Melatonin: The smart killer. The human trophoblast as a model

Molecular and Cellular Endocrinology

Volumn 348, Issue 1, 2012, Pages 1-11

  Lanoix, Dave ^a   Lacasse, Andrée Anne ^a   Reiter, Russel J ^b   Vaillancourt, Cathy ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Extrinsic apoptosis; Intrinsic apoptosis; Non tumor cells; Placenta; Tumor cells

Indexed keywords

MELATONIN; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE;

ANTIOXIDANT ACTIVITY; APOPTOSIS; CELL SURVIVAL; CHORIOCARCINOMA; HORMONE ACTION; HUMAN; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; REVIEW; TROPHOBLAST;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL SURVIVAL; HUMANS; MELATONIN; MITOCHONDRIA; NEOPLASMS; SIGNAL TRANSDUCTION; TROPHOBLASTS;

EID: 80755188882     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.08.025     Document Type: Review

References (126)

1. Acuna-Castroviejo D., Escames G., Rodriguez M.I., Lopez L.C. Melatonin role in the mitochondrial function. Front Biosci. 2007, 12:947-963.
2. Albertini M.C., Radogna F., Accorsi A., Uguccioni F., Paternoster L., Cerella C., De Nicola M., D'Alessio M., Bergamaschi A., Magrini A., Ghibelli L. Intracellular pro-oxidant activity of melatonin deprives U937 cells of reduced glutathione without affecting glutathione peroxidase activity. Ann. N. Y. Acad. Sci. 2006, 1091:10-16.
3. Allaire A.D., Ballenger K.A., Wells S.R., McMahon M.J., Lessey B.A. Placental apoptosis in preeclampsia. Obstet. Gynecol. 2000, 96:271-276.
4. Alsat E. Le cytotrophoblaste humain, un casse-tête pour le biologiste. Médecine-Sci. 1999, 15:1236-1243.
5. Alscher R.G., Erturk N., Heath L.S. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 2002, 53:1331-1341.
6. Apel K., Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55:373-399.
7. Bejarano I., Espino J., Barriga C., Reiter R.J., Pariente J.A., Rodriguez A.B. Pro-oxidant effect of melatonin in tumour leucocytes: relation with its cytotoxic and pro-apoptotic effects. Basic Clin. Pharmacol. Toxicol. 2011, 108:14-20.
8. Bejarano I., Espino J., Marchena A.M., Barriga C., Paredes S.D., Rodriguez A.B., Pariente J.A. Melatonin enhances hydrogen peroxide-induced apoptosis in human promyelocytic leukaemia HL-60 cells. Mol. Cell. Biochem. 2011.
9. Bhat K.P., Pezzuto J.M. Cancer chemopreventive activity of resveratrol. Ann. N. Y. Acad. Sci. 2002, 957:210-229.
10. Bjelakovic G., Gluud L.L., Nikolova D., Bjelakovic M., Nagorni A., Gluud C. Antioxidant supplements for liver diseases. Cochrane Database Syst. Rev. 2011, 3:CD007749.
11. Black S., Kadyrov M., Kaufmann P., Ugele B., Emans N., Huppertz B. Syncytial fusion of human trophoblast depends on caspase 8. Cell Death Differ. 2004, 11:90-98.
12. Blask D.E., Dauchy R.T., Sauer L.A. Putting cancer to sleep at night: the neuroendocrine/circadian melatonin signal. Endocrine 2005, 27:179-188.
13. Bonnefont-Rousselot D., Collin F. Melatonin: action as antioxidant and potential applications in human disease and aging. Toxicology 2010, 278:55-67.
14. Boyd J.D., Hamilton W.J. Electron microscopic observations on the cytotrophoblast contribution to the syncytium in the human placenta. J. Anat. 1966, 100:535-548.
15. Bromme H.J., Morke W., Peschke D., Ebelt H. Scavenging effect of melatonin on hydroxyl radicals generated by alloxan. J. Pineal Res. 2000, 29:201-208.
