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TBC1D5 controls the GTPase cycle of Rab7b

Borg Distefano, Marita, Hofstad Haugen, Linda, Wang, Yan, Perdreau-Dahl, Harmonie, Kjos, Ingrid, Jia, Da, Morth, Jens Preben, Neefjes, Jacques, Bakke, Oddmund, Progida, Cinzia·2018·Journal of Cell Science

Abstract

Rab GTPases are key regulators of intracellular trafficking, and cycle between a GTP-bound active state and a GDP-bound inactive state. This cycle is regulated by guanine-nucleotide exchange factors (GEFs) and GTPase-activating proteins (GAPs). Several efforts have been made in connecting the correct GEFs and GAPs to their specific Rab. Here, we aimed to identify GAPs for Rab7b, the small GTPase involved in transport from late endosomes to the trans-Golgi. An siRNA screen targeting proteins containing TBC domains critical for Rab GAPs was performed and coupled to a phenotypic read-out that visualized the distribution of Rab7b. Silencing of TBC1D5 provided the strongest phenotype and this protein was subsequently validated in various in vitro and cell-based assays. TBC1D5 localizes to Rab7b-positive vesicles, interacts with Rab7b and has GAP activity towards Rab7b in vitro, which is further increased by retromer proteins. Similarly to the constitutively active mutant of Rab7b, inactivation of TBC1D5 also reduces the number of CI-MPR- and sortilin-positive vesicles. Together, the results show that TBC1D5 is a GAP for Rab7b in the control of endosomal transport to the trans-Golgi. This article has an associated First Person interview with the first author of the paper.

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  • The Retromer sub-domain proximity proteome included the RAB7 GAP TBC1D5, the RAB21/RAB32/RAB38 GEF VARP, and the RAB10 GEFs DENND4A and DENND4C.

    “These included known Retromer accessory proteins, the RAB7 GAP TBC1D546,77–81, the RAB21/RAB32/RAB38 GEF VARP (a.k.a. ANKRD27)47,48,82, and the RAB10 GEFs DENND4A and DENND4C83,84.”

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Research works printed but not linked: 54

