Melatonin induces the expression of Nrf2-regulated antioxidant enzymes via PKC and Ca2+ influx activation in mouse pancreatic acinar cells

Free Radical Biology and Medicine

Volumn 87, Issue , 2015, Pages 226-236

  Santofimia Castaño, Patricia ^a   Clea Ruy, Deborah ^b   Garcia Sanchez, Lourdes ^a   Jimenez Blasco, Daniel ^c   Fernandez Bermejo, Miguel ^a,d   Bolaños, Juan P ^c   Salido, Gines M ^a   Gonzalez, Antonio ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b UNIVERSITY OF BRASILIA   (Brazil)

^c UNIVERSITY OF SALAMANCA   (Spain)

^d San Pedro de Alcantara Hospital   (Spain)

Author keywords

Antioxidantresponse; Calcium; Melatonin; Nrf2; Pancreas; ProteinkinaseC

Indexed keywords

2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; CALCIUM ION; CHOLECYSTOKININ OCTAPEPTIDE; FURA 2; GLUTAMATE CYSTEINE LIGASE; HEME OXYGENASE 1; INDOLEAMINE; MELATONIN; PROTEIN KINASE C; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; CALCIUM; GCLM PROTEIN, MOUSE; NFE2L2 PROTEIN, MOUSE; NOQ1 PROTEIN, MOUSE;

ACINAR CELL; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; FLUOROMETRY; IMMUNOCYTOCHEMISTRY; MALE; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CALCIUM SIGNALING; CYTOLOGY; GENETICS; METABOLISM; PANCREAS; PHOSPHORYLATION;

ACINAR CELLS; ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; ANTIOXIDANTS; CALCIUM; CALCIUM SIGNALING; GLUTAMATE-CYSTEINE LIGASE; HEME OXYGENASE-1; MALE; MELATONIN; MICE; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; PANCREAS; PHOSPHORYLATION; PROTEIN KINASE C;

EID: 84940039877     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.06.033     Document Type: Article

References (70)

