Gene-specific transcriptional activation mediated by the p150 subunit of the chromatin assembly factor 1

Sung-Bau Lee, Derick S C Ou, Chung-Fan Lee, Li-Jung Juan

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Chromatin assembly factor 1 contains three subunits, p150, p60, and p48. It is essential for coupling nucleosome assembly to newly synthesized DNA. Whether chromatin assembly factor 1 subunits have functions beyond escorting histones, which depends on the complex formation of p150 and p60, has been an issue of great interest. This study reveals a novel role of p150, but not p60, in gene-specific transcriptional activation. We found that p150 transcriptionally activated an essential viral promoter, the major immediate early promoter (MIEP) of the human cytomegalovirus, independently of p60. Knocking down p150 decreased the MIEP function in both transfected and virally infected cells. The chromatin immunoprecipitation analysis and the in vitro protein-DNA binding assay demonstrated that p150 used its KER domain to associate with the MIEP from -593 to -574 bp. The N-terminal 244 residues were also found essential for p150-mediated MIEP activation, likely through recruiting the acetyltransferase p300 to acetylate local histones. Domain swapping experiments further showed that the KER and theNterminus of p150 acted as an independent DNA binding and transcriptional activation domain, respectively. Because p60 did not seem involved in the reaction, together these results indicate for the first time that p150 directly activates transcription, independently of its histone deposition function. © 2009 by The American Society for Biochemistry and Molecular Biology, Inc.
Original languageEnglish
Pages (from-to)14040-14049
Number of pages10
JournalJournal of Biological Chemistry
Volume284
Issue number21
DOIs
Publication statusPublished - 2009
Externally publishedYes

Fingerprint

Chromatin Assembly Factor-1
Histones
Transcriptional Activation
Genes
Chemical activation
Nucleosomes
Chromatin Immunoprecipitation
DNA
DNA-Binding Proteins
Transcription
Cytomegalovirus
Chromatin
Assays
Experiments

Keywords

  • Acetyl transferase
  • Chromatin assembly
  • Chromatin immunoprecipitation analysis
  • Complex formations
  • DNA binding
  • Domain swapping
  • Human cytomegalovirus
  • In-vitro
  • Infected cells
  • N-terminal
  • Nucleosome assembly
  • Protein-DNA binding
  • Transcriptional activation domain
  • Transcriptional activations
  • Viral promoters
  • Genes
  • Nucleic acids
  • Transcription
  • DNA
  • acyltransferase
  • acyltransferase p300
  • arginine
  • chromatin assembly factor 1
  • chromatin assembly factor 1 subunit p150
  • chromatin assembly factor 1 subunit p60
  • glutamic acid
  • histone
  • lysine
  • unclassified drug
  • chromatin assembly factor I
  • DNA binding protein
  • histone acetyltransferase PCAF
  • immediate early protein
  • nonhistone protein
  • p300-CBP-associated factor
  • protein subunit
  • amino terminal sequence
  • article
  • chromatin assembly and disassembly
  • chromatin immunoprecipitation
  • controlled study
  • cytomegalovirus infection
  • human
  • human cell
  • in vitro study
  • major immediate early promoter
  • priority journal
  • promoter region
  • protein DNA binding
  • protein domain
  • protein function
  • transcription initiation
  • base pairing
  • chemistry
  • Cytomegalovirus
  • gene expression regulation
  • genetic transfection
  • genetics
  • metabolism
  • protein binding
  • protein tertiary structure
  • tumor cell line
  • Human herpesvirus 5
  • Base Pairing
  • Cell Line, Tumor
  • Chromosomal Proteins, Non-Histone
  • DNA-Binding Proteins
  • Gene Expression Regulation, Viral
  • Humans
  • Immediate-Early Proteins
  • p300-CBP Transcription Factors
  • Promoter Regions, Genetic
  • Protein Binding
  • Protein Structure, Tertiary
  • Protein Subunits
  • Transcriptional Activation
  • Transfection

Cite this

Gene-specific transcriptional activation mediated by the p150 subunit of the chromatin assembly factor 1. / Lee, Sung-Bau; Ou, Derick S C; Lee, Chung-Fan; Juan, Li-Jung.

In: Journal of Biological Chemistry, Vol. 284, No. 21, 2009, p. 14040-14049.

