Melatonin inhibits TPA-induced oral cancer cell migration by suppressing matrix metalloproteinase-9 activation through the histone acetylation

Oncotarget

Volumn 7, Issue 16, 2016, Pages 21952-21967

  Yeh, Chia Ming ^a   Lin, Chiao Wen ^a,b   Yang, Jia Sin ^a,b   Yang, Wei En ^a,b   Su, Shih Chi ^c   Yang, Shun Fa ^a,b  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

CREBBP; EP300; Melatonin; MMP; Oral cancer

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; E1A ASSOCIATED P300 PROTEIN; GELATINASE B; MELATONIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; PHORBOL 13 ACETATE 12 MYRISTATE; ANTINEOPLASTIC AGENT; ANTIOXIDANT; HISTONE; MMP9 PROTEIN, HUMAN;

ARTICLE; CANCER TISSUE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REPRESSION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; METASTASIS INHIBITION; MOUTH CANCER; ORAL CANCER CELL LINE; PHOSPHORYLATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ZYMOGRAPHY; ACETYLATION; CELL MOTION; DRUG EFFECTS; ENZYME ACTIVATION; METABOLISM; MOUTH TUMOR; PATHOLOGY; TUMOR CELL LINE;

ACETYLATION; ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME ACTIVATION; HISTONES; HUMANS; MATRIX METALLOPROTEINASE 9; MELATONIN; MOUTH NEOPLASMS;

EID: 84965048047     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8009     Document Type: Article

