Extract of Cordyceps militaris inhibits angiogenesis and suppresses tumor growth of human malignant melanoma cells

International Journal of Oncology

Volumn 45, Issue 1, 2014, Pages 209-218

  Ruma, I Made Winarsa ^a   Putranto, Endy Widya ^a   Kondo, Eisaku ^b   Watanabe, Risayo ^b   Saito, K E N ^b   Inoue, Yusuke ^c   Yamamoto, Ken Ichi ^a   Nakata, Susumu ^b   Kaihata, Masaji ^d   Murata, Hitoshi ^a   Sakaguchi, Masakiyo ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b AICHI CANCER CENTER HOSPITAL   (Japan)

^c GUNMA UNIVERSITY   (Japan)

^d CAITAC Corporation   (Japan)

Author keywords

Akt and GSK 3 ; Angiogenesis; Cordyceps militaris; Melanoma; Vascular endothelial growth factor receptor

Indexed keywords

CORDYCEPS MILITARIS EXTRACT; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE 14; PLANT EXTRACT; PROTEIN KINASE B; UNCLASSIFIED DRUG; VASCULOTROPIN; ANTINEOPLASTIC AGENT; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; HERBACEOUS AGENT; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; CORDYCEPS; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; MELANOMA; MELANOMA CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; EXPERIMENTAL MELANOMA; GENE EXPRESSION REGULATION; ISOLATION AND PURIFICATION; MEDICINAL PLANT; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; CORDYCEPS; DRUGS, CHINESE HERBAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; PLANTS, MEDICINAL; PROTO-ONCOGENE PROTEINS C-AKT; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84902593089     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2397     Document Type: Article

References (56)

