NF-κB p50/RelA and c-Rel-containing dimers: Opposite regulators of neuron vulnerability to ischaemia

Journal of Neurochemistry

Volumn 108, Issue 2, 2009, Pages 475-485

  Sarnico, Ilenia ^b   Lanzillotta, Annamaria ^b   Boroni, Flora ^b   Benarese, Marina ^b   Alghisi, Manuela ^b   Schwaninger, Markus ^c   Inta, Ioana ^c   Battistin, Leontino ^d   Spano, PierFranco ^b,e   Pizzi, Marina ^a,b,e  

^a Division of Pharmacology   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d IRCCS SAN CAMILLO HOSPITAL   (Italy)

^e National Institute of Neuroscience   (Italy)

Author keywords

Bcl xL; Brain ischaemia; c Rel; Primary cortical neurons; RelA; SK N SH

Indexed keywords

DIMER; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OXYGEN; PROTEIN BCL XL; TRANSCRIPTION FACTOR REL; BCL2L1 PROTEIN, MOUSE; PROTEIN BCL X; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIM GENE; BRAIN HYPOXIA; BRAIN ISCHEMIA; CONTROLLED STUDY; GENE; GENE CONTROL; GENE EXPRESSION; NERVE CELL; NEUROPROTECTION; NONHUMAN; NOXA GENE; PERIKARYON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN TARGETING; ANIMAL; ANIMAL EMBRYO; ANOXIA; C57BL MOUSE; CELL CULTURE; CELL SURVIVAL; CEREBRAL ARTERY DISEASE; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HUMAN; IMMUNOPRECIPITATION; METABOLISM; METHODOLOGY; MOUSE; NEUROBLASTOMA; NICK END LABELING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

MUS;

ANIMALS; ANOXIA; BCL-X PROTEIN; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; IMMUNOPRECIPITATION; IN SITU NICK-END LABELING; INFARCTION, MIDDLE CEREBRAL ARTERY; MICE; MICE, INBRED C57BL; NEUROBLASTOMA; NEURONS; NF-KAPPA B P50 SUBUNIT; PROTO-ONCOGENE PROTEINS C-REL; RNA, SMALL INTERFERING; TRANSCRIPTION FACTOR RELA; TRANSFECTION;

EID: 57549112366     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05783.x     Document Type: Article

References (51)