Research output: Contribution to journalArticle

Lee, Sung-Bau ; Ou, Derick S C ; Lee, Chung-Fan ; Juan, Li-Jung. / Gene-specific transcriptional activation mediated by the p150 subunit of the chromatin assembly factor 1. In: Journal of Biological Chemistry. 2009 ; Vol. 284, No. 21. pp. 14040-14049.
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title = "Gene-specific transcriptional activation mediated by the p150 subunit of the chromatin assembly factor 1",
abstract = "Chromatin assembly factor 1 contains three subunits, p150, p60, and p48. It is essential for coupling nucleosome assembly to newly synthesized DNA. Whether chromatin assembly factor 1 subunits have functions beyond escorting histones, which depends on the complex formation of p150 and p60, has been an issue of great interest. This study reveals a novel role of p150, but not p60, in gene-specific transcriptional activation. We found that p150 transcriptionally activated an essential viral promoter, the major immediate early promoter (MIEP) of the human cytomegalovirus, independently of p60. Knocking down p150 decreased the MIEP function in both transfected and virally infected cells. The chromatin immunoprecipitation analysis and the in vitro protein-DNA binding assay demonstrated that p150 used its KER domain to associate with the MIEP from -593 to -574 bp. The N-terminal 244 residues were also found essential for p150-mediated MIEP activation, likely through recruiting the acetyltransferase p300 to acetylate local histones. Domain swapping experiments further showed that the KER and theNterminus of p150 acted as an independent DNA binding and transcriptional activation domain, respectively. Because p60 did not seem involved in the reaction, together these results indicate for the first time that p150 directly activates transcription, independently of its histone deposition function. {\circledC} 2009 by The American Society for Biochemistry and Molecular Biology, Inc.",
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author = "Sung-Bau Lee and Ou, {Derick S C} and Chung-Fan Lee and Li-Jung Juan",
note = "被引用次數:7 Export Date: 28 March 2016 CODEN: JBCHA 通訊地址: Juan, L.-J.; Genomics Research Center, Academia Sinica, 128 Academia Rd., Nankang, Taipei 115, Taiwan; 電子郵件: ljjuan@gate.sinica.edu.tw 化學物質/CAS: acyltransferase, 9012-30-0, 9054-54-0; arginine, 1119-34-2, 15595-35-4, 7004-12-8, 74-79-3; glutamic acid, 11070-68-1, 138-15-8, 56-86-0, 6899-05-4; histone, 9062-68-4; lysine, 56-87-1, 6899-06-5, 70-54-2; Chromosomal Proteins, Non-Histone; DNA-Binding Proteins; Immediate-Early Proteins; Protein Subunits; chromatin assembly factor I; p300-CBP Transcription Factors, 2.3.1.48; p300-CBP-associated factor, 2.3.1.48 參考文獻: Kaufman, P.D., Kobayasho, R., Kessler, N., Stillman, B., (1995) Cell, 81, pp. 1105-1114; Takami, Y., Ono, T., Fukagawa, T., Shibahara, K., Nakayama, T., (2007) Mol. Biol. Cell, 18, pp. 