Melatonin decreases breast cancer metastasis by modulating Rho-associated kinase protein-1 expression

Journal of Pineal Research

Volumn 60, Issue 1, 2016, Pages 3-15

  Borin, Thaiz Ferraz ^a   Arbab, Ali Syed ^b   Gelaleti, Gabriela Bottaro ^a,c   Ferreira, Lívia Carvalho ^a,c   Moschetta, Marina Gobbe ^a   Jardim Perassi, Bruna Victorasso ^a   Iskander, Asm ^b   Varma, Nadimpalli Ravi S ^d   Shankar, Adarsh ^b   Coimbra, Verena Benedick ^a   Fabri, Vanessa Alves ^a   De Oliveira, Juliana Garcia ^e   Zuccari, Debora Aparecida Pires De Campos ^a,c  

^a FACULDADE DE MEDICINA DE SÃO JOSÉ DO RIO PRETO   (Brazil)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^d HENRY FORD HOSPITAL   (United States)

^e UNIVERSIDADE DO SAGRADO CORAÇÃO   (Brazil)

Author keywords

99mTc tetrofosmin; breast cancer; lung metastasis; MCF 7 cells; MDA MB 231 cells; melatonin; Rho associated kinase protein 1 inhibitor; single photon emission computed tomography

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; MELATONIN; RHO ASSOCIATED KINASE PROTEIN 1; RHO KINASE; UNCLASSIFIED DRUG; AMIDE; PYRIDINE DERIVATIVE; ROCK1 PROTEIN, HUMAN; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST METASTASIS; CELL INVASION; CELL MIGRATION; CELL VIABILITY; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TUMOR GROWTH; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; DIAGNOSTIC IMAGING; DRUG SCREENING; ENZYMOLOGY; METABOLISM; METASTASIS; NUDE MOUSE; PATHOLOGY; SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY-COMPUTED TOMOGRAPHY; TUMOR CELL LINE;

AMIDES; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; MELATONIN; MICE; MICE, NUDE; NEOPLASM METASTASIS; NEOPLASM PROTEINS; PYRIDINES; RHO-ASSOCIATED KINASES; SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY COMPUTED TOMOGRAPHY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84955212354     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12270     Document Type: Article

References (52)

