SNX-1 and RME-8 oppose the assembly of HGRS-1/ ESCRT-0 degradative microdomains on endosomes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 3, 2017, Pages E307-E316

  Norris, Anne ^a   Tammineni, Prasad ^a   Wang, Simon ^a   Gerdes, Julianne ^a   Murr, Alexandra ^a   Kwan, Kelvin Y ^b   Cai, Qian ^a   Grant, Barth D ^a  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Clathrin; Endosome; Hrs; RME 8; SNX 1

Indexed keywords

ESCRT PROTEIN; MUTANT PROTEIN; PROTEIN; PROTEIN HGRS 1; PROTEIN RME 8; PROTEIN VPS 35; SORTING NEXIN 1; SORTING NEXIN 2; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; HEPATOCYTE GROWTH FACTOR-REGULATED TYROSINE KINASE SUBSTRATE; PHOSPHOPROTEIN; RECOMBINANT PROTEIN; RME-8 PROTEIN, C ELEGANS; SMALL INTERFERING RNA; SNX-1 PROTEIN, C ELEGANS; SNX1 PROTEIN, HUMAN; SNX2 PROTEIN, HUMAN; SORTING NEXIN;

CAENORHABDITIS ELEGANS; CELL CYCLE; CELL FRACTIONATION; CONFERENCE PAPER; CONTROLLED STUDY; ENDOSOME; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ANIMAL; ANTAGONISTS AND INHIBITORS; GENE KNOCKDOWN; GENETICS; HELA CELL LINE; METABOLISM; PROTEIN TRANSPORT; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; PHOSPHOPROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; PROTEOLYSIS; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; SORTING NEXINS;

EID: 85009736667     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1612730114     Document Type: Article

References (97)