16. Brown G.C. Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem. J. 1992, 284(Pt 1):1-13.
17. Camins A., Sureda F.X., Junyent F., Verdaguer E., Folch J., Beas-Zarate C., Pallas M. An overview of investigational antiapoptotic drugs with potential application for the treatment of neurodegenerative disorders. Expert Opin. Investig. Drugs 2010, 19:587-604.
18. Carrillo-Vico A., Guerrero J.M., Lardone P.J., Reiter R.J. A review of the multiple actions of melatonin on the immune system. Endocrine 2005, 27:189-200.
19. Casado-Zapico S., Rodriguez-Blanco J., Garcia-Santos G., Martin V., Sanchez-Sanchez A.M., Antolin I., Rodriguez C. 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.
20. Castellucci M., Kaufmann P., Bischof P. Extracellular matrix influences hormone and protein production by human chorionic villi. Cell Tissue Res. 1990, 262:135-142.
21. Chiu P.M., Ngan Y.S., Khoo U.S., Cheung A.N. Apoptotic activity in gestational trophoblastic disease correlates with clinical outcome: assessment by the caspase-related M30 CytoDeath antibody. Histopathology 2001, 38:243-249.
22. Choi S.I., Dadakhujaev S., Ryu H., Im Kim T., Kim E.K. Melatonin protects against oxidative stress in granular corneal dystrophy type 2 corneal fibroblasts by mechanisms that involve membrane melatonin receptors. J. Pineal Res. 2011.
23. Claustrat B., Brun J., Chazot G. The basic physiology and pathophysiology of melatonin. Sleep Med. Rev. 2005, 9:11-24.
24. Cos S., Fernandez R., Guezmes A., Sanchez-Barcelo E.J. Influence of melatonin on invasive and metastatic properties of MCF-7 human breast cancer cells. Cancer Res. 1998, 58:4383-4390.
25. Crocker I.P., Tansinda D.M., Jones C.J., Baker P.N. The influence of oxygen and tumor necrosis factor-alpha on the cellular kinetics of term placental villous explants in culture. J. Histochem. Cytochem. 2004, 52:749-757.
26. Das A., Belagodu A., Reiter R.J., Ray S.K., Banik N.L. Cytoprotective effects of melatonin on C6 astroglial cells exposed to glutamate excitotoxicity and oxidative stress. J. Pineal Res. 2008, 45:117-124.
27. Das A., McDowell M., Pava M.J., Smith J.A., Reiter R.J., Woodward J.J., Varma A.K., Ray S.K., Banik N.L. The inhibition of apoptosis by melatonin in VSC4.1 motoneurons exposed to oxidative stress, glutamate excitotoxicity, or TNF-alpha toxicity involves membrane melatonin receptors. J. Pineal Res. 2010, 48:157-169.
28. Deigner H.P., Haberkorn U., Kinscherf R. Apoptosis modulators in the therapy of neurodegenerative diseases. Expert Opin. Investig. Drugs 2000, 9:747-764.
29. Dopfel R.P., Schulmeister K., Schernhammer E.S. Nutritional and lifestyle correlates of the cancer-protective hormone melatonin. Cancer Detect. Prev. 2007, 31:140-148.
30. Dubbels R., Reiter R.J., Klenke E., Goebel A., Schnakenberg E., Ehlers C., Schiwara H.W., Schloot W. Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry. J. Pineal Res. 1995, 18:28-31.
31. Dziegiel P., Podhorska-Okolow M., Surowiak P., Ciesielska U., Rabczynski J., Zabel M. Influence of exogenous melatonin on doxorubicin-evoked effects in myocardium and in transplantable Morris hepatoma in rats. In Vivo 2003, 17:325-328.
32. Edeas M., Attaf D., Mailfert A.S., Nasu M., Joubet R. Maillard reaction, mitochondria and oxidative stress: potential role of antioxidants. Pathol. Biol. (Paris) 2010, 58:220-225.
33. Ekmekcioglu C. Melatonin receptors in humans: biological role and clinical relevance. Biomed. Pharmacother. 2006, 60:97-108.
