The kinesin KIF1C transports APC-dependent mRNAs to cell protrusions (original) (raw)

1. Konstadinos Moissoglu3,12,
2. Emeline Coleno1,2,4,
3. Tianhong Wang3,
4. Arthur Imbert5,6,7,
5. Marie-Cécile Robert1,2,4,
6. Marion Peter1,2,
7. Racha Chouaib1,2,8,
8. Thomas Walter5,6,7,
9. Florian Mueller9,10,
10. Kazem Zibara8,11,
11. Edouard Bertrand1,2,4 and
12. Stavroula Mili3
13. 1Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS, 34293 Montpellier, France
14. 2Equipe labélisée Ligue Nationale Contre le Cancer, University of Montpellier, CNRS, 34000 Montpellier, France
15. 3Laboratory of Cellular and Molecular Biology, Center for Cancer Research, National Cancer Institute, NIH, Bethesda, Maryland 20814, USA
16. 4Institut de Génétique Humaine, University of Montpellier, CNRS, 34396 Montpellier, France
17. 5MINES ParisTech, PSL-Research University, CBIO-Centre for Computational Biology, 77300 Fontainebleau, France
18. 6Institut Curie, 75248 Paris Cedex, France
19. 7INSERM, U900, 75248 Paris Cedex, France
20. 8Biology Department, Faculty of Sciences-I, Lebanese University, Beirut, Lebanon
21. 9Unité Imagerie et Modélisation, Institut Pasteur and CNRS UMR 3691, 75015 Paris, France
22. 10C3BI, USR 3756 IP CNRS – Paris, France
23. 11ER045, PRASE, DSST, Lebanese University, Beirut, Lebanon
24. Corresponding authors: edouard.bertrand{at}igh.cnrs.fr, voula.mili{at}nih.gov
25. ↵12 These authors contributed equally to this work.

Abstract

RNA localization and local translation are important for numerous cellular functions. In mammals, a class of mRNAs localize to cytoplasmic protrusions in an APC-dependent manner, with roles during cell migration. Here, we investigated this localization mechanism. We found that the KIF1C motor interacts with APC-dependent mRNAs and is required for their localization. Live cell imaging revealed rapid, active transport of single mRNAs over long distances that requires both microtubules and KIF1C. Two-color imaging directly revealed single mRNAs transported by single KIF1C motors, with the 3′UTR being sufficient to trigger KIF1C-dependent RNA transport and localization. Moreover, KIF1C remained associated with peripheral, multimeric RNA clusters and was required for their formation. These results reveal a widespread RNA transport pathway in mammalian cells, in which the KIF1C motor has a dual role in transporting RNAs and clustering them within cytoplasmic protrusions. Interestingly, KIF1C also transports its own mRNA, suggesting a possible feedback loop acting at the level of mRNA transport.

• RNA localization
• local translation
• RNA transport
• cytoplasmic protrusions

Footnotes

• Article is online at http://www.rnajournal.org/cgi/doi/10.1261/rna.078576.120.

• Freely available online through the RNA Open Access option.

• Received December 7, 2020.

• Accepted September 1, 2021.

• © 2021 Pichon et al.; Published by Cold Spring Harbor Laboratory Press for the RNA Society

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24. Profile for Pichon, X.http://orcid.org/0000-0002-0755-2305

25. Profile for Moissoglu, K.http://orcid.org/0000-0001-7211-4320

26. Profile for Peter, M.http://orcid.org/0000-0002-5720-4798

27. Profile for Mueller, F.http://orcid.org/0000-0002-9622-4396

28. Profile for Bertrand, E.http://orcid.org/0000-0002-9642-7994

29. Profile for Mili, S.http://orcid.org/0000-0002-9161-8660