1. Jemal A, Bray F, Center MM, et al., Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
2. Moreau JE, Anderson K, Mauney JR, et al., Tissue-engineered bone serves as a target for metastasis of human breast cancer in a mouse model. Cancer Res 2007; 67: 10304-10308.
3. Song NR, Hwang MK, Heo YS, et al., Piceatannol suppresses the metastatic potential of MCF10A human breast epithelial cells harboring mutated H-ras by inhibiting MMP-2 expression. Int J Mol Med 2013; 32: 775-784.
4. Schackmann RC, van Amersfoort M, Haarhuis JH, et al., Cytosolic p120-catenin regulates growth of metastatic lobular carcinoma through Rock1-mediated anoikis resistance. J Clin Invest 2011; 121: 3176-3188.
5. Ridley AJ,. Rho GTPases and cell migration. J Cell Sci 2001; 114: 2713-2722.
6. Ortíz-Lõpez L, Morales-Mulia S, Ramírez-Rodríguez G, et al., ROCK-regulated cytoskeletal dynamics participate in the inhibitory effect of melatonin on cancer cell migration. J Pineal Res 2009; 46: 15-21.
7. Liu S, Goldstein RH, Scepansky EM, et al., Inhibition of rho-associated kinase signaling prevents breast cancer metastasis to human bone. Cancer Res 2009; 69: 8742-8751.
8. Acuña-Castroviejo D, Escames G, Venegas C, et al., Extrapineal melatonin: sources, regulation, and potential functions. Cell Mol Life Sci 2014; 71: 2997-3025.
9. Luchetti F, Canonico B, Betti M, et al., Melatonin signaling and cell protection function. FASEB J 2010; 24: 3603-3624.
10. Cos S, Fernández R, Güézmes A, et al., Influence of melatonin on invasive and metastatic properties of MCF-7 human breast cancer cells. Cancer Res 1998; 58: 4383-4390.
11. Proietti S, Cucina A, Reiter RJ, et al., Molecular mechanisms of melatonin's inhibitory actions on breast cancers. Cell Mol Life Sci 2013; 70: 2139-2157.
12. Cos S, Recio J, Sánchez-Barcelõ EJ,. Modulation of the length of the cell cycle time of MCF-7 human breast cancer cells by melatonin. Life Sci 1996; 58: 811-816.
13. Sanchez-Barcelo EJ, Mediavilla MD, Alonso-Gonzalez C, et al., Melatonin uses in oncology: breast cancer prevention and reduction of the side effects of chemotherapy and radiation. Expert Opin Investig Drugs 2012; 21: 819-831.
14. Jardim-Perassi BV, Arbab AS, Ferreira LC, et al., Effect of melatonin on tumor growth and angiogenesis in xenograft model of breast cancer. PLoS ONE 2014; 9: e85311.
15. Livak KJ, Schmittgen TD,. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
16. Schmittgen TD, Livak KJ,. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008; 3: 1101-1108.
17. Chen Q, Manning CD, Millar H, et al., CNTO 95, a fully human anti alphav integrin antibody, inhibits cell signaling, migration, invasion, and spontaneous metastasis of human breast cancer cells. Clin Exp Metastasis 2008; 25: 139-148.
18. Cowey S, Szafran AA, Kappes J, et al., Breast cancer metastasis to bone: evaluation of bioluminescent imaging and microSPECT/CT for detecting bone metastasis in immunodeficient mice. Clin Exp Metastasis 2007; 24: 389-401.
19. Gambini JP, Cabral P, Alonso O, et al., Evaluation of 99 mTc-glucarate as a breast cancer imaging agent in a xenograft animal model. Nucl Med Biol 2011; 38: 255-260.
20. Arbab AS, Koizumi K, Arai T, et al., Application of Tc-99m-tetrofosmin as a tumor imaging agent: comparison with Tl-201. Ann Nucl Med 1996; 10: 271-274.
21. Buccheri G, Ferrigno D,. Lung tumour markers in oncology practice: a study of TPA and CA125. Br J Cancer 2002; 87: 1112-1118.
22. Schillaci O, Spanu A, Scopinaro F, et al., Mediastinal lymph node involvement in non-small cell lung cancer: evaluation with 99mTc-tetrofosmin SPECT and comparison with CT. J Nucl Med 2003; 44: 1219-1224.
23. Wathen CA, Foje N, van Avermaete T, et al., In vivo X-ray computed tomographic imaging of soft tissue with native, intravenous, or oral contrast. Sensors (Basel) 2013; 13: 6957-6980.
24. Jardim-Perassi BV, Lourenco MR, Doho GM, et al., Melatonin regulates angiogenic factors under hypoxia in breast cancer cell lines. Anticancer Agents Med Chem 2015; 15. (in press)
25. Shi M, Liu D, Duan H, et al., Metastasis-related miRNAs, active players in breast cancer invasion, and metastasis. Cancer Metastasis Rev 2010; 29: 785-799.
26. Eck KM, Yuan L, Duffy L, et al., A sequential treatment regimen with melatonin and all-trans retinoic acid induces apoptosis in MCF-7 tumour cells. Br J Cancer 1998; 77: 2129-2137.
27. Cos S, Mediavilla MD, Fernández R, et al., Does melatonin induce apoptosis in MCF-7 human breast cancer cells in vitro? J Pineal Res 2002; 32: 90-96.
