Stress-induced expression of the p75 neurotrophin receptor is regulated by O-GlcNAcylation of the Sp1 transcription factor

Journal of Neurochemistry

Volumn 116, Issue 3, 2011, Pages 396-405

  Kommaddi, Reddy P ^a   Dickson, Kathleen M ^a   Barker, Philip A ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

injury; nerve growth factor receptor; neurotrophin; osmolarity; promoter; transcription

Indexed keywords

N ACETYLGLUCOSAMINE; N ACETYLGLUCOSAMINE TRANSFERASE; NEUROTROPHIN RECEPTOR P75; TRANSCRIPTION FACTOR SP1; TRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MOUSE; NERVE CELL CULTURE; NONHUMAN; OSMOLARITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RNA INTERFERENCE; STRESS;

ACETYLGLUCOSAMINE; ACYLATION; ANIMALS; APOPTOSIS; CELLS, CULTURED; DOWN-REGULATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEK293 CELLS; HUMANS; MICE; MUTATION; N-ACETYLGLUCOSAMINYLTRANSFERASES; OSMOLAR CONCENTRATION; OSMOTIC PRESSURE; RECEPTORS, NERVE GROWTH FACTOR; SP1 TRANSCRIPTION FACTOR; STRESS, PHYSIOLOGICAL;

EID: 78651332787     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07120.x     Document Type: Article

References (55)

