Transcription factor IIA τ is associated with undifferentiated cells and its gene expression is repressed in primary neurons at the chromatin level in vivo

Stem Cells and Development

Volumn 15, Issue 2, 2006, Pages 175-190

  Howe, Mariko L ^a   Mehmud, Zareen F ^a   Saha, Shamol ^a   Buratovich, Michael ^b   Stutius, Erica A ^a   Schmidt, Heath D ^a   Lenon, Angela L ^a   Reddicks, Candice ^a   Ivanov, Gleb S ^a,e   Przyborski, Stefan A ^c   Ozer, Josef S ^a,d  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SPRING ARBOR UNIVERSITY   (United States)

^c DURHAM UNIVERSITY   (United Kingdom)

^d MERCK RESEARCH LABORATORIES   (United States)

^e TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID; GENOMIC DNA; RETINOIC ACID; SULFUR 35; TRANSCRIPTION FACTOR IIA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; ISOTOPE LABELING; MAMMAL CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; BRAIN; BUTYRATES; CELL DIFFERENTIATION; CELL LINE; CELL LINE, TUMOR; CHROMATIN; FIBROBLASTS; GENE EXPRESSION; HELA CELLS; HISTONES; HT29 CELLS; HUMANS; JURKAT CELLS; MALE; MOLECULAR SEQUENCE DATA; NEURONS; PROTEIN SUBUNITS; RATS; SEQUENCE HOMOLOGY, AMINO ACID; SP TRANSCRIPTION FACTORS; TESTIS; TRANSCRIPTION FACTOR TFIIA; TRETINOIN;

MAMMALIA;

EID: 33646550160     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2006.15.175     Document Type: Article

References (93)

