DOI: 10.1073/pnas.0603728103. Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development

Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development

10.1073/pnas.0603728103

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

In maturing T lineage cells, the helix–loop–helix protein E47 has been shown to enforce a critical proliferation and developmental checkpoint commonly referred to as β selection. To examine how E47 regulates cellular expansion and developmental progression, we have used an E2A-deficient lymphoma cell line and DNA microarray analysis to identify immediate E47 target genes. Hierarchical cluster analysis of gene expression patterns revealed that E47 coordinately regulates the expression of genes involved in cell survival, cell cycle progression, lipid metabolism, stress response, and lymphoid maturation. These include Plcγ2, Cdk6, CD25, Tox, Gadd45a, Gadd45b, Gfi1, Gfi1b, Socs1, Socs3, Id2, Eto2, and Xbp1. We propose a regulatory network linking Janus kinase (JAK)/signal transducer and activator of transcription (STAT)-mediated signaling, E47, and suppressor of cytokine signaling (SOCS) proteins in a common pathway. Finally, we suggest that the aberrant activation of Cdk6 in E47-deficient T lineage cells contributes to the development of lymphoid malignancy.

Bibliography

Schwartz, R., Engel, I., Fallahi-Sichani, M., Petrie, H. T., & Murre, C. (2006). Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development. Proceedings of the National Academy of Sciences, 103(26), 9976â9981.

Authors 5

Ruth Schwartz (first)
Isaac Engel (additional)
Mohammad Fallahi-Sichani (additional)
Howard T. Petrie (additional)
Cornelis Murre (additional)

References 44 Referenced 111

10.1038/ni1260
10.1016/0092-8674(94)90077-9
10.1016/0092-8674(94)90076-0
10.1111/j.1600-065X.2000.imr017514.x
10.1128/MCB.17.8.4782
10.1084/jem.186.9.1597
10.1128/MCB.20.18.6677-6685.2000
10.1084/jem.194.6.733
10.1016/S1074-7613(02)00264-9
10.1038/84273
10.1038/sj.emboj.7600017
10.1084/jem.190.11.1605
10.1016/S1074-7613(00)80155-7
10.1128/MCB.17.12.7317
10.1073/pnas.96.3.996
10.1038/ni923
C. Penit, B. Lucas, F. F. Vasseur J. Immunol. 154, 5103–5113 (1995). (10.4049/jimmunol.154.10.5103) / J. Immunol. by Penit C. (1995)
10.4049/jimmunol.173.2.1094
10.1128/MCB.17.10.5888
E. D. Cueva, I. Garcia-Cao, M. Herranz, P. Lopez, P. Garcia-Palencia, J. M. Flores, M. Serranto, J. Fernandez-Piqueras, J. Martin-Caballero Oncogene 6, 1–5 (2006). / Oncogene by Cueva E. D. (2006)
10.1073/pnas.86.24.10128
10.1002/j.1460-2075.1990.tb08126.x
10.1016/j.ccr.2004.05.023
10.1016/S0037-1963(03)00195-1
10.1016/S1535-6108(02)00018-1
10.1128/MCB.16.1.121
10.1126/science.1097937
10.1126/science.1071914
10.1111/j.0105-2896.2006.00345.x
10.1038/ni767
10.1038/35085509
10.1083/jcb.200408117
10.1038/nri979
10.1126/science.1092009
10.1038/ni844
10.1016/S1074-7613(00)00028-5
10.1084/jem.20032202
10.1093/emboj/cdg522
10.1101/gad.9.21.2609
10.1016/S0092-8674(00)00040-4
10.1084/jem.20021417
10.1093/bioinformatics/18.12.1633
10.1677/jme.0.0330001
10.1093/bioinformatics/btg242

Dates

Type	When
Created	19 years, 2 months ago (June 16, 2006, 9:16 p.m.)
Deposited	2 years, 3 months ago (May 7, 2023, 3:19 p.m.)
Indexed	5 months ago (March 30, 2025, 12:20 a.m.)
Issued	19 years, 2 months ago (June 27, 2006)
Published	19 years, 2 months ago (June 27, 2006)
Published Online	19 years, 2 months ago (June 27, 2006)
Published Print	19 years, 2 months ago (June 27, 2006)

