Exposure to lead in the pre- and neonatal periods may result in brain inflammation

Karina Chibowska, Dariusz Chlubek, Irena Baranowska-Bosiacka

Abstract


One of the proinflammatory agents in the human body is lead (Pb), which can enter the blood through the skin, respiratory tract and digestive tract, causing poisoning. Its most significant target is the central nervous system (CNS). Although studies on Pb neurotoxicity have been conducted for many years, the proinflammatory effect of Pb on the brain is rarely reported in contrast to other human tissues and organs. Lead neurotoxicity has been defined as a significant paediatric health problem as the foetal stage is a very susceptible period for Pb exposure at whole blood levels below 10 µg/dL (Pb neurotoxicity threshold in children). However, the mechanisms of the neurotoxic action of Pb in causing brain defects remain unclear. In this review we discuss the role of the blood-brain barrier in the neurotoxicity of Pb, and the role of cytokines as inflammatory mediators (specially interleukin-1 and interleukin-6, nuclear transcription factor κB, cyclooxygenase-1 and cyclooxygenase-2, prostaglandin E2, transforming growth factor β. We also discuss the influence of pre- and neonatal exposure to Pb on inflammatory reactions in the brain.


Keywords


lead; inflammation; cytokines; cyclooxygenases (COX); prostaglandin E2 (PGE2); transforming growth factor beta (TGF-β)

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References


Brough D, Rothwell NJ, Allan SM. Interleukin-1 as a pharmacological target in acute brain injury. Exp Physiol 2015;100(12):1488-94. doi: 10.1113/EP085135.

Rock KL, Latz E, Ontiveros F, Kono H. The sterile inflammatory response. Annu Rev Immunol 2010;28:321-42. doi: 10.1146/annurev-immunol-030409-101311.

Li N, Liu X, Zhang P, Qiao M, Li H, Li X, et al. The effects of early life lead exposure on the expression of interleukin (IL) 1β, IL-6, and glial fibrillary acidic protein in the hippocampus of mouse pups. Hum Exp Toxicol 2015;34(4):357-63. doi: 10.1177/0960327114529451.

Liu MC, Liu XQ, Wang W, Shen XF, Che HL, Guo YY, et al. Involvement of microglia activation in the lead induced long-term potentiation impairment. PLoS One 2012;7(8):e43924. doi: 10.1371/journal.pone.0043924.

García-Lestón J, Roma-Torres J, Mayan O, Schroecksnadel S, Fuchs D, Moreira AO, et al. Assessment of immunotoxicity parameters in individuals occupationally exposed to lead. J Toxicol Environ Health A 2012;75(13-15):807-18. doi: 10.1080/15287394.2012.690327.

Suresh C, Dennis AO, Heinz J, Vemuri MC, Chetty CS. Melatonin protection against lead-induced changes in human neuroblastoma cell cultures. Int J Toxicol 2006;25(6):459-64. doi: 10.1080/10915810600959576.

Canfield RL, Henderson CR Jr, Cory-Slechta DA, Cox C, Jusko TA, Lanphear BP. Intellectual impairment in children with blood lead concentrations below 10 microg per deciliter. N Engl J Med 2003;348(16):1517-26. doi: 10.1056/NEJMoa022848.

Bunn TL, Parsons PJ, Kao E, Dietert RR. Exposure to lead during critical windows of embryonic development: differential immunotoxic outcome based on stage of exposure and gender. Toxicol Sci 2001;64(1):57-66. doi: 10.1093/toxsci/64.1.57.

Plusquellec P, Muckle G, Dewailly E, Ayotte P, Jacobson SW, Jacobson JL. The relation of low-level prenatal lead exposure to behavioral indicators of attention in Inuit infants in Arctic Quebec. Neurotoxicol Teratol 2007;29(5):527-37. doi: 10.1016/j.ntt.2007.07.002.

Baranowska-Bosiacka I, Gutowska I, Rybicka M, Nowacki P, Chlubek D. Neurotoxicity of lead. Hypothetical molecular mechanisms of synaptic function disorders. Neurol Neurochir Pol 2012;46(6):569-78.

Qian Y, Harris ED, Zheng Y, Tiffany-Castiglioni E. Lead targets GRP78, a molecular chaperone, in C6 rat glioma cells. Toxicol Appl Pharmacol 2000;163(3):260-6. doi: 10.1006/taap.1999.8878.

Stolp HB, Dziegielewska KM, Ek CJ, Habgood MD, Lane MA, Potter AM, et al. Breakdown of the blood-brain barrier to proteins in white matter of the developing brain following systemic inflammation. Cell Tissue Res 2005;320(3):369-78. doi: 10.1007/s00441-005-1088-6.

Stolp HB, Dziegielewska KM, Ek CJ, Potter AM, Saunders NR. Long-term changes in blood-brain barrier permeability and white matter following prolonged systemic inflammation in early development in the rat. Eur J Neurosci 2005;22(11):2805-16. doi: 10.1111/j.1460-9568.2005.04483.x.

