Beneficial actions of melatonin in the management of viral infections: A new use for this "molecular handyman"?

Reviews in Medical Virology

Volumn 22, Issue 5, 2012, Pages 323-338

  Boga, Jose Antonio ^a   Coto Montes, Ana ^a   Rosales Corral, Sergio A ^a   Tan, Dun Xian ^a   Reiter, Russel J ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MELATONIN;

ALEUTIAN MINK DISEASE; ANTIOXIDANT ACTIVITY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; HUMAN; NONHUMAN; REVIEW; TREATMENT OUTCOME; VENEZUELAN EQUINE ENCEPHALITIS; VIRUS ENCEPHALITIS; VIRUS INFECTION;

ANTIOXIDANTS; HUMANS; IMMUNOLOGIC FACTORS; MELATONIN; TREATMENT OUTCOME; VIRUS DISEASES;

EID: 84865793302     PISSN: 10529276     EISSN: 10991654     Source Type: Journal    
DOI: 10.1002/rmv.1714     Document Type: Review

References (194)

1. Lerner AB, Case JD, Takahashi Y, Lee TH, Mori N. Isolation of melatonin, a pineal factor that lightens melanocytes. Journal of the American Chemical Society 1958; 80: 2587.
2. Lerner AB, Case JD, Heinzelmann RV. Structure of melatonin. Journal of the American Chemical Society 1959; 81: 6084-6085.
3. Tamarkin L, Baird CJ, Alameida OF. Melatonin: a coordinating signal for mammalian reproduction. Science 1985; 227: 714-720.
4. Armstrong SM, Cassone VM, Chesworth MJ, Redman JR, Short RV. Synchronization of mammalian circadian rhythms by melatonin. Journal of Neural Transmission. Supplementum 1986; 21: 375-394.
5. Reiter RJ. The melatonin rhythm: both a clock and a calendar. Experientia 1993; 49: 654-664.
6. Reiter RJ, Tan DX, Manchester LC, Paredes SD, Mayo JC, Sainz RM. Melatonin and reproduction revisited. Biology of Reproduction 2009; 81: 445-456.
7. Reiter RJ, Tan DX, Sanchez-Barcelo E, Mediavilla MD, Gitto E, Korkmaz A. Circadian mechanisms in the regulation of melatonin synthesis: disruption with light at night and pathophysiological consequences. Journal of Experimental and Integrative Medicine 2011; 1: 13-22.
8. Reiter RJ. Melatonin: that ubiquitously acting pineal hormone. News in Physiology Science 1991; 6: 223-227.
9. Jou MJ, Peng TI, Yu PZ, et al. Melatonin protects against common deletion of mitochondrial DNA-augmented mitochondrial oxidative stress and apoptosis. Journal of Pineal Research 2007, 43:389-404.
10. Hardeland R, Poeggeler B. Melatonin beyond its classical functions. Open Physiology Journal 2008; 1: 1-23.
11. Hardeland R, Coto-Montes A. New vistas on oxidative damage and aging. Open Biology Journal 2010; 3: 39-52.
12. Acuna-Castroviejo D, Lopez LC, Escames G, Lopez A, Garcia JA, Reiter RJ. Melatonin-mitochondrial interplay in health and disease. Current Topics in Medicinal Chemistry 2011; 11: 221-240.
13. 2+-mediated permeability transition and beyond in rat brain astrocytes. Journal of Pineal Research 2010; 48: 20-38.
14. Reiter RJ, Richardson BA, Johnson LY, Ferguson BN, Dinh DT. Pineal melatonin rhythm: reduction in aging Syrian hamsters. Science 1980; 210: 1272-1273.
15. Reiter RJ, Craft CM, Johnson JE Jr, et al. Age-associated reduction in nocturnal pineal melatonin levels in female rats. Endocrinology 1981; 109: 1295-1297.
16. Sack RL, Lewy AJ, Erb DL, Vollmer WM, Singer CM. Human melatonin production decreases with age. Journal of Pineal Research 1986; 3: 379-388.
17. de Castro Silva C, de Bruin VMS, Cunho GMA, Nunes DM, Medieros CAM, de Bruin PFC. Melatonin improves sleep and reduces nitrite in the exhaled breath condensate in cystic fibrosis-randomized, double-blind, placebo-controlled study. Journal of Pineal Research 2010; 48: 65-71.
18. Rodella LF, Fillipini F, Bonomini F, Bresciani R, Reiter RJ, Rezzani R. Beneficial effects of melatonin on nicotine-induced vasculopathy. Journal of Pineal Research 2010; 48: 126-132.
19. Park SY, Jang WJ, Yi EY, et al. Melatonin suppresses tumor angiogenesis by inhibiting HIF-1α stabilization under hypoxia. Journal of Pineal Research 2010; 48: 178-184.
20. Chen CF, Wang D, Reiter RJ, Yeh DY. Oral melatonin attenuates lung inflammation and airway hyperactivity induced by aerosolized pancreatic fluid in rats. Journal of Pineal Research 2011; 50: 46-53.
21. Gitto E, Aversa S, Reiter RJ, Barberi I, Pellegrino S. Update on the use of melatonin in pediatrics. Journal of Pineal Research 2011; 50: 21-28.
