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Chromatin Remodeling Factors and BRM/BRG1 Expression as Prognostic Indicators in Non-Small Cell Lung Cancer

Junya Fukuoka, Takeshi Fujii, Joanna H. Shih, Tatiana Dracheva, Daoud Meerzaman, Audrey Player, Kyeong Hong, Sharon Settnek, Ajay Gupta, Kenneth Buetow, Stephen Hewitt, William D. Travis and Jin Jen
Junya Fukuoka
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Takeshi Fujii
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Joanna H. Shih
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Tatiana Dracheva
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Daoud Meerzaman
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Audrey Player
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Kyeong Hong
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Sharon Settnek
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Ajay Gupta
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Kenneth Buetow
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Stephen Hewitt
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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William D. Travis
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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Jin Jen
1Laboratory of Population Genetics, 2Biometric Research Branch, 3Center for Bioinformatics, 4Laboratory of Pathology, National Cancer Institute, Bethesda, Maryland; 5Department of Pulmonary and Mediastinal Pathology, Armed Forces Institute of Pathology, Washington, D.C.; and 6Department of Pathology, Shiga University of Medical Science, Shiga, Japan
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DOI: 10.1158/1078-0432.CCR-03-0489 Published July 2004
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  • Fig. 1.
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    Fig. 1.

    Organization of lung tumor tissue microarray (TMA). A, H&E staining of the entire TMA section. B, scheme of TMA. Tissues samples are represented by small rectangles that are arrayed in groups of 25 each. Tumor types are indicated as light gray (adenocarcinoma) or black (squamous cell carcinoma). The clear areas are control tissues including normal lung from patients with adenocarcinoma (#1), or squamous cell carcinoma (#2), and normal nonpulmonary organs (#3).

  • Fig. 2.
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    Fig. 2.

    Chromatin remodeling factors in lung cancer cell lines. A, immunoblotting of BRG1, BRM, BAF155, and Ini-1 among nine lung cancer cell lines. The EKVX cell line showed a band reactive to anti-BRM but nonimmunoreactive for anti-BRG1 antibody. The apparent sizes of BRG1 and BRM were a little larger than the known molecular size (180 kDa) but are the same as those shown in the data sheet from the supplier (http://www.scbt.com/). BAF155 and Ini-1 showed an immunoreactive band in eight cell lines. H358 appeared to be negative for Ini-1. B, anti-BRM immunohistochemical staining of the same lung cancer cells. Hop92 did not show positive staining by immunohistochemistry but showed a weak positive band on Western blot. Consistent with immunoblotting, immunohistochemical signals of BRM were lower than those of BRG1 in lung cancer cell lines. H520, EKVX, and H2170 showed membranous and cytoplasmic staining, whereas H358 and H226 showed weak and focal nuclear staining.

  • Fig. 3.
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    Fig. 3.

    Examples of immunohistochemical staining by BRG1 and BRM antibodies in primary lung tissues. A, BRG1 in normal lung. Most of the cells including pneumocytes and interstitial cells were positively stained in the nucleus. B, a lung tumor negative for BRG1 [TS0]. C, a tumor positive for BRG1 (TS3). D, BRM in normal lung. Most of the cells including pneumocytes and other interstitial cells are positive in the nucleus. E, tumor with negative BRM staining (TS0); the surrounding inflammatory cells were positive. F, tumor positive for BRM (TS3). G and H, membranous BRM staining in tumor cells. I, high magnifications (×400) of images shown in G and H. Diameter of tissue core = 0.6 mm.

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    Fig. 4.

    Association of staining between each pair of antibodies. A, P values of χ2 test between each antibody are shown for adenocarcinoma (gray area) and squamous cell carcinoma (white area). P ≤ 0.01 is considered significant and is indicated in the table. B, one-way clustering indicating the relatedness of expression patterns among all antibodies. Note that all nonnuclear signals clustered distantly from the nuclear signals of the same antibody. C, identification of two highly correlated sets of chromatin remodeling proteins in NSCLC.

  • Fig. 5.
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    Fig. 5.

