The Recycling Endosome in Nerve Cell Development: One Rab to Rule Them All?

Overview

Journal Front Cell Dev Biol

Specialty Cell Biology

Date 2021 Jan 11

PMID 33425908

Citations 7

Authors

Victoria Rozes-Salvador

Christian Gonzalez-Billault

Cecilia Conde

Affiliations

Soon will be listed here.

Abstract

Endocytic recycling is an intracellular process that returns internalized molecules back to the plasma membrane and plays crucial roles not only in the reuse of receptor molecules but also in the remodeling of the different components of this membrane. This process is required for a diversity of cellular events, including neuronal morphology acquisition and functional regulation, among others. The recycling endosome (RE) is a key vesicular component involved in endocytic recycling. Recycling back to the cell surface may occur with the participation of several different Rab proteins, which are master regulators of membrane/protein trafficking in nerve cells. The RE consists of a network of interconnected and functionally distinct tubular subdomains that originate from sorting endosomes and transport their cargoes along microtubule tracks, by fast or slow recycling pathways. Different populations of REs, particularly those formed by Rab11, Rab35, and Arf6, are associated with a myriad of signaling proteins. In this review, we discuss the cumulative evidence suggesting the existence of heterogeneous domains of REs, controlling different aspects of neurogenesis, with a particular focus on the commonalities and singularities of these REs and their contribution to nerve development and differentiation in several animal models.

Citing Articles

The CHD family chromatin remodeling enzyme, Kismet, promotes both clathrin-mediated and activity-dependent bulk endocytosis.

Hendricks E, Liebl F PLoS One. 2024; 19(3):e0300255.

PMID: 38512854 PMC: 10956772. DOI: 10.1371/journal.pone.0300255.

The CHD Protein Kismet Restricts the Synaptic Localization of Cell Adhesion Molecules at the Neuromuscular Junction.

Smith I, Hendricks E, Latcheva N, Marenda D, Liebl F Int J Mol Sci. 2024; 25(5).

PMID: 38474321 PMC: 10931923. DOI: 10.3390/ijms25053074.

A neurodevelopmental disorder associated with a loss-of-function missense mutation in RAB35.

Aguila A, Salah S, Kulasekaran G, Shweiki M, Shaul-Lotan N, Mor-Shaked H J Biol Chem. 2024; 300(4):107124.

PMID: 38432637 PMC: 10966776. DOI: 10.1016/j.jbc.2024.107124.

How neurons maintain their axons long-term: an integrated view of axon biology and pathology.

Smith G, Sweeney S, OKane C, Prokop A Front Neurosci. 2023; 17:1236815.

PMID: 37564364 PMC: 10410161. DOI: 10.3389/fnins.2023.1236815.

Spatial regulation of endosomes in growing dendrites.

Yap C, Winckler B Dev Biol. 2022; 486:5-14.

PMID: 35306006 PMC: 10646839. DOI: 10.1016/j.ydbio.2022.03.004.

References

Kramer R, Rode S, Rumpf S . Rab11 is required for neurite pruning and developmental membrane protein degradation in Drosophila sensory neurons. Dev Biol. 2019; 451(1):68-78. DOI: 10.1016/j.ydbio.2019.03.003. View

Villarroel-Campos D, Henriquez D, Bodaleo F, Oguchi M, Bronfman F, Fukuda M . Rab35 Functions in Axon Elongation Are Regulated by P53-Related Protein Kinase in a Mechanism That Involves Rab35 Protein Degradation and the Microtubule-Associated Protein 1B. J Neurosci. 2016; 36(27):7298-313. PMC: 6705529. DOI: 10.1523/JNEUROSCI.4064-15.2016. View

Bhartur S, Calhoun B, Woodrum J, Kurkjian J, Iyer S, Lai F . Genomic structure of murine Rab11 family members. Biochem Biophys Res Commun. 2000; 269(2):611-7. DOI: 10.1006/bbrc.2000.2334. View

Reish N, Boitet E, Bales K, Gross A . Nucleotide bound to rab11a controls localization in rod cells but not interaction with rhodopsin. J Neurosci. 2014; 34(45):14854-63. PMC: 4220021. DOI: 10.1523/JNEUROSCI.1943-14.2014. View

