14-3-3ζ Cooperates with ErbB2 to Promote Ductal Carcinoma In Situ Progression to Invasive Breast Cancer by Inducing Epithelial-Mesenchymal Transition

Jing Lu; Hua Guo; Warapen Treekitkarnmongkol; Ping Li; Jian Zhang; Bin Shi; Chen Ling; Xiaoyan Zhou; Tongzhen Chen; Paul J. Chiao; Xinhua Feng; Victoria L. Seewaldt; William J. Muller; Aysegul Sahin; Mien Chie Hung; Dihua Yu

doi:10.1016/j.ccr.2009.08.010

14-3-3ζ Cooperates with ErbB2 to Promote Ductal Carcinoma In Situ Progression to Invasive Breast Cancer by Inducing Epithelial-Mesenchymal Transition

Jing Lu, Hua Guo, Warapen Treekitkarnmongkol, Ping Li, Jian Zhang, Bin Shi, Chen Ling, Xiaoyan Zhou, Tongzhen Chen, Paul J. Chiao, Xinhua Feng, Victoria L. Seewaldt, William J. Muller, Aysegul Sahin, Mien Chie Hung, Dihua Yu

Research output: Contribution to journal › Article › peer-review

175 Scopus citations

Abstract

ErbB2, a metastasis-promoting oncoprotein, is overexpressed in ∼25% of invasive/metastatic breast cancers, but in 50%-60% of noninvasive ductal carcinomas in situ (DCIS). It has been puzzling how a subset of ErbB2-overexpressing DCIS develops into invasive breast cancer (IBC). We found that co-overexpression of 14-3-3ζ in ErbB2-overexpressing DCIS conferred a higher risk of progression to IBC. ErbB2 and 14-3-3ζ overexpression, respectively, increased cell migration and decreased cell adhesion, two prerequisites of tumor cell invasion. 14-3-3ζ overexpression reduced cell adhesion by activating the TGF-β/Smads pathway that led to ZFHX1B/SIP-1 upregulation, E-cadherin loss, and epithelial-mesenchymal transition. Importantly, patients whose breast tumors overexpressed both ErbB2 and 14-3-3ζ had higher rates of metastatic recurrence and death than those whose tumors overexpressed only one.

Original language	English (US)
Pages (from-to)	195-207
Number of pages	13
Journal	Cancer cell
Volume	16
Issue number	3
DOIs	https://doi.org/10.1016/j.ccr.2009.08.010
State	Published - Sep 8 2009

Keywords

CELLCYCLE

ASJC Scopus subject areas

Oncology
Cell Biology
Cancer Research

MD Anderson CCSG core facilities

Flow Cytometry and Cellular Imaging Facility

Access to Document

10.1016/j.ccr.2009.08.010

Cite this

Lu, J., Guo, H., Treekitkarnmongkol, W., Li, P., Zhang, J., Shi, B., Ling, C., Zhou, X., Chen, T., Chiao, P. J., Feng, X., Seewaldt, V. L., Muller, W. J., Sahin, A., Hung, M. C., & Yu, D. (2009). 14-3-3ζ Cooperates with ErbB2 to Promote Ductal Carcinoma In Situ Progression to Invasive Breast Cancer by Inducing Epithelial-Mesenchymal Transition. Cancer cell, 16(3), 195-207. https://doi.org/10.1016/j.ccr.2009.08.010

Lu, J, Guo, H, Treekitkarnmongkol, W , Li, P, Zhang, J, Shi, B, Ling, C, Zhou, X, Chen, T, Chiao, PJ, Feng, X, Seewaldt, VL, Muller, WJ, Sahin, A, Hung, MC & Yu, D 2009, '14-3-3ζ Cooperates with ErbB2 to Promote Ductal Carcinoma In Situ Progression to Invasive Breast Cancer by Inducing Epithelial-Mesenchymal Transition', Cancer cell, vol. 16, no. 3, pp. 195-207. https://doi.org/10.1016/j.ccr.2009.08.010

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title = "14-3-3ζ Cooperates with ErbB2 to Promote Ductal Carcinoma In Situ Progression to Invasive Breast Cancer by Inducing Epithelial-Mesenchymal Transition",

abstract = "ErbB2, a metastasis-promoting oncoprotein, is overexpressed in ∼25% of invasive/metastatic breast cancers, but in 50%-60% of noninvasive ductal carcinomas in situ (DCIS). It has been puzzling how a subset of ErbB2-overexpressing DCIS develops into invasive breast cancer (IBC). We found that co-overexpression of 14-3-3ζ in ErbB2-overexpressing DCIS conferred a higher risk of progression to IBC. ErbB2 and 14-3-3ζ overexpression, respectively, increased cell migration and decreased cell adhesion, two prerequisites of tumor cell invasion. 14-3-3ζ overexpression reduced cell adhesion by activating the TGF-β/Smads pathway that led to ZFHX1B/SIP-1 upregulation, E-cadherin loss, and epithelial-mesenchymal transition. Importantly, patients whose breast tumors overexpressed both ErbB2 and 14-3-3ζ had higher rates of metastatic recurrence and death than those whose tumors overexpressed only one.",

