Histone deacetylase 4 promotes ubiquitin-dependent proteasomal degradation of Sp3 in SH-SY5Y cells treated with di(2-ethylhexyl)phthalate (DEHP), determining neuronal death

Toxicology and Applied Pharmacology

Volumn 280, Issue 1, 2014, Pages 190-198

  Guida, Natascia ^a   Laudati, Giusy ^a   Galgani, Mario ^b   Santopaolo, Marianna ^b   Montuori, Paolo ^c   Triassi, Maria ^c   Di Renzo, Gianfranco ^a   Canzoniero, Lorella M T ^a,d   Formisano, Luigi ^a,d  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d UNIVERSITY OF SANNIO   (Italy)

Author keywords

Acetylation; DEHP; HDAC4; MC 1568; Ubiquitination

Indexed keywords

3 [4 [3 (3 FLUOROPHENYL) 3 OXO 1 PROPENYL] 1 METHYL 1H PYRROL 2 YL]ACRYLOHYDROXAMIC ACID; ANTISENSE OLIGODEOXYNUCLEOTIDE; CASPASE 3; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE INHIBITOR; MESSENGER RNA; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; PROTEASOME; SYNAPSIN II; TRANSCRIPTION FACTOR SP; TRANSCRIPTION FACTOR SP3; TRICHOSTATIN A; UBIQUITIN; HDAC4 PROTEIN, HUMAN; HISTONE DEACETYLASE; REPRESSOR PROTEIN;

ARTICLE; DEACETYLATION; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LONG TERM EXPOSURE; NERVE CELL NECROSIS; NEUROBLASTOMA CELL; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; TOXICITY; UBIQUITINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL DEATH; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; RAT; TUMOR CELL LINE; WISTAR RAT;

ANIMALS; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; DIETHYLHEXYL PHTHALATE; DOSE-RESPONSE RELATIONSHIP, DRUG; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RATS, WISTAR; REPRESSOR PROTEINS; UBIQUITIN;

EID: 84908637072     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.07.014     Document Type: Article

References (44)