1. Ahn H. J., Hernandez C. M., Levenson J. M., Lubin F. D., Liou H. C. Sweatt J. D. (2008) c-Rel, an NF-kappaB family transcription factor, is required for hippocampal long-term synaptic plasticity and memory formation. Learn Mem. 15, 539 549.
2. Bakalkin G. Y., Yakovleva T. Terenius L. (1993) NF-kappa B-like factors in the murine brain. Developmentally-regulated and tissue-specific expression. Brain Res. Mol. Brain Res. 20, 137 146.
3. Banerjee A., Grumont R., Gugasyan R., White C., Strasser A. Gerondakis S. (2008) NF-{kappa}B1 and c-Rel cooperate to promote the survival of TLR4 activated B cells by neutralizing Bim via distinct mechanisms. Blood [Epub ahead of print] doi :.
4. Bhakar A. L., Tannis L. L., Zeindler C., Russo M. P., Jobin C., Park D. S., MacPherson S. Barker P. A. (2002) Constitutive nuclear factor-kappa B activity is required for central neuron survival. J. Neurosci. 22, 8466 8475.
5. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P. Lipton S. A. (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl Acad. Sci. USA 92, 7162 7166.
6. Campbell K. J. Perkins N. D. (2004) Reprogramming RelA. Cell Cycle 3, 869 872 (Review).
7. Campbell K. J., Rocha S. Perkins N. D. (2004) Active repression of antiapoptotic gene expression by RelA(p65) NF-kappa B. Mol. Cell 13, 853 865.
8. Cao G., Pei W., Ge H., Liang Q., Luo Y., Sharp F. R., Lu A., Ran R., Graham S. H. Chen J. (2002) In vivo delivery of a Bcl-xL fusion protein containing the TAT protein transduction domain protects against ischemic brain injury and neuronal apoptosis. J. Neurosci. 22, 5423 5431.
9. Chen C., Edelstein L. C. Gelinas C. (2000) The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol. Cell. Biol. 20, 2687 2695.
10. Chen M., Guerrero A. D., Huang L., Shabier Z., Pan M., Tan T. H. Wang J. (2007) Caspase-9-induced mitochondrial disruption through cleavage of anti-apoptotic BCL-2 family members. J. Biol. Chem. 282, 33888 33895.
11. Clemens J. A., Stephenson D. T., Smalstig E. B., Dixon E. P. Little S. P. (1997) Global ischemia activates nuclear factor-kappa B in forebrain neurons of rats. Stroke 28, 1073 1080.
12. Crack P. J., Taylor J. M., Ali U., Mansell A. Hertzog P. J. (2006) Potential contribution of NF-kappaB in neuronal cell death in the glutathione peroxidase-1 knockout mouse in response to ischemia-reperfusion injury. Stroke 37, 1533 1538.
13. Crenon I., Beraud C., Simard P., Montagne J., Veschambre P. Jalinot P. (1993) The transcriptionally active factors mediating the effect of the HTLV-I Tax transactivator on the IL-2R alpha kappa B enhancer include the product of the c-rel proto-oncogene. Oncogene 8, 867 875.
14. Dong Q. G., Sclabas G. M., Fujioka S. et al. (2002) The function of multiple IkappaB: NF-kappaB complexes in the resistance of cancer cells to taxol-induced apoptosis. Oncogene 21, 6510 6519.
15. Gillardon F., Lenz C., Waschke K. F., Krajewski S., Reed J. C., Zimmermann M. Kuschinsky W. (1996) Altered expression of Bcl-2, Bcl-X, Bax, and c-Fos colocalizes with DNA fragmentation and ischemic cell damage following middle cerebral artery occlusion in rats. Brain Res. Mol. Brain Res. 40, 254 260.
16. Graham S. H. Chen J. (2001) Programmed cell death in cerebral ischemia. J. Cereb. Blood Flow Metab. 21, 99 109.
17. Grilli M., Pizzi M., Memo M. Spano P. (1996) Neuroprotection by aspirin and sodium salicylate through blockade of NF-kappaB activation. Science 274, 1383 1385.
18. Herrmann O., Tarabin V., Suzuki S. et al. (2003) Regulation of body temperature and neuroprotection by endogenous interleukin-6 in cerebral ischemia. J. Cereb. Blood Flow Metab. 23, 406 415.
19. Herrmann O., Baumann B., de Lorenzi R. et al. (2005) IKK mediates ischemia-induced neuronal death. Nat. Med. 11, 1322 1329.
20. Hoffmann A., Leung T. H. Baltimore D. (2003) Genetic analysis of NF-kappaB/Rel transcription factors defines functional specificities. EMBO J. 22, 5530 5539.
21. Inta I., Paxian S., Zhang W. et al. (2006) Bim and Noxa are candidates to mediate the deleterious effect of the NF-κB subunit RelA in cerebral ischemia. J. Neurosci. 26, 12896 12903.
22. Kaltschmidt B., Uherek M., Wellmann H., Volk B. Kaltschmidt C. (1999) Inhibition of NF-kappaB potentiates amyloid beta-mediated neuronal apoptosis. Proc. Natl Acad. Sci. USA 96, 9409 9414.
23. Kirito K., Watanabe T., Sawada K., Endo H., Ozawa K. Komatsu N. (2002) Thrombopoietin regulates Bcl-xL gene expression through Stat5 and phosphatidylinositol 3-kinase activation pathways. J. Biol. Chem. 277, 8329 8337.
24. Kögel D., Peters M., König H. G., Hashemi S. M., Bui N. T., Arolt V., Rothermundt M. Prehn J. H. (2004) S100B potently activates p65/c-Rel transcriptional complexes in hippocampal neurons: clinical implications for the role of S100B in excitotoxic brain injury. Neuroscience 127, 913 920.
25. Kuwana T., Bouchier-Hayes L., Chipuk J. E., Bonzon C., Sullivan B. A., Green D. R. Newmeyer D. D. (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell 17, 525 535.
