Neuronal TGF-β 1 mediates IL-9/mast cell interaction and exacerbates excitotoxicity in newborn mice

Neurobiology of Disease

Volumn 18, Issue 1, 2005, Pages 193-205

  Mesplès, Bettina ^a   Fontaine, Romain H ^a   Lelièvre, Vincent ^a,b   Launay, Jean Marie ^c   Gressens, Pierre ^a  

^a HÔPITAL ROBERT DEBRÉ   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Laboratoire de Biologie Cellulaire   (France)

Author keywords

Cerebral palsy; Cytokines; Glutamate; Histamine; Kit; N methyl D aspartate

Indexed keywords

ANTIHISTAMINIC AGENT; CROMOGLYCATE DISODIUM; DEXCHLORPHENIRAMINE; HISTAMINE; IBOTENIC ACID; INTERLEUKIN 9; NEUTRALIZING ANTIBODY; RANITIDINE; STEM CELL FACTOR; TRANSFORMING GROWTH FACTOR BETA1; ANTIBODY; HISTAMINE RECEPTOR; NEUROTOXIN; TGFB1 PROTEIN, HUMAN; TGFB1 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL INTERACTION; CELL LINE; CONTROLLED STUDY; DISEASE EXACERBATION; EMBRYO; EXCITOTOXICITY; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MAST CELL; MAST CELL DEGRANULATION; MOUSE; NERVE CELL; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SUPERNATANT; WESTERN BLOTTING; ANIMAL; BRAIN; C57BL MOUSE; CEREBRAL PALSY; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DRUG EFFECT; IMMUNOLOGY; METABOLISM; NERVE DEGENERATION; SECRETION;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; BRAIN; CELL LINE; CEREBRAL PALSY; DISEASE MODELS, ANIMAL; FEMALE; HISTAMINE; HISTAMINE ANTAGONISTS; INTERLEUKIN-9; MALE; MAST CELLS; MICE; MICE, INBRED C57BL; NERVE DEGENERATION; NEURONS; NEUROTOXINS; RECEPTORS, HISTAMINE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 11844254514     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2004.09.018     Document Type: Article

References (45)