Neuwelt E, Abbott NJ, Abrey L, Banks WA, Blakley B, Davis T, et al. Strategies to advance translational research into brain barriers. Lancet Neurol 2008;7(1):84-96. doi: 10.1016/S1474-4422(07)70326-5.

Nag S. Pathophysiology of blood-brain barrier breakdown. Methods Mol Med 2003;89:97-119. doi: 10.1385/1-59259-419-0:97.

Hu Y, Wang Z, Pan S, Zhang H, Fang M, Jiang H, et al. Melatonin protects against blood-brain barrier damage by inhibiting the TLR4/NF-κB signaling pathway after LPS treatment in neonatal rats. Oncotarget 2017;8(19):31638-54. doi: 10.18632/oncotarget.15780.

Zendedel A, Mönnink F, Hassanzadeh G, Zaminy A, Ansar MM, Habib P, et al. Estrogen attenuates local inflammasome expression and activation after spinal cord injury. Mol Neurobiol 2018;55(2):1364-75. doi: 10.1007/s12035-017-0400-2.

Walsh JG, Muruve DA, Power C. Inflammasomes in the CNS. Nat Rev Neurosci 2014;15(2):84-97. doi: 10.1038/nrn3638.

Lin C, Chao H, Li Z, Xu X, Liu Y, Bao Z, et al. Omega-3 fatty acids regulate NLRP3 inflammasome activation and prevent behavior deficits after traumatic brain injury. Exp Neurol 2017;290:115-22. doi: 10.1016/j.expneurol.2017.01.005.

Zendedel A, Johann S, Mehrabi S, Joghataei MT, Hassanzadeh G, Kipp M, et al. Activation and regulation of NLRP3 inflammasome by intrathecal application of SDF-1a in a spinal cord injury model. Mol Neurobiol 2016;53(5):3063-75. doi: 10.1007/s12035-015-9203-5.

Gensel JC, Zhang B. Macrophage activation and its role in repair and pathology after spinal cord injury. Brain Res 2015;1619:1-11. doi: 10.1016/j.brainres.2014.12.045.

Naruse M, Shibasaki K, Yokoyama S, Kurachi M, Ishizaki Y. Dynamic changes of CD44 expression from progenitors to subpopulations of astrocytes and neurons in developing cerebellum. PLoS One 2013;8(1):e53109. doi: 10.1371/journal.pone.0053109.

Bernal GM, Peterson DA. Phenotypic and gene expression modification with normal brain aging in GFAP-positive astrocytes and neural stem cells. Aging Cell 2011;10(3):466-82. doi: 10.1111/j.1474-9726.2011.00694.x.

Karimi-Abdolrezaee S, Billakanti R. Reactive astrogliosis after spinal cord injury-beneficial and detrimental effects. Mol Neurobiol 2012;46(2):251-64. doi: 10.1007/s12035-012-8287-4.

Back SA. Brain injury in the preterm infant: new horizons for pathogenesis and prevention. Pediatr Neurol 2015;53(3):185-92. doi: 10.1016/j.pediatrneurol.2015.04.006.

Back SA, Rosenberg PA. Pathophysiology of glia in perinatal white matter injury. Glia 2014;62(11):1790-815. doi: 10.1002/glia.22658.

Khwaja O, Volpe JJ. Pathogenesis of cerebral white matter injury of prematurity. Arch Dis Child Fetal Neonatal Ed 2008;93(2):F153-61. doi: 10.1136/adc.2006.108837.

Sofroniew MV. Astrogliosis. Cold Spring Harb Perspect Biol 2015;7(2):a020420. doi: 10.1101/cshperspect.a020420.

Williams A, Piaton G, Lubetzki C. Astrocytes – friends or foes in multiple sclerosis? Glia 2007;55(13):1300-12. doi: 10.1002/glia.20546.

Liddelow SA, Guttenplan KA, Clarke LE, Bennett FC, Bohlen CJ, Schirmer L, et al. Neurotoxic reactive astrocytes are induced by activated microglia. Nature 2017;541(7638):481-7. doi: 10.1038/nature21029.

Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG, et al. Genomic analysis of reactive astrogliosis. J Neurosci 2012;32(18):6391-410. doi: 10.1523/JNEUROSCI.6221-11.2012.

Dinarello CA, Ikejima T, Warner SJ, Orencole SF, Lonnemann G, Cannon JG, et al. Interleukin 1 induces interleukin 1. I. Induction of circulating interleukin 1 in rabbits in vivo and in human mononuclear cells in vitro. J Immunol 1987;139(6):1902-10.

McColl BW, Rothwell NJ, Allan SM. Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1- and neutrophil-dependent mechanisms. J Neurosci 2007;27(16):4403-12. doi: 10.1523/JNEUROSCI.5376-06.2007.

McColl BW, Rothwell NJ, Allan SM. Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J Neurosci 2008;28(38):9451-62. doi: 10.1523/JNEUROSCI.2674-08.2008.

Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, et al. Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 2003;23(25):8692-700.

