Tumor necrosis factor p55 and p75 receptors are involved in chemical-induced apoptosis of dentate granule neurons

Journal of Neurochemistry

Volumn 106, Issue 1, 2008, Pages 281-298

  Harry, G Jean ^a   Lefebvre D'Hellencourt, Christian ^a,b   McPherson, Christopher A ^a   Funk, Jason A ^a   Aoyama, Mineyoshi ^a,c   Wine, Robert N ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b UNIVERSITÉ DE LA RÉUNION   (France)

^c NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

Apoptosis; Hippocampus; Microglia; Neuroinflammation; Trimethyltin; Tumor necrosis factor

Indexed keywords

BIOTIN; CASPASE 3; CASPASE 8; DNA NUCLEOTIDYLEXOTRANSFERASE; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; PROTEIN P55; PROTEIN P75; TRANSFORMING GROWTH FACTOR BETA1; TRIMETHYLTIN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INJURY; CELL DAMAGE; CONTROLLED STUDY; DENTATE NUCLEUS; GRANULE CELL; HIPPOCAMPUS; IMMUNOREACTIVITY; MALE; MICROGLIA; MOUSE; NERVE CELL LESION; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CYTOKINES; DENTATE GYRUS; ENDOCYTOSIS; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; NERVE DEGENERATION; NEURONS; NEUROTOXINS; RECEPTORS, NERVE GROWTH FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; TRIMETHYLTIN COMPOUNDS;

MUS;

EID: 45249110462     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05382.x     Document Type: Article

References (66)