1. Andsberg G., Kokaia Z., and, Lindvall O., (2001) Upregulation of p75 neurotrophin receptor after stroke in mice does not contribute to differential vulnerability of striatal neurons. Exp. Neurol. 169, 351-363.
2. Bhakar A. L., Howell J. L., Paul C. E., Salehi A. H., Becker E. B., Said F., Bonni A., and, Barker P. A., (2003) Apoptosis induced by p75NTR overexpression requires Jun kinase-dependent phosphorylation of Bad. J. Neurosci. 23, 11373-11381.
3. Bouwman P., and, Philipsen S., (2002) Regulation of the activity of Sp1-related transcription factors. Mol. Cell. Endocrinol. 195, 27-38.
4. Brasse-Lagnel C., Fairand A., Lavoinne A., and, Husson A., (2003) Glutamine stimulates argininosuccinate synthetase gene expression through cytosolic O-glycosylation of Sp1 in Caco-2 cells. J. Biol. Chem. 278, 52504-52510.
5. Brasse-Lagnel C., Lavoinne A., Loeber D., Fairand A., Bole-Feysot C., Deniel N., and, Husson A., (2007) Glutamine and interleukin-1beta interact at the level of Sp1 and nuclear factor-kappaB to regulate argininosuccinate synthetase gene expression. FEBS J. 274, 5250-5262.
6. Caprini M., Gomis A., Cabedo H., Planells-Cases R., Belmonte C., Viana F., and, Ferrer-Montiel A., (2003) GAP43 stimulates inositol trisphosphate-mediated calcium release in response to hypotonicity. EMBO J. 22, 3004-3014.
7. Casha S., Yu W. R., and, Fehlings M. G., (2001) Oligodendroglial apoptosis occurs along degenerating axons and is associated with FAS and p75 expression following spinal cord injury in the rat. Neuroscience 103, 203-218.
8. Cheung W. D., and, Hart G. W., (2008) AMP-activated protein kinase and p38 MAPK activate O-GlcNAcylation of neuronal proteins during glucose deprivation. J. Biol. Chem. 283, 13009-13020.
9. Chung S. S., Kim J. H., Park H. S., Choi H. H., Lee K. W., Cho Y. M., Lee H. K., and, Park K. S., (2008) Activation of PPARgamma negatively regulates O-GlcNAcylation of Sp1. Biochem. Biophys. Res. Commun. 372, 713-718.
10. Copray J. C., Jaarsma D., Kust B. M., Bruggeman R. W., Mantingh I., Brouwer N., and, Boddeke H. W., (2003) Expression of the low affinity neurotrophin receptor p75 in spinal motoneurons in a transgenic mouse model for amyotrophic lateral sclerosis. Neuroscience 116, 685-694.
11. Du X. L., Edelstein D., Rossetti L., Fantus I. G., Goldberg H., Ziyadeh F., Wu J., and, Brownlee M., (2000) Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc. Natl Acad. Sci. USA 97, 12222-12226.
12. Fischer R., Schliess F., and, Haussinger D., (1997) Characterization of the hypo-osmolarity-induced Ca2+ response in cultured rat astrocytes. Glia 20, 51-58.
13. Goldberg H. J., Scholey J., and, Fantus I. G., (2000) Glucosamine activates the plasminogen activator inhibitor 1 gene promoter through Sp1 DNA binding sites in glomerular mesangial cells. Diabetes 49, 863-871.
14. Goldberg H. J., Whiteside C. I., and, Fantus I. G., (2002) The hexosamine pathway regulates the plasminogen activator inhibitor-1 gene promoter and Sp1 transcriptional activation through protein kinase C-beta I and-delta. J. Biol. Chem. 277, 33833-33841.
15. Goldberg H. J., Whiteside C. I., Hart G. W., and, Fantus I. G., (2006) Posttranslational, reversible O-glycosylation is stimulated by high glucose and mediates plasminogen activator inhibitor-1 gene expression and Sp1 transcriptional activity in glomerular mesangial cells. Endocrinology 147, 222-231.
16. Han I., and, Kudlow J. E., (1997) Reduced O glycosylation of Sp1 is associated with increased proteasome susceptibility. Mol. Cell. Biol. 17, 2550-2558.
17. Husson A., Quillard M., Fairand A., Chedeville A., and, Lavoinne A., (1996) Hypoosmolarity and glutamine increased the beta-actin gene transcription in isolated rat hepatocytes. FEBS Lett. 394, 353-355.
18. Ishimaru N., Tabuchi A., Hara D., Hayashi H., Sugimoto T., Yasuhara M., Shiota J., and, Tsuda M., (2007) Regulation of neurotrophin-3 gene transcription by Sp3 and Sp4 in neurons. J. Neurochem. 100, 520-531.
19. Jackson S. P., and, Tjian R., (1988) O-glycosylation of eukaryotic transcription factors: implications for mechanisms of transcriptional regulation. Cell 55, 125-133.
20. King V. R., Bradbury E. J., McMahon S. B., and, Priestley J. V., (2000) Changes in truncated trkB and p75 receptor expression in the rat spinal cord following spinal cord hemisection and spinal cord hemisection plus neurotrophin treatment. Exp. Neurol. 165, 327-341.
21. Kokaia Z., Andsberg G., Martinez-Serrano A., and, Lindvall O., (1998) Focal cerebral ischemia in rats induces expression of P75 neurotrophin receptor in resistant striatal cholinergic neurons. Neuroscience 84, 1113-1125.
22. Li T., Chen Y. H., Liu T. J., Jia J., Hampson S., Shan Y. X., Kibler D., and, Wang P. H., (2003) Using DNA microarray to identify Sp1 as a transcriptional regulatory element of insulin-like growth factor 1 in cardiac muscle cells. Circ. Res. 93, 1202-1209.
23. Li L., He S., Sun J. M., and, Davie J. R., (2004) Gene regulation by Sp1 and Sp3. Biochem. Cell Biol. 82, 460-471.
24. Lim K., and, Chang H. I., (2009) O-GlcNAc inhibits interaction between Sp1 and Elf-1 transcription factors. Biochem. Biophys. Res. Commun. 380, 569-574.
25. Lim K., and, Chang H. I., (2010) O-GlcNAc inhibits interaction between Sp1 and sterol regulatory element binding protein 2. Biochem. Biophys. Res. Commun. 393, 314-318.
26. Lopez S. M., Perez-Perez M., Marquez J. M., Naves F. J., Represa J., and, Vega J. A., (1998) p75 and TrkA neurotrophin receptors in human skin after spinal cord and peripheral nerve injury, with special reference to sensory corpuscles. Anat. Rec. 251, 371-383.