34. Fisher S.J., Cui T.Y., Zhang L., Hartman L., Grahl K., Zhang G.Y., Tarpey J., Damsky C.H. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J. Cell. Biol. 1989, 109:891-902.
35. Fox H. Effect of hypoxia on trophoblast in organ culture. A morphologic and autoradiographic study. Am. J. Obstet. Gynecol. 1970, 107:1058-1064.
36. Fukutomi J., Fukuda A., Fukuda S., Hara M., Terada A., Yoshida M. Scavenging activity of indole compounds against cisplatin-induced reactive oxygen species. Life Sci. 2006, 80:254-257.
37. Gilgun-Sherki Y., Melamed E., Offen D. The role of oxidative stress in the pathogenesis of multiple sclerosis: the need for effective antioxidant therapy. J. Neurol. 2004, 251:261-268.
38. Gonzalez C.A., Travier N., Lujan-Barroso L., Castellsague X., Bosch F.X., Roura E., Bueno-de-Mesquita H.B., Palli D., Boeing H., Pala V., Sacerdote C., Tumino R., Panico S., Manjer J., Dillner J., Hallmans G., Kjellberg L., Sanchez M.J., Altzibar J.M., Barricarte A., Navarro C., Rodriguez L., Allen N., Key T.J., Kaaks R., Rohrmann S., Overvad K., Olsen A., Tjonneland A., Munk C., Kjaer S.K., Peeters P.H., van Duijnhoven F.J., Clavel-Chapelon F., Boutron-Ruault M.C., Trichopoulou A., Benetou V., Naska A., Lund E., Engeset D., Skeie G., Franceschi S., Slimani N., Rinaldi S., Riboli E. Dietary factors and in situ and invasive cervical cancer risk in the European prospective investigation into cancer and nutrition study. Int. J. Cancer 2010.
39. Guenther A.L., Schmidt S.I., Laatsch H., Fotso S., Ness H., Ressmeyer A.R., Poeggeler B., Hardeland R. Reactions of the melatonin metabolite AMK (N1-acetyl-5-methoxykynuramine) with reactive nitrogen species: formation of novel compounds, 3-acetamidomethyl-6-methoxycinnolinone and 3-nitro-AMK. J. Pineal Res. 2005, 39:251-260.
40. Gunawardena K., Murray D.K., Meikle A.W. Vitamin E and other antioxidants inhibit human prostate cancer cells through apoptosis. Prostate 2000, 44:287-295.
41. Hardeland R., Tan D.X., Reiter R.J. Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J. Pineal Res. 2009, 47:109-126.
42. Hattori A., Migitaka H., Iigo M., Itoh M., Yamamoto K., Ohtani-Kaneko R., Hara M., Suzuki T., Reiter R.J. Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates. Biochem. Mol. Biol. Int. 1995, 35:627-634.
43. Heazell A.E., Buttle H.R., Baker P.N., Crocker I.P. Altered expression of regulators of caspase activity within trophoblast of normal pregnancies and pregnancies complicated by preeclampsia. Reprod. Sci. 2008, 15:1034-1043.
44. Heazell A.E., Sahasrabudhe N., Grossmith A.K., Martindale E.A., Bhatia K. A case of intrauterine growth restriction in association with placental mesenchymal dysplasia with abnormal placental lymphatic development. Placenta 2009, 30:654-657.
45. Huppertz B., Frank H.G., Reister F., Kingdom J., Korr H., Kaufmann P. Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab. Invest. 1999, 79:1687-1702.
46. Iriti M., Varoni E.M., Vitalini S. Melatonin in traditional Mediterranean diets. J. Pineal Res. 2010, 49:101-105.
47. Ishihara N., Matsuo H., Murakoshi H., Laoag-Fernandez J.B., Samoto T., Maruo T. Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation. Am. J. Obstet. Gynecol. 2002, 186:158-166.
48. Jackson M.J. Skeletal muscle aging: role of reactive oxygen species. Crit. Care Med. 2009, 37:S368-S371.
49. Jedrychowski W., Maugeri U. An apple a day may hold colorectal cancer at bay: recent evidence from a case-control study. Rev. Environ. Health 2009, 24:59-74.