22. Bonnefont-Rousselot D, Collin F. Melatonin: action as antioxidant and potential applications in human disease and aging. Toxicology 2010; 278: 55-67.
23. Sánchez-Barceló EJ, Mediavilla MD, Tan DX, Reiter RJ. Clinical uses of melatonin: evaluation of human trials. Current Medicinal Chemistry 2010; 17: 2070-2095.
24. Reiter RJ, Tan DX, Sainz RM, Mayo JC, Lopez-Burillo S. Melatonin: reducing the toxicity and increasing the efficacy of drugs. Journal of Pharmacy and Pharmacology 2002; 54: 1299-1321.
25. Tan DX, Chen LD, Poeggeler B, Manchester LC, Reiter RJ. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocrine Journal 1993; 1: 57-60.
26. Reiter RJ, Tan DX, Manchester LC, Qi W. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochemistry and Biophysics 2001; 34: 237-256.
27. Guerrero JM, Pozo D, García-Mauriño S, Osuna C, Molinero P, Calvo JR. Involvement of nuclear receptors in the enhanced IL-2 production by melatonin in Jurkat cells. Annals of the New York Academy of Sciences 2000; 917: 397-403.
28. Guerrero JM, Reiter RJ, Melatonin-immune system relationships. Current Topics in Medicinal Chemistry 2002; 2: 167-179.
29. Mediavilla MD, Sanchez-Barcelo EJ, Tan DX, Manchester L, Reiter RJ. Basic mechanisms involved in the anti-cancer effects of melatonin. Current Medicinal Chemistry 2010; 17: 4462-4481.
30. Maestroni GJ. Therapeutic potential of melatonin in immunodeficiency states, viral diseases, and cancer. Advances in Experimental Medicine and Biology 1999; 467: 217-226.
31. Huang SH, Cao XJ, Liu W, Shi XY, Wei W. Inhibitory effect of melatonin on lung oxidative stress induced by respiratory syncytial virus infection in mice. Journal of Pineal Research 2010; 48: 109-116.
32. Maestroni GJ, Conti A, Pierpaoli W. Pineal melatonin, its fundamental immunoregulatory role in aging and cancer. Annals of the New York Academy of Sciences 1988; 521: 140-148.
33. Ben-Nathan D, Maestroni GJM, Lustig S, Conti A. Protective effects of melatonin in mice infected with encephalitis viruses. Archives of Virology 1995; 140: 223-230.
34. Bonilla E, Valero-Fuenmayor N, Pons H, Chacín-Bonilla L. Melatonin protects mice infected with Venezuelan equine encephalomyelitis virus. Cellular and Molecular Life Sciences 1997; 53: 430-434.
35. Ellis LC. Melatonin reduces mortality from Aleutian disease in mink (Mustela vison). Journal of Pineal Research 1996; 21: 214-217.
36. de Groot H. Reactive oxygen species in tissue injury. Hepato-Gastroenterology 1994; 41: 328-332.
37. Toyokuni S. Reactive oxygen species-induced molecular damage and its application in pathology. Pathology International 1999; 49: 91-102.
38. Granger DL, Hibbs JB Jr, Perfect JR, Durack DT. Specific amino acid (l-arginine) requirement for microbiostatic activity of murine macrophages. The Journal of Clinical Investigation 1988; 81: 1129-1136.
39. Nathan CF, Hibbs JB Jr. Role of nitric oxide synthesis in macrophage antimicrobial activity. Current Opinion in Immunology 1991; 3: 65-70.
40. James SL. Role of nitric oxide in parasitic infections. Microbiological Reviews 1995; 59: 533-547.
41. Nathan C, Shiloh MU. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. The Journal of Clinical Investigation 2000; 97: 8841-8848.
42. Peterhans E, Grob M, Bürge T, Zanoni R. Virus-induced formation of reactive oxygen intermediates in phagocytic cells. Free Radical Research Communications 1987; 3: 39-46.
43. Oda T, Akaike T, Hamamoto T, Suzuki F, Hirano T, Maeda H. Oxygen radicals in influenza-induced pathogenesis and treatment with pyran polymer-conjugated SOD. Science 1989; 244: 974-976.
44. 2 generation by xanthine oxidase of pathogenesis of influenza virus infection in mice. The Journal of Clinical Investigation 1990; 85: 739-745.
45. Ikeda T, Shimokata K, Daikoku T, Fukatsu T, Tsutsui Y, Nishiyama Y. Pathogenesis of cytomegalovirus-associated pneumonitis in ICR mice: possible involvement of superoxide radicals. Archives of Virology 1992; 127: 11-24.
46. Schwartz KB. Oxidative stress during viral infection: a review. Free Radical Biology & Medicine 1996; 21: 641-649.
47. Stuehr DJ, Griffith OW. Mammalian nitric oxide synthase. Advances in Enzymology and Related Areas of Molecular Biology 1992; 65: 287-346.
48. Bukrinsky MI, Nottet HS, Schmidtmayerova H, et al. Regulation of nitric oxide synthase activity in human immunodeficiency virus type 1 (HIV-1)-infected monocytes: implications for HIV-associated neurological disease. The Journal of Experimental Medicine 1995; 181: 735-745.
