A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration

Menachem Katz; Ido Amit; Ami Citri; Tal Shay; Silvia Carvalho; Sara Lavi; Fernanda Milanezi; Ljuba Lyass; Ninette Amariglio; Jasmine Jacob-Hirsch; Nir Ben-Chetrit; Gabi Tarcic; Moshit Lindzen; Roi Avraham; Yi Chun Liao; Patricia Trusk; Asya Lyass; Gideon Rechavi; Neil L. Spector; Su Hao Lo; Fernando Schmitt; Sarah S. Bacus; Yosef Yarden

doi:10.1038/ncb1622

A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration

Menachem Katz, Ido Amit, Ami Citri, Tal Shay, Silvia Carvalho, Sara Lavi, Fernanda Milanezi, Ljuba Lyass, Ninette Amariglio, Jasmine Jacob-Hirsch, Nir Ben-Chetrit, Gabi Tarcic, Moshit Lindzen, Roi Avraham, Yi Chun Liao, Patricia Trusk, Asya Lyass, Gideon Rechavi, Neil L. Spector, Su Hao LoFernando Schmitt, Sarah S. Bacus, Yosef Yarden

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

162 Scopus citations

Abstract

Cell migration driven by the epidermal growth factor receptor (EGFR) propels morphogenesis and involves reorganization of the actin cytoskeleton. Although de novo transcription precedes migration, transcript identity remains largely unknown. Through their actin-binding domains, tensins link the cytoskeleton to integrin-based adhesion sites. Here we report that EGF downregulates tensin-3 expression, and concomitantly upregulates cten, a tensin family member that lacks the actin-binding domain. Knockdown of cten or tensin-3, respectively, impairs or enhances mammary cell migration. Furthermore, cten displaces tensin-3 from the cytoplasmic tail of integrin β₁, thereby instigating actin fibre disassembly. In invasive breast cancer, cten expression correlates not only with high EGFR and HER2, but also with metastasis to lymph nodes. Moreover, treatment of inflammatory breast cancer patients with an EGFR/HER2 dual-specificity kinase inhibitor significantly downregulated cten expression. In conclusion, a transcriptional tensin-3-cten switch may contribute to the metastasis of mammary cancer.

Original language	English
Pages (from-to)	961-969
Number of pages	9
Journal	Nature Cell Biology
Volume	9
Issue number	8
DOIs	https://doi.org/10.1038/ncb1622
State	Published - 1 Aug 2007
Externally published	Yes

ASJC Scopus subject areas

Cell Biology

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This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/ncb1622

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Katz, M., Amit, I., Citri, A., Shay, T., Carvalho, S., Lavi, S., Milanezi, F., Lyass, L., Amariglio, N., Jacob-Hirsch, J., Ben-Chetrit, N., Tarcic, G., Lindzen, M., Avraham, R., Liao, Y. C., Trusk, P., Lyass, A., Rechavi, G., Spector, N. L., ... Yarden, Y. (2007). A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration. Nature Cell Biology, 9(8), 961-969. https://doi.org/10.1038/ncb1622

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title = "A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration",

abstract = "Cell migration driven by the epidermal growth factor receptor (EGFR) propels morphogenesis and involves reorganization of the actin cytoskeleton. Although de novo transcription precedes migration, transcript identity remains largely unknown. Through their actin-binding domains, tensins link the cytoskeleton to integrin-based adhesion sites. Here we report that EGF downregulates tensin-3 expression, and concomitantly upregulates cten, a tensin family member that lacks the actin-binding domain. Knockdown of cten or tensin-3, respectively, impairs or enhances mammary cell migration. Furthermore, cten displaces tensin-3 from the cytoplasmic tail of integrin β1, thereby instigating actin fibre disassembly. In invasive breast cancer, cten expression correlates not only with high EGFR and HER2, but also with metastasis to lymph nodes. Moreover, treatment of inflammatory breast cancer patients with an EGFR/HER2 dual-specificity kinase inhibitor significantly downregulated cten expression. In conclusion, a transcriptional tensin-3-cten switch may contribute to the metastasis of mammary cancer.",

