Toll-Like Receptor-3 Activation Increases the Vulnerability of the Neonatal Brain to Hypoxia-Ischemia

Journal of Neuroscience

Volumn 33, Issue 29, 2013, Pages 12041-12051

  Stridh, Linnea ^a   Mottahedin, Amin ^a   Johansson, Maria E ^a   Valdez, Raul Chavez ^b   Northington, Frances ^b   Wang, Xiaoyang ^a   Mallard, Carina ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELIN BASIC PROTEIN; POLYINOSINIC ACID; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DAMAGE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; GENOTYPING TECHNIQUE; HEMISPHERE; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICROGLIA; MOUSE; NEUROPATHOLOGY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WHITE MATTER INJURY;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BRAIN; HYPOXIA-ISCHEMIA, BRAIN; I-KAPPA B PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; PHOSPHORYLATION; POLY I-C; PROTO-ONCOGENE PROTEINS C-AKT; TOLL-LIKE RECEPTOR 3;

EID: 84880419367     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0673-13.2013     Document Type: Article

References (46)

1. Bhatia S, Fei M, Yarlagadda M, Qi Z, Akira S, Saijo S, Iwakura Y, van Rooijen N, Gibson GA, St Croix CM, Ray A, Ray P (2011) Rapid host defense against Aspergillus fumigatus involves alveolar macrophages with a predominance of alternatively activated phenotype. PLoS One 6:e15943CrossRef Medline
2. Brywe KG, Mallard C, Gustavsson M, Hedtjärn M, Leverin AL, Wang X, Blomgren K, Isgaard J, Hagberg H (2005) IGF-I neuroprotection in the immature brain after hypoxia-ischemia, involvement of Akt and GSK3beta? Eur J Neurosci 21:1489-1502CrossRef Medline
3. Campbell IL, Stalder AK, Chiang CS, Bellinger R, Heyser CJ, Steffensen S, Masliah E, Powell HC, Gold LH, Henriksen SJ, Siggins GR (1997) Transgenic models to assess the pathogenic actions of cytokines in the central nervous system. Mol Psychiatry 2:125-129CrossRef Medline
4. Colton CA (2009) Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 4:399-418CrossRef Medline
5. Craig A, Ling Luo N, Beardsley DJ, Wingate-Pearse N, Walker DW, Hohimer AR, Back SA (2003) Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Exp Neurol 181:231-240CrossRef Medline
6. Cunningham C, Campion S, Teeling J, Felton L, Perry VH (2007) The sickness behaviour and CNS inflammatory mediator profile induced by systemic challenge of mice with synthetic double-stranded RNA (poly I:C). Brain Behav Immun 21:490-502CrossRef Medline
7. Cusson-Hermance N, Khurana S, Lee TH, Fitzgerald KA, Kelliher MA (2005) Rip1 mediates the Trif-dependent toll-like receptor 3- and 4-induced NF-kB activation but does not contribute to interferon regulatory factor 3 activation. J Biol Chem 280:36560-36566CrossRef Medline
8. Dammann O, Leviton A (1997) Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 42:1-8CrossRef Medline
9. Deleidi M, Hallett PJ, Koprich JB, Chung CY, Isacson O (2010) The Tolllike receptor-3 agonist polyinosinic:polycytidylic acid triggers nigrostriatal dopaminergic degeneration. J Neurosci 30:16091-16101CrossRef Medline
10. Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, Hagberg H (2001) Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 13:1101-1106CrossRef Medline
11. Eklind S, Mallard C, Arvidsson P, Hagberg H (2005) Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain. Pediatr Res 58:112-116CrossRef Medline
12. Famakin BM, Mou Y, Ruetzler CA, Bembry J, Maric D, Hallenbeck JM (2011) Disruption of downstream MyD88 or TRIF Toll-like receptor signaling does not protect against cerebral ischemia. Brain Res 1388:148-156CrossRef Medline
13. Favrais G, Schwendimann L, Gressens P, Lelièvre V (2007) Cyclooxygenase-2 mediates the sensitizing effects of systemic IL-1-beta on excitotoxic brain lesions in newborn mice. Neurobiol Dis 25:496-505CrossRef Medline
