Melatonin blunts the mitochondrial/NLRP3 connection and protects against radiation-induced oral mucositis

Journal of Pineal Research

Volumn 58, Issue 1, 2015, Pages 34-49

  Ortiz, Francisco ^a   Acuña Castroviejo, Darío ^a,b   Doerrier, Carolina ^a   Dayoub, José C ^a   Lõpez, Luis C ^a,b   Venegas, Carmen ^a   García, José A ^a   Lõpez, Ana ^a   Volt, Huayqui ^a,b   Luna Sánchez, Marta ^a,b   Escames, Germaine ^a,b  

^a Centro de Investigaciõn Biomédica Parque Tecnolõgico de Ciencias de la Salud ^*  (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

inflammasome; melatonin; mitochondria; mucositis; NF B; NLRP3; radiotherapy; tongue

Indexed keywords

CASPASE 3; CITRATE SYNTHASE; I KAPPA B; INFLAMMASOME; INTERLEUKIN 1BETA; MELATONIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NLRP 3 PROTEIN; PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ANTIOXIDANTS; INFLAMMASOMES; NOD-LIKE RECEPTOR 3, RAT; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOENERGY; CONTROLLED STUDY; DNA DEGRADATION; GAMMA BLOOD IRRADIATOR; HISTOPATHOLOGY; INNATE IMMUNITY; IONIZING RADIATION; LIMIT OF QUANTITATION; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; ORAL MUCOSITIS; OXIDATIVE STRESS; RADIATION DOSE; RADIATION INDUCED ORAL MUCOSITIS; RADIATION INJURY; RANDOMIZED CONTROLLED TRIAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ULCEROGENESIS; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ADVERSE EFFECTS; ANIMALS; DRUG EFFECTS; METABOLISM; MITOCHONDRIA; PATHOLOGY; RADIATION EFFECTS; RADIATION INJURIES, EXPERIMENTAL; RATS; RATS, WISTAR; STOMATITIS; TONGUE; X-RAYS;

ANIMALS; ANTIOXIDANTS; INFLAMMASOMES; MALE; MELATONIN; MITOCHONDRIA; OXIDATIVE STRESS; RADIATION INJURIES, EXPERIMENTAL; RATS; RATS, WISTAR; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; STOMATITIS; TONGUE; X-RAYS;

EID: 84919599154     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12191     Document Type: Article

References (58)

