The transcription factor CCAAT enhancer-binding protein β protects rat cerebellar granule neurons from apoptosis through its transcription-activating isoforms

European Journal of Neuroscience

Volumn 39, Issue 2, 2014, Pages 176-185

  Peña Altamira, Emiliano ^a   Polazzi, Elisabetta ^a   Moretto, Edoardo ^a   Lauriola, Mattia ^a   Monti, Barbara ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Neuroprotection; Phosphorylation; Sumoylation; Survival

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; LIVER ACTIVATOR PROTEIN 1; LIVER ACTIVATOR PROTEIN 2; LIVER INHIBITORY PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CELLULAR DISTRIBUTION; CEREBELLUM; CONTROLLED STUDY; DENSITOMETRY; ENZYME ACTIVATION; GRANULE CELL; IMMUNOPRECIPITATION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SUMOYLATION; TRANSCRIPTION REGULATION;

NEUROPROTECTION; PHOSPHORYLATION; SUMOYLATION; SURVIVAL;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; HUMANS; IMMUNOHISTOCHEMISTRY; NEURONS; PHOSPHORYLATION; POTASSIUM; PROTEIN ISOFORMS; RATS; RATS, WISTAR; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUBCELLULAR FRACTIONS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

EID: 84892675277     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12407     Document Type: Article

References (65)

