Melatonin suppresses tumor angiogenesis by inhibiting HIF-1α stabilization under hypoxia

Journal of Pineal Research

Volumn 48, Issue 2, 2010, Pages 178-184

  Park, Shi Young ^a   Jang, Won Jun ^a   Yi, Eui Yeun ^a   Jang, Ji Yeong ^a   Jung, Yunjin ^a   Jeong, Joo Won ^b   Kim, Yung Jin ^a  

^a Pusan National University   (South Korea)

^b Kyung Hee University Hospital   (South Korea)

Author keywords

Angiogenesis; Anti oxidant; HIF 1 ; Melatonin; ROS; VEGF

Indexed keywords

ANGIOGENESIS INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MELATONIN; REACTIVE OXYGEN METABOLITE; VASCULOTROPIN;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL STRAIN HCT116; COLON CANCER; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPOXIA; PINEAL BODY; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

ANTIOXIDANTS; CELL HYPOXIA; CELLS, CULTURED; COLONIC NEOPLASMS; CULTURE MEDIA, CONDITIONED; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MELATONIN; NEOVASCULARIZATION, PATHOLOGIC; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 75149158379     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2009.00742.x     Document Type: Article

References (43)

1. Vaupel P. The role of hypoxia-induced factors in tumor progression. Oncologist 2004 9 (Suppl. 5 10 17.
2. Ryan HE, Poloni M, Mcnulty W et al. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res 2000 60 : 4010 4015.
3. Greco O, Marples B, Joiner MC et al. How to overcome (and exploit) tumor hypoxia for targeted gene therapy. J Cell Physiol 2003 197 : 312 325.
4. Brizel DM, Scully SP, Harrelson JM et al. Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res 1996 56 : 941 943.
5. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev 2003 3 : 401 410.
6. Jeong JW, Bae MK, Ahn MY et al. Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation. Cell 2002 111 : 709 720.
7. Melillo G. Targeting hypoxia cell signaling for cancer therapy. Cancer Metastasis Rev 2007 26 : 341 352.
8. Reiter RJ. Melatonin: the chemical expression of darkness. Mol Cell Endocrinol 1991 79 : C153 C158.
9. Hardeland R, Tan DX, Reiter RJ. Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J Pineal Res 2009 47 : 109 126.
10. Simko F, Pechanova O. Potential roles of melatonin and chronotherapy among the new trends in hypertension treatment. J Pineal Res 2009 47 : 127 133.
11. Veneroso C, Tunon MJ, Gonzalez-Gallego J et al. Melatonin reduces cardiac inflammatory injury induced by acute exercise. J Pineal Res 2009 47 : 184 191.
12. Nosjean O, Nicolas JP, Klupsch F et al. Comparative pharmacological studies of melatonin receptors: MT1, MT2 and MT3/QR2. Tissue distribution of MT3/QR2. Biochem Pharmacol 2001 61 : 1369 1379.
13. Reiter RJ, Paredes SD, Manchester LC et al. Reducing oxidative/ nitrosative stress: a newly-discovered genre for melatonin. Crit Rev Biochem Mol Biol 2009 44 : 175 200.
14. Peyrot F, Ducrocq C. Potential role of tryptophan derivatives in stress responses characterized by the generation of reactive oxygen and nitrogen species. J Pineal Res 2008 45 : 235 246.
15. Vijayalaxmi, Thomas CR Jr., Reiter RJ et al. Melatonin: from basic research to cancer treatment clinics. J Clin Oncol 2002 20 : 2575 2601.
16. Kivela A, Kauppila A, Ylostalo P et al. Seasonal, menstrual and circadian secretions of melatonin, gonadotropins and prolactin in women. Acta Physiol Scand 1988 132 : 321 327.
17. Ravindra T, Lakshmi NK, Ahuja YR. Melatonin in pathogenesis and therapy of cancer. Indian J Med Sci 2006 60 : 523 535.
18. Reiter RJ. Mechanisms of cancer inhibition by melatonin. J Pineal Res 2004 37 : 213 214.
