Melatonin as a selective estrogen enzyme modulator

Current Cancer Drug Targets

Volumn 8, Issue 8, 2008, Pages 691-702

  Cos, S ^a,b   Gonzalez A ^a   Martinez Campa C ^a   Mediavilla, M D ^a   Alonso Gonzalez C ^a   Sanchez Barcelo E J ^a  

^a UNIVERSITY OF CANTABRIA   (Spain)

^b UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

17 hydroxysteroid dehydrogenase; Aromatase; Breast cancer; Estradiol; Melatonin; Pineal gland; Sulfatase; Sulfotransferase

Indexed keywords

AMINOGLUTETHIMIDE; ANASTROZOLE; AROMATASE; AROMATASE INHIBITOR; ESTROGEN SULFOTRANSFERASE; EXEMESTANE; FORMESTANE; LETROZOLE; MELATONIN; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SULFATASE; TESTOSTERONE 17BETA DEHYDROGENASE;

ANTINEOPLASTIC ACTIVITY; BREAST CANCER; CANCER HORMONE THERAPY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; PROTEIN EXPRESSION; REVIEW;

17-HYDROXYSTEROID DEHYDROGENASES; AROMATASE; BREAST NEOPLASMS; ESTROGENS; HUMANS; MELATONIN; NEOPLASMS, HORMONE-DEPENDENT; SELECTIVE ESTROGEN RECEPTOR MODULATORS; SULFATASES;

EID: 57449086571     PISSN: 15680096     EISSN: None     Source Type: Journal    
DOI: 10.2174/156800908786733469     Document Type: Review

References (82)