1. Abel T., Zukin R. Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders. Curr. Opin. Pharmacol. 2008, 8:57-64.
2. Alique M., Herrero J.F., Lucio-Cazana F.J. All-trans retinoic acid induces COX-2 and prostaglandin E2 synthesis in SH-SY5Y human neuroblastoma cells: involvement of retinoic acid receptors and extracellular-regulated kinase 1/2. J. Neuroinflammation 2007, 4:1.
3. Ammanamanchi S., Brattain M.G. Sp3 Is a Transcriptional Repressor of Transforming Growth Factor-β Receptors. J. Biol. Chem. 2001, 276:3348-3352.
4. Ammanamanchi S., Freeman J.W., Brattain M.G. Acetylated Sp3 is a transcriptional activator. J. Biol. Chem. 2003, 278:35775-35780.
5. Aung K.H., Win-Shwe T.T., Kanaya M., Takano H., Tsukahara S. Involvement of hemeoxygenase-1 in di(2-ethylhexyl) phthalate (DEHP)-induced apoptosis of Neuro-2a cells. J. Toxicol. Sci. 2014, 39:217-229.
6. Boscia F., D'Avanzo C., Pannaccione A., Secondo A., Casamassa A., Formisano L., Guida N., Sokolow S., Herchuelz A., Annunziato L. Silencing or knocking out the Na(+)/Ca(2/>+) exchanger-3 (NCX3) impairs oligodendrocyte differentiation. Cell Death Differ. 2012, 19:562-572.
7. Cooper B.W., Cho T.M., Thompson P.M., Wallace A.D. Phthalate induction of CYP3A4 is dependent on glucocorticoid regulation of PXR expression. Toxicol. Sci. 2008, 103:268-277.
8. de Ruijter A.J., van Gennip A.H., Caron H.N., Kemp S., van Kuilenburg A.B. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J. 2003, 370:737-749.
9. Fernández-López D., Faustino J., Daneman R., Zhou L., Lee S.Y., Derugin N., Wendland M.F., Vexler Z.S. Blood-brain barrier permeability is increased after acute adult stroke but not neonatal stroke in the rat. J. Neurosci. 2012, 32:9588-9600.
10. Fordel E., Thijs L., Martinet W., Lenjou M., Laufs T., Van Bockstaele D., Moens L., Dewilde S. Neuroglobin and cytoglobin overexpression protects human SH-SY5Y neuroblastoma cells against oxidative stress-induced cell death. Neurosci. Lett. 2006, 410:146-151.
11. Formisano L., Guida N., Cocco S., Secondo A., Sirabella R., Ulianich L., Paturzo F., Di Renzo G., Canzoniero L.M. The repressor element 1-silencing transcription factor is a novel molecular target for the neurotoxic effect of the polychlorinated biphenyl mixture aroclor 1254 in neuroblastoma SH-SY5Y cells. J. Pharmacol. Exp. Ther. 2011, 338:997-1003.
12. Formisano L., Guida N., Valsecchi V., Pignataro G., Vinciguerra A., Pannaccione A., Secondo A., Boscia F., Molinaro P., Sisalli M.J., Sirabella R., Casamassa A., Canzoniero L.M., Di Renzo G., Annunziato L. NCX1 is a new rest target gene: role in cerebral ischemia. Neurobiol. Dis. 2013, 50:76-85.
13. Galmozzi A., Mitro N., Ferrari A., Gers E., Gilardi F., Godio C., Cermenati G., Gualerzi A., Donetti E., Rotili D., Valente S., Guerrini U., Caruso D., Mai A., Saez E., De Fabiani E., Crestani M. Inhibition of class I histone deacetylases unveils a mitochondrial signature and enhances oxidative metabolism in skeletal muscle and adipose tissue. Diabetes 2013, 62:732-742.
14. Haberland M., Montgomery R.L., Olson E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 2009, 10:32-42.
15. Heudorf U., Mersch-Sundermann V., Angerer J. Phthalates: toxicology and exposure. Int. J. Hyg. Environ. Health 2007, 210:623-634.
16. Hornan D.M., Peirson S.N., Hardcastle A.J., Molday R.S., Cheetham M.E., Webster A.R. Novel retinal and cone photoreceptor transcripts revealed by human macular expression profiling. Invest. Ophthalmol. Vis. Sci. 2007, 48:5388-5396.
17. Kavlock R., Boekelheide K., Chapin R., Cunningham M., Faustman E., Foster P., Golub M., Henderson R., Hinberg I., Little R., Seed J., Shea K., Tabacova S., Tyl R., Williams P., Zacharewski T. NTP Center for the Evaluation of Risks to Human Reproduction: phthalates expert panel report on the reproductive and developmental toxicity of di(2-ethylhexyl) phthalate. Reprod. Toxicol. 2002, 16:529-653.
18. Kawabata T., Nishida K., Takasugi K., Ogawa H., Sada K., Kadota Y., Inagaki J., Hirohata S., Ninomiya Y., Makino H. Increased activity and expression of histone deacetylase 1 in relation to tumor necrosis factor-alpha in synovial tissue of rheumatoid arthritis. Arthritis Res. Ther. 2010, 12:R133.
19. Korn A., Golan H., Melamed I., Pascual-Marqui R., Friedman A. Focal cortical dysfunction and blood-brain barrier disruption in patients with postconcussion syndrome. J. Clin. Neurophysiol. 2005, 22:1-9.
20. Lee J., Kosaras B., Aleyasin H., Han J.A., Park D.S., Ratan R.R., Kowall N.W., Ferrante R.J., Lee S.W., Ryu H. Role of cyclooxygenase-2 induction by transcription factor Sp1 and Sp3 in neuronal oxidative and DNA damage response. FASEB J. 2006, 20:2375-2377.
21. Lin C.H., Chen T.J., Chen S.S., Hsiao P.C., Yang R.C. Activation of Trim17 by PPARγ is involved in di(2-ethylhexyl) phthalate (DEHP)-induced apoptosis on Neuro-2a cells. Toxicol. Lett. 2011, 206:245-251.
22. Mao X., Yang S.H., Simpkins J.W., Barger S.W. Glutamate receptor activation evokes calpain-mediated degradation of Sp3 and Sp4, the prominent Sp-family transcription factors in neurons. J. Neurochem. 2007, 100:1300-1314.
