Protective effect of melatonin against human leukocyte apoptosis induced by intracellular calcium overload: Relation with its antioxidant actions

Journal of Pineal Research

Volumn 51, Issue 2, 2011, Pages 195-206

  Espino, Javier ^a   Bejarano, Ignacio ^a   Paredes, Sergio D ^a   Barriga, Carmen ^a   Rodríguez, Ana B ^a   Pariente, José A ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

Author keywords

antioxidants; calcium signal; caspases; leukocytes; melatonin; mitochondria

Indexed keywords

CALCIUM; DNA; FORMYLMETHIONYLLEUCYLPHENYLALANINE; MELATONIN; REACTIVE OXYGEN METABOLITE; THAPSIGARGIN;

ADULT; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL PROTECTION; CYTOSOL; DNA FRAGMENTATION; FEMALE; HUMAN; HUMAN EXPERIMENT; INCUBATION TIME; LEUKOCYTE; MALE; NORMAL HUMAN;

ACETYLCYSTEINE; ADULT; APOPTOSIS; CALCIUM; CHELATING AGENTS; DNA FRAGMENTATION; EGTAZIC ACID; ENZYME INHIBITORS; FEMALE; FREE RADICAL SCAVENGERS; HUMANS; LEUKOCYTES; MALE; MELATONIN; MIDDLE AGED; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; REACTIVE OXYGEN SPECIES; RUTHENIUM COMPOUNDS; THAPSIGARGIN;

EID: 80051667506     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2011.00876.x     Document Type: Article

References (56)

