Interleukin-10 overexpression does not synergize with the neuroprotective action of RGD-containing vectors after postnatal brain excitotoxicity but modulates the main inflammatory cell responses

Journal of Neuroscience Research

Volumn 90, Issue 1, 2012, Pages 143-159

  Gonzalez, Pau ^a,b   Peluffo, Hugo ^c   Acarin, Laia ^a   Villaverde, Antonio ^a,d   Gonzalez, Berta ^a   Castellano, Bernardo ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b Biomechanics and Technical support   (Spain)

^c DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^d BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

Author keywords

Brain; Excitotoxicity; Gene therapy; IL 10; Postnatal

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; BACTERIAL VECTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; N METHYL DEXTRO ASPARTIC ACID; TUMOR NECROSIS FACTOR ALPHA; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXCITOTOXICITY; FEMALE; MALE; MICROGLIA; NERVE CELL; NERVE DEGENERATION; NEUROPROTECTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SURVIVAL TIME; TRANSGENE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD11B; CELL DEATH; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION; GENETIC VECTORS; GLIAL FIBRILLARY ACIDIC PROTEIN; HISTIDINE; INTERLEUKIN-10; MACROPHAGES; MALE; N-METHYLASPARTATE; NEUROGLIA; NEUROPROTECTIVE AGENTS; NEUROTOXICITY SYNDROMES; NEUTROPHILS; OLIGOPEPTIDES; ORGANIC CHEMICALS; PEROXIDASE; PLANT LECTINS; RATS; RATS, LONG-EVANS; TRANSDUCTION, GENETIC; VIMENTIN;

EID: 81255168189     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22741     Document Type: Article

References (103)

1. Abraham KE, McMillen D, Brewer KL. 2004. The effects of endogenous interleukin-10 on gray matter damage and the development of pain behaviors following excitotoxic spinal cord injury in the mouse. Neuroscience 124: 945-952.
2. Acarin L, Vela JM, Gonzalez B, Castellano B. 1994. Demonstration of poly-N-acetyl lactosamine residues in ameboid and ramified microglial cells in rat brain by tomato lectin binding. J Histochem Cytochem 42: 1033-1041.
3. Acarin L, Gonzalez B, Castellano B, Castro AJ. 1996. Microglial response to N-methyl-D-aspartate-mediated excitotoxicity in the immature rat brain. J Comp Neurol 367: 361-374.
4. Acarin L, Gonzalez B, Castellano B, Castro AJ. 1997. Quantitative analysis of microglial reaction to a cortical excitotoxic lesion in the early postnatal brain. Exp Neurol 147: 410-417.
5. Acarin L, Gonzalez B, Castro AJ, Castellano B. 1999a. Primary cortical glial reaction vs. secondary thalamic glial response in the excitotoxically injured young brain: microglial/macrophage response and major histocompatibility complex class I and II expression. Neuroscience 89: 549-565.
6. Acarin L, Gonzalez B, Hidalgo J, Castro AJ, Castellano B. 1999b. Primary cortical glial reaction vs. secondary thalamic glial response in the excitotoxically injured young brain: astroglial response and metallothionein expression. Neuroscience 92: 827-839.
7. Acarin L, Gonzalez B, Castellano B. 2000. Neuronal, astroglial and microglial cytokine expression after an excitotoxic lesion in the immature rat brain. Eur J Neurosci 12: 3505-3520.
8. Acarin L, Gonzalez B, Castellano B. 2001. Triflusal posttreatment inhibits glial nuclear factor-kappaB, downregulates the glial response, and is neuroprotective in an excitotoxic injury model in postnatal brain. Stroke 32: 2394-2402.
9. Acarin L, Peluffo H, Gonzalez B, Castellano B. 2002. Expression of inducible nitric oxide synthase and cyclooxygenase-2 after excitotoxic damage to the immature rat brain. J Neurosci Res 68: 745-754.
10. Agnello DVP, Ghezzi P. 2000. Increased tumor necrosis factor and interleukin-6 production in the central nervous system of interleukin-10-deficient mice. Brain Res 869: 241-243.
