J Appl Biomed 9:197-207, 2011 | DOI: 10.2478/v10136-011-0006-3

Oral melatonin administration and programmed cell death of neutrophils, lymphocytes, and other cell types from rats injected with HL-60 cells

Jonathan Delgado1, María del Pilar Terrón2,*, Virginio García-Martinez3, Carmen López-Sanchez3, Carmen Barriga2, José Antonio Pariente2, Ana Beatriz Rodríguez2
1 Technological Agri-food Institute (INTAEX), 06071 Badajoz, Spain
2 Department of Physiology, Faculty of Science, University of Extremadura, 06006 Badajoz, Spain
3 Department of Anatomy, Faculty of Medicine, University of Extremadura, 06006 Badajoz, Spain

Recent years have seen mounting evidence for the role of melatonin in mediating programmed cell death, with a protective, anti-apoptotic effect in healthy cells, but an anti-tumoural, pro-apoptotic action in many tumour cells. In this study, we evaluated the effect of melatonin on the programmed cell death induced by thapsigargin (TG), on lymphocytes and neutrophils, and on various tissues obtained from rats injected with human promyelocytic leukæmia cells (HL-60), treated with melatonin in their drinking water (20 μm), and fed ad libitum. Melatonin treatment significantly reduced caspase-3 and -9 activity, and caused the proportions of lymphocytes, neutrophils, and eosinophils to revert to their basal values. No histological differences were observed. In conclusion, melatonin has anti-apoptotic effects on lymphocytes and neutrophils obtained from rats injected with HL-60 leukæmia cells.

Keywords: melatonin; neutrophils; lymphocytes; apoptosis; HL-60 cells

Received: February 23, 2011; Revised: April 15, 2011; Published: July 31, 2011  Show citation

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Delgado J, del Pilar Terrón M, García-Martinez V, López-Sanchez C, Barriga C, Pariente JA, Rodríguez AB. Oral melatonin administration and programmed cell death of neutrophils, lymphocytes, and other cell types from rats injected with HL-60 cells. J Appl Biomed. 2011;9(4):197-207. doi: 10.2478/v10136-011-0006-3.
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    References

