DOI: 10.1146/annurev.genet.38.072902.091907. Epigenetic Regulation of Cellular Memory by the Polycomb and Trithorax Group Proteins

Epigenetic Regulation of Cellular Memory by the Polycomb and Trithorax Group Proteins

10.1146/annurev.genet.38.072902.091907

Crossref journal-article

Annual Reviews

Annual Review of Genetics (22)

Abstract

▪ Abstract During the development of multicellular organisms, cells become different from one another by changing their genetic program in response to transient stimuli. Long after the stimulus is gone, “cellular memory” mechanisms enable cells to remember their chosen fate over many cell divisions. The Polycomb and Trithorax groups of proteins, respectively, work to maintain repressed or active transcription states of developmentally important genes through many rounds of cell division. Here we review current ideas on the protein and DNA components of this transcriptional memory system and how they interact dynamically with each other to orchestrate cellular memory for several hundred genes.

Bibliography

Ringrose, L., & Paro, R. (2004). Epigenetic Regulation of Cellular Memory by the Polycomb and Trithorax Group Proteins. Annual Review of Genetics, 38(1), 413â443.

Authors 2

Leonie Ringrose (first)
Renato Paro (additional)

References 134 Referenced 853

Deleted in proof
10.1093/genetics/160.4.1561 / Genetics by Americo J (2002)
10.1093/emboj/cdg124
10.1101/gad.269503
10.1242/dev.127.4.779 / Development by Barges S (2000)
10.1006/scel.1995.0026
10.1038/nature01126
10.1016/j.ydbio.2004.01.006
10.1242/dev.129.21.4923 / Development by Bender W (2002)
10.1242/dev.128.6.993 / Development by Beuchle D (2001)
10.1242/dev.127.7.1541 / Development by Bevilacqua A (2000)
10.1016/S0012-1606(03)00314-2
10.1093/genetics/164.1.195 / Genetics by Boivin A (2003)
10.1038/35088090
10.1016/S0959-437X(00)00176-3
10.1242/dev.00204
10.1083/jcb.141.2.469
10.1242/dev.124.21.4343 / Development by Busturia A (1997)
10.1126/science.1076997
10.1016/S0092-8674(00)81181-2
10.1126/science.286.5441.955
10.1002/j.1460-2075.1994.tb06545.x
10.1002/j.1460-2075.1993.tb05856.x
10.1128/MCB.24.8.3157-3167.2004
10.1126/science.1078572
10.1002/j.1460-2075.1995.tb07197.x
10.1093/emboj/18.24.7029
10.1101/gad.854300
10.1016/S0076-6879(03)77004-9
10.1016/S0092-8674(02)00975-3
10.1038/sj.emboj.7600108
10.1016/S1097-2765(04)00128-5
{'key': 'B33', 'first-page': '4736', 'volume': '62', 'author': 'Dimri GP', 'year': '2002', 'journal-title': 'Cancer Res.'} / Cancer Res. by Dimri GP (2002)
10.1128/MCB.23.4.1181-1195.2003
10.1016/0925-4773(95)00412-T
10.1126/science.1078694
10.1101/gad.1110503
10.1038/nature02017
10.1016/S1097-2765(01)00316-1
10.1242/dev.126.17.3905 / Development by Fritsch C (1999)
10.1002/gene.10173
10.1038/ncb1077
10.1093/genetics/139.2.797 / Genetics by Gindhart JG (1995)
10.1038/scientificamerican1168-110
10.1093/genetics/146.4.1365 / Genetics by Hagstrom K (1997)
10.1073/pnas.96.25.14372
10.1128/MCB.21.14.4528-4543.2001
10.1242/dev.129.21.4915 / Development by Hogga I (2002)
10.1128/MCB.20.9.3187-3197.2000
10.1016/S1360-1385(03)00189-4
10.1016/S0076-6879(03)77016-5
10.1128/MCB.22.17.6261-6271.2002
10.1242/dev.129.6.1339 / Development by Hur M (2002)
10.1093/nar/23.21.4457
10.1101/gad.13.20.2678
10.1006/scdb.1999.0304
{'key': 'B57', 'first-page': '151', 'volume': '1602', 'author': 'Jacobs JJ', 'year': '2002', 'journal-title': 'Biochim. Biophys. Acta'} / Biochim. Biophys. Acta by Jacobs JJ (2002)