14. Field R, Campion S, Warren C, Murray C, Cunningham C (2010) Systemic challenge with the TLR3 agonist poly I:C induces amplified IFNalpha/ beta and IL-1beta responses in the diseased brain and exacerbates chronic neurodegeneration. Brain Behav Immun 24:996-1007CrossRef Medline
15. 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 101:737-744CrossRef Medline
16. Galic MA, Riazi K, Henderson AK, Tsutsui S, Pittman QJ (2009) Viral-like brain inflammation during development causes increased seizure susceptibility in adult rats. Neurobiol Dis 36:343-351CrossRef Medline
17. Hua F, Wang J, Sayeed I, Ishrat T, Atif F, Stein DG (2009) The TRIFdependent signaling pathway is not required for acute cerebral ischemia/ reperfusion injury in mice. Biochem Biophys ResCommun390:678-683CrossRef Medline
18. Hyakkoku K, Hamanaka J, Tsuruma K, Shimazawa M, Tanaka H, Uematsu S, Akira S, Inagaki N, Nagai H, Hara H (2010) Toll-like receptor 4 (TLR4), but not TLR3 or TLR9, knock-out mice have neuroprotective effects against focal cerebral ischemia. Neuroscience 171:258-267CrossRef Medline
19. Joung SM, Park ZY, Rani S, Takeuchi O, Akira S, Lee JY (2011) Akt contributes to activation of the TRIF-dependent signaling pathways of TLRs by interacting with TANK-binding kinase 1 J Immunol 186:499-507CrossRef Medline
20. Kendall GS, Hristova M, Horn S, Dafou D, Acosta-Saltos A, Almolda B, Zbarsky V, Rumajogee P, Heuer H, Castellano B, Pfeffer K, Nedospasov SA, Peebles DM, Raivich G (2011) TNF gene cluster deletion abolishes lipopolysaccharide-mediated sensitization of the neonatal brain to hypoxic ischemic insult. Lab Invest 91:328-341CrossRef Medline
21. Kim H, Yang E, Lee J, Kim SH, Shin JS, Park JY, Choi SJ, Kim SJ, Choi IH (2008) Double-stranded RNA mediates interferon regulatory factor 3 activation and interleukin-6 production by engaging Toll-like receptor 3 in human brain astrocytes. Immunology 124:480-488CrossRef Medline
22. Konat GW, Borysiewicz E, Fil D, James I (2009) Peripheral challenge with double-stranded RNA elicits global up-regulation of cytokine gene expression in the brain. J Neurosci Res 87:1381-1388CrossRef Medline
23. Lathia JD, Okun E, Tang SC, Griffioen K, Cheng A, Mughal MR, Laryea G, Selvaraj PK, ffrench-Constant C, Magnus T, Arumugam TV, Mattson MP (2008) Toll-like receptor 3 is a negative regulator of embryonic neural progenitor cell proliferation. J Neurosci 28:13978-13984CrossRef Medline
24. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T (2003) Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A 100:8514-8519CrossRef Medline
25. Liu Y, Kimura K, Yanai R, Chikama T, Nishida T (2008) Cytokine, chemokine, and adhesion molecule expression mediated by MAPKs in human corneal fibroblasts exposed to poly(I:C). Invest Ophthalmol Vis Sci 49: 3336-3344CrossRef Medline
26. Marsh B, Stevens SL, Packard AE, Gopalan B, Hunter B, Leung PY, Harrington CA, Stenzel-Poore MP (2009) Systemic lipopolysaccharide protects the brain from ischemic injury by reprogramming the response of the brain to stroke: a critical role for IRF3 J Neurosci 29:9839-9849CrossRef Medline
27. McWhirter SM, Fitzgerald KA, Rosains J, Rowe DC, Golenbock DT, Maniatis T (2004) IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc Natl Acad Sci U S A 101:233-238CrossRef Medline
28. Meyer U, Nyffeler M, Engler A, Urwyler A, Schedlowski M, Knuesel I, Yee BK, Feldon J (2006) The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci 26:4752-4762CrossRef Medline
29. Meylan E, Burns K, Hofmann K, Blancheteau V, Martinon F, Kelliher M, Tschopp J (2004) RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat Immunol 5:503-507CrossRef Medline
