CoChat
Sign Up
Cited by 181

The DOI matches its Crossref record; 6 of the 6 references it cites were found in a registry or an index.

Who’s in control? Principles of Rab GTPase activation in endolysosomal membrane trafficking and beyond

Borchers, Ann-Christin, Langemeyer, Lars, Ungermann, Christian·2021·Journal of Cell Biology
DOI 10.1083/jcb.202105120PMC PMC8366711
Open this paper in CoChat — free account

Abstract

The eukaryotic endomembrane system consists of multiple interconnected organelles. Rab GTPases are organelle-specific markers that give identity to these membranes by recruiting transport and trafficking proteins. During transport processes or along organelle maturation, one Rab is replaced by another, a process termed Rab cascade, which requires at its center a Rab-specific guanine nucleotide exchange factor (GEF). The endolysosomal system serves here as a prime example for a Rab cascade. Along with endosomal maturation, the endosomal Rab5 recruits and activates the Rab7-specific GEF Mon1-Ccz1, resulting in Rab7 activation on endosomes and subsequent fusion of endosomes with lysosomes. In this review, we focus on the current idea of Mon1-Ccz1 recruitment and activation in the endolysosomal and autophagic pathway. We compare identified principles to other GTPase cascades on endomembranes, highlight the importance of regulation, and evaluate in this context the strength and relevance of recent developments in in vitro analyses to understand the underlying foundation of organelle biogenesis and maturation.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1083/jcb.202105120

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The CCDC22-CCDC93 heterodimer is destabilized whenever any given COMMD protein is knocked out in cells or tissues.

    “This could explain why the CCDC22-CCDC93 heterodimer is destabilized whenever any given COMMD protein is knocked out in cells or in tissues14,25,46.”

    From Structural organization of the retriever–CCC endosomal recycling complex (2024) · cites this paper as [25]

    The passages from “GEF function and regulation in endosomal maturation” and “Lessons from reconstitution” discuss the Mon1-Ccz1 Rab7 activation complex, not the CCDC22-CCDC93 heterodimer. Searches for CCDC22, CCDC93, COMMD knockout, and complex destabilization found no passage addressing the claimed effect in cells or tissues. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 161

  1. Achstetter, 1988, SEC7 encodes an unusual, high molecular weight protein required for membrane traffic from the yeast Golgi apparatus, J. Biol. Chem., 263, 11711, 10.1016/S0021-9258(18)37842-6 · DOI
  2. Allaire, 2013, Interplay between Rab35 and Arf6 controls cargo recycling to coordinate cell adhesion and migration, J. Cell Sci., 126, 722, 10.1242/jcs.112375 · DOI · Paper page
  3. Babst, 2014, Quality control: quality control at the plasma membrane: one mechanism does not fit all, J. Cell Biol., 205, 11, 10.1083/jcb.201310113 · DOI
  4. Balderhaar, 2010, The Rab GTPase Ypt7 is linked to retromer-mediated receptor recycling and fusion at the yeast late endosome, J. Cell Sci., 123, 4085, 10.1242/jcs.071977 · DOI
  5. Balla, 2013, Phosphoinositides: tiny lipids with giant impact on cell regulation, Physiol. Rev., 93, 1019, 10.1152/physrev.00028.2012 · DOI · Paper page
  6. Ballabio, 2020, Lysosomes as dynamic regulators of cell and organismal homeostasis, Nat. Rev. Mol. Cell Biol., 21, 101, 10.1038/s41580-019-0185-4 · DOI · Paper page