1. Al-Dasooqi N, Sonis ST, Bowen JM, et al. Emerging evidence on the pathobiology of mucositis. Support Care Cancer 2013; 21: 3233-3241.
2. Campos MI, Campos CN, Aarestrup FM, et al. Oral mucositis in cancer treatment: natural history, prevention and treatment. Mol Clin Oncol 2014; 2: 337-340.
3. Vitale KM, Violago L, Cofnas P, et al. Impact of palifermin on incidence of oral mucositis and healthcare utilization in children undergoing autologous hematopoietic stem cell transplantation for malignant diseases. Pediatr Transplant 2014; 18: 211-216.
4. Henke M, Alfonsi M, Foa P, et al. Palifermin decreases severe oral mucositis of patients undergoing postoperative radiochemotherapy for head and neck cancer: a randomized, placebo-controlled trial. J Clin Oncol 2011; 29: 2815-2820.
5. Curra M, Martins MA, Lauxen IS, et al. Effect of topical chamomile on immunohistochemical levels of IL-1beta and TNF-alpha in 5-fluorouracil-induced oral mucositis in hamsters. Cancer Chemother Pharmacol 2013; 71: 293-299.
6. Li QH, Chen QM, Zeng X,. [Application of Cochrane systematic reviews in diagnosis and treatment for oral mucosal diseases]. Hua Xi Kou Qiang Yi Xue Za Zhi 2010; 28: 573-575.
7. Zhou R, Yazdi AS, Menu P, et al. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011; 469: 221-225.
8. Mariathasan S, Monack DM,. Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol 2007; 7: 31-40.
9. Escames G, Leon J, Macias M, et al. Melatonin counteracts lipopolysaccharide-induced expression and activity of mitochondrial nitric oxide synthase in rats. FASEB J 2003; 17: 932-934.
10. Tan DX, Manchester LC, Burkhardt S, et al. N1-acetyl-N2-formyl-5-methoxykynuramine, a biogenic amine and melatonin metabolite, functions as a potent antioxidant. FASEB J 2001; 15: 2294-2296.
11. Galano A, Tan DX, Reiter RJ,. On the free radical scavenging activities of melatonin's metabolites, AFMK and AMK. J Pineal Res 2013; 54: 245-257.
12. Zhang HM, Zhang Y,. Melatonin: a well-documented antioxidant with conditional pro-oxidant actions. J Pineal Res 2014; 57: 131-146.
13. Acuña-Castroviejo D, Lopez LC, Escames G, et al. Melatonin-mitochondria interplay in health and disease. Curr Top Med Chem 2011; 11: 221-240.
14. Escames G, Lopez LC, Garcia JA, et al. Mitochondrial DNA and inflammatory diseases. Hum Genet 2012; 131: 161-173.
15. Jimenez-Aranda A, Fernandez-Vazquez G, Mohammad A-S, et al. Melatonin improves mitochondrial function in inguinal white adipose tissue of Zucker diabetic fatty rats. J Pineal Res 2014; 57: 103-109.
16. Onal C, Kayaselcuk F, Topkan E, et al. Protective effects of melatonin and octreotide against radiation-induced intestinal injury. Dig Dis Sci 2011; 56: 359-367.
17. Kolli VK, Abraham P, Isaac B, et al. Preclinical efficacy of melatonin to reduce methotrexate-induced oxidative stress and small intestinal damage in rats. Dig Dis Sci 2013; 58: 959-969.
18. Cassatt DR, Fazenbaker CA, Bachy CM, et al. Amifostine (ETHYOL) protects rats from mucositis resulting from fractionated or hyperfractionated radiation exposure. Int J Radiat Oncol Biol Phys 2005; 61: 901-907.
19. Venegas C, Garcia JA, Escames G, et al. Extrapineal melatonin: analysis of its subcellular distribution and daily fluctuations. J Pineal Res 2011; 52: 217-227.
20. Esterbauer H, Cheeseman KH,. Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol 1990; 186: 407-421.
21. Jaskot RH, Charlet EG, Grose EC, et al. An automated analysis of glutathione peroxidase, S-transferase, and reductase activity in animal tissue. J Anal Toxicol 1983; 7: 86-88.
22. Hissin PJ, Hilf R,. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976; 74: 214-226.
23. Barrientos A,. In vivo and in organello assessment of OXPHOS activities. Methods 2002; 26: 307-316.
24. Brusque AM, Borba RR, Schuck PF, et al. Inhibition of the mitochondrial respiratory chain complex activities in rat cerebral cortex by methylmalonic acid. Neurochem Int 2002; 40: 593-601.
25. Srere P,. Citrate synthase. Methods Enzymol 1969; 13: 3-11.
26. Gnaiger E,. Polarographic oxygen sensors, the oxygraph and high-resolution respirometry to assess mitochondrial function. In: Mitochondrial Dysfunction in Drug-Induced Toxicity., Dykens JA, Will Y, eds. John Wiley, New Jersey, 2008; pp. 327-352.
27. Venegas C, Garcia JA, Doerrier C, et al. Analysis of the daily changes of melatonin receptors in the rat liver. J Pineal Res 2013; 54: 313-321.
28. Lopez LC, Quinzii CM, Area E, et al. Treatment of CoQ(10) deficient fibroblasts with ubiquinone, CoQ analogs, and vitamin C: time- and compound-dependent effects. PLoS ONE 2010; 5: e11897.
29. Chahbouni M, Escames G, Venegas C, et al. Melatonin treatment normalizes plasma pro-inflammatory cytokines and nitrosative/oxidative stress in patients suffering from Duchenne muscular dystrophy. J Pineal Res 2010; 48: 282-289.