11. Allan SM, Rothwell NJ. 2001. Cytokines and acute neurodegeneration. Nat Rev Neurosci 2: 734-744.
12. +, hypotonic stress, and cortical spreading depression on astrocyte swelling in GFAP-deficient mice. Glia 35: 189-203.
13. Apelt J, Schliebs R. 2001. Beta-amyloid-induced glial expression of both pro-and anti-inflammatory cytokines in cerebral cortex of aged transgenic Tg2576 mice with Alzheimer plaque pathology. Brain Res 894: 21-30.
14. Aris A, Villaverde A. 2003. Engineering nuclear localization signals in modular protein vehicles for gene therapy. Biochem Biophys Res Commun 304: 625-631.
15. Arvin KL, Han BH, Du Y, Lin SZ, Paul SM, Holtzman DM. 2002. Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann Neurol 52: 54-61.
16. Balasingam V, Yong VW. 1996. Attenuation of astroglial reactivity by interleukin-10. J Neurosci 16: 2945-2955.
17. Balasingam V, Tejada-Berges T, Wright E, Bouckova R, Yong VW. 1994. Reactive astrogliosis in the neonatal mouse brain and its modulation by cytokines. J Neurosci 14: 846-856.
18. Benveniste EN, Tang LP, Law RM. 1995. Differential regulation of astrocyte TNF-alpha expression by the cytokines TGF-beta, IL-6 and IL-10. Int J Dev Neurosci 13: 341-349.
19. Breckwoldt MO, Chen JW, Stangenberg L, Aikawa E, Rodriguez E, Qiu S, Moskowitz MA, Weissleder R. 2008. Tracking the inflammatory response in stroke in vivo by sensing the enzyme myeloperoxidase. Proc Natl Acad Sci U S A 105: 18584-18589.
20. Brewer KL, Bethea JR, Yezierski RP. 1999. Neuroprotective effects of interleukin-10 following excitotoxic spinal cord injury. Exp Neurol 159: 484-493.
21. Buchwald UK, Geerdes-Fenge HF, Vockler J, Ziege S, Lode H. 1999. Interleukin-10: effects on phagocytosis and adhesion molecule expression of granulocytes and monocytes in a comparison with prednisolone. Eur J Med Res 4: 85-94.
22. Buisson A, Lesne S, Docagne F, Ali C, Nicole O, MacKenzie ET, Vivien D. 2003. Transforming growth factor-beta and ischemic brain injury. Cell Mol Neurobiol 23: 539-550.
23. Bush TG, Puvanachandra N, Horner CH, Polito A, Ostenfeld T, Svendsen CN, Mucke L, Johnson MH, Sofroniew MV. 1999. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23: 297-308.
24. Cai Z, Lin S, Pang Y, Rhodes PG. 2004. Brain injury induced by intracerebral injection of interleukin-1beta and tumor necrosis factor-alpha in the neonatal rat. Pediatr Res 56: 377-384.
25. Campuzano O, Castillo-Ruiz MD, Acarin L, Gonzalez B, Castellano B. 2011. Decreased myeloperoxidase expressing cells in the aged rat brain after excitotoxic damage. Exp Gerontol (in press).
26. Chew LJ, Takanohashi A, Bell M. 2006. Microglia and inflammation: impact on developmental brain injuries. Ment Retard Dev Disabil Res Rev 12: 105-112.
27. Cornette L. 2004. Fetal and neonatal inflammatory response and adverse outcome. Semin Fetal Neonatal Med 9: 459-470.
28. Cuadros MA, Navascues J. 1998. The origin and differentiation of microglial cells during development. Prog Neurobiol 56: 173-189.
29. Dammann O, Leviton A. 1997. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 42: 1-8.
30. Dietrich WD, Busto R, Bethea JR. 1999. Postischemic hypothermia and IL-10 treatment provide long-lasting neuroprotection of CA1 hippocampus following transient global ischemia in rats. Exp Neurol 158: 444-450.
31. Ehrlich LC, Hu S, Peterson PK, Chao CC. 1998. IL-10 down-regulates human microglial IL-8 by inhibition of NF-kappaB activation. Neuroreport 9: 1723-1726.
