Tags

Type your tag names separated by a space and hit enter

Rab35 GTPase Triggers Switch-like Recruitment of the Lowe Syndrome Lipid Phosphatase OCRL on Newborn Endosomes.
Curr Biol 2016; 26(1):120-8CB

Abstract

Phosphoinositide (PtdIns) homeostasis requires a tight spatial and temporal regulation during the endocytic process [1]. Indeed, PtdIns(4,5)P2 plays a crucial role in endocytosis by controlling clathrin-coated pit formation, whereas its conversion into PtdIns4P right after scission of clathrin-coated vesicles (CCVs) is essential for successful uncoating and cargo sorting [1-6]. In non-neuronal cells, endosomal PtdIns(4,5)P2 hydrolysis critically relies on the lipid phosphatase OCRL [7-9], the inactivation of which causes the Oculo-Cerebro-Renal syndrome of Lowe [10, 11]. To understand the coupling between PtdIns(4,5)P2 hydrolysis and endosome formation, a key issue is thus to unravel the mechanism by which OCRL is recruited on CCVs precisely after their scission from the plasma membrane. Here we found that the Rab35 GTPase, which plays a fundamental but poorly understood role in endosomal trafficking after cargo internalization [12-21], directly recruits the OCRL phosphatase immediately after scission of the CCVs. Consistent with Rab35 and OCRL acting together, depletion of either Rab35 or OCRL leads to retention of internalized receptors such as the endogenous cation-independent mannose-6-phosphate receptor (CI-MPR) in peripheral clathrin-positive endosomes that display abnormal association with PtdIns(4,5)P2- and actin-binding proteins. Remarkably, Rab35 loading on CCVs rapidly follows the recruitment of the AP2-binding Rab35 GEF/activator DENND1A (connecdenn 1) and the disappearance of the Rab35 GAP/inhibitor EPI64B. We propose that the precise spatial and temporal activation of Rab35 acts as a major switch for OCRL recruitment on newborn endosomes, post-scission PtdIns(4,5)P2 hydrolysis, and subsequent endosomal trafficking.

Authors+Show Affiliations

Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department, Institut Pasteur, 25-28 Rue du Dr. Roux, 75724 Paris Cedex 15, France; Centre National de la Recherche Scientifique UMR3691, 75015 Paris, France; Institut de Formation Doctorale, Sorbonne Universités and Université Pierre et Marie Curie, Université Paris 06, 75252 Paris, France.University of Bordeaux, 33000 Bordeaux, France; Centre National de la Recherche Scientifique, Interdisciplinary Institute for Neuroscience, UMR 5297, 33000 Bordeaux, France.Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department, Institut Pasteur, 25-28 Rue du Dr. Roux, 75724 Paris Cedex 15, France; Centre National de la Recherche Scientifique UMR3691, 75015 Paris, France.Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department, Institut Pasteur, 25-28 Rue du Dr. Roux, 75724 Paris Cedex 15, France; Centre National de la Recherche Scientifique UMR3691, 75015 Paris, France.Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department, Institut Pasteur, 25-28 Rue du Dr. Roux, 75724 Paris Cedex 15, France; Centre National de la Recherche Scientifique UMR3691, 75015 Paris, France.Service de Néphrologie Pédiatrique, AP-HP Hôpital Necker, INSERM U983, 75015 Paris, France.University of Bordeaux, 33000 Bordeaux, France; Centre National de la Recherche Scientifique, Interdisciplinary Institute for Neuroscience, UMR 5297, 33000 Bordeaux, France. Electronic address: david.perrais@u-bordeaux.fr.Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department, Institut Pasteur, 25-28 Rue du Dr. Roux, 75724 Paris Cedex 15, France; Centre National de la Recherche Scientifique UMR3691, 75015 Paris, France. Electronic address: arnaud.echard@pasteur.fr.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