  7. Barr, 2013, Review series: Rab GTPases and membrane identity: causal or inconsequential?, J. Cell Biol., 202, 191, 10.1083/jcb.201306010 · DOI
  8. Bean, 2015, Rab5-family guanine nucleotide exchange factors bind retromer and promote its recruitment to endosomes, Mol. Biol. Cell., 26, 1119, 10.1091/mbc.E14-08-1281 · DOI
  9. Bergbrede, 2009, Biophysical analysis of the interaction of Rab6a GTPase with its effector domains, J. Biol. Chem., 284, 2628, 10.1074/jbc.M806003200 · DOI
  10. Bezeljak, 2020, Stochastic activation and bistability in a Rab GTPase regulatory network, Proc. Natl. Acad. Sci. USA., 117, 6540, 10.1073/pnas.1921027117 · DOI
  11. Bharat, 2014, SNARE and regulatory proteins induce local membrane protrusions to prime docked vesicles for fast calcium-triggered fusion, EMBO Rep., 15, 308, 10.1002/embr.201337807 · DOI
  12. Blümer, 2013, RabGEFs are a major determinant for specific Rab membrane targeting, J. Cell Biol., 200, 287, 10.1083/jcb.201209113 · DOI
  13. Bonifacino, 2017, Moving and positioning the endolysosomal system, Curr. Opin. Cell Biol., 47, 1, 10.1016/j.ceb.2017.01.008 · DOI · Paper page
  14. Bowman, 2019, The road to lysosome-related organelles: Insights from Hermansky-Pudlak syndrome and other rare diseases, Traffic., 20, 404, 10.1111/tra.12646 · DOI · Paper page
  15. Bridges, 2012, Rab5 proteins regulate activation and localization of target of rapamycin complex 1, J. Biol. Chem., 287, 20913, 10.1074/jbc.M111.334060 · DOI
  16. Cabrera, 2013, Guanine nucleotide exchange factors (GEFs) have a critical but not exclusive role in organelle localization of Rab GTPases, J. Biol. Chem., 288, 28704, 10.1074/jbc.M113.488213 · DOI
  17. Cabrera, 2014, The Mon1-Ccz1 GEF activates the Rab7 GTPase Ypt7 via a longin-fold-Rab interface and association with PI3P-positive membranes, J. Cell Sci., 127, 1043, 10.1242/jcs.140921 · DOI
  18. Cabukusta, 2018, Mechanisms of lysosomal positioning and movement, Traffic., 19, 761, 10.1111/tra.12587 · DOI
  19. Cantalupo, 2001, Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes, EMBO J., 20, 683, 10.1093/emboj/20.4.683 · DOI · Paper page
  20. Cezanne, 2020, A non-linear system patterns Rab5 GTPase on the membrane, eLife., 9, 10.7554/elife.54434 · DOI
  21. Chen, 2009, Rab5 isoforms differentially regulate the trafficking and degradation of epidermal growth factor receptors, J. Biol. Chem., 284, 30328, 10.1074/jbc.M109.034546 · DOI
  22. Chen, 2014, Rab5 isoforms orchestrate a “division of labor” in the endocytic network; Rab5C modulates Rac-mediated cell motility, PLoS One., 9, 10.1371/journal.pone.0090384 · DOI
  23. Christoforidis, 1999, Phosphatidylinositol-3-OH kinases are Rab5 effectors, Nat. Cell Biol., 1, 249, 10.1038/12075 · DOI · Paper page
  24. Cui, 2014, Activation of the Rab7 GTPase by the MON1-CCZ1 Complex Is Essential for PVC-to-Vacuole Trafficking and Plant Growth in Arabidopsis, Plant Cell., 26, 2080, 10.1105/tpc.114.123141 · DOI
  25. Day, 2018, Budding Yeast Has a Minimal Endomembrane System, Dev. Cell., 44, 56, 10.1016/j.devcel.2017.12.014 · DOI
  26. de Renzis, 2002, Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes, Nat. Cell Biol., 4, 124, 10.1038/ncb744 · DOI
  27. Dehnen, 2020, A trimeric metazoan Rab7 GEF complex is crucial for endocytosis and scavenger function, J. Cell Sci., 133, 10.1242/jcs.247080 · DOI
  28. Del Conte-Zerial, 2008, Membrane identity and GTPase cascades regulated by toggle and cut-out switches, Mol. Syst. Biol., 4, 206, 10.1038/msb.2008.45 · DOI