32. Fan LW, Pang Y, Lin S, Rhodes PG, Cai Z. 2005. Minocycline attenuates lipopolysaccharide-induced white matter injury in the neonatal rat brain. Neuroscience 133: 159-168.
33. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. 2004. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24: 2143-2155.
34. Ferriero DM. 2004. Neonatal brain injury. N Engl J Med 351: 1985-1995.
35. Ferriero DM, Holtzman DM, Black SM, Sheldon RA. 1996. Neonatal mice lacking neuronal nitric oxide synthase are less vulnerable to hypoxic-ischemic injury. Neurobiol Dis 3: 64-71.
36. Froen JF, Munkeby BH, Stray-Pedersen B, Saugstad OD. 2002. Interleukin-10 reverses acute detrimental effects of endotoxin-induced inflammation on perinatal cerebral hypoxia-ischemia. Brain Res 942: 87-94.
37. Gadient RA, Otten UH. 1997. Interleukin-6 (IL-6)-a molecule with both beneficial and destructive potentials. Prog Neurobiol 52: 379-390.
38. Galasso JM, Liu Y, Szaflarski J, Warren JS, Silverstein FS. 2000. Monocyte chemoattractant protein-1 is a mediator of acute excitotoxic injury in neonatal rat brain. Neuroscience 101: 737-744.
39. Gonzalez FF, Ferriero DM. 2008. Therapeutics for neonatal brain injury. Pharmacol Ther 120: 43-53.
40. Gonzalez P, Burgaya F, Acarin L, Peluffo H, Castellano B, Gonzalez B. 2009. Interleukin-10 and interleukin-10 receptor-I are upregulated in glial cells after an excitotoxic injury to the postnatal rat brain. J Neuropathol Exp Neurol 68: 391-403.
41. Guo H, Jin YX, Ishikawa M, Huang YM, van der Meide PH, Link H, Xiao BG. 1998. Regulation of beta-chemokine mRNA expression in adult rat astrocytes by lipopolysaccharide, proinflammatory and immunoregulatory cytokines. Scand J Immunol 48: 502-508.
42. Hagan P, Barks JD, Yabut M, Davidson BL, Roessler B, Silverstein FS. 1996. Adenovirus-mediated over-expression of interleukin-1 receptor antagonist reduces susceptibility to excitotoxic brain injury in perinatal rats. Neuroscience 75: 1033-1045.
43. Hagberg H, Gilland E, Bona E, Hanson LA, Hahin-Zoric M, Blennow M, Holst M, McRae A, Soder O. 1996. Enhanced expression of interleukin (IL)-1 and IL-6 messenger RNA and bioactive protein after hypoxia-ischemia in neonatal rats. Pediatr Res 40: 603-609.
44. Hamada Y, Hayakawa T, Hattori H, Mikawa H. 1994. Inhibitor of nitric oxide synthesis reduces hypoxic-ischemic brain damage in the neonatal rat. Pediatr Res 35: 10-14.
45. Hartl R, Schurer L, Schmid-Schonbein GW, del Zoppo GJ. 1996. Experimental antileukocyte interventions in cerebral ischemia. J Cereb Blood Flow Metab 16: 1108-1119.
46. Hudome S, Palmer C, Roberts RL, Mauger D, Housman C, Towfighi J. 1997. The role of neutrophils in the production of hypoxic-ischemic brain injury in the neonatal rat. Pediatr Res 41: 607-616.
47. Hulshof S, Montagne L, De Groot CJ, Van Der Valk P. 2002. Cellular localization and expression patterns of interleukin-10, interleukin-4, and their receptors in multiple sclerosis lesions. Glia 38: 24-35.
48. Jackson CA, Messinger J, Peduzzi JD, Ansardi DC, Morrow CD. 2005. Enhanced functional recovery from spinal cord injury following intrathecal or intramuscular administration of poliovirus replicons encoding IL-10. Virology 336: 173-183.
49. Jander S, Pohl J, D'Urso D, Gillen C, Stoll G. 1998. Time course and cellular localization of interleukin-10 mRNA and protein expression in autoimmune inflammation of the rat central nervous system. Am J Pathol 152: 975-982.