26725203

Citation

Cauvin, Clothilde, et al. "Rab35 GTPase Triggers Switch-like Recruitment of the Lowe Syndrome Lipid Phosphatase OCRL On Newborn Endosomes." Current Biology : CB, vol. 26, no. 1, 2016, pp. 120-8.
Cauvin C, Rosendale M, Gupta-Rossi N, et al. Rab35 GTPase Triggers Switch-like Recruitment of the Lowe Syndrome Lipid Phosphatase OCRL on Newborn Endosomes. Curr Biol. 2016;26(1):120-8.
Cauvin, C., Rosendale, M., Gupta-Rossi, N., Rocancourt, M., Larraufie, P., Salomon, R., ... Echard, A. (2016). Rab35 GTPase Triggers Switch-like Recruitment of the Lowe Syndrome Lipid Phosphatase OCRL on Newborn Endosomes. Current Biology : CB, 26(1), pp. 120-8. doi:10.1016/j.cub.2015.11.040.
Cauvin C, et al. Rab35 GTPase Triggers Switch-like Recruitment of the Lowe Syndrome Lipid Phosphatase OCRL On Newborn Endosomes. Curr Biol. 2016 Jan 11;26(1):120-8. PubMed PMID: 26725203.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Rab35 GTPase Triggers Switch-like Recruitment of the Lowe Syndrome Lipid Phosphatase OCRL on Newborn Endosomes. AU - Cauvin,Clothilde, AU - Rosendale,Morgane, AU - Gupta-Rossi,Neetu, AU - Rocancourt,Murielle, AU - Larraufie,Pierre, AU - Salomon,Rémi, AU - Perrais,David, AU - Echard,Arnaud, Y1 - 2015/12/24/ PY - 2015/06/18/received PY - 2015/10/23/revised PY - 2015/11/11/accepted PY - 2016/1/4/entrez PY - 2016/1/5/pubmed PY - 2016/11/5/medline SP - 120 EP - 8 JF - Current biology : CB JO - Curr. Biol. VL - 26 IS - 1 N2 - Phosphoinositide (PtdIns) homeostasis requires a tight spatial and temporal regulation during the endocytic process [1]. Indeed, PtdIns(4,5)P2 plays a crucial role in endocytosis by controlling clathrin-coated pit formation, whereas its conversion into PtdIns4P right after scission of clathrin-coated vesicles (CCVs) is essential for successful uncoating and cargo sorting [1-6]. In non-neuronal cells, endosomal PtdIns(4,5)P2 hydrolysis critically relies on the lipid phosphatase OCRL [7-9], the inactivation of which causes the Oculo-Cerebro-Renal syndrome of Lowe [10, 11]. To understand the coupling between PtdIns(4,5)P2 hydrolysis and endosome formation, a key issue is thus to unravel the mechanism by which OCRL is recruited on CCVs precisely after their scission from the plasma membrane. Here we found that the Rab35 GTPase, which plays a fundamental but poorly understood role in endosomal trafficking after cargo internalization [12-21], directly recruits the OCRL phosphatase immediately after scission of the CCVs. Consistent with Rab35 and OCRL acting together, depletion of either Rab35 or OCRL leads to retention of internalized receptors such as the endogenous cation-independent mannose-6-phosphate receptor (CI-MPR) in peripheral clathrin-positive endosomes that display abnormal association with PtdIns(4,5)P2- and actin-binding proteins. Remarkably, Rab35 loading on CCVs rapidly follows the recruitment of the AP2-binding Rab35 GEF/activator DENND1A (connecdenn 1) and the disappearance of the Rab35 GAP/inhibitor EPI64B. We propose that the precise spatial and temporal activation of Rab35 acts as a major switch for OCRL recruitment on newborn endosomes, post-scission PtdIns(4,5)P2 hydrolysis, and subsequent endosomal trafficking. SN - 1879-0445 UR - https://www.unboundmedicine.com/medline/citation/26725203/Rab35_GTPase_Triggers_Switch_like_Recruitment_of_the_Lowe_Syndrome_Lipid_Phosphatase_OCRL_on_Newborn_Endosomes_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0960-9822(15)01434-7 DB - PRIME DP - Unbound Medicine ER -