 1999;249:109-15.
28. Kimura Y, Okuda H. Resveratrol isolated from Polygonum cuspidatum root prevents tumor growth and metastasis to lung and tumor-induced neovascularization in Lewis lung carcinoma-bearing mice. J Nutr 2001;131:1844-9.
29. Couldwell WT, Antel JP, Yong VW. Enhanced protein kinase C activity correlates with the growth rate of malignant gliomas: Part II. Effects of glioma mitogens and modulators of PKC. Neurosurgery 1992;31:717-24.
30. Couldwell WT, Uhm J, Antel JP, Yong VW. Enhanced protein kinase C activity correlates with the growth rate of malignant human gliomas. Neurosurgery 1991;29:880-7.
31. Brem S, Corran R, Folkman J. Tumor angiogenesis: a quantitative method for histologic grading. J Natl Cancer Inst 1972;48:347-56.
32. Brem S. The role of vascular proliferation in the growth of brain tumors. Clin Neurosurg 1976;23:440-53.
33. Swiatecka J, Dzieciol J, Anchim T, Dabrowska M, Pietruczuk M, Wolczynski S. Influence of estrogen, antiestrogen and UV-light on the balance between proliferation and apoptosis in MCF-7 breast adenocarcinoma cell culture. Neoplasma 2000;47:15-24.
34. Okajima E, Thorgeirsson UP. Different regulation of vascular endothelial growth factor expression by the ERK and p38 kinase pathways in v-ras, v-raf, and v-myc transformed cells. Biochem Biophys Res Commun 2000;270:108-11.
35. Barros LF, Young M, Saklatvala J, Baldwin SA. Evidence of two mechanisms for the activation of the glucose transporter GLUT1 by anisomycin: p38 (MAP kinase) activation and protein synthesis inhibition in mammalian cells. J Physiol 1997;504:517-25.
36. Park DS, Stefanis L, Yan CYI, Farinelli SE, Greene LA. Ordering the cell death pathway: differential effects of Bcl2, and interleukin-1-converting enzyme family protease inhibitor, and other survival agents on JNK activation in serum/nerve growth factor-deprived PC12 cells. J Biol Chem 1996;271:21898-905.
37. Verheij M, Bose R, Lin XH, Yao B, Jarvis WD, Grant S, et al. Requirement for ceramide-initiated SAPK/JNK signaling in stress-induced apoptosis. Nature (Lond) 1996;380:75-9.
38. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995;270:1326-31.
39. Xu X, Raber J, Yang D, Su B, Mucke L. Dynamic regulation of c-jun N-terminal kinase activity in mouse brain by environmental stimuli. Proc Natl Acad Sci USA 1997;94:12655-60.
40. Copeland DD, Talley FA, Bigner DD. The fine structure of intracranial neoplasms induced by the inoculation of avian sarcoma virus in neonatal and adult rats. Am J Pathol 1976;83:149-76.
41. Takahashi K, Sawasaki Y, Hata J, Mukai K, Goto T. Spontaneous transformation and immortalization of human endothelial cells. In Vitro Cell Dev Biol 1990;26:265-74.
42. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxic assays. J Immunol Methods 1983;65:55-63.
43. Caltagirone S, Rossi C, Poggi A, et al. Flavonoid apigenin and quercetin inhibit melanoma growth and metastatic potential. Int J Cancer 2000;87:595-600.
44. Turrens JF, Lariccia J, Nair MG. Resveratrol has no effect on lipoprotein profile and does not prevent peroxidation of serum lipids in normal rats. Free Radical Res 1997;27:557-62.
45. Weizsaecker M, Deen DF, Rosenblum ML, Hoshino T, Gutin PH, Barker M. The 9L rat brain tumor: description and application of an animal model. J Neurol 1981;224:183-92.
46. Weidner N, Folkman J, Pozza F, et al. Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast cancer. J Natl Cancer Inst 1992;84:1875-87.
47. Chau YP, Shiah SG, Don MJ, Kuo ML. Involvement of hydrogen peroxide in topoisomerase inhibitor β-lapachone-induced apoptosis and differentiation in human leukemia cells. Free Radic Biol Med 1998;24: 660-70.
48. Brakenhielm E, Cao R, Cao Y. Suppression of angiogenesis, tumor growth, and wound healing by resveratrol, a natural compound in red wine and grapes. FASEB J 2001;15:1798-800.
