Cellular mechanisms of toll-like receptor-3 activation in the thalamus are associated with white matter injury in the developing brain

Journal of Neuropathology and Experimental Neurology

Volumn 74, Issue 3, 2015, Pages 273-285

  Vontell, Regina ^a   Supramaniam, Veena ^a   Wyatt Ashmead, Josephine ^b   Gressens, Pierre ^a,d   Rutherford, Mary ^a   Hagberg, Henrik ^a,c   Thornton, Claire ^a  

^a ST THOMAS HOSPITAL   (United Kingdom)

^b ST MARY S HOSPITAL   (United Kingdom)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d INSERM   (France)

Author keywords

Interferon regulatory factor 3; Microtubule associated protein light chain; Toll like receptor 3; White matter injury

Indexed keywords

ADAPTOR PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERFERON REGULATORY FACTOR 3; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; TLR3 PROTEIN, HUMAN;

ARTICLE; AUTOPHAGOSOME; BRAIN DEVELOPMENT; CAPSULA INTERNA; CELL DENSITY; CELL SURVIVAL; CELLULAR DISTRIBUTION; CELLULAR STRESS RESPONSE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOSOME; GENE ACTIVATION; GENE EXPRESSION; GRAY MATTER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; INFANT; MACROGLIA; MITOPHAGY; MOTOR DYSFUNCTION; PREMATURITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; THALAMOCORTICAL TRACT; THALAMUS NUCLEUS; UPREGULATION; WHITE MATTER INJURY; BIOSYNTHESIS; CELL CULTURE; EMBRYOLOGY; METABOLISM; NEWBORN; PATHOLOGY; PILOT STUDY; PROSPECTIVE STUDY; THALAMUS; WHITE MATTER;

CELLS, CULTURED; HUMANS; INFANT, EXTREMELY PREMATURE; INFANT, NEWBORN; PILOT PROJECTS; PROSPECTIVE STUDIES; THALAMUS; TOLL-LIKE RECEPTOR 3; WHITE MATTER;

EID: 84923650510     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0000000000000172     Document Type: Article

References (53)