30. Mullonkal CJ, Toledo-Pereyra LH (2007) Akt in ischemia and reperfusion. J Invest Surg 20:195-203CrossRef Medline
31. Packard AE, Hedges JC, Bahjat FR, Stevens SL, Conlin MJ, Salazar AM, Stenzel-Poore MP (2012) Poly-IC preconditioning protects against cerebral and renal ischemia-reperfusion injury. J Cereb Blood Flow Metab 32:242-247CrossRef Medline
32. Park D, Lapteva N, Seethammagari M, Slawin KM, Spencer DM (2006) An essential role for Akt1 in dendritic cell function and tumor immunotherapy. Nat Biotechnol 24:1581-1590CrossRef Medline
33. Penkowa M, Hidalgo J (2000) IL-6 deficiency leads to reduced metallothionein-I_II expression and increased oxidative stress in the brain stem after 6-aminonicotinamide treatment. Exp Neurol 163:72-84CrossRef Medline
34. Ratnayake U, Quinn TA, Castillo-Melendez M, Dickinson H, Walker DW (2012) Behaviour and hippocampus-specific changes in spiny mouse neonates after treatment of the mother with the viral-mimetic Poly I:C at mid-pregnancy. Brain Behav Immun 26:1288-1299CrossRef Medline
35. Roda JM, Carceller F, Díez-Tejedor E, Avendaño C (1995) Reduction of infarct size by intra-arterial nimodipine administered at reperfusion in a rat model of partially reversible brain focal ischemia. Stroke 26: 1888-1892CrossRef Medline
36. Sasai M, Oshiumi H, Matsumoto M, Inoue N, Fujita F, Nakanishi M, Seya T (2005) Cutting Edge: NF-kappaB-activating kinase-associated protein 1 participates in TLR3/Toll-IL-1 homology domain-containing adapter molecule-1-mediated IFN regulatory factor 3 activation. J Immunol 174: 27-30. Medline
37. Sato S, Sugiyama M, Yamamoto M, Watanabe Y, Kawai T, Takeda K, Akira S (2003) Toll/IL-1 receptor domain-containing adaptor inducing IFN-beta (TRIF) associates with TNF receptor-associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-kappa B and IFN-regulatory factor-3, in the Toll-like receptor signaling. J Immunol 171: 4304-4310. Medline
38. Sävman K, Blennow M, Gustafson K, Tarkowski E, Hagberg H (1998) Cytokine response in cerebrospinal fluid after birth asphyxia. Pediatr Res 43:746-751CrossRef Medline
39. Smith SE, Li J, Garbett K, Mirnics K, Patterson PH (2007) Maternal immune activation alters fetal brain development through interleukin-6, J Neurosci 27:10695-10702CrossRef Medline
40. Svedin P, Hagberg H, Sävman K, Zhu C, Mallard C (2007) Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia. J Neurosci 27:1511-1518CrossRef Medline
41. Volpe JJ (2008) Neonatal encephalitis and white matter injury: more than just inflammation? Ann Neurol 64:232-236CrossRef Medline
42. Vontell R, Supramaniam V, Thornton C, Wyatt-Ashmead J, Mallard C, Gressens P, Rutherford M, Hagberg H (2013) Toll-like receptor 3 expression in glia and neurons alters in response to white matter injury in preterm infants. Dev Neurosci. Advance online publication. Retrieved June 18, 2013. doi:10.1159/000346158CrossRef Medline
43. Vuillermot S, Joodmardi E, Perlmann T, Ö gren SO, Feldon J, Meyer U (2012) Prenatal immune activation interacts with genetic Nurr1 deficiency in the development of attentional impairments. J Neurosci 32: 436-451 CrossRef Medline
44. Wang X, Stridh L, Li W, Dean J, Elmgren A, Gan L, Eriksson K, Hagberg H, Mallard C (2009) Lipopolysaccharide sensitizes neonatal hypoxicischemic brain injury in a MyD88-dependent manner. J Immunol 183: 7471-7477CrossRef Medline
45. Winerdal M, Winerdal ME, Kinn J, Urmaliya V, Winqvist O, Adén U (2012) Long lasting local and systemic inflammation after cerebral hypoxic ischemia in newborn mice. PLoS One 7:e36422CrossRef Medline
46. Xiong T, Tang J, Zhao J, Chen H, Zhao F, Li J, Qu Y, Ferriero D, Mu D (2012) Involvement of the Akt/GSK-3beta/CRMP-2 pathway in axonal injury after hypoxic-ischemic brain damage in neonatal rat. Neuroscience 216: 123-132CrossRef Medline