Melatonin reduces endothelin-1 expression and secretion in colon cancer cells through the inactivation of FoxO-1 and NF-κβ

Journal of Pineal Research

Volumn 56, Issue 4, 2014, Pages 415-426

  León, Josefa ^a,b   Casado, Jorge ^a   Jiménez Ruiz, Sergio M ^a   Zurita, María Sol ^a   González Puga, Cristina ^a   Rejón, Juan D ^c   Gila, Ana ^b   Muñoz De Rueda, Paloma ^a,b   Pavón, Esther J ^a   Reiter, Russel J ^d   Ruiz Extremera, Angela ^b   Salmerón, Javier ^b  

^a HOSPITAL UNIVERSITARIO SAN CECILIO   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c Andalusian Public Health System Biobank   (Spain)

^d UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

colorectal cancer; endothelin 1; FoxO 1; melatonin; NF

Indexed keywords

ACETYLSEROTONIN METHYLTRANSFERASE; ARALKYLAMINE ACETYLTRANSFERASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENDOTHELIN 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MELATONIN; MESSENGER RNA; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR FKHR; TRYPTOPHAN; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, HUMAN; PROTEIN KINASE B; RNA;

ANGIOGENESIS; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CELL PROTECTION; COLON CARCINOMA; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; EDN 1 GENE; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SECRETION; TUMOR GROWTH; BIOSYNTHESIS; CACO 2 CELL LINE; COLON TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY;

BASE SEQUENCE; CACO-2 CELLS; COLONIC NEOPLASMS; ENDOTHELIN-1; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELATONIN; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; RNA, NEOPLASM;

EID: 84898941204     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12131     Document Type: Article

References (54)