1. Reiter, R. J. The pineal and its hormones in the control of reproduction in mammals. Endocr. Rev. 1980, 1, 109-131.
2. Cos, S.; Sánchez-Barceló, E. J. Melatonin and mammary pathological growth. Front. Neuroendocrinol. 2000, 21, 133-170.
3. Cos, S.; Sánchez-Barceló, E. J. Melatonin, experimental basis for a possible application in breast cancer prevention and treatment. Histol. Histopathol. 2000, 15, 637-647.
4. Blask, D. E.; Sauer, L. A.; Dauchy, R. T. Melatonin as a chronobiotic/anticancer agent: cellular, biochemical and molecular mechanisms of action and their implications for circadian-based cancer therapy. Curr. Top. Med. Chem. 2002, 2, 113-132.
5. Sánchez-Barceló, E. J.; Cos, S.; Fernández, R.; Mediavilla, M. D. Melatonin and mammary cancer: a short review. Endocr. Relat. Cancer 2003, 10, 153-159.
6. Sánchez-Barceló, E. J.; Cos, S.; Mediavilla, M. D.; Martínez-Campa, C. M.; González, A.; Alonso-González, C. Melatonin-estrogen interactions in breast cancer. J. Pineal Res. 2005, 38, 217-222.
7. Cos, S.; González, A.; Martínez-Campa, C.; Mediavilla, M. D.; Alonso-González, C.; Sánchez-Barceló, E. J. Estrogen-signaling pathway: a link between breast cancer and melatonin oncostatic actions. Cancer Detect. Prev. 2006, 30, 118-128.
8. Molis, T. M.; Spriggs, L. L.; Hill, S. M. Modulation of estrogen receptor mRNA expression by melatonin in MCF-7 human breast cancer cells. Mol. Endocrinol. 1994, 8, 1681-1690.
9. Cos, S.; Blask, D. E.; Lemus-Wilson, A.; Hill, S. M. Effects of melatonin on the cell cycle kinetics and estrogen rescue of MCF-7 human breast cancer cells in culture. J. Pineal Res. 1991, 10, 36-42.
10. Allegra, M.; Reiter, R. J.; Tan, D. X.; Gentile, C.; Tesoriere, L.; Livrea, M. A. The chemistry of melatonin's interaction with reactive species. J. Pineal Res. 2003, 34, 1-10.
11. Fraschini, F.; Demartini, G.; Esposti, D.; Scaglione, F. Melatonin involvement in immunity and cancer. Biol. Signals Recept. 1998, 7, 61-72.
12. Leon-Blanco, M. M.; Guerrero, J. M.; Reiter, R. J.; Calvo, J. R.; Pozo, D. Melatonin inhibits telomerase activity in the MCF-7 tumor cell line both in vivo and in vitro. J. Pineal Res. 2003, 35, 204-211.
13. Blask, D. E.; Dauchy, R. T.; Sauer, L. A.; Krause, J. A; Brainard, G. C. Growth and fatty acid metabolism of human breast cancer (MCF-7) xenografts in nude rats: impact of constant light-induced nocturnal melatonin suppression. Breast Cancer Res. Treat. 2003, 79, 313-320.
14. Blask, D. E.; Dauchy, R. T.; Sauer, L. A. Putting cancer to sleep at night. Endocrine 2005, 27, 179-188.
15. Dumitrescu, R. G.; Cotarla, I. Understanding breast cancer risk - where do we stand in 2005? J. Cell Mol. Med. 2005, 9, 208-221.
16. Russo, I. H.; Russo, J. Role of hormones in mammary cancer initiation and progression. J. Mammary Gland Biol. Neoplasia 1998, 3, 49-61.
17. Russo, J.; Russo, I. H. The role of estrogen in the initiation of breast cancer. J. Steroid Biochem. Mol. Biol. 2006, 102, 89-96.
18. Howell, A.; Clarke, R. B.; Anderson, E. Oestrogens, Beatson and endocrine therapy. Endocr. Relat. Cancer 1997, 4, 371-380.
19. Preston-Martin, S.; Pike, M. C.; Ross, R. K.; Jones, P. A.; Henderson, B. E. Increased cell division as a cause of human cancer. Cancer Res. 1990, 50, 7415-7421.
20. Yue, W.; Santen, R. J.; Wang, J. P.; Li, Y.; Verdearme, M. F.; Bocchinfuso, W. P.; Korach, K. S.; Devanesan, P.; Todorovic, R; Rogan, E. G.; Cavalieri, E. L. Genotoxic metabolites of estradiol in breast: potential mechanism of estradiol induced carcinogenesis. J. Steroid Biochem. Mol. Biol. 2003, 86, 477-486.
21. Simpson, E. R. Role of aromatase in sex steroid action. J. Mol. Endocrinol. 2000, 25, 149-156.
22. Landeghem, A. A.; Poortman, J.; Nabuurs, M.; Thijssen, J. H. Endogenous concentration and subcellular distribution of estrogens in normal and malignant human breast tissue. Cancer Res. 1985, 45, 2900-2906.