Funders 0

None

BibTeX

@article{Schwartz_2006, title={Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development}, volume={103}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0603728103}, DOI={10.1073/pnas.0603728103}, number={26}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Schwartz, Ruth and Engel, Isaac and Fallahi-Sichani, Mohammad and Petrie, Howard T. and Murre, Cornelis}, year={2006}, month=jun, pages={9976–9981} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        3,
        30
      ]
    ],
    "date-time": "2025-03-30T04:20:01Z",
    "timestamp": 1743308401641
  },
  "reference-count": 44,
  "publisher": "Proceedings of the National Academy of Sciences",
  "issue": "26",
  "content-domain": {
    "domain": [
      "www.pnas.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2006,
        6,
        27
      ]
    ]
  },
  "abstract": "<jats:p>In maturing T lineage cells, the helix\u2013loop\u2013helix protein E47 has been shown to enforce a critical proliferation and developmental checkpoint commonly referred to as \u03b2 selection. To examine how E47 regulates cellular expansion and developmental progression, we have used an E2A-deficient lymphoma cell line and DNA microarray analysis to identify immediate E47 target genes. Hierarchical cluster analysis of gene expression patterns revealed that E47 coordinately regulates the expression of genes involved in cell survival, cell cycle progression, lipid metabolism, stress response, and lymphoid maturation. These include Plc\u03b32, Cdk6, CD25, Tox, Gadd45a, Gadd45b, Gfi1, Gfi1b, Socs1, Socs3, Id2, Eto2, and Xbp1. We propose a regulatory network linking Janus kinase (JAK)/signal transducer and activator of transcription (STAT)-mediated signaling, E47, and suppressor of cytokine signaling (SOCS) proteins in a common pathway. Finally, we suggest that the aberrant activation of Cdk6 in E47-deficient T lineage cells contributes to the development of lymphoid malignancy.</jats:p>",
  "DOI": "10.1073/pnas.0603728103",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        6,
        17
      ]
    ],
    "date-time": "2006-06-17T01:16:25Z",
    "timestamp": 1150506985000
  },
  "page": "9976-9981",
  "update-policy": "http://dx.doi.org/10.1073/pnas.cm10313",
  "source": "Crossref",
  "is-referenced-by-count": 111,
  "title": "Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development",
  "prefix": "10.1073",
  "volume": "103",
  "author": [
    {
      "given": "Ruth",
      "family": "Schwartz",
      "sequence": "first",
      "affiliation": [
        {
          "name": "*Division of Biological Sciences, University of California at San Diego, La Jolla, CA 92093-0377; and"
        }
      ]
    },
    {
      "given": "Isaac",
      "family": "Engel",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "*Division of Biological Sciences, University of California at San Diego, La Jolla, CA 92093-0377; and"
        }
      ]
    },
    {
      "given": "Mohammad",
      "family": "Fallahi-Sichani",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Scripps/Florida Research Institute, 5353 Parkside Drive, RF-1, Jupiter, FL 33458"
        }
      ]
    },
    {
      "given": "Howard T.",
      "family": "Petrie",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Scripps/Florida Research Institute, 5353 Parkside Drive, RF-1, Jupiter, FL 33458"
        }
      ]
    },
    {
      "given": "Cornelis",
      "family": "Murre",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "*Division of Biological Sciences, University of California at San Diego, La Jolla, CA 92093-0377; and"
        }
      ]
    }
  ],
  "member": "341",
  "published-online": {
    "date-parts": [
      [
        2006,
        6,
        27
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_3_3_1_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ni1260"
    },
    {
      "key": "e_1_3_3_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(94)90077-9"
    },
    {
      "key": "e_1_3_3_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(94)90076-0"
    },
    {
      "key": "e_1_3_3_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1600-065X.2000.imr017514.x"
    },
    {
      "key": "e_1_3_3_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.17.8.4782"
    },
    {
      "key": "e_1_3_3_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.186.9.1597"
    },
    {
      "key": "e_1_3_3_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.20.18.6677-6685.2000"
    },
    {
      "key": "e_1_3_3_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.194.6.733"
    },
    {
      "key": "e_1_3_3_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1074-7613(02)00264-9"
    },
    {
      "key": "e_1_3_3_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/84273"
    },
    {
      "key": "e_1_3_3_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/sj.emboj.7600017"
    },
    {
      "key": "e_1_3_3_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.190.11.1605"