10.1534/genetics.166.1.187
10.1016/S0092-8674(03)00159-4
10.1101/gad.14.9.1058 / Genes Dev. by Kal AJ (2000)
10.1093/genetics/136.3.1025 / Genetics by Kassis JA (1994)
10.1093/emboj/18.3.698
10.1146/annurev.ge.29.120195.001445
10.1016/S0076-6879(03)77003-7
{'key': 'B65', 'first-page': '453', 'volume': '9', 'author': 'Kim CA', 'year': '2002', 'journal-title': 'Nat. Struct. Biol.'} / Nat. Struct. Biol. by Kim CA (2002)
10.1038/sj.embor.7400111
10.1101/gad.1035902
10.1242/jcs.00493
10.1073/pnas.94.8.3602
10.1016/S1097-2765(04)00006-1
{'key': 'B71', 'volume-title': 'The Making of a Fly', 'author': 'Lawrence PA', 'year': '1992'} / The Making of a Fly by Lawrence PA (1992)
10.1038/nature01572
10.1128/MCB.22.17.6070-6078.2002
10.1073/pnas.92.18.8403
10.1093/emboj/21.7.1775
10.1093/nar/gkg479
10.1101/gad.242702
10.1007/BF00583898
10.1242/dev.124.9.1809 / Development by Mihaly J (1997)
10.1016/S1097-2765(02)00741-4
10.1101/gad.269603
10.1128/MCB.21.4.1311-1318.2001
10.1007/s00418-003-0551-2
10.1128/MCB.22.21.7473-7483.2002
10.1128/MCB.24.8.3077-3088.2004
10.1038/nature02060
10.1101/gad.1143303
10.1242/dev.121.9.2847 / Development by Müller J (1995)
10.1016/S0092-8674(02)00976-5
10.1093/genetics/153.3.1333 / Genetics by Muller M (1999)
10.1038/sj.emboj.7600013
10.1038/sj.onc.1207904
10.1242/dev.01003
10.1093/emboj/17.17.5141
10.1016/0959-437X(95)80005-0
10.1016/S0959-437X(03)00108-4
10.1242/dev.125.20.3955 / Development by Papoulas O (1998)
10.1073/pnas.93.7.2822
10.1093/genetics/136.4.1341 / Genetics by Pelegri F (1994)
10.1126/science.1065683
10.1016/S1534-5807(03)00164-3
10.1093/genetics/141.4.1439 / Genetics by Pirrotta V (1995)
10.1002/j.1460-2075.1995.tb00069.x
10.1007/BF00352263
10.1126/science.1084274
10.1242/dev.129.10.2483 / Development by Poux S (2002)
10.1242/dev.128.1.75 / Development by Poux S (2001)
10.1101/gad.208901
10.1016/j.jmb.2004.01.051
10.1128/MCB.22.22.8026-8034.2002
10.1002/j.1460-2075.1993.tb05795.x
10.1002/bies.1082
10.1016/S1534-5807(03)00337-X
10.1093/emboj/20.24.7137
10.1128/MCB.19.9.6441
10.1038/35088096
10.1242/dev.01084
10.1016/S0076-6879(03)77017-7
10.1016/S1534-5807(03)00068-6
10.1242/dev.114.2.493 / Development by Simon J (1992)
10.1006/dbio.1993.1174
10.1016/S0959-437X(02)00288-5
10.1038/ncb1088
10.1093/emboj/16.12.3621
10.1128/MCB.17.12.6773
10.1242/dev.128.2.275 / Development by Tie F (2001)
10.1128/MCB.23.9.3352-3362.2003
10.1128/MCB.19.7.5189
10.1093/genetics/143.2.913 / Genetics by Tripoulas N (1996)
10.1002/(SICI)1526-968X(200001)26:1<67::AID-GENE9>3.0.CO;2-2
10.1016/j.molcel.2004.05.009
10.1093/nar/23.21.4353
10.1002/j.1460-2075.1991.tb07931.x
10.1038/337468a0

Dates

Type	When
Created	20 years, 9 months ago (Nov. 2, 2004, 10:16 a.m.)
Deposited	2 years, 3 months ago (April 29, 2023, 5:38 p.m.)
Indexed	9 hours, 23 minutes ago (Aug. 29, 2025, 6:04 a.m.)
Issued	20 years, 8 months ago (Dec. 1, 2004)
Published	20 years, 8 months ago (Dec. 1, 2004)
Published Print	20 years, 8 months ago (Dec. 1, 2004)

Funders 0

None

BibTeX

@article{Ringrose_2004, title={Epigenetic Regulation of Cellular Memory by the Polycomb and Trithorax Group Proteins}, volume={38}, ISSN={1545-2948}, url={http://dx.doi.org/10.1146/annurev.genet.38.072902.091907}, DOI={10.1146/annurev.genet.38.072902.091907}, number={1}, journal={Annual Review of Genetics}, publisher={Annual Reviews}, author={Ringrose, Leonie and Paro, Renato}, year={2004}, month=dec, pages={413–443} }

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