Journal of Embryo Transfer (한국수정란이식학회지)

The Korean Society of Embryo Transfer (한국수정란이식학회)
권호 표지

Melatonin-induced Calbindin-D9k is Involved in Protecting Cells against Conditions That Cause Cell Death

  • Yoo, Yeong-Min (Laboratory of Veterinary Biochemistry and Molecular Biology, College of Veterinary Medicine, Chungbuk National University) ;
  • Jeung, Eui-Bae (Laboratory of Veterinary Biochemistry and Molecular Biology, College of Veterinary Medicine, Chungbuk National University)
  • Published : 2009.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Melatonin (N-acetyl-5-methoxytryptamine) is the major neurohormone secreted during the night by the vertebrate pineal gland. The circadian pattern of pineal melatonin secretion is related to the biological clock within the suprachiasmatic nucleus (SCN) of the hypothalamus in mammals. The SCN coordinates the body's rhythms to the environmental light-dark cycle in response to light perceived by the retina, which acts mainly on retinal ganglion cells that contain the photopigment melanopsin. Calbindin-D9k (CaBP-9k) is a member of the S100 family of intracellular calcium- binding proteins, and in this review, we discuss the involvement of melatonin and CaBP-9k with respect to calcium homeostasis and apoptotic cell death. In future studies, we hope to provide important information on the roles played by CaBP-9k in cell signal transduction, cell proliferation, and $Ca^{2+}$ homeostasis in vivo and in vitro.

Keywords

References

  1. Absi E, Ayala A, Machado A and Parrado J. 2000. Protective effect of melatonin against the 1-methyl-4-phenylpyridiniuminduced inhibition of complex I of the mitochondrial respiratory chain, J. Pineal. Res. 29:40-47 https://doi.org/10.1034/j.1600-079X.2000.290106.x
  2. Acuna-Castroviejo D, Martin M, Macias M, Escames G, Leon J, Khaldy H and Reiter RJ. 2001. Melatonin, mitochondria, and cellular bioenergetics. J. Pineal. Res. 30:65-74 https://doi.org/10.1034/j.1600-079X.2001.300201.x
  3. Ahlemeyer B, Beier H, Semkova I, Schaper C and Krieglstein J. 2000. S100$\beta$ protects cultured neurons against glutamateand stauroporine-induced damage and is involved in the antiapoptotic action of the 5HT1A-receptor agonist, Bay x 3702. Brain. Res. 858:121-128
  4. Alexanian AR and Bamburg JR. 1999. Neuronal survival activity of S100$\beta$ is enhanced by calcineurin inhibitors and requires activation of NF-kB. FASEB. J. 13:1611-1620
  5. Antolin I, Mayo JC, Sainz RM, del Brio ML, Herrera F, Martin V and Rodriguez C. 2002. Protective effect of melatonin in a chronic experimental model of Parkinson's disease, Brain. Res. 943:163-173 https://doi.org/10.1016/S0006-8993(02)02551-9
  6. Axelrod J and Wurtman RJ. 1968. Photic and neural control of indoleamine metabolism in the rat pineal gland. Adv. Pharmacol. 6:157-166 https://doi.org/10.1016/S1054-3589(08)61169-2
  7. Barger SW, Van Eldik LJ and Mattson MP. 1995. S100$\beta$ protects hippocampal neurons from damage induced by glucose deprivation. Brain. Res. 677:167-170 https://doi.org/10.1016/0006-8993(95)00160-R
  8. Baudier J, Delphin C, Grunwald D, Khochbin S and Lawrence JJ. 1992. Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein. Proc. Natl. Acad. Sci. USA. 89:11627-11631 https://doi.org/10.1073/pnas.89.23.11627
  9. Beal MF, Brouillet E, Jenkins BG, Ferrante RJ, Kowall NW, Miller JM, Storey E, Srivastava R, Rosen BR and Hyman BT. 1993. Neurochemical and histologic characterization of striatal excitotoxic lesion produced by the mitochondrial toxin 3-nitropropionic acid. J. Neurochem. 13: 4181-4192