    1. Andrabi SA, Sayeed I, Siemen D, Wolf G, Horn TF. Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for anti-apoptotic effects of melatonin. FASEB J. 18: 869-871, 2004. Go to original source... Go to PubMed...
    2. Anisimov VN, Popovich IG, Shtylik AV, Zabezhinski MA, Ben-Huh H, Gurevich P, Berman V, Tendler Y, Zusman I. Melatonin and colon carcinogenesis III. Effect of melatonin on proliferative activity and apoptosis in colon mucosa and tumours induced by 1,2-dimethylhydrazine in rats. Exp Toxicol Pathol. 52: 71-76, 2000. Go to original source... Go to PubMed...
    3. Bejarano I, Redondo PC, Espino J, Rosado JA, Paredes SD, Barriga C, Reiter RJ, Pariente JA, Rodríguez AB. Melatonin induces mitochondrial-mediated apoptosis in human myeloid HL-60 cells. J Pineal Res. 46: 392-400, 2009. Go to original source... Go to PubMed...
    4. Berger J. A two-clock model of circadian timing in the immune system of mammals. Pathol Biol. 56: 286-291, 2008. Go to original source... Go to PubMed...
    5. Büyükavci M, Özdemir O, Buck S, Stout M, Ravindranth Y, Savaºan S. Melatonin cytotoxicity in human leukemia cell: relation with its pro-oxidant effect. Fundam Clin Pharmacol. 20: 73-79, 2006. Go to original source... Go to PubMed...
    6. Carrillo-Vico A, Lardone PJ, Fernández-Santos JM, Martín-Lacave I, Calvo JR, Karasek M, Guerrero JM. Human lymphocyte-synthesized melatonin is involved in the regulation of the interleukin-2/interleukin-2 receptor system. J Clin Endocrinol Metab. 9: 992-1000, 2005. Go to original source... Go to PubMed...
    7. Chahbouni M, Escames G, Venegas C, Sevilla B, García JA, López LC, Muñoz-Hoyos A, Molina-Carballo A, Acuña-Castroviejo D. Melatonin treatment normalizes plasma pro-inflammatory cytokines and nitrosative/oxidative stress in patients suffering from duchenne muscular dystrophy. J Pineal Res. 48: 282-289, 2010. Go to original source... Go to PubMed...
    8. Cos S, García-Bolado A, Sanchez-Barcelo EJ. Direct antiproliferative effects of melatonin on two metastatic cell sublines of mouse melanoma (B16BL6 and PG19). Melanoma Res. 11: 197-201, 2001. Go to original source... Go to PubMed...
    9. Cos S, González A, Güezmes A, Mediavilla MD, Martínez-Campa C, Alonso-González C, Sánchez-Barceló EJ. Melatonin inhibits the growth of DMBA-induced mammary tumours by decreasing the local biosynthesis of estrogens through the modulation of aromatase activity. Int J Cancer. 118: 274-278, 2006. Go to original source... Go to PubMed...
    10. Cucina A, Proietti S, D'Anselmi F, Coluccia P, Dinicola S, Frati L, Bizzarri M. Evidence for a biphasic apoptotic pathway induced by melatonin in MCF-7 breast cancer cells. J Pineal Res. 46: 172-180, 2009. Go to original source... Go to PubMed...
    11. Dauchy RT, Blask DE, Dauchy EM, Davidson LK, Tirrell PC, Greene MW, Tirrell RP, Hill CR, Sauer LA. Antineoplastic effects of melatonin on a rare malignancy of mesenchymal origin: melatonin receptor-mediated inhibition of signal transduction, linoleic acid metabolism and growth in tissue-isolated human leiomyosarcoma xenografts. J Pineal Res. 47: 32-42, 2009. Go to original source... Go to PubMed...
    12. El-Missiry MA, Abd El-Aziz AF. Influence of melatonin on proliferation and antioxidant system in Ehrlich ascites carcinoma cells. Cancer Lett. 151: 119-125, 2000. Go to original source... Go to PubMed...
    13. Espino J, Bejarano I, Redondo PC, Rosado JA, Barriga C, Reiter JR, Pariente JA, Rodríguez AB. Melatonin reduces apoptosis induced by calcium signaling in human leukocytes: Evidence for the involvement of mitochondria and Bax activation. J Membr Biol. 233: 105-118, 2010. Go to original source... Go to PubMed...
    14. Fang M, Zhang H, Xue S. Role of calcium in apoptosis of HL-60 cells induced by harringtonine. Sci China C Life Sci. 41: 600-607, 1998. Go to original source... Go to PubMed...