49. Bertelli AA, Giovannini L, Stradi R, Urien S, Tillement JP, Bertelli A. Kinetics of trans- and cis-resveratrol (3,4′,5-trihydroxystilbene) after red wine oral administration in rats. Int J Clin Pharmacol Res 1996;16: 77-81.
50. Mgbonyebi OP, Russo J, Russo H. Antiproliferative effect of synthetic resveratrol on human breast epithelial cells. Int J Oncol 1998;12: 865-9.
51. Igura K, Ohta T, Kuroda Y, Kaji K. Resveratrol and quercetin inhibit angiogenesis in vitro. Cancer Lett 2001;171:11-6.
52. Gimbrone MA Jr, Leapman SB, Cotran RS, Folkman J. Tumor dormancy in vivo by prevention of neovascularization. J Exp Med 1972;136:261-76.
53. Millauer B, Shawver LK, Plate KH, Risau W, Ullrich A. Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant. Nature 1994;367:576-9.
54. Saleh M, Stacker SA, Wilks AF. Inhibition of growth of C6 glioma cells in vivo by expression of antisense vascular endothelial growth factor sequence. Cancer Res 1996;56:393-401.
55. Weinstst-Saslow D, Steeg PS. Angiogenesis and colonization in the tumor metastatic process: basic and applied advances. FASEB J 1994; 8:401-7.
56. Weidner N, Carroll PR, Flax J, Blumenfeld W, Folkman J. Tumor angiogenesis correlates with metastasis in invasive prostate carcinoma. J Natl Cancer Inst 1993;143:401-9.
57. Plate KH, Breier G, Weich HA, Risau W. Vascular endothelial growth factor is a potential tumor angiogenesis factors in human gliomas in vivo. Nature 1992;359:845-8.
58. v integrins. Science 1995;270:1500-2.
59. D'Amore PA, Thompson RW. Mechanisms of angiogenesis. Annu Rev Physiol 1987;49:453-64.
60. Folkman J, Klagsburn M. Angiogenic factors. Science 1987;235: 442-7.
61. Borgstrom P, Hillan KJ, Sriramaro P, Ferrara N. Complete inhibition of angiogenesis and growth of microtumors by anti-vascular endothelial growth factor neutralizing antibody: novel concepts of angiostatic therapy from intravital videomicroscopy. Cancer Res 1996;56:4032-9.
62. Price DJ, Miralem T, Jiang S, Steinberg R, Avraham H. Role of vascular endothelial growth factor in the stimulation of cellular invasion and signaling of breast cancer cells. Cell Growth Differ 2001;12: 129-35.
63. Yoshiji H, Harris SR, Thorgeirsson UP. Vascular endothelial growth factor is essential for initial but not continued in vivo growth of human breast carcinoma cells. Cancer Res 1997;57:3924-8.
64. Maxwell M, Naber SP, Wolfe HJ, et al. Expression of angiogenic growth factor genes in primary human astrocytomas may contribute to their growth and progression. Cancer Res 1991;51:1345-51.
65. Von Marschall Z, Cramer T, Hocker M, et al. De novo expression of vascular endothelial growth factor in human pancreatic cancer: evidence for an autocrine mitogenic loop. Gastroenterology 2000;119: 1358-72.
66. Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 1995;80:179-85.
67. Van Golen KL, Bao LW, Pan Q, Miller FR, Wu ZF, Merajver SD. Mitogen activated protein kinase pathway is involved in RhoC GTPase induced motility. Invasion and angiogenesis in inflammatory breast cancer. Clin Exp Metastasis 2002;19:301-11.
68. Ono K, Han J. The p38 signal transduction pathway: activation and function. Cell Signalling 2000;12:1-13.
69. Xiong S, Grijalva R, Zhang L, et al. Up-regulation of vascular endothelial growth factor in breast cancer cells by the heregulin-β 1-activated p38 signaling pathway enhances endothelial cell migration. Cancer Res 2001;61:1727-32.
70. Mori K, Tani M, Kamata K, et al. Mitogen-activated protein kinase, ERK1/2, is essential for the induction of vascular endothelial growth factor by ionizing radiation mediated by activator protein-1 in human glioblastoma cells. Free Radical Res 2000;33:157-66.
71. She QB, Huang C, Dong Z. Involvement of c-Jun NH2-terminal kinases in resveratrol-induced activation of p53 and apoptosis. Mol Carcinog 2002;33:244-50.