    },
    {
      "key": "e_1_3_3_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1074-7613(00)80155-7"
    },
    {
      "key": "e_1_3_3_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.17.12.7317"
    },
    {
      "key": "e_1_3_3_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.96.3.996"
    },
    {
      "key": "e_1_3_3_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ni923"
    },
    {
      "key": "e_1_3_3_17_2",
      "doi-asserted-by": "crossref",
      "first-page": "5103",
      "DOI": "10.4049/jimmunol.154.10.5103",
      "volume": "154",
      "author": "Penit C.",
      "year": "1995",
      "unstructured": "C. Penit, B. Lucas, F. F. Vasseur J. Immunol. 154, 5103\u20135113 (1995).",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_3_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.4049/jimmunol.173.2.1094"
    },
    {
      "key": "e_1_3_3_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.17.10.5888"
    },
    {
      "key": "e_1_3_3_20_2",
      "first-page": "1",
      "volume": "6",
      "author": "Cueva E. D.",
      "year": "2006",
      "unstructured": "E. D. Cueva, I. Garcia-Cao, M. Herranz, P. Lopez, P. Garcia-Palencia, J. M. Flores, M. Serranto, J. Fernandez-Piqueras, J. Martin-Caballero Oncogene 6, 1\u20135 (2006).",
      "journal-title": "Oncogene"
    },
    {
      "key": "e_1_3_3_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.24.10128"
    },
    {
      "key": "e_1_3_3_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1990.tb08126.x"
    },
    {
      "key": "e_1_3_3_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.ccr.2004.05.023"
    },
    {
      "key": "e_1_3_3_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0037-1963(03)00195-1"
    },
    {
      "key": "e_1_3_3_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1535-6108(02)00018-1"
    },
    {
      "key": "e_1_3_3_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/MCB.16.1.121"
    },
    {
      "key": "e_1_3_3_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1097937"
    },
    {
      "key": "e_1_3_3_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1071914"
    },
    {
      "key": "e_1_3_3_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.0105-2896.2006.00345.x"
    },
    {
      "key": "e_1_3_3_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ni767"
    },
    {
      "key": "e_1_3_3_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/35085509"
    },
    {
      "key": "e_1_3_3_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.200408117"
    },
    {
      "key": "e_1_3_3_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nri979"
    },
    {
      "key": "e_1_3_3_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1092009"
    },
    {
      "key": "e_1_3_3_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ni844"
    },
    {
      "key": "e_1_3_3_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1074-7613(00)00028-5"
    },
    {
      "key": "e_1_3_3_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.20032202"
    },
    {
      "key": "e_1_3_3_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/emboj/cdg522"
    },
    {
      "key": "e_1_3_3_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.9.21.2609"
    },
    {
      "key": "e_1_3_3_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)00040-4"
    },
    {
      "key": "e_1_3_3_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.20021417"
    },
    {
      "key": "e_1_3_3_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/18.12.1633"
    },
    {
      "key": "e_1_3_3_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1677/jme.0.0330001"
    },
    {
      "key": "e_1_3_3_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/bioinformatics/btg242"
    }
  ],
  "container-title": "Proceedings of the National Academy of Sciences",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://pnas.org/doi/pdf/10.1073/pnas.0603728103",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        5,
        7
      ]
    ],
    "date-time": "2023-05-07T19:19:37Z",
    "timestamp": 1683487177000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://pnas.org/doi/full/10.1073/pnas.0603728103"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2006,
        6,
        27
      ]
    ]
  },
  "references-count": 44,
  "journal-issue": {
    "issue": "26",
    "published-print": {
      "date-parts": [
        [
          2006,
          6,
          27
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1073/pnas.0603728103"
  ],
  "URL": "http://dx.doi.org/10.1073/pnas.0603728103",
  "relation": {},
  "ISSN": [
    "0027-8424",
    "1091-6490"
  ],
  "subject": [],
  "container-title-short": "Proc. Natl. Acad. Sci. U.S.A.",
  "published": {
    "date-parts": [
      [
        2006,
        6,
        27
      ]
    ]
  },
  "assertion": [
    {
      "value": "2006-04-07",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2006-06-27",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}