keywords = "CELLCYCLE",

author = "Jing Lu and Hua Guo and Warapen Treekitkarnmongkol and Ping Li and Jian Zhang and Bin Shi and Chen Ling and Xiaoyan Zhou and Tongzhen Chen and Chiao, {Paul J.} and Xinhua Feng and Seewaldt, {Victoria L.} and Muller, {William J.} and Aysegul Sahin and Hung, {Mien Chie} and Dihua Yu",

note = "Funding Information: We thank J.M. Shu, Dr. J.P. Issa, and Dr. X. Lin (MDACC), and Dr. Y. Higashi (Osaka University) for their technical support and ZFHX1B antiserum. D.Y. is the Nylene Eckles Distinguished Professor in Breast Cancer Research at MDACC. W.T. is partially supported by the Royal Golden Jubilee Program, Thailand Research Fund. This work is supported by National Institutes of Health grants P30-CA 16672 (MDACC), RO1-CA109570, RO1-CA112567, PO1-CA099031 project 4, and P50 CA116199 project 4; Department of Defense Center of Excellence grant subproject W81XWH-06-2-0033 and Synergistic Award W81XWH-08-1-0712; and Susan G. Komen Breast Cancer Foundation Promise Grant KG091020 (D.Y.). ",

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doi = "10.1016/j.ccr.2009.08.010",

language = "English (US)",

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T1 - 14-3-3ζ Cooperates with ErbB2 to Promote Ductal Carcinoma In Situ Progression to Invasive Breast Cancer by Inducing Epithelial-Mesenchymal Transition

AU - Lu, Jing

AU - Guo, Hua

AU - Treekitkarnmongkol, Warapen

AU - Li, Ping

AU - Zhang, Jian

AU - Shi, Bin

AU - Ling, Chen

AU - Zhou, Xiaoyan

AU - Chen, Tongzhen

AU - Chiao, Paul J.

AU - Feng, Xinhua

AU - Seewaldt, Victoria L.

AU - Muller, William J.

AU - Sahin, Aysegul

AU - Hung, Mien Chie

AU - Yu, Dihua

N1 - Funding Information: We thank J.M. Shu, Dr. J.P. Issa, and Dr. X. Lin (MDACC), and Dr. Y. Higashi (Osaka University) for their technical support and ZFHX1B antiserum. D.Y. is the Nylene Eckles Distinguished Professor in Breast Cancer Research at MDACC. W.T. is partially supported by the Royal Golden Jubilee Program, Thailand Research Fund. This work is supported by National Institutes of Health grants P30-CA 16672 (MDACC), RO1-CA109570, RO1-CA112567, PO1-CA099031 project 4, and P50 CA116199 project 4; Department of Defense Center of Excellence grant subproject W81XWH-06-2-0033 and Synergistic Award W81XWH-08-1-0712; and Susan G. Komen Breast Cancer Foundation Promise Grant KG091020 (D.Y.).

PY - 2009/9/8

Y1 - 2009/9/8

N2 - ErbB2, a metastasis-promoting oncoprotein, is overexpressed in ∼25% of invasive/metastatic breast cancers, but in 50%-60% of noninvasive ductal carcinomas in situ (DCIS). It has been puzzling how a subset of ErbB2-overexpressing DCIS develops into invasive breast cancer (IBC). We found that co-overexpression of 14-3-3ζ in ErbB2-overexpressing DCIS conferred a higher risk of progression to IBC. ErbB2 and 14-3-3ζ overexpression, respectively, increased cell migration and decreased cell adhesion, two prerequisites of tumor cell invasion. 14-3-3ζ overexpression reduced cell adhesion by activating the TGF-β/Smads pathway that led to ZFHX1B/SIP-1 upregulation, E-cadherin loss, and epithelial-mesenchymal transition. Importantly, patients whose breast tumors overexpressed both ErbB2 and 14-3-3ζ had higher rates of metastatic recurrence and death than those whose tumors overexpressed only one.

AB - ErbB2, a metastasis-promoting oncoprotein, is overexpressed in ∼25% of invasive/metastatic breast cancers, but in 50%-60% of noninvasive ductal carcinomas in situ (DCIS). It has been puzzling how a subset of ErbB2-overexpressing DCIS develops into invasive breast cancer (IBC). We found that co-overexpression of 14-3-3ζ in ErbB2-overexpressing DCIS conferred a higher risk of progression to IBC. ErbB2 and 14-3-3ζ overexpression, respectively, increased cell migration and decreased cell adhesion, two prerequisites of tumor cell invasion. 14-3-3ζ overexpression reduced cell adhesion by activating the TGF-β/Smads pathway that led to ZFHX1B/SIP-1 upregulation, E-cadherin loss, and epithelial-mesenchymal transition. Importantly, patients whose breast tumors overexpressed both ErbB2 and 14-3-3ζ had higher rates of metastatic recurrence and death than those whose tumors overexpressed only one.

KW - CELLCYCLE

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SN - 1535-6108

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JF - Cancer cell

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ER -

14-3-3ζ Cooperates with ErbB2 to Promote Ductal Carcinoma In Situ Progression to Invasive Breast Cancer by Inducing Epithelial-Mesenchymal Transition

Abstract

Keywords

ASJC Scopus subject areas

MD Anderson CCSG core facilities

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