1. Abreu, M.M. & Sealy, L. (2010) The C/EBPbeta isoform, liver-inhibitory protein (LIP), induces autophagy in breast cancer cell lines. Exp. Cell Res., 316, 3227-3238.
2. Abreu, M. & Sealy, L. (2012) Cells expressing the C/EBPbeta isoform, LIP, engulf their neighbors. PLoS ONE, 7, e41807.
3. Aguilar-Morante, D., Cortés-Canteli, M., Sanz-Sancristobal, M., Santos, A. & Perez-Castillo, A. (2011) Decreased CCAAT/enhancer binding protein β expression inhibits the growth of glioblastoma cells. Neuroscience, 176, 110-119.
4. Buck, M. & Chojkier, M. (2003) Signal transduction in the liver: C/EBPbeta modulates cell proliferation and survival. Hepatology, 37, 731-738.
5. Buck, M., Turler, H. & Chojkier, M. (1994) LAP (NF-IL-6), a tissue-specific transcriptional activator, is an inhibitor of hepatoma cell proliferation. EMBO J., 13, 851-860.
6. Buck, M., Poli, V., van der Geer, P., Chojkier, M. & Hunter, T. (1999) Phosphorylation of rat serine 105 or mouse threonine 217 in C/EBP beta is required for hepatocyte proliferation induced by TGF alpha. Mol. Cell, 4, 1087-1092.
7. Buck, M., Zhang, L., Halasz, N.A., Hunter, T. & Chojkier, M. (2001) Nuclear export of phosphorylated C/EBPbeta mediates the inhibition of albumin expression by TNF-alpha. EMBO J., 20, 6712-6723.
8. Calella, A.M., Nerlov, C., Lopez, R.G., Sciarretta, C., von Bohlen Halbach, O., Bereshchenko, O. & Minichiello, L. (2007) Neurotrophin/Trk receptor signaling mediates C/EBPalpha, -beta and NeuroD recruitment to immediate-early gene promoters in neuronal cells and requires C/EBPs to induce immediate-early gene transcription. Neural Dev., 2, 4.
9. Cardinaux, J.R., Allaman, I. & Magistrett, P.J. (2000) Pro-inflammatory cytokines induce the transcription factors C/EBPbeta and C/EBPdelta in astrocytes. Glia, 29, 91-97.
10. Caruccio, L. & Banerjee, R. (1999) An efficient method for simultaneous isolation of biologically active transcription factors and DNA. J. Immunol. Methods, 230, 1-10.
11. Chiribau, C.B., Gaccioli, F., Huang, C.C., Yuan, C.L. & Hatzoglou, M. (2010) Molecular symbiosis of CHOP and C/EBP beta isoform LIP contributes to endoplasmic reticulum stress-induced apoptosis. Mol. Cell. Biol., 30, 3722-3731.
12. Contestabile, A. (2002) Cerebellar granule cells as a model to study mechanisms of neuronal apoptosis or survival in vivo and in vitro. Cerebellum, 1, 41-55.
13. Cortés-Canteli, M., Pignatelli, M., Santos, A. & Perez-Castillo, A. (2002) CCAAT/enhancer-binding protein beta plays a regulatory role in differentiation and apoptosis of neuroblastoma cells. J. Biol. Chem., 277, 5460-5467.
14. Cortés-Canteli, M., Wagner, M., Ansorge, W. & Pérez-Castillo, A. (2004) Microarray analysis supports a role for ccaat/enhancer-binding protein-beta in brain injury. J. Biol. Chem., 279, 14409-14417.
15. Cortés-Canteli, M., Luna-Medina, R., Sanz-Sancristobal, M., Alvarez-Barrientos, A., Santos, A. & Perez-Castillo, A. (2008) CCAAT/enhancer binding protein beta deficiency provides cerebral protection following excitotoxic injury. J. Cell Sci., 121, 1224-1234.
16. Cortés-Canteli, M., Aguilar-Morante, D., Sanz-Sancristobal, M., Megias, D., Santos, A. & Perez-Castillo, A. (2011) Role of C/EBPβ transcription factor in adult hippocampal neurogenesis. PLoS ONE, 6, e24842.
17. Descombes, P. & Schibler, U. (1991) A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell, 67, 569-579.
18. Dorval, V. & Fraser, P.E. (2007) SUMO on the road to neurodegeneration. Biochim. Biophys. Acta, 1773, 694-706.
19. Eaton, E.M. & Sealy, L. (2003) Modification of CCAAT/enhancer-binding protein-beta by the small ubiquitin-like modifier (SUMO) family members, SUMO-2 and SUMO-3. J. Biol. Chem., 278, 33416-33421.
20. Ejarque-Ortiz, A., Medina, M.G., Tusell, J.M., Pérez-González, A.P., Serratosa, J. & Saura, J. (2007) Upregulation of CCAAT/enhancer binding protein beta in activated astrocytes and microglia. Glia, 55, 178-188.
21. Fields, J. & Ghorpade, A. (2012) C/EBPβ regulates multiple IL-1β-induced human astrocyte inflammatory genes. J. Neuroinflamm., 20, 177-188.
22. Gallo, V., Kingsbury, A., Balázs, R. & Jørgensen, O.S. (1987) The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J. Neurosci., 7, 2203-2213.
23. Garcia-Osta, A., Tsokas, P., Pollonini, G., Landau, E.M., Blitzer, R. & Alberini, C.M. (2006) MuSK expressed in the brain mediates cholinergic responses, synaptic plasticity, and memory formation. J. Neurosci., 26, 7919-7932.