23. Yue, W.; Wang, J. P.; Hamilton, C. J.; Demers, L. M.; Santen, R. J. In situ aromatization enhances breast tumor estradiol levels and cellular proliferation. Cancer Res. 1998, 58, 927-932.
24. Sasano, H.; Suzuki, T.; Nakata, T.; Moriya, T. New development in intracrinology of breast carcinoma. Breast Cancer 2006, 13, 129-136.
25. Pasqualini, J. R. The selective estrogen enzyme modulators in breast cancer: a review. Biochim. Biophys. Acta 2004, 1654, 123-143.
26. Pasqualini, J. R.; Chetrite, G. S. Recent insight on the control of enzymes involved in estrogen formation and transformation in human breast cancer. J. Steroid Biochem. Mol. Biol. 2005, 93, 221-236.
27. Conley, A.; Hinshelwood, M. Mammalian aromatases. Reproduction 2001, 121, 685-695.
28. Santen, R. J.; Harvey, H. A. Use of aromatase inhibitors in breast carcinoma. Endocr. Relat. Cancer 1999, 6, 75-92.
29. Suzuki, T.; Miki, Y.; Nakamura, Y.; Moriya, T.; Ito, K.; Ohuchi, N.; Sasano, H. Sex steroid-producing enzymes in human breast cancer. Endocr. Relat. Cancer 2005, 12, 701-720.
30. Suzuki, T.; Miki, Y.; Nakata, T.; Shiotsu, Y.; Akinaga, S.; Inoue, K.; Ishida, T.; Kimura, M.; Moriya, T.; Sasano, H. Steroid sulfatase and estrogen sulfotransferase in normal human tissue and breast cancer. J. Steroid Biochem. Mol. Biol. 2003, 86, 449-454.
31. Wong, Z. W.; Ellis, M. J. First-line endocrine treatment of breast cancer: aromatase inhibitor or antioestrogen? Br. J. Cancer 2004, 90, 20-25.
32. Bush, N. J. Advances in hormonal therapy for breast cancer. Semin. Oncol. Nurs. 2007, 23, 46-54.
33. Lerner, A. B.; Case, J. D.; Takahashi, Y.; Lee, T. H.; Mori, W. Isolation of melatonin, the pineal gland factor that lightens melanocytes. J. Amer. Chem. Soc. 1958, 80, 2587.
34. Vanecek, J. Cellular mechanisms of melatonin action. Physiol. Rev. 1998, 78, 687-721.
35. Becker-Andre, M.; Wiesenberg, I.; Schaeren-Wiemers, N.; Andre, E.; Missbach, M.; Saurat, J. H.; Carlberg, C. Pineal gland hormone melatonin binds and activates an orphan of the nuclear receptor superfamily. J. Biol. Chem. 1994, 269, 28531-28534.
36. Anton-Tay, F.; Martínez, I.; Tovar, R.; Benitez-King, G. Modulation of the subcellular distribution of calmodulin by melatonin in MDCK cells. J. Pineal Res. 1998, 24, 35-42.
37. Arendt, J. Role of the pineal gland and melatonin in seasonal reproductive function in mammals. Oxf. Rev. Reprod. Biol. 1986, 8, 266-320.
38. Malpaux, B.; Migaud, M.; Tricoire, H.; Chemineau, P. Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. J. Biol. Rhythms 2001, 16, 336-347.
39. Dubocovich, M. L.; Rivera-Bermudez, M. A.; Gerdin, M. J.; Masana, M. I. Molecular pharmacology, regulation and function of mammalian melatonin receptors. Front. Biosci. 2003, 8, 1093-1108.
40. Yellon, S. M.; Foster, D. L. Melatonin rhythms time photoperiod-induced puberty in the female lamb. Endocrinology 1986, 119, 44-49.
41. Kauppila, A.; Kivela, A.; Pakarinen, A.; Vakkuri, O. Inverse seasonal relationship between melatonin and ovarian activity in humans in a region with a strong seasonal contrast in luminosity. J. Clin. Endocrinol. Metab. 1987, 65, 823-828.
42. Luboshitzky, R.; Lavie, P. Melatonin and sex hormone interrelationships-a review. J. Pediatr. Endocrinol. Metab. 1999, 12, 355-362.
43. Woo, M. M.; Tai, C. J.; Kang, S. K.; Nathwani, P. S.; Pang, S. F.; Leung, P. C. Direct action of melatonin in human granulosa-luteal cells. J. Clin. Endocr. Metab. 2001, 86, 4789-4797.
44. Webley, G. E.; Luck, M. R. Melatonin directly stimulates the secretion of progesterone by human and bovine granulosa cells in vitro. J. Reprod. Fertil. 1986, 78, 711-717.
45. Cohen, M.; Lippman, M.; Chabner, B. Role of pineal gland in aetiology and treatment of breast cancer. Lancet 1978, 2, 814-816.