1. Lieberman PM and AJ Berk. (1994). A mechanism for TAFs in transcriptional activation: activation domain enhancement of TFIID-TFIIA-promoter DNA complex formation. Genes Dev 8:995-1006.
2. Wang W, JD Gralla and M Carey. (1992). The acidic activator GAL4-AH can stimulate polymerase II transcription by promoting assembly of a closed complex requiring TFIID and TFIIA. Genes Dev 6:1716-1727.
3. Lieberman PM. (1994). Identification of functional targets of the Zta transcriptional activator by formation of stable preinitiation complex intermediates. Mol Cell Biol 14:8354-8375.
4. Ozer J, PA Moore, AH Bolder, A Lee, CA Rosen and PM Lieberman. (1994). Molecular cloning of the small (gamma) subunit of human TFIIA reveals functions critical for activated transcription. Genes Dev 8:2324-2335.
5. DeJong J and RG Roeder. (1993). A single cDNA, hTFIIA/alpha, encodes both the p35 and p19 subunits of human TFIIA. Genes Dev 7:2220-2234.
6. Ma D, H Watanabe, F Mermelstein, A Admon, K Oguri, X Sun, T Wada, T Imai, T Shiroya and D Reinberg. (1993). Isolation of the cDNA encoding the largest subunit of TFIIA reveals functions important for activated transcription. Genes Dev 7:2246-2257.
7. Geiger JH, S Hahn, S Lee and PB Sigler. (1996). Crystal structure of the yeast TFIIA/TBP/DNA complex. Science 272:830-836.
8. Ozer J, AH Bolden and PM Lieberman. (1996). Transcription factor IIA mutations show activator-specific defects and reveal a IIA function distinct from stimulation of TBP-DNA binding. J Biol Chem 271:11182-11190.
9. Ozer J, K Mitsouras, D Zerby, M Carey and PM Lieberman. (1998). Transcription factor HA derepresses TATA-binding protein (TBP)-associated factor inhibition of TBP-DNA binding. J Biol Chem 273:14293-14300.
10. Ozer J, LE Lezina, J Ewing, S Audi and PM Lieberman. (1998). Association of transcription factor UA with TATA binding protein is required for transcriptional activation of a subset of promoters and cell cycle progression in Saccharomyces cerevisiae. Mol Cell Biol 18:2559-2570.
11. Tan S, Y Hunziker, DF Sargent and TJ Richmond. (1996). Crystal structure of a yeast TFIIA/TBP/DNA complex. Nature 381:127-151.
12. Hansen SK and R Tjian. (1995), TAFs and TFIIA mediate differential utilization of the tandem Adh promoters. Cell 82:565-575.
13. Bryant GO, LS Martel, SK Burley and AJ Berk. (1996). Radical mutations reveal TATA-box binding protein surfaces required for activated transcription in vivo. Genes Dev 10:2491-2504.
14. Ozer J, PA Moore and PM Lieberman. (2000). A testis-specific transcription factor ITA (TFIIAtau) stimulates TATA-binding protein-DNA binding and transcription activation. J Biol Chem 275:122-128.
15. Upadhyaya AB, SH Lee and J DeJong. (1999). Identification of a general transcription factor TFIIAalpha/beta homolog selectively expressed in testis, J Biol Chem 274:18040-18048.
16. Upadhyaya AB, M Khan, TC Mou, M Junker, DM Gray and J DeJong. (2002). The germ cell-specific transcription factor ALF. Structural properties and stabilization of the TATA-binding protein (TBP)-DNA complex. J Biol Chem 277:34208-34216.
17. Yokomori K, MP Zeidler, JL Chen, CP Verrijzer, M Mlodzik and R Tjian. (1994). Drosophila TFIIA directs cooperative DNA binding with TBP and mediates transcriptional activation. Genes Dev 8:2313-2323.
18. Andrews PW. (1984). Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro, Dev Biol 103:285-293.
19. Pleasure SJ, C Page and VM Lee. (1992). Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J Neurosci 12:1802-1815.
20. Andrews PW, SA Przyborski and JA Thomson. (2001). Embryonal Carcinoma Cells as Embryonic Stem Cells. Cold Spring Harbor Press, Cold Spring Harbor, New York.
21. Przyborski SA, VB Christie, MW Haynian, R Stewart and GM Horrocks. (2004). Human embryonal carcinoma cells: models of human embryonic development in man. Stem Cells Dev 13:400-408.
22. Stewart R, V Christie and SA Przyborski. (2003). Manipulation of human pluripotent embryonal carcinoma stem cells and the development of neural subtypes. Stem Cells 21:248-256.
23. Przyborski SA, IE Morton, A Wood and PW Andrews. (2000). Developmental regulation of neurogenesis in the pluripotent human embryonal carcinoma cell line NTERA-2. Eur J Neurosci 12:3521-3528.
24. Horton C and M Maden. (1995). Endogenous distribution of retinoids during normal development and teratogenesis in the mouse embryo. Dev Dyn 202:312-323.