1. L. Acarin, B. Gonzalez, J. Hidalgo, A.J. Castro, and B. Castellano Primary cortical glial reaction versus secondary thalamic glial response in the excitotoxically injured young brain: astroglial response and metallothionein expression Neuroscience 92 1999 827 839
2. D.R. Brown Dependence of neurones on astrocytes in a coculture system renders neurones sensitive to transforming growth factor beta1-induced glutamate toxicity J. Neurochem. 72 1999 943 953
3. R.E. Brown, D.R. Stevens, and H.L. Haas The physiology of brain histamine Prog. Neurobiol. 63 2001 637 672
4. V. Dimitriadou, A. Rouleau, M.D. Tuong, X. Ligneau, G.F. Newlands, H.R. Miller, J.C. Schwartz, and M. Garbarg Rat cerebral mast cells undergo phenotypic changes during development Brain Res., Dev. Brain Res. 97 1996 29 41
5. K.C. Dines, and H.C. Powell Mast cell interactions with the nervous system: relationship to mechanisms of disease J. Neuropathol. Exp. Neurol. 56 1997 627 640
6. F. Docagne, O. Nicole, C. Gabriel, M. Fernandez-Monreal, S. Lesne, C. Ali, L. Plawinski, P. Carmeliet, E.T. MacKenzie, A. Buisson, and D. Vivien Smad3-dependent induction of plasminogen activator inhibitor-1 in astrocytes mediates neuroprotective activity of transforming growth factor-beta 1 against NMDA-induced necrosis Mol. Cell. Neurosci. 21 2002 634 644
7. M.A. Dommergues, J. Patkai, J.C. Renauld, P. Evrard, and P. Gressens Proinflammatory cytokines and interleukin-9 exacerbate excitotoxic lesions of the newborn murine neopallium Ann. Neurol. 47 2000 54 63
8. J.J. Dropp Mast cells in mammalian brain Acta Anat. (Basel) 94 1976 1 21
9. P.L. Follett, P.A. Rosenberg, J.J. Volpe, and F.E. Jensen NBQX attenuates excitotoxic injury in developing white matter J. Neurosci. 20 2000 9235 9241
10. J.R. Gordon, P.R. Burd, and S.J. Galli Mast cells as a source of multifunctional cytokines Immunol. Today 11 1990 458 464
11. P. Gressens, S. Marret, J.M. Hill, D.E. Brenneman, I. Gozes, M. Fridkin, and P. Evrard Vasoactive intestinal peptide prevents excitotoxic cell death in the murine developing brain J. Clin. Invest. 100 1997 390 397
12. B.L. Gruber, M.J. Marchese, and R.R. Kew Transforming growth factor-beta 1 mediates mast cell chemotaxis J. Immunol. 152 1994 5860 5867
13. B. Hagberg, and G. Hagberg The changing panorama of cerebral palsy-bilateral spastic forms in particular Acta Paediatr., Suppl. 416 1996 48 52
14. M. Haimart, J.M. Launay, G. Zurcher, N. Cauet, C. Dreux, and M. Da Prada Simultaneous determination of histamine and N alpha-methylhistamine in biological samples by an improved enzymatic single isotope assay Agents Actions 16 1985 71 75
15. T.W. Ho, L.A. Bristol, C. Coccia, Y. Li, J. Milbrandt, E. Johnson, L. Jin, O. Bar-Peled, J.W. Griffin, and J.D. Rothstein TGFbeta trophic factors differentially modulate motor axon outgrowth and protection from excitotoxicity Exp. Neurol. 161 2000 664 675
16. I. Husson, B. Mesples, P. Bac, J. Vamecq, P. Evrard, and P. Gressens Melatoninergic neuroprotection of the murine periventricular white matter against neonatal excitotoxic challenge Ann. Neurol. 51 2002 82 92
17. M.D. Johnson, M.T. Jennings, L.I. Gold, and H.L. Moses Transforming growth factor-beta in neural embryogenesis and neoplasia Hum. Pathol. 24 1993 457 462
18. S.U. Kim Cytokine networks in human CNS identified in cultured human neurons, astrocytes and microglia Ann. Neurol. 42 1997 424
19. K. Krieglstein, S. Richter, L. Farkas, N. Schuster, N. Dunker, R.W. Oppenheim, and K. Unsicker Reduction of endogenous transforming growth factors beta prevents ontogenetic neuron death Nat. Neurosci. 3 2000 1085 1090
20. V. Laudenbach, G. Calo, R. Guerrini, G. Lamboley, J.F. Benoist, P. Evrard, and P. Gressens Nociceptin/orphanin FQ exacerbates excitotoxic white-matter lesions in the murine neonatal brain J. Clin. Invest. 107 2001 457 466
21. V. Laudenbach, F. Medja, M. Zoli, F.M. Rossi, P. Evrard, J.P. Changeux, and P. Gressens Selective activation of central subtypes of the nicotinic acetylcholine receptor has opposite effects on neonatal excitotoxic brain injuries FASEB J. 16 2002 423 425
22. E. Lehrmann, R. Kiefer, T. Christensen, K.V. Toyka, J. Zimmer, N.H. Diemer, H.P. Hartung, and B. Finsen Microglia and macrophages are major sources of locally produced transforming growth factor-beta1 after transient middle cerebral artery occlusion in rats Glia 24 1998 437 448
23. K.A. Lindstedt, Y. Wang, N. Shiota, J. Saarinen, M. Hyytiainen, J.O. Kokkonen, J. Keski-Oja, and P.T. Kovanen Activation of paracrine TGF-beta1 signaling upon stimulation and degranulation of rat serosal mast cells: a novel function for chymase FASEB J. 15 2001 1377 1388
