Magnolol inhibits angiogenesis by regulating ROS-mediated apoptosis and the PI3K/AKT/mTOR signaling pathway in mES/EB-derived endothelial-like cells

International Journal of Oncology

Volumn 43, Issue 2, 2013, Pages 600-610

  Kim, Gi Dae ^a   Oh, Jedo ^a   Park, Hyen Joo ^a   Bae, Kihwan ^b   Lee, Sang Kook ^a  

^a Seoul National University   (South Korea)

^b Chungnam National University   (South Korea)

Author keywords

Anti angiogenesis; Magnolol; Mouse embryonic stem cells; PI3K AKT mTOR; Platelet endothelial cell adhesion molecule

Indexed keywords

ACETYLCYSTEINE; CASPASE 3; LIPOCORTIN 5; MAGNOLOL; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; EMBRYOID BODY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; ENZYME ACTIVATION; INTRACELLULAR SIGNALING; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACETYLCYSTEINE; ANGIOGENESIS INHIBITORS; ANIMALS; ANTIGENS, CD31; APOPTOSIS; BIPHENYL COMPOUNDS; CASPASE 3; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIGNANS; MAP KINASE SIGNALING SYSTEM; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE SYNTHASE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; TOR SERINE-THREONINE KINASES;

EID: 84879658969     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2013.1959     Document Type: Article

References (47)