25. Rossant J, R Zirngibl, D Cado, M Shago and V Giguère. (1991). Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogencsis. Genes Dev 5:1333-1344.
26. Giller T, U Hennes and HJ Kempen. (1995). Regulation of human apolipoprotein A-1 expression in Caco-2 and HepG2 cells by all-trans and 9-cis retinoic acids. J Lipid Res 36:1021-1028.
27. Ginsburg GS, J Ozer and SK Karathanasis. (1995). Intestinal apolipoprotein A1 gene transcription is regulated by multiple distinct DNA elements and is synergistically activated by the orphan nuclear receptor, hepatocyte nuclear factor 4. J Clin Invest 96:528-538.
28. Ivanov GS, JM Kater, SH Jha, EA Stutius. R Sabharwal, MD Tricarico, GS Ginsburg and JS Ozer. (2003). Sp and GATA factors are critical for Apolipoprotein A1 down-stream enhancer activity in human HepG2 cells. Gene 323:31-42.
29. Freemantle SJ, MJ Spinella and E Dmitrovsky. (2003). Retinoids in cancer therapy and chemoprevention: promise meets resistance. Oncogene 22:7305-7315.
30. Brewer GJ and CW Cotman. (1989). Survival and growth of hippocampal neurons in defined medium at low density: advantages of a sandwich culture technique or low oxygen. Brain Res 494:65-74.
31. Dignam JD, RM Lebovitz and RG Roeder. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nuclei Acids Res 11:1475-1489.
32. Dice JF. (1990). Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem Sci 15:305-309.
33. Russek SJ, S Bandyopadhyay and DH Farb. (2000). An initiator element mediates autologous downregulation of the human type A gamma-aminobutyric acid receptor beta 1 subunit gene. Proc Natl Acad Sci USA 97:8600-8605.
34. Mori N, F Kashanchi and D Prager. (1997). Repression of transcription from the human T-cell leukemia virus type I long terminal repeat and cellular gene promoters by wild-type p53. Blood 90:4924-4932.
35. Kees UR, SE Peroni, PR Ranford and J Ford. (1994). A new human cell line for the molecular dissection of the requirement for interleukin-1 in the production of interleukin-2 by immature T cells. J Immunol Methods 168:1-8.
36. Warrington JA, A Nair, M Mahadevappa and M Tsyganskaya. (2000). Comparison of human adult and fetal expression and identification of 535 housekeeping/maintenance genes. Physiol Genomics 2:143-147.
37. Caldwell MA, X He, N Wilkie, S Pollack, G Marshall, KA Wafford and CN Svendsen. (2001). Growth factors regulate the survival and fate of cells derived from human neurospheres. Nature Biotechnol 19:475-479.
38. Paquet-Durand F, S Tan and G Bicker. (2003). Turning teratocarcinoma cells into neurons: rapid differentiation of NT-2 cells in floating spheres. Brain Res Dev Brain Res 142:161-167.
39. Ferrington DA, AG Krainev and DJ Bigelow. (1998). Altered turnover of calcium regulatory proteins of the sarcoplasmic reticulum in aged skeletal muscle. J Biol Chem 273:5885-5891.
40. Perletti L, E Kopf, L Carré and I Davidson. (2001). Coordinate regulation of RARgamma2, TBP, and TAFIII35 by targeted proteolysis during retinoic acid-induced differentiation of F9 embryonal carcinoma cells. BMC Mol Biol 2:4.
41. Caccamo D, CD Katsetos, MM Herman, A Frankfurter, VP Collins and LJ Rubinstein. (1989). Immunohistochemistry of a spontaneous murine ovarian teratoma with neuroepithelial differentiation. Neuron-associated beta-tubulin as a marker for primitive neuroepithelium. Lab Invest 60:390-398.
42. Lee MK, JB Tuttle, LI Rebhum, DW Cleveland and A Frankfurter. (1990). The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton 17:118-132.
43. Rifkin JT, VJ Todd, LW Anderson and F Lefcort. (2000). Dynamic expression of neurotrophin receptors during sensory neuron genesis and differentiation. Dev Biol 227:465-480.
44. Moasser MM, VE Reuter and E Dmitrovsky. (1995). Overexpression of the retinoic acid receptor gamma directly induces terminal differentiation of human embryonal carcinoma cells. Oncogene 10:1537-1543.
45. Valcarcel R, M Meyer, M Meisterernst and HG Stunnenberg. (1997). Requirement of cofactors for RXR/RAR-mediated transcriptional activation in vitro, Biochim Biophys Acta 1350:229-234.
46. Gieni RS, Y Li and KT HayGlass. (1995). Comparison of [3H]thymidine incorporation with MTT- and MTS-based bioassays for human and murine IL-2 and IL-4 analysis. Tetrazolium assays provide markedly enhanced sensitivity, J Immunol Methods 187:85-93.