  29. Delprato, 2007, Structural basis for Rab GTPase activation by VPS9 domain exchange factors, Nat. Struct. Mol. Biol., 14, 406, 10.1038/nsmb1232 · DOI
  30. Dirac-Svejstrup, 1997, Identification of a GDI displacement factor that releases endosomal Rab GTPases from Rab-GDI, EMBO J., 16, 465, 10.1093/emboj/16.3.465 · DOI
  31. Distefano, 2018, 10.1242/jcs.216630 · DOI · Paper page
  32. Dong, 2007, A catalytic coiled coil: structural insights into the activation of the Rab GTPase Sec4p by Sec2p, Mol. Cell., 25, 455, 10.1016/j.molcel.2007.01.013 · DOI
  33. Franke, 2019, Correlative single-molecule localization microscopy and electron tomography reveals endosome nanoscale domains, Traffic., 20, 601, 10.1111/tra.12671 · DOI
  34. Friedman, 2013, Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature, Mol. Biol. Cell., 24, 1030, 10.1091/mbc.e12-10-0733 · DOI
  35. Fujita, 2017, Genetic screen in Drosophila muscle identifies autophagy-mediated T-tubule remodeling and a Rab2 role in autophagy, eLife., 6, 10.7554/elife.23367 · DOI
  36. Galindo, 2021, Cryo-EM structure of metazoan TRAPPIII, the multi-subunit complex that activates the GTPase Rab1, EMBO J., 40, 10.15252/embj.2020107608 · DOI
  37. Gao, 2018, Molecular mechanism to target the endosomal Mon1-Ccz1 GEF complex to the pre-autophagosomal structure, eLife., 7, 10.7554/elife.31145 · DOI
  38. Gao, 2018, A novel in vitro assay reveals SNARE topology and the role of Ykt6 in autophagosome fusion with vacuoles, J. Cell Biol., 217, 3670, 10.1083/jcb.201804039 · DOI · Paper page
  39. Gerondopoulos, 2012, BLOC-3 mutated in Hermansky-Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor, Curr. Biol., 22, 2135, 10.1016/j.cub.2012.09.020 · DOI
  40. Gillingham, 2014, Toward a comprehensive map of the effectors of rab GTPases, Dev. Cell., 31, 358, 10.1016/j.devcel.2014.10.007 · DOI · Paper page
  41. Goody, 2017, Mechanisms of action of Rab proteins, key regulators of intracellular vesicular transport, Biol. Chem., 398, 565, 10.1515/hsz-2016-0274 · DOI
  42. Gorvel, 1991, rab5 controls early endosome fusion in vitro, Cell., 64, 915, 10.1016/0092-8674(91)90316-Q · DOI
  43. Guerra, 2016, Multiple Roles of the Small GTPase Rab7, Cells., 5, 34, 10.3390/cells5030034 · DOI
  44. Gustafson, 2017, Regulation of Arf activation occurs via distinct mechanisms at early and late Golgi compartments, Mol. Biol. Cell., 28, 3660, 10.1091/mbc.e17-06-0370 · DOI
  45. Gutierrez, 2004, Rab7 is required for the normal progression of the autophagic pathway in mammalian cells, J. Cell Sci., 117, 2687, 10.1242/jcs.01114 · DOI
  46. Hattula, 2002, A Rab8-specific GDP/GTP exchange factor is involved in actin remodeling and polarized membrane transport, Mol. Biol. Cell., 13, 3268, 10.1091/mbc.e02-03-0143 · DOI
  47. Hegedűs, 2016, The Ccz1-Mon1-Rab7 module and Rab5 control distinct steps of autophagy, Mol. Biol. Cell., 27, 3132, 10.1091/mbc.e16-03-0205 · DOI
  48. Horiuchi, 1997, A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function, Cell., 90, 1149, 10.1016/S0092-8674(00)80380-3 · DOI
  49. Huotari, 2011, Endosome maturation, EMBO J., 30, 3481, 10.1038/emboj.2011.286 · DOI
  50. Hutagalung, 2011, Role of Rab GTPases in membrane traffic and cell physiology, Physiol. Rev., 91, 119, 10.1152/physrev.00059.2009 · DOI · Paper page
  51. Itzen, 2007, Sec2 is a highly efficient exchange factor for the Rab protein Sec4, J. Mol. Biol., 365, 1359, 10.1016/j.jmb.2006.10.096 · DOI