49. Majano PL, García-Monzón C, López-Cabrera M, et al. Inducible nitric oxide synthase expression in chronic viral hepatitis. Evidence for a virus-induced gene upregulation. The Journal of Clinical Investigation 1998; 101: 1343-1352.
50. Dustin LB, Rice CM. Flying under the radar: the immunobiology of hepatitis C. Annual Review of Immunology 2007; 25: 71-99.
51. Zaki Mel S, Saudy N, El Diasty A. Study of nitric oxide in patients with chronic hepatitis C genotype 4: relationship to viremia and response to antiviral therapy. Immunological Investigations 2010; 39: 598-610.
52. Koprowski H, Zheng YM, Heber-Katz E, et al. In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases. Proceedings of the National Academy of Science USA 1993; 90: 3024-7.
53. Zheng YM, Schäfer MK, Weihe E, et al. Severity of neurological signs and degree of inflammatory lesions in the brains of the rats with Borna disease correlate with the induction of nitric oxide synthase. Journal of Virology 1993; 67: 5786-5791.
54. Karupiah G, Xie QW, Buller RM, Nathan C, Duarte C, MacMicking JD. Inhibition of viral replication by interferon-gamma-induced nitric oxide synthase. Science 1993; 261: 1445-1448.
55. Akaike T, Noguchi Y, Ijiri S, et al. Pathogenesis of influenza virus-induced pneumonia: involvement of both nitric oxide and oxygen radicals. Proceedings of the National Academy of Science USA 1996; 93: 2448-2453.
56. Akaike T, Suga M, Maeda H. Free radicals in viral pathogenesis: molecular mechanisms involving superoxide and NO. Proceedings of the Society for Experimental Biology and Medicine 1998; 217: 64-73.
57. Fujii S, Akaike T, Maeda H. Role of nitric oxide in pathogenesis of herpes simplex virus encephalitis in rats. Virology 1999; 256: 203-212.
58. Akaike T, Maeda H. Pathophysiological effects of high-output production of nitric oxide. In Nitric Oxide: Biology and Pathobiology, Ignarro LJ (ed.). Academic Press: San Diego, CA, 2000; 733-745.
59. Akaike T, Maeda H. Nitric oxide and virus infection. Immunology 2000; 101: 300-308.
60. Cunha FQ, Moncada S, Liew FY. Interleukin-10 (IL-10) inhibits the induction of nitric oxide synthase by interferon-gamma in murine macrophages. Biochemical and Biophysical Research Communications 1992; 182: 1155-1159.
61. Vodovotz Y, Bogdan C, Paik J, Xie QW, Nathan C. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor beta. The Journal of Experimental Medicine 1993; 178: 605-613.
62. Bogdan C, Vodovotz Y, Paik J, Xie QW, Nathan C. Mechanism of suppression of nitric oxide synthase expression by interleukin-4 in primary mouse macrophages. Journal of Leukocyte Biology 1994; 55: 227-233.
63. Adamson DC, Kopnisky KL, Dawson TM, Dawson VL. Mechanisms and structural determinants of HIV-1coat protein, gp41-induced neurotoxicity. Journal of Neuroscience 1999; 19: 64-71.
64. Hori K, Burd PR, Furuke K, et al. Human immunodeficiency virus-1-infected macrophages induce inducible nitric oxide synthase and nitric oxide (NO) production on astrocytes: astrocytic NO as a possible mediator of neuronal damage in acquired immunodeficiency syndrome. Blood 1999; 93: 1843-1850.
65. Tsutsumi H, Takeuchi R, Ohsaki M, Seki K, Chiba S. Respiratory syncytial virus infection of human respiratory epithelial cells enhances inducible nitric oxide synthase gene expression. Journal of Leukocyte Biology 1999; 66: 99-104.
66. Croen KD. Evidence for an antiviral effect of nitric oxide. Inhibition of herpes simplex virus type 1 replication. The Journal of Clinical Investigation 1993; 91: 2446-2452.
67. Mannick JB, Asano K, Izumi K, Kieff E, Stamler JS. Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell 1994; 79: 1137-1146.
68. Karupiah G, Chen JH, Nathan CF, Mahalingam S, MacMicking JD. Identification of nitric oxide synthase 2 as an innate resistance locus against ectromelia virus infection. Journal of Virology 1998; 72: 7703-7706.
69. Gao X, Tajima M, Sairenji T. Nitric oxide downregulates Epstein-Barr virus reactivation in epithelial cell lines. Virology 1999; 258: 375-381.
70. Saura M, Zaragoza C, McMillan A, et al. An antiviral mechanism of nitric oxide: inhibition of a viral proteinase. Immunity 1999; 10: 21-28.
71. Zaragoza C, Ocampo CJ, Saura M, et al. Inducible nitric oxide synthase protection against coxsackievirus pancreatitis.Journal of Immunology 1999; 163: 5497-5504.
72. Akaike T, Maeda H. Nitric oxide in influenza. In Nitric Oxide in Infection, Fang FC (ed.). Kluwer Academic/Plenum Publishers: New York, 1999; 397-415.