Thornton P, Pinteaux E, Gibson RM, Allan SM, Rothwell NJ. Interleukin-1-induced neurotoxicity is mediated by glia and requires caspase activation and free radical release. J Neurochem 2006;98(1):258-66. doi: 10.1111/j.1471-4159.2006.03872.x.

Latz E, Xiao TS, Stutz A. Activation and regulation of the inflammasomes. Nat Rev Immunol 2013;13(6):397-411. doi: 10.1038/nri3452.

Gustin A, Kirchmeyer M, Koncina E, Felten P, Losciuto S, Heurtaux T, et al. NLRP3 inflammasome is expressed and functional in mouse brain microglia but not in astrocytes. PLoS One 2015;10(6):e0130624. doi: 10.1371/journal.pone.0130624.

de Rivero Vaccari JP, Lotocki G, Alonso OF, Bramlett HM, Dietrich WD, Keane RW. Therapeutic neutralization of the NLRP1 inflammasome reduces the innate immune response and improves histopathology after traumatic brain injury. J Cereb Blood Flow Metab 2009;29(7):1251-61. doi: 10.1038/jcbfm.2009.46.

Mortezaee K, Khanlarkhani N, Beyer C, Zendedel A. Inflammasome: Its role in traumatic brain and spinal cord injury. J Cell Physiol 2018;233(7):5160-9. doi: 10.1002/jcp.26287.

Holmin S, Mathiesen T. Intracerebral administration of interleukin-1beta and induction of inflammation, apoptosis, and vasogenic edema. J Neurosurg 2000;92(1):108-20. doi: 10.3171/jns.2000.92.1.0108.

de Rivero Vaccari JP, Lotocki G, Marcillo AE, Dietrich WD, Keane RW. A molecular platform in neurons regulates inflammation after spinal cord injury. J Neurosci 2008;28(13):3404-14. doi: 10.1523/JNEUROSCI.0157-08.2008.

Clausen F, Hånell A, Björk M, Hillered L, Mir AK, Gram H, et al. Neutralization of interleukin-1beta modifies the inflammatory response and improves histological and cognitive outcome following traumatic brain injury in mice. Eur J Neurosci 2009;30(3):385-96. doi: 10.1111/j.1460-9568.2009.06820.x.

Kim B, Lee Y, Kim E, Kwak A, Ryoo S, Bae SH, et al. The interleukin-1α precursor is biologically active and is likely a key alarmin in the IL-1 family of cytokines. Front Immunol 2013;4:391. doi: 10.3389/fimmu.2013.00391.

Afonina IS, Tynan GA, Logue SE, Cullen SP, Bots M, Lüthi AU, et al. Granzyme B-dependent proteolysis acts as a switch to enhance the proinflammatory activity of IL-1α. Mol Cell 2011;44(2):265-78. doi: 10.1016/j.molcel.2011.07.037.

Zheng Y, Humphry M, Maguire JJ, Bennett MR, Clarke MC. Intracellular interleukin-1 receptor 2 binding prevents cleavage and activity of interleukin-1α, controlling necrosis-induced sterile inflammation. Immunity 2013;38(2):285-95. doi: 10.1016/j.immuni.2013.01.008.

Gross O, Yazdi AS, Thomas CJ, Masin M, Heinz LX, Guarda G, et al. Inflammasome activators induce interleukin-1α secretion via distinct pathways with differential requirement for the protease function of caspase-1. Immunity 2012;36(3):388-400. doi: 10.1016/j.immuni.2012.01.018.

England H, Summersgill HR, Edye ME, Rothwell NJ, Brough D. Release of interleukin-1α or interleukin-1β depends on mechanism of cell death. J Biol Chem 2014;289(23):15942-50. doi: 10.1074/jbc.M114.557561.

Pasparakis M, Vandenabeele P. Necroptosis and its role in inflammation. Nature 2015;517(7534):311-20. doi: 10.1038/nature14191.

Luheshi NM, Kovács KJ, Lopez-Castejon G, Brough D, Denes A. Interleukin-1α expression precedes IL-1β after ischemic brain injury and is localised to areas of focal neuronal loss and penumbral tissues. J Neuroinflammation 2011;8:186. doi: 10.1186/1742-2094-8-186.

Greenhalgh AD, Brough D, Robinson EM, Girard S, Rothwell NJ, Allan SM. Interleukin-1 receptor antagonist is beneficial after subarachnoid haemorrhage in rat by blocking haem-driven inflammatory pathology. Dis Model Mech 2012;5(6):823-33. doi: 10.1242/dmm.008557.

Boutin H, LeFeuvre RA, Horai R, Asano M, Iwakura Y, Rothwell NJ. Role of IL-1alpha and IL-1beta in ischemic brain damage. J Neurosci 2001;21(15):5528-34.

Giles JA, Greenhalgh AD, Davies CL, Denes A, Shaw T, Coutts G, et al. Requirement for interleukin-1 to drive brain inflammation reveals tissue-specific mechanisms of innate immunity. Eur J Immunol 2015;45(2):525-30. doi: 10.1002/eji.201444748.