46. Blask, D. E.; Brainard, G. C.; Dauchy, R. T.; Hanifin, J. P.; Davidson, L. K.; Krause, J. A.; Sauer, L. A.; Rivera-Bermudez, M. A.; Dubocovich, M. L.; Jasser, S. A.; Lynch, D. T.; Rollag, M. D.; Zalatan, F. Melatonin-depleted blood from premenopausal women exposed to light at night stimulates growth of human breast cancer xenografts in nude rats. Cancer Res. 2005, 65, 11174-11184.
47. Tamarkin, L.; Danforth, D. N.; Lichter, A.; Demoss, E.; Cohen, M.; Chabner, B.; Lippman, M. Decreased nocturnal plasma melatonin peak in patients with estrogen receptor positive breast cancer. Science 1982, 216, 1003-1005.
48. Maestroni, J. M.; Conti, A. Melatonin in human breast cancer tissue: association with nuclear grade and estrogen receptor status. Lab. Invest. 1996, 75, 557-561.
49. Bartsch, C.; Bartsch, H.; Jain, A. K.; Laumas, K. R.; Wetterberg, L. Urinary melatonin levels in human breast cancer patients. J. Neural Transm. 1981, 52, 281-294.
50. Coleman, M. P.; Reiter, R. J. Breast cancer, blindness and melatonin. Eur. J. Cancer 1992, 28, 501-503.
51. Verkasalo, P. K.; Pukkala, E.; Stevens, R. G.; Ojamo, M.; Rudanko, S. L. Inverse association between breast cancer incidence and degree of visual impairment in Finland. Br. J. Cancer 1999, 80, 1459-1460.
52. Hrushesky, W. Tumor cronobiology. J. Control Release 2001, 74, 27-30.
53. Cos, S.; Mediavilla, M. D.; Martínez-Campa, C.; González, A.; Alonso-González, C.; Sánchez-Barceló, E. J. Exposure to light at night increases the growth of DMBA-induced mammary adenocarcinomas in rats. Cancer Lett. 2006, 235, 266-271.
54. Blask, D. E.; Hill, S. M. Effects of melatonin on cancer: studies on MCF-7 human breast cancer cells in culture. J. Neural Transm. (Suppl.) 1986, 21, 433-449.
55. Hill, S. M.; Spriggs, L. L.; Simon, M. A.; Muraoka, H.; Blask, D. E. The growth inhibitory action of melatonin on human breast cancer cells is linked to the estrogen response system. Cancer Lett. 1992, 64, 249-256.
56. Cos, S.; Fernández, F.; Sánchez-Barceló, E. J. Melatonin inhibits DNA synthesis in MCF-7 human breast cancer cells in vitro. Life Sci. 1996, 58, 2447-2453.
57. Molis, T. M.; Walters, M. R.; Hill, S. M. Melatonin modulation of estrogen receptor expression in MCF-7 human breast cancer cells. Int. J. Oncol. 1993, 3, 687-694.
58. Cos, S.; Blask, D. E. Melatonin modulates growth factor activity in MCF-7 human breast cancer cells. J. Pineal Res. 1994, 17, 25-32.
59. Molis, T. M.; Spriggs, L. L.; Jupiter, Y.; Hill, S. M. Melatonin modulation of estrogen-regulated proteins, growth factors and proto-oncogenes in human breast cancer. J. Pineal Res. 1995, 18, 93-103.
60. Yuan, L.; Collins, A. R.; Dai, J.; Dubocovich, M. L.; Hill, S. M. MT-1 melatonin receptor overexpression enhances the growth suppressive effect of melatonin in human breast cancer cells. Mol. Cell Endocrinol. 2002, 192, 147-156.
61. Cos, S.; Fernández, R.; Güezmes, A.; Sánchez- Barceló, E. J. Influence of melatonin on invasive and metastatic properties of MCF-7 human breast cancer cells. Cancer Res. 1998, 58, 4383-4390.
62. Soule, H. D.; Vazquez, J.; Long A.; Albert, S.; Brennan, M. J. A human cell line from a pleural effusion derived from a breast carcinoma. J. Natl. Cancer Inst. 1973, 51, 1409-1412.
63. Ram, P. T.; Dai, J.; Yuan, L.; Dong, C.; Kiefer, T. L.; Lai, L.; Hill, S. M. Involvement of the MT-1 melatonin receptor in human breast cancer. Cancer Lett. 2002, 179, 141-150.
64. Cos, S.; Martínez-Campa, C.; Mediavilla, M. D.; Sánchez-Barceló, E. J. Melatonin modulates aromatase activity in MCF-7 human breast cancer cells. J. Pineal Res. 2005, 38, 136-142.
65. González, A.; Martínez-Campa, C.; Mediavilla, M. D.; Alonso-González, C.; Sánchez-Mateos, S.; Hill, S. M.; Sanchez-Barcelo, E. J.; Cos, S. Effects of MT1 melatonin receptor overexpression on the aromatase-suppressive effect of melatonin in MCF-7 human breast cancer cells. Oncol. Rep. 2007, 17, 947-955.