19. Jung B, Ahmad N. Melatonin in cancer management: progress and promise. Cancer Res 2006 66 : 9789 9793.
20. Kaur C, Sivakumar V, Lu J et al. Increased vascular permeability and nitric oxide production in response to hypoxia in the pineal gland. J Pineal Res 2007 42 : 338 349.
21. Liao D, Johnson RS. Hypoxia: a key regulator of angiogenesis in cancer. Cancer Metastasis Rev 2007 26 : 281 290.
22. Forsythe JA, Jiang BH, Iyer NV et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996 16 : 4604 4613.
23. Ivan M, Kondo K, Yang H et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science (New York, NY) 2001 292 : 464 468.
24. Jaakkola P, Mole DR, Tian YM et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science (New York, NY) 2001 292 : 468 472.
25. Callapina M, Zhou J, Schmid T et al. NO restores HIF-1alpha hydroxylation during hypoxia: role of reactive oxygen species. Free Radic Biol Med 2005 39 : 925 936.
26. Qutub AA, Popel AS. Reactive oxygen species regulate hypoxia-inducible factor 1alpha differentially in cancer and ischemia. Mol Cell Biol 2008 28 : 5106 5119.
27. Koga F, Kihara K, Neckers L. Inhibition of cancer invasion and metastasis by targeting the molecular chaperone heat-shock protein 90. Anticancer Res 2009 29 : 797 807.
28. Yeo EJ, Chun YS, Park JW. New anticancer strategies targeting HIF-1. Biochem Pharmacol 2004 68 : 1061 1069.
29. Kizaka-Kondoh S, Tanaka S, Harada H et al. The HIF-1-active microenvironment: an environmental target for cancer therapy. Adv Drug Deliv Rev 2009 61 : 623 632.
30. Lerner A, Case J, Takahasi Y. Isolation of melatonin, a pineal gland factor that lightens melanocytes. J Am Chem Soc 1958 80 : 2587.
31. Gomez-Corvera A, Cerrillo I, Molinero P et al. Evidence of immune system melatonin production by two pineal melatonin deficient mice, C57BL/6 and Swiss strains. J Pineal Res 2009 47 : 15 22.
32. Konturek SJ, Konturek PC, Brzozowska I et al. Localization and biological activities of melatonin in intact and diseased gastrointestinal tract (GIT). J Physiol Pharmacol 2007 58 : 381 405.
33. Sakotnik A, Liebmann PM, Stoschitzky K et al. Decreased melatonin synthesis in patients with coronary artery disease. Eur Heart J 1999 20 : 1314 1317.
34. Cui P, Luo Z, Zhang H et al. Effect and mechanism of melatonin's action on the proliferation of human umbilical vein endothelial cells. J Pineal Res 2006 41 : 358 362.
35. Roskoski R Jr. Vascular endothelial growth factor (VEGF) signaling in tumor progression. Crit Rev Oncol Hematol 2007 62 : 179 213.
36. Guba M, Seeliger H, Kleespies A et al. Vascular endothelial growth factor in colorectal cancer. Int J Colorectal Dis 2004 19 : 510 517. (Pubitemid 39445405)
37. Dai M, Cui P, Yu M et al. Melatonin modulates the expression of VEGF and HIF-1 alpha induced by CoCl2 in cultured cancer cells. J Pineal Res 2008 44 : 121 126.
38. Cockman ME, Masson N, Mole DR et al. Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem 2000 275 : 25733 25741. (Pubitemid 30687077)
39. Brunelle JK, Bell EL, Quesada NM et al. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab 2005 1 : 409 414.
40. Guzy RD, Hoyos B, Robin E et al. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 2005 1 : 401 408.
41. Mansfield KD, Guzy RD, Pan Y et al. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab 2005 1 : 393 399.
42. Chandel NS, Maltepe E, Goldwasser E et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA 1998 95 : 11715 11720.
43. Park JW, Hwang MS, Suh SI et al. Melatonin down-regulates HIF-1 alpha expression through inhibition of protein translation in prostate cancer cells. J Pineal Res 2009 46 : 415 421.