1. Badie B., Schartner J., Vorpahl J. Preston K. (2000) Interferon-gamma induces apoptosis and augments the expression of Fas and Fas ligand by microglia in vitro. Exp. Neurol. 162, 290 296.
2. Bechmann I., Mor G., Nilsen J., Eliza M., Nitsch R. Naftolin F. (1999) FasL (CD95L, Apo1L) is expressed in the normal rat and human brain: evidence for the existence of an immunological brain barrier. Glia 27, 62 74.
3. Bohatschek M., Kloss C. U. A., Hristova M., Pfeffer K. Raivich G. (2004) Microglial major histocompatibility complex glycoprotein-1 in the axotomized facial motor nucleus: regulation and role of tumor necrosis factor receptors 1 and 2. J. Comp. Neurol. 470, 382 399.
4. Boldin M. P., Varfolomeev E. E., Pancer Z., Mett I. L., Camonis J. H. Wallach D. (1995) A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain. J. Biol. Chem. 270, 7795 7798.
5. Botchkina G. I., Meistrell M. E., Botchkina I. L. Tracey K. J. (1997) Expression of TNF and TNF receptors (p55 and p75) in the rat brain after focal cerebral ischemia. Mol. Med. 3, 765 781.
6. Bruccoleri A. Harry G. J. (2000) Chemical-induced hippocampal neurodegeneration and elevations in TNFα, TNFβ, IL-1β, IP-10, and MCP-1 mRNA in osteopetrotic (op/op) mice. J. Neurosci. Res. 62, 146 155.
7. Bruccoleri A., Brown H. Harry G. J. (1998) Cellular localization and temporal elevation of tumor necrosis factor-alpha, interleukin-1 alpha, and transforming growth factor-beta 1 mRNA in hippocampal injury response induced by trimethyltin. J. Neurochem. 71, 1577 1587.
8. Bruce A. J., Boling W., Kindy M. S., Peschon J., Kraemer P. J., Carpenter M. K., Holtsberg F. W. Mattson M. P. (1996) Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat. Med. 2, 788 794.
9. Buckley C. A., Rouhani F. N., Kaler M., Adamic B., Hawari F. I. Levine S. T. (2005) Amino-terminal TACE prodomain attenuates TNFR2 cleavage independently of the cysteine switch. Am. J. Physiol. Lung Cell Mol. Physiol. 288, L1132 L1138.
10. Chan F. K. Lenardo M. J. (2000) A crucial role for p80 TNF-R2 in amplifying p60 TNF-R1 apoptosis signals in T lymphocytes. Eur. J. Immunol. 30, 652 660.
11. Cheema Z. F., Santillano D. R., Wade S. B., Newman J. M. Miranda R. C. (2004) The extracellular matrix, p53 and estrogen compete to regulate cell-surface Fas/Apo-1 suicide receptor expression in proliferating embryonic cerebral cortical precursors, and reciprocally, Fas-ligand modifies estrogen control of cell-cycle proteins. BMC Neurosci. 5, 11.
12. Chinnaiyan A. M., O'Rourke K., Tewari M. Dixit V. M. (1995) FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81, 505 512.
13. Declerecq W., Denecker G., Fiers W. Vandenabeele P. (1998) Cooperation of both TNF receptors in inducing apoptosis: involvement of the TNF receptor-associated factor binding domain of the TNF receptor 75. J. Immunol. 161, 390 399.
14. Dopp J. M., Mackenzie-Graham A., Otero G. C. Merrill J. E. (1997) Differential expression, cytokine modulation, and specific functions of type-1 and type-2 tumor necrosis factor receptors in rat glia. J. Neuroimmunol. 75, 104 112.
15. Eskes C., Juillerat-Jeanneret L., Leuba G., Honegger P. Monnet-Tschudi F. (2003) Involvement of microglia-neuron interactions in the tumor necrosis factor-alpha release, microglial activation, and neurodegeneration induced by trimethyltin. J. Neurosci. Res. 71, 583 590.
16. Fenger C., Drojdahl N., Wirenfeldt M., Sylvest L., Jorgensen O. S., Meldgaard M., Lambertsen K. L. Finsen B. (2006) Tumor necrosis factor and its p55 and p75 receptors are not required for axonal lesion-induced microgliosis in mouse facia dentate. Glia 54, 591 605.
17. Fiedorowicz A., Figiel I., Kaminska B., Zaremba M., Wilk S. Oderfeld-Nowak B. (2001) Dentate granule neuron apoptosis and glia activation in murine hippocampus induced by trimethyltin exposure. Brain Res. 912, 116 127.
18. Fotin-Mleczek M., Henkler F., Samel D., Reichwein M., Hausser A., Parmryd I., Scheurich P., Schmid J. A. Wajant H. (2002) Apoptotic crosstalk of TNF receptors: TNF-R2 induces depletion of TRAF2 and IAP proteins and accelerated TNF-R1-dependent activation of caspase 8. J. Cell Sci. 115, 2757 2770.
19. Gary D. S., Bruce-Keller A. J., Kindy M. S. Mattson M. P. (1998) Ischemic and excitotoxic brain injury is enhanced in mice lacking the p55 tumor necrosis factor receptor. J. Cereb. Blood Flow Metab. 18, 1283 1287.
20. Glynn M. W. McAllister A. K. (2006) Immunocytochemistry and quantification of protein colocalization in cultured neurons. Nat. Protoc. 1, 1287 1296.
21. Gregersen R., Lambertsen K. Finsen B. (2000) Microglia and macrophages are the major source of tumor necrosis factor in permanent middle cerebral artery occlusion in mice. J. Cereb. Blood Flow Metab. 20, 53 65.
