Noncanonical function of Capicua as a growth termination signal inDrosophilaoogenesis

Author:

Rodríguez-Muñoz Laura1ORCID,Lagares Clàudia1ORCID,González-Crespo Sergio1,Castel Pau2,Veraksa Alexey3ORCID,Jiménez Gerardo14ORCID

Affiliation:

1. Department of Developmental Biology, Instituto de Biología Molecular de Barcelona, Consejo Superior de Investigaciones Científicas, Barcelona, 08028 Spain

2. Department of Biochemistry and Molecular Pharmacology, New York University Grossman School of Medicine, New York, NY 10016

3. Department of Biology, University of Massachusetts, Boston, MA 02125

4. Institució Catalana de Recerca i Estudis Avançats, 08010 Barcelona, Spain

Abstract

Capicua (Cic) proteins are conserved HMG-box transcriptional repressors that control receptor tyrosine kinase (RTK) signaling responses and are implicated in human neurological syndromes and cancer. While Cic is known to exist as short (Cic-S) and long (Cic-L) isoforms with identical HMG-box and associated core regions but distinct N termini, most previous studies have focused on Cic-S, leaving the function of Cic-L unexplored. Here we show that Cic-L acts in two capacities duringDrosophilaoogenesis: 1) as a canonical sensor of RTK signaling in somatic follicle cells, and 2) as a regulator of postmitotic growth in germline nurse cells. In these latter cells, Cic-L behaves as a temporal signal that terminates endoreplicative growth before they dump their contents into the oocyte. We show that Cic-L is necessary and sufficient for nurse cell endoreplication arrest and induces both stabilization of CycE and down-regulation of Myc. Surprisingly, this function depends mainly on the Cic-L–specific N-terminal module, which is capable of acting independently of the Cic HMG-box–containing core. Mirroring these observations, basal metazoans possess truncated Cic-like proteins composed only of Cic-L N-terminal sequences, suggesting that this module plays unique, ancient roles unrelated to the canonical function of Cic.

Funder

MEC | Spanish National Plan for Scientific and Technical Research and Innovation

Generalitat de Catalunya

HHS | National Institutes of Health

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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