1. Kerr JFR, Wyllie AH, Currie AR,. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239-257.
2. Thompson CB,. Apoptosis in the pathogenesis and treatment of disease. Science 1995; 267: 1456-1462.
3. Wesche-Soldato DE, Swan RZ, Chung CS, et al., The apoptotic pathway as a therapeutic target in sepsis. Curr Drug Targets 2007; 8: 493-500. (Pubitemid 46672616)
4. Bolitho P, Voskoboinik I, Trapani JA, et al., Apoptosis induced by the lymphocyte effector molecule perforin. Curr Opin Immunol 2007; 19: 339-347. (Pubitemid 46687012)
5. Ravichandran KS, Lorenz U,. Engulfment of apoptotic cells: signals for a good meal. Nat Rev Immunol 2007; 7: 964-974. (Pubitemid 350166061)
6. Schlegel RA, Williamson P,. Phosphatidylserine, a death knell. Cell Death Differ 2001; 8: 551-563. (Pubitemid 32586592)
7. Brookes PS, Yoon Y, Robotham JL, et al., Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004; 287: 817-833.
8. Espino J, Bejarano I, Redondo PC, et al., Melatonin reduces apoptosis induced by calcium signaling in human leukocytes: evidence for the involvement of mitochondria and Bax activation. J Membr Biol 2010; 233: 105-118.
9. Tan S, Sagara Y, Liu Y, et al., The regulation of reactive oxygen species production during programmed cell death. J Cell Biol 1998; 141: 1423-1432. (Pubitemid 28289917)
10. Tan DX, Hardeland R, Manchester LC, et al., The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness. Biol Rev Camb Philos Soc 2010; 85: 607-623.
11. Paredes SD, Korkmaz A, Manchester LC, et al., Phytomelatonin: a review. J Exp Bot 2009; 60: 57-69.
12. Reiter RJ, Tan DX, Manchester LC, et al., Melatonin and reproduction revisited. Biol Reprod 2009; 81: 445-456.
13. Rosenstein RE, Pandi-Perumal SR, Srinivasan V, et al., Melatonin as a therapeutic tool in ophthalmology: implications for glaucoma and uveitis. J Pineal Res 2010; 49: 1-13.
14. Reiter RJ, Paredes SD, Manchester LC, et al., Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin. Crit Rev Biochem Mol Biol 2009; 44: 175-200.
15. Hardeland R, Tan DX, Reiter RJ, et al., Kynuramines metabolites of melatonin and other indoles. The resurrection of an almost forgotten class of biogenic amines. J Pineal Res 2009; 47: 109-126.
16. Juknat AA, Mendez Mdel V, Quaglino A, et al., Melatonin prevents hydrogen peroxide-induced Bax expression in cultured rat astrocytes. J Pineal Res 2005; 38: 84-92. (Pubitemid 40293232)
17. Mayo JC, Sainz RM, Uria H, et al., Inhibition of cell proliferation: a mechanism likely to mediate the prevention of neuronal cell death by melatonin. J Pineal Res 1998; 25: 12-18. (Pubitemid 28319911)
18. Menendez-Pelaez A, Reiter RJ,. Distribution of melatonin in mammalian tissues: the relative importance of nuclear versus cytosolic localization. J Pineal Res 1993; 15: 59-69. (Pubitemid 24028611)
19. Reiter RJ, Paredes SD, Korkmaz A, et al., Melatonin combats molecular terrorism at the mitochondrial level. Interdiscip Toxicol 2008; 1: 137-149.
20. Paradies G, Petrosillo G, Paradies V, et al., Melatonin, cardiolipin and mitochondrial bioenergetics in health and disease. J Pineal Res 2010; 48: 297-310.
21. Sainz RM, Mayo JC, Rodríguez C, et al., Melatonin and cell death: differential actions on apoptosis in normal and cancer cells. Cell Mol Life Sci 2003; 60: 1407-1426. (Pubitemid 36900523)
22. Paredes SD, Terrón MP, Marchena AM, et al., Tryptophan modulates cell viability, phagocytosis and oxidative metabolism in old ringdoves. Basic Clin Pharmacol Toxicol 2007; 101: 56-62. (Pubitemid 46934651)
23. Carrillo-Vico A, Reiter RJ, Lardone PJ, et al., The modulatory role of melatonin on immune responsiveness. Curr Opin Investig Drugs 2006; 7: 423-431. (Pubitemid 43772981)
24. Tan DX, Manchester LC, Reiter RJ, et al., Identification of highly elevated levels of melatonin in bone marrow: its origin and significance. Biochim Biophys Acta 1999; 1472: 206-214. (Pubitemid 29486531)
25. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985; 260: 3440-3450. (Pubitemid 15114340)
26. Rothe G, Oser A, Valet G,. Dihydrorhodamine 123: a new flow cytometric indicator for respiratory burst activity in neutrophil granulocytes. Naturwissenschaften 1988; 75: 354-355.
27. Emmendörffer A, Hecht M, Lohmann-Matthes ML, et al., A fast and easy method to determine the production of reactive oxygen intermediates by human and murine phagocytes using dihydrorhodamine 123. J Immunol Methods 1990; 131: 269-275. (Pubitemid 20241527)