47. Gibson RM. (1999). Caspase activation is downstream of commitment to apoptosis of Ntera-2 neuronal cells. Exp Cell Res 251:203-212.
48. Taylor WR. (1986). The classification of amino acid conservation. J Theor Biol 119:205-218.
49. Katsetos CD, MM Herman and SJ Mörk. (2003). Class III beta-tubulin in human development and cancer. Cell Motil Cytoskeleton 55:77-96.
50. Kondo Y, L Shen, PS Yan, TH Huang and JP Issa. (2004). Chromatin immunoprecipitations microarrays for identification of genes silenced by histone H3 lysine 9 methylation. Proc Natl Acad Sci USA 101:7398-7403.
51. Willnow TE, J Hilpert, SA Armstrong, A Rohlmann, RE Hammer, DK Burns and J Herz. (1996). Defective forebrain development in mice lacking gp330/megalin. Proc Natl Acad Sci USA 93:8460-8464.
52. Alisi A, S Leoni, A Piacentani and L Conti Devirgiliis. (2003). Retinoic acid modulates the cell-cycle in fetal rat hepatocytes and HepG2 cells by regulating cyclin-cdk activities. Liver Int 23:179-186.
53. Falasca L, P Marcellini, C Ara, A Rufo and LC Devirgiliis. (1999). Growth inhibition and induction of specific hepatic phenotype expression by retinoic acid in HEPG2 cells. Anticancer Res 19:3283-3292.
54. Fu ZW, T Kubo, K Sugahara, T Noguchi and H Kato. (2001). Retinoid nutritional status differently affects the expression of Japanese quail retinoic acid receptor-beta isoform transcripts in a tissue-specific manner. J Endocrinol 169:281-290.
55. Beg AA, TS Finco, PV Nantermet and AS Baldwin Jr. (1993). Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of I kappa B alpha: a mechanism for NF-kappa B activation. Mol Cell Biol 13:3301-3310.
56. Tsutsumi T, A Ido, K Nakao, K Hamasaki, Y Kato, A Ohtsuru, K Nakata, T Tamaoki and S Nagataki. (1994). Reciprocal regulation of alpha-fetoprotein and albumin gene expression by butyrate in human hepatoma cells. Gastroenterology 107:499-504.
57. Emanuele S, A D'Anneo, G Bellavia, B Vassallo, M Lauricella, A De Blasio, R Vento and G Tesoriere. (2004). Sodium butyrate induces apoptosis in human hepatoma cells by a mitochondria/caspase pathway, associated with degradation of beta-catenin, pRb and Bel-XL. Eur J Cancer 40:1441-1452.
58. Chen W-J and JK Lin. (2004). Induction of G1 arrest and apoptosis in human jurkat T cells by pentagalloylglucose through inhibiting proteasome activity and elevating p27Kip1, p21Cip1/WAF1, and Bax proteins. J Biol Chem 279:13496-13505.
59. Yoo J, MJ Jeong, BM Kwon, MW Hur, YM Park and MY Han. (2002), Activation of dynamin I gene expression by Sp1 and Sp3 is required for neuron differentiation of N1E-115 cells. J Biol Chem 277:11904-11909.
60. Satoh J and Y Kuroda. (2000). Differential gene expression between human neurons and neuronal progenitor cells in culture: an analysis of arrayed cDNA clones in NTera2 human embryonal carcinoma cell line as a model system. J Neurosci Methods 94:155-164.
61. Um M, J Yamauchi, S Kato and JL Manley. (2001). Heterozygous disruption of the TATA-binding protein gene in DT40 cells causes reduced cdc25B phosphatase expression and delayed mitosis. Mol Cell Biol 21:2435-2448.
62. Johnson SA, L Dubeau, M Kawalek, A Dervan, AH Schonthal, CV Dang and DL Johnson. (2003). Increased expression of TATA-binding protein, the central transcription factor, can contribute to oncogenesis. Mol Cell Biol 23:3043-3051.
63. Collins MK, G Tanigawa, AM Kissonerghis, M Ritter, KM Price, S Tonegawa and MJ Owen. (1985). Regulation of T-cell receptor gene expression in human T-cell development. Proc Natl Acad Sci USA 82:4503-4507.
64. Johnson JE, K Zimmerman, T Saito and DJ Anderson. (1992). Induction and repression of mammalian achaetescute homologue (MASH) gene expression during neuronal differentiation of PI9 embryonal carcinoma cells. Development 114:75-87.
65. Chambers I, D Colby, M Robertson, J Nichols, S Lee, S Tweedie and A Smith. (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643-655.
66. Matsuda T, T Nakamura, K Nakao, T Arai, M Katsuki, T Heike and T Yokota. (1999). STAT3 activation is sufficient to maintain an undifferentialed state of mouse embryonic stem cells. EMBO J 18:4261-4269.
67. Okuda A, A Fukushima, M Nishimoto, A Orimo, T Yamagishi, Y Nabeshima, M Kuro-o, Y Nabeshima, K Boon, M Keaveney, HG Stunnenberg and M Muramatsu. (1998). UTF1, a novel transcriptional coactivator expressed in pluripoient embryonic stem cells and extra-embryonic cells. EMBO J 17:2019-2032.
