Selective protection of the cerebellum against intracerebroventricular LPS is mediated by local melatonin synthesis

Brain Structure and Function

Volumn 220, Issue 2, 2015, Pages 827-840

  Pinato, Luciana ^a,b   da Silveira Cruz Machado, Sanseray ^a   Franco, Daiane G ^a   Campos, Leila M G ^a   Cecon, Erika ^a   Fernandes, Pedro A C M ^a   Bittencourt, Jackson C ^a   Markus, Regina P ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Arylalkylamine N acetyltransferase (AA NAT); Immune pineal axis; Melatonin receptors; Neuroinflammation; Nuclear factor kappa B (NF B); Pineal gland

Indexed keywords

LIPOPOLYSACCHARIDE; MELATONIN;

ANIMAL; BIOSYNTHESIS; CELL SURVIVAL; CEREBELLUM; CHEMICALLY INDUCED; DRUG EFFECTS; ENCEPHALITIS; GLIA; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; MALE; METABOLISM; NERVE CELL; PINEAL BODY; RAT; WISTAR RAT;

ANIMALS; CELL SURVIVAL; CEREBELLUM; ENCEPHALITIS; INFUSIONS, INTRAVENTRICULAR; LIPOPOLYSACCHARIDES; MALE; MELATONIN; NEUROGLIA; NEURONS; PINEAL GLAND; RATS; RATS, WISTAR;

EID: 84890362870     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0686-4     Document Type: Article

References (75)