73. van den Broek M, Bachmann MF, Köhler G, et al. IL-4 and IL-10 antagonize IL-12-mediated protection against acute vaccinia virus infection with a limited role of IFN-gamma and nitric oxide synthetase 2. Journal of Immunology 2000; 164: 371-378.
74. Karupiah G, Chen JH, Mahalingam S, Nathan CF, MacMicking JD. Rapid interferon gamma-dependent clearance of influenza A virus and protection from consolidating pneumonitis in nitric oxide synthase 2-deficient mice. The Journal of Experimental Medicine 1998; 188: 1541-1546.
75. Bartholdy C, Nansen A, Christensen JE, Marker O, Thomsen AR. Inducible nitric-oxide synthase plays a minimal role in lymphocytic choriomeningitis virus induced, T cell-mediated protective immunity and immunopathology. The Journal of General Virology 1999; 80: 2997-3005.
76. Wu GF, Pewe L, Perlman S. Coronavirus-induced demyelination occurs in the absence of inducible nitric oxide synthase. Journal of Virology 2000; 74: 7683-7686.
77. Guillemard E, Varano B, Belardelli F, Quero AM, Gessani S. Inhibitory activity of constitutive nitric oxide on the expression of alpha/beta interferon genes in murine peritoneal macrophages. Journal of Virology 1999; 73: 7328-7333.
78. Kreil TR, Eibl MM. Nitric oxide and viral infection: no antiviral activity against a flavivirus in vitro, and evidence for contribution to pathogenesis in experimental infection in vivo. Virology 1996; 219: 304-306.
79. Adler H, Beland JL, Del-Pan NC, et al. Suppression of herpes simplex virus type 1 (HSV-1)-induced pneumonia in mice by inhibition of inducible nitric oxide synthase (iNOS, NOS2). The Journal of Experimental Medicine 1997; 185: 1533-1540.
80. Nishio R, Matsumori A, Shioi T, Ishida H, Sasayama S. Treatment of experimental viral myocarditis with interleukin-10. Circulation 1999; 100: 1102-1108.
81. Hirasawa K, Jun HS, Han HS, Zhang ML, Hollenberg MD, Yoon JW. Prevention of encephalomyocarditis virus-induced diabetes in mice by inhibition of the tyrosine kinase signaling pathway and subsequent suppression of nitric oxide production in macrophages. Journal of Virology 1999; 73: 8541-8548.
82. Andrews DM, Matthews VB, Sammels LM, Carrello AC, McMinn PC. The severity of Murray Valley encephalitis in mice is linked to neutrophil infiltration and inducible nitric oxide synthase activity in the central nervous system. Journal of Virology 1999; 73: 8781-8790.
83. Maeda H, Akaike T. Oxygen free radicals as pathogenic molecules in viral diseases. Proceedings of the Society for Experimental Biology and Medicine 1991; 198: 721-727.
84. Sidwell RW, Huffman JH, Bailey KW, Wong MH, Nimrod A, Panet A. Inhibitory effects of recombinant manganese superoxide dismutase on influenza virus infections in mice. Antimicrobial Agents and Chemotherapy 1996; 40: 2626-2631.
85. González-Gallego J, García-Mediavilla MV, Sánchez-Campos S. Hepatitis C virus, oxidative stress and steatosis: current status and perspectives. Current Molecular Medicine 2011; 11: 373-390.
86. Bureau C, Bernad J, Chaouche N, et al. Non-structural 3 protein of hepatitis C virus triggers ROS production in human monocytes via activation of NADPH oxidase. Journal of Biological Chemistry 2001; 276: 23077-23083.
87. Hiraku Y, Tabata T, Ma N, Murata M, Ding X, Kawanishi S. Nitrative and oxidative DNA damage in cervical intraepithelial neoplasia associated with human papilloma virus infection. Cancer Science 2007; 98: 964-972.
88. Lassoued S, Ben Ameur R, Ayadi W, Gargouri B, Ben Mansour R, Attia H. Epstein-Barr virus induces an oxidative stress during the early stages of infection in B lymphocytes, epithelial, and lymphoblastoid cell lines. Molecular and Cellular Biochemistry 2008; 313: 179-186.
89. Newman GW, Balcewicz-Sablinska MK, Guarnaccia JR, Remold HG, Silberstein DS. Opposing regulatory effects of thioredoxin and eosinophil cytotoxicity-enhancing factor on the development of human immunodeficiency virus 1. The Journal of Experimental Medicine 1994; 180: 359-363.
90. Suzuki YJ, Aggarwal BB, Packer L. Alpha-lipoic acid is a potent inhibitor of NF-kappa B activation in human T cells. Biochemical and Biophysical Research Communications 1992; 189: 1709-1715.
91. Holroyd KJ, Buhl R, Borok Z, et al. Correction of glutathione deficiency in the lower respiratory tract of HIV seropositive individuals by glutathione aerosol treatment. Thorax 1993; 48: 985-989.
92. Uchide N, Toyoda H. Antioxidant therapy as a potential approach to severe influenza-associated complications. Molecules 2011; 16: 2032-2052.