Allen C, Thornton P, Denes A, McColl BW, Pierozynski A, Monestier M, et al. Neutrophil cerebrovascular transmigration triggers rapid neurotoxicity through release of proteases associated with decondensed DNA. J Immunol 2012;189(1):381-92. doi: 10.4049/jimmunol.1200409.

Pradillo JM, Denes A, Greenhalgh AD, Boutin H, Drake C, McColl BW, et al. Delayed administration of interleukin-1 receptor antagonist reduces ischemic brain damage and inflammation in comorbid rats. J Cereb Blood Flow Metab 2012;32(9):1810-9. doi: 10.1038/jcbfm.2012.101.

Relton JK, Rothwell NJ. Interleukin-1 receptor antagonist inhibits ischaemic and excitotoxic neuronal damage in the rat. Brain Res Bull 1992;29(2):243-6. doi: 10.1016/0361-9230(92)90033-t.

Mulcahy NJ, Ross J, Rothwell NJ, Loddick SA. Delayed administration of interleukin-1 receptor antagonist protects against transient cerebral ischaemia in the rat. Br J Pharmacol 2003;140(3):471-6. doi: 10.1038/sj.bjp.0705462.

Greenhalgh AD, Galea J, Dénes A, Tyrrell PJ, Rothwell NJ. Rapid brain penetration of interleukin-1 receptor antagonist in rat cerebral ischaemia: pharmacokinetics, distribution, protection. Br J Pharmacol 2010;160(1):153-9. doi: 10.1111/j.1476-5381.2010.00684.x.

Girard S, Murray KN, Rothwell NJ, Metz GA, Allan SM. Long-term functional recovery and compensation after cerebral ischemia in rats. Behav Brain Res 2014;270:18-28. doi: 10.1016/j.bbr.2014.05.008.

Galea J, Ogungbenro K, Hulme S, Greenhalgh A, Aarons L, Scarth S, et al. Intravenous anakinra can achieve experimentally effective concentrations in the central nervous system within a therapeutic time window: results of a dose-ranging study. J Cereb Blood Flow Metab 2011;31(2):439-47. doi: 10.1038/jcbfm.2010.103.

Schielke GP, Yang GY, Shivers BD, Betz AL. Reduced ischemic brain injury in interleukin-1 beta converting enzyme-deficient mice. J Cereb Blood Flow Metab 1998;18(2):180-5. doi: 10.1097/00004647-199802000-00009.

Ross J, Brough D, Gibson RM, Loddick SA, Rothwell NJ. A selective, non-peptide caspase-1 inhibitor, VRT-018858, markedly reduces brain damage induced by transient ischemia in the rat. Neuropharmacology 2007;53(5):638-42. doi: 10.1016/j.neuropharm.2007.07.015.

Emsley HC, Smith CJ, Georgiou RF, Vail A, Hopkins SJ, Rothwell NJ, et al. A randomised phase II study of interleukin-1 receptor antagonist in acute stroke patients. J Neurol Neurosurg Psychiatry 2005;76(10):1366-72. doi: 10.1136/jnnp.2004.054882.

Denes A, Wilkinson F, Bigger B, Chu M, Rothwell NJ, Allan SM. Central and haematopoietic interleukin-1 both contribute to ischaemic brain injury in mice. Dis Model Mech 2013;6(4):1043-8. doi: 10.1242/dmm.011601.

Spooren A, Kolmus K, Laureys G, Clinckers R, De Keyser J, Haegeman G, et al. Interleukin-6, a mental cytokine. Brain Res Rev 2011;67(1-2):157-83. doi: 10.1016/j.brainresrev.2011.01.002.

Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta 2011;1813(5):878-88. doi: 10.1016/j.bbamcr.2011.01.034.

Campbell IL, Erta M, Lim SL, Frausto R, May U, Rose-John S, et al. Trans-signaling is a dominant mechanism for the pathogenic actions of interleukin-6 in the brain. J Neurosci 2014;34(7):2503-13. doi: 10.1523/JNEUROSCI.2830-13.2014.

Lust JA, Donovan KA, Kline MP, Greipp PR, Kyle RA, Maihle NJ. Isolation of an mRNA encoding a soluble form of the human interleukin-6 receptor. Cytokine 1992;4(2):96-100. doi: 10.1016/1043-4666(92)90043-q.

Müllberg J, Schooltink H, Stoyan T, Günther M, Graeve L, Buse G, et al. The soluble interleukin-6 receptor is generated by shedding. Eur J Immunol 1993;23(2):473-80. doi: 10.1002/eji.1830230226.

Müllberg J, Vollmer P, Althoff K, März P, Rose-John S. Generation and function of the soluble interleukin-6 receptor. Biochem Soc Trans 1999;27(2):211-9. doi: 10.1042/bst0270211.

Rose-John S, Heinrich PC. Soluble receptors for cytokines and growth factors: generation and biological function. Biochem J 1994;300(Pt 2):281-90. doi: 10.1042/bj3000281.