26. Levenson J. M., Choi S., Lee S. Y., Cao Y. A., Ahn H. J., Worley K. C., Pizzi M., Liou H. C. Sweatt J. D. (2004) A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-rel. J. Neurosci. 24, 3933 3943.
27. Mattson M. P. Camandola S. (2001) NF-kappaB in neuronal plasticity and neurodegenerative disorders. J. Clin. Invest. 107, 247 254.
28. Mattson M. P. Meffert M. K. (2006) Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ. 13, 852 860.
29. Meffert M. K. Baltimore D. (2005) Physiological functions for brain NF-κB. Trends Neurosci. 28, 37 43.
30. Meffert M. K., Chang J. M., Wiltgen B. J., Fanselow M. S. Baltimore D. (2003) NF-kappa B functions in synaptic signaling and behavior. Nat. Neurosci. 6, 1072 1078.
31. Miyawaki T., Mashiko T., Ofengeim D., Flannery R. J., Noh K. M., Fujisawa S., Bonanni L., Bennett M. V., Zukin R. S. Jonas E. A. (2008) Ischemic preconditioning blocks BAD translocation, Bcl-xL cleavage, and large channel activity in mitochondria of postischemic hippocampal neurons. Proc. Natl Acad. Sci. USA 105, 4892 4897.
32. Movsesyan V. A., Stoica B. A. Faden A. I. (2004) MGLuR5 activation reduces beta-amyloid-induced cell death in primary neuronal cultures and attenuates translocation of cytochrome c and apoptosis-inducing factor. J. Neurochem. 89, 1528 1536.
33. Nurmi A., Lindsberg P. J., Koistinaho M., Zhang W., Juettler E., Karjalainen-Lindsberg M. L., Weih F., Frank N., Schwaninger M. Koistinaho J. (2004) Nuclear factor-kappaB contributes to infarction after permanent focal ischemia. Stroke 35, 987 991.
34. O'Neill L. A. Kaltschmidt C. (1997) NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci. 20, 252 258.
35. O'Riordan K. J., Huang I. C., Pizzi M. et al. (2006) Regulation of nuclear factor kappaB in the hippocampus by group I metabotropic glutamate receptors. J. Neurosci. 26, 4870 4879.
36. Pizzi M. Spano P. (2006) Distinct roles of diverse nuclear factor-kappaB complexes in neuropathological mechanisms. Eur. J. Pharmacol. 545, 22 28. Review.
37. Pizzi M., Boroni F., Bianchetti A., Moraitis C., Sarnico I., Benarese M., Goffi F., Valerio A. Spano P. (2002a) Expression of functional NR1/NR2B-type NMDA receptors in neuronally differentiated SK-N-SH human cell line. Eur. J. Neurosci. 16, 2342 2350.
38. Pizzi M., Goffi F., Boroni F., Benarese M., Perkins S. E., Liou H. C. Spano P. (2002b) Opposing roles for NF-kappa B/Rel factors p65 and c-Rel in the modulation of neuron survival elicited by glutamate and interleukin-1beta. J. Biol. Chem. 277, 20717 20723.
39. Pizzi M., Sarnico I., Boroni F., Benarese M., Steimberg N., Mazzoleni G., Dietz G. P., Bähr M., Liou H. C. Spano P. F. (2005) NF-κB factor c-Rel mediates neuroprotection elicited by mGlu5 receptor agonists against amyloid β-peptide toxicity. Cell Death Differ. 12, 761 772.
40. Puthalakath H. Strasser A. (2002) Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ. 9, 505 512.
41. Qin Z. H., Chen R. W., Wang Y., Nakai M., Chuang D. M. Chase T. N. (1999) Nuclear factor kappaB nuclear translocation upregulates c-Myc and p53 expression during NMDA receptor-mediated apoptosis in rat striatum. J. Neurosci. 19, 4023 4033.
42. Qiu J., Grafe M. R., Schmura S. M., Glasgow J. N., Kent T. A., Rassin D. K. Perez-Polo J. R. (2001) Differential NF-kappa B regulation of bcl-x gene expression in hippocampus and basal forebrain in response to hypoxia. J. Neurosci. Res. 64, 223 234.
43. Ridder D. A. Schwaninger M. (2008) NF-kappaB signaling in cerebral ischemia. Neuroscience [Epub ahead of print] doi :.
44. Rocha S., Campbell K. J. Perkins N. D. (2003) p53- and Mdm2-independent repression of NF-kappa B transactivation by the ARF tumor suppressor. Mol. Cell 12, 15 25.
45. Rocha S., Garrett M. D., Campbell K. J., Schumm K. Perkins N. D. (2005) Regulation of NF-kappaB and p53 through activation of ATR and Chk1 by the ARF tumour suppressor. EMBO J. 24, 1157 1169.
46. Schneider A., Martin-Villalba A., Weih F., Vogel J., Wirth T. Schwaninger M. (1999) NF-kappaB is activated and promotes cell death in focal cerebral ischemia. Nat. Med. 5, 554 559.
47. Valerio A., Dossena M., Bertolotti P. et al. (2008) Leptin is induced in the ischemic cerebral cortex and exerts neuroprotection through NF-κB/c-Rel-dependent transcription. Stroke [Epub ahead of print] doi :.
48. Willis S. N., Fletcher J. I., Kaufmann T. et al. (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315, 856 859.
49. Yu Z., Zhou D., Bruce-Keller A. J., Kindy M. S. Mattson M. P. (1999) Lack of the p50 subunit of nuclear factor-kappaB increases the vulnerability of hippocampal neurons to excitotoxic injury. J. Neurosci. 19, 8856 8865.
50. Zhang W., Potrovita I., Tarabin V., Herrmann O., Beer V., Weih F., Schneider A. Schwaninger M. (2005) Neuronal activation of NF-kappaB contributes to cell death in cerebral ischemia. J. Cereb. Blood Flow Metab. 25, 30 40.
51. Zhang L., Xing D. Chen M. (2008) Bim(L) displacing Bcl-x(L) promotes Bax translocation during TNFalpha-induced apoptosis. Apoptosis 13, 950 958.