24. A. Logan, M. Berry, A.M. Gonzalez, S.A. Frautschy, M.B. Sporn, and A. Baird Effects of transforming growth factor beta 1 on scar production in the injured central nervous system of the rat Eur. J. Neurosci. 6 1994 355 363
25. A. Logan, C. Smith, G.P. Becks, A.M. Gonzalez, I.D. Phillips, and D.J. Hill Enhanced expression of transforming growth factor-beta 1 during thyroid hyperplasia in rats J. Endocrinol. 141 1994 45 57
26. S. Marret, R. Mukendi, J.F. Gadisseux, P. Gressens, and P. Evrard Effect of ibotenate on brain development: an excitotoxic mouse model of microgyria and posthypoxic-like lesions J. Neuropathol. Exp. Neurol. 54 1995 358 370
27. E. Martinez, R. Figueroa, D. Garry, P. Visintainer, K. Patel, U. Verma, P.B. Sehgal, and N. Tejani Elevated amniotic fluid interleukin-6 as a predictor of neonatal periventricular leukomalacia and intraventricular hemorrhage J. Matern.-Fetal Investig. 8 1998 101 107
28. M.F. Mehler, R. Rozental, M. Dougherty, D.C. Spray, and J.A. Kessler Cytokine regulation of neuronal differentiation of hippocampal progenitor cells Nature 362 1993 62 65
29. M.F. Mehler, P.C. Mabie, D. Zhang, and J.A. Kessler Bone morphogenetic proteins in the nervous system Trends Neurosci. 20 1997 309 317
30. H.R. Miller, S.H. Wright, P.A. Knight, and E.M. Thornton A novel function for transforming growth factor-beta1: up-regulation of the expression and the IgE-independent extracellular release of a mucosal mast cell granule-specific beta-chymase, mouse mast cell protease-1 Blood 93 1999 3473 3486
31. K.B. Nelson, J.M. Dambrosia, J.K. Grether, and T.M. Phillips Neonatal cytokines and coagulation factors in children with cerebral palsy Ann. Neurol. 44 1998 665 675
32. N. Olsson, E. Piek, M. Sundstrom, P. ten Dijke, and G. Nilsson Transforming growth factor-beta-mediated mast cell migration depends on mitogen-activated protein kinase activity Cell Signalling 13 2001 483 490
33. J. Patkai, B. Mesples, M.A. Dommergues, G. Fromont, E.M. Thornton, J.C. Renauld, P. Evrard, and P. Gressens Deleterious effects of IL-9-activated mast cells and neuroprotection by antihistamine drugs in the developing mouse brain Pediatr. Res. 50 2001 222 230
34. M. Pilartz, T. Jess, D. Indefrei, and J.M. Schroder Adoptive transfer-experimental allergic neuritis in newborn Lewis rats results in inflammatory infiltrates, mast cell activation, and increased Ia expression with only minor nerve fiber degeneration Acta Neuropathol. (Berlin) 104 2002 513 524
35. J.H. Prehn, and J. Krieglstein Opposing effects of transforming growth factor-beta 1 on glutamate neurotoxicity Neuroscience 60 1994 7 10
36. J.H. Prehn, and R.J. Miller Opposite effects of TGF-beta 1 on rapidly- and slowly-triggered excitotoxic injury Neuropharmacology 35 1996 249 256
37. M. Robbie-Ryan, and M. Brown The role of mast cells in allergy and autoimmunity Curr. Opin. Immunol. 14 2002 728 733
38. A. Ruocco, O. Nicole, F. Docagne, C. Ali, L. Chazalviel, S. Komesli, F. Yablonsky, S. Roussel, E.T. MacKenzie, D. Vivien, and A. Buisson A transforming growth factor-beta antagonist unmasks the neuroprotective role of this endogenous cytokine in excitotoxic and ischemic brain injury J. Cereb. Blood Flow Metab. 19 1999 1345 1353
39. R. Silver, A.J. Silverman, L. Vitkovic, and I.I. Lederhendler Mast cells in the brain: evidence and functional significance Trends Neurosci. 19 1996 25 31
40. S.L. Tahraoui, S. Marret, C. Bodenant, P. Leroux, M.A. Dommergues, P. Evrard, and P. Gressens Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter Brain Pathol. 11 2001 56 71
41. M. Tsai, T. Takeishi, H. Thompson, K.E. Langley, K.M. Zsebo, D.D. Metcalfe, E.N. Geissler, and S.J. Galli Induction of mast cell proliferation, maturation, and heparin synthesis by the rat c-kit ligand, stem cell factor Proc. Natl. Acad. Sci. U. S. A. 88 1991 6382 6386
42. B.H. Yoon, R. Romero, S.H. Yang, J.K. Jun, I.O. Kim, J.H. Choi, and H.C. Syn Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia Am. J. Obstet. Gynecol. 174 1996 1433 1440
43. B.H. Yoon, J.K. Jun, R. Romero, K.H. Park, R. Gomez, J.H. Choi, and I.O. Kim Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1beta, and tumor necrosis factor-alpha), neonatal brain white matter lesions, and cerebral palsy Am. J. Obstet. Gynecol. 177 1997 19 26
44. J.P. Zappulla, M. Arock, L.T. Mars, and R.S. Liblau Mast cells: new targets for multiple sclerosis therapy? J. Neuroimmunol. 131 2002 5 20
45. X. Zhuang, A.J. Silverman, and R. Silver Distribution and local differentiation of mast cells in the parenchyma of the forebrain J. Comp. Neurol. 408 1999 477 488