129-141; Nabatiyan, A., Krude, T., (2004) Mol. Cell. Biol, 24, pp. 2853-2862; Hoek, M., Stillman, B., (2003) Proc. Natl. Acad. Sci. U. S. A, 100, pp. 12183-12188; Shibahara, K., Stillman, B., (1999) Cell, 96, pp. 575-585; Moggs, J.G., Grandi, P., Quivy, J.P., Jonsson, Z.O., Hubscher, U., Becker, P.B., Almouzni, G., (2000) Mol. Cell. Biol, 20, pp. 1206-1218; Verreault, A., Kaufman, P.D., Kobayashi, R., Stillman, B., (1996) Cell, 87, pp. 95-104; Rogers, S., Wells, R., Rechsteiner, M., (1986) Science, 234, pp. 364-368; Belizario, J.E., Alves, J., Garay-Malpartida, M., Occhiucci, J.M., (2008) Curr. Protein Pept. Sci, 9, pp. 210-220; Enomoto, S., Berman, J., (1998) Genes Dev, 12, pp. 219-232; Monson, E.K., de Bruin, D., Zakian, V.A., (1997) Proc. Natl. Acad. Sci. U. S. A, 94, pp. 13081-13086; Huang, S., Zhou, H., Tarara, J., Zhang, Z., (2007) EMBO J, 26, pp. 2274-2283; Ramirez-Parra, E., Gutierrez, C., (2007) Trends Plant Sci, 12, pp. 570-576; Quivy, J.P., Roche, D., Kirschner, D., Tagami, H., Nakatani, Y., Almouzni, G., (2004) EMBO J, 23, pp. 3516-3526; Zabaronick, S.R., Tyler, J.K., (2005) Mol. Cell. Biol, 25, pp. 652-660; Schonrock, N., Exner, V., Probst, A., Gruissem, W., Hennig, L., (2006) J. Biol. Chem, 281, pp. 9560-9568; Kitagawa, H., Fujiki, R., Yoshimura, K., Mezaki, Y., Uematsu, Y., Matsui, D., Ogawa, S., Kato, S., (2003) Cell, 113, pp. 905-917; Marheineke, K., Krude, T., (1998) J. Biol. Chem, 273, pp. 15279-15286; Quivy, J.P., Gerard, A., Cook, A.J., Roche, D., Almouzni, G., (2008) Nat. Struct. Mol. Biol, 15, pp. 972-979; Murzina, N., Verreault, A., Laue, E., Stillman, B., (1999) Mol. Cell, 4, pp. 529-540; Reese, B.E., Bachman, K.E., Baylin, S.B., Rountree, M.R., (2003) Mol. Cell. Biol, 23, pp. 3226-3236; Qian, Y.W., Wang, Y.C., Hollingsworth Jr., R.E., Jones, D., Ling, N., Lee, E.Y., (1993) Nature, 364, pp. 648-652; Parthun, M.R., Widom, J., Gottschling, D.E., (1996) Cell, 87, pp. 85-94; Huang, C.F., Wang, Y.C., Tsao, D.A., Tung, S.F., Lin, Y.S., Wu, C.W., (2000) J. Biol. Chem, 275, pp. 12313-12320; Ye, X., Franco, A.A., Santos, H., Nelson, D.M., Kaufman, P.D., Adams, P.D., (2003) Mol. Cell, 11, pp. 341-351; Spaete, R.R., Mocarski, E.S., (1987) Proc. Natl. Acad. Sci. U. S. A, 84, pp. 7213-7217; Hsu, C.H., Chang, M.D., Tai, K.Y., Yang, Y.T., Wang, P.S., Chen, C.J., Wang, Y.H., Juan, L.J., (2004) EMBO J, 23, pp. 2269-2280; Ruthenburg, A.J., Li, H., Patel, D.J., Allis, C.D., (2007) Nat. Rev. Mol. Cell Biol, 8, pp. 983-994; Jones, M.H., Hamana, N., Nezu, J., Shimane, M., (2000) Genomics, 63, pp. 40-45; Banks, G.C., Mohr, B., Reeves, R., (1999) J. Biol. Chem, 274, pp. 16536-16544; Park, Y.J., Luger, K., (2006) Biochem. Cell Biol, 84, pp. 549-558; Compagnone, N.A., Zhang, P., Vigne, J.L., Mellon, S.H., (2000) Mol. Endocrinol, 14, pp. 875-888",
year = "2009",
doi = "10.1074/jbc.M901833200",
language = "English",
volume = "284",
pages = "14040--14049",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "21",