author = "Menachem Katz and Ido Amit and Ami Citri and Tal Shay and Silvia Carvalho and Sara Lavi and Fernanda Milanezi and Ljuba Lyass and Ninette Amariglio and Jasmine Jacob-Hirsch and Nir Ben-Chetrit and Gabi Tarcic and Moshit Lindzen and Roi Avraham and Liao, {Yi Chun} and Patricia Trusk and Asya Lyass and Gideon Rechavi and Spector, {Neil L.} and Lo, {Su Hao} and Fernando Schmitt and Bacus, {Sarah S.} and Yosef Yarden",

year = "2007",

month = aug,

day = "1",

doi = "10.1038/ncb1622",

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Katz, M, Amit, I, Citri, A, Shay, T, Carvalho, S, Lavi, S, Milanezi, F, Lyass, L, Amariglio, N, Jacob-Hirsch, J, Ben-Chetrit, N, Tarcic, G, Lindzen, M, Avraham, R, Liao, YC, Trusk, P, Lyass, A, Rechavi, G, Spector, NL, Lo, SH, Schmitt, F, Bacus, SS & Yarden, Y 2007, 'A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration', Nature Cell Biology, vol. 9, no. 8, pp. 961-969. https://doi.org/10.1038/ncb1622

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T1 - A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration

AU - Katz, Menachem

AU - Amit, Ido

AU - Citri, Ami

AU - Shay, Tal

AU - Carvalho, Silvia

AU - Lavi, Sara

AU - Milanezi, Fernanda

AU - Lyass, Ljuba

AU - Amariglio, Ninette

AU - Jacob-Hirsch, Jasmine

AU - Ben-Chetrit, Nir

AU - Tarcic, Gabi

AU - Lindzen, Moshit

AU - Avraham, Roi

AU - Liao, Yi Chun

AU - Trusk, Patricia

AU - Lyass, Asya

AU - Rechavi, Gideon

AU - Spector, Neil L.

AU - Lo, Su Hao

AU - Schmitt, Fernando

AU - Bacus, Sarah S.

AU - Yarden, Yosef

PY - 2007/8/1

Y1 - 2007/8/1

N2 - Cell migration driven by the epidermal growth factor receptor (EGFR) propels morphogenesis and involves reorganization of the actin cytoskeleton. Although de novo transcription precedes migration, transcript identity remains largely unknown. Through their actin-binding domains, tensins link the cytoskeleton to integrin-based adhesion sites. Here we report that EGF downregulates tensin-3 expression, and concomitantly upregulates cten, a tensin family member that lacks the actin-binding domain. Knockdown of cten or tensin-3, respectively, impairs or enhances mammary cell migration. Furthermore, cten displaces tensin-3 from the cytoplasmic tail of integrin β1, thereby instigating actin fibre disassembly. In invasive breast cancer, cten expression correlates not only with high EGFR and HER2, but also with metastasis to lymph nodes. Moreover, treatment of inflammatory breast cancer patients with an EGFR/HER2 dual-specificity kinase inhibitor significantly downregulated cten expression. In conclusion, a transcriptional tensin-3-cten switch may contribute to the metastasis of mammary cancer.

AB - Cell migration driven by the epidermal growth factor receptor (EGFR) propels morphogenesis and involves reorganization of the actin cytoskeleton. Although de novo transcription precedes migration, transcript identity remains largely unknown. Through their actin-binding domains, tensins link the cytoskeleton to integrin-based adhesion sites. Here we report that EGF downregulates tensin-3 expression, and concomitantly upregulates cten, a tensin family member that lacks the actin-binding domain. Knockdown of cten or tensin-3, respectively, impairs or enhances mammary cell migration. Furthermore, cten displaces tensin-3 from the cytoplasmic tail of integrin β1, thereby instigating actin fibre disassembly. In invasive breast cancer, cten expression correlates not only with high EGFR and HER2, but also with metastasis to lymph nodes. Moreover, treatment of inflammatory breast cancer patients with an EGFR/HER2 dual-specificity kinase inhibitor significantly downregulated cten expression. In conclusion, a transcriptional tensin-3-cten switch may contribute to the metastasis of mammary cancer.

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JO - Nature Cell Biology

JF - Nature Cell Biology

IS - 8

ER -

A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration

Abstract

ASJC Scopus subject areas

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