  1. Baginski, 1967, Microdetermination of inorganic phosphate, phospholipids, and total phosphate in biologic materials, Clin. Chem., 13, 326, 10.1093/clinchem/13.4.326 · DOI
  2. Bärlocher, 2017, Structural insights into Legionella RidL-Vps29 retromer subunit interaction reveal displacement of the regulator TBC1D5, Nat. Commun., 8, 1543, 10.1038/s41467-017-01512-5 · DOI
  3. Barr, 2010, Rab GEFs and GAPs, Curr. Opin. Cell Biol., 22, 461, 10.1016/j.ceb.2010.04.007 · DOI
  4. Bergeland, 2006, Precise calculation of photoactivation kinetics, Nat. Methods, 3, 2042, 10.1038/nmeth982 · DOI
  5. Bergeland, 2008, Cell-cycle-dependent binding kinetics for the early endosomal tethering factor EEA1, EMBO Rep., 9, 171, 10.1038/sj.embor.7401152 · DOI
  6. Borg, 2014, A novel interaction between Rab7b and actomyosin reveals a dual role in intracellular transport and cell migration, J. Cell Sci., 127, 4927, 10.1242/jcs.155861 · DOI
  7. Bruinsma, 2012, Switching Polo-like kinase-1 on and off in time and space, Trends Biochem. Sci., 37, 534, 10.1016/j.tibs.2012.09.005 · DOI
  8. Cariani, 2004, Bismuth citrate in the quantification of inorganic phosphate and its utility in the determination of membrane-bound phosphatases, Anal. Biochem., 324, 79, 10.1016/j.ab.2003.09.008 · DOI
  9. Chaineau, 2013, Rab35: GEFs, GAPs and effectors, Traffic, 14, 1109, 10.1111/tra.12096 · DOI · Paper page
  10. Finsel, 2013, The Legionella effector RidL inhibits retrograde trafficking to promote intracellular replication, Cell Host Microbe, 14, 38, 10.1016/j.chom.2013.06.001 · DOI
  11. Frasa, 2010, Armus is a Rac1 effector that inactivates Rab7 and regulates E-cadherin degradation, Curr. Biol., 20, 198, 10.1016/j.cub.2009.12.053 · DOI
  12. Fuchs, 2007, Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways, J. Cell Biol., 177, 1133, 10.1083/jcb.200612068 · DOI
  13. Gavriljuk, 2012, Catalytic mechanism of a mammalian Rab.RabGAP complex in atomic detail, Proc. Natl. Acad. Sci. USA, 109, 21348, 10.1073/pnas.1214431110 · DOI
  14. Grosshans, 2006, Rabs and their effectors: achieving specificity in membrane traffic, Proc. Natl. Acad. Sci. USA, 103, 11821, 10.1073/pnas.0601617103 · DOI · Paper page
  15. Hanono, 2006, EPI64 regulates microvillar subdomains and structure, J. Cell Biol., 175, 803, 10.1083/jcb.200604046 · DOI
  16. Haugen, 2017, Endosomal binding kinetics of Eps15 and Hrs specifically regulate the degradation of RTKs, Sci. Rep., 7, 17962, 10.1038/s41598-017-17320-2 · DOI
  17. Hsu, 2010, Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C, J. Cell Biol., 189, 223, 10.1083/jcb.200911018 · DOI
  18. Itoh, 2006, Identification of EPI64 as a GTPase-activating protein specific for Rab27A, J. Biol. Chem., 281, 31823, 10.1074/jbc.M603808200 · DOI
  19. Itoh, 2011, OATL1, a novel autophagosome-resident Rab33B-GAP, regulates autophagosomal maturation, J. Cell Biol., 192, 839, 10.1083/jcb.201008107 · DOI
  20. Jia, 2016, Structural and mechanistic insights into regulation of the retromer coat by TBC1d5, Nat. Commun., 7, 13305, 10.1038/ncomms13305 · DOI · Paper page
  21. Jimenez-Orgaz, 2018, Control of RAB7 activity and localization through the retromer-TBC1D5 complex enables RAB7-dependent mitophagy, EMBO J., 37, 235, 10.15252/embj.201797128 · DOI · Paper page
  22. Jongsma, 2016, An ER-associated pathway defines endosomal architecture for controlled cargo transport, Cell, 166, 152, 10.1016/j.cell.2016.05.078 · DOI
  23. Kjos, 2017, Rab7b modulates autophagic flux by interacting with Atg4B, EMBO Rep., 18, 1727, 10.15252/embr.201744069 · DOI
  24. Lamb, 2016, TBC1D14 regulates autophagy via the TRAPP complex and ATG9 traffic, EMBO J., 35, 281, 10.15252/embj.201592695 · DOI
  25. Langemeyer, 2014, Diversity and plasticity in Rab GTPase nucleotide release mechanism has consequences for Rab activation and inactivation, eLife, 3, e01623, 10.7554/eLife.01623 · DOI
  26. Lippincott-Schwartz, 2001, Studying protein dynamics in living cells, Nat. Rev. Mol. Cell Biol., 2, 444, 10.1038/35073068 · DOI
  27. Longatti, 2012, TBC1D14 regulates autophagosome formation via Rab11- and ULK1-positive recycling endosomes, J. Cell Biol., 197, 659, 10.1083/jcb.201111079 · DOI
  28. Minowa-Nozawa, 2017, Rab35 GTPase recruits NPD52 to autophagy targets, EMBO J., 36, 2790, 10.15252/embj.201796463 · DOI
  29. Mishra, 2015, High-throughput assay for profiling the substrate specificity of Rab GTPase-activating proteins, Methods Mol. Biol., 1298, 47, 10.1007/978-1-4939-2569-8_4 · DOI
  30. Mukhopadhyay, 2007, An endocytic pathway as a target of tubby for regulation of fat storage, EMBO Rep., 8, 931, 10.1038/sj.embor.7401055 · DOI
  31. Muller, 2017, Molecular control of Rab activity by GEFs, GAPs and GDI, Small GTPases, 9, 5, 10.1080/21541248.2016.1276999. · DOI