24. Halterman, M.W., De Jesus, C., Rempe, D.A., Schor, N.F. & Federoff, H.J. (2008) Loss of c/EBP-beta activity promotes the adaptive to apoptotic switch in hypoxic cortical neurons. Mol. Cell. Neurosci., 38, 125-137.
25. Hansen, M.B., Nielsen, S.E. & Berg, K. (1989) Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods, 119, 203-210.
26. Kapadia, R., Tureyen, K., Bowen, K.K., Kalluri, H., Johnson, P.F. & Vemuganti, R. (2006) Decreased brain damage and curtailed inflammation in transcription factor CCAAT/enhancer binding protein beta knockout mice following transient focal cerebral ischemia. J. Neurochem., 98, 1718-1731.
27. Kim, J., Cantwell, C.A., Johnson, P.F., Pfarr, C.M. & Williams, S.C. (2002) Transcriptional activity of CCAAT/enhancer-binding proteins is controlled by a conserved inhibitory domain that is a target for sumoylation. J. Biol. Chem., 277, 38037-38044.
28. Kowenz-Leutz, E., Pless, O., Dittmar, G., Knoblich, M. & Leutz, A. (2010) Crosstalk between C/EBPbeta phosphorylation, arginine methylation, and SWI/SNF/Mediator implies an indexing transcription factor code. EMBO J., 29, 1105-1115.
29. Li, Y., Bevilacqua, E., Chiribau, C.B., Majumder, M., Wang, C., Croniger, C.M., Snider, M.D., Johnson, P.F. & Hatzoglou, M. (2008) Differential control of the CCAAT/enhancer-binding protein beta (C/EBPbeta) products liver-enriched transcriptional activating protein (LAP) and liver-enriched transcriptional inhibitory protein (LIP) and the regulation of gene expression during the response to endoplasmic reticulum stress. J. Biol. Chem., 283, 22443-22456.
30. Lieberman, A.P. (2004) SUMO, a ubiquitin-like modifier implicated in neurodegeneration. Exp. Neurol., 185, 204-207.
31. Lowry, O.H., Rosenbrough, R.J., Farr, A.L. & Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193, 265-275.
32. Mahoney, C.W., Shuman, J., McKnight, S.L., Chen, H.C. & Huang, K.P. (1992) Phosphorylation of CCAAT-enhancer binding protein by protein kinase C attenuates site-selective DNA binding. J. Biol. Chem., 267, 19396-19403.
33. Marshall, J., Dolan, B.M., Garcia, E.P., Sathe, S., Tang, X., Mao, Z. & Blair, L.A. (2003) Calcium channel and NMDA receptor activities differentially regulate nuclear C/EBPbeta levels to control neuronal survival. Neuron, 39, 625-639.
34. Meir, O., Dvash, E., Werman, A. & Rubinstein, M. (2010) C/EBP-beta regulates endoplasmic reticulum stress-triggered cell death in mouse and human models. PLoS ONE, 5, e9516.
35. Monti, B., Zanghellini, P. & Contestabile, A. (2001) Characterization of ceramide-induced apoptotic death in cerebellar granule cells in culture. Neurochem. Int., 39, 11-18.
36. Nadeau, S., Hein, P., Fernandes, K.J., Peterson, A.C. & Miller, F.D. (2005) A transcriptional role for C/EBP beta in the neuronal response to axonal injury. Mol. Cell. Neurosci., 29, 525-535.
37. Nerlov, C. (2007) The C/EBP family of transcription factors: a paradigm for interaction between gene expression and proliferation control. Trends Cell Biol., 17, 318-324.
38. Nerlov, C. (2008) C/EBPs: recipients of extracellular signals through proteome modulation. Curr. Opin. Cell Biol., 20, 180-185.
39. Nikitin, V.P. (2007) A new mechanism of synapse-specific neuronal plasticity. Neurosci. Behav. Physiol., 37, 559-570.
40. Obrietan, K. & Hoyt, K.R. (2004) CRE-mediated transcription is increased in Huntington's disease transgenic mice. J. Neurosci., 24, 791-796.
41. Ossipow, V., Descombes, P. & Schibler, U. (1993) CCAAT/enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials. Proc. Natl. Acad. Sci. USA, 90, 8219-8223.
42. Paquin, A., Barnabé-Heider, F., Kageyama, R. & Miller, F.D. (2005) CCAAT/enhancer-binding protein phosphorylation biases cortical precursors to generate neurons rather than astrocytes in vivo. J. Neurosci., 25, 10747-10758.
43. Pasquini, L.A., Besio Moreno, M., Adamo, A.M., Pasquini, J.M. & Soto, E.F. (2000) Lactacystin, a specific inhibitor of the proteasome, induces apoptosis and activates caspase-3 in cultured cerebellar granule cells. J. Neurosci. Res., 59, 601-611.
44. Peña-Altamira, E., Petazzi, P. & Contestabile, A. (2010) Nitric oxide control of proliferation in nerve cells and in tumor cells of nervous origin. Curr. Pharm. Design, 16, 440-450.