  10. Berson DM, Dunn FA and Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073 https://doi.org/10.1126/science.1067262
  11. Bhattacharyya A, Oppenheim RW, Prevette D, Moore BW, Brackenbury R and Ratner N. 1992. S100 is present in developing chicken neurons and Schwann cells and promotes motor neuron survival in vitro. J. Neurobiol. 23:451-466 https://doi.org/10.1002/neu.480230410
  12. Brouillet E, Hantraye P, Ferrante RJ, Dolan R, Leroy-Willig A, Kowall NW and Beal MF. 1995. Chronic mitochondrial energy impairment produces selective striatal degeneration and abnormal choreiform movements in primates. Proc. Natl. Acad. Sci. USA. 92:7105-7109 https://doi.org/10.1073/pnas.92.15.7105
  13. Brouillet E, Jenkins BG, Hyman BT, Ferrante RJ, Kowall NW, Srivastava R, Roy DS, Rosen BR and Beal MF. 1993. Agedependent vulnerability of the striatum to the mitochondrial toxin 3-nitropropioni acid. J. Neurochem. 60: 56-359
  14. Bubenik GA. 2001. Localization, physiological significance and possible clinical implication of gastrointestinal melatonin. Biol. Signals. Recept. 10:350-366 https://doi.org/10.1159/000046903
  15. Buijs RM, Hermes MH and Kalsbeek A. 1998. The suprachiasmatic nucleus-paraventricular nucleus interactions: a bridge to the neuroendocrine and autonomic nervous system. Prog. Brain. Res. 119:365-382 https://doi.org/10.1016/S0079-6123(08)61581-2
  16. Cardinali DP and Pevet P. 1998. Basic aspects of melatonin action, Sleep. Med. Rev. 2:175-190 https://doi.org/10.1016/S1087-0792(98)90020-X
  17. Carrillo-Vico A, Calvo JR, Abreu P, Lardone PJ, Garcia-Maurino S, Reiter RJ and Guerrero JM. 2004. Evidence of melatonin synthesis by human lymphocytes and its physiological significance: possible role as intracrine, autocrine, and/or paracrine substance. FASEB. J. 18:537-539 https://doi.org/10.1096/fj.03-0694fje
  18. Carrillo-Vico A, Reiter RJ, Lardone PJ, Herrera JL, Fernandez-Montesinos R, Guerrero JM and Pozo D. 2006. The modulatory role of melatonin on immune responsiveness. Curr. Opin. Investig. Drugs. 7:423-431
  19. Carvalho AC, Sharpe J, Rosenstock TR, Teles AF, Youle RJ and Smaili SS. 2004. Bax affects intracellular $Ca^{2+}$ stores and induces $Ca^{2+}$ wave propagation. Cell. Death. Diff. 11: 1265-1276 https://doi.org/10.1038/sj.cdd.4401508
  20. Chen H, Fernig DG, Rudland PS, Sparks A, Wilkinson MC and Barraclough R. 2001. Binding to intracellular targets of the metastasis-inducing protein, S100A4 (p9Ka). Biochem. Biophys. Res. Commun. 286:1212-1217 https://doi.org/10.1006/bbrc.2001.5517
  21. Choi KC, Leung PC and Jeung EB. 2005. Biology and physiology of calbindin-D9k in female reproductive tissues: involvement of steroids and endocrine disruptors. Reprod. Biol. Endocrinol. 3: 66 https://doi.org/10.1186/1477-7827-3-66
  22. Chuang JI, Chen ST, Chang YH and Jen LS. 2001. Alteration of Bcl-2 expression in the nigrostriatal system after kainite injection with or without melatonin co-treatment. J. Chem. Neuroanat. 21:215-223 https://doi.org/10.1016/S0891-0618(01)00109-0
  23. Conti A, Conconi S, Hertens E, Skwarlo-Sonta K, Markowska M and Maestroni JM. Evidence for melatonin synthesis in mouse and human bone marrow cells. J. Pineal. Res. 28: 193-202 https://doi.org/10.1034/j.1600-079X.2000.280401.x
  24. Cos S, Gonzalez A, Martinez-Campa C, Mediavilla MD, Alonso-Gonzalez C and Sanchez-Barcelo EJ. 2008. Melatonin as a selective estrogen enzyme modulator. Curr. Cancer. Drug. Targets. 8:691-702 https://doi.org/10.2174/156800908786733469