50. Jezek P., Hlavata L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int. J. Biochem. Cell. Biol. 2005, 37:2478-2503.
51. Joo S.S., Yoo Y.M. Melatonin induces apoptotic death in LNCaP cells via p38 and JNK pathways: therapeutic implications for prostate cancer. J. Pineal Res. 2009, 47:8-14.
52. Jou M.J., Peng T.I., Hsu L.F., Jou S.B., Reiter R.J., Yang C.M., Chiao C.C., Lin Y.F., Chen C.C. Visualization of melatonin's multiple mitochondrial levels of protection against mitochondrial Ca(2+)-mediated permeability transition and beyond in rat brain astrocytes. J. Pineal Res. 2010, 48:20-38.
53. Kale A., Soylemez F., Ensari A. Expressions of proliferation markers (Ki-67, proliferating cell nuclear antigen, and silver-staining nucleolar organizer regions) and of p53 tumor protein in gestational trophoblastic disease. Am. J. Obstet. Gynecol. 2001, 184:567-574.
54. Kaur C., Ling E.A. Antioxidants and neuroprotection in the adult and developing central nervous system. Curr. Med. Chem. 2008, 15:3068-3080.
55. Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 1972, 26:239-257.
56. Kim C.H., Yoo Y.M. Melatonin induces apoptotic cell death via p53 in LNCaP cells. Korean J. Physiol. Pharmacol. 2010, 14:365-369.
57. King A., Thomas L., Bischof P. Cell culture models of trophoblast II: trophoblast cell lines - a workshop report. Placenta 2000, 21(Suppl. A):S113-S119.
58. Kivela A. Serum melatonin during human pregnancy. Acta Endocrinol. (Copenh) 1991, 124:233-237.
59. Koh W., Jeong S.J., Lee H.J., Ryu H.G., Lee E.O., Ahn K.S., Bae H., Kim S.H. Melatonin promotes puromycin-induced apoptosis with activation of caspase-3 and 5'-adenosine monophosphate-activated kinase-alpha in human leukemia HL-60 cells. J. Pineal Res. 2011.
60. Korkmaz A., Reiter R.J., Topal T., Manchester L.C., Oter S., Tan D.X. Melatonin: an established antioxidant worthy of use in clinical trials. Mol. Med. 2009, 15:43-50.
61. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87:99-163.
62. Lakhani S.A., Masud A., Kuida K., Porter G.A., Booth C.J., Mehal W.Z., Inayat I., Flavell R.A. Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science 2006, 311:847-851.
63. Lala P.K., Lee B.P., Xu G., Chakraborty C. Human placental trophoblast as an in vitro model for tumor progression. Can. J. Physiol. Pharmacol. 2002, 80:142-149.
64. Lanoix D., Ouellette R., Vaillancourt C. Expression of melatoninergic receptors in human placental choriocarcinoma cell lines. Hum. Reprod. 2006, 21:1981-1989.
65. Lanoix D., Beghdadi H., Lafond J., Vaillancourt C. Human placental trophoblasts synthesize melatonin and express its receptors. J. Pineal Res. 2008, 45:50-60.
66. Lardone P.J., Guerrero J.M., Fernández-Santos J.M., Rubio A., Martín-Lacave I., Carrillo-Vico A. Melatonin synthesized by T lymphocytes as a ligand of the retinoid-acid related orphan receptor, RORα. J. Pineal Res. 2011.
67. Lee C.K., Kang H.S., Lee B.J., Kang H.M., Choi W.S., Kang S.G. Effects of dopamine and melatonin on the regulation of the PIT-1 isotype, placental growth hormone and lactogen gene expressions in the rat placenta. Mol. Cells 1999, 9:646-651.
68. Leja-Szpak A., Jaworek J., Pierzchalski P., Reiter R.J. Melatonin induces pro-apoptotic signaling pathway in human pancreatic carcinoma cells (PANC-1). J. Pineal Res. 2010, 49:248-255.