1. Adamah-Biassi E, Zhang Y, Jung H, Vissapragada S, Miller R, Dubocovich M (2013) Distribution of MT1 melatonin receptor promoter-driven RFP expression in the brains of BAC C3H/HeN transgenic mice. J Histochem Cytochem. doi:10.1369/0022155413507453 (Epub ahead of print)
2. Al-Ghoul WM, Herman MD, Dubocovich ML (1998) Melatonin receptor subtype expression in human cerebellum. Neuroreport 9:4063–4068
3. Alonso-Alconada D, Alvarez A, Lacalle J, Hilario E (2012) Histological study of the protective effect of melatonin on neural cells after neonatal hypoxia-ischemia. Histol Histopathol 27:771–783
4. Barrett P, Bolborea M (2012) Molecular pathways involved in seasonal body weight and reproductive responses governed by melatonin. J Pineal Res 52:376–388. doi:10.1111/j.1600-079X.2011.00963.x
5. Bubenik GA (2001) Localization, physiological significance and possible clinical implication of gastrointestinal melatonin. Neurosignals 10:350–366. doi:10.1159/000046903
6. Butovsky O, Hauben E, Schwartz M (2001) Morphological aspects of spinal cord autoimmune neuroprotection: colocalization of T cells with B7-2 (CD86) and prevention of cyst formation. FASEB J 15:1065–1067. doi:10.1096/fj.00-0550fje
7. Butovsky O, Talpalar AE, Ben-Yaakov K, Schwartz M (2005) Activation of microglia by aggregated β-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-γ and IL-4 render them protective. Mol Cell Neurosci 29:381–393. doi:10.1016/j.mcn.2005.03.005
8. Cardinali DP, Furio AM, Brusco LI (2010) Clinical aspects of melatonin intervention in Alzheimer’s disease progression. Curr Neuropharmacol 8:218–227. doi:10.2174/157015910792246209
9. Carrillo-Vico A, Calvo JR, Abreu P, Lardone PJ, Garcia-Maurino S, Reiter RJ, Guerrero JM (2004) Evidence of melatonin synthesis by human lymphocytes and its physiological significance: possible role as intracrine, autocrine, and/or paracrine substance. FASEB J 18:537–539. doi:10.1096/fj.03-0694fje
10. Carrillo-Vico A, Lardone PJ, Alvarez-Sánchez N, Rodríguez-Rodríguez A, Guerrero JM (2013) Melatonin: buffering the immune system. Int J Mol Sci 14:8638–8683. doi:10.3390/ijms14048638
11. Carvalho-Sousa CE, da Silveira Cruz-Machado S, Tamura EK, Fernandes PA, Pinato L, Muxel SM, Cecon E, Markus RP (2011) Molecular basis for defining pineal gland and pinealocytes as targets for tumor necrosis factor (TNF). Fr Endocrinol 2:1–11. doi:10.3389/fendo.2011.00010
12. Cary GA, Cuttler AS, Duda KA, Kusema ET, Myers JA, Tilden AR (2012) Melatonin: neuritogenesis and neuroprotective effects in crustacean x-organ cells. Comp Biochem Physiol A: Mol Integr Physiol 161:355–360. doi:10.1016/j.cbpa.2011.12.005
13. Cecon E, Fernandes PA, Pinato L, Ferreira ZS, Markus RP (2010) Daily variation of constitutively activated nuclear factor kappa B (NFKB) in rat pineal gland. Chronobiol Int 27:52–67. doi:10.3109/07420521003661615
14. Cecon E, Markus RP (2011) Relevance of the chronobiological and non-chronobiological actions of melatonin for enhancing therapeutic efficacy in neurodegenerative disorders. Recent Pat Endocr Metab Immune Drug Discov 5:91–99. doi:10.2174/187221411799015381
15. Conti A, Conconi S, Hertens E, Skwarlo-Sonta K, Markowska M, Maestroni GJM (2000) Evidence for melatonin synthesis in mouse and human bone marrow cells. J Pineal Res 28:193–202. doi:10.1034/j.1600-079X.2000.280401.x
16. Da Silveira Cruz-Machado S, Carvalho-Sousa CE, Tamura EK, Pinato L, Cecon E, Fernandes PACM, De Avellar MCW, Ferreira ZS, Markus RP (2010) TLR4 and CD14 receptors expressed in rat pineal gland trigger NFKB pathway. J Pineal Res 49:183–192. doi:10.1111/j.1600-079X.2010.00785.x
17. Da Silveira Cruz-Machado S, Pinato L, Tamura EK, Carvalho-Sousa CE, Markus RP (2012) Glia-pinealocyte network: the paracrine modulation of melatonin synthesis by Tumor Necrosis Factor (TNF). PLoS One 7:e40142. doi:10.1371/journal.pone.0040142