1. J.A. Armstrong, N. Cash, P.M. Soares, M.H. Souza, R. Sutton, D.N. Criddle Oxidative stress in acute pancreatitis: lost in translation? Free Radic. Res. 47 2013 917 933
2. J.R. Peinado, A. Diaz-Ruiz, G. Frühbeck, M.M. Malagon Mitochondria in metabolic disease: getting clues from proteomic studies Proteomics 14 2014 452 466
3. C.R. Reczek, N.S. Chandel ROS-dependent signal transduction Curr. Opin. Cell Biol. 33C 2014 8 13
4. J.H. Yu, H. Kim Oxidative stress and inflammatory signaling in cerulein pancreatitis World J. Gastroenterol 20 2014 17324 17329
5. 2+ signals: physiology and pathophysiology Biol. Res. 37 2004 661 664
6. O.V. Gerasimenko, J.V. Gerasimenko Mitochondrial function and malfunction in the pathophysiology of pancreatitis Pflugers Arch. 464 2012 89 99
7. H. Streb, R.F. Irvine, M.J. Berridge, I. Schulz Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate Nature 306 1983 67 69
8. J.W. Putney A model for receptor-regulated calcium entry Cell Calcium 7 1988 1 12
9. E. Carafoli Calcium pump of the plasma membrane Physiol. Rev. 71 1991 129 153
10. A. González, P.J. Camello, J.A. Pariente, G.M. Salido Free cytosolic calcium levels modify intracellular pH in rat pancreatic acini Biochem. Biophys. Res. Commun. 230 1997 652 656
11. A. González, G.M. Salido Participation of mitochondria in calcium signalling in the exocrine pancreas J. Physiol. Biochem. 57 2010 331 339
12. A. Dabrowski Exocrine pancreas; molecular basis for intracellular signaling, damage and protection - Polish experience J. Physiol. Pharmacol. 54 2003 167 181
13. M. Buelna-Chontal, J.G. Guevara-Chávez, A. Silva-Palacios, O.N. Medina-Campos, J. Pedraza-Chaverri, C. Zazueta Nrf2-regulated antioxidant response is activated by protein kinase C in postconditioned rat hearts Free Radic. Biol. Med. 74 2014 145 156
14. M. Zhang, C. An, Y. Gao, R.K. Leak, J. Chen, F. Zhang Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection Prog. Neurobiol. 100 2013 30 47
15. T.A. Beyer, U. Auf dem Keller, S. Braun, M. Schäfer, S. Werner Roles and mechanisms of action of the Nrf2 transcription factor in skin morphogenesis, wound repair and skin cancer Cell Death Differ. 14 2007 1250 1254
16. R.M. Slominski, R.J. Reiter, N. Schlabritz-Loutsevitch, R.S. Ostrom, A.T. Slominski Melatonin membrane receptors in peripheral tissues: distribution and functions Mol. Cell. Endocrinol. 351 2012 152 166
17. F. Luchetti, B. Canonico, M. Betti, M. Arcangeletti, F. Pilolli, M. Piroddi, L. Canesi, S. Papa, F. Galli Melatonin signaling and cell protection function FASEB J. 24 2010 3603 3624
18. A. González, A. del Castillo-Vaquero, A. Miró-Morán, J.A. Tapia, G.M. Salido Melatonin reduces pancreatic tumor cell viability by altering mitochondrial physiology. J. Pineal Res 50 2011 250 260
19. E. Mühlbauer, E. Gross, K. Labucay, S. Wolgast, E. Peschke Loss of melatonin signalling and its impact on circadian rhythms in mouse organs regulating blood glucose Eur. J. Pharmacol. 606 2009 61 71
20. J. Jaworek, K. Nawrot, S.J. Konturek, A. Leja-Szpak, P. Thor, W.W. Pawlik Melatonin and its precursor, L-tryptophan: influence on pancreatic amylase secretion in vivo and in vitro J. Pineal Res. 36 2004 155 164
21. 2+ mobilization and amylase release in response to cholecystokinin octapeptide in mouse pancreatic acinar cells J. Physiol. Biochem 69 2013 897 908
22. S. Aust, B. Brucker, J. Graf, M. Klimpfinger, T. Thalhammer Melatonin modulates acid/base transport in human pancreatic carcinoma cells Cell Physiol. Biochem. 18 2006 91 102
23. W. Tan, W. Zhou, H.S. Luo, C.B. Liang, H. Xia The inhibitory effect of melatonin on colonic motility disorders induced by water avoidance stress in rats Eur. Rev. Med. Pharmacol. Sci. 17 2013 3060 3067
24. O. Celik, M. Naziroʇlu Melatonin modulates apoptosis and TRPM2 channels in transfected cells activated by oxidative stress Physiol. Behav. 107 2012 458 465
25. P. Santofimia-Castaño, D.C. Ruy, M. Fernandez-Bermejo, G.M. Salido, A. Gonzalez Pharmacological dose of melatonin reduces cytosolic calcium load in response to cholecystokinin in mouse pancreatic acinar cells Mol. Cell Biochem. 397 2014 75 86
26. J. Jaworek, A. Leja-Szpak, J. Bonior, K. Nawrot, R. Tomaszewska, J. Stachura, R. Sendur, W. Pawlik, T. Brzozowski, S.J. Konturek Protective effect of melatonin and its precursor L-tryptophan on acute pancreatitis induced by caerulein overstimulation or ischemia/reperfusion J. Pineal Res 34 2003 40 52