28. Bejarano I, Redondo PC, Espino J, et al., Melatonin induces mitochondrial-mediated apoptosis in human myeloid HL-60 cells. J Pineal Res 2009; 46: 392-400.
29. Espino J, Bejarano I, Paredes SD, et al., Melatonin is able to delay endoplasmic reticulum stress-induced apoptosis in leukocytes from elderly humans. Age (Dordr) 2010 (in press). doi: 10.1007/s11357-010-9194-0.
30. Nicholson DW, Ali A, Thornberry NA, et al., Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995; 376: 37-43.
31. Li P, Nijhawan D, Budihardjo I, et al., Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997; 91: 479-489. (Pubitemid 27508237)
32. Zou H, Li Y, Liu X, et al., An APAF-1-cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 1999; 274: 11549-11556.
33. Heatwole VM,. TUNEL assay for apoptotic cells. Methods Mol Biol 1999; 115: 141-148.
34. Orrenius S, Zhivotovsky B, Nicotera P,. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003; 4: 552-565. (Pubitemid 36773407)
35. Hajnóczky G, Davis E, Madesh M,. Calcium and apoptosis. Biochem Biophys Res Commun 2003; 304: 445-454.
36. 2+ uptake in apoptosis. Cell Calcium 2006; 40: 553-560. (Pubitemid 44660721)
37. Bejarano I, Lozano GM, Ortiz A, et al., Caspase 3 activation in human spermatozoa in response to hydrogen peroxide and progesterone. Fertil Steril 2008; 90: 1340-1347.
38. Pariente JA, Camello C, Camello PJ, et al., Release of calcium from mitochondrial and nonmitochondrial intracellular stores in mouse pancreatic acinar cells by hydrogen peroxide. J Membr Biol 2001; 179: 27-35. (Pubitemid 32125829)
39. 2+ responses. Science 1998; 280: 1763-1766. (Pubitemid 28283502)
40. Csordás G, Thomas AP, Hajnóczky G,. Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO J 1999; 18: 96-108. (Pubitemid 29005027)
41. 2+ signalling between sarco-endoplasmic reticulum and mitochondria. J Physiol 2000; 529: 69-81.
42. 2+ signals in pancreatic acinar cells. Biochem Pharmacol 2002; 63: 283-292. (Pubitemid 34158830)
43. Filippin L, Magalhães PJ, Di Benedetto G, et al., Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J Biol Chem 2003; 278: 39224-39234. (Pubitemid 37221826)
44. 2+ uniporter stimulation. J Physiol 2007; 580: 39-49. (Pubitemid 46470643)
45. Paredes SD, Marchena AM, Bejarano I, et al., Melatonin and tryptophan affect the activity-rest rhythm, core and peripheral temperatures, and interleukin levels in the ringdove: changes with age. J Gerontol A Biol Sci Med Sci 2009; 64: 340-350.
46. Paredes SD, Bejarano I, Terrón MP, et al., Melatonin and tryptophan counteract lipid peroxidation and modulate superoide dismutase activity in ringdove heterophils in vivo. Effect of antigen-induced activation and age. Age (Dordr) 2009; 31: 179-188.
47. Terrón MP, Delgado J, Paredes SD, et al., Effect of melatonin and tryptophan on humoral immunity in young and old ringdoves (Streptopelia risoria). Exp Gerontol 2009; 44: 653-658.
48. 2+ entry resulting in apoptosis. J Neurochem 2008; 104: 1177-1189.
49. Lin H, Sue YM, Chou Y, et al., Activation of a nuclear factor of activated T-lymphocyte-3 (NFAT3) by oxidative stress in carboplatin-induced apoptosis. Br J Pharmacol 2010 (in press). doi:.
50. Tan DX, Reiter RJ, Manchester LC, et al., Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger. Curr Top Med Chem 2002; 2: 181-197.
51. Rodríguez AB, Terrón MP, Durán J, et al., Physiological concentrations of melatonin and corticosterone affect phagocytosis and oxidative metabolism of ring dove heterophils. J Pineal Res 2001; 31: 31-38. (Pubitemid 32626043)
52. López A, García JA, Escames G, et al., Melatonin protects the mitochondria from oxidative damage reducing oxygen consumption, membrane potential, and superoxide anion production. J Pineal Res 2009; 46: 188-198.
53. Rodríguez C, Mayo JC, Sainz RM, et al., Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36: 1-9. (Pubitemid 38130283)
54. Radogna F, Paternoster L, De Nicola M, et al., Rapid and transient stimulation of intracellular reactive oxygen species by melatonin in normal and tumor leukocytes. Toxicol Appl Pharmacol 2009; 239: 37-45.
55. Petrosillo G, Moro N, Ruggiero FM, et al., Melatonin inhibits cardiolipin peroxidation in mitochondria and prevents the mitochondrial permeability transition and cytochrome c release. Free Radic Biol Med 2009; 47: 969-974.
56. Bejarano I, Espino J, Barriga C, et al., Pro-oxidant effect of melatonin in tumour leucocytes: relation with its cytotoxic and pro-apoptotic effects. Basic Clin Pharmacol Toxicol 2011; 108: 14-20.