Mackiewicz A, Schooltink H, Heinrich PC, Rose-John S. Complex of soluble human IL-6-receptor/IL-6 up-regulates expression of acute-phase proteins. J Immunol 1992;149(6):2021-7.

Narazaki M, Yasukawa K, Saito T, Ohsugi Y, Fukui H, Koishihara Y, et al. Soluble forms of the interleukin-6 signal-transducing receptor component gp130 in human serum possessing a potential to inhibit signals through membrane-anchored gp130. Blood 1993;82(4):1120-6.

Jostock T, Müllberg J, Ozbek S, Atreya R, Blinn G, Voltz N, et al. Soluble gp130 is the natural inhibitor of soluble interleukin-6 receptor transsignaling responses. Eur J Biochem 2001;268(1):160-7. doi: 10.1046/j.1432-1327.2001.01867.x.

Rabe B, Chalaris A, May U, Waetzig GH, Seegert D, Williams AS, et al. Transgenic blockade of interleukin 6 transsignaling abrogates inflammation. Blood 2008;111(3):1021-8. doi: 10.1182/blood-2007-07-102137.

Rose-John S, Scheller J, Elson G, Jones SA. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol 2006;80(2):227-36. doi: 10.1189/jlb.1105674.

März P, Herget T, Lang E, Otten U, Rose-John S. Activation of gp130 by IL-6/soluble IL-6 receptor induces neuronal differentiation. Eur J Neurosci 1997;9(12):2765-73. doi: 10.1111/j.1460-9568.1997.tb01705.x.

Van Wagoner NJ, Oh JW, Repovic P, Benveniste EN. Interleukin-6 (IL-6) production by astrocytes: autocrine regulation by IL-6 and the soluble IL-6 receptor. J Neurosci 1999;19(13):5236-44.

März P, Heese K, Dimitriades-Schmutz B, Rose-John S, Otten U. Role of interleukin-6 and soluble IL-6 receptor in region-specific induction of astrocytic differentiation and neurotrophin expression. Glia 1999;26(3):191-200.

Lin HW, Levison SW. Context-dependent IL-6 potentiation of interferon- gamma-induced IL-12 secretion and CD40 expression in murine microglia. J Neurochem 2009;111(3):808-18. doi: 10.1111/j.1471-4159.2009.06366.x.

Burton MD, Sparkman NL, Johnson RW. Inhibition of interleukin-6 trans-signaling in the brain facilitates recovery from lipopolysaccharide-induced sickness behavior. J Neuroinflammation 2011;8:54. doi: 10.1186/1742-2094-8-54.

Burton MD, Rytych JL, Freund GG, Johnson RW. Central inhibition of interleukin-6 trans-signaling during peripheral infection reduced neuroinflammation and sickness in aged mice. Brain Behav Immun 2013;30:66-72. doi: 10.1016/j.bbi.2013.01.002.

Li XQ, Lv HW, Tan WF, Fang B, Wang H, Ma H. Role of the TLR4 pathway in blood-spinal cord barrier dysfunction during the bimodal stage after ischemia/reperfusion injury in rats. J Neuroinflammation 2014;11:62. doi: 10.1186/1742-2094-11-62.

Wang X, Stridh L, Li W, Dean J, Elmgren A, Gan L, et al. Lipopolysaccharide sensitizes neonatal hypoxic-ischemic brain injury in a MyD88-dependent manner. J Immunol 2009;183(11):7471-7. doi: 10.4049/jimmunol.0900762.

Minghetti L. Cyclooxygenase-2 (COX-2) in inflammatory and degenerative brain diseases. J Neuropathol Exp Neurol 2004;63(9):901-10. doi: 10.1093/jnen/63.9.901.

Smith WL, Garavito RM, DeWitt DL. Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J Biol Chem 1996;271(52):33157-60. doi: 10.1074/jbc.271.52.33157.

Hinz B, Brune K. Cyclooxygenase-2 – 10 years later. J Pharmacol Exp Ther 2002;300(2):367-75. doi: 10.1124/jpet.300.2.367.

Kurumbail RG, Stevens AM, Gierse JK, McDonald JJ, Stegeman RA, Pak JY, et al. Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature 1996;384(6610):644-8. doi: 10.1038/384644a0.

Yamagata K, Andreasson KI, Kaufmann WE, Barnes CA, Worley PF. Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 1993;11(2):371-86. doi: 10.1016/0896-6273(93)90192-t.

Breder CD, Dewitt D, Kraig RP. Characterization of inducible cyclooxygenase in rat brain. J Comp Neurol 1995;355(2):296-315. doi: 10.1002/cne.903550208.

Minghetti L, Levi G. Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide. Prog Neurobiol 1998;54(1):99-125. doi: 10.1016/s0301-0082(97)00052-x.

O’Banion MK. Cyclooxygenase-2: molecular biology, pharmacology, and neurobiology. Crit Rev Neurobiol 1999;13(1):45-82.

Teather LA, Packard MG, Bazan NG. Post-training cyclooxygenase-2 (COX-2) inhibition impairs memory consolidation. Learn Mem 2002;9(1):41-7. doi: 10.1101/lm.43602.