    15. García-Navarro A, González-Puga C, Escames G, López LC, López A, López-Cantarero M, Camacho E, Espinosa A, Gallo MA, Acuña-Castroviejo D. Cellular mechanisms involved in the melatonin inhibition of HT-29 human colon cancer cell proliferation in culture. J Pineal Res. 43: 195-205, 2007. Go to original source... Go to PubMed...
    16. Hajnóczyk G, Davies E, Madesh M. Calcium signaling and apoptosis. Biochem Biophys Res Commun. 304: 445-454, 2003. Go to original source... Go to PubMed...
    17. Hardeland R, Fuhrberg B. Ubiquitous melatonin-presence and effects in unicells, plants and animals. Trends Comp Biochem Physiol. 2: 25-45, 1996.
    18. Hibaoui Y, Roulet E, Ruegg UT. Melatonin prevents oxidative stress-mediated mitochondrial permeability transition and death in skeletal muscle cells. J Pineal Res. 47: 238-252, 2009. Go to original source... Go to PubMed...
    19. Jou MJ, Peng TI, Hsu LF, Jou SB, Reiter RJ, Yang CM, Chiao CC, Lin YF, Chen CC. 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. 48: 20-38, 2010. Go to original source... Go to PubMed...
    20. Kobayashi H, Kromminga A, Dunlop TW, Tychsen B, Conrad F, Suzuki N, Memezawa A, Bettermann A, Aiba S, Carlberg C, Paus R. A role of melatonin in neuroectodermal-mesodermal interactions: the hair follicle synthesizes melatonin and expresses functional melatonin receptors. FASEB J. 19: 1710-1712, 2005. Go to original source... Go to PubMed...
    21. Korsmeyer SJ, Wei MC, Saito M, Weiler S, Oh KJ, Schlesinger PH. Pro-apoptotic cascade activates BiD, which oligomerizes Bak or Bax into pores that result in the release of cytochrome c. Cell Death Differ. 7: 1166-1173, 2000. Go to original source... Go to PubMed...
    22. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev. 87: 99-163, 2007. Go to original source... Go to PubMed...
    23. Kunduzova OR, Escourrou G, Seguelas MH, Delagrange P, De La Farge F, Cambon C, Parini A. Prevention of apoptotic and necrotic cell death, caspase-3 activation, and renal dysfunction by melatonin after ischemia/reperfusion. FASEB J. 17: 872-874, 2003. Go to original source... Go to PubMed...
    24. Luchetti F, Canonico B, Curci R, Battistelli M, Mannello F, Papa S, Tarzia G, Falcieri E. Melatonin prevents apoptosis induced by UV-B treatment in U937 cell line. J Pineal Res. 40: 158-167, 2006. Go to original source... Go to PubMed...
    25. Martín-Renedo J, Mauriz JL, Jorquera F, Ruiz-Andrés O, González P, González-Gallego J. Melatonin induces cell cycle arrest and apoptosis in hepatocarcinoma HepG2 cell line. J Pineal Res. 45: 532-540, 2008. Go to original source... Go to PubMed...
    26. Melen-Mucha G, Winczyk K, Pawlikowski M. Somatostatin analogue oxtreotide and melatonin inhibit bromodeoxyuridine incorporation into cell nuclei and enhance apoptosis in the transplantable murine colon 38 cancer. Anticancer Res. 18: 3615-3620, 1998.
    27. Panke ES, Rollag MD, Reiter RJ. Pineal melatonin concentrations in the Syrian hamster. Endocrinology. 104: 194-197, 1979. Go to original source... Go to PubMed...
    28. Paradies G, Petrosillo G, Paradies V, Reiter RJ, Ruggiero FM. Melatonin, cardiolipin and mitochondrial bioenergetics in health and disease. J Pineal Res. 48: 297-310, 2010. Go to original source... Go to PubMed...
    29. Park SY, Jang WJ, Yi EY, Jang JY, Jung Y, Jeong JW, Kim YJ. Melatonin suppresses tumour angiogenesis by inhibiting HIF-1alpha stabilization under hypoxia. J Pineal Res. 48: 178-184, 2010. Go to original source... Go to PubMed...
    30. Petrosillo G, Moro N, Ruggiero FM, Paradies G. Melatonin inhibits cardiolipin peroxidation in mitochondria and prevents the mitochondrial permeability transition and cytochrome c release. Free Radic Biol Med. 47: 969-974, 2009. Go to original source... Go to PubMed...