27. F.C. Muñoz-Casares, F.J. Padillo, J. Briceño, J.A. Collado, J.R. Muñoz-Castañeda, R. Ortega, A. Cruz, I. Túnez, P. Montilla, C. Pera, J. Muntané Melatonin reduces apoptosis and necrosis induced by ischemia/reperfusion injury of the pancreas J. Pineal Res 40 2006 195 203
28. K. Gülben, H. Ozdemir, U. Berberoʇlu, H. Mersin, F. Yrkin, E. Cakýr, S. Aksaray Melatonin modulates the severity of taurocholate-induced acute pancreatitis in the rat Dig. Dis. Sci. 55 2010 941 946
29. J. Jaworek, K. Zwirska-Korczala, J. Szklarczyk, K. Nawrot-Porąbka, A. Leja-Szpak, A.K. Jaworek, R. Tomaszewska Pinealectomy aggravates acute pancreatitis in the rat Pharmacol. Rep. 62 2010 864 873
30. W. Qi, D.X. Tan, R.J. Reiter, S.J. Kim, L.C. Manchester, J. Cabrera, R.M. Sainz, J.C. Mayo Melatonin reduces lipid peroxidation and tissue edema in cerulein-induced acute pancreatitis in rats Dig. Dis. Sci. 44 1999 2257 2262
31. Y. Deng, J. Zhu, C. Mi, B. Xu, C. Jiao, Y. Li, D. Xu, W. Liu, Z. Xu Melatonin antagonizes Mn-induced oxidative injury through the activation of keap1-Nrf2-ARE signaling pathway in the striatum of mice Neurotox. Res. 27 2015 156 171
32. K.H. Jung, S.W. Hong, H.M. Zheng, H.S. Lee, H. Lee, D.H. Lee, S.Y. Lee, S.S. Hong Melatonin ameliorates cerulein-induced pancreatitis by the modulation of nuclear erythroid 2-related factor 2 and nuclear factor-kappaB in rats J. Pineal Res 48 2010 239 250
33. J. Vriend, R.J. Reiter The Keap1-Nrf2-antioxidant response element pathway: a review of its regulation by melatonin and the proteasome Mol. Cell. Endocrinol. 401 2015 213 220
34. Jimenez-Blasco, D.; Santofimia-Castaño, P.; Gonzalez, A.; Almeida, A.; Bolaños, J.P. Astrocyte NMDA receptors' activity sustains neuronal survival through a Cdk5-Nrf2 pathway. Cell Death Differ. 2015 Apr 24. 10.1038/cdd.2015.49. [Epub ahead of print]. PMID: 25909891
35. 2+ channels in vitro induces neuronal hyperexcitability through the phosphatidylinositol 3-kinase-dependent protein kinase C delta pathway J. Pineal Res 58 2015 321 334
36. Baba, K.; Benleulmi-Chaachoua, A.; Journé, A.S.; Kamal, M.; Guillaume, J.L.; Dussaud, S.; Gbahou, F.; Yettou, K.; Liu, C.; Contreras-Alcantara, S.; Jockers, R.; Tosini, G. Heteromeric MT1/MT2 melatonin receptors modulate photoreceptor function. Sci. Signal. 6:ra89; 2013.
37. I. Ben Soussia, F. Mies, R. Naeije, V. Shlyonsky Melatonin down-regulates volume-sensitive chloride channels in fibroblasts Pflugers Arch. 464 2012 273 285
38. J.T. Sharkey, C. Cable, J. Olcese Melatonin sensitizes human myometrial cells to oxytocin in a protein kinase C alpha/extracellular-signal regulated kinase-dependent manner J. Clin. Endocrinol. Metab. 95 2010 2902 2908
39. A. González, A. Schmid, L. Sternfeld, E. Krause, G.M. Salido, I. Schulz Cholecystokinin-evoked Ca2+ waves in isolated mouse pancreatic acinar cells are modulated by activation of cytosolic phospholipase A2, phospholipase D, and protein kinase C Biochem. Biophys. Res. Commun 261 1999 726 733
40. 2+ indicators with greatly improved fluorescence properties J. Biol. Chem. 260 1985 3440 3450
41. P. Santofimia-Castaño, D.C. Ruy, M. Fernandez-Bermejo, G.M. Salido, A. Gonzalez Pharmacological dose of melatonin reduces cytosolic calcium load in response to cholecystokinin in mouse pancreatic acinar cells Mol. Cell. Biochem. 397 2014 75 86
42. 2+-independent phospholipase A2 and cytochrome P-450 in store-operated calcium entry in 3T6 fibroblasts Biochem. Pharmacol 70 2005 733 739
43. 2+ release from RyR1 in skeletal muscle Am. J. Physiol. Cell Physiol 286 2004 C73 C78
44. 2+]i rise and apoptosis in human glioblastoma cells Life Sci. 90 2012 703 771
45. L. Wagner-Britz, J. Wang, L. Kaestner, I. Bernhardt Protein kinase Cα and P-type Ca channel CaV2.1 in red blood cell calcium signalling Cell Physiol. Biochem. 31 2013 883 891
46. M.P. Granados, G.M. Salido, J.A. Pariente, A. González Modulation of CCK-8-evoked intracellular Ca2+ waves by hydrogen peroxide in mouse pancreatic acinar cells J. Physiol. Pharmacol. 58 2007 423 440
47. H.S. Marinho, C. Real, L. Cyrne, H. Soares, F. Antunes Hydrogen peroxide sensing, signaling and regulation of transcription factors Redox Biol. 2 2014 535 562
48. M.P. Granados, G.M. Salido, J.A. Pariente, A. González Generation of ROS in response to CCK-8 stimulation in mouse pancreatic acinar cells Mitochondrion 3 2004 285 296