  52. Jahn, 2006, SNAREs--engines for membrane fusion, Nat. Rev. Mol. Cell Biol., 7, 631, 10.1038/nrm2002 · DOI · Paper page
  53. Jeschke, 2016, Deciphering the roles of phosphoinositide lipids in phagolysosome biogenesis, Commun. Integr. Biol., 9, 10.1080/19420889.2016.1174798 · DOI
  54. 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
  55. Joiner, 2021, Structural basis of TRAPPIII-mediated Rab1 activation, EMBO J., 40, 10.15252/embj.2020107607 · DOI
  56. Jongsma, 2016, An ER-Associated Pathway Defines Endosomal Architecture for Controlled Cargo Transport, Cell., 166, 152, 10.1016/j.cell.2016.05.078 · DOI
  57. Jongsma, 2020, SKIP-HOPS recruits TBC1D15 for a Rab7-to-Arl8b identity switch to control late endosome transport, EMBO J., 39, 10.15252/embj.2019102301 · DOI
  58. Jordens, 2001, The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors, Curr. Biol., 11, 1680, 10.1016/S0960-9822(01)00531-0 · DOI · Paper page
  59. Kälin, 2015, Rabaptin5 is recruited to endosomes by Rab4 and Rabex5 to regulate endosome maturation, J. Cell Sci., 128, 4126, 10.1242/jcs.174664 · DOI
  60. Khatter, 2015, The small GTPase Arl8b regulates assembly of the mammalian HOPS complex on lysosomes, J. Cell Sci., 128, 1746, 10.1242/jcs.162651 · DOI
  61. Kinchen, 2010, Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells, Nature., 464, 778, 10.1038/nature08853 · DOI
  62. Kiontke, 2017, Architecture and mechanism of the late endosomal Rab7-like Ypt7 guanine nucleotide exchange factor complex Mon1-Ccz1, Nat. Commun., 8, 14034, 10.1038/ncomms14034 · DOI
  63. Kjos, 2017, Rab7b modulates autophagic flux by interacting with Atg4B, EMBO Rep., 18, 1727, 10.15252/embr.201744069 · DOI
  64. Klinkert, 2016, Rab35 GTPase: A Central Regulator of Phosphoinositides and F-actin in Endocytic Recycling and Beyond, Traffic., 17, 1063, 10.1111/tra.12422 · DOI · Paper page
  65. Knödler, 2010, Coordination of Rab8 and Rab11 in primary ciliogenesis, Proc. Natl. Acad. Sci. USA., 107, 6346, 10.1073/pnas.1002401107 · DOI
  66. Korolchuk, 2011, Lysosomal positioning coordinates cellular nutrient responses, Nat. Cell Biol., 13, 453, 10.1038/ncb2204 · DOI · Paper page
  67. Kouranti, 2006, Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis, Curr. Biol., 16, 1719, 10.1016/j.cub.2006.07.020 · DOI · Paper page
  68. Kovtun, 2018, Structure of the membrane-assembled retromer coat determined by cryo-electron tomography, Nature., 561, 561, 10.1038/s41586-018-0526-z · DOI · Paper page
  69. Kucera, 2016, Spatiotemporal Resolution of Rab9 and CI-MPR Dynamics in the Endocytic Pathway, Traffic., 17, 211, 10.1111/tra.12357 · DOI
  70. Kuchitsu, 2018, Revisiting Rab7 Functions in Mammalian Autophagy: Rab7 Knockout Studies, Cells., 7, 215, 10.3390/cells7110215 · DOI
  71. Kulasekaran, 2015, Phosphorylation-dependent Regulation of Connecdenn/DENND1 Guanine Nucleotide Exchange Factors, J. Biol. Chem., 290, 17999, 10.1074/jbc.M115.636712 · DOI
  72. Kulasekaran, 2021, An Arf/Rab cascade controls the growth and invasiveness of glioblastoma, J. Cell Biol., 220, 10.1083/jcb.202004229 · DOI
  73. Kvainickas, 2019, Retromer and TBC1D5 maintain late endosomal RAB7 domains to enable amino acid-induced mTORC1 signaling, J. Cell Biol., 218, 3019, 10.1083/jcb.201812110 · DOI · Paper page
  74. Lai, 2017, Molecular Mechanisms of Synaptic Vesicle Priming by Munc13 and Munc18, Neuron., 95, 591, 10.1016/j.neuron.2017.07.004 · DOI
  75. Laidlaw, 2018, Endosomal trafficking of yeast membrane proteins, Biochem. Soc. Trans., 46, 1551, 10.1042/BST20180258 · DOI