1. Folkman J: Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1: 27-31, 1995.
2. Dewing D, Emmett M and Pritchard Jones R: The roles of angiogenesis in malignant melanoma: trends in basic science research over the last 100 years. ISRN Oncol 2012: 546927, 2012.
3. Folkman J: Role of angiogenesis in tumor growth and metastasis. Semin Oncol 29: 15-18, 2002.
4. Zetter BR: Angiogenesis and tumor metastasis. Annu Rev Med 49: 407-424, 1998.
5. Naumov GN, Bender E, Zurakowski D, et al: A model of human tumor dormancy: an angiogenic switch from the non-angiogenic phenotype. J Natl Cancer Inst 98: 316-325, 2006.
6. Nanus DM, Schmitz-Dräger BJ, Motzer RJ, et al: Expression of basic fibroblast growth factor in primary human renal tumors: correlation with poor survival. J Natl Cancer Inst 85: 1597-1599, 1993.
7. Toi M, Hoshina S, Takayanagi T and Tominaga T: Association of vascular endothelial growth factor expression with tumor angiogenesis and with early relapse in primary breast cancer. Jpn J Cancer Res 85: 1045-1048, 1994.
8. Relf M, LeJeune S, Scott PA, et al: Expression of the angiogenic factors, vascular endothelial growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet derived growth endothelial cell growth factor, placental growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res 57: 963-969, 1997.
9. Kandel J, Bossy-Wetzel E, Radvanyi F, Klagsbrun M, Folkman J and Hanahan D: Neovascularization is associated with a switch to the export of bFGF in the multistep development of fibrosarcoma. Cell 66: 1095-1104, 1991.
10. Hanahan D and Folkman J: Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86: 353-364, 1996.
11. Ferrara N: Vascular endothelial growth factor. Eur J Cancer 32A: 2413-2422, 1996.
12. Risau W: Mechanisms of angiogenesis. Nature 386: 671-674, 1997.
13. Shibuya M: Vascular endothelial growth factor-dependent and independent regulation of angiogenesis. BMB Rep 41: 278-286, 2008.
14. Benjamin LE and Keshet E: Conditional switching of vascular endothelial growth factor (VEGF) expression in tumors: induction of endothelial cell shedding and regression of hemangioblastoma-like vessels by VEGF withdrawal. Proc Natl Acad Sci USA 94: 8761-8766, 1997.
15. Shibuya M: Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J Biochem Mol Biol 39: 469-478, 2006.
16. Ellis LM and Hicklin DJ: VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer 8: 579-591, 2008.
17. Dvorak HF: Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J Clin Oncol 20: 4368-4380, 2002.
18. Erhard H, Rietveld FJ, van Altena MC, Bröcker EB, Ruiter DJ and de Waal RM: Transition of horizontal to vertical growth phase melanoma is accompanied by induction of vascular endothelial growth factor expression and angiogenesis. Melanoma Res 7 (Suppl 2): S19-S26, 1997.
19. Bergers G and Hanahan D: Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 8: 592-603, 2008.
20. Potente M, Gerhardt H and Carmeliet P: Basic and therapeutic aspects of angiogenesis. Cell 146: 873-887, 2011.
21. Cunningham KG, Hutchinson SA, Manson W and Spring FS: Cordycepin, a metabolic product from cultures of C. militaris (Linn.) Link. Part I. Isolation and characterisation. J Chem Soc: 508: 2299-3200, 1951.
22. Song CH, Jeon YJ, Yang BK, Ra KS and Sung JM: Anti-complementary activity of exo-polymers produced from submerged mycelial cultures of higher fungi with particular reference to Cordyceps militaris. J Microbiol Biotechnol 8: 536-539, 1998.
23. Mizuno T: Medicinal effects and utilization of Cordyceps (Fr.) Link (Ascomycetes) and Isaria Fr. (Mitosporic Fungi) Chinese caterpillar fungi, 'Tochukaso' (Review). Int J Med Mushroom 1: 251-261, 1999.
24. Nag TB and Wang HX: Pharmacological actions of Cordyceps, a prized folk medicine. J Pharm Pharmacol 57: 1509-1519, 2005.
25. Das SK, Masuda M, Hatashita M, Sakurai A and Sakakibara M: A new approach for improving cordycepin productivity in surface liquid culture of C. militaris using high-energy ion beam irradiation. Lett Appl Microbiol 47: 534-538, 2008.
26. Das SK, Masuda M, Sakurai A and Sakakibara M: Medicinal uses of the mushroom Cordyceps militaris: current state and prospects. Fitoterapia 8: 961-968, 2010.
27. Sakaguchi M, Huh N and Namba M: A novel tumor suppressor, REIC/Dkk-3 gene identified by our in vitro transformation model of normal human fibroblasts works as a potent therapeutic anti-tumor agent. Adv Exp Med Biol 720: 209-215, 2012.
28. Das SK, Masuda M, Hatashita M, Sakurai A and Sakakibara M: Optimization of culture medium for cordycepin production using C. militaris mutant obtained by ion beam irradiation. Proc Biochem 45: 129-132, 2010.
29. Graupera M and Potente M: Regulation of angiogenesis by PI3K signaling networks. Exp Cell Res 319: 1348-1355, 2013.