  25. Dabbeni-Sala F, Di Santo S, Franceschini D, Skaper SD and Giusti P. 2001a. Melatonin protects against 6-OHDA-induced neurotoxicity in rats: a role for mitochondrial complex I activity. FASEB. J. 15:164-170 https://doi.org/10.1096/fj.00-0129com
  26. Dabbeni-Sala F, Floreani F, Franceschini D, S Skaper SD and Giusti P. 2001b. Kainic acid induces selective mitochondrial oxidative phosphorylation enzyme dysfunction in cerebellar granule neurons: protective effects of melatonin and GSH ethyl ester. FASEB. J. 15:1786-1788 https://doi.org/10.1096/fj.00-0427fje
  27. Dijk DJ and von Schantz M. 2005. Timing and consolidation of human sleep, wakefulness, and performance by a symphony of oscillators. J. Biol. Rhythms. 20:279-290 https://doi.org/10.1177/0748730405278292
  28. Donato R. 1999. Functional roles of S100 proteins, calciumbinding proteins of the EF-hand type. Biochim. Biophys. Acta. 1450:191-231 https://doi.org/10.1016/S0167-4889(99)00058-0
  29. Donato R. 2001. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int. J. Biochem. Cell. Biol. 33:637-668 https://doi.org/10.1016/S1357-2725(01)00046-2
  30. Emberley ED, Murphy LC and Watson PH. 2004. S100 proteins and their influence on pro-survival pathways in cancer. Biochem. Cell. Biol. 82:508-515 https://doi.org/10.1139/o04-052
  31. Fulle S, Pietrangelo T, Mariggio MA, Lorenzon P, Racanicchi L, Mozrzymas J, Guarnieri S, Zucconi-Grassi G and Fano G. 2000. Calcium and fos involvement in brain-derived $Ca^{2+}$ binding protein (S100)-dependent apoptosis in rat phaeochromocytoma cells. Exp. Physiol. 85:243-253 https://doi.org/10.1017/S0958067000019746
  32. Gastel JA, Roseboom PH, Rinaldi PA, Weller JL and Klein DC. 1998. Melatonin production: proteasomal proteolysis in serotonin N-acetyltransferase regulation. Science 279:1358- 1360 https://doi.org/10.1126/science.279.5355.1358
  33. Goncalves DS, Lenz G, Karl J, Gonçalves CA and Rodnight R. 2000. Extracellular S100B protein modulates ERK in astrocyte cultures. NeuroReport. 11:807-809 https://doi.org/10.1097/00001756-200003200-00030
  34. Grossman E, Laudon M, Yalcin R, Zengil H, Peleg E, Sharabi Y, Kamari Y, Shen-Orr Z and Zisapel N. 2006. Melatonin reduces night blood pressure in patients with nocturnal hypertension. Am. J. Med. 119:898-902 https://doi.org/10.1016/j.amjmed.2006.02.002
  35. Haglid KG, Yang Q, Hamberger A, Bergman S, Widerberg A and Danielsen N. 1997. S100$\beta$ stimulates neurite outgrowth in the rat sciatic nerve grafted with acellular muscle transplants. Brain. Res. 753:196-201 https://doi.org/10.1016/S0006-8993(96)01463-1
  36. Haimov I, Laudon M, Zisapel N, Souroujon M, Nof D, Shlitner A, Herer P, Tzischinsky O and Lavie P. 1994. Sleep disorders and melatonin rhythms in elderly people. BMJ. 309:167 https://doi.org/10.1136/bmj.309.6948.167
  37. Hardeland R, Tan DX and Reiter RJ. 2009. Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J. Pineal. Res. 47:109-126 https://doi.org/10.1111/j.1600-079X.2009.00701.x
  38. Hardeland R. 2005. Antioxidative protection by melatonin: multiplicity of mechanisms from radical detoxification to radical avoidance, Endocrine. 27:119-130 https://doi.org/10.1385/ENDO:27:2:119
  39. Heizmann CW, Fritz G and Schafer BW. 2002. S100 proteins: structure, functions and pathology. Front. Biosci. 7: d1356-d1368 https://doi.org/10.2741/heizmann
  40. Ho AK and Klein DC. 1987. Activation of alpha 1-adrenoceptors, protein kinase C, or treatment with intracellular free $Ca^{2+}$ elevating agents increases pineal phospholipase A2 activity. Evidence that protein kinase C may participate in $Ca^{2+}$-dependent alpha 1-adrenergic stimulation of pineal phospholipase A2 activity. J. Biol. Chem. 262:11764-11770