  76. Langemeyer, 2018, Rab GTPase Function in Endosome and Lysosome Biogenesis, Trends Cell Biol., 28, 957, 10.1016/j.tcb.2018.06.007 · DOI
  77. Langemeyer, 2018, A guanine nucleotide exchange factor (GEF) limits Rab GTPase-driven membrane fusion, J. Biol. Chem., 293, 731, 10.1074/jbc.M117.812941 · DOI
  78. Langemeyer, 2020, A conserved and regulated mechanism drives endosomal Rab transition, eLife., 9, 10.7554/elife.56090 · DOI
  79. Law, 2017, The VPS34 PI3K negatively regulates RAB-5 during endosome maturation, J. Cell Sci., 130, 2007, 10.1242/jcs.194746 · DOI
  80. Lawrence, 2014, Dynamic association of the PI3P-interacting Mon1-Ccz1 GEF with vacuoles is controlled through its phosphorylation by the type 1 casein kinase Yck3, Mol. Biol. Cell., 25, 1608, 10.1091/mbc.e13-08-0460 · DOI
  81. Lee, 2006, Structural basis for ubiquitin recognition and autoubiquitination by Rabex-5, Nat. Struct. Mol. Biol., 13, 264, 10.1038/nsmb1064 · DOI
  82. Leneva, 2021, Architecture and mechanism of metazoan retromer:SNX3 tubular coat assembly, Sci. Adv., 7, 10.1126/sciadv.abf8598 · DOI · Paper page
  83. Li, 2015, FgMon1, a guanine nucleotide exchange factor of FgRab7, is important for vacuole fusion, autophagy and plant infection in Fusarium graminearum, Sci. Rep., 5, 18101, 10.1038/srep18101 · DOI
  84. Linford, 2012, Rab14 and Its Exchange Factor FAM116 Link Endocytic Recycling and Adherens Junction Stability in Migrating Cells, Dev. Cell., 22, 952, 10.1016/j.devcel.2012.04.010 · DOI
  85. Ling, 2014, Osh4p is needed to reduce the level of phosphatidylinositol-4-phosphate on secretory vesicles as they mature, Mol. Biol. Cell., 25, 3389, 10.1091/mbc.e14-06-1087 · DOI
  86. Lipatova, 2019, Ypt/Rab GTPases and their TRAPP GEFs at the Golgi, FEBS Lett., 593, 2488, 10.1002/1873-3468.13574 · DOI
  87. Lippé, 2001, Functional synergy between Rab5 effector Rabaptin-5 and exchange factor Rabex-5 when physically associated in a complex, Mol. Biol. Cell., 12, 2219, 10.1091/mbc.12.7.2219 · DOI
  88. Liu, 2012, Rab GTPase regulation of retromer-mediated cargo export during endosome maturation, Mol. Biol. Cell., 23, 2505, 10.1091/mbc.e11-11-0915 · DOI
  89. Lombardi, 1993, Rab9 functions in transport between late endosomes and the trans Golgi network, EMBO J., 12, 677, 10.1002/j.1460-2075.1993.tb05701.x · DOI
  90. Lőrincz, 2017, Rab2 promotes autophagic and endocytic lysosomal degradation, J. Cell Biol., 216, 1937, 10.1083/jcb.201611027 · DOI
  91. Malsam, 2012, Complexin arrests a pool of docked vesicles for fast Ca2+-dependent release, EMBO J., 31, 3270, 10.1038/emboj.2012.164 · DOI
  92. Marat, 2016, Phosphatidylinositol 3-phosphates-at the interface between cell signalling and membrane traffic, EMBO J., 35, 561, 10.15252/embj.201593564 · DOI · Paper page
  93. Marwaha, 2017, The Rab7 effector PLEKHM1 binds Arl8b to promote cargo traffic to lysosomes, J. Cell Biol., 216, 1051, 10.1083/jcb.201607085 · DOI
  94. Mattera, 2006, The Rab5 guanine nucleotide exchange factor Rabex-5 binds ubiquitin (Ub) and functions as a Ub ligase through an atypical Ub-interacting motif and a zinc finger domain, J. Biol. Chem., 281, 6874, 10.1074/jbc.M509939200 · DOI
  95. McDonold, 2014, Four GTPases differentially regulate the Sec7 Arf-GEF to direct traffic at the trans-golgi network, Dev. Cell., 30, 759, 10.1016/j.devcel.2014.07.016 · DOI
  96. McEwan, 2015, PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins, Mol. Cell., 57, 39, 10.1016/j.molcel.2014.11.006 · DOI · Paper page