22. Grell M., Wajant H., Zimmermann G. Scheurich P. (1998) The type 1 receptor (CD120a) is the high-affinity receptor for soluble tumor necrosis factor. Proc. Natl Acad. Sci. USA 95, 570 575.
23. Hanisch U.-W. (2002) Microglia as a source and target of cytokines. Glia 40, 140 155.
24. Harry G. J., Tyler K., Lefevbvre d'Hellencourt C., Tilson H. A. Maier W. E. (2002) Morphological alterations and elevations in tumor necrosis factor-alpha, interleukin (IL-1alpha, and IL-6 in mixed glia cultures following exposure to trimethyltin: modulation by proinflammatory cytokine recombinant proteins and neutralizing antibodies. Toxicol. Appl. Pharmacol. 180, 205 218.
25. Harry G. J., Bruccoleri A. Lefebvre d'Hellencourt C. (2003) Differential modulation of hippocampal chemical-induced injury response by ebselen, pentoxifylline, and TNFα-, IL-1α-, and IL-6-neutralizing antibodies. J. Neurosci. Res. 73, 526 536.
26. Henshall D. C. Simon R. P. (2005) Epilepsy and apoptosis pathways. J. Cereb. Blood Flow Metab. 25, 1557 1572.
27. Hsu H., Shu H. B., Pan M. G. Goeddel D. V. (1996) TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84, 299 308.
28. Jones S. J., Ledgerwood E. C., Prins J. B., Galbraith J., Johnson D. R., Pober J. S. Bradley J. R. (1999) TNF recruits TRADD to the plasma membrane but not the trans-Golgi network, the principal subcellular location of TNF-R1. J. Immunol. 162, 1042 1048.
29. Kassed C. A., Butler T. L., Patton G. W., Demesquita D. D., Navidomskis M. T., Memet S., Israel A. Pennypacker K. R. (2004) Injury-induced NF-kappaB activation in the hippocampus: implications for neuronal survival. FASEB J. 18, 723 724.
30. Kinouchi K., Brown G., Pasternak G. Donner D. B. (1991) Identification and characterization of receptors for tumor necrosis factor-alpha in the brain. Biochem. Biophys. Res. Commun. 181, 1532 1538.
31. Kischkel F. C., Helbardt S., Behrmann I., Germer M., Pawlita M., Krammer P. H. Peter M. E. (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J. 14, 5579 5588.
32. Kohno T., Brewer M. T., Baker S. L., Schwartz P. E., King M. W., Hale K. K., Squires C. H., Thompson R. C. Vannice J. L. (1990) A second tumor necrosis factor receptor gene product can shed a naturally occurring tumor necrosis factor inhibitor. Proc. Natl Acad. Sci. USA 87, 8331 8335.
33. Krammer P. H. (2000) CD95's deadly mission in the immune system. Nature 407, 789 795.
34. Lambertsen K. L., Clausen B. H., Fenger C., Wulf H., Owens T., Dagnaes-Hansen F., Meldgaard M. Finsen B. (2007) Microglia and macrophages express tumor necrosis factor receptor p75 following middle cerebral artery occlusion in mice. Neuroscience 144, 934 949.
35. Lefebvre d'Hellencourt C. Harry G. J. (2005) Molecular profiles of mRNA levels in laser capture microdissected murine hippocampal regions differentially responsive to TMT-induced cell death. J. Neurochem. 93, 206 220.
36. Liu Z.-G., Hsu H., Goeddel D. V. Karin M. (1996) Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell 87, 565 576.
37. Martin-Villalba A., Hahne M., Kleber S., Vogel J., Falk W., Schenkel J. Krammer P. H. (2001) Therapeutic neutralization of CD95-ligand and TNF attenuates brain damage in stroke. Cell Death Diff. 8, 679 686.
38. Micheau O. Tschopp J. (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181 190.
39. Micheau O., Lens S., Gaide O., Alevizopoulos K. Tschopp J. (2001) NF-kappaB signals induce the expression of c-FLIP. Mol. Cell. Biol. 21, 5299 5305.
40. Muppidi J. R., Tschopp J. Siegel R. M. (2004) Life and death decisions: secondary complexes and lipid rafts in TNF receptor family signal transduction. Immunity 21, 461 465.
41. Ogita K., Nitta Y., Watanabe M., Nakatani Y., Nishiyama N., Sugiyama C. Yoneda Y. (2004) In vivo activation of c-Jun N-terminal kinase signaling cascade prior to granule cell death induced by trimethyltin in the dentate gyrus of mice. Neuropharmacology 47, 619 630.
42. Peschon J. J., Torrance D. S., Stocking K. L., Glaccum M. B., Otten C., Willis C. R., Charrier K., Morrissey P. J., Ware C. B. Mohler K. M. (1998) TNF receptor-deficient mice reveal divergent roles for p55 and p75 in several models of inflammation. J. Immunol. 160, 943 952.
43. Quintana A., Giralt M., Rojas S., Penkowa M., Campbell I. L., Hidalgo J. Molinero A. (2005) Differential role of tumor necrosis factor receptors in mouse brain inflammatory responses in cryolesion brain injury. J. Neurosci. Res. 82, 701 716.
44. Raivich G., Liu Z. Q., Kloss C. U., Labow M., Bluethmann H. Bohatschek M. (2002) Cytotoxic potential of proinflammatory cytokines: combined deletion of TNF receptors TNFR1 and TNFR2 prevents motoneuron cell death after facial axotomy in adult mouse. Exp. Neurol. 178, 186 193.