  32. Nagai, 2013, All members of the EPI64 subfamily of TBC/RabGAPs also have GAP activities towards Ras, J. Biochem., 153, 283, 10.1093/jb/mvs147 · DOI
  33. Nordeng, 2002, The cytoplasmic tail of invariant chain regulates endosome fusion and morphology, Mol. Biol. Cell, 13, 1846, 10.1091/mbc.01-10-0478 · DOI
  34. Pan, 2006, TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism, Nature, 442, 303, 10.1038/nature04847 · DOI
  35. Paul, 2013, Studying MHC class II transport in dendritic cells, Methods Mol. Biol., 960, 489, 10.1007/978-1-62703-218-6_36 · DOI
  36. Pedro, 2017, Individual S-acylated cysteines differentially contribute to H-Ras endomembrane trafficking and acylation/deacylation cycles, Mol. Biol. Cell, 28, 962, 10.1091/mbc.e16-08-0603 · DOI
  37. Pelkmans, 2001, Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER, Nat. Cell Biol., 3, 473, 10.1038/35074539 · DOI
  38. Personnic, 2016, Subversion of retrograde trafficking by translocated pathogen effectors, Trends Microbiol., 24, 450, 10.1016/j.tim.2016.02.003 · DOI
  39. Popovic, 2012, Rab GTPase-activating proteins in autophagy: regulation of endocytic and autophagy pathways by direct binding to human ATG8 modifiers, Mol. Cell. Biol., 32, 1733, 10.1128/MCB.06717-11 · DOI
  40. Progida, 2007, RILP is required for the proper morphology and function of late endosomes, J. Cell Sci., 120, 3729, 10.1242/jcs.017301 · DOI
  41. Progida, 2010, Rab7b controls trafficking from endosomes to the TGN, J. Cell Sci., 123, 1480, 10.1242/jcs.051474 · DOI
  42. Progida, 2012, Dynamics of Rab7b-dependent transport of sorting receptors, Traffic, 13, 1273, 10.1111/j.1600-0854.2012.01388.x · DOI
  43. Pylypenko, 2017, Rab GTPases and their interacting protein partners: structural insights into Rab functional diversity, Small GTPases, 9, 22, 10.1080/21541248.2017.1336191 · DOI
  44. Reits, 2001, From fixed to FRAP: measuring protein mobility and activity in living cells, Nat. Cell Biol., 3, E145, 10.1038/35078615 · DOI
  45. Romano-Moreno, 2017, Molecular mechanism for the subversion of the retromer coat by the Legionella effector RidL, Proc. Natl. Acad. Sci. USA, 114, E11151, 10.1073/pnas.1715361115 · DOI
  46. Seaman, 2009, Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5, J. Cell Sci., 122, 2371, 10.1242/jcs.048686 · DOI · Paper page
  47. Skjeldal, 2012, The fusion of early endosomes induces molecular-motor-driven tubule formation and fission, J. Cell Sci., 125, 1910, 10.1242/jcs.092569 · DOI
  48. Stang, 1997, MHC class II-associated invariant chain-induced enlarged endosomal structures: a morphological study, Exp. Cell Res., 235, 79, 10.1006/excr.1997.3617 · DOI
  49. Wijdeven, 2016, Cholesterol and ORP1L-mediated ER contact sites control autophagosome transport and fusion with the endocytic pathway, Nat. Commun., 7, 11808, 10.1038/ncomms11808 · DOI
  50. Wubbolts, 1996, Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface, J. Cell Biol., 135, 611, 10.1083/jcb.135.3.611 · DOI
  51. Yang, 2004, Rab7b, a novel lysosome-associated small GTPase, is involved in monocytic differentiation of human acute promyelocytic leukemia cells, Biochem. Biophys. Res. Commun., 318, 792, 10.1016/j.bbrc.2004.04.115 · DOI
  52. Yao, 2018, Mechanism of inhibition of retromer transport by the bacterial effector RidL, Proc. Natl. Acad. Sci. USA, 115, E1446, 10.1073/pnas.1717383115 · DOI
  53. Yguerabide, 1982, Lateral mobility in membranes as detected by fluorescence recovery after photobleaching, Biophys. J., 40, 69, 10.1016/S0006-3495(82)84459-7 · DOI
  54. Zhang, 2005, TBC domain family, member 15 is a novel mammalian Rab GTPase-activating protein with substrate preference for Rab7, Biochem. Biophys. Res. Commun., 335, 154, 10.1016/j.bbrc.2005.07.070 · DOI

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Metadata

Authors
Borg Distefano, M., Hofstad Haugen, L., Wang, Y., Perdreau-Dahl, H., Kjos, I., Jia, D., Morth, J. P., Neefjes, J., Bakke, O., & Progida, C.
Affiliations
  • Centre for Immune Regulation, University of Oslo 1 Department of Biosciences , , 0316 Oslo , Norway
  • Key Laboratory of Birth Defects and Related Diseases of Women and Children 2 , Department of Paediatrics , , Chengdu 610041 , China
  • Norwegian Center of Molecular Medicine, Nordic EMBL Partnership, University of Oslo 3 , 0318 Oslo , Norway
  • Leiden University Medical Center LUMC 5 Department of Cell and Chemical Biology , , 2300 RC Leiden , The Netherlands
Venue
Journal of Cell Science
Published
2018-09-01
Volume
131
Issue
17
ISSN
  • 1477-9137
  • 0021-9533
Cited by
45
References
1
Language
en
Funders
  • Norwegian Cancer Society (5760850, 4604944)
  • Research Council of Norway (239903, 230779)

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