Shiow LR, Favrais G, Schirmer L, Schang AL, Cipriani S, Andres C, et al. Reactive astrocyte COX2-PGE2 production inhibits oligodendrocyte maturation in neonatal white matter injury. Glia 2017;65(12):2024-37. doi: 10.1002/glia.23212.

Legler DF, Bruckner M, Uetz-von Allmen E, Krause P. Prostaglandin E2 at new glance: novel insights in functional diversity offer therapeutic chances. Int J Biochem Cell Biol 2010;42(2):198-201. doi: 10.1016/j.biocel.2009.09.015.

Molina-Holgado E, Ortiz S, Molina-Holgado F, Guaza C. Induction of COX-2 and PGE(2) biosynthesis by IL-1beta is mediated by PKC and mitogen-activated protein kinases in murine astrocytes. Br J Pharmacol 2000;131(1):152-9. doi: 10.1038/sj.bjp.0703557.

Xia Q, Hu Q, Wang H, Yang H, Gao F, Ren H, et al. Induction of COX-2-PGE2 synthesis by activation of the MAPK/ERK pathway contributes to neuronal death triggered by TDP-43-depleted microglia. Cell Death Dis 2015;6(3):e1702. doi: 10.1038/cddis.2015.69.

Xu J, Chalimoniuk M, Shu Y, Simonyi A, Sun AY, Gonzalez FA, et al. Prostaglandin E2 production in astrocytes: regulation by cytokines, extracellular ATP, and oxidative agents. Prostaglandins Leukot Essent Fatty Acids 2003;69(6):437-48. doi: 10.1016/j.plefa.2003.08.016.

Qi Y, Cai J, Wu Y, Wu R, Lee J, Fu H, et al. Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor. Development 2001;128(14):2723-33.

Sharma K, Schmitt S, Bergner CG, Tyanova S, Kannaiyan N, Manrique-Hoyos N, et al. Cell type- and brain region-resolved mouse brain proteome. Nat Neurosci 2015;18(12):1819-31. doi: 10.1038/nn.4160.

Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O’Keeffe S, et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 2014;34(36):11929-47. doi: 10.1523/JNEUROSCI.1860-14.2014.

Watanabe K, Kawamori T, Nakatsugi S, Ohta T, Ohuchida S, Yamamoto H, et al. Role of the prostaglandin E receptor subtype EP1 in colon carcino genesis. Cancer Res 1999;59(20):5093-6.

Hallinan EA, Hagen TJ, Husa RK, Tsymbalov S, Rao SN, vanHoeck JP, et al. N-substituted dibenzoxazepines as analgesic PGE2 antagonists. J Med Chem 1993;36(22):3293-9. doi: 10.1021/jm00074a010.

Bazan NG. Synaptic lipid signaling: significance of polyunsaturated fatty acids and platelet-activating factor. J Lipid Res 2003;44(12):2221-33. doi: 10.1194/jlr.R300013-JLR200.

Niwa K, Araki E, Morham SG, Ross ME, Iadecola C. Cyclooxygenase-2 contributes to functional hyperemia in whisker-barrel cortex. J Neurosci 2000;20(2):763-70.

Diniz LP, Matias I, Siqueira M, Stipursky J, Gomes FCA. Astrocytes and the TGF-β1 pathway in the healthy and diseased brain: a double-edged sword. Mol Neurobiol 2019;56(7):4653-79. doi: 10.1007/s12035-018-1396-y.

Weiss A, Attisano L. The TGFbeta superfamily signaling pathway. Wiley Interdiscip Rev Dev Biol 2013;2(1):47-63. doi: 10.1002/wdev.86.

de Caestecker M. The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev 2004;15(1):1-11.

Gantus MA, Alves LM, Stipursky J, Souza EC, Teodoro AJ, Alves TR, et al. Estradiol modulates TGF-β1 expression and its signaling pathway in thyroid stromal cells. Mol Cell Endocrinol 2011;337(1-2):71-9. doi: 10.1016/j.mce.2011.02.001.

Massagué J, Gomis RR. The logic of TGFbeta signaling. FEBS Lett 2006;580(12):2811-20. doi: 10.1016/j.febslet.2006.04.033.

Tinoco-Veras CM, Santos AAQA, Stipursky J, Meloni M, Araujo APB, Foschetti DA, et al. Transforming growth factor β1/SMAD signaling pathway activation protects the intestinal epithelium from Clostridium difficile toxin A-induced damage. Infect Immun 2017;85(10). pii: e00430-17. doi: 10.1128/IAI.00430-17.

Robertson IB, Horiguchi M, Zilberberg L, Dabovic B, Hadjiolova K, Rifkin DB. Latent TGF-β-binding proteins. Matrix Biol 2015;47:44-53. doi: 10.1016/j.matbio.2015.05.005.

