Role of Tissue-Derived Plasminogen Activator (t-PA) in an Excitotoxic Mouse Model of Neonatal White Matter Lesions

Journal of Neuropathology and Experimental Neurology

Volumn 63, Issue 1, 2004, Pages 53-63

  Hennebert, Olivier ^a   Marret, Stéphane ^a,b   Carmeliet, Peter ^c   Gressens, Pierre ^d   Laquerrière, Annie ^a,b   Leroux, Philippe ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b ROUEN UNIVERSITY HOSPITAL   (France)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

Astrocytes; Glial fibrillary acidic protein; Hemosiderin; Ibotenic acid; Microglia; Myelin basic protein; Neurofilament

Indexed keywords

IBOTENIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BRAIN CYST; BRAIN INJURY; CELL ACTIVATION; CEREBRAL PALSY; DEMYELINATION; DOSE RESPONSE; HISTOPATHOLOGY; KNOCKOUT MOUSE; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; WHITE MATTER; WILD TYPE;

EID: 0346789090     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/63.1.53     Document Type: Article

References (44)

1. Kuban K, Sanocka U, Leviton A, et al. White matter disorders of prematurity: Association with intraventricular hemorrhage and ventriculomegaly. The developmental epidemiology network. J Pediatr 1999;134:539-46
2. Saliba E, Marret S. Cerebral white matter damage in the preterm infant: Pathophysiology and risk factors. Semin Neonatol 2001;6:121-33
3. Dammann O, Leviton A. Brain damage in preterm newborns: Might enhancement of developmentally regulated endogenous protection open a door for prevention. Pediatrics 1999;104:541-50
4. Volpe JJ. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 2001;50:553-62
5. Evrard P. Pathophysiology of perinatal brain damage. Dev Neurosci 2001;23:171-74
6. Marin-Padilla M. Developmental neuropathology and impact of perinatal brain damage. 11: White matter lesions of the neocortex. J Neuropathol Exp Neurol 1997;56:219-35
7. Sheldon RA, Chuai J, Ferriero DM. A rat model for hypoxic-ischemic brain damage in very premature infants. Biol Neonate 1996;69:327-41
8. Ohyu J, Marumo G, Ozawa H, et al. Early axonal and glial pathology in fetal sheep brains with leukomalacia induced by repeated umbilical cord occlusion. Brain Dev 1999;21:248-52
9. Debillon T, Gras-Leguen C, Verielle V, et al. Intrauterine infection induces programmed cell death in rabbit periventricular white matter. Pediatr Res 2000;47:736-42
10. Cai Z, Pan ZL, Pang Y, Evans OB, Rhodes PG. Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr Res 2000;47:64-72
11. Lipton SA, Rosenberg PA. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 1994;330:613-22
12. Follett PL, Rosenberg PA, Volpe JJ, Jensen FE. NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 2000;20:9235-41
13. Marret S, Mukendi R, Gadisseux JF, Gressens P, Evrard P. Effect of ibotenate on brain development: An excitotoxic mouse model of microgyria and posthypoxic-like lesions. J Neuropathol Exp Neurol 1995;95:358-70
14. Tahraoui SL, Marret S, Bodénant C, et al. Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol 2001;11:56-71
15. Dommergues MA, Patkai J, Renaud JC, Evrard P, Gressens P. Proinflammatory cytokines and interleukin-9 exacerbate excitotoxic lesions of the newborn murine neopallium. Ann Neurol 2000;47:54-63
16. Arquié C, Leroux P, Bodenant C, Laquerrière A, Marpeau L, Marret S. Glucocorticoid treatment in an ischaemic-like excitotoxic model of leucomalacia in mice. Brit J Obstet Gynaecol 2002;109:989-96
17. Fitch MT, Doller C, Combs CK, Landreth GE, Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: In vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci 1999;19:8182-98
18. Perry VH, Bell MD, Anthony DC. Unique aspects of inflammation in the central nervous system. In: Ruffolo RR, Feuerstein GZ, Hunter A J, Poste G, Metclaff BW. eds. Inflammatory cells and mediators in CNS diseases. Philadelphia: Smith Kline Beecham Pharmaceuticals, 1999:21-38
19. Flavin MP, Zhao G, Ho LT. Microglial tissue plasminogen activator (tPA) triggers neuronal apoptosis in vitro. Glia 2000;29:347-54
20. Tsirka SE, Gualandris A, Amaral DG, Strickland S. Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nat Med 1995:377:340-44