  97. Medkova, 2006, The rab exchange factor Sec2p reversibly associates with the exocyst, Mol. Biol. Cell., 17, 2757, 10.1091/mbc.e05-10-0917 · DOI
  98. Mima, 2009, Complex lipid requirements for SNARE- and SNARE chaperone-dependent membrane fusion, J. Biol. Chem., 284, 27114, 10.1074/jbc.M109.010223 · DOI
  99. Mizuno-Yamasaki, 2010, Phosphatidylinositol 4-phosphate controls both membrane recruitment and a regulatory switch of the Rab GEF Sec2p, Dev. Cell., 18, 828, 10.1016/j.devcel.2010.03.016 · DOI
  100. Nakatogawa, 2020, Mechanisms governing autophagosome biogenesis, Nat. Rev. Mol. Cell Biol., 21, 439, 10.1038/s41580-020-0241-0 · DOI
  101. Nordmann, 2010, The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7, Curr. Biol., 20, 1654, 10.1016/j.cub.2010.08.002 · DOI
  102. Ohya, 2009, Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes, Nature., 459, 1091, 10.1038/nature08107 · DOI
  103. Ortiz, 2002, Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast, J. Cell Biol., 157, 1005, 10.1083/jcb.200201003 · DOI
  104. Perini, 2014, Mammalian CORVET is required for fusion and conversion of distinct early endosome subpopulations, Traffic., 15, 1366, 10.1111/tra.12232 · DOI
  105. Pobbati, 2006, N- to C-terminal SNARE complex assembly promotes rapid membrane fusion, Science., 313, 673, 10.1126/science.1129486 · DOI
  106. Ponsford, 2021, Live imaging of intra-lysosome pH in cell lines and primary neuronal culture using a novel genetically encoded biosensor, Autophagy., 17, 1500, 10.1080/15548627.2020.1771858 · DOI
  107. Poteryaev, 2010, Identification of the switch in early-to-late endosome transition, Cell., 141, 497, 10.1016/j.cell.2010.03.011 · DOI · Paper page
  108. Progida, 2010, Rab7b controls trafficking from endosomes to the TGN, J. Cell Sci., 123, 1480, 10.1242/jcs.051474 · DOI
  109. Raiborg, 2015, ER-endosome contact sites: molecular compositions and functions, EMBO J., 34, 1848, 10.15252/embj.201591481 · DOI
  110. Ravikumar, 2008, Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease, J. Cell Sci., 121, 1649, 10.1242/jcs.025726 · DOI
  111. Reinisch, 2021, Mechanisms of nonvesicular lipid transport, J. Cell Biol., 220, 10.1083/jcb.202012058 · DOI
  112. Richardson, 2012, The Sec7 Arf-GEF is recruited to the trans-Golgi network by positive feedback, Dev. Cell., 22, 799, 10.1016/j.devcel.2012.02.006 · DOI
  113. Richardson, 2016, The Sec7 N-terminal regulatory domains facilitate membrane-proximal activation of the Arf1 GTPase, eLife., 5, 10.7554/eLife.12411 · DOI
  114. Riedel, 2018, The two TRAPP complexes of metazoans have distinct roles and act on different Rab GTPases, J. Cell Biol., 217, 601, 10.1083/jcb.201705068 · DOI
  115. Rink, 2005, Rab conversion as a mechanism of progression from early to late endosomes, Cell., 122, 735, 10.1016/j.cell.2005.06.043 · DOI
  116. Rocha, 2009, Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150 Glued and late endosome positioning, J. Cell Biol., 185, 1209, 10.1083/jcb.200811005 · DOI
  117. Rojas, 2008, Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7, J. Cell Biol., 183, 513, 10.1083/jcb.200804048 · DOI · Paper page
  118. Rowland, 2014, ER contact sites define the position and timing of endosome fission, Cell., 159, 1027, 10.1016/j.cell.2014.10.023 · DOI
  119. Sardana, 2021, Membrane Protein Quality Control Mechanisms in the Endo-Lysosome System, Trends Cell Biol., 31, 269, 10.1016/j.tcb.2020.11.011 · DOI
  120. Sato, 2008, Regulation of endocytic recycling by C. elegans Rab35 and its regulator RME-4, a coated-pit protein, EMBO J., 27, 1183, 10.1038/emboj.2008.54 · DOI · Paper page