Munger JS, Harpel JG, Gleizes PE, Mazzieri R, Nunes I, Rifkin DB. Latent transforming growth factor-beta: structural features and mechanisms of activation. Kidney Int 1997;51(5):1376-82. doi: 10.1038/ki.1997.188.

Guo X, Wang XF. Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res 2009;19(1):71-88. doi: 10.1038/cr.2008.302.

Romão LF, Sousa Vde O, Neto VM, Gomes FC. Glutamate activates GFAP gene promoter from cultured astrocytes through TGF-beta1 pathways. J Neurochem 2008;106(2):746-56. doi: 10.1111/j.1471-4159.2008.05428.x.

Stipursky J, Francis D, Gomes FC. Activation of MAPK/PI3K/SMAD pathways by TGF-β(1) controls differentiation of radial glia into astrocytes in vitro. Dev Neurosci 2012;34(1):68-81. doi: 10.1159/000338108.

Javelaud D, Mauviel A. Crosstalk mechanisms between the mitogen-activated protein kinase pathways and Smad signaling downstream of TGF-beta: implications for carcinogenesis. Oncogene 2005;24(37):5742-50. doi: 10.1038/sj.onc.1208928.

Miller MW. Expression of transforming growth factor-beta in developing rat cerebral cortex: effects of prenatal exposure to ethanol. J Comp Neurol 2003;460(3):410-24. doi: 10.1002/cne.10658.

Stipursky J, Francis D, Dezonne RS, Bérgamo de Araújo AP, Souza L, Moraes CA, et al. TGF-β1 promotes cerebral cortex radial glia-astrocyte differentiation in vivo. Front Cell Neurosci 2014;8:393. doi: 10.3389/fncel.2014.00393.

Mecha M, Rabadán MA, Peña-Melián A, Valencia M, Mondéjar T, Blanco MJ. Expression of TGF-betas in the embryonic nervous system: analysis of interbalance between isoforms. Dev Dyn 2008;237(6):1709-17. doi: 10.1002/dvdy.21558.

Galter D, Böttner M, Unsicker K. Developmental regulation of the serotonergic transmitter phenotype in rostral and caudal raphe neurons by transforming growth factor-betas. J Neurosci Res 1999;56(5):531-8. doi: 10.1002/(SICI)1097-4547(19990601)56:5<531::AID-JNR8>3.0.CO;2-O.

Böttner M, Krieglstein K, Unsicker K. The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions. J Neurochem 2000;75(6):2227-40. doi: 10.1046/j.1471-4159.2000.0752227.x.

Böttner M, Unsicker K, Suter-Crazzolara C. Expression of TGF-beta type II receptor mRNA in the CNS. Neuroreport 1996;7(18):2903-7. doi: 10.1097/00001756-199611250-00019.

Tomoda T, Shirasawa T, Yahagi YI, Ishii K, Takagi H, Furiya Y, et al. Transforming growth factor-beta is a survival factor for neonate cortical neurons: coincident expression of type I receptors in developing cerebral cortices. Dev Biol 1996;179(1):79-90. doi: 10.1006/dbio.1996.0242.

Vivien D, Bernaudin M, Buisson A, Divoux D, MacKenzie ET, Nouvelot A. Evidence of type I and type II transforming growth factor-beta receptors in central nervous tissues: changes induced by focal cerebral ischemia. J Neurochem 1998;70(6):2296-304. doi: 10.1046/j.1471-4159.1998.70062296.x.

Diniz LP, Almeida JC, Tortelli V, Vargas Lopes C, Setti-Perdigão P, Stipursky J, et al. Astrocyte-induced synaptogenesis is mediated by transforming growth factor β signaling through modulation of D-serine levels in cerebral cortex neurons. J Biol Chem 2012;287(49):41432-45. doi: 10.1074/jbc.M112.380824.

Sousa Vde O, Romão L, Neto VM, Gomes FC. Glial fibrillary acidic protein gene promoter is differently modulated by transforming growth factor-beta 1 in astrocytes from distinct brain regions. Eur J Neurosci 2004;19(7):1721-30. doi: 10.1111/j.1460-9568.2004.03249.x.

Siqueira M, Francis D, Gisbert D, Gomes FCA, Stipursky J. Radial glia cells control angiogenesis in the developing cerebral cortex through TGF-β1 signaling. Mol Neurobiol 2018;55(5):3660-75. doi: 10.1007/s12035-017-0557-8.

de Sampaio e Spohr TC, Martinez R, da Silva EF, Neto VM, Gomes FC. Neuro-glia interaction effects on GFAP gene: a novel role for transforming growth factor-beta1. Eur J Neurosci 2002;16(11):2059-69. doi: 10.1046/j.1460-9568.2002.02283.x.

Ageta H, Murayama A, Migishima R, Kida S, Tsuchida K, Yokoyama M, et al. Activin in the brain modulates anxiety-related behavior and adult neurogenesis. PLoS One 2008;3(4):e1869. doi: 10.1371/journal.pone.0001869.

Espósito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, et al. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 2005;25(44):10074-86. doi: 10.1523/JNEUROSCI.3114-05.2005.