  41. Hsu Y-T, Wolter K and Youle RJ. 1997. Cytosol-to-membrane redistribution of Bax and Bcl-x(l) during apoptosis. Proc. Natl. Acad. Sci. USA. 94:3668-3672 https://doi.org/10.1073/pnas.94.8.3668
  42. Hu J, Ferreira A and Van Eldik LJ. 1997. S100$\beta$ induces neuronal cell death through nitric oxide release from astrocytes. J. Neurochem. 69:2294-2301 https://doi.org/10.1046/j.1471-4159.1997.69062294.x
  43. Hung MW, Tipoe GL, Poon AM, Reiter RJ and Fung ML. 2008. Protective effect of melatonin against hippocampal injury of rats with intermittent hypoxia, J. Pineal. Res. 44: 214-221 https://doi.org/10.1111/j.1600-079X.2007.00514.x
  44. Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R and Rauvala H. 2000. Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. J. Biol. Chem. 275:40096-40105 https://doi.org/10.1074/jbc.M006993200
  45. Iwasaki Y, Shiojima T and Kinoshita M. 1997. S100$\beta$ prevents the death of motor neurons in newborn rats after sciatic nerve section. J. Neurol. Sci. 151:7-12 https://doi.org/10.1016/S0022-510X(97)00073-7
  46. Jou MJ, Jou SB, Guo MJ, Wu HY and Peng TI. 2009a. Mitochondrial reactive oxygen species generation and calcium increase induced by visible light in astrocytes. Ann. N. Y. Acad. Sci. 1011:45-56 https://doi.org/10.1196/annals.1293.005
  47. Jou MJ, Peng TI, Hsu LF, Jou SB, Reiter RJ, Yang CM, Chiao CC, Lin YF and Chen CC. 2009b. Visualization of melatonin's multiple mitochondrial levels of protection against mitochondrial Ca-mediated permeability transition and beyond in rat brain astrocytes. J. Pineal. Res. in press https://doi.org/10.1111/j.1600-079X.2009.00721.x
  48. Jou MJ, Peng TI, Reiter RJ, Jou SB, Wu HY and Wen ST. 2004. Visualization of the antioxidative effects of melatonin at the mitochondrial level during oxidative stress-induced apoptosis of rat brain astrocytes. J. Pineal. Res. 37:55-70 https://doi.org/10.1111/j.1600-079X.2004.00140.x
  49. Jou MJ, Peng TI, Yu PZ, Jou SB, Reiter RJ, Chen JY, Wu HY, Chen CC and Hsu LF. 2007. Melatonin protects against common deletion of mitochondrial DNA-augmented mitochondrial oxidative stress and apoptosis. J. Pineal. Res. 43:389-403 https://doi.org/10.1111/j.1600-079X.2007.00490.x
  50. Karasek M. 2004. Melatonin, human aging, and age-related diseases. Exp. Gerontol. 39:1723-1729 https://doi.org/10.1016/j.exger.2004.04.012
  51. Kim YJ, Lee GS, Hyun SH, Ka HH, Choi KC, Lee CK and Jeung EB. 2009. Uterine expression of epidermal growth factor family during the course of pregnancy in pigs. Reprod. Domest. Anim. 44:797-804 https://doi.org/10.1111/j.1439-0531.2008.01082.x
  52. Klein DC and Moore RY. 1979. Pineal N-acetyltransferase and hydroxyindole-O-methyltransferase: control by the retinohypothalamic tract and the suprachiasmatic nucleus. Brain. Res. 174:245-262 https://doi.org/10.1016/0006-8993(79)90848-5
  53. Klein DC, Ganguly S, Coon S, Weller JL, Obsil T, Hickman A and Dyda F. 2002. 14-3-3 Proteins and photoneuroendo crine transduction: role in controlling the daily rhythm in melatonin. Biochem. Soc. Trans. 30:365-73 https://doi.org/10.1042/BST0300365
  54. Klein DC, Weller JL and Moore RY. 1971. Melatonin metabolism:neural regulation of pineal serotonin: acetyl coenzyme A N-acetyltransferase activity. Proc. Natl. Acad. Sci. USA. 68:3107-3110 https://doi.org/10.1073/pnas.68.12.3107
  55. Kligman D and Marshak DR. 1985. Purification and characterization of a neurite extension factor from bovine brain. Proc. Natl. Scad. Sci. USA. 82:7136-7139 https://doi.org/10.1073/pnas.82.20.7136