References (61)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin. 2009; 59:225-249.
2. Ichikawa Y, Ishikawa T, Tanaka K, Togo S, Shimada H. [Extracellular matrix degradation enzymes: important factors in liver metastasis of colorectal cancer and good targets for anticancer metastatic therapy]. Nihon Geka Gakkai Zasshi. 2001; 102:376-380.
3. Lin CW, Chou YE, Chiou HL, Chen MK, Yang WE, Hsieh MJ, Yang SF. Pterostilbene suppresses oral cancer cell invasion by inhibiting MMP-2 expression. Expert Opin Ther Targets. 2014; 18:1109-1120.
4. Weng CJ, Chen MK, Lin CW, Chung TT, Yang SF. Single nucleotide polymorphisms and haplotypes of MMP-14 are associated with the risk and pathological development of oral cancer. Ann Surg Oncol. 2012; 19:S319-327.
5. Yang SF, Lee WJ, Tan P, Tang CH, Hsiao M, Hsieh FK, Chien MH. Upregulation of miR-328 and inhibition of CREBDNA-binding activity are critical for resveratrol-mediated suppression of matrix metalloproteinase-2 and subsequent metastatic ability in human osteosarcomas. Oncotarget. 2015; 6:2736-2753. doi: 10.18632/oncotarget.3088.
6. Gao ZB, Duan YQ, Zhang L, Chen DW, Ding PT. Expression of matrix metalloproteinase 2 and its tissue inhibitor in oral squamous cell carcinoma. Int J Mol Med. 2005; 16:599-603.
7. Shah FD, Shukla SN, Shah PM, Shukla HK, Patel PS. Clinical significance of matrix metalloproteinase 2 and 9 in breast cancer. Indian J Cancer. 2009; 46: 194-202.
8. LotfiA, Mohammadi G, Saniee L, Mousaviagdas M, Chavoshi H, Tavassoli A. Serum Level of Matrix Metalloproteinase-2 and-9 in Patients with Laryngeal Squamous Cell Carcinoma and Clinical Significance. Asian Pac J Cancer Prev. 2015; 16:6749-6751.
9. Chien MH, Lin CW, Cheng CW, Wen YC, Yang SF. Matrix metalloproteinase-2 as a target for head and neck cancer therapy. Expert Opin Ther Targets. 2013; 17:203-216.
10. Chao R, Chow JM, Hsieh YH, Chen CK, Lee WJ, Hsieh FK, Yu NY, Chou MC, Cheng CW, Yang SF, Chien MH. Tricetin suppresses the migration/invasion of human glioblastoma multiforme cells by inhibiting matrix metalloproteinase-2 through modulation of the expression and transcriptional activity of specificity protein 1. Expert Opin Ther Targets. 2015; 19:1293-1306.
11. Chien SY, Hsieh MJ, Chen CJ, Yang SF, Chen MK. Nobiletin inhibits invasion and migration of human nasopharyngeal carcinoma cell lines by involving ERK1/2 and transcriptional inhibition of MMP-2. Expert Opin Ther Targets. 2015; 19:307-320.
12. Lin CW, Chen PN, Chen MK, Yang WE, Tang CH, Yang SF, Hsieh YS. Kaempferol reduces matrix metalloproteinase-2 expression by down-regulating ERK1/2 and the activator protein-1 signaling pathways in oral cancer cells. PLoS One. 2013; 8:e80883.
13. Lin FY, Hsieh YH, Yang SF, Chen CT, Tang CH, Chou MY, Chuang YT, Lin CW, Chen MK. Resveratrol suppresses TPA-induced matrix metalloproteinase-9 expression through the inhibition of MAPK pathways in oral cancer cells. J Oral Pathol Med. 2015; 44:699-706.
14. Acuna-Castroviejo D, Escames G, Venegas C, Diaz-Casado ME, Lima-Cabello E, Lopez LC, Rosales-Corral S, Tan DX, Reiter RJ. Extrapineal melatonin: sources, regulation, and potential functions. Cell Mol Life Sci. 2014; 71:2997-3025.
15. Calvo JR, Gonzalez-Yanes C, Maldonado MD. The role of melatonin in the cells of the innate immunity: a review. J Pineal Res. 2013; 55:103-120.
16. Zhang HM, Zhang Y. Melatonin: a well-documented antioxidant with conditional pro-oxidant actions. J Pineal Res. 2014; 57:131-146.
17. Manchester LC, Coto-Montes A, Boga JA, Andersen LP, Zhou Z, Galano A, Vriend J, Tan DX, Reiter RJ. Melatonin: an ancient molecule that makes oxygen metabolically tolerable. J Pineal Res. 2015; 59:403-419.
18. Loureiro R, Magalhaes-Novais S, Mesquita KA, Baldeiras I, Sousa IS, Tavares LC, Barbosa IA, Oliveira PJ, Vega-Naredo I. Melatonin antiproliferative effects require active mitochondrial function in embryonal carcinoma cells. Oncotarget. 2015; 6:17081-17096. doi: 10.18632/oncotarget.4012.
19. Vriend J, Reiter RJ. Breast cancer cells: Modulation by melatonin and the ubiquitin-proteasome system-a review. Mol Cell Endocrinol. 2015; 417:1-9.
20. Reiter RJ, Rosales-Corral SA, Liu XY, Acuna-Castroviejo D, Escames G, Tan DX. Melatonin in the oral cavity: physiological and pathological implications. J Periodontal Res. 2015; 50:9-17.