18. De Butte M, Pappas BA (2007) Pinealectomy causes hippocampal CA1 and CA3 cell loss: reversal by melatonin supplementation. Neurobiol Aging 28:306–313. doi:10.1016/j.neurobiolaging.2005.12.004
19. Espinosa-Oliva AM, de Pablos RM, Villarán RF, Argüelles S, Venero JL, Machado A, Cano J (2011) Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol Aging 32:85–102. doi:10.1016/j.neurobiolaging.2009.01.012
20. Fan X, van Bel F (2010) Pharmacological neuroprotection after perinatal asphyxia. J Matern Fetal Neonatal Med 23:17–19. doi:10.3109/14767058.2010.505052
21. Fernandes P, Markus R (2011) Melatonin and inflammation. The role of the immune-pineal axis and the sympathetic tonus. In: Watson RR (ed) Melatonin in the promotion of health. CRC Press, Taylor & Francis Group, NW, pp 435–446
22. Fernandes PACM, Cecon E, Markus RP, Ferreira ZS (2006) Effect of TNF-α on the melatonin synthetic pathway in the rat pineal gland: basis for a ‘feedback’ of the immune response on circadian timing. J Pineal Res 41:344–350. doi:10.1111/j.1600-079X.2006.00373.x
23. Fink T, Glas M, Wolf A, Kleber A, Reus E, Wolff M, Kiefer D, Wolf B, Rensing H, Volk T, Mathes AM (2013) Melatonin receptors mediate improvements of survival in a model of polymicrobial sepsis. Crit Care Med. doi:10.1097/CCM.0b013e3182a63e2b (Epub ahead of print)
24. Finocchiaro LM, Nahmod VE, Launay JM (1991) Melatonin biosynthesis and metabolism in peripheral blood mononuclear leukocytes. Biochem J 280:727–731
25. Fraschini F, Cesarani A, Alpini D, Esposti D, Stankov BM (1999) Melatonin influences human balance. Biol Signals Recept 8:111–119. doi:10.1159/000014578
26. Galano A, Tan DX, Reiter RJ (2011) Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 51:1–16. doi:10.1111/j.1600-079X.2011.00916.x
27. Galano A, Tan DX, Reiter RJ (2013) On the free radical scavenging activities of melatonin’s metabolites, AFMK and AMK. J Pineal Res 54:245–257. doi:10.1111/jpi.12010
28. Gern WA, Ralph CL (1979) Melatonin synthesis by the retina. Science 204:183–184. doi:10.1126/science.432640
29. Gupta S, Haldar C (2013) Physiological crosstalk between melatonin and glucocorticoid receptor modulates T-cell mediated immune responses in a wild tropical rodent, Funambulus pennanti. J Steroid Biochem Mol Biol 134:23–36. doi:10.1016/j.jsbmb.2012.09.013
30. Hald A, Lotharius J (2005) Oxidative stress and inflammation in Parkinson’s disease: is there a causal link? Exp Neurol 193:279–290. doi:10.1016/j.expneurol.2005.01.013
31. Hardeland R (2012) Neurobiology, pathophysiology, and treatment of melatonin deficiency and dysfunction. Sci World J 2012:640389. doi:10.1100/2012/640389
32. Hardeland R, Madrid JA, Tan DX, Reiter RJ (2012) Melatonin, the circadian multioscillator system and health: the need for detailed analyses of peripheral melatonin signaling. J Pineal Res 52:139–166. doi:10.1111/j.1600-079X.2011.00934.x
33. K-i Hashimoto, Ueda S, Ehara A, Sakakibara S-i, Yoshimoto K, Hirata K (2012) Neuroprotective effects of melatonin on the nigrostriatal dopamine system in the zitter rat. Neurosci Lett 506:79–83. doi:10.1016/j.neulet.2011.10.053
34. Huan C, Zhou M, Wu M, Zhang Z, Mei Y (2001) Activation of melatonin receptor increases a delayed rectifier K+ current in rat cerebellar granule cells. Brain Res 917:182–190. doi:10.1016/S0006-8993(01)02915-8
35. Husson I, Mesplès B, Bac P, Vamecq J, Evrard P, Gressens P (2002) Melatoninergic neuroprotection of the murine periventricular white matter against neonatal excitotoxic challenge. Ann Neurol 51:82–92. doi:10.1002/ana.10072
36. Imbesi M, Uz T, Manev H (2008) Role of melatonin receptors in the effects of melatonin on BDNF and neuroprotection in mouse cerebellar neurons. J Neural Transm 115:1495–1499. doi:10.1007/s00702-008-0066-z
37. Jimenez-Jorge S, Guerrero JM, Jimenez-Caliani AJ, Naranjo MC, Lardone PJ, Carrillo-Vico A, Osuna C, Molinero P (2007) Evidence for melatonin synthesis in the rat brain during development. J Pineal Res 42:240–246. doi:10.1111/j.1600-079X.2006.00411.x