69. Maillard V., Kuriki K., Lefebvre B., Boutron-Ruault M.C., Lenoir G.M., Joulin V., Clavel-Chapelon F., Chajes V. Serum carotenoid, tocopherol and retinol concentrations and breast cancer risk in the E3N-EPIC study. Int. J. Cancer 2010, 127:1188-1196.
70. Malassiné A. Le placenta. Médecine-Science 2000, 16:329-335.
71. Maldonado M.D., Murillo-Cabezas F., Terron M.P., Flores L.J., Tan D.X., Manchester L.C., Reiter R.J. The potential of melatonin in reducing morbidity-mortality after craniocerebral trauma. J. Pineal Res. 2007, 42:1-11.
72. Mates J.M. Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 2000, 153:83-104.
73. Mates J.M., Segura J.A., Alonso F.J., Marquez J. Intracellular redox status and oxidative stress: implications for cell proliferation, apoptosis, and carcinogenesis. Arch. Toxicol. 2008, 82:273-299.
74. Mathai J.P., Germain M., Shore G.C. BH3-only BIK regulates BAX, BAK-dependent release of Ca2+ from endoplasmic reticulum stores and mitochondrial apoptosis during stress-induced cell death. J. Biol. Chem. 2005, 280:23829-23836.
75. Matuszak Z., Reszka K., Chignell C.F. Reaction of melatonin and related indoles with hydroxyl radicals: EPR and spin trapping investigations. Free Radic. Biol. Med. 1997, 23:367-372.
76. Mediavilla M.D., Sanchez-Barcelo E.J., Tan D.X., Manchester L., Reiter R.J. Basic mechanisms involved in the anti-cancer effects of melatonin. Curr. Med. Chem. 2010, 17:4462-4481.
77. Menendez-Pelaez A., Reiter R.J. Distribution of melatonin in mammalian tissues: the relative importance of nuclear versus cytosolic localization. J. Pineal Res. 1993, 15:59-69.
78. Menveille-Bourg F.J. La superoxyde dismutase, puissant antioxydant nsturel, désormais disponible par voie orale. Phytothérapie 2005, 3:118-121.
79. Miller S.C., Pandi-Perumal S.R., Esquifino A.I., Cardinali D.P., Maestroni G.J. The role of melatonin in immuno-enhancement: potential application in cancer. Int. J. Exp. Pathol. 2006, 87:81-87.
80. Mitchell M.D., Bibby J.G., Sayers L., Anderson A.B., Turnbull A.C. Melatonin in the maternal and umbilical circulations during human parturition. Br. J. Obstet. Gynaecol. 1979, 86:29-31.
81. Mounier C., Barbeau B., Vaillancourt C., Lafond J. Endocrinology and cell signaling in human villous trophoblast. Methods Mol. Biol. 2009, 550:89-102.
82. Muller K., Carpenter K.L., Challis I.R., Skepper J.N., Arends M.J. Carotenoids induce apoptosis in the T-lymphoblast cell line Jurkat E6.1. Free Radic. Res. 2002, 36:791-802.
83. Murch S.J., Hall B.A., Le C.H., Saxena P.K. Changes in the levels of indoleamine phytochemicals during veraison and ripening of wine grapes. J. Pineal Res. 2010, 49:95-100.
84. Nagata C., Nagao Y., Shibuya C., Kashiki Y., Shimizu H. Association of vegetable intake with urinary 6-sulfatoxymelatonin level. Cancer Epidemiol Biomarkers Prev. 2005, 14:1333-1335.
85. Nakamura Y., Tamura H., Kashida S., Takayama H., Yamagata Y., Karube A., Sugino N., Kato H. Changes of serum melatonin level and its relationship to feto-placental unit during pregnancy. J. Pineal Res. 2001, 30:29-33.
86. Namura S., Nagata I., Takami S., Masayasu H., Kikuchi H. Ebselen reduces cytochrome c release from mitochondria and subsequent DNA fragmentation after transient focal cerebral ischemia in mice. Stroke 2001, 32:1906-1911.
87. Neuzil J., Weber T., Terman A., Weber C., Brunk U.T. Vitamin E analogues as inducers of apoptosis: implications for their potential antineoplastic role. Redox Rep. 2001, 6:143-151.