30. Graupera M, Guillermet-Guibert J, Foukas LC, et al: Angiogenesis selectively requires the p110 alpha isoform of PI3K to control endothelial cell migration. Nature 453: 662-666, 2008.
31. Wang F, Yamauchi M, Muramatsu M, Osawa T, Tsuchid R and Shibuya M: MRACK1 regulates VEGF/Flt1-mediated cell migration via activation of a PI3K/Akt pathway. J Biol Chem 286: 9097-9106, 2011.
32. Zhao P, Meng Q, Liu LZ, You YP, Liu N and Jiang BH: Regulation of survivin by PI3K/Akt/p70S6K1 pathway. Biochem Biophys Res Commun 395: 219-224, 2010.
33. Maity A, Pore N, Lee J, Solomon D and O'Rourke DM: Epidermal growth factor receptor transcriptionally up-regulates vascular endothelial growth factor expression in human glioblastoma cells via a pathway involving phosphatidylinositol 3-kinase and distinct from that induced by hypoxia. Cancer Res 60: 5879-5886, 2000.
34. Zhong H, Chiles K, Feldse D, et al: Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol3- kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res 60: 1541-1545, 2000.
35. Karar J and Maity A: PI3K/AKT/mTOR pathway in angiogenesis. Front Mol Neurosci 4: 51, 2011.
36. Grimes CA and Jope RS: The multifaceted roles of glycogen synthase kinase 3β in cellular signaling. Prog Neurobiol 65: 391-426, 2001.
37. Forde JE and Dale TC: Glycogen synthase kinase 3: a key regulator of cellular fate. Cell Mol Life Sci 64: 1930-1944, 2007.
38. Rayasam GV, Tulasi VK, Sodhi R, Davis JA and Ray A: Glycogen synthase kinase 3: more than a namesake. Br J Pharmacol 156: 885-898, 2009.
39. Tekle C, Giovannetti E, Sigmond J, Graff JR, Smid K and Peters GJ: Molecular pathways involved in the synergistic interaction of the PKCβ inhibitor enzastaurin with the antifolate pemetrexed in non-small cell lung cancer cells. Br J Cancer 99: 750-759, 2008.
40. Graff JR, McNulty AM, Hanna KR, et al: The protein kinase Cbeta-selective inhibitor, Enzastaurin (LY317615.HCl), suppresses signaling through the AKT pathway, induces apoptosis, and suppresses growth of human colon cancer and glioblastoma xenografts. Cancer Res 65: 7462-7469, 2005.
41. Hanauske AR, Oberschmidt O, Hanauske-Abel H, Lahn MM and Eismann U: Antitumor activity of enzastaurin (LY317615.HCl) against human cancer cell lines and freshly explanted tumors investigated in in-vitro (corrected) soft-agar cloning experiments. Invest New Drugs 25: 205-210, 2007.
42. Lee KW, Kim SG, Kim HP, et al: Enzastaurin, a protein kinase C beta inhibitor, suppresses signaling through the ribosomal S6 kinase and bad pathways and induces apoptosis in human gastric cancer cells. Cancer Res 68: 1916-1926, 2008.
43. Manning BD and Cantley LC: AKT/PKB signaling: navigating downstream. Cell 129: 1261-1274, 2007.
44. Kandel ES and Hay N: The regulation and activities of the multi-functional serine/threonine kinase Akt/PKB. Exp Cell Res 253: 210-229, 1999.
45. Chen J, Somanath PR, Razorenova OV, Chen WS, Hay N, Bornstein P and Byzova TV: Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nature Med 11: 1188-1196, 2005.
46. Somanath PR, Razorenova OV, Chen J and Byzova TV: Akt1 in Endothelial cell and angiogenesis. Cell Cycle 5: 512-518, 2006.
47. Ruoslahti E and Engvall E: Integrins and vascular extracellular matrix assembly. J Clin Invest 99: 1149-1152, 1997.
48. Carmeliet P, Moons L, Luttun A, et al: Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7: 575-583, 2001.
49. Luangdilok S, Box C, Harrington K, Rhys-Evans P and Eccles S: MAPK and PI3K signalling differentially regulate angiogenic and lymphangiogenic cytokine secretion in squamous cellcarcinoma of the head and neck. Eur J Cancer 47: 520-529, 2011.
50. Kyriakis JM and Avruch J: Sounding the alarm: Protein kinase cascades activated by stress and inflammation. J Biol Chem 271: 24313-24316, 1996.
51. Conrad PW, Rust RT, Han J, Millhorn DE and Beitner-Johnson D: Selective activation of p38alpha and p38gamma by hypoxia. Role in regulation of cyclin D1 by hypoxia in PC12 cells. J Biol Chem 274: 23570-23576, 1999.
52. Lai WC, Zhou M, Shankavaram U, Peng G and Wahl LM: Differential regulation of lipopolysaccharide induced monocyte matrix metalloproteinase (MMP)-1 and MMP-9 by p38 and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinases. J Immunol 170: 6244-6249, 2003.
53. Xia Z, Dickens M, Raingeaud J, Davis RJ and Greenberg ME: Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326-1331, 1995.
54. De S, Razorenova O, McCabe NP, O'Toole T, Qin J and Byzova TV: VEGF-integrin interplay controls tumor growth and vascularization. Proc Natl Acad Sci USA 102: 7589-7594, 2005.
55. Franco CA, Liebner S and Gerhardt H: Vascular morphogenesis: a Wnt for every vessel? Curr Opin Genet Dev 19: 476-483, 2009.
56. Fischer C, Mazzone M, Jonckx B and Carmeliet P: FLT1 and its ligands VEGFB and PlGF: drug targets for anti-angiogenic therapy? Nature Rev Cancer 8: 942-956, 2008.