  56. Krajewski S, Krajewska M, Ellerby LM, Welsh K, Xie Z, Deveraux QL, Salvesen GS, Bredesen DE, Rosenthal RE, Fiskum G and Reed JC. 1999. Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc. Natl. Acad. Sci. USA. 96:5752-5757 https://doi.org/10.1073/pnas.96.10.5752
  57. Krajewski S, Krajewski M, Shabaik A, MIyashita, Wang HG and Reed JC. 1994. Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am. J. Pathol. 145:1326-1336
  58. Krause DN and Dubocovich ML. 1990. Regulatory sites in the melatonin system of mammals. Trends. Neurosci. 13:464-470 https://doi.org/10.1016/0166-2236(90)90100-O
  59. LeBlanc H, Lawrence D, Varfolomeev E, Totpal K, Morlan J, Schow P, Fong S, Schwall R, Sinicropi D and Ashkenazi A. 2002. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat. Med. 8:274-281 https://doi.org/10.1038/nm0302-274
  60. Lee GS, Choi KC, Park SM, An BS, Cho MC and Jeung EB. 2003. Expression of human Calbindin-D(9k) correlated with age, vitamin D receptor and blood calcium level in the gastrointestinal tissues. Clin. Biochem. 36: 255-261 https://doi.org/10.1016/S0009-9120(03)00010-9
  61. Leger D, Laudon M and Zisapel N. 2004. Nocturnal 6-sulfatoxymelatonin excretion in insomnia and its relation to the response to melatonin replacement therapy. Am. J. Med. 116:91-95 https://doi.org/10.1016/j.amjmed.2003.07.017
  62. Lerner AB, Case JD, Takahashi Y, Lee TH and Mori W. 1958. Isolation of melatonin, the pineal gland factor that lightens melanocytes. J. Am. Chem. Soc. 80:2587
  63. Li H, Zhu H, Xu CJ and Yuan J. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:491-501 https://doi.org/10.1016/S0092-8674(00)81590-1
  64. Ling X, Zhang LM, Lu SD Li XJ and Sun FY. 1999. Protective effect of melatonin on injuried cerebral neurons is associated with bcl-2 protein over-expression. Zhongguo. Yao. Li. Xue. Bao. 20:409-414
  65. Mariggio MA, Fulle S, Calissano P, Nicoletti I and Fano G. 1994. The brain protein S100ab induces apoptosis in PC12 cells. Neuroscience. 60:29-35 https://doi.org/10.1016/0306-4522(94)90201-1
  66. McCord CP and Fallen FP. 1917. Evidence associating pineal gland function with alterations in pigmentation. J. Exp. Zool. 23:207-224 https://doi.org/10.1002/jez.1400230108
  67. Most P, Boerries M, Eicher C, Schweda C, Ehlermann P, Pleger ST, Loeffler E, Koch WJ, Katus HA, Schoenenberger CA and Remppis A. 2003. Extracellular S100A1 protein inhibits apoptosis in ventricular cardiomyocytes via activation of the extracellular signal-regulated protein kinase 1/2 (ERK1/2). J. Biol. Chem. 278:48404-48412 https://doi.org/10.1074/jbc.M308587200
  68. Mueller A, Schafer BW, Ferrari S, Weibel M, Makek M, Hochli M and Heizmann CW. 2005. The calcium-binding protein S100A2 interacts with p53 and modulates its transcriptional activity. J. Biol. Chem. 280:29186-29193 https://doi.org/10.1074/jbc.M505000200
  69. Nava M, Romero F, Quiroz Y, Parra G, Bonet L and Rodriguez-Iturbe B. 2000. Melatonin attenuates acute renal failure and oxidative stress induced by mercuric chloride in rats. Am. J. Physiol. 279:F910-918
  70. Novitskaya V, Grigorian M, Kriajevska M, Tarabykina S, Bronstein I, Berezin V, Bock E and Lukanidin E. 2000. Oligomeric forms of the metastasis related Mts1 (S100A4) protein, stimulate neuronal differentiation in cultures of rat hippocampal neurons. J. Biol. Chem. 275:41278-41286 https://doi.org/10.1074/jbc.M007058200
  71. Nutt LK, Pataer A, Pahler J, Fang B, Roth J, McConkey DJ and Swisher SG. 2001. Bax and Bak promote apoptosis by modulating endoplasmic reticular and mitochondrial $Ca^{2+}$ stores. J. Biol. Chem. 277:20301-20308 https://doi.org/10.1074/jbc.M201604200