88. Nosjean O., Nicolas J.P., Klupsch F., Delagrange P., Canet E., Boutin J.A. Comparative pharmacological studies of melatonin receptors: MT1, MT2 and MT3/QR2. Tissue distribution of MT3/QR2. Biochem. Pharmacol. 2001, 61:1369-1379.
89. Oberholzer C., Oberholzer A., Clare-Salzler M., Moldawer L.L. Apoptosis in sepsis: a new target for therapeutic exploration. FASEB J. 2001, 15:879-892.
90. Orrenius S., Gogvadze V., Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu. Rev. Pharmacol. Toxicol. 2007, 47:143-183.
91. Paternoster L., Radogna F., Accorsi A., Cristina Albertini M., Gualandi G., Ghibelli L. Melatonin as a modulator of apoptosis in B-lymphoma cells. Ann. N. Y. Acad. Sci. 2009, 1171:345-349.
92. Pelicano H., Carney D., Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist. Updat. 2004, 7:97-110.
93. Peschke E., Bach A.G., Muhlbauer E. Parallel signaling pathways of melatonin in the pancreatic beta-cell. J. Pineal Res. 2006, 40:184-191.
94. 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.
95. Pitkanen S., Robinson B.H. Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J. Clin. Invest. 1996, 98:345-351.
96. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N. Engl. J. Med. 2010, 362:329-344.
97. Reiter R.J., Paredes S.D., Manchester L.C., Tan D.X. Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin. Crit. Rev. Biochem. Mol. Biol. 2009, 44:175-200.
98. Reiter R.J., Tan D.X., Manchester L.C., Paredes S.D., Mayo J.C., Sainz R.M. Melatonin and reproduction revisited. Biol. Reprod. 2009, 81:445-456.
99. Richart R. Studies of placental morphogenesis. I. Radioautographic studies of human placenta utilizing tritiated thymidine. Proc. Soc. Exp. Biol. Med. 1961, 106:829-831.
100. Richter H.G., Hansell J.A., Raut S., Giussani D.A. Melatonin improves placental efficiency and birth weight and increases the placental expression of antioxidant enzymes in undernourished pregnancy. J. Pineal Res. 2009, 46:357-364.
101. Rodriguez C., Mayo J.C., Sainz R.M., Antolin I., Herrera F., Martin V., Reiter R.J. Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal Res. 2004, 36:1-9.
102. Sainz R.M., Mayo J.C., Rodriguez C., Tan D.X., Lopez-Burillo S., Reiter R.J. Melatonin and cell death: differential actions on apoptosis in normal and cancer cells. Cell. Mol. Life Sci. 2003, 60:1407-1426.
103. Sainz R.M., Mayo J.C., Tan D.X., Lopez-Burillo S., Natarajan M., Reiter R.J. Antioxidant activity of melatonin in Chinese hamster ovarian cells: changes in cellular proliferation and differentiation. Biochem. Biophys. Res. Commun. 2003, 302:625-634.
104. Sainz R.M., Mayo J.C., Tan D.X., Leon J., Manchester L., Reiter R.J. Melatonin reduces prostate cancer cell growth leading to neuroendocrine differentiation via a receptor and PKA independent mechanism. Prostate 2005, 63:29-43.
105. Smith S.C., Baker P.N., Symonds E.M. Increased placental apoptosis in intrauterine growth restriction. Am. J. Obstet. Gynecol. 1997, 177:1395-1401.
106. Sofic E., Rimpapa Z., Kundurovic Z., Sapcanin A., Tahirovic I., Rustembegovic A., Cao G. Antioxidant capacity of the neurohormone melatonin. J. Neural Transm. 2005, 112:349-358.
107. Soundararajan R., Rao A.J. Trophoblast 'pseudo-tumorigenesis': significance and contributory factors. Reprod. Biol. Endocrinol. 2004, 2:15.
108. Stege P.W., Sombra L.L., Messina G., Martinez L.D., Silva M.F. Determination of melatonin in wine and plant extracts by capillary electrochromatography with immobilized carboxylic multi-walled carbon nanotubes as stationary phase. Electrophoresis 2010, 31:2242-2248.