Macia E, Partisani M, Wang H, Lacas-Gervais S, Clainche C, Luton F . The C-terminal domain of EFA6A interacts directly with F-actin and assembles F-actin bundles. Sci Rep. 2019; 9(1):19209. PMC: 6915736. DOI: 10.1038/s41598-019-55630-9. View

Calhoun B, Goldenring J . Rab proteins in gastric parietal cells: evidence for the membrane recycling hypothesis. Yale J Biol Med. 1997; 69(1):1-8. PMC: 2588980. View

Nadarajah B, Parnavelas J . Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci. 2002; 3(6):423-32. DOI: 10.1038/nrn845. View

Chesneau L, Dambournet D, Machicoane M, Kouranti I, Fukuda M, Goud B . An ARF6/Rab35 GTPase cascade for endocytic recycling and successful cytokinesis. Curr Biol. 2012; 22(2):147-53. DOI: 10.1016/j.cub.2011.11.058. View

Kobayashi H, Fukuda M . Rab35 establishes the EHD1-association site by coordinating two distinct effectors during neurite outgrowth. J Cell Sci. 2013; 126(Pt 11):2424-35. DOI: 10.1242/jcs.117846. View

10.

Vetter I, Wittinghofer A . The guanine nucleotide-binding switch in three dimensions. Science. 2001; 294(5545):1299-304. DOI: 10.1126/science.1062023. View

11.

Gerges N, Backos D, Esteban J . Local control of AMPA receptor trafficking at the postsynaptic terminal by a small GTPase of the Rab family. J Biol Chem. 2004; 279(42):43870-8. DOI: 10.1074/jbc.M404982200. View

12.

George A, Hayden S, Stanton G, Brockerhoff S . Arf6 and the 5'phosphatase of synaptojanin 1 regulate autophagy in cone photoreceptors. Bioessays. 2016; 38 Suppl 1:S119-35. DOI: 10.1002/bies.201670913. View

13.

Houalla T, Shi L, van Meyel D, Rao Y . Rab-mediated vesicular transport is required for neuronal positioning in the developing Drosophila visual system. Mol Brain. 2010; 3:19. PMC: 2891732. DOI: 10.1186/1756-6606-3-19. View

14.

Huh M, Han J, Lim C, Lee S, Kim S, Kim E . Regulation of neuritogenesis and synaptic transmission by msec7-1, a guanine nucleotide exchange factor, in cultured Aplysia neurons. J Neurochem. 2003; 85(1):282-5. DOI: 10.1046/j.1471-4159.2003.01718.x. View

15.

Miyazaki H, Yamazaki M, Watanabe H, Maehama T, Yokozeki T, Kanaho Y . The small GTPase ADP-ribosylation factor 6 negatively regulates dendritic spine formation. FEBS Lett. 2005; 579(30):6834-8. DOI: 10.1016/j.febslet.2005.11.022. View

16.

Kouranti I, Sachse M, Arouche N, Goud B, Echard A . Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol. 2006; 16(17):1719-25. DOI: 10.1016/j.cub.2006.07.020. View

17.

Bhuin T, Roy J . Rab11 is required for embryonic nervous system development in Drosophila. Cell Tissue Res. 2008; 335(2):349-56. DOI: 10.1007/s00441-008-0711-8. View

18.

Eva R, Dassie E, Caswell P, Dick G, ffrench-Constant C, Norman J . Rab11 and its effector Rab coupling protein contribute to the trafficking of beta 1 integrins during axon growth in adult dorsal root ganglion neurons and PC12 cells. J Neurosci. 2010; 30(35):11654-69. PMC: 6633432. DOI: 10.1523/JNEUROSCI.2425-10.2010. View

19.

Nishino H, Saito T, Wei R, Takano T, Tsutsumi K, Taniguchi M . The LMTK1-TBC1D9B-Rab11A Cascade Regulates Dendritic Spine Formation via Endosome Trafficking. J Neurosci. 2019; 39(48):9491-9502. PMC: 6880470. DOI: 10.1523/JNEUROSCI.3209-18.2019. View

20.

Ang A, Taguchi T, Francis S, Folsch H, Murrells L, Pypaert M . Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J Cell Biol. 2004; 167(3):531-43. PMC: 2172492. DOI: 10.1083/jcb.200408165. View