1. Mosesson Y, Mills GB, Yarden Y (2008) Derailed endocytosis: An emerging feature of cancer. Nat Rev Cancer 8(11):835-850.
2. Seaman MN, Marcusson EG, Cereghino JL, Emr SD (1997) Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J Cell Biol 137(1):79-92.
3. Hierro A, et al. (2007) Functional architecture of the retromer cargo-recognition complex. Nature 449(7165):1063-1067.
4. Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 165(1):123-133.
5. Swarbrick JD, et al. (2011) VPS29 is not an active metallo-phosphatase but is a rigid scaffold required for retromer interaction with accessory proteins. PLoS One 6(5): e20420.
6. Harbour ME, Seaman MN (2011) Evolutionary variations of VPS29, and their implications for the heteropentameric model of retromer. Commun Integr Biol 4(5):619-622.
7. Harterink M, et al. (2011) A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat Cell Biol 13(8):914-923.
8. Horazdovsky BF, et al. (1997) A sorting nexin-1 homologue, Vps5p, forms a complex with Vps17p and is required for recycling the vacuolar protein-sorting receptor. Mol Biol Cell 8(8):1529-1541.
9. Liu TT, Gomez TS, Sackey BK, Billadeau DD, Burd CG (2012) Rab GTPase regulation of retromer-mediated cargo export during endosome maturation. Mol Biol Cell 23(13): 2505-2515.
10. Wassmer T, et al. (2007) A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J Cell Sci 120(pt 1):45-54.
11. Lu N, Shen Q, Mahoney TR, Liu X, Zhou Z (2011) Three sorting nexins drive the degradation of apoptotic cells in response to PtdIns(3)P signaling. Mol Biol Cell 22(3): 354-374.
12. Carlton J, et al. (2004) Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Curr Biol 14(20):1791-1800.
13. van Weering JR, et al. (2012) Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO J 31(23):4466-4480.
14. Burd C, Cullen PJ (2014) Retromer: A master conductor of endosome sorting. Cold Spring Harb Perspect Biol 6(2):a016774.
15. McGough IJ, Cullen PJ (2011) Recent advances in retromer biology. Traffic 12(8): 963-971.
16. Shi A, et al. (2009) Regulation of endosomal clathrin and retromer-mediated endosome to Golgi retrograde transport by the J-domain protein RME-8. EMBO J 28(21): 3290-3302.
17. Popoff V, et al. (2009) Analysis of articulation between clathrin and retromer in retrograde sorting on early endosomes. Traffic 10(12):1868-1880.
18. Fujibayashi A, et al. (2008) Human RME-8 is involved in membrane trafficking through early endosomes. Cell Struct Funct 33(1):35-50.
19. Zhang Y, Grant B, Hirsh D (2001) RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol Biol Cell 12(7):2011-2021.
20. Walsh P, Bursać D, Law YC, Cyr D, Lithgow T (2004) The J-protein family: Modulating protein assembly, disassembly and translocation. EMBO Rep 5(6):567-571.
21. Ungewickell E, et al. (1995) Role of auxilin in uncoating clathrin-coated vesicles. Nature 378(6557):632-635.
22. Greener T, et al. (2001) Caenorhabditis elegans auxilin: A J-domain protein essential for clathrin-mediated endocytosis in vivo. Nat Cell Biol 3(2):215-219.
23. Xhabija B, Vacratsis PO (2015) Receptor-mediated endocytosis 8 utilizes an N-terminal phosphoinositide-binding motif to regulate endosomal clathrin dynamics. J Biol Chem 290(35):21676-21689.
24. Freeman CL, Hesketh G, Seaman MN (2014) RME-8 coordinates the activity of the WASH complex with the function of the retromer SNX dimer to control endosomal tubulation. J Cell Sci 127(pt 9):2053-2070.
25. Hurley JH (2010) The ESCRT complexes. Crit Rev Biochem Mol Biol 45(6):463-487.
26. Babst M (2011) MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Curr Opin Cell Biol 23(4):452-457.
27. Henne WM, Buchkovich NJ, Emr SD (2011) The ESCRT pathway. Dev Cell 21(1):77-91.
28. Polo S, et al. (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416(6879):451-455.
29. Bishop N, Horman A, Woodman P (2002) Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J Cell Biol 157(1):91-101.
30. Hofmann K, Falquet L (2001) A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem Sci 26(6):347-350.
31. Raiborg C, Stenmark H (2002) Hrs and endocytic sorting of ubiquitinated membrane proteins. Cell Struct Funct 27(6):403-408.
32. Raiborg C, et al. (2002) Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol 4(5):394-398.
33. Raiborg C, et al. (2001) FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. J Cell Sci 114(pt 12):2255-2263.
34. Sönnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149(4):901-914.
35. Sachse M, Urbé S, Oorschot V, Strous GJ, Klumperman J (2002) Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol Biol Cell 13(4):1313-1328.
36. Dinneen JL, Ceresa BP (2004) Continual expression of Rab5(Q79L) causes a ligandindependent EGFR internalization and diminishes EGFR activity. Traffic 5(8):606-615.
37. Gulappa T, Clouser CL, Menon KM (2011) The role of Rab5a GTPase in endocytosis and post-endocytic trafficking of the hCG-human luteinizing hormone receptor complex. Cell Mol Life Sci 68(16):2785-2795.
38. Stenmark H, et al. (1994) Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J 13(6):1287-1296.
39. Chen CC-H, et al. (2006) RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol Biol Cell 17(3):1286-1297.
40. Sato M, et al. (2011) Caenorhabditis elegans SNAP-29 is required for organellar integrity of the endomembrane system and general exocytosis in intestinal epithelial cells. Mol Biol Cell 22(14):2579-2587.
41. Gu M, et al. (2013) AP2 hemicomplexes contribute independently to synaptic vesicle endocytosis. eLife 2:e00190.
42. Waguri S, et al. (2003) Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol Biol Cell 14(1):142-155.
43. Ghosh RN, Mallet WG, Soe TT, McGraw TE, Maxfield FR (1998) An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J Cell Biol 142(4):923-936.
44. Bai Z, Grant BD (2015) A TOCA/CDC-42/PAR/WAVE functional module required for retrograde endocytic recycling. Proc Natl Acad Sci USA 112(12):E1443-E1452.
45. Belenkaya TY, et al. (2008) The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell 14(1):120-131.
46. Franch-Marro X, et al. (2008) Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat Cell Biol 10(2):170-177.
47. Pan CL, et al. (2008) C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/Wntless. Dev Cell 14(1):132-139.
48. Yang PT, et al. (2008) Wnt signaling requires retromer-dependent recycling of MIG- 14/Wntless in Wnt-producing cells. Dev Cell 14(1):140-147.
49. Port F, et al. (2008) Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat Cell Biol 10(2):178-185.
50. Seaman MN (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 165(1):111-122.
51. Lin SX, Grant B, Hirsh D, Maxfield FR (2001) Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat Cell Biol 3(6):567-572.
52. Lieu ZZ, Gleeson PA (2010) Identification of different itineraries and retromer components for endosome-to-Golgi transport of TGN38 and Shiga toxin. Eur J Cell Biol 89(5):379-393.
53. Rojas R, Kametaka S, Haft CR, Bonifacino JS (2007) Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol Cell Biol 27(3):1112-1124.
54. Raiborg C, Bache KG, Mehlum A, Stang E, Stenmark H (2001) Hrs recruits clathrin to early endosomes. EMBO J 20(17):5008-5021.
55. Chin LS, Raynor MC, Wei X, Chen HQ, Li L (2001) Hrs interacts with sorting nexin 1 and regulates degradation of epidermal growth factor receptor. J Biol Chem 276(10): 7069-7078.