  121. Schmitt, 1994, Synthesis and Characterization of Chelator-Lipids for Reversible Immobilization of Engineered Proteins at Self-Assembled Lipid Interfaces, J. Am. Chem. Soc., 116, 8485, 10.1021/ja00098a008 · DOI
  122. Schoebel, 2009, RabGDI displacement by DrrA from Legionella is a consequence of its guanine nucleotide exchange activity, Mol. Cell., 36, 1060, 10.1016/j.molcel.2009.11.014 · DOI
  123. Schu, 1993, Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting, Science., 260, 88, 10.1126/science.8385367 · DOI · Paper page
  124. Scorrano, 2019, Coming together to define membrane contact sites, Nat. Commun., 10, 1287, 10.1038/s41467-019-09253-3 · DOI
  125. 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
  126. Shin, 2020, The Lysosome at the Intersection of Cellular Growth and Destruction, Dev. Cell., 54, 226, 10.1016/j.devcel.2020.06.010 · DOI
  127. Simonetti, 2018, Endosomal Sorting: Architecture of the Retromer Coat, Curr. Biol., 28, R1350, 10.1016/j.cub.2018.10.040 · DOI
  128. Singer-Krüger, 1994, Role of three rab5-like GTPases, Ypt51p, Ypt52p, and Ypt53p, in the endocytic and vacuolar protein sorting pathways of yeast, J. Cell Biol., 125, 283, 10.1083/jcb.125.2.283 · DOI
  129. Singh, 2014, Protein delivery to vacuole requires SAND protein-dependent Rab GTPase conversion for MVB-vacuole fusion, Curr. Biol., 24, 1383, 10.1016/j.cub.2014.05.005 · DOI
  130. Sot, 2013, Ras GTPase activating (RasGAP) activity of the dual specificity GAP protein Rasal requires colocalization and C2 domain binding to lipid membranes, Proc. Natl. Acad. Sci. USA., 110, 111, 10.1073/pnas.1201658110 · DOI
  131. Spanò, 2018, Taking control: Hijacking of Rab GTPases by intracellular bacterial pathogens, Small GTPases., 9, 182, 10.1080/21541248.2017.1336192 · DOI
  132. Stalder, 2016, The casein kinases Yck1p and Yck2p act in the secretory pathway, in part, by regulating the Rab exchange factor Sec2p, Mol. Biol. Cell., 27, 686, 10.1091/mbc.E15-09-0651 · DOI
  133. Stalder, 2013, Phosphorylation of the Rab exchange factor Sec2p directs a switch in regulatory binding partners, Proc. Natl. Acad. Sci. USA., 110, 19995, 10.1073/pnas.1320029110 · DOI
  134. Südhof, 2009, Membrane fusion: grappling with SNARE and SM proteins, Science., 323, 474, 10.1126/science.1161748 · DOI · Paper page
  135. Sztul, 2019, ARF GTPases and their GEFs and GAPs: concepts and challenges, Mol. Biol. Cell., 30, 1249, 10.1091/mbc.E18-12-0820 · DOI
  136. Takahashi, 2012, Rab11 regulates exocytosis of recycling vesicles at the plasma membrane, J. Cell Sci., 125, 4049, 10.1242/jcs.102913 · DOI · Paper page
  137. Thomas, 2016, GTPase cross talk regulates TRAPPII activation of Rab11 homologues during vesicle biogenesis, J. Cell Biol., 215, 499, 10.1083/jcb.201608123 · DOI
  138. Thomas, 2018, The TRAPPIII complex activates the GTPase Ypt1 (Rab1) in the secretory pathway, J. Cell Biol., 217, 283, 10.1083/jcb.201705214 · DOI
  139. Thomas, 2019, A Steric Gating Mechanism Dictates the Substrate Specificity of a Rab-GEF, Dev. Cell., 48, 100, 10.1016/j.devcel.2018.11.013 · DOI
  140. Tremel, 2021, Structural basis for VPS34 kinase activation by Rab1 and Rab5 on membranes, Nat. Commun., 12, 1564, 10.1038/s41467-021-21695-2 · DOI
  141. Ungermann, 2019, Structure of membrane tethers and their role in fusion, Traffic., 20, 479, 10.1111/tra.12655 · DOI