1. Inder T, Neil J, Yoder B, et al. Patterns of cerebral injury in a primate model of preterm birth and neonatal intensive care. J Child Neurol 2005; 20:965-67
2. Ajayi-Obe M, Saeed N, Cowan FM, et al. Reduced development of cerebral cortex in extremely preterm infants. Lancet 2000;356:1162-63
3. Northington FJ, Traystman RJ, Koehler RC, et al. GLT1, glial glutamate transporter, is transiently expressed in neurons and develops astrocyte specificity only after midgestation in the ovine fetal brain. J Neurobiol 1999;39:515-26
4. Back S, Volpe J. Cellular and molecular pathogenesis of periventricular white matter injury. Ment Retard Dev Disabil Res Rev1997;3:96-107
5. Nagasunder AC, Kinney HC, Bluml S, et al. Abnormal microstructure of the atrophic thalamus in preterm survivors with periventricular leukomalacia. AJNR Am J Neuroradiol 2011;32:185-91
6. Graham EM, Sheldon RA, Flock DL, et al. Neonatal mice lacking functional Fas death receptors are resistant to hypoxic-ischemic brain injury. Neurobiol Dis 2004;17:89-98
7. Martinez-Biarge M, Diez-Sebastian J, Rutherford MA, et al. Outcomes after central grey matter injury in term perinatal hypoxic-ischaemic encephalopathy. Early Hum Dev 2010;86:675-82
8. Zubiaurre-Elorza L, Soria-Pastor S, Junque C, et al. Gray matter volume decrements in preterm children with periventricular leukomalacia. Pediatr Res 2011;69:554-60
9. de Vries LS, van Haastert IC, Benders MJ, et al. Myth: Cerebral palsy cannot be predicted by neonatal brain imaging. Semin Fetal Neonatal Med 2011;16:279-87
10. Ligam P, Haynes RL, Folkerth RD, et al. Thalamic damage in periventricular leukomalacia: Novel pathologic observations relevant to cognitive deficits in survivors of prematurity. Pediatr Res 2009;65:524-29
11. Thornton C, Rousset CI, Kichev A, et al. Molecular mechanisms of neonatal brain injury. Neurol Res Int 2012;2012:506320. doi: 10.1155/2012/506320
12. Hagberg H, Mallard C, Rousset CI, et al. Mitochondria: Hub of injury responses in the developing brain. Lancet Neurol 2014;13:217-32
13. Johnston MV, Fatemi A, Wilson MA, et al. Treatment advances in neonatal neuroprotection and neurointensive care. Lancet Neurol 2011;10: 372-82
14. Botos I, Segal DM, Davies DR. The structural biology of Toll-like receptors. Structure 2011;19:447-59
15. Hagberg H, Gressens P, Mallard C. Inflammation during fetal and neonatal life: Implications for neurologic and neuropsychiatric disease in children and adults. Ann Neurol 2012;71:444-57
16. Harashima N, Inao T, Imamura R, et al. Roles of the PI3K/Akt pathway and autophagy in TLR3 signalingYinduced apoptosis and growth arrest of human prostate cancer cells. Cancer Immunol Immunother 2012;61: 667-76
17. Lee BL, Barton GM. Trafficking of endosomal Toll-like receptors. Trends Cell Biol 2014;24:360-69
18. Kim YM, Brinkmann MM, Paquet ME, et al. UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 2008; 452:234-38
19. Brinkmann MM, Spooner E, Hoebe K, et al. The interaction between the ER membrane protein UNC93B and TLR3, 7, and 9 is crucial for TLR signaling. J Cell Biol 2007;177:265-75
20. Johnsen IB, Nguyen TT, Ringdal M, et al. Toll-like receptor 3 associates with c-Src tyrosine kinase on endosomes to initiate antiviral signaling. EMBO J 2006;25:3335-46
21. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004; 4:499-511
22. Sun R, Zhang Y, Lv Q, et al. Toll-like receptor 3 (TLR3) induces apoptosis via death receptors and mitochondria by up-regulating the transactivating p63 isoform alpha (TAP63alpha). J Biol Chem 2011;286: 15918-28
23. He S, Liang Y, Shao F, et al. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3Ymediated pathway. Proc Natl Acad Sci U S A 2011;108:20054-59
24. Kaiser WJ, Offermann MK. Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J Immunol 2005;174:4942-52
25. Lathia JD, Okun E, Tang SC, et al. Toll-like receptor 3 is a negative regulator of embryonic neural progenitor cell proliferation. J Neurosci 2008;28:13978-84
26. Cameron JS, Alexopoulou L, Sloane JA, et al. Toll-like receptor 3 is a potent negative regulator of axonal growth in mammals. J Neurosci 2007; 27:13033-41
27. Stridh L, Mottahedin A, JohanssonME, et al. Toll-like receptor-3 activation increases the vulnerability of the neonatal brain to hypoxia-ischemia. J Neurosci 2013;33:12041-51
28. Meyer U. Prenatal poly(i:C) exposure and other developmental immune activation models in rodent systems. Biol Psychiatry 2014;75:307-15
29. Meyer U, Feldon J. To poly(I:C) or not to poly(I:C): Advancing preclinical schizophrenia research through the use of prenatal immune activation models. Neuropharmacology 2012;62:1308-21
30. Vontell R, Supramaniam V, Thornton C, et al. Toll-like receptor 3 expression in glia and neurons alters in response to white matter injury in preterm infants. Dev Neurosci 2013;35:130-39
31. Sherman SM. The function of metabotropic glutamate receptors in thalamus and cortex. Neuroscientist 2013;20:136-49
32. Jones EG. The Thalamus. 2nd ed. Cambridge, United Kingdom: Cambridge University Press, 2007
33. Misselwitz B, Strittmatter G, Periaswamy B, et al. Enhanced CellClassifier: A multi-class classification tool for microscopy images. BMC Bioinformatics 2010;11:30. doi: 10.1186/1471-2105-11-30
34. Sherman SM, Guillery RW. Functional Connections of Cortical Areas: A New View From the Thalamus. London, England: The MIT Press, 2013
35. Oh JE, Lee HK. Pattern recognition receptors and autophagy. Front Immunol 2014;5:300
36. Xu Y, Liu XD, Gong X, et al. Signaling pathway of autophagy associated with innate immunity. Autophagy 2008;4:110-12
37. Zhan Z, Xie X, Cao H, et al. Autophagy facilitates TLR4-And TLR3-Triggered migration and invasion of lung cancer cells through the promotion of TRAF6 ubiquitination. Autophagy 2014;10:257-68
38. Henault J, Martinez J, Riggs JM, et al. Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity 2012;37:986-97
39. Rousset CI, Baburamani AA, Thornton C, et al. Mitochondria and perinatal brain injury. J Matern Fetal Neonatal Med 2012;25(Suppl 1):35-38
40. Liu QA, Shio H. Mitochondrial morphogenesis, dendrite development, and synapse formation in cerebellum require both Bcl-w and the glutamate receptor delta2. PLoS Genet 2008;4:e1000097
41. Zubiaurre-Elorza L, Soria-Pastor S, Junque C, et al. Thalamic changes in a preterm sample with periventricular leukomalacia: Correlation with white-matter integrity and cognitive outcome at school age. Pediatr Res 2012;71:354-60
42. Sherman SM, Guillery RW, Sherman SM. Exploring the Thalamus and Its Role in Cortical Function. 2nd ed. Cambridge, MA: MIT Press, 2006
43. Spittle AJ, Orton J. Cerebral palsy and developmental coordination disorder in children born preterm. Semin Fetal Neonatal Med 2014;19:84-89
44. Lagercrantz H. The Newborn Brain: Neuroscience and Clinical Applications. Cambridge, United Kingdom: Cambridge University Press 2010
45. Hagberg H, Mallard C. Effect of inflammation on central nervous system development and vulnerability. Curr Opin Neurol 2005;18:117-23
46. Kinney H, Back S. Human oligodendroglial development: Relationship to periventricular leukomalacia. Semin Pediatr Neonat 1997;5:180-89
47. Haynes RL, Xu G, Folkerth RD, et al. Potential neuronal repair in cerebral white matter injury in the human neonate. Pediatr Res 2011;69: 62-67
48. Supramaniam V, Vontell R, Srinivasan L, et al. Microglia activation in the extremely preterm human brain. Pediatr Res 2013;73:301-9
49. Rezaie P, Dean A. Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathology 2002;22:106-32
50. Kariko K, Ni H, Capodici J, et al. mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 2004;279:12542-50
51. Bsibsi M, Bajramovic JJ, Vogt MH, et al. The microtubule regulator stathmin is an endogenous protein agonist for TLR3. J Immunol 2010; 184:6929-37
52. Desjardins M. ER-mediated phagocytosis: A new membrane for new functions. Nat Rev Immunol 2003;3:280-91
53. Zhu C, Wang X, Xu F, et al. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 2005;12:162-6