21. Mao L, Dauchy RT, Blask DE, Slakey LM, Xiang S, Yuan L, Dauchy EM, Shan B, Brainard GC, Hanifin JP, Frasch T, Duplessis TT, Hill SM. Circadian gating of epithelialto-mesenchymal transition in breast cancer cells via melatonin-regulation of GSK3beta. Mol Endocrinol. 2012; 26:1808-1820.
22. Jardim-Perassi BV, Arbab AS, Ferreira LC, Borin TF, Varma NR, Iskander AS, Shankar A, Ali MM, de Campos Zuccari DA. Effect of melatonin on tumor growth and angiogenesis in xenograft model of breast cancer. PLoS One. 2014; 9:e85311.
23. Wang Z, Dabrosin C, Yin X, Fuster MM, Arreola A, Rathmell WK, Generali D, Nagaraju GP, El-Rayes B, Ribatti D, Chen YC, Honoki K, Fujii H, et al. Broad targeting of angiogenesis for cancer prevention and therapy. Semin Cancer Biol. 2015; in press.
24. Swarnakar S, Paul S, Singh LP, Reiter RJ. Matrix metalloproteinases in health and disease: regulation by melatonin. J Pineal Res. 2011; 50:8-20.
25. Rudra DS, Pal U, Maiti NC, Reiter RJ, Swarnakar S. Melatonin inhibits matrix metalloproteinase-9 activity by binding to its active site. J Pineal Res. 2013; 54:398-405.
26. Zhang Y, Liu Q, Wang F, Ling EA, Liu S, Wang L, Yang Y, Yao L, Chen X, Wang F, Shi W, Gao M, Hao A. Melatonin antagonizes hypoxia-mediated glioblastoma cell migration and invasion via inhibition of HIF-1alpha. J Pineal Res. 2013; 55:121-130.
27. Ordonez R, Carbajo-Pescador S, Prieto-Dominguez N, Garcia-Palomo A, Gonzalez-Gallego J, Mauriz JL. Inhibition of matrix metalloproteinase-9 and nuclear factor kappa B contribute to melatonin prevention of motility and invasiveness in HepG2 liver cancer cells. J Pineal Res. 2014; 56:20-30.
28. Goncalves Ndo N, Rodrigues RV, Jardim-Perassi BV, Moschetta MG, Lopes JR, Colombo J, Zuccari DA. Molecular markers of angiogenesis and metastasis in lines of oral carcinoma after treatment with melatonin. Anticancer Agents Med Chem. 2014; 14:1302-1311.
29. Lauricella-Lefebvre MA, Castronovo V, Sato H, Seiki M, French DL, Merville MP. Stimulation of the 92-kD type IV collagenase promoter and enzyme expression in human melanoma cells. Invasion Metastasis. 1993; 13:289-300.
30. Chen YJ, Wang YN, Chang WC. ERK2-mediated C-terminal serine phosphorylation of p300 is vital to the regulation of epidermal growth factor-induced keratin 16 gene expression. J Biol Chem. 2007; 282:27215-27228.
31. Meissner JD, Freund R, Krone D, Umeda PK, Chang KC, Gros G, Scheibe RJ. Extracellular signal-regulated kinase 1/2-mediated phosphorylation of p300 enhances myosin heavy chain I/beta gene expression via acetylation of nuclear factor of activated T cells c1. Nucleic Acids Res. 2011; 39:5907-5925.
32. Sharma N, Nyborg JK. The coactivators CBP/p300 and the histone chaperone NAP1 promote transcription-independent nucleosome eviction at the HTLV-1 promoter. Proc Natl Acad Sci U S A. 2008; 105:7959-7963.
33. Pons D, de Vries FR, van den Elsen PJ, Heijmans BT, Quax PH, Jukema JW. Epigenetic histone acetylation modifiers in vascular remodelling: new targets for therapy in cardiovascular disease. Eur Heart J. 2009; 30:266-277.
34. Carbajo-Pescador S, Ordonez R, Benet M, Jover R, Garcia-Palomo A, Mauriz JL, Gonzalez-Gallego J. Inhibition of VEGF expression through blockade of Hif1alpha and STAT3 signalling mediates the anti-angiogenic effect of melatonin in HepG2 liver cancer cells. Br J Cance. 2013; 109:83-91.
35. Hong Y, Won J, Lee Y, Lee S, Park K, Chang KT, Hong Y. Melatonin treatment induces interplay of apoptosis, autophagy, and senescence in human colorectal cancer cells. J Pineal Res. 2014; 56:264-274.
36. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011; 147:275-292.
37. Liotta LA, Stetler-Stevenson WG. Tumor invasion and metastasis: an imbalance of positive and negative regulation. Cancer Res. 1991; 51:5054s-5059s.
38. Coussens LM, Werb Z. Matrix metalloproteinases and the development of cancer. Chem Biol. 1996; 3:895-904.
39. Okada N, Ishida H, Murata N, Hashimoto D, Seyama Y, Kubota S. Matrix metalloproteinase-2 and-9 in bile as a marker of liver metastasis in colorectal cancer. Biochem Biophys Res Commun. 2001; 288:212-216.
40. Liu JF, Crepin M, Liu JM, Barritault D, Ledoux D. FGF-2 and TPA induce matrix metalloproteinase-9 secretion in MCF-7 cells through PKC activation of the Ras/ERK pathway. Biochem Biophys Res Commun. 2002; 293:1174-1182.