66. Cos, S.; González, A.; Güezmes, A.; Mediavilla, M. D.; Martínez-Campa, C.; Alonso-González, C.; Sánchez- Barceló, E. J. Melatonin inhibits the growth of DMBA-induced mammary tumors by decreasing the local biosynthesis of estrogens through the modulation of aromatase activity. Int. J. Cancer 2006, 118, 274-278.
67. Bulun, S. E.; Sebastian, S.; Takayama, K.; Suzuki, T.; Sasano, H.; Shozu, M. The human CYP 19 (aromatase p450) gene: update on physiologic roles and genomic organization of promoters. J. Steroid Biochem. Mol. Biol. 2003, 86, 219-224.
68. Godson, C.; Reppert, S. M. The mel1a melatonin receptor is coupled to parallel signal transduction pathways. Endocrinology 1997, 138, 397-404.
69. Kiefer, T.; Ram, P. T.; Yuan, L.; Hill, S. M. Melatonin inhibits estrogen receptor transactivation and cAMP levels in breast cancer cells. Breast Cancer Res. Treat. 2002, 71, 37-45.
70. Cardinali, D. P.; Bonanni Rey, R. A.; Mediavilla, M. D.; Sánchez-Barceló, E. J. Diurnal changes in cyclic nucleotide response to pineal indoles in murine mammary glands. J. Pineal Res. 1992, 13, 111-116.
71. Martínez-Campa, C.; González, A.; Mediavilla, M. D.; Alonso-González, C.; Sánchez-Barceló, E. J.; Cos, S. Melatonin enhances the inhibitory effect of aminoglutethimide on aromatase activity in MCF-7 human breast cancer cells. Breast Cancer Res. Treat. 2005, 94, 249-254.
72. Kao, Y. C.; Okubo, T.; Sun, X. Z.; Chen, S. Induction of aromatase expression by aminoglutethimide, an aromatase inhibitor that is used to treat breast cancer in postmenopausal women. Anticancer Res. 1999, 19, 2049-2056.
73. González, A.; Martínez-Campa, C.; Mediavilla, M. D.; Alonso-González, C.; Sánchez-Barceló, E. J.; Cos, S. Inhibitory effects of pharmacological doses of melatonin on aromatase activity and expresión in rat glioma cells. Br. J. Cancer 2007, 97, 755-760.
74. Bulun, S. E.; Lin, Z.; Imir, G.; Amin, S.; Demura, M.; Yilmaz, B.; Martin, R.; Utsunomiya, H.; Thung, S.; Gurates, B.; Tamura, M.; Langoi, D.; Deb, S. Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol. Rev. 2005, 57, 359-383.
75. Wu, K. K. Control of cyclooxygenase-2 transcriptional activation by pro-inflammatory mediators. Prostaglandins Leukot Essent Fatty Acids 2005, 72, 89-93.
76. Purohit, A.; Newman, S. P.; Reed, M. J. The role of cytokines in regulating estrogen synthesis: implications for the etiology of breast cancer. Breast Cancer Res. 2002, 4, 65-69.
77. Santner, S. J.; Rosen, H.; Osawa, Y.; Santen, R. J. Additive effects of aminoglutethimide, testololactone, and 4-hydroxyandrostenedione as inhibitors of aromatase. J. Steroid Biochem. 1984, 20, 1239-1242.
78. González, A.; Cos, S.; Martínez-Campa, C.; Alonso-González, C.; Sánchez-Mateos, S.; Mediavilla, M. D.; Sánchez-Barceló, E. J. Selective estrogen enzime modulator actions of melatonin in human breast cancer cells. J. Pineal Res. 2008, 45, 86-92.
79. Evans, T. R.; Rowlands, M. G.; Luqmani, Y. A.; Chander, S. K.; Coombes, R. C. Detection of breast cancer-associated estrone sulfatase in breast cancer biopsies and cell lines using polymerase chain reaction. J. Steroid Biochem. Mol. Biol. 1993, 46, 195-201.
80. Fournier, S.; Brihmat, F.; Durand, J. C.; Sterkers, N.; Martin, P. M.; Kutten, F.; Mauvais-Jarvis, P. Estradiol 17β-hydroxysteroid dehydrogenases, a marker of breast cancer hormone dependency. Cancer Res. 1985, 45, 2895-2899.
81. Maitra, S. K.; Ray, A. K. Role of light in the mediation of acute effects of a single afternoon melatonin injection on steroidogenic activity of testis in the rat. J. Biosci. 2000, 25, 253-256.
82. Frungieri, M. B.; Mayerhofer, A.; Zitta, K.; Pignataro, O. P.; Calandra, R. S.; González-Calvar, S. I. Direct effect of melatonin on Syrian hamster testes: melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system. Endocrinology 2005, 146, 1541-1552.