    31. Radogna F, Cristofanon S, Paternoster L, D'Alessio M, De Nicola M, Cerella C, Dicato M, Diederich M, Ghibelli L. Melatonin antagonizes the intrinsic pathway of apoptosis via mitochondrial targeting of Bcl-2. J Pineal Res. 44: 316-325, 2008. Go to original source... Go to PubMed...
    32. Rasola A, Bernardi P. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis.12: 815-833, 2007. Go to original source... Go to PubMed...
    33. Ratanachoo K, Gascoyne PRC, Ruchirawat M. Detection of cellular responses to toxicants by dielectrophoresis. BBA. 1564: 449-458, 2002. Go to original source... Go to PubMed...
    34. Reiter RJ. Pineal control of a seasonal reproductive rhythm in male golden hamsters exposed to natural daylight and temperature. Endocrinology. 92: 423-430, 1973. Go to original source... Go to PubMed...
    35. Reiter RJ. Pineal melatonin: cell biology of its synthesis and of its physiological interaction. Endocr Rev. 12: 151-180, 1991. Go to original source... Go to PubMed...
    36. Reiter RJ, Fraschini F. Endocrine aspects of the mammalian pineal gland: a review. Neuroendocrinology. 5: 219-255, 1969. Go to original source... Go to PubMed...
    37. Rodríguez AB, Barriga C, Paredes SD, Terrón MP. Age, melatonin and the immune system. In Pandalai SG (ed.): Recent Research Developments in Molecular and Cellular Biochemistry, Vol. 2, Part II., Research SignPost, 2005, pp. 255-287.
    38. Rubio S, Estevez F, Cabrera J, Reiter RJ, Loro J, Quintana J. Inhibition of proliferation and induction of apoptosis by melatonin in human myeloid HL-60 cells. J Pineal Res. 42: 131-138, 2007. Go to original source... Go to PubMed...
    39. Sainz RM, Mayo JC, Rodriguez C, Tan DX, Lopez-Burillo S, Reiter RJ. Melatonin and cell death: differential actions on apoptosis in normal and cancer cells. Cell Mol Life Sci. 60: 1407-1426, 2003. Go to original source... Go to PubMed...
    40. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ, Debatin KM, Krammer PH, Peter ME. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17: 1675-1687, 1998. Go to original source... Go to PubMed...
    41. Shen YX, Xu SY, Wei W, Wang XL, Wang H, Sun X. Melatonin blocks rat hippocampal neuronal apoptosis induced by amyloid beta-peptide 25-35. J Pineal Res. 32: 163-167, 2002. Go to original source... Go to PubMed...
    42. Sugimoto K, Yamada K, Egashira M, Yazaki Y, Hirai H, Kikuchi A, Oshimi K. Temporal and spatial distribution of DNA topoisomerase II alters during proliferation, differentiation, and apoptosis in HL-60 cells. Blood. 91: 1407-1417, 1998. Go to original source...
    43. Tan DX, Hardeland R, Manchester LC, Paredes SD, Korkmaz A, Sainz RM, Mayo JC, Fuentes-Broto L, Reiter RJ. The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness. Biol Rev Camb Philos Soc. 85: 607-623, 2010. Go to original source... Go to PubMed...
    44. Trubiani O, Recchioni R, Moroni F, Pizzicannella J, Caputi S, Di Primio R. Melatonin provokes cell death in human B-lymphoma cells by mitochondrial-dependent apoptotic pathways activation. J Pineal Res. 39: 425-431, 2005. Go to original source... Go to PubMed...
    45. Wenzel U, Nickel A, Daniel H. Melatonin potentiates flavone-induced apoptosis in human colon cancer cells by increasing the level of glycolytic end products. Int J Cancer. 116: 236-242, 2005. Go to original source... Go to PubMed...
    46. Yang QH, Xu JN, Xu RK, Pang SF. Antiproliferative effects of melatonin on the growth of rat pituitary prolactin-secreting tumour cells in vitro. J Pineal Res. 42: 172-179, 2007. Go to original source... Go to PubMed...
    47. Yoo YM, Yim SV, Kim SS, Jang HY, Lea HZ, Hwang GC, Kim JW, Kim SA, Lee HJ, Kim CJ, Chung JH, Leem KH. Melatonin suppresses NO-induced apoptosis via induction of Bcl-2 expression in PGT-beta immortalized pineal cells. J Pineal Res. 33: 146-150, 2002. Go to original source... Go to PubMed...

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