38. Kim W-G, Mohney RP, Wilson B, Jeohn G-H, Liu B, Hong J-S (2000) Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci 20:6309–6316
39. Kipp M, Norkute A, Johann S, Lorenz L, Braun A, Hieble A, Gingele S, Pott F, Richter J, Beyer C (2008) Brain-region-specific astroglial responses in vitro after LPS exposure. J Mol Neurosci 35:235–243. doi:10.1007/s12031-008-9057-7
40. 1 receptor impairs the activation of Jurkat T cells. Cell Mol Life Sci 67:3163–3172. doi:10.1007/s00018-010-0374-y
41. Laudon M, Nir I, Zisapel N (1998) Melatonin receptors in discrete brain areas of the male rat. Impact of aging on density and on circadian rhythmicity. Neuroendocrinology 48:577–583. doi:10.1159/000125066
42. Liu LY, Hoffman GE, Fei XW, Li Z, Zhang ZH, Mei YA (2007a) Delayed rectifier outward K+ current mediates the migration of rat cerebellar granule cells stimulated by melatonin. J Neurochem 102:333–344. doi:10.1111/j.1471-4159.2007.04669.x
43. Liu Y-J, Zhuang J, Zhu H-Y, Shen Y-X, Tan Z-L, Zhou J-N (2007b) Cultured rat cortical astrocytes synthesize melatonin: absence of a diurnal rhythm. J Pineal Res 43:232–238. doi:10.1111/j.1600-079X.2007.00466.x
44. McCall CE, El Gazzar M, Liu T, Vachharajani V, Yoza B (2011) Epigenetics, bioenergetics, and microRNA coordinate gene-specific reprogramming during acute systemic inflammation. J Leukoc Biol 90:439–446. doi:10.1189/jlb.0211075
45. Markus R, Cecon E, Pires-Lapa M (2013) Immune-pineal axis: Nuclear Factor κB (NF-kB) mediates the shift in the melatonin source from pinealocytes to immune competent cells. Int J Mol Sci 14:10979–10997. doi:10.3390/ijms140610979
46. Markus RF, Ferreira ZS, Fernandes PACM, Cecon E (2007) The immune-pineal axis: a shuttle between endocrine and paracrine melatonin sources. NeuroImmunoModulation 14:126–133. doi:10.1159/000110635
47. Markus RP, Ferreira ZS (2011) The immune-pineal axis: the role of pineal and extra-pineal melatonin in modulating inflammation. Adv Neuroimmune Biol 1:95–104. doi:10.3233/nib-2011-009
48. Martins EJr, Ferreira AC, Skorupa AL, Afeche SC, Cipolla-Neto J, Costa Rosa LF (2004) Trptophan consumption and indoleamines production by peritoneal cavity macrophages. J Leukoc Biol 75:1116–1121. doi:10.1189/jlb.1203614
49. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201–211
50. Muxel SM, Pires-Lapa MA, Monteiro AWA, Cecon E, Tamura EK, Floeter-Winter LM, Markus RP (2012) NF-κB drives the synthesis of melatonin in RAW 264.7 macrophages by inducing the transcription of the Arylalkylamine-N-Acetyltransferase (AA-NAT) gene. PLoS One 7:e52010. doi:10.1371/journal.pone.0052010
51. O’Neill LAJ, Kaltschmidt C (1997) NF-kB: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20:252–258. doi:10.1016/s0166-2236(96)01035-1
52. Pandi-Perumal S, BaHammam A, Brown G, Spence DW, Bharti V, Kaur C, Hardeland R, Cardinali D (2012) Melatonin antioxidative defense: therapeutical implications for aging and neurodegenerative processes. Neurotox Res 23:267–300. doi:10.1007/s12640-012-9337-4
53. Pintado C, Revilla E, Vizuete ML, Jiménez S, García-Cuervo L, Vitorica J, Ruano D, Castaño A (2011) Regional difference in inflammatory response to LPS-injection in the brain: role of microglia cell density. J Neuroimmunol 238:44–51. doi:10.1016/j.jneuroim.2011.06.017
54. Pontes GN, Cardoso EC, Carneiro-Sampaio MMS, Markus RP (2006) Injury switches melatonin production source from endocrine (pineal) to paracrine (phagocytes)—melatonin in human colostrum and colostrum phagocytes. J Pineal Res 41:136–141. doi:10.1111/j.1600-079X.2006.00345.x
55. Pires-Lapa MA, Tamura EK, Salustiano EM, Markus RP (2013) Melatonin synthesis in human colostrum mononuclear cells enhances dectin-1-mediated phagocytosis by mononuclear cells. J Pineal Res 55:240–246. doi:10.1111/jpi.12066