1. Kedzierski RM, Yanagisawa M,. Endothelin system: the double-edged sword in health and disease. Annu Rev Pharmacol Toxicol 2001; 41: 851-876.
2. Sumitomo M, Shen R, Nanus DM,. Involvement of neutral endopeptidase in neoplastic progression. Biochim Biophys Acta 2005; 1751: 52-59.
3. Stow LR, Jacobs ME, Wingo CS, et al. Endothelin-1 gene regulation. FASEB J 2011; 25: 16-28.
4. Welch AK, Jacobs ME, Wingo CS, et al. Early progress in epigenetic regulation of endothelin pathway genes. Br J Pharmacol 2013; 168: 327-334.
5. Jacobs ME, Wingo CS, Cain BD,. An emerging role for microRNA in the regulation of endothelin-1. Front Physiol 2013; 4: 22-28.
6. Rosanò L, Spinella F, Bagnato A,. Endothelin 1 in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2013; 13: 637-651.
7. Kim TH, Xiong H, Zhang Z, et al. Beta-Catenin activates the growth factor endothelin-1 in colon cancer cells. Oncogene 2005; 24: 597-604.
8. Ali H, Loizidou M, Dashwood M, et al. Stimulation of colorectal cancer cell line growth by ET-1 and its inhibition by ET(A) antagonists. Gut 2000; 47: 685-688.
9. Eberl LP, Egidy G, Pinet F, et al. Endothelin receptor blockade potentiates FasL-induced apoptosis in colon carcinoma cells via the protein kinase C-pathway. J Cardiovasc Pharmacol 2000; 36: 354-356.
10. Ali H, Dashwood M, Dawas K, et al. Endothelin receptor expression in colorectal cancer. J Cardiovasc Pharmacol 2000; 36: S69-S71.
11. Egidy G, Juillerat-Jeanneret L, Jeannin JF, et al. Modulation of human colon tumor-stromal interactions by the endothelin system. Am J Pathol 2000; 157: 1863-1874.
12. Asham E, Shankar A, Loizidou M, et al. Increased endothelin-1 in colorectal cancer and reduction of tumor growth by ET(A) receptor antagonism. Br J Cancer 2001; 85: 1759-1763.
13. Arun C, Swift B, Porter KE, et al. The role of big endothelin-1 in colorectal cancer. Int J Biol Markers 2002; 17: 268-274.
14. 125I]iodomelatonin binding sites in the human colon. Endocr Res 1996; 22: 77-94.
15. Vician M, Zeman M, Herichová I, et al. Melatonin content in plasma and large intestine of patients with colorectal carcinoma before and after surgery. J Pineal Res 1999; 27: 164-169.
16. Alvarez-García V, González A, Alonso-González C, et al. Melatonin interferes in the desmoplastic reaction in breast cancer by regulating cytokine production. J Pineal Res 2012; 52: 282-290.
17. Uguz AC, Cig B, Espino J, et al. Melatonin potentiates chemotherapy-induced cytotoxicity and apoptosis in rat pancreatic tumor cells. J Pineal Res 2012; 53: 91-98.
18. Sánchez-Hidalgo M, Lee M, de la Lastra CA, et al. Melatonin inhibits cell proliferation and induces caspase activation and apoptosis in human malignant lymphoid cell lines. J Pineal Res 2012; 53: 366-373.
19. Mediavilla MD, Sanchez-Barcelo EJ, Tan DX, et al. Basic mechanisms involved in the anti-cancer effects of melatonin. Curr Med Chem 2010; 17: 4462-4481.
20. Granzotto M, Rapozzi V, Decorti G, et al. Effects of melatonin on doxorubicin cytotoxicity in sensitive and pleiotropically resistant tumor cells. J Pineal Res 2001; 31: 206-213.
21. Cerea G, Vaghi M, Ardizzoia A, et al. Biomodulation of cancer chemotherapy for metastatic colorectal cancer: a randomized study of weekly low-dose irinotecan alone versus irinotecan plus the oncostatic pineal hormone melatonin in metastatic colorectal cancer patients progressing on 5-fluorouracil-containing combinations. Anticancer Res 2003; 23: 1951-1954.
22. Jung B, Ahmad N,. Melatonin in cancer management: progress and promise. Cancer Res 2006; 66: 9789-9793.
23. Kilic E, Kilic U, Reiter RJ, et al. Prophylactic use of melatonin protects against focal cerebral ischemia in mice: role of endothelin converting enzyme-1. J Pineal Res 2004; 37: 247-251.
24. Rodella LF, Favero G, Rossini C, et al. Aging and vascular dysfunction: beneficial melatonin effects. Age (Dordr) 2013; 35: 103-115.
25. Reiter RJ,. Mechanisms of cancer inhibition by melatonin. J Pineal Res 2004; 37: 213-214.
26. Patterson C, Perrella MA, Hsieh CM, et al. Cloning and functional analysis of the promoter for KDR/flk-1, a receptor for vascular endothelial growth factor. J Biol Chem 1995; 270: 23111-23118.
27. Granchi S, Brocchi S, Bonaccorsi L, et al. Endothelin-1 production by prostate cancer cell lines is up-regulated by factors involved in cancer progression and down-regulated by androgens. Prostate 2001; 49: 267-277.
28. Tajes Orduña M, Pelegrí Gabalda C, Vilaplana Hortensi J, et al. An evaluation of the neuroprotective effects of melatonin in an in vitro experimental model of age-induced neuronal apoptosis. J Pineal Res 2009; 46: 262-267.