}

TY - JOUR

T1 - Gene-specific transcriptional activation mediated by the p150 subunit of the chromatin assembly factor 1

AU - Lee, Sung-Bau

AU - Ou, Derick S C

AU - Lee, Chung-Fan

AU - Juan, Li-Jung

N1 - 被引用次數:7 Export Date: 28 March 2016 CODEN: JBCHA 通訊地址: Juan, L.-J.; Genomics Research Center, Academia Sinica, 128 Academia Rd., Nankang, Taipei 115, Taiwan; 電子郵件: ljjuan@gate.sinica.edu.tw 化學物質/CAS: acyltransferase, 9012-30-0, 9054-54-0; arginine, 1119-34-2, 15595-35-4, 7004-12-8, 74-79-3; glutamic acid, 11070-68-1, 138-15-8, 56-86-0, 6899-05-4; histone, 9062-68-4; lysine, 56-87-1, 6899-06-5, 70-54-2; Chromosomal Proteins, Non-Histone; DNA-Binding Proteins; Immediate-Early Proteins; Protein Subunits; chromatin assembly factor I; p300-CBP Transcription Factors, 2.3.1.48; p300-CBP-associated factor, 2.3.1.48 參考文獻: Kaufman, P.D., Kobayasho, R., Kessler, N., Stillman, B., (1995) Cell, 81, pp. 1105-1114; Takami, Y., Ono, T., Fukagawa, T., Shibahara, K., Nakayama, T., (2007) Mol. Biol. Cell, 18, pp. 129-141; Nabatiyan, A., Krude, T., (2004) Mol. Cell. Biol, 24, pp. 2853-2862; Hoek, M., Stillman, B., (2003) Proc. Natl. Acad. Sci. U. S. A, 100, pp. 12183-12188; Shibahara, K., Stillman, B., (1999) Cell, 96, pp. 575-585; Moggs, J.G., Grandi, P., Quivy, J.P., Jonsson, Z.O., Hubscher, U., Becker, P.B., Almouzni, G., (2000) Mol. Cell. Biol, 20, pp. 1206-1218; Verreault, A., Kaufman, P.D., Kobayashi, R., Stillman, B., (1996) Cell, 87, pp. 95-104; Rogers, S., Wells, R., Rechsteiner, M., (1986) Science, 234, pp. 364-368; Belizario, J.E., Alves, J., Garay-Malpartida, M., Occhiucci, J.M., (2008) Curr. Protein Pept. Sci, 9, pp. 210-220; Enomoto, S., Berman, J., (1998) Genes Dev, 12, pp. 219-232; Monson, E.K., de Bruin, D., Zakian, V.A., (1997) Proc. Natl. Acad. Sci. U. S. A, 94, pp. 13081-13086; Huang, S., Zhou, H., Tarara, J., Zhang, Z., (2007) EMBO J, 26, pp. 2274-2283; Ramirez-Parra, E., Gutierrez, C., (2007) Trends Plant Sci, 12, pp. 570-576; Quivy, J.P., Roche, D., Kirschner, D., Tagami, H., Nakatani, Y., Almouzni, G., (2004) EMBO J, 23, pp. 3516-3526; Zabaronick, S.R., Tyler, J.K., (2005) Mol. Cell. Biol, 25, pp. 652-660; Schonrock, N., Exner, V., Probst, A., Gruissem, W., Hennig, L., (2006) J. Biol. Chem, 281, pp. 9560-9568; Kitagawa, H., Fujiki, R., Yoshimura, K., Mezaki, Y., Uematsu, Y., Matsui, D., Ogawa, S., Kato, S., (2003) Cell, 113, pp. 905-917; Marheineke, K., Krude, T., (1998) J. Biol. Chem, 273, pp. 15279-15286; Quivy, J.P., Gerard, A., Cook, A.J., Roche, D., Almouzni, G., (2008) Nat. Struct. Mol. Biol, 15, pp. 972-979; Murzina, N., Verreault, A., Laue, E., Stillman, B., (1999) Mol. Cell, 4, pp. 529-540; Reese, B.E., Bachman, K.E., Baylin, S.B., Rountree, M.R., (2003) Mol. Cell. Biol, 23, pp. 3226-3236; Qian, Y.W., Wang, Y.C., Hollingsworth Jr., R.E., Jones, D., Ling, N., Lee, E.Y., (1993) Nature, 364, pp. 648-652; Parthun, M.R., Widom, J., Gottschling, D.E., (1996) Cell, 87, pp. 85-94; Huang, C.F., Wang, Y.C., Tsao, D.A., Tung, S.F., Lin, Y.S., Wu, C.W., (2000) J. Biol. Chem, 275, pp. 12313-12320; Ye, X., Franco, A.A., Santos, H., Nelson, D.M., Kaufman, P.D., Adams, P.D., (2003) Mol. Cell, 11, pp. 341-351; Spaete, R.R., Mocarski, E.S., (1987) Proc. Natl. Acad. Sci. U. S. A, 84, pp. 7213-7217; Hsu, C.H., Chang, M.D., Tai, K.Y., Yang, Y.T., Wang, P.S., Chen, C.J., Wang, Y.H., Juan, L.J., (2004) EMBO J, 23, pp. 2269-2280; Ruthenburg, A.J., Li, H., Patel, D.J., Allis, C.D., (2007) Nat. Rev. Mol. Cell Biol, 8, pp. 983-994; Jones, M.H., Hamana, N., Nezu, J., Shimane, M., (2000) Genomics, 63, pp. 40-45; Banks, G.C., Mohr, B., Reeves, R., (1999) J. Biol. Chem, 274, pp. 16536-16544; Park, Y.J., Luger, K., (2006) Biochem. Cell Biol, 84, pp. 549-558; Compagnone, N.A., Zhang, P., Vigne, J.L., Mellon, S.H., (2000) Mol. Endocrinol, 14, pp. 875-888