  72. Ortiz GG, Crespo-Lopez ME, Moran-Moguel C, Garcia JJ, Reiter RJ and Acuna-Castroviejo D. 2001. Protective role of melatonin against MPTP-induced mouse brain cell DNA fragmentation and apoptosis in vivo. Neuroendocrinology. Lett. 22:101-108
  73. Pan Z, Bhat MB, Nieminen AL and Ma J. 2001. Synergistic movements of $Ca^{2+}$ and Bax in cells undergoing apoptosis. J. Biol. Chem. 276:32257-32263 https://doi.org/10.1074/jbc.M100178200
  74. Pandi-Perumal SR, Smits M, Spence W, Srinivasan V, Cardinali DP, Lowe AD and Kayumov L. 2007. Dim light melatonin onset (DLMO): a tool for the analysis of circadian phase in human sleep and chronobiological disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry. 31:1-11 https://doi.org/10.1192/pb.31.1.1
  75. Pappolla MA, Chyan YJ, Poeggeler B, Frangione B, Wilson G, Ghiso J and Reiter RJ. 2000. An assessment of the antioxidant and the antiamyloidogenic properties of melatonin: implications for Alzheimer's disease. J. Neural. Transm. 107:203-231 https://doi.org/10.1007/s007020050018
  76. Peyrot F and Ducrocq C. 2008. Potential role of tryptophan derivatives in stress responses characterized by the generation of reactive oxygen and nitrogen species. J. Pineal. Res. 45:235-246 https://doi.org/10.1111/j.1600-079X.2008.00580.x
  77. Pizarro JG, Yeste-Velasco M, Esparza JL, Verdaguer E, Pallàs M, Camins A and Folch J. 2008. The antiproliferative activity of melatonin in B65 rat dopaminergic neuroblastoma cells is related to the downregulation of cell cycle-related genes. J. Pineal. Res. 45:8-16 https://doi.org/10.1111/j.1600-079X.2007.00548.x
  78. Reiter RJ, Paredes SD, Manchester LC and Tan DX. 2009. Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin. Crit. Rev. Biochem. Mol. Biol. 44:175-200 https://doi.org/10.1080/10409230903044914
  79. Reiter RJ, Tan DX and Korkmaz A. 2009. The circadian melatonin rhythm and its modulation: possible impact on hypertension. J. Hypertens. 27: Suppl. 6, S17-20 https://doi.org/10.1097/01.hjh.0000358832.41181.bf
  80. Reiter RJ, Tan DX, Korkmaz A, Erren TC, Piekarski C, Tamura H and Manchester LC. 2007a. Light at night, chronodisruption, melatonin suppression, and cancer risk: a review. Crit. Rev. Oncog. 13:303-328 https://doi.org/10.1615/CritRevOncog.v13.i4.30
  81. Reiter RJ, Tan DX, Terron MP, Flores LJ and Czarnocki Z. 2007b. Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta. Biochim. Pol. 54:1-9
  82. Reiter RJ. 1980. Photoperiod: its importance as an impeller of pineal and seasonal reproductive rhythms. Int. J. Biometeorol. 24:57-63 https://doi.org/10.1007/BF02245542
  83. Reiter RJ. 1998. Cytoprotective properties of melatonin: presumed association with oxidative damage and aging. Nutrition. 14:691-696 https://doi.org/10.1016/S0899-9007(98)00064-1
  84. Rizzuto R and Pozzan T. 2006. Microdomains of intracellular $Ca^{2+}$: molecular determinants and functional consequences. Physiol. Rev. 86:369-408 https://doi.org/10.1152/physrev.00004.2005
  85. Rodriguez C, Mayo JC, Sainz RM, Antolin I, Herrera F, Martin V and Reiter RJ. 2004. Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal. Res. 36:1-9 https://doi.org/10.1046/j.1600-079X.2003.00092.x
  86. Rong Y and Distelhorst CW. 2008. Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu. Rev. Physiol. 70:73-91 https://doi.org/10.1146/annurev.physiol.70.021507.105852
  87. Sainz RM, Reiter RJ, Tan DX, Roldan F, Natarajan M, Quiros I, Hevia D, Rodriguez C and Mayo JC. 2008. Critical role of glutathione in melatonin enhancement of tumor necrosis factor and ionizing radiation-induced apoptosis in prostate cancer cells in vitro. J. Pineal. Res. 45:258-270 https://doi.org/10.1111/j.1600-079X.2008.00585.x
