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Drosophila actin-Capping Protein limits JNK activation by the Src proto-oncogene

Oncogene volume 33, pages 2027–2039 (2014)Cite this article

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Abstract

The Src family kinases c-Src, and its downstream effectors, the Rho family of small GTPases RhoA and Jun N-terminal kinase (JNK) have a significant role in tumorigenesis. In this report, using the Drosophila wing disc epithelium as a model system, we demonstrate that the actin-Capping Protein (CP) αβ heterodimer, which regulates actin filament (F-actin) polymerization, limits Src-induced apoptosis or tissue overgrowth by restricting JNK activation. We show that overexpressing Src64B drives JNK-independent loss of epithelial integrity and JNK-dependent apoptosis via Btk29A, p120ctn and Rho1. However, when cells are kept alive with the Caspase inhibitor P35, JNK acts as a potent inducer of proliferation via activation of the Yorkie oncogene. Reducing CP levels direct apoptosis of overgrowing Src64B-overexpressing tissues. Conversely, overexpressing capping protein inhibits Src64B and Rho1, but not Rac1-induced JNK signaling. CP requires the actin-binding domain of the α-subunit to limit Src64B-induced apoptosis, arguing that the control of F-actin mediates this effect. In turn, JNK directs F-actin accumulation. Moreover, overexpressing capping protein also prevents apoptosis induced by ectopic JNK expression. Our data are consistent with a model in which the control of F-actin by CP limits Src-induced apoptosis or tissue overgrowth by acting downstream of Btk29A, p120ctn and Rho1, but upstream of JNK. In turn, JNK may counteract the effect of CP on F-actin, providing a positive feedback, which amplifies JNK activation. We propose that cytoskeletal changes triggered by misregulation of F-actin modulators may have a significant role in Src-mediated malignant phenotypes during the early stages of cellular transformation.

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Acknowledgements

We thank T Xu, B Hay, R Mann, A Laughon, G Morata, J Whited, the Bloomington Drosophila Stock Center, the National Institute of Genetics, The Vienna Drosophila Research Center and the Developmental Studies Hybridoma Bank for fly stocks and reagents. The manuscript was improved by the critical comments of Miguel G. Ferreira, Joana Vaz, Monica Bettencourt Dias and Christen Mirth. This work was supported by grants from Fundação para a Ciência e Tecnologia (FCT) (Grants PTDC/SAU-OBD/73191/2006 and PTDC/BIA-BCM/121455/2010). BGF and BJ were the recipients of fellowships from FCT SFRH/BPD/35915/2007 and SFRH/BD/33215/2007, respectively).

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  1. B G Fernández and B Jezowska: These authors contributed equally to this work.

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    B G Fernández, B Jezowska & F Janody

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Fernández, B., Jezowska, B. & Janody, F. Drosophila actin-Capping Protein limits JNK activation by the Src proto-oncogene. Oncogene 33, 2027–2039 (2014). https://doi.org/10.1038/onc.2013.155

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