93. Pieri C, Marra M, Moroni F, Recchioni R, Marcheselli F. Melatonin: a peroxyl radical scavenger more effective than vitamin E. Life Sciences 1994; 55: PL271-PL276.
94. Reiter RJ, Melchiorri D, Sewerynek E, et al. A review of the evidence supporting melatonin's role as an antioxidant. Journal of Pineal Research 1995; 18: 1-11.
95. Reiter RJ. Functional aspects of the pineal hormone melatonin in combating cell and tissue damage induced by free radicals. European Journal of Endocrinology 1996; 134: 412-420.
96. Galano A, Tan DX, Reiter RJ. Melatonin as a natural ally against oxidative stress: a physiochemical examination. Journal of Pineal Research 2011; 51: 1-16.
97. Hardeland R. Melatonin and its metabolites as anti-nitrosating and anti-nitrating agents. Journal of Experimental and Integrative Medicine 2011; 1: 67-81.
98. Pablos MI, Agapito MT, Gutierrez R, et al. Melatonin stimulates the activity of the detoxifying enzyme glutathione in several tissues of chicks. Journal of Pineal Research 1995, 19:111-115.
99. Coto-Montes A, Boga JA, Tomás-Zapico C, et al. Physiological oxidative stress model: Syrian hamster Harderian gland-sex differences in antioxidant enzymes. Free Radical Biology & Medicine 2001, 30:785-792.
100. Rodriguez C, Mayo JC, Sainz RM, et al. Regulation of antioxidant enzymes: a significant role for melatonin. Journal of Pineal Research 2004; 36: 1-9.
101. Tomas-Zapico C, Coto-Montes A. A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. Journal of Pineal Research 2005; 39: 99-104.
102. Reiter RJ, Acuña-Castroviejo D, Tan DX, Burkhardt S. Free radical-mediated molecular damage. Ann NY Academy Sciences 2001; 939: 200-215.
103. Lanoix D, Lacasse AA, Reiter RJ, Vaillancourt C. Melatonin, the smart killer. The human trophoblast as a model. Molecular and Cellular Endocrinology 2012; 348: 1-111.
104. Venegas C, Garcia JA, Escames G, et al. Extra pineal melatonin: analysis of subcellular distribution and daily fluctuations. Journal of Pineal Research 2012; 52: 217-227.
105. Valero N, Meleán E, Bonilla E, et al. In vitro, melatonin treatment decreases nitric oxide levels in murine splenocytes cultured with the Venezuelan equine encephalomyelitis virus. Neurochemical Research 2005; 30: 1439-1442.
106. Valero N, Espina LM, Mosquera J. Melatonin decreases nitric oxide production, inducible nitric oxide synthase expression and lipid peroxidation induced by Venezuelan encephalitis equine virus in neuroblastoma cell cultures. Neurochemical Research 2006; 31: 925-932.
107. Valero N, Espina LM, Bonilla E, Mosquera J. Melatonin decreases nitric oxide production and lipid peroxidation and increases interleukin-1 beta in the brain of mice infected by the Venezuelan equine encephalomyelitis virus. Journal of Pineal Research 2007; 42: 107-112.
108. Parra F, Prieto M. Purification and characterization of a calicivirus as the causative agent of a lethal hemorrhagic disease in rabbits. Journal of Virology 1990; 64: 4013-4015.
109. Crespo I, Miguel BS, Laliena A, et al. Melatonin prevents the decreased activity of antioxidant enzymes and activates nuclear erythroid 2-related factor 2 signaling in an animal model of fulminant hepatic failure of viral origin. Journal of Pineal Research 2010; 49: 193-200.
110. Jung KH, Hong SW, Zheng HM, et al. Melatonin ameliorates cerulein-induced pancreatitis by the modulation of nuclear erythroid 2-related factor 2 and nuclear factor-kappaB in rats. Journal of Pineal Research 2010; 48: 239-250.
111. Brennan K, Bowie AG. Activation of host pattern recognition receptors by viruses. Current Opinion in Microbiology 2010; 13: 503-507.
112. Kanneganti TD. Central roles of NLRs and inflammasomes in viral infection. Nature Reviews Immunology 2010; 10: 688-698.
113. Mikula I Jr, Pastoreková S, Mikula I Sr. Toll-like receptors in immune response to the viral infections. Acta Virologica 2010; 54: 231-245.
114. Loo YM, Gale M Jr. Immune signaling by RIG-I-like receptors. Immunity 2011; 34: 680-692.
115. Fensteri V, Sen GC. Interferons and viral infections. BioFactors 2009; 35: 14-20.
116. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nature Reviews Immunology 2008; 8: 559-568.
117. Silverman RH. Viral encounters with 20, 50-oligoadenylate synthetase and RNase L during the interferon antiviral response. Journal of Virology 2007; 81: 12720-12729.
118. Espert L, Degols G, Gongora C, et al. ISG20, a new interferon-induced RNase specific for single-stranded RNA, defines an alternative antiviral pathway against RNA genomic viruses. Journal of Biological Chemistry 2003; 278: 16151-16158.
119. White CL, Sen GC. Interferons and antiviral action. In Cellular Signaling and Innate Immune Responses to RNA Virus Infections. Brasier AR, Garcia-Sastre A, Lemon SM (eds.) ASM Press: Washington, DC, 2002; 91-106.