49. M. Sledzinski, A. Borkowska, A. Sielicka-Dudzin, M. Halon, M. Wozniak, J.H. Spodnik, A.H. Antosiewicz, J. Antosiewicz Cerulein-induced acute pancreatitis is associated with c-Jun NH(2)-terminal kinase 1-dependent ferritin degradation and iron-dependent free radicals formation Pancreas 42 2013 1070 1077
50. A.E. Hunt, W.M. Al-Ghoul, M.U. Gillette, M.L. Dubocovich Activation of MT(2) melatonin receptors in rat suprachiasmatic nucleus phase advances the circadian clock Am. J. Physiol. Cell. Physiol. 280 2001 C110 C118
51. A.J. McArthur, A.E. Hunt, M.U. Gillette Melatonin action and signal transduction in the rat suprachiasmatic circadian clock: activation of protein kinase C at dusk and dawn Endocrinology 138 1997 627 634
52. J. Jaworek Ghrelin and melatonin in the regulation of pancreatic exocrine secretion and maintaining of integrity J. Physiol. Pharmacol. 57 2006 83 96
53. S.D. Paredes, A. Korkmaz, L.C. Manchester, D.X. Tan, R.J. Reiter Phytomelatonin: a review J. Exp. Bot. 60 2009 57 69
54. S.R. Pandi-Perumal, I. Trakht, V. Srinivasan, D.W. Spence, G.J. Maestroni, N. Zisapel, D.P. Cardinali Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways Prog. Neurobiol. 85 2008 335 353
55. C. Martínez-Campa, A. González, M.D. Mediavilla, C. Alonso-González, V. Alvarez-García, E.J. Sánchez-Barceló, S. Cos Melatonin inhibits aromatase promoter expression by regulating cyclooxygenases expression and activity in breast cancer cells Br. J. Cancer 101 2009 1613 1619
56. J. Messner, J. Graf Reactive oxygen species facilitate the insulin-dependent inhibition of glucagon-induced glucose production in the isolated perfused rat liver Wien Med. Wochenschr. 158 2008 570 574
57. I. Stumpf, I. Bazwinsky, E. Peschke Modulation of the cGMP signaling pathway by melatonin in pancreatic beta-cells J. Pineal Res 46 2009 140 147
58. A. Del Castillo-Vaquero, G.M. Salido, A. González Melatonin induces calcium release from CCK-8- and thapsigargin-sensitive cytosolic stores in pancreatic AR42J cells J. Pineal. Res. 49 2010 256 263
59. R.D. Ramracheya, D.S. Muller, P.E. Squires, H. Brereton, D. Sugden, G.C. Huang, S.A. Amiel, P.M. Jones, S.J. Persaud Function and expression of melatonin receptors on human pancreatic islets J. Pineal Res 44 2008 273 279
60. C. Carrasco, A.B. Rodriguez, J.A. Pariente Effects of melatonin on the oxidative damage and pancreatic antioxidant defenses in cerulein-induced acute pancreatitis in rats Hepatobiliary Pancreat. Dis. Int. 13 2014 442 446
61. 2+-selective (ARC) channels in murine parotid and pancreatic acinar cells J. Physiol 564 2005 791 801
62. 2+ entry in cultured astrocytes Biochem. Biophys. Res. Commun 331 2005 603 613
63. H. Kelestimur, M. Ozcan, E. Kacar, E. Alcin, B. YIlmaz, A. Ayar Melatonin elicits protein kinase C-mediated calcium response in immortalized GT1-7 GnRH neurons Brain Res. 1435 2012 24 28
64. 2+ entry J. Thromb. Haemost 8 2010 1604 1613
65. Vriend, J.; Reiter, R.J. The Keap1-Nrf2-antioxidant response element pathway: A review of its regulation by melatonin and the proteasome. Mol. Cell. Endocrinol. 2014; 401C:213-20. 10.1016/j.mce.2014.12.013.
66. K. Ding, H. Wang, J. Xu, T. Li, L. Zhang, Y. Ding, L. Zhu, J. He, M. Zhou Melatonin stimulates antioxidant enzymes and reduces oxidative stress in experimental traumatic brain injury: the Nrf2-ARE signaling pathway as a potential mechanism Free Radic. Biol. Med 73 2014 1 11
67. M. Aparicio-Soto, C. Alarcón-de-la-Lastra, A. Cárdeno, S. Sánchez-Fidalgo, M. Sanchez-Hidalgo Melatonin modulates microsomal PGE synthase 1 and NF-E2-related factor-2-regulated antioxidant enzyme expression in LPS-induced murine peritoneal macrophages Br. J. Pharmacol 171 2014 134 144
68. U. Kilic, E. Kilic, Z. Tuzcu, M. Tuzcu, I.H. Ozercan, O. Yilmaz, F. Sahin, K. Sahin Melatonin suppresses cisplatin-induced nephrotoxicity via activation of Nrf-2/HO-1 pathway Nutr. Metab. (Lond.) 10 2013 7
69. R.R. Tao, J.Y. Huang, X.J. Shao, W.F. Ye, Y. Tian, M.H. Liao, K. Fukunaga, Y.J. Lou, F. Han, Y.M. Lu Ischemic injury promotes Keap1 nitration and disturbance of antioxidative responses in endothelial cells: a potential vasoprotective effect of melatonin J. Pineal Res 54 2013 271 281
70. J.W. Kang, S.M. Lee Melatonin inhibits type 1 interferon signaling of toll-like receptor 4 via heme oxygenase-1 induction in hepatic ischemia/reperfusion J. Pineal Res 53 2012 67 76