PY - 2009

Y1 - 2009

N2 - Chromatin assembly factor 1 contains three subunits, p150, p60, and p48. It is essential for coupling nucleosome assembly to newly synthesized DNA. Whether chromatin assembly factor 1 subunits have functions beyond escorting histones, which depends on the complex formation of p150 and p60, has been an issue of great interest. This study reveals a novel role of p150, but not p60, in gene-specific transcriptional activation. We found that p150 transcriptionally activated an essential viral promoter, the major immediate early promoter (MIEP) of the human cytomegalovirus, independently of p60. Knocking down p150 decreased the MIEP function in both transfected and virally infected cells. The chromatin immunoprecipitation analysis and the in vitro protein-DNA binding assay demonstrated that p150 used its KER domain to associate with the MIEP from -593 to -574 bp. The N-terminal 244 residues were also found essential for p150-mediated MIEP activation, likely through recruiting the acetyltransferase p300 to acetylate local histones. Domain swapping experiments further showed that the KER and theNterminus of p150 acted as an independent DNA binding and transcriptional activation domain, respectively. Because p60 did not seem involved in the reaction, together these results indicate for the first time that p150 directly activates transcription, independently of its histone deposition function. © 2009 by The American Society for Biochemistry and Molecular Biology, Inc.

AB - Chromatin assembly factor 1 contains three subunits, p150, p60, and p48. It is essential for coupling nucleosome assembly to newly synthesized DNA. Whether chromatin assembly factor 1 subunits have functions beyond escorting histones, which depends on the complex formation of p150 and p60, has been an issue of great interest. This study reveals a novel role of p150, but not p60, in gene-specific transcriptional activation. We found that p150 transcriptionally activated an essential viral promoter, the major immediate early promoter (MIEP) of the human cytomegalovirus, independently of p60. Knocking down p150 decreased the MIEP function in both transfected and virally infected cells. The chromatin immunoprecipitation analysis and the in vitro protein-DNA binding assay demonstrated that p150 used its KER domain to associate with the MIEP from -593 to -574 bp. The N-terminal 244 residues were also found essential for p150-mediated MIEP activation, likely through recruiting the acetyltransferase p300 to acetylate local histones. Domain swapping experiments further showed that the KER and theNterminus of p150 acted as an independent DNA binding and transcriptional activation domain, respectively. Because p60 did not seem involved in the reaction, together these results indicate for the first time that p150 directly activates transcription, independently of its histone deposition function. © 2009 by The American Society for Biochemistry and Molecular Biology, Inc.

KW - Acetyl transferase

KW - Chromatin assembly

KW - Chromatin immunoprecipitation analysis

KW - Complex formations

KW - DNA binding

KW - Domain swapping

KW - Human cytomegalovirus

KW - In-vitro

KW - Infected cells

KW - N-terminal

KW - Nucleosome assembly

KW - Protein-DNA binding

KW - Transcriptional activation domain

KW - Transcriptional activations

KW - Viral promoters

KW - Genes

KW - Nucleic acids

KW - Transcription

KW - DNA

KW - acyltransferase

KW - acyltransferase p300

KW - arginine

KW - chromatin assembly factor 1

KW - chromatin assembly factor 1 subunit p150

KW - chromatin assembly factor 1 subunit p60

KW - glutamic acid

KW - histone

KW - lysine

KW - unclassified drug

KW - chromatin assembly factor I

KW - DNA binding protein

KW - histone acetyltransferase PCAF

KW - immediate early protein

KW - nonhistone protein

KW - p300-CBP-associated factor

KW - protein subunit

KW - amino terminal sequence

KW - article

KW - chromatin assembly and disassembly

KW - chromatin immunoprecipitation

KW - controlled study

KW - cytomegalovirus infection

KW - human

KW - human cell

KW - in vitro study

KW - major immediate early promoter

KW - priority journal

KW - promoter region

KW - protein DNA binding

KW - protein domain

KW - protein function

KW - transcription initiation

KW - base pairing

KW - chemistry

KW - Cytomegalovirus

KW - gene expression regulation

KW - genetic transfection

KW - genetics

KW - metabolism

KW - protein binding

KW - protein tertiary structure

KW - tumor cell line

KW - Human herpesvirus 5

KW - Base Pairing

KW - Cell Line, Tumor

KW - Chromosomal Proteins, Non-Histone

KW - DNA-Binding Proteins

KW - Gene Expression Regulation, Viral

KW - Humans

KW - Immediate-Early Proteins

KW - p300-CBP Transcription Factors

KW - Promoter Regions, Genetic

KW - Protein Binding

KW - Protein Structure, Tertiary

KW - Protein Subunits

KW - Transcriptional Activation

KW - Transfection

U2 - 10.1074/jbc.M901833200

DO - 10.1074/jbc.M901833200

M3 - Article

VL - 284

SP - 14040

EP - 14049

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 21

ER -