  88. Samantaray S, Sribnick EA, Das A, Knaryan VH, Matzelle DD, Yallapragada AV, ReiterRJ, Ray SK and Banik NL. 1008. Melatonin attenuates calpain upregulation, axonal damage, and neuronal death in spinal cord injury, J. Pineal. Res. 44:348-357 https://doi.org/10.1111/j.1600-079X.2007.00534.x
  89. Schafer BW and Heizmann CW. 1996. The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends. Biochem. Sci. 21:134-140 https://doi.org/10.1016/S0968-0004(96)80167-8
  90. Scheer FA, Van Montfrans GA, van Someren EJ, Mairuhu G and Buijs RM. 2004. Daily nighttime melatonin reduces blood pressure in male patients with essential hypertension. Hypertension. 43:192-197 https://doi.org/10.1161/01.HYP.0000113293.15186.3b
  91. Schernhammer ES and Hankinson SE. 2009. Urinary melatonin levels and postmenopausal breast cancer risk in the Nurses' Health Study cohort. Cancer. Epidemiol. Biomarkers. Prev. 18:74-79 https://doi.org/10.1158/1055-9965.EPI-08-0637
  92. Schomerus C and Korf HW. 2005. Mechanisms regulating melatonin synthesis in the mammalian pineal organ. Ann. N. Y. Acad. Sci. 1057:372-383 https://doi.org/10.1196/annals.1356.028
  93. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T and Korsmeyer SJ. 2003. BAX and BAK regulation of endoplasmic reticulum $Ca^{2+}$: a control point for apoptosis. Science 300: 135-139 https://doi.org/10.1126/science.1081208
  94. Siu AW, Maldonado M, Sanchez-Hidalgo M, Tan DX and Reiter RJ. 2006. Protective effects of melatonin in experimental free radical-related ocular diseases. J. Pineal. Res. 40:101-109 https://doi.org/10.1111/j.1600-079X.2005.00304.x
  95. Slominski A, Fischer TW, Zmijewski MA, Wortsman J, Semak I, Zbytek B, Slominski RM and Tobin DJ. 2005. On the role of melatonin in skin physiology and pathology. Endocrine. 27:137-148 https://doi.org/10.1385/ENDO:27:2:137
  96. Smaili SS and Russell JT. 1999. Permeability transition pore regulates both mitochondrial membrane potential and agonist-evoked $Ca^{2+}$ signals in oligodendrocytes progenitors. Cell. Calcium. 26:121-130 https://doi.org/10.1054/ceca.1999.0061
  97. Smaili SS, Hsu YT, Sander K, Russell JT and Youle RJ. 2001. Bax translocation to mitochondria subsequent to a rapid loss of mitochondrial membrane potential. Cell. Death. Differ. 8: 909-920 https://doi.org/10.1038/sj.cdd.4400889
  98. Smaili SS, Hsu YT, Youle RJ and Russell JT. 2000. Mitochondria in $Ca^{2+}$ Signaling and Apoptosis. J. Bioenerg. Biomembr. 32:35-46 https://doi.org/10.1023/A:1005508311495
  99. Smaili SS, Rosenstock TR and Hsu Y-T. 2008. Evaluation of some cell death features by real-time, real-space microscopy. Methods. Enzymol. 442:27-50 https://doi.org/10.1016/S0076-6879(08)01402-X
  100. Smith TS and Bennett JP Jr. 1997. Mitochondrial toxins in neurodegenerative diseases: In vivo brain hydroxyl radical production during systemic MPTP treatment or following microdialysis infusion of methylpyridinium or azide ions. Brain. Res. 765:183-186 https://doi.org/10.1016/S0006-8993(97)00429-0
  101. Srinivasan V, Maestroni GJ, Cardinali DP, Esquifino AI, Perumal SR and Miller SC. Melatonin, immune function and aging. Immun. Ageing. 2:17 https://doi.org/10.1186/1742-4933-2-17
  102. Tan DX, Chen LD, Poeggeler B and Reiter RJ. 1993. Melatonin; a potent, endogenous hydroxyl radical scavenger. Endocr. J. 1:57-60