1. Carmeliet P and Jain RK: Molecular mechanisms and clinical applications of angiogenesis. Nature 473: 298-307, 2011.
2. Holderfield MT and Hughes CC: Crosstalk between vascular endothelial growth factor, notch and transforming growth factor-beta in vascular morphogenesis. Circ Res 102: 637-652, 2008. (Pubitemid 351457853)
3. Volz KS, Miljan E, Khoo A and Cooke JP: Development of pluripotent stem cells for vascular therapy. Vascul Pharmacol 56: 288-296, 2012.
4. Xu Z, Fang S, Zuo Y, et al: Combination of pigment epithelium-derived factor with radiotherapy enhances the antitumor effects on nasopharyngeal carcinoma by downregulating vascular endothelial growth factor expression and angiogenesis. Cancer Sci 102: 1789-1798, 2011.
5. Sauer H, Gunther J, Hescheler J and Wartenberg M: Thalidomide inhibits angiogenesis in embryoid bodies by the generation of hydroxyl radicals. Am J Pathol 156: 151-158, 2000. (Pubitemid 30644447)
6. Abid MR, Kachra Z, Spokes KC and Aird WC: NADPH oxidase activity is required for endothelial cell proliferation and migration. FEBS Lett 486: 252-256, 2000.
7. van Wetering S, van Buul JD, Quik S, et al: Reactive oxygen species mediate Rac-induced loss of cell-cell adhesion in primary human endothelial cells. J Cell Sci 115: 1837-1846, 2002. (Pubitemid 34567245)
8. Turrens JF: Mitochondrial formation of reactive oxygen species. J Physiol 552: 335-344, 2003.
9. Yap TA, Garrett MD, Walton MI, Raynaud F, de Bono JS and Workman P: Targeting the PI3K-AKT-mTOR pathway: progress, pitfalls and promises. Curr Opin Pharmacol 8: 393-412, 2008.
10. McCubrey JA, Lahair MM and Franklin RA: Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 8: 1775-1789, 2006. (Pubitemid 44726351)
11. El-Najjar N, Chatila M, Moukadem H, et al: Reactive oxygen species mediate thymoquinone-induced apoptosis and activate ERK and JNK signaling. Apoptosis 15: 183-195, 2010.
12. Risau W, Sariola H, Zerwes HG, et al: Vasculogenesis and angiogenesis in embryonic-stem-cell-derived embryoid bodies. Development 102: 471-478, 1988. (Pubitemid 18084930)
13. Wang R, Clark R and Bautch VL: Embryonic stem cellderived cystic embryoid bodies form vascular channels: an in vitro model of blood vessel development. Development 114: 303-316, 1992.
14. Li X and Claesson-Welsh L: Embryonic stem cell models in vascular biology. J Thromb Haemost (Suppl) 1: 53-56, 2009.
15. Descamps B and Emanueli C: Vascular differentiation from embryonic stem cells: novel technologies and therapeutic promises. Vascul Pharmacol 56: 267-279, 2012.
16. Kawamura H, Li X, Goishi K, et al: Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization. Blood 112: 3638-3649, 2008.
17. Han HJ, Heo JS and Lee YJ: Estradiol-17beta stimulates proliferation of mouse embryonic stem cells: involvement of MAPKs and CDKs as well as protooncogenes. Am J Physiol Cell Physiol 290: C1067-C1075, 2006.
18. Heo JS, Lee YJ and Han HJ: EGF stimulates proliferation of mouse embryonic stem cells: involvement of Ca2+ influx and p44/42 MAPKs. Am J Physiol Cell Physiol 290: C123-C133, 2006.
19. Kim GD, Rhee GS, Chung HM, Chee KM and Kim GJ: Cytotoxicity of 5-fluorouracil: effect on endothelial differentiation via cell cycle inhibition in mouse embryonic stem cells. Toxicol In Vitro 23: 719-727, 2009.
20. Kim GD, Bae SY, Park HJ, Bae K and Lee SK: Honokiol inhibits vascular vessel formation of mouse embryonic stem cell-derived endothelial cells via the suppression of PECAM and MAPK/mTOR signaling pathway. Cell Physiol Biochem 30: 758-770, 2012.
21. Ho JW and Jie M: Pharmacological activity of cardiovascular agents from herbal medicine. Cardiovasc Hematol Agents Med Chem 5: 273-277, 2007. (Pubitemid 47595737)
22. Amblard F, Govindarajan B, Lefkove B, et al: Synthesis, cytotoxicity and antiviral activities of new neolignans related to honokiol and magnolol. Bioorg Med Chem Lett 17: 4428-4431, 2007. (Pubitemid 47058969)
23. Park J, Lee J, Jung E, et al: In vitro antibacterial and antiinflammatory effects of honokiol and magnolol against Propionibacterium sp. Eur J Pharmacol 496: 189-195, 2004. (Pubitemid 39024332)
24. Tsai YC, Cheng PY, Kung CW, et al: Beneficial effects of magnolol in a rodent model of endotoxin shock. Eur J Pharmacol 641: 67-73, 2010.
25. Park JB, Lee MS, Cha EY, et al: Magnolol-induced apoptosis in HCT-116 colon cancer cells is associated with the AMP-activated protein kinase signaling pathway. Biol Pharm Bull 35: 1614-1620, 2012.
26. Chuang TC, Hsu SC, Cheng YT, et al: Magnolol down-regulates HER2 gene expression, leading to inhibition of HER2-mediated metastatic potential in ovarian cancer cells. Cancer Lett 311: 11-19, 2011.
27. Lin SY, Liu JD, Chang HC, Yeh SD, Lin CH and Lee WS: Magnolol suppresses proliferation of cultured human colon and liver cancer cells by inhibiting DNA synthesis and activating apoptosis. J Cell Biochem 84: 532-544, 2002. (Pubitemid 34111187)
28. Park EJ, Zhao YZ, Na M, et al: Protective effects of honokiol and magnolol on tertiary butyl hydroperoxide- or D-galactosamine-induced toxicity in rat primary hepatocytes. Planta Med 69: 33-37, 2003. (Pubitemid 36228454)
29. Heuer J, Bremer S, Pohl I and Spielmann H: Development of an in vitro embryotoxicity test using murine embryonic stem cell cultures. Toxicol In Vitro 7: 551-556, 1993.
30. Scholz G, Pohl I, Genschow E, Klemm M and Spielmann H: Embryotoxicity screening using embryonic stem cells in vitro: correlation to in vivo teratogenicity. Cells Tissues Organs 165: 203-211, 1999.
31. Jakobsson L, Kreuger J, Holmborn K, et al: Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev Cell 10: 625-634, 2006.
32. Newman PJ: The biology of PECAM-1. J Clin Invest 99: 3-8, 1997.
33. Sauer H, Rahimi G, Hescheler J and Wartenberg M: Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells. J Cell Biochem 75: 710-723, 1999. (Pubitemid 29529925)
34. Sauer H and Wartenberg M: Reactive oxygen species as signaling molecules in cardiovascular differentiation of embryonic stem cells and tumor-induced angiogenesis. Antioxid Redox Signal 7: 1423-1434, 2005. (Pubitemid 41767977)
35. Karar J and Maity A: PI3K/AKT/mTOR pathway in angiogenesis. Front Mol Neurosci 4: 51, 2011.
36. Olsson AK, Dimberg A, Kreuger J and Claesson-Welsh L: VEGF receptor signalling-in control of vascular function. Nat Rev Mol Cell Biol 7: 359-371, 2006.
37. Sato Y: The vasohibin family: a novel family for angiogenesis regulation. J Biochem 153: 5-11, 2013.
38. Frampton JE: Ranibizumab: in diabetic macular oedema. Drugs 72: 509-523, 2012.
39. Hong SW, Jung KH, Lee HS, et al: SB365 inhibits angiogenesis and induces apoptosis of hepatocellular carcinoma through modulation of PI3K/Akt/mTOR signaling pathway. Cancer Sci 103: 1929-1937, 2012.
40. Hong SW, Jung KH, Lee HS, et al: Apoptotic and anti-angiogenic effects of Pulsatilla koreana extract on hepatocellular carcinoma. Int J Oncol 40: 452-460, 2012.
41. Nishikawa T, Tsuno NH, Okaji Y, et al: The inhibition of autophagy potentiates anti-angiogenic effects of sulforaphane by inducing apoptosis. Angiogenesis 13: 227-238, 2010.
42. Xu HL, Tang W, Du GH and Kokudo N: Targeting apoptosis pathways in cancer with magnolol and honokiol, bioactive constituents of the bark of Magnolia officinalis. Drug Discov Ther 5: 202-210, 2011.
43. Simon HU, Haj-Yehia A and Levi-Schaffer F: Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5: 415-418, 2000. (Pubitemid 32162623)
44. 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.
45. McCubrey JA, Steelman LS, Chappell WH, et al: Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 1773: 1263-1284, 2007. (Pubitemid 47125967)
46. Cho DH, Choi YJ, Jo SA, et al: Troglitazone acutely inhibits protein synthesis in endothelial cells via a novel mechanism involving protein phosphatase 2A-dependent p70 S6 kinase inhibition. Am J Physiol Cell Physiol 291: C317-C326, 2006.
47. Manning BD and Cantley LC: AKT/PKB signaling: navigating downstream. Cell 129: 1261-1274, 2007. (Pubitemid 46962095)