27. Majdan M., Lachance C., Gloster A., et al. (1997) Transgenic mice expressing the intracellular domain of the p75 neurotrophin receptor undergo neuronal apoptosis. J. Neurosci. 17, 6988-6998.
28. Majumdar G., Harmon A., Candelaria R., Martinez-Hernandez A., Raghow R., and, Solomon S. S., (2003) O-glycosylation of Sp1 and transcriptional regulation of the calmodulin gene by insulin and glucagon. Am. J. Physiol. Endocrinol. Metab. 285, E584-E591.
29. Majumdar G., Harrington A., Hungerford J., Martinez-Hernandez A., Gerling I. C., Raghow R., and, Solomon S., (2006) Insulin dynamically regulates calmodulin gene expression by sequential o-glycosylation and phosphorylation of sp1 and its subcellular compartmentalization in liver cells. J. Biol. Chem. 281, 3642-3650.
30. Meisse D., Renouf S., Husson A., and, Lavoinne A., (1998) Cell swelling increased the alpha2-macroglobulin gene expression in cultured rat hepatocytes. FEBS Lett. 422, 346-348.
31. Michalke M., Cariers A., Schliess F., and, Haussinger D., (2000) Hypoosmolarity influences the activity of transcription factor NF-kappaB in rat H4IIE hepatoma cells. FEBS Lett. 465, 64-68.
32. Milagre I., Nunes M. J., Gama M. J., Silva R. F., Pascussi J. M., Lechner M. C., and, Rodrigues E., (2008) Transcriptional regulation of the human CYP46A1 brain-specific expression by Sp transcription factors. J. Neurochem. 106, 835-849.
33. Pang R. T., Lee L. T., Ng S. S., Yung W. H., and, Chow B. K., (2004) CpG methylation and transcription factors Sp1 and Sp3 regulate the expression of the human secretin receptor gene. Mol. Endocrinol. 18, 471-483.
34. Papadopoulos M. C., Saadoun S., Binder D. K., Manley G. T., Krishna S., and, Verkman A. S., (2004) Molecular mechanisms of brain tumor edema. Neuroscience 129, 1011-1020.
35. Paul C. E., Vereker E., Dickson K. M., and, Barker P. A., (2004) A pro-apoptotic fragment of the p75 neurotrophin receptor is expressed in p75NTRExonIV null mice. J. Neurosci. 24, 1917-1923.
36. Peterson S., and, Bogenmann E., (2003) Osmotic swelling induces p75 neurotrophin receptor (p75NTR) expression via nitric oxide. J. Biol. Chem. 278, 33943-33950.
37. Ramos A., Ho W. C., Forte S., Dickson K., Boutilier J., Favell K., and, Barker P. A., (2007) Hypo-osmolar stress induces p75NTR expression by activating Sp1-dependent transcription. J. Neurosci. 27, 1498-1506.
38. Roos M. D., Su K., Baker J. R., and, Kudlow J. E., (1997) O glycosylation of an Sp1-derived peptide blocks known Sp1 protein interactions. Mol. Cell. Biol. 17, 6472-6480.
39. Roux P. P., Colicos M. A., Barker P. A., and, Kennedy T. E., (1999) p75 neurotrophin receptor expression is induced in apoptotic neurons after seizure. J. Neurosci. 19, 6887-6896.
40. Shaw G., Morse S., Ararat M., and, Graham F. L., (2002) Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J. 16, 869-871.
41. Slawson C., Housley M. P., and, Hart G. W., (2006) O-GlcNAc cycling: how a single sugar post-translational modification is changing the way we think about signaling networks. J. Cell. Biochem. 97, 71-83.
42. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., and, Klenk D. C., (1985) Measurement of protein using bicinchoninic acid. Anal Biochem. 150, 76-85.
43. Solomon S. S., Palazzolo M. R., Takahashi T., and, Raghow R., (1997a) Transcription factor Sp1 is necessary for basal calmodulin gene transcription and for its selective stimulation by insulin. Endocrinology 138, 5052-5054.
44. Solomon S. S., Palazzolo M. R., Takahashi T., and, Raghow R., (1997b) Insulin stimulates rat calmodulin I gene transcription through activation of Sp1. Proc. Assoc. Am. Physicians 109, 470-477.
45. Su K., Roos M. D., Yang X., Han I., Paterson A. J., and, Kudlow J. E., (1999) An N-terminal region of Sp1 targets its proteasome-dependent degradation in vitro. J. Biol. Chem. 274, 15194-15202.
46. Troy C. M., Friedman J. E., and, Friedman W. J., (2002) Mechanisms of p75-mediated death of hippocampal neurons. Role of caspases. J. Biol. Chem. 277, 34295-34302.
47. Vosseller K., Wells L., and, Hart G. W., (2001) Nucleocytoplasmic O-glycosylation: O-GlcNAc and functional proteomics. Biochimie 83, 575-581.
48. Warskulat U., Kreuels S., Muller H. W., and, Haussinger D., (2001) Identification of osmosensitive and ammonia-regulated genes in rat astrocytes by Northern blotting and differential display reverse transcriptase-polymerase chain reaction. J. Hepatol. 35, 358-366.
49. Wells L., Vosseller K., and, Hart G. W., (2001) Glycosylation of nucleocytoplasmic proteins: signal transduction and O-GlcNAc. Science 291, 2376-2378.
50. Wong W. K., Chen K., and, Shih J. C., (2003) Decreased methylation and transcription repressor Sp3 up-regulated human monoamine oxidase (MAO) B expression during Caco-2 differentiation. J. Biol. Chem. 278, 36227-36235.
51. Yang X., Su K., Roos M. D., Chang Q., Paterson A. J., and, Kudlow J. E., (2001) O-linkage of N-acetylglucosamine to Sp1 activation domain inhibits its transcriptional capability. Proc. Natl Acad. Sci. USA 98, 6611-6616.
52. Yang X., Zhang F., and, Kudlow J. E., (2002) Recruitment of O-GlcNAc transferase to promoters by corepressor mSin3A: coupling protein O-GlcNAcylation to transcriptional repression. Cell 110, 69-80.
53. Zachara N. E., and, Hart G. W., (2006) Cell signaling, the essential role of O-GlcNAc!. Biochim. Biophys. Acta 1761, 599-617.
54. Zachara N. E., O'Donnell N., Cheung W. D., Mercer J. J., Marth J. D., and, Hart G. W., (2004) Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. J. Biol. Chem. 279, 30133-30142.
55. Zhang F., Su K., Yang X., Bowe D. B., Paterson A. J., and, Kudlow J. E., (2003) O-GlcNAc modification is an endogenous inhibitor of the proteasome. Cell 115, 715-725.