41. Sun Y, Liu WZ, Liu T, Feng X, Yang N, Zhou HF. Signaling pathway of MAPK/ERK in cell proliferation, differentiation, migration, senescence and apoptosis. J Recept Signal Transduct Res. 2015; 35:600-604.
42. Simon C, Goepfert H, Boyd D. Inhibition of the p38 mitogen-activated protein kinase by SB 203580 blocks PMA-induced Mr 92, 000 type IV collagenase secretion and in vitro invasion. Cancer Res. 1998; 58:1135-1139.
43. Genersch E, Hayess K, Neuenfeld Y, Haller H. Sustained ERK phosphorylation is necessary but not sufficient for MMP-9 regulation in endothelial cells: involvement of Ras-dependent and-independent pathways. J Cell Sci. 2000; 113:4319-4330.
44. Hsu HH, Hu WS, Lin YM, Kuo WW, Chen LM, Chen WK, Hwang JM, Tsai FJ, Liu CJ, Huang CY. JNK suppression is essential for 17beta-Estradiol inhibits prostaglandin E2-Induced uPA and MMP-9 expressions and cell migration in human LoVo colon cancer cells. J Biomed Sci. 2011; 18:61.
45. Mao L, Yuan L, Slakey LM, Jones FE, Burow ME, Hill SM. Inhibition of breast cancer cell invasion by melatonin is mediated through regulation of the p38 mitogen-activated protein kinase signaling pathway. Breast Cancer Res. 2010; 12:R107.
46. Zhou Q, Gui S, Zhou Q, Wang Y. Melatonin inhibits the migration of human lung adenocarcinoma A549 cell lines involving JNK/MAPK pathway. PLoS One. 2014; 9:e101132.
47. Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T. Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem. 2003; 253:269-285.
48. Hah N, Lee ST. An absolute role of the PKC-dependent NFkappaB activation for induction of MMP-9 in hepatocellular carcinoma cells. Biochem Biophys Res Commun. 2003; 305:428-433.
49. Shin Y, Yoon SH, Choe EY, Cho SH, Woo CH, Rho JY, Kim JH. PMA-induced up-regulation of MMP-9 is regulated by a PKCalpha-NF-kappaB cascade in human lung epithelial cells. Exp Mol Med. 2007; 39:97-105.
50. Lin CW, Hou WC, Shen SC, Juan SH, Ko CH, Wang LM, Chen YC. Quercetin inhibition of tumor invasion via suppressing PKC delta/ERK/AP-1-dependent matrix metalloproteinase-9 activation in breast carcinoma cells. Carcinogenesis. 2008; 29:1807-1815.
51. Guarente L. Transcriptional coactivators in yeast and beyond. Trends Biochem Sci. 1995; 20:517-521.
52. Lackey DE, Hoag KA. Vitamin A upregulates matrix metalloproteinase-9 activity by murine myeloid dendritic cells through a nonclassical transcriptional mechanism. J Nutr. 2010; 140:1502-1508.
53. Santer FR, Hoschele PP, Oh SJ, Erb HH, Bouchal J, Cavarretta IT, Parson W, Meyers DJ, Cole PA, Culig Z. Inhibition of the acetyltransferases p300 and CBP reveals a targetable function for p300 in the survival and invasion pathways of prostate cancer cell lines. Mol Cancer Ther. 2011; 10:1644-1655.
54. Ma Z, Shah RC, Chang MJ, Benveniste EN. Coordination of cell signaling, chromatin remodeling, histone modifications, and regulator recruitment in human matrix metalloproteinase 9 gene transcription. Mol Cell Biol. 2004; 24:5496-5509.
55. Claustrat B, Leston J. Melatonin: Physiological effects in humans. Neurochirurgie. 2015; 61:77-84.
56. Jenwitheesuk A, Nopparat C, Mukda S, Wongchitrat P, Govitrapong P. Melatonin regulates aging and neurodegeneration through energy metabolism, epigenetics, autophagy and circadian rhythm pathways. Int J Mol Sci. 2014; 15:16848-16884.
57. Rizvi SI, Jha R. Strategies for the discovery of anti-aging compounds. Expert Opin Drug Discov. 2011; 6:89-102.
58. Berk L, Berkey B, Rich T, Hrushesky W, Blask D, Gallagher M, Kudrimoti M, McGarry RC, Suh J, Mehta M. Randomized phase II trial of high-dose melatonin and radiation therapy for RPA class 2 patients with brain metastases (RTOG 0119). Int J Radiat Oncol Biol Phys. 2007; 68:852-857.
59. Harpsoe NG, Andersen LP, Gogenur I, Rosenberg J. Clinical pharmacokinetics of melatonin: a systematic review. Eur J Clin Pharmacol. 2015; 71:901-909.
60. Yang CY, Meng CL. Regulation of PG synthase by EGF and PDGF in human oral, breast, stomach, and fibrosarcoma cancer cell lines. J Dent Res. 1994; 73: 1407-1415.
61. Yang SF, Chu SC, Chiang IC, Kuo WF, Chiou HL, Chou FP, Kuo WH, Hsieh YS. Excessive matrix metalloproteinase-9 in the plasma of community-acquired pneumonia. Clin Chim Acta. 2005; 352:209-215.