109. Sullivan M.H. Endocrine cell lines from the placenta. Mol. Cell. Endocrinol. 2004, 228:103-119.
110. Sunderland C.A., Naiem M., Mason D.Y., Redman C.W., Stirrat G.M. The expression of major histocompatibility antigens by human chorionic villi. J. Reprod. Immunol. 1981, 3:323-331.
111. Tamura H., Nakamura Y., Terron M.P., Flores L.J., Manchester L.C., Tan D.X., Sugino N., Reiter R.J. Melatonin and pregnancy in the human. Reprod. Toxicol. 2008, 25:291-303.
112. Tan D.X., Chen L.D., Poeggeler B., Manchester L., Reiter R. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocrine J. 1993, 1:57-60.
113. Tan D.X., Manchester L.C., Reiter R.J., Plummer B.F., Hardies L.J., Weintraub S.T., Vijayalaxmi, Shepherd A.M. A novel melatonin metabolite, cyclic 3-hydroxymelatonin: a biomarker of in vivo hydroxyl radical generation. Biochem. Biophys. Res. Commun. 1998, 253:614-620.
114. Tan D.X., Manchester L.C., Reiter R.J., Plummer B.F. Cyclic 3-hydroxymelatonin: a melatonin metabolite generated as a result of hydroxyl radical scavenging. Biol. Signals Recept. 1999, 8:70-74.
115. Tan D.X., Manchester L.C., Hardeland R., Lopez-Burillo S., Mayo J.C., Sainz R.M., Reiter R.J. Melatonin: a hormone, a tissue factor, an autocoid, a paracoid, and an antioxidant vitamin. J. Pineal Res. 2003, 34:75-78.
116. Than N.N., Heer C., Laatsch H., Hardeland R. Reactions of the melatonin metabolite N1-acetyl-5-methoxykynuramine (AMK) with the ABTS cation radical: identification of new oxidation products. Redox Rep. 2006, 11:15-24.
117. Tomas-Zapico C., Coto-Montes A. A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. J. Pineal Res. 2005, 39:99-104.
118. Tomas S.Z., Prusac I.K., Roje D., Tadin I. Trophoblast apoptosis in placentas from pregnancies complicated by preeclampsia. Gynecol. Obstet. Invest. 2011.
119. Vaillancourt C., Lanoix D., Le Bellego F., Daoud G., Lafond J. Involvement of MAPK signalling in human villous trophoblast differentiation. Mini Rev. Med. Chem. 2009, 9:962-973.
120. Valko M., Morris H., Cronin M.T. Metals, toxicity and oxidative stress. Curr. Med. Chem. 2005, 12:1161-1208.
121. Valko M., Rhodes C.J., Moncol J., Izakovic M., Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 2006, 160:1-40.
122. Winczyk K., Pawlikowski M., Karasek M. Melatonin and RZR/ROR receptor ligand CGP 52608 induce apoptosis in the murine colonic cancer. J. Pineal Res. 2001, 31:179-182.
123. Winczyk K., Pawlikowski M., Lawnicka H., Kunert-Radek J., Spadoni G., Tarzia G., Karasek M. Effects of melatonin and melatonin receptors ligand N-[(4-methoxy-1H-indol-2-yl)methyl]propanamide on murine Colon 38 cancer growth in vitro and in vivo. Neuroendocrinol. Lett. 2002, 23(Suppl. 1):50-54.
124. Wong S.Y., Ngan H.Y., Chan C.C., Cheung A.N. Apoptosis in gestational trophoblastic disease is correlated with clinical outcome and Bcl-2 expression but not Bax expression. Mod. Pathol. 1999, 12:1025-1033.
125. Yusuf K., Smith S.D., Sadovsky Y., Nelson D.M. Trophoblast differentiation modulates the activity of caspases in primary cultures of term human trophoblasts. Pediatr. Res. 2002, 52:411-415.
126. Zamzami N., Kroemer G. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell. Biol. 2001, 2:67-71.