68. Chandrasekaran K, PT Mora, L Nagarajan and WB Anderson. (1982). The amount of a specific cellular protein (p53) is a correlate of differentiation in embryonal carcinoma cells. J Cell Physiol 113:134-140.
69. Oren M, NC Reich and AJ Levine. (1982). Regulation of the cellular p53 tumor antigen in teratocarcinoma cells and their differentiated progeny. Mol Cell Biol 2:443-449.
70. Scholtz B, K Lamb, E Rosfjord, M Kingsley and A Rizzino. (1996). Appearance of nuclear protease activity after embryonal carcinoma cells undergo differentiation. Dev Biol 173:420-427.
71. McLean PJ, D Shpektor, S Bandyopadhyay, SJ Russek and DH Farb. (2000). A minimal promoter for the GABA(A) receptor alpha6-subunit gene controls tissue specificity. J Neurochem 74:1858-1869.
72. Parks CL and T Shenk. (1996). The serotonin 1a receptor gene contains a TATA-less promoter that responds to MAZ and Sp1. J Biol Chem 271:4417-4430.
73. Sugino H, Y Yoshihara, NG Copeland, DJ Gilbert, NA Jenkins and K Mori. (1997). Genomic organization and chromosomal localization of the mouse telencephalin gene, a neuronal member of the ICAM family. Genomics 43:209-215.
74. Wieczorek E, M Brand, X Jacq and L Tora. (1998). Function of TAF(II)-containing complex without TBP in transcription by RNA polymerase II. Nature 393:187-191.
75. Guillemot F. (1995). Analysis of the role of basic-helix-loop-helix transcription factors in the development of neural lineages in the mouse. Biol Cell 84:3-6.
76. Cheung WM, AH Chu, PW Chu and NY Ip. (2001). Cloning and expression of a novel nuclear matrix-associated protein that is regulated during the retinoic acid-induced neuronal differentiation. J Biol Chem 276:7083-17091.
77. Schoenherr CJ and DJ Anderson. (1995). The neuron-restrictive silencer factor (NRSF): a coordinate represser of multiple neuron-specific genes. Science 267:1360-1363.
78. Sakakibara S, Y Nakamura, H Satoh and H Okano. (2001), Rna-binding protein Musashi2: developmentally regulated expression in neural precursor cells und subpopulations of neurons in mammalian CNS. J Neurosci 21:8091-8107.
79. Levine RA, J Campisi, SY Wang and LJ Gudas. (1984). Butyrate inhibits the retinoic acid-induced differentiation of F9 teratocarcinoma stem cells. Dev Biol. 105:443-450.
80. Kruh J. (1982). Effects of sodium butyrale, a new pharmacological agent, on cells in culture. Mol Cell Biochem. 42:65-82.
81. McCue PA, ML Gubler, MI Sherman and BN Cohen. (1984). Sodium butyrale induces histone hyperacetylation and differentiation of murine embryonal carcinoma cells. J Cell Biol. 98:602-608.
82. Martin CA, LM Ziegler and JL Napoli. (1990). Retinoic acid, dibutyryl-cAMP, and differentiation affect the expression of retinoic acid receptors in F9 cells. Proc Natl Acad Sci USA 87:4804-4808.
83. Spinella MJ, S Kitareewan, B Mellado, D Sekula, KS Khoo and E Dmitrovsky. (1998). Specific retinoid receptors cooperate to signal growth suppression and maturation of human embryonal carcinoma cells. Oncogene 16:3471-3480.
84. Lim AC and RZ Qi. (2003). Cyclin-dependent kinases in neural development and degeneration. J Alzheimers Dis. 5:329-335.
85. Awad MM, H Enslen, JM Boylan, RJ Davis and PA Gruppuso. (2000). Growth regulation via p38 mitogen-activaled protein kinase in developing liver. J Biol Chem 275:38716-38721.
86. Ram PT and RM Schultz. (1993). Reporter gene expression in G2 of the 1-cell mouse embryo. Dev Biol 156:552-556.
87. Bai G and JW Kusiak. (1993). Cloning and analysis of the 5′ flanking sequence of the rat N-methyl-D-aspartate receptor 1 (NMDARI) gene. Biochim Biophys Acta 1152:197-200.
88. Suchanek B, PH Seeburg and R Sprengel. (1995). Gene structure of the Murine N-melhyl-D-aspartale receptor subunit NR2C. J Biol Chem 270:41-44.
89. Wepsic HT. (1983). Overview of oncofetal antigens in cancer. Ann Clin Lab Sci 13:261-266.
90. Sell S, FF Becker, HL Leffert and L Watabe. (1976). Expression of an oncodevelopmental gene product (alpha-fetoprotein) during fetal development and adult oncogenesis. Cancer Res 36:4239-4249.
91. Tomasi TB, Jr. (1977). Structure and function of alpha-fetoprotein. Annu Rev Med 28:453-465.
92. Hanausek M, J Szemraj, AK Adams and Z Walaszek. (1996). The oncofetal protein p65: a new member of the steroid/thyroid receptor superfamily. Cancer Detect Prev 20:94-102.
93. Itzkowitz SH and X Yio. (2004). Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 287:G7-G17.