45. Pérez-Capote, K., Saura, J., Serratosa, J. & Solà, C. (2006) Expression of C/EBPalpha and C/EBPbeta in glial cells in vitro after inducing glial activation by different stimuli. Neurosci. Lett., 410, 25-30.
46. Piwien-Pilipuk, G., Van Mater, D., Ross, S.E., MacDougald, O.A. & Schwartz, J. (2001) Growth hormone regulates phosphorylation and function of CCAAT/enhancer-binding protein beta by modulating Akt and glycogen synthase kinase-3. J. Biol. Chem., 276, 19664-19671.
47. Piwien-Pilipuk, G., MacDougald, O. & Schwartz, J. (2002) Dual regulation of phosphorylation and dephosphorylation of C/EBPbeta modulate its transcriptional activation and DNA binding in response to growth hormone. J. Biol. Chem., 277, 44557-44565.
48. Ramathal, C., Bagchi, I.C. & Bagchi, M.K. (2010) Lack of CCAAT enhancer binding protein beta (C/EBPbeta) in uterine epithelial cells impairs estrogen-induced DNA replication, induces DNA damage response pathways, and promotes apoptosis. Mol. Cell. Biol., 30, 1607-1619.
49. Rininger, A., Dejesus, C., Totten, A., Wayland, A. & Halterman, M.W. (2012) MKP-1 antagonizes C/EBPβ activity and lowers the apoptotic threshold after ischemic injury. Cell Death Differ., 19, 1634-1643.
50. Ruffell, D., Mourkioti, F., Gambardella, A., Kirstetter, P., Lopez, R.G., Rosenthal, N. & Nerlov, C. (2009) A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc. Natl. Acad. Sci. USA, 106, 17475-17480.
51. Samuelsson, M., Ramberg, V. & Iverfeldt, K. (2008) Alzheimer amyloid-beta peptides block the activation of C/EBPbeta and C/EBPdelta in glial cells. Biochem. Bioph. Res. Co., 370, 619-622.
52. Sandhir, R. & Berman, N.E. (2010) Age-dependent response of CCAAT/enhancer binding proteins following traumatic brain injury in mice. Neurochem. Int., 56, 188-193.
53. Sebastian, T. & Johnson, P.F. (2006) Stop and go: anti-proliferative and mitogenic functions of the transcription factor C/EBPbeta. Cell Cycle, 5, 953-957.
54. Seeler, J.S. & Dejean, A. (2003) Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell Bio., 4, 690-699.
55. Soga, Y., Yamanaka, R., Nishino, K. & Tanaka, R. (2003) CCAAT/enhancer binding proteins are expressed in the gerbil hippocampus after transient forebrain ischemia. Neurosci. Lett., 337, 106-110.
56. Straccia, M., Gresa-Arribas, N., Dentesano, G., Ejarque-Ortiz, A., Tusell, J.M., Serratosa, J., Solà, C. & Saura, J. (2011) Pro-inflammatory gene expression and neurotoxic effects of activated microglia are attenuated by absence of CCAAT/enhancer binding protein β. J. Neuroinflamm., 8, 156-171.
57. Su, W.C., Chou, H.Y., Chang, C.J., Lee, Y.M., Chen, W.H., Huang, K.H., Lee, M.Y. & Lee, S.C. (2003) Differential activation of a C/EBP beta isoform by a novel redox switch may confer the lipopolysaccharide-inducible expression of interleukin-6 gene. J. Biol. Chem., 278, 51150-51158.
58. Taubenfeld, S.M., Milekic, M.H., Monti, B. & Alberini, C.M. (2001a) The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat. Neurosci., 4, 813-818.
59. Taubenfeld, S.M., Wiig, K.A., Monti, B., Dolan, B., Pollonini, G. & Alberini, C.M. (2001b) Fornix-dependent induction of hippocampal CCAAT enhancer-binding protein [beta] and [delta] co-localizes with phosphorylated cAMP response element-binding protein and accompanies long-term memory consolidation. J. Neurosci., 21, 84-91.
60. Trautwein, C., Caelles, C., van der Geer, P., Hunter, T., Karin, M. & Chojkier, M. (1993) Transactivation by NF-IL6/LAP is enhanced by phosphorylation of its activation domain. Nature, 364, 544-547.
61. Trautwein, C., van der Geer, P., Karin, M., Hunter, T. & Chojkier, M. (1994) Protein kinase A and C site-specific phosphorylations of LAP (NF-IL6) modulate its binding affinity to DNA recognition elements. J. Clin. Invest., 93, 2554-2561.
62. Tsukada, J., Yoshida, Y., Kominato, Y. & Auron, P.E. (2011) The CCAAT/enhancer (C/EBP) family of basic-leucine zipper (bZIP) transcription factors is a multifaceted highly-regulated system for gene regulation. Cytokine, 54, 6-19.
63. Wegner, M., Cao, Z. & Rosenfeld, M.G. (1992) Calcium-regulated phosphorylation within the leucine zipper of C/EBP beta. Science, 256, 370-373.
64. 2+/calmodulin kinases activation in hippocampal neurons. J. Biol. Chem., 273, 31345-31351.
65. Zeitelhofer, M., Vessey, J.P., Thomas, S., Kiebler, M. & Dahm, R. (2009) Transfection of cultured primary neurons via nucleofection. Curr. Protoc. Neurosci., 32, 1-21.