29. Accili D, Arden KC,. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 2004; 117: 421-426.
30. Park J, Leong ML, Buse P, et al. Serum and glucocorticoid-inducible kinase (SGK) is a target of the PI3-kinase-stimulated signalling pathway. EMBO J 1999; 18: 3024-3033.
31. Lee JW, Chen H, Pullikotil P, et al. Protein kinase A-alpha directly phosphorylates FoxO1 in vascular endothelial cells to regulate expression of vascular cellular adhesion molecule-1 mRNA. J Biol Chem 2011; 286: 6423-6432.
32. Brandvold KR, Steffey ME, Fox CC, et al. Development of a highly selective c-Src kinase inhibitor. ACS Chem Biol 2012; 7: 1393-1398.
33. Zhang S, Yu D,. Targeting Src family kinases in anti-cancer therapies: turning promise into triumph. Trends Pharmacol Sci 2012; 33: 122-128.
34. Huang H, Tindall DJ,. Regulation of FOXO protein stability via ubiquitination and proteasome degradation. Biochim Biophys Acta 2011; 1813: 1961-1964.
35. Fredriksson JM, Lindquist JM, Bronnikov GE, et al. Norepinephrine induces vascular endothelial growth factor gene expression in brown adipocytes through a beta-adrenoreceptor/cAMP/protein kinase A pathway involving Src but independently of Erk1/2. J Biol Chem 2000; 275: 13802-13811.
36. Martín V, Herrera F, Carrera-Gonzalez P, et al. Intracellular signaling pathways involved in the cell growth inhibition of glioma cells by melatonin. Cancer Res 2006; 66: 1081-1088.
37. Luchetti F, Canonico B, Betti M, et al. Melatonin signaling and cell protection function. FASEB J 2010; 24: 3603-3624.
38. Zhang H, Zhang S, He H, et al. RasGAP-derived peptide 38GAP potentiates the cytotoxicity of cisplatin through inhibitions of Akt, ERK and NF-κB in colon carcinoma HCT116 cells. Cancer Lett 2011; 308: 62-70.
39. Martín V, Herrera F, García-Santos G, et al. Involvement of protein kinase C in melatonin's oncostatic effect in C6 glioma cells. J Pineal Res 2007; 43: 239-244.
40. Cui P, Yu M, Luo Z, et al. Intracellular signaling pathways involved in cell growth inhibition of human umbilical vein endothelial cells by melatonin. J Pineal Res 2008; 44: 107-114.
41. León J, Casado J, Carazo A, et al. Gender-related invasion differences associated with mRNA expression levels of melatonin membrane receptors in colorectal cancer. Mol Carcinog 2012; 51: 608-618.
42. Knowles JP, Shi-Wen X, Haque SU, et al. Endothelin-1 stimulates colon cancer adjacent fibroblasts. Int J Cancer 2012; 130: 1264-1272.
43. Nie S, Zhou J, Bai F, et al. Role of endothelin a receptor in colon cancer metastasis: in vitro and in vivo evidence. Mol Carcinog 2013; 53: E85-E91.
44. Casado-Zapico S, Rodriguez-Blanco J, García-Santos G, et al. Synergistic antitumor effect of melatonin with several chemotherapeutic drugs on human Ewing sarcoma cancer cells: potentiation of the extrinsic apoptotic pathway. J Pineal Res 2010; 48: 72-80.
45. Wang J, Guo W, Chen W, et al. Melatonin potentiates the antiproliferative and pro-apoptotic effects of ursolic acid in colon cancer cells by modulating multiple signaling pathways. J Pineal Res 2013; 54: 406-416.
46. Galano A, Tan DX, Reiter RJ,. On the free radical scavenging activities of melatonin's metabolites, AFMK and AMK. J Pineal Res 2013; 54: 245-257.
47. Mauriz JL, Collado PS, Veneroso C, et al. A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J Pineal Res 2013; 54: 1-14.
48. García-Navarro A, González-Puga C, Escames G, et al. Cellular mechanisms involved in the melatonin inhibition of HT-29 human colon cancer cell proliferation in culture. J Pineal Res 2007; 43: 195-205.
49. Santoro R, Marani M, Blandino G, et al. Melatonin triggers p53Ser phosphorylation and prevents DNA damage accumulation. Oncogene 2012; 31: 2931-2942.
50. Turner AJ, Barnes K, Schweizer A, et al. Isoforms of endothelin- converting enzyme: why and where? Trends Pharmacol Sci 1998; 19: 483-486.
51. Kawanabe Y, Nauli SM,. Endothelin. Cell Mol Life Sci 2011; 68: 195-203.
52. Yanagisawa H, Hammer RE, Richardson JA, et al. Disruption of ECE-1 and ECE-2 reveals a role for endothelin-converting enzyme-2 in murine cardiac development. J Clin Invest 2000; 105: 1373-1382.
53. Yanagisawa H, Yanagisawa M, Kapur RP, et al. Dual genetic pathways of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene. Development 1998; 125: 825-836.
54. Ling L, Maguire JJ, Davenport AP,. Endothelin-2, the forgotten isoform: emerging role in the cardiovascular system, ovarian development, immunology and cancer. Br J Pharmacol 2013; 168: 283-295.