28. Yuan L, Collins AR, Dai J, et al., MT(1) melatonin receptor overexpression enhances the growth suppressive effect of melatonin in human breast cancer cells. Mol Cell Endocrinol 2002; 192: 147-156.
29. Mao L, Yuan L, Slakey LM, et al., 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.
30. Mirunalini S, Karthishwaran K, Dhamodharan G, et al., Studies on the chemopreventive potential of melatonin on 7, 12- dimethylbenz(a)anthracene induced mammary carcinogenesis in rats. J Appl Sci Res 2010; 6: 245-253.
31. Yerneni LK, Jayaraman S,. Pharmacological action of high doses of melatonin on B16 murine melanoma cells depends on cell number at time of exposure. Melanoma Res 2003; 13: 113-117.
32. Dubocovich ML, Delagrange P, Krause DN, et al., International Union of Basic and Clinical Pharmacology. LXXV. Nomenclature, classification, and pharmacology of G protein-coupled melatonin receptors. Pharmacol Rev 2010; 62: 343-380.
33. Juszczak M, Roszczyk M, Kowalczyk E, et al., The influence od melatonin receptors antagonists, luzindole and 4-phenyl-2-propionamidotetralin (4-P-PDOT), on melatonin-dependent vasopressin and adrenocorticotropic hormone (ACTH) release from the rat hypothalamo-hypophysial system. In vitro and in vivo studies. J Physiol Pharmacol 2014; 65: 777-784.
34. Hill SM, Frasch T, Xiang S, et al., Molecular mechanisms of melatonin anticancer effects. Integr Cancer Ther 2009; 8: 337-346.
35. Hill SM, Spriggs LL, Simon MA, et al., The growth inhibitory action of melatonin on human breast cancer cells is linked to the estrogen response system. Cancer Lett 1992; 64: 249-256.
36. Cos S, Sánchez-Barcelõ EJ,. Melatonin, experimental basis for a possible application in breast cancer prevention and treatment. Histol Histopathol 2000; 15: 637-647.
37. Mao L, Yuan L, Xiang S, et al., Molecular deficiency (ies) in MT melatonin signaling pathway underlies the melatonin-unresponsive phenotype in MDA-MB-231 human breast cancer cells. J Pineal Res 2014; 56: 246-253.
38. Hill SM, Cheng C, Yuan L, et al., Declining melatonin levels and MT1 receptor expression in aging rats is associated with enhanced mammary tumor growth and decreased sensitivity to melatonin. Breast Cancer Res Treat 2011; 127: 91-98.
39. Jablonska K, Pula B, Zemla A, et al., Expression of melatonin receptor MT1 in cells of human invasive ductal breast carcinoma. J Pineal Res 2013; 54: 334-345.
40. Liu H, Xu L, Wei JE, et al., Role of CD4+ CD25+ regulatory T cells in melatonin-mediated inhibition of murine gastric cancer cell growth in vivo and in vitro. Anat Rec (Hoboken) 2011; 294: 781-788.
41. Rao GN, Ney E, Herbert RA,. Effect of melatonin and linolenic acid on mammary cancer in transgenic mice with c-neu breast cancer oncogene. Breast Cancer Res Treat 2000; 64: 287-296.
42. Yang S, Kim HM,. ROCK inhibition activates MCF-7 cells. PLoS ONE 2014; 9: e88489.
43. Matsui DH, Machado-Santelli GM,. Alterations in F-actin distribution in cells treated with melatonin. J Pineal Res 1997; 23: 169-175.
44. Benítez-King G,. PKC activation by melatonin modulates vimentin intermediate filament organization in N1E-115 cells. J Pineal Res 2000; 29: 8-14.
45. Wang DS, Dou KF, Li KZ, et al., Enhancement of migration and invasion of hepatoma cells via a Rho GTPase signaling pathway. World J Gastroenterol 2004; 10: 299-302.
46. Barkan D, Kleinman H, Simmons JL, et al., Inhibition of metastatic outgrowth from single dormant tumor cells by targeting the cytoskeleton. Cancer Res 2008; 68: 6241-6250.
47. Ramírez-Rodríguez G, Ortiz-Lõpez L, Benítez-King G,. Melatonin increases stress fibers and focal adhesions in MDCK cells: participation of Rho-associated kinase and protein kinase C. J Pineal Res 2007; 42: 180-190.
48. Joshi B, Strugnell SS, Goetz JG, et al., Phosphorylated caveolin-1 regulates Rho/ROCK-dependent focal adhesion dynamics and tumor cell migration and invasion. Cancer Res 2008; 68: 8210-8220.
49. Raviraj V, Fok S, Zhao J, et al., Regulation of ROCK1 via Notch1 during breast cancer cell migration into dense matrices. BMC Cell Biol 2012; 13: 12.
50. Ramírez-Rodríguez G, Meza I, Hernández ME, et al., Melatonin induced cyclic modulation of vectorial water transport in kidney-derived MDCK cells. Kidney Int 2003; 63: 1356-1364.
51. Leon-Blanco MM, Guerrero JM, Reiter RJ, et al., Melatonin inhibits telomerase activity in the MCF-7 tumor cell line both in vivo and in vitro. J Pineal Res 2003; 35: 204-211.
52. Anisimov VN, Alimova IN, Baturin DA, et al., The effect of melatonin treatment regimen on mammary adenocarcinoma development in HER-2/neu transgenic mice. Int J Cancer 2003; 103: 300-305.