50. Kadhim H, Tabarki B, Verellen G, De Prez C, Rona AM, Sebire G. 2001. Inflammatory cytokines in the pathogenesis of periventricular leukomalacia. Neurology 56: 1278-1284.
51. Kamm K, Vanderkolk W, Lawrence C, Jonker M, Davis AT. 2006. The effect of traumatic brain injury upon the concentration and expression of interleukin-1beta and interleukin-10 in the rat. J Trauma 60: 152-157.
52. Kaur C, Hao AJ, Wu CH, Ling EA. 2001. Origin of microglia. Microsc Res Techniq 54: 2-9.
53. Kline AE, Bolinger BD, Kochanek PM, Carlos TM, Yan HQ, Jenkins LW, Marion DW, Dixon CE. 2002. Acute systemic administration of interleukin-10 suppresses the beneficial effects of moderate hypothermia following traumatic brain injury in rats. Brain Res 937: 22-31.
54. Knoblach SM, Faden AI. 1998. Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury. Exp Neurol 153: 143-151.
55. Kochanek PM, Hallenbeck JM. 1992. Polymorphonuclear leukocytes and monocytes/macrophages in the pathogenesis of cerebral ischemia and stroke. Stroke 23: 1367-1379.
56. Krakauer T. 1995. IL-10 inhibits the adhesion of leukocytic cells to IL-1-activated human endothelial cells. Immunol Lett 45: 61-65.
57. Kremlev SG, Roberts RL, Palmer C. 2007. Minocycline modulates chemokine receptors but not interleukin-10 mRNA expression in hypoxic-ischemic neonatal rat brain. J Neurosci Res 85: 2450-2459.
58. Lawson LJ, Perry VH. 1995. The unique characteristics of inflammatory responses in mouse brain are acquired during postnatal development. Eur J Neurosci 7: 1584-1595.
59. Ledeboer A, Breve JJ, Poole S, Tilders FJ, Van Dam AM. 2000. Interleukin-10, interleukin-4, and transforming growth factor-beta differentially regulate lipopolysaccharide-induced production of pro-inflammatory cytokines and nitric oxide in co-cultures of rat astroglial and microglial cells. Glia 30: 134-142.
60. Ledeboer A, Wierinckx A, Bol JG, Floris S, Renardel de Lavalette C, De Vries HE, van den Berg TK, Dijkstra CD, Tilders FJ, van dam AM. 2003. Regional and temporal expression patterns of interleukin-10, interleukin-10 receptor and adhesion molecules in the rat spinal cord during chronic relapsing EAE. J Neuroimmunol 136: 94-103.
61. Leviton A, Dammann O. 2004. Coagulation, inflammation, and the risk of neonatal white matter damage. Pediatr Res 55: 541-545.
62. Liberto CM, Albrecht PJ, Herx LM, Yong VW, Levison SW. 2004. Pro-regenerative properties of cytokine-activated astrocytes. J Neurochem 89: 1092-1100.
63. Lin S, Cox HJ, Rhodes PG, Cai Z. 2006. Neuroprotection of alpha-phenyl-n-tert-butyl-nitrone on the neonatal white matter is associated with anti-inflammation. Neurosci Lett 405: 52-56.
64. Lodge PA, Sriram S. 1996. Regulation of microglial activation by TGF-beta, IL-10, and CSF-1. J Leukoc Biol 60: 502-508.
65. Mesples B, Plaisant F, Gressens P. 2003. Effects of interleukin-10 on neonatal excitotoxic brain lesions in mice. Brain Res Dev Brain Res 141: 25-32.
66. Mesples B, Fontaine RH, Lelievre V, Launay JM, Gressens P. 2005. Neuronal TGF-beta1 mediates IL-9/mast cell interaction and exacerbates excitotoxicity in newborn mice. Neurobiol Dis 18: 193-205.
67. Molina-Holgado E, Vela JM, Arevalo-Martin A, Guaza C. 2001a. LPS/IFN-gamma cytotoxicity in oligodendroglial cells: role of nitric oxide and protection by the anti-inflammatory cytokine IL-10. Eur J Neurosci 13: 493-502.