Brionne TC, Tesseur I, Masliah E, Wyss-Coray T. Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron 2003;40(6):1133-45. doi: 10.1016/s0896-6273(03)00766-9.

Colak D, Mori T, Brill MS, Pfeifer A, Falk S, Deng C, et al. Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci 2008;28(2):434-46. doi: 10.1523/JNEUROSCI.4374-07.2008.

Diniz LP, Matias IC, Garcia MN, Gomes FC. Astrocytic control of neural circuit formation: highlights on TGF-beta signaling. Neurochem Int 2014;78:18-27. doi: 10.1016/j.neuint.2014.07.008.

Diniz LP, Tortelli V, Garcia MN, Araújo AP, Melo HM, Silva GS, et al. Astrocyte transforming growth factor beta 1 promotes inhibitory synapse formation via CaM kinase II signaling. Glia 2014;62(12):1917-31. doi: 10.1002/glia.22713.

Yi JJ, Barnes AP, Hand R, Polleux F, Ehlers MD. TGF-beta signaling specifies axons during brain development. Cell 2010;142(1):144-57. doi: 10.1016/j.cell.2010.06.010.

Stipursky J, Gomes FC. TGF-beta1/SMAD signaling induces astrocyte fate commitment in vitro: implications for radial glia development. Glia 2007;55(10):1023-33. doi: 10.1002/glia.20522.

Hellbach N, Weise SC, Vezzali R, Wahane SD, Heidrich S, Roidl D, et al. Neural deletion of Tgfbr2 impairs angiogenesis through an altered secretome. Hum Mol Genet 2014;23(23):6177-90. doi: 10.1093/hmg/ddu338.

Hirota S, Clements TP, Tang LK, Morales JE, Lee HS, Oh SP, et al. Neuropilin 1 balances β8 integrin-activated TGFβ signaling to control sprouting angiogenesis in the brain. Development 2015;142(24):4363-73. doi: 10.1242/dev.113746.

Kasten-Jolly J, Heo Y, Lawrence DA. Central nervous system cytokine gene expression: modulation by lead. J Biochem Mol Toxicol 2011;25(1):41-54. doi: 10.1002/jbt.20358.

Gruol DL, Nelson TE. Physiological and pathological roles of interleukin-6 in the central nervous system. Mol Neurobiol 1997;15(3):307-39. doi: 10.1007/BF02740665.

Van Wagoner NJ, Benveniste EN. Interleukin-6 expression and regulation in astrocytes. J Neuroimmunol 1999;100(1-2):124-39. doi: 10.1016/s0165-5728(99)00187-3.

Wyss-Coray T, Borrow P, Brooker MJ, Mucke L. Astroglial overproduction of TGF-beta 1 enhances inflammatory central nervous system disease in transgenic mice. J Neuroimmunol 1997;77(1):45-50. doi: 10.1016/s0165-5728(97)00049-0.

Wei J, Du K, Cai Q, Ma L, Jiao Z, Tan J, et al. Lead induces COX-2 expression in glial cells in a NFAT-dependent, AP-1/NFκB-independent manner. Toxicology 2014;325:67-73. doi: 10.1016/j.tox.2014.08.012.

Ding J, Li J, Xue C, Wu K, Ouyang W, Zhang D, et al. Cyclooxygenase-2 induction by arsenite is through a nuclear factor of activated T-cell-dependent pathway and plays an antiapoptotic role in Beas-2B cells. J Biol Chem 2006;281(34):24405-13. doi: 10.1074/jbc.M600751200.

Zhang D, Li J, Wu K, Ouyang W, Ding J, Liu ZG, et al. JNK1, but not JNK2, is required for COX-2 induction by nickel compounds. Carcinogenesis 2007;28(4):883-91. doi: 10.1093/carcin/bgl186.

Cai T, Li X, Ding J, Luo W, Li J, Huang C. A cross-talk between NFAT and NF-κB pathways is crucial for nickel-induced COX-2 expression in Beas-2B cells. Curr Cancer Drug Targets 2011;11(5):548-59. doi: 10.2174/156800911795656001.

Ouyang W, Zhang D, Ma Q, Li J, Huang C. Cyclooxygenase-2 induction by arsenite through the IKKbeta/NFkappaB pathway exerts an antiapoptotic effect in mouse epidermal Cl41 cells. Environ Health Perspect 2007;115(4):513-8. doi: 10.1289/ehp.9588.

Zuo Z, Ouyang W, Li J, Costa M, Huang C. Cyclooxygenase-2 (COX-2) mediates arsenite inhibition of UVB-induced cellular apoptosis in mouse epidermal Cl41 cells. Curr Cancer Drug Targets 2012;12(6):607-16. doi: 10.2174/156800912801784802.

Strużyńska L, Dąbrowska-Bouta B, Koza K, Sulkowski G. Inflammation-like glial response in lead-exposed immature rat brain. Toxicol Sci 2007;95(1):156-62. doi: 10.1093/toxsci/kfl134.




DOI: https://doi.org/10.21164/pomjlifesci.622

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