  142. Vaites, 2017, Systematic Analysis of Human Cells Lacking ATG8 Proteins Uncovers Roles for GABARAPs and the CCZ1/MON1 Regulator C18orf8/RMC1 in Macroautophagic and Selective Autophagic Flux, Mol. Cell. Biol., 38, 10.1128/MCB.00392-17 · DOI · Paper page
  143. van den Boomen, 2020, A trimeric Rab7 GEF controls NPC1-dependent lysosomal cholesterol export, Nat. Commun., 11, 5559, 10.1038/s41467-020-19032-0 · DOI
  144. van der Kant, 2013, Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L, J. Cell Sci., 126, 3462, 10.1242/jcs.129270 · DOI
  145. van der Kant, 2015, Characterization of the Mammalian CORVET and HOPS Complexes and Their Modular Restructuring for Endosome Specificity, J. Biol. Chem., 290, 30280, 10.1074/jbc.M115.688440 · DOI
  146. Walch-Solimena, 1997, Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles, J. Cell Biol., 137, 1495, 10.1083/jcb.137.7.1495 · DOI
  147. Wallroth, 2018, Phosphoinositide conversion in endocytosis and the endolysosomal system, J. Biol. Chem., 293, 1526, 10.1074/jbc.r117.000629 · DOI · Paper page
  148. Wang, 2015, Activation of Rab8 guanine nucleotide exchange factor Rabin8 by ERK1/2 in response to EGF signaling, Proc. Natl. Acad. Sci. USA., 112, 148, 10.1073/pnas.1412089112 · DOI
  149. Wasmeier, 2006, Rab38 and Rab32 control post-Golgi trafficking of melanogenic enzymes, J. Cell Biol., 175, 271, 10.1083/jcb.200606050 · DOI · Paper page
  150. Weber, 1998, SNAREpins: minimal machinery for membrane fusion, Cell., 92, 759, 10.1016/S0092-8674(00)81404-X · DOI
  151. Wichmann, 1992, Endocytosis in yeast: evidence for the involvement of a small GTP-binding protein (Ypt7p), Cell., 71, 1131, 10.1016/S0092-8674(05)80062-5 · DOI
  152. Wickner, 2017, A cascade of multiple proteins and lipids catalyzes membrane fusion, Mol. Biol. Cell., 28, 707, 10.1091/mbc.e16-07-0517 · DOI
  153. Wu, 2021, Reticulon-3 Promotes Endosome Maturation at ER Membrane Contact Sites, Dev. Cell., 56, 52, 10.1016/j.devcel.2020.12.014 · DOI
  154. Xing, 2021, The Rab7 effector WDR91 promotes autophagy-lysosome degradation in neurons by regulating lysosome fusion, J. Cell Biol., 220, 10.1083/jcb.202007061 · DOI
  155. Xu, 2015, Phosphorylation of the exchange factor DENND3 by ULK in response to starvation activates Rab12 and induces autophagy, EMBO Rep., 16, 709, 10.15252/embr.201440006 · DOI
  156. Yamano, 2018, Endosomal Rab cycles regulate Parkin-mediated mitophagy, eLife., 7, 10.7554/eLife.31326 · DOI
  157. Yasuda, 2016, Mon1-Ccz1 activates Rab7 only on late endosomes and dissociates from the lysosome in mammalian cells, J. Cell Sci., 129, 329, 10.1242/jcs.178095 · DOI
  158. Zhang, 2014, Molecular mechanism for Rabex-5 GEF activation by Rabaptin-5, eLife., 3, 10.7554/eLife.02687 · DOI
  159. Zhao, 2019, Autophagosome maturation: An epic journey from the ER to lysosomes, J. Cell Biol., 218, 757, 10.1083/jcb.201810099 · DOI
  160. Zhou, 2017, A Rab5 GTPase module is important for autophagosome closure, PLoS Genet., 13, e1007020, 10.1371/journal.pgen.1007020 · DOI
  161. Zhou, 2019, Rab5-dependent autophagosome closure by ESCRT, J. Cell Biol., 218, 1908, 10.1083/jcb.201811173 · DOI

Cited by

Sorted by citations

Metadata

Authors
Borchers, A.-C., Langemeyer, L., & Ungermann, C.
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2021-08-12
Volume
220
Issue
9
ISSN
  • 0021-9525
  • 1540-8140
DOI
10.1083/jcb.202105120
PMC
PMC8366711
Cited by
181
References
6
Language
en
Licence
Funders
Deutsche Forschungsgemeinschaft (SFB 944, P11, UN111/13-1)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review