120. Terenzi F, Hui DJ, Merrick WC, Sen GC. Distinct induction patterns and functions of two closely related interferon-inducible human genes, ISG54 and ISG56. Journal of Biological Chemistry 2006; 281: 34064-34071.
121. Wang C, Pflugheber J, Sumpter R Jr, et al. Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. Journal of Virology 2003; 77: 3898-3912.
122. Haller O, Kochs G, Weber F. Interferon, Mx, and viral countermeasures. Cytokine & Growth Factor Reviews 2007; 18: 425-433.
123. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signaling, antiviral responses and virus countermeasures. The Journal of General Virology 2008; 89: 1-47.
124. Aguiar RS, Peterlin BM. APOBEC3 proteins and reverse transcription. Virus Research 2008; 134: 74-85.
125. Guidotti LG, Chisari FV. Noncytolytic control of viral infections by the innate and adaptive immune response. Annual Review of Immunology 2001; 19: 65-91.
126. Malmgaard L. Induction and regulation of IFNs during viral infections. Journal of Interferon and Cytokine Research 2004; 24: 439-454.
127. Benyon RC, Bissonnette EY, Befus AD. Tumor necrosis factor-alpha dependent cytotoxicity of human skin mast cells is enhanced by anti-IgE antibodies. Journal of Immunology 1991; 147: 2253-2258.
128. Bradding P, Feather IH, Wilson S, et al. Immunolocalization of cytokines in the nasal mucosa of normal and perennial rhinitic subjects. The mast cell as a source of IL-4, IL-5, and IL-6 in human allergic mucosal inflammation. Journal of Immunology 1993; 151: 3853-3865.
129. Kaplan AP, Kuna P, Reddigari SR. Chemokines and the allergic response. Experimental Dermatology 1995; 4: 260-265.
130. Sampson AP. The role of eosinophils and neutrophils in inflammation. Clinical and Experimental Allergy 2000; 1(Suppl.): 22-27.
131. Mosmann TR, Coffman RL. Th-1and Th-2 cells: different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology 1989; 7: 145-173.
132. +) T cells and Th1 dominance during lymphocytic choriomeningitis virus infection. Journal of Virology 2000; 74: 4429-4432.
133. Tan DX, Manchester LC, Reiter RJ, et al. Identification of highly elevated levels of melatonin in bone marrow: its origin and significance. Biochimica et Biophysica Acta 1999; 1471: 206-214.
134. Kvetnoy IM. Extrapineal melatonin: location and role within diffuse neuroendocrine system. The Histochemical Journal 1999; 31: 1-12.
135. Carrillo-Vico A, Calvo JR, Abreu P, et al. Evidence of melatonin synthesis by human lymphocytes and its physiological significance: possible role as intracrine, autocrine, and/or paracrine substance. The FASEB Journal 2004; 18: 537-539.
136. Pozo D, Delgado M, Fernandez-Santos JM, et al. Expression of the Mel1a-melatonin receptor mRNA in T and B subsets of lymphocytes from rat thymus and spleen. The FASEB Journal 1997; 11: 466-473.
137. Garcia-Mauriño S, Gonzalez-Haba MG, Calvo IR, et al. Melatonin enhances IL-2, lL-6, and IFN-gamma production by human circulating CD4+ cells: a possible nuclear receptor-mediated mechanism involving T helper type I lymphocytes and monocytes. Journal of Immunology 1997; 159: 574-581.
138. Lardone PJ, Carrillo-Vico A, Molinero P, Rubio A, Guerrero JM. A novel interplay between membrane and nuclear melatonin receptors in human lymphocytes: significance in IL-2 production. Cellular and Molecular Life Sciences 2009; 66: 516-525.
139. Carrillo-Vico A, Guerrero JM, Lardone PJ, Reiter RJ. A review of the multiple actions of melatonin on the immune system. Endocrine 2005; 27: 189-200.
140. Lardone PJ, Alvarez-García O, Carrillo-Vico A, et al. Inverse correlation between endogenous melatonin levels and oxidative damage in some tissues of SAMP8 mice. Journal of Pineal Research 2006; 40: 153-157.
141. Szczepanik M. Melatonin and its influence on immune system. Journal of Physiology and Pharmacology 2007; 58: 115-124.
142. Caballero B, Vega-Naredo I, Sierra V, et al. Autophagy upregulation and loss of NF-kappaB in oxidative stress-related immunodeficient SAMP8 mice. Mechanisms of Ageing and Development 2009; 130: 722-730.
143. Belyaer O, Herzog T, Munding J, et al. Protective role of endogenous melatonin in the early course of acute pancreatitis. Journal of Pineal Research 2011; 50: 71-77.
144. Radogna F, Diederich M, Ghibelli L. Melatonin: a pleiotropic molecule regulating inflammation. Biochemical Pharmacology 2010; 80: 1844-1852.
145. Morrey KM, McLachlan JA, Serkin CD, Bakouche O. Activation of human monocytes by the pineal hormone melatonin. Journal of Immunology 1994; 153: 2671-2680.