68. Molina-Holgado F, Grencis R, Rothwell NJ. 2001b. Actions of exogenous and endogenous IL-10 on glial responses to bacterial LPS/cytokines. Glia 33: 97-106.
69. Molina-Holgado E, Arevalo-Martin A, Castrillo A, Bosca L, Vela JM, Guaza C. 2002a. Interleukin-4 and interleukin-10 modulate nuclear factor kappaB activity and nitric oxide synthase-2 expression in Theiler's virus-infected brain astrocytes. J Neurochem 81: 1242-1252.
70. Molina-Holgado E, Arevalo-Martin A, Ortiz S, Vela JM, Guaza C. 2002b. Theiler's virus infection induces the expression of cyclooxygenase-2 in murine astrocytes: inhibition by the anti-inflammatory cytokines interleukin-4 and interleukin-10. Neurosci Lett 324: 237-241.
71. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. 2001. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19: 683-765.
72. Mostafa Mtairag E, Chollet-Martin S, Oudghiri M, Laquay N, Jacob MP, Michel JB, Feldman LJ. 2001. Effects of interleukin-10 on monocyte/endothelial cell adhesion and MMP-9/TIMP-1 secretion. Cardiovasc Res 49: 882-890.
73. Myer DJ, Gurkoff GG, Lee SM, Hovda DA, Sofroniew MV. 2006. Essential protective roles of reactive astrocytes in traumatic brain injury. Brain 129: 2761-2772.
74. Nawashiro H, Messing A, Azzam N, Brenner M. 1998. Mice lacking GFAP are hypersensitive to traumatic cerebrospinal injury. Neuroreport 9: 1691-1696.
75. Nawashiro H, Brenner M, Fukui S, Shima K, Hallenbeck JM. 2000. High susceptibility to cerebral ischemia in GFAP-null mice. J Cereb Blood Flow Metab 20: 1040-1044.
76. Northington FJ. 2006. Brief update on animal models of hypoxic-ischemic encephalopathy and neonatal stroke. Ilar J 47: 32-38.
77. O'Keefe GM, Nguyen VT, Benveniste EN. 1999. Class II transactivator and class II MHC gene expression in microglia: modulation by the cytokines TGF-beta, IL-4, IL-13 and IL-10. Eur J Immunol 29: 1275-1285.
78. Ooboshi H, Ibayashi S, Shichita T, Kumai Y, Takada J, Ago T, Arakawa S, Sugimori H, Kamouchi M, Kitazono T, Iida M. 2005. Postischemic gene transfer of interleukin-10 protects against both focal and global brain ischemia. Circulation 111: 913-919.
79. Palmer C, Roberts RL, Young PI. 2004. Timing of neutrophil depletion influences long-term neuroprotection in neonatal rat hypoxic-ischemic brain injury. Pediatr Res 55: 549-556.
80. Pang Y, Rodts-Palenik S, Cai Z, Bennett WA, Rhodes PG. 2005. Suppression of glial activation is involved in the protection of IL-10 on maternal E. coli induced neonatal white matter injury. Brain Res Dev Brain Res 157: 141-149.
81. Peluffo H, Aris A, Acarin L, Gonzalez B, Villaverde A, Castellano B. 2003. Nonviral gene delivery to the central nervous system based on a novel integrin-targeting multifunctional protein. Hum Gene Ther 14: 1215-1223.
82. Peluffo H, Acarin L, Faiz M, Castellano B, Gonzalez B. 2005. Cu/Zn Superoxide dismutase expression in the postnatal rat brain following an excitotoxic injury. J Neuroinflammation 2: 12.
83. Peluffo H, Acarin L, Aris A, Gonzalez P, Villaverde A, Castellano B, Gonzalez B. 2006. Neuroprotection from NMDA excitotoxic lesion by Cu/Zn superoxide dismutase gene delivery to the postnatal rat brain by a modular protein vector. BMC Neurosci 7: 35.