    Immunohistochemistry scoring and Kaplan-Meier survival analyses for BRG1 and BRM in non-small cell lung cancer. A, immunohistochemical scoring for nuclear BRG1, nuclear BRM, and membranous BRM signals. Grids corresponded to tumor arrangements on the TMA as shown in Fig. 1B<$REFLINK> (gray and black blocks). Total scores (TSs) are shown, and the colors corresponded to the TS values. Red, TS3; yellow, TS2; white, TS1/TS0; black, excluded or missing tissues. B, Kaplan-Meier survival plots. The overall patient survival status for antibodies and selected cellular locations are shown. The number of patients in each arm and the associated P values are as indicated.

Tables

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  • Table 1

    Clinical characteristics of all non-small cell lung cancer patients used in this study

    VariableCategoryNo. of patients (n = 230)Median survival (yrs)
    GenderMale1662.8
    Female644.6
    Mean age ± SD (yrs)64.6 ± 9.2 (36–86)
    StageI115]4.2
    II29
    III30]1.3
    IV7
    Vital statusAlive527.3a
    Dead[Tumor related461.6
    Other cause201.7
    Unknown802.8
    Median follow-up (yrs)3.2 ± 3.2
    • a Median term of last follow-up.

  • Table 2

    Antibodies and protocols used for immunohistochemical staining

    AntibodySpeciesSourceCloneTypeProtocolTitrationRetrieval
    HDAC1RaSanta CruzH-51IgG2aABC50DC
    HDAC2RSanta CruzH-54IgGABC200MW
    BRG1RSanta CruzH-88IgGABC200DC
    BRMGSanta CruzC-20IgGABC100DC
    BRMGSanta CruzN-19IgGABC100DC
    BAF170RSanta CruzH-116IgGABC100MW
    BAF155RSanta CruzH-76IgGABC100MW
    RbAp48GSanta CruzK-15IgGABC300MW
    RBMZymedRB-1IgG1, κABC100DC
    Ini1RSanta CruzH-300IgGABC50DC
    mSin3ARSanta CruzAK-11IgGABC50DC
    HAT1GSanta CruzC-20IgGABC1000DC
    Tip60GSanta CruzK-17IgGABC100DC
    AE1/AE3MDAKOAE1/AE3IgG1ABC100None
    PGP9.5RBiogenesisn/an/aABC8000DC
    • a R, rabbit; DC, Decloaking Chamber; MW, microwave; G, goat; M, mouse; n/a, not available.

  • Table 3

    Immunohistochemical staining of chromatin remodeling factors using TMAa

    The actual number of cases is shown for each scoring, whereas percentages are given for − and + cells. N, nuclear, C, cytoplasmic, M, membranous. Total scores 2 and 3 were designated as positive, whereas scores 0 and 1 were recognized as negative.

    Total scoreBRG1BRMBAF155Ini-1BAF170HDAC1HDAC2RbAP48RBmSin3AHAT1Tip60
    NCNMNCNCNNNNNNNC
    07422115622212216213514843731105571722784
    1444451651211719252028374593836
    27773815446973536075467878605464
    350132915302125281227063716810012754
    −48927489706758472736543544293737
    +5282611303342337364466556716363
    • a TMA, tissue microarray.

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Clinical Cancer Research: 10 (13)
July 2004
Volume 10, Issue 13
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Chromatin Remodeling Factors and BRM/BRG1 Expression as Prognostic Indicators in Non-Small Cell Lung Cancer
Junya Fukuoka, Takeshi Fujii, Joanna H. Shih, Tatiana Dracheva, Daoud Meerzaman, Audrey Player, Kyeong Hong, Sharon Settnek, Ajay Gupta, Kenneth Buetow, Stephen Hewitt, William D. Travis and Jin Jen
Clin Cancer Res July 1 2004 (10) (13) 4314-4324; DOI: 10.1158/1078-0432.CCR-03-0489

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Chromatin Remodeling Factors and BRM/BRG1 Expression as Prognostic Indicators in Non-Small Cell Lung Cancer
Junya Fukuoka, Takeshi Fujii, Joanna H. Shih, Tatiana Dracheva, Daoud Meerzaman, Audrey Player, Kyeong Hong, Sharon Settnek, Ajay Gupta, Kenneth Buetow, Stephen Hewitt, William D. Travis and Jin Jen
Clin Cancer Res July 1 2004 (10) (13) 4314-4324; DOI: 10.1158/1078-0432.CCR-03-0489
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