21. Wang YF, Tsirka SE, Strickland S, Stieg PE, Soriano SG, Lipton SA. Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat Med 1998;4:228-31
22. Chen ZL, Strickland S. Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 1997;91:917-25
23. Nagai N, Urano T, Endo A, Takahashi H, Takada Y, Takada A. Neuronal degeneration and a decrease in laminin-like immunoreactivity is associated with elevated tissue-type plasminogen activator in the rat hippocampus after kainic acid injection. Neurosci Res 1999;33:147-54
24. Rogove AD, Siao C, Keyt B, Strickland S, Tsirka SE. Activation of microglia reveals a non proteolytic cytokine function for tissue plasminogen activator in the central nervous system. J Cell Sci 1999;112:4007-16
25. Siao C, Tsirka SE. Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. J Neurosci 2002;22:3352-58
26. Nicole O, Docagne F, Ali C, et al. The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat Med 2001;7:59-64
27. Whitelaw A, Thorensen M, Pople I. Posthaemorrhagic ventricular dilatation. Arch Dis Child Fetal Neonat Ed 2002;86:F72-F74
28. Carmeliet P, Schoonjans L, Kieckens L, et al. Physiological consequences of loss of plasminogen activator gene function in mice. Nature 1994;368:419-24
29. Marret S, Bonnier C, Raymackers JM, Delpech A, Evrard P, Gressens P. Glycine antagonist and NO synthase inhibitor protect the developing mouse brain against neonatal excitotoxic lesions. Pediatr Res 1999;45:337-42
30. Marret S, Gressens P, Gadisseux JF, Evrard P. Prevention by magnesium of excitotoxic neuronal death in the developing brain: An animal model for clinical intervention studies. Dev Med Child Neurol 1995;37:473-84
31. Carmeliet P, Stassen JM, Vlaenderen IV, Meidell RS, Collen D, Gerard RD. Adenovirus-mediated transfer of tissue type plasminogen activator augments thrombolysis in tissue type plasminogen activator deficient and plasminogen activator inhibitor-1 overexpressing mice. Blood 1997;90:1527-34
32. Nelson K, Dambrosia J, Grether J, Phillips T. Neonatal cytokines and coagulation factors in children with cerebral palsy. Ann Neurol 1998;44:665-75
33. Krizbai IA, Deli MA, Pestenacz A, et al. Expression of glutamate receptors on cultured cerebral endothelial cells. J Neurosci Res 1998;54:814-19
34. Buisson A, Nicole O, Docagne F, Sartelet H, Mac Kenzie ET, Vivien D. Up-regulation of a serine protease inhibitor in astrocytes mediates the neuroprotective activity of transforming growth factor beta-1. FASEB J 1998;12:1683-91
35. Hastings GA, Coleman TA, Haudenschild CC, et al. Neuroserpin, a brain-associated inhibitor of tissue plasminogen activator is localized primarily in neurons. J Biol Chem 1997;272:33062-67
36. Sharon R, Abramovitz R, Miskin R. Plasminogen mRNA induction in the mouse brain after kainate excitation: Codistribution with plasminogen activator inhibitor-2 (PAI-2) mRNA. Brain Res Brain Res Rev 2002;104:170-75
37. Matsuoka Y, Kitamura Y, Taniguchi T. Induction of plasminogen in rat hippocampal pyramidal neurons by kainic acid. Neurosci Letters 1998;252:119-22
38. Rogove AD, Tsirka SE. Neurotoxic responses by microglia elicited by excitotoxic injury in the mouse hippocampus. Curr Biol 1997;8:19-25
39. Hirayama M, Kuriyama M. MK-801 is cytotoxic to microglia in vitro and its toxicity is attenuated by glutamate, other excitotoxic agents and atropine. Possible presence of glutamate receptor and muscarinic receptor on microglia. Brain Res 2001;897:204-6
40. Noda M, Nakanishi H, Nabekura J, Akaike N. AMPA-kainate subtypes of glutamate receptor in rat cerebral microglia. J Neurosci 2000;20:251-58
41. Gressens P, Marret S, Hill JM, et al. Vasoactive intestinal peptide prevents excitotoxic cell death in the murine developing brain. J Clin Invest 1997;100:390-97
42. Husson I, Mesplès B, Bac P, Vamecq J, Evrard P, Gressens P. Melatoninergic neuroprotection of the murine periventricular white matter against neonatal excitotoxic challenge. Ann Neurol 2001;51:82-92
43. Laudenbach V, Calo G, Guerrini R, et al. Nociceptin/orphanin FQ exacerbates excitotoxic white-matter lesions in the murine neonatal brain. J Clin Invest 2001;107:457-66
44. Larroque B, Marret S, Ancel P, et al. White matter damage and intraventricular hemorrhage in very preterm infants: The EPIPAGE study. J Pediatr 2003;143:477-83