23. Marinova Z., Leng Y., Leeds P., Chuang D.M. Histone deacetylase inhibition alters histone methylation associated with heat shock protein 70 promoter modifications in astrocytes and neurons. Neuropharmacology 2011, 60:1109-1115.
24. Masuo Y., Ishido M., Morita M., Oka S. Effects of neonatal treatment with 6-hydroxydopamine and endocrine disruptors on motor activity and gene expression in rats. Neural Plast. 2004, 11:59-76.
25. Masuo Y., Morita M., Oka S., Ishido M. Motor hyperactivity caused by a deficit in dopaminergic neurons and the effects of endocrine disruptors: a study inspired by the physiological roles of PACAP in the brain. Regul. Pept. 2004, 123:225-234.
26. Matsuda K.I., Mori H., Nugent B.M., Pfaff D.W., McCarthy M.M., Kawata M. Histone deacetylation during brain development is essential for permanent masculinization of sexual behavior. Endocrinology 2011, 152:2760-2767.
27. Nebbioso A., Dell'Aversana C., Bugge A., Sarno R., Valente S., Rotili D., Manzo F., Teti D., Mandrup S., Ciana P., Maggi A., Mai A., Gronemeyer H., Altucci L. HDACs class II-selective inhibition alters nuclear receptor-dependent differentiation. J. Mol. Endocrinol. 2010, 45:219-228.
28. Oehme I., Linke J.P., Böck B.C., Milde T., Lodrini M., Hartenstein B., Wiegand I., Eckert C., Roth W., Kool M., Kaden S., Gröne H.J., Schulte J.H., Lindner S., Hamacher-Brady A., Brady N.R., Deubzer H.E., Witt O. Histone deacetylase 10 promotes autophagy-mediated cell survival. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E2592-E2601.
29. Qiu Z., Norflus F., Singh B., Swindell M.K., Buzescu R., Bejarano M., Chopra R., Zucker B., Benn C.L., DiRocco D.P., Cha J.H., Ferrante R.J., Hersch S.M. Sp1 is up-regulated in cellular and transgenic models of Huntington disease, and its reduction is neuroprotective. J. Biol. Chem. 2006, 281:16672-16680.
30. Ravache M., Weber C., Mérienne K., Trottier Y. Transcriptional activation of REST by Sp1 in Huntington's disease models. PLoS ONE 2010, 5:e14311.
31. Rossignol D.A., Genuis S.J., Frye R.E. Environmental toxicants and autism spectrum disorders: a systematic review. Transl. Psychiatry 2014, 4:e360.
32. Ryu H., Lee J., Zaman K., Kubilis J., Ferrante R.J., Ross B.D., Neve R., Ratan R.R. Sp1 and Sp3 are oxidative stress-inducible, antideath transcription factors in cortical neurons. J. Neurosci. 2003, 23:3597-3606.
33. Santpere G., Nieto M., Puig B., Ferrer I. Abnormal Sp1 transcription factor expression in Alzheimer disease and tauopathies. Neurosci. Lett. 2006, 397:30-34.
34. Smith C.A., Macdonald A., Holahan M.R. Acute postnatal exposure to di(2-ethylhexyl) phthalate adversely impacts hippocampal development in the male rat. Neuroscience 2011, 193:100-108.
35. Spallotta F., Tardivo S., Nanni S., Rosati J.D., Straino S., Mai A., Vecellio M., Valente S., Capogrossi M.C., Farsetti A., Martone J., Bozzoni I., Pontecorvi A., Gaetano C., Colussi C. Detrimental effect of class-selective histone deacetylase inhibitors during tissue regeneration following hindlimb ischemia. J. Biol. Chem. 2013, 288:22915-22929.
36. Strbian D., Durukan A., Pitkonen M., Marinkovic I., Tatlisumak E., Pedrono E., Abo-Ramadan U., Tatlisumak T. The blood-brain barrier is continuously open for several weeks following transient focal cerebral ischemia. Neuroscience 2008, 153:175-181.
37. Subramanian C., Jarzembowski J.A., Opipari A.W., Castle V.P., Kwok R.P. HDAC6 deacetylates Ku70 and regulates Ku70-Bax binding in neuroblastoma. Neoplasia 2011, 13:726-734.
38. Sun Y., Liu P.Y., Scarlett C.J., Malyukova A., Liu B., Marshall G.M., Mackenzie K.L., Biankin A.V., Liu T. Histone deacetylase 5 blocks neuroblastoma cell differentiation by interacting with N-Myc. Oncogene 2013, 33(23):2987-2994.
39. Suske G. The Sp-family of transcription factors. Gene 1999, 238:291-300.
40. Tanida T., Warita K., Ishihara K., Fukui S., Mitsuhashi T., Sugawara T., Tabuchi Y., Nanmori T., Qi W.M., Inamoto T., Yokoyama T., Kitagawa H., Hoshi N. Fetal and neonatal exposure to three typical environmental chemicals with different mechanisms of action: mixed exposure to phenol, phthalate, and dioxin cancels the effects of sole exposure on mouse midbrain dopaminergic nuclei. Toxicol. Lett. 2009, 189:40-47.
41. Testa C., Nuti F., Hayek J., De Felice C., Chelli M., Rovero P., Latini G., Papini A.M. Di-(2-ethylhexyl) phthalate and autism spectrum disorders. ASN Neuro 2012, 4:223-229.
42. Wu Y., Li K., Zuo H., Yuan Y., Sun Y., Yang X. Primary neuronal-astrocytic co-culture platform for neurotoxicity assessment of di-(2-ethylhexyl) phthalate. J. Environ. Sci. 2013, 10.1016/S1001-0742 (13) 60504-5.
43. Xu K., Shu H.K. EGFR activation results in enhanced cyclooxygenase-2 expression through p38 mitogen-activated protein kinase-dependent activation of the Sp1/Sp3 transcription factors in human gliomas. Cancer Res. 2007, 67:6121-6129.
44. Zhang W., Tian Z., Sha S., Cheng L.Y., Philipsen S., Tan-Un K.C. Functional and sequence analysis of human neuroglobin gene promoter region. Biochim. Biophys. Acta 2011, 1809:236-244.