56. Qian L, Flood PM, Hong JS (2010) Neuroinflammation is a key player in Parkinson’s disease and a prime target for therapy. J Neural Transm 117:971–979. doi:10.1007/s00702-010-0428-1
57. Radogna F, Paternoster L, Albertini MC, Cerella C, Accorsi A, Bucchini A, Spadoni G, Diamantini G, Tarzia G, De Nicola M, DAlessio M, Ghibelli L (2007) Melatonin antagonizes apoptosis via receptor interaction in U937 monocytic cells. J Pineal Res 43:154–162. doi:10.1111/j.1600-079X.2007.00455.x
58. Raikhlin NT, Kvetnoy IM, Tolkachev VN (1975) Melatonin may be synthesised in enterochromaffin cells. Nature 255:344–345. doi:10.1038/255344a0
59. Rennie K, De Butte M, Pappas BA (2009) Melatonin promotes neurogenesis in dentate gyrus in the pinealectomized rat. J Pineal Res 47:313–317. doi:10.1111/j.1600-079X.2009.00716.x
60. Rivest S (2009) Regulation of innate immune responses in the brain. Nat Rev Immunol 9:429–439. doi:10.1038/nri2565
61. Sastre M, Klockgether T, Heneka MT (2006) Contribution of inflammatory processes to Alzheimer’s disease: molecular mechanisms. Int J Dev Neurosci 24:167–176. doi:10.1016/j.ijdevneu.2005.11.014
62. Schmidt OI, Heyde CE, Ertel W, Stahel PF (2005) Closed head injury-an inflammatory disease? Brain Res Brain Res Rev 48:388–399
63. Srinivasan V, Cardinali DP, Srinivasan US, Kaur C, Brown GM, Spence DW, Hardeland R, Pandi-Perumal SR (2011) Therapeutic potential of melatonin and its analogs in Parkinson’s disease: focus on sleep and neuroprotection. Ther Adv Neurol Disord 4:297–317. doi:10.1177/1756285611406166
64. Tan D-X, Hardeland R, Manchester LC, Paredes SD, Korkmaz A, Sainz RM, Mayo JC, Fuentes-Broto L, Reiter RJ (2010a) The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness. Biol Rev 85:607–623. doi:10.1111/j.1469-185X.2009.00118.x
65. Tan DX, Manchester LC, Sanchez-Barcelo E, Mediavilla MD, Reiter RJ (2010b) Significance of high levels of endogenous melatonin in mammalian cerebrospinal fluid and in the central nervous system. Curr Neuropharmacol 8:162–167. doi:10.2174/157015910792246182
66. Tansey MG, Goldberg MS (2010) Neuroinflammation in Parkinson’s disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol Dis 37:510–518. doi:10.1016/j.nbd.2009.11.004
67. Tosini G, Menaker M (1996) Circadian rhythms in cultured mammalian retina. Science 272:419–421. doi:10.1126/science.272.5260.419
68. Uz T, Qu T, Sugaya K, Manev H (2002) Neuronal expression of arylalkylamine N-acetyltransferase (AANAT) mRNA in the rat brain. Neurosci Res 42:309–316. doi:10.1016/s0168-0102(02)00011-1
69. Venegas C, García JA, Escames G, Ortiz F, López A, Doerrier C, García-Corzo L, López LC, Reiter RJ, Acuña-Castroviejo D (2012) Extrapineal melatonin: analysis of its subcellular distribution and daily fluctuations. J Pineal Res 52:217–227. doi:10.1111/j.1600-079X.2011.00931.x
70. Wang FW, Wang Z, Zhang YM, Du ZX, Zhang XL, Liu Q, Guo YJ, Li XG, Hao AJ (2013) Protective effect of melatonin on bone marrow mesenchymal stem cells against hydrogen peroxide-induced apoptosis in vitro. J Cell Biochem 114:2346–2355. doi:10.1002/jcb.24582
71. Wang X (2009) The antiapoptotic activity of melatonin in neurodegenerative diseases. CNS Neurosci Ther 15:345–357. doi:10.1111/j.1755-5949.2009.00105.x
72. Weyer A, Schilling K (2003) Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J Neurosci Res 73:400–409. doi:10.1002/jnr.10655
73. Williams A, Piaton G, Lubetzki C (2007) Astrocytes-friends or foes in multiple sclerosis? Glia 55:1300–1312. doi:10.1002/glia.20546
74. Williams LM, Hannah LT, Bassett JM (1999) Melatonin receptors in neonatal pig brain and pituitary gland. J Pineal Res 26:43–49. doi:10.1111/j.1600-079X.1999.tb00565.x
75. Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Wiestler OD, Blümcke I (1996) NeuN: a useful neuronal marker for diagnostic histopathology. J Histochem Cytochem 44:1167–1171. doi:10.1177/44.10.8813082