84. Peluffo H, Gonzalez P, Aris A, Acarin L, Saura J, Villaverde A, Castellano B, Gonzalez B. 2007. RGD domains neuroprotect the immature brain by a glial-dependent mechanism. Ann Neurol 62: 251-261.
85. Pousset F, Cremona S, Dantzer R, Kelley K, Parnet P. 1999. Interleukin-4 and interleukin-10 regulate IL1-beta induced mouse primary astrocyte activation: a comparative study. Glia 26: 12-21.
86. Pousset F, Cremona S, Dantzer R, Kelley KW, Parnet P. 2001. IL-10 and IL-4 regulate type-I and type-II IL-1 receptors expression on IL-1 beta-activated mouse primary astrocytes. J Neurochem 79: 726-736.
87. Rezaie P, Dean A. 2002. Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathology 22: 106-132.
88. Rodts-Palenik S, Wyatt-Ashmead J, Pang Y, Thigpen B, Cai Z, Rhodes P, Martin JN, Granger J, Bennett WA. 2004. Maternal infection-induced white matter injury is reduced by treatment with interleukin-10. Am J Obstet Gynecol 191: 1387-1392.
89. Rothwell N. 2003. Interleukin-1 and neuronal injury: mechanisms, modification, and therapeutic potential. Brain Behav Immun 17: 152-157.
90. Sawada M, Suzumura A, Hosoya H, Marunouchi T, Nagatsu T. 1999. Interleukin-10 inhibits both production of cytokines and expression of cytokine receptors in microglia. J Neurochem 72: 1466-1471.
91. Schultz C, Temming P, Bucsky P, Gopel W, Strunk T, Hartel C. 2004. Immature anti-inflammatory response in neonates. Clin Exp Immunol 135: 130-136.
92. Shohami E, Ginis I, Hallenbeck JM. 1999. Dual role of tumor necrosis factor alpha in brain injury. Cytokine Growth Factor Rev 10: 119-130.
93. Shrikant P, Weber E, Jilling T, Benveniste EN. 1995. Intercellular adhesion molecule-1 gene expression by glial cells. Differential mechanisms of inhibition by IL-10 and IL-6. J Immunol 155: 1489-1501.
94. Silverstein FS, Barks JD, Hagan P, Liu XH, Ivacko J, Szaflarski J. 1997. Cytokines and perinatal brain injury. Neurochem Int 30: 375-383.
95. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. 1985. Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85.
96. Spera PA, Ellison JA, Feuerstein GZ, Barone FC. 1998. IL-10 reduces rat brain injury following focal stroke. Neurosci Lett 251: 189-192.
97. Strle K, Zhou JH, Shen WH, Broussard SR, Johnson RW, Freund GG, Dantzer R, Kelley KW. 2001. Interleukin-10 in the brain. Crit Rev Immunol 21: 427-449.
98. Tahraoui SL, Marret S, Bodenant C, Leroux P, Dommergues MA, Evrard P, Gressens P. 2001. Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol 11: 56-71.
99. Touzani O, Boutin H, Chuquet J, Rothwell N. 1999. Potential mechanisms of interleukin-1 involvement in cerebral ischaemia. J Neuroimmunol 100: 203-215.
100. Tsuji M, Higuchi Y, Shiraishi K, Kume T, Akaike A, Hattori H. 2000. Protective effect of aminoguanidine on hypoxic-ischemic brain damage and temporal profile of brain nitric oxide in neonatal rat. Pediatr Res 47: 79-83.
101. Vannucci SJ, Hagberg H. 2004. Hypoxia-ischemia in the immature brain. J Exp Biol 207: 3149-3154.
102. Woiciechowsky C, Schoning B, Stoltenburg-Didinger G, Stockhammer F, Volk HD. 2004. Brain-IL-1 beta triggers astrogliosis through induction of IL-6: inhibition by propranolol and IL-10. Med Sci Monit 10: BR325-330.
103. Zhai QH, Futrell N, Chen FJ. 1997. Gene expression of IL-10 in relationship to TNF-alpha, IL-1beta and IL-2 in the rat brain following middle cerebral artery occlusion. J Neurol Sci 152: 119-124.