30. Wang H, Walaszczyk EJ, Li K, et al. High-performance liquid chromatography with fluorescence detection and ultra-performance liquid chromatography with electrospray tandem mass spectrometry method for the determination of indoleamine neurotransmitters and their metabolites in sea lamprey plasma. Anal Chim Acta 2012; 721: 147-153.
31. Iglesias-Bartolome R, Patel V, Cotrim A, et al. mTOR inhibition prevents epithelial stem cell senescence and protects from radiation-induced mucositis. Cell Stem Cell 2012; 11: 401-414.
32. Yoshida T, Goto S, Kawakatsu M, et al. Mitochondrial dysfunction, a probable cause of persistent oxidative stress after exposure to ionizing radiation. Free Radic Res 2012; 46: 147-153.
33. Martin M, Macias M, Escames G, et al. Melatonin but not vitamins C and E maintains glutathione homeostasis in t-butyl hydroperoxide-induced mitochondrial oxidative stress. FASEB J 2000; 14: 1677-1679.
34. Sonis ST,. The pathobiology of mucositis. Nat Rev Cancer 2004; 4: 277-284.
35. Coto-Montes A, Boga JA, Rosales-Corral S, et al. Role of melatonin in the regulation of autophagy and mitophagy: a review. Mol Cell Endocrinol 2012; 361: 12-23.
36. Jain MV, Paczulla AM, Klonisch T, et al. Interconnections between apoptotic, autophagic and necrotic pathways: implications for cancer therapy development. J Cell Mol Med 2013; 17: 12-29.
37. Tschopp J,. Mitochondria: sovereign of inflammation? Eur J Immunol 2011; 41: 1196-1202.
38. Logan RM, Gibson RJ, Sonis ST, et al. Nuclear factor-kappaB (NF-kappaB) and cyclooxygenase-2 (COX-2) expression in the oral mucosa following cancer chemotherapy. Oral Oncol 2007; 43: 395-401.
39. Mauriz JL, Collado PS, Veneroso C, et al. A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J Pineal Res 2012; 54: 1-14.
40. Lima-Junior RC, Figueiredo AA, Freitas HC, et al. Involvement of nitric oxide on the pathogenesis of irinotecan-induced intestinal mucositis: role of cytokines on inducible nitric oxide synthase activation. Cancer Chemother Pharmacol 2012; 69: 931-942.
41. Reiter RJ,. Melatonin: clinical relevance. Best Pract Res Clin Endocrinol Metab 2003; 17: 273-285.
42. Li JH, Yu JP, Yu HG, et al. Melatonin reduces inflammatory injury through inhibiting NF-kappaB activation in rats with colitis. Mediators Inflamm 2005; 2005: 185-193.
43. Reiter RJ, Rosales-Corral SA, Liu XY, et al. Melatonin in the oral cavity: physiological and pathological implications. J Periodontal Res 2014; doi: 10.1111/jre.12176.
44. Manda K, Ueno M, Anzai K,. AFMK, a melatonin metabolite, attenuates X-ray-induced oxidative damage to DNA, proteins and lipids in mice. J Pineal Res 2007; 42: 386-393.
45. Kepp O, Galluzzi L, Kroemer G,. Mitochondrial control of the NLRP3 inflammasome. Nat Immunol 2011; 12: 199-200.
46. Tsutsui H, Imamura M, Fujimoto J, et al. The TLR4/TRIF-mediated activation of NLRP3 inflammasome underlies endotoxin-induced liver injury in mice. Gastroenterol Res Pract 2010; 2010: 641865.
47. Fistarol SK, Itin PH,. Anti-inflammatory treatment. Curr Probl Dermatol 2011; 40: 58-70.
48. Reiter RJ, Tan DX, Rosales-Corral S, et al. The universal nature, unequal distribution and antioxidant functions of melatonin and its derivatives. Mini Rev Med Chem 2013; 13: 373-384.
49. Acuña-Castroviejo D, Escames G, Venegas C, et al. Extrapineal melatonin: sources, regulation, and potential functions. Cell Mol Life Sci 2014; 71: 2997-3025.
50. Tan DX, Zanghi BM, Manchester LC, et al. Melatonin identified in meats and other food stuffs: potentially nutritional impact. J Pineal Res 2014; 57: 213-218.
51. Slominski AT, Kleszczynski K, Semak I, et al. Local melatoninergic system as the protector of skin integrity. Int J Mol Sci 2014; 15: 17705-17732.
52. Kedziora-Kornatowska K, Szewczyk-Golec K, Czuczejko J, et al. Antioxidative effects of melatonin administration in elderly primary essential hypertension patients. J Pineal Res 2008; 45: 312-317.
53. Mihandoost E, Shirazi A, Mahdavi SR, et al. Can melatonin help us in radiation oncology treatments? Biomed Res Int 2014; 2014: 578137.
54. Wang YM, Jin BZ, Ai F, et al. The efficacy and safety of melatonin in concurrent chemotherapy or radiotherapy for solid tumors: a meta-analysis of randomized controlled trials. Cancer Chemother Pharmacol 2012; 69: 1213-1220.
55. Martin V, Sanchez-Sanchez AM, Herrera F, et al. Melatonin-induced methylation of the ABCG2/BCRP promoter as a novel mechanism to overcome multidrug resistance in brain tumour stem cells. Br J Cancer 2013; 108: 2005-2012.
56. Erren TC, Reiter RJ,. Sleep duration, melatonin and breast cancer in the Singapore Chinese Health Study: on null results and their interpretation. Int J Cancer 2013; 133: 2010-2011.
57. Rodriguez C, Martin V, Herrera F, et al. Mechanisms involved in the pro-apoptotic effect of melatonin in cancer cells. Int J Mol Sci 2013; 14: 6597-6613.
58. Zhang S, Qi Y, Zhang H, et al. Melatonin inhibits cell growth and migration, but promotes apoptosis in gastric cancer cell line, SGC7901. Biotech Histochem 2013; 88: 281-289.