  103. Tan DX, Reiter RJ, Manchester LC, Yan MT, El-Sawi M, Sainz RM, Mayo JC, Kohen R, Allegra M and Hardeland R. 2002. Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger, Curr. Top. Med. Chem. 2:181-197 https://doi.org/10.2174/1568026023394443
  104. Tinnanooru P, Dang VH, Nguyen TH, Lee GS, Choi KC and Jeung EB. 2008. Estrogen regulates the localization and expression of calbindin-D9k in the pituitary gland of immature male rats via the ERalpha-pathway. Mol. Cell. Endocrinol. 285:26-33 https://doi.org/10.1016/j.mce.2008.01.011
  105. Tosini G and Menaker M. 1998. The clock in the mouse retina: melatonin synthesis and photoreceptor degeneration. Brain. Res. 789:221-228 https://doi.org/10.1016/S0006-8993(97)01446-7
  106. Tricoire H, Moller M, Chemineau P and Malpaux B. 2003. Origin of cerebrospinal fluid melatonin and possible function in the integration of photoperiod. Reprod. Suppl. 61:311-321
  107. Ueda S, Leonardi ETK, Bell J and Azmitia EC. 1995. Serotoninergic sprouting into transplanted C-6 gliomas is blocked by S100$\beta$ antisense gene. Mol. Brain. Res. 29:365-368 https://doi.org/10.1016/0169-328X(94)00269-K
  108. Vacas MI, Lowenstein P and Cardinali DP. 1980. Dihydroergocryptine binding sites in bovine and rat pineal glands, J. Auton. Nerv. Syst. 2:305-313 https://doi.org/10.1016/0165-1838(80)90029-6
  109. Van Eldik LJ, Christie-Pope B, Bolin LM, Shooter EM and Whetsell WO Jr. 1991. Neurotrophic activity of S100$\beta$ in cultured dorsal root ganglia from embryonic chick and fetal rat. Brain. Res. 542:280-285 https://doi.org/10.1016/0006-8993(91)91579-P
  110. Wang S, Rosengren LE, Franlund M, Hamberger A and Haglid KG. 1999. Bcl-2 expression regulates cell sensitivity to S100$\beta$-mediated apoptosis. Mol. Brain Res. 70:167-176 https://doi.org/10.1016/S0169-328X(99)00145-X
  111. Whitaker-Azmitia PM, Murphy R and Azmitia EC. 1990. S100 protein is released from astroglial cells by stimulation of 5-HT1A receptors. Brain. Res. 528:155-158 https://doi.org/10.1016/0006-8993(90)90210-3
  112. Winningham-Major F, Staecker JL, Barger SW, Coats S and Van Eldik LJ. 1989. Neurite extension and neuronal survival activities of recombinant S100$\beta$ proteins that differ in the content and position of cysteine residues. J. Cell. Biol. 109: 3036-3071 https://doi.org/10.1083/jcb.109.6.3063
  113. Yang E and Korsmeyer SJ. 1996. Molecular apoptosis: a discourse on the Bcl-2 family and cell death. Blood. 88:386-401
  114. Yoo YM and Jeung EB. 2010. Melatonin-induced calbindin-D9k expression reduces hydrogen peroxide-mediated cell death in rat pituitary GH3 cells. J. Pineal. Res. in press https://doi.org/10.1111/j.1600-079X.2009.00730.x
  115. Yoo YM, Yim SV, Kim SS, Jang HY, Lea HZ, Hwang GC, Kim JW, Kim SA, Lee HJ, Kim CJ, Chung JH and Leem KH. 2002. Melatonin suppresses NO-induced apoptosis via induction of Bcl-2 expression in PGT-beta immortalized pineal cells. J. Pineal. Res. 33:146-150 https://doi.org/10.1034/j.1600-079X.2002.02899.x
  116. Youle RJ and Strasser A. 2008. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell. Biol. 9:47-59 https://doi.org/10.1038/nrm2308
  117. Zisapel N. 2001. Melatonin-dopamine interactions: from basic neurochemistry to a clinical setting. Cell. Mol. Neurobiol. 21:605-616 https://doi.org/10.1023/A:1015187601628
  118. Zisapel N. 2007. Sleep and sleep disturbances: biological basis and clinical implications. Cell. Mol. Life. Sci. 64:1174-1186 https://doi.org/10.1007/s00018-007-6529-9
  119. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J and Thompson CB. 2003. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell. Biol. 162:59-69 https://doi.org/10.1083/jcb.200302084