45. Rath P. C. Aggarwal B. B. (1999) TNF-induced signaling in apoptosis. J. Clin. Immunol. 19, 350 364.
46. Sairanen T. R., Lindsberg P. J., Brenner M., Carpen O. Siren A.-L. (2001) Differential cellular expression of tumor necrosis factor-α and type I tumor necrosis factor receptor after transient global forebrain ischemia. J. Neurological Sci. 186, 87 99.
47. Schneider-Brachert W., Tchikov V., Neumeyer J. et al. (2004) Compartmentalization of TNF receptor 1 signaling: internalized TNF receptosomes as death signaling vesicles. Immunity 21, 415 428.
48. Shen Y., Li R. Shiosaki K. (1997) Inhibition of p75 tumor necrosis factor receptor by antisense oligonucleotides increases hypoxic injury and beta-amyloid toxicity in human neuronal cell line. J. Biol. Chem. 272, 3550 3553.
49. Shinoda S., Skradski S. L., Araki T., Schindler C. K., Meller R., Lan J.-Q., Taki W., Simon R. P. Henshall D. C. (2003) Formation of a tumour necrosis factor receptor 1 molecular scaffolding complex and activation of apoptosis signal-regulating kinase 1 during seizure-induced neuronal death. Eur. J. Neurosci. 17, 2065 2076.
50. Shohami E., Ginis I. Hallenbeck J. M. (1999) Dual role of tumor necrosis factor alpha in brain injury. Cytokine Growth Factor Rev. 10, 119 130.
51. Sriram K., Matheson J. M., Benkovic S. A., Miller D. B., Luster M. I. O'Callaghan J. P. (2006) Deficiency of TNF receptors suppresses microglial activation and alters the susceptibility of brain regions to MPTP-induced neurotoxicity: role of TNF-α. FASEB J. 20, 670 682.
52. Sullivan P. G., Bruce-Keller A. J., Rabchevsky A. G., Christakos S. Clair. D. K., Mattson M. P. Scheff S. W. (1999) Exacerbation of damage and altered NF-kappaB activation in mice lacking tumor necrosis factor receptors after traumatic brain injury. J. Neurosci. 19, 6248 6256.
53. Suvannavejh G. C., Lee H. O., Padilla J., Dal Canto M. C., Barrett T. A. Miller S. D. (2000) Divergent roles for p55 and p75 tumor necrosis factor receptors in the pathogenesis of MOG(35-55)-induced experimental autoimmune encephalomyelitis. Cell Immunol. 205, 24 33.
54. Tan Z., Levid J. Schreiber S. S. (2001) Increased expression of Fas (CD95/APO-1) in adult rat brain after kainate-induced seizures. Neuroreport 12, 1979 1982.
55. Taoufik E., Valable S., Muller G. J. et al. (2007) FLIP(L) protects neurons against in vivo ischemia and in vitro glucose deprivation-induced cell death. J. Neurosci. 27, 6633 6646.
56. Tartaglia L. A. Goeddel D. V. (1992) Two TNF receptors. Immunol. Today 13, 151 153.
57. Taylor D. L., Jones F., Kubota E. S. Pocock J. M. (2005) Stimulation of microglia metabotropic glutamate receptor mGlu2 triggers tumor necrosis factor α-induced neurotoxicity in concert with microglial-derived fas ligand. J. Neurosci. 25, 2945 2964.
58. Tchelingerian J. L., Le Saux F. Jacque C. (1996) Identification and topography of neuronal cell populations expressing TNFα and IL-1α in response to hippocampal lesion. J. Neurosci. Res. 43, 99 106.
59. Vandenabeele P., Declercq W., Beyaert R. Fiers W. (1995) Two tumour necrosis factor receptors: structure and function. Trends Cell Biol. 5, 392 399.
60. Waetzig V. Herdegen T. (2004) Neurodegenerative and physiological actions of c-Jun N-terminal kinases in the mammalian brain. Neurosci. Lett. 361, 64 67.
61. Wajant H., Henkler F. Scheurich P. (2001) The TNF-receptor-associated factor family: scaffold molecules for cytokine receptors, kinases and their regulators. Cell Signal. 13, 389 400.
62. Wajant H., Pfizenmaier K. Scheurich P. (2003) Tumor necrosis factor signaling. Cell Death Differ. 10, 45 65.
63. Wang H. D., Fukuda T., Suzuki T., Hashimoto K., Liou S. Y., Momoi T., Kosaka T., Yamamoto K. Nakanishi H. (1999) Differential effects of Bcl-2 overexpression on hippocampal CA1 neurons and dentate granule cells following hypoxic ischemia in adult mice. J. Neurosci. Res. 57, 1 12.
64. Weiss T., Grell M., Hessabi B., Bourteele S., Müller G., Scheurich P. Wajant H. (1997) Enhancement of the TNF receptor p60-mediated cytotoxicity by TNF receptor p80. Requirement of the TNF receptor-associated factor-2 binding site. J. Immunol. 158, 2398 2404.
65. Yang L., Lindholm K., Konishi Y., Li R. Shen Y. (2002) Target depletion of distinct tumor necrosis factor receptor subtypes reveals hippocampal neuron death and survival through different signal transduction pathways. J. Neurosci. 22, 3025 3032.
66. Yin L., Ohtaki H., Nakamachi T., Kudo Y., Makino R. Shioda S. (2004) Delayed expressed TNFR1 co-localized with ICAM-1 in astrocyte in mice brain after transient focal ischemia. Neurosci. Lett. 370, 30 35.