146. Finocchiaro LM, Arzt ES, Fernandez-Castelo S, Crisculo M, Finkielman S, Nahmod VE. Serotonin and melatonin synthesis in peripheral blood mononuclear cells: stimulation by interferon-gamma as part of an immunomodulatory pathway. Journal of Interferon Research 1988; 8: 705-716
147. Bonilla E, Nereida V, Chacín-Bonilla L, Medina-Leendertz S. Melatonin and viral infections. Journal of Pineal Research 2004; 36: 73-79.
148. Currier NL, Sun LZ, Miller SC. Exogenous melatonin: quantitative enhancement in vivo of cells mediating non-specific immunity. Journal of Neuroimmunology 2000; 104: 101-108.
149. Castrillon PO, Esquifino AI, Varas A, Zapata A, Cutrera RA, Cardinali DP. Effect of melatonin treatment on 24-h variations in responses to mitogens and lymphocyte subset populations in rat submaxillary lymph nodes. Journal of Neuroendocrinology 2000; 12: 758-765.
150. Carrillo-Vico A, Reiter RJ, Lardone PJ, et al. The modulatory role of melatonin on immune responsiveness. Current Opinion in Investigational Drugs 2006; 7: 423-431.
151. Gazzinelli RT, Makino M, Chattopadhyay SK, et al. CD4+ subset regulation in viral infection. Preferential activation of Th2 cells during progression of retrovirus-induced immunodeficiency in mice. Journal of Immunology 1992; 148: 182-188.
152. Bradley WG, Ogata N, Good RA, Day NK. Alteration of in vivo cytokine gene expression in mice infected with a molecular clone of the defective MAIDS virus. Journal of Acquired Immune Deficiency Syndromes 1994; 7: 1-9.
153. Clerici M, Hakim FT, Venzon DJ, et al. Changes in interleukin-2 and interleukin-4 production in asymptomatic, human immunodeficiency virus-seropositive individuals. The Journal of Clinical Investigation 1993; 91: 759-765.
154. Wang Y, Huang DS, Liang B, Watson RR. Nutritional status and immune responses in mice with murine AIDS are normalized by vitamin E supplementation. Journal of Nutrition 1994; 124: 2024-2032.
155. Zhang Z, Araghi-Niknam M, Liang B, et al. Prevention of immune dysfunction and vitamin E loss by dehydroepiandrosterone and melatonin supplementation during murine retrovirus infection. Immunology 1999; 96: 291-297.
156. Srinivasan V, Spence DW, Trakhi I, Pandi-Perumal SR, Cardinali DP, Maestroni GJ. lmmunomodulation by melatonin: its significance for seasonally occurring diseases. Neuroimmuno-modulation 2008; 15: 93-101.
157. Nunnari G, Nigro L, Palermo F, Leto D, Pomerantz RJ, Cacopardo B. Reduction of serum melatonin levels in HIV-1-infected individuals' parallel disease progression: correlation with serum interleukin-12 levels. Infection 2003; 31: 379-382.
158. Bonilla E, Rodón C, Valero N, et al. Melatonin prolongs survival of immunodepressed mice infected with the Venezuelan equine encephalomyelitis virus. Transactions of the Royal Society of Tropical Medicine and Hygiene 2001; 95: 207-210.
159. Valero N, Bonilla E, Pons H, et al. Melatonin induces changes to serum cytokines in mice infected with the Venezuelan equine encephalomyelitis virus. Transactions of the Royal Society of Tropical Medicine and Hygiene 2002; 96: 348-351.
160. Dinarello CA. The biological properties of interleukin-1. European Cytokine Network 1994; 5: 517-531.
161. Liang XH, Goldman JE, Jiang HH, Levine B. Resistance of interleukin-1 beta-deficient mice to fatal Sindbis virus encephalitis. Journal of Virology 1999; 73: 2563-2567.
162. Kozak W. Thermal and behavioural effects of lipopolysaccharide and influenza in interleukin-1 beta deficient mice. American Journal of Physiology 1995; 269: R969-R977.
163. Spriggs MK, Hruby DE, Maliszewski CR, et al. Vaccinia and cowpox viruses encode a novel secreted interleukin-1-binding protein. Cell 1992; 71: 145-152.
164. Carman-Krzan M, Wise BC. Arachidonic acid lipoxygenation may mediate interleukin-1 stimulation of nerve growth factor secretion in astroglial cultures. Journal of Neuroscience Research 1993; 34: 225-232.
165. Tweardy DJ, Glazer EW, Mott PL, Anderson K. Modulation by tumor necrosis factor-a of human astroglial cell production of granulocyte-macrophage colony stimulating factor (G-CSF).Journal of Neuroimmunology 1991; 32: 269-278.
166. McCarron RM, Wang L, Racke MK, McFarlin DE, Spatz M. Cytokine-regulated adhesion between encephalitogenic T lymphocytes and cerebrovascular endothelial cells. Journal of Neuroimmunology 1993; 43: 23-30.
167. Baydas G, Nedzvetsky NS, Nerush PA, Kiricheuko SV, Demchenko HM, Reiter RJ. A novel role for melatonin: regulation of the expression of cell adhesion molecules in the rat hippocampus and cortex. Neuroscience Letters 2002; 326: 109-112.
168. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-jB by Toll-like receptor 3. Nature 2001; 413: 732-738.
169. Tian B, Zhang Y, Luxon BA, et al. Identification of NF-kappaB-dependent gene networks in respiratory syncytial virus-infected cells. Journal of Virology 2002; 76: 6800-6814.
170. Huang SH, Cao XJ, Wei W. Melatonin decreases TLR3-mediated inflammatory factor expression via inhibition of NF-kappa B activation in respiratory syncytial virus-infected RAW264.7 macrophages. Journal of Pineal Research 2008; 45: 93-100.
171. Koyama AH, Irie H, Fukumori T, Hata S, Iida S, et al. Role of virus-induced apoptosis in a host defense mechanism against virus infection. The Journal of Medical Investigation 1998, 45:37-45.
172. Danthi P. Enter the kill zone: initiation of death signaling during virus entry. Virology 2011; 411: 316-324.
173. 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. Cellular and Molecular Life Sciences 2003; 60: 1407-1426.
174. Casao A, Mendoza N, Perez-Pe R, et al. Melatonin prevents capacitation and apoptotic-like changes in ram spermatozoa and increases fertility. Journal of Pineal Research 2010; 48: 39-46.
175. Kim CH, Kim KH, Yoo YM. Melatonin protects against apoptotic and autophagic cell death in C2 C12 murine myoblast cells. Journal of Pineal Research 2011; 50: 241-249.
176. Espino J, Bejarano I, Paredes SD, Barriga C, Rodriguez AB, Pariente JA. Protective effect of melatonin against human leucocyte apoptosis induced by intracellular calcium overload: relation with its antioxidant actions. Journal of Pineal Research 2011; 51: 195-206.
177. 1-adenosine monophosphate-activated kinase-alpha in human leukemia HL-60 cells. Journal of Pineal Research 2011; 50: 369-373.
178. Alonso C, Oviedo JM, Martín-Alonso JM, Díaz E, Boga JA, Parra F. Programmed cell death in the pathogenesis of rabbit hemorrhagic disease. Archives of Virology 1998; 143: 321-332.
179. Tuñón MJ, San Miguel B, Crespo I, et al. Melatonin attenuates apoptotic liver damage in fulminant hepatic failure induced by the rabbit hemorrhagic disease virus. Journal of Pineal Research 2011; 50: 38-45.
180. Grose C. Autophagy during common bacterial and viral infections of children. Pediatric Infectious Disease Journal 2010; 29: 1040-1042.
181. Takahashi MN, Jackson W, Laird DT, et al. Varicella-zoster virus infection induces autophagy in both cultured cells and human skin vesicles. Journal of Virology 2009; 83: 5466-5476.
182. Dreux M, Chisari FV. Autophagy proteins promote hepatitis C virus replication. Autophagy 2009; 5: 1224-1225.
183. Casais R, Molleda LG, Machín A, et al. Structural and functional analysis of virus factories purified from Rabbit vesivirus-infected Vero cells. Virus Research 2008; 137: 112-121.
184. Suhy DA, Giddings TH Jr., Kirkegaard K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. Journal of Virology 2000; 74: 8953-8965.
185. Vega-Naredo I, Caballero B, Sierra V, et al. Melatonin modulates autophagy through a redox-mediated action in female Syrian hamster Harderian gland controlling cell types and gland activity. Journal of Pineal Research 2012; 52: 80-92.
186. Nunes Oda S, Pereira Rde S. Regression of herpes viral infection symptoms using melatonin and SB-73: comparison with Acyclovir. Journal of Pineal Research 2008; 44: 373-378.
187. Reiter RJ. Pineal melatonin: cell biology of its synthesis and of its physiological interactions. Endocrine Reviews 1991; 12: 151-180.
188. Reiter RJ, Tan DX, Fuentes-Broto L. Melatonin: a multitasking molecule. Progress in Brain Research 2010; 181: 127-151.
189. Stehle J, Saade A, Rawashdeh O, et al. A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function and chronobiological diseases. Journal of Pineal Research 2011; 51: 17-43.
190. Jung-Hynes B, Reiter RJ, Ahmad N. Sirtuins, melatonin and circadian rhythms: building a bridge between aging and cancer. Journal of Pineal Research 2010; 48: 9-19.
191. Paradies G, Petroillo G, Paradies V, Reiter RJ, Ruggiero FM. Melatonin, cardiolipin and mitochondrial bioenergetics in health and disease. Journal of Pineal Research 2010; 48: 297-310.
192. Rosenstein RE, Pandi-Perumal SR, Srinivasan V, Spence DW, Brown GM, Cardinali DP. Melatonin as a therapeutic tool in ophthalmology: implications for glaucoma and uveitis. Journal of Pineal Research 2010; 49: 1-13.
193. Reiter RJ, Tan DX, Korkmaz A, Fuentes-Broto C. Drug-mediated ototoxicity and tinnitus: alleviation with melatonin. Journal of Physiology and Pharmacology 2011; 62: 151-154.
194. Swarnakar S, Paul S, Singh LP, Reiter RJ. Matrix metalloproteinases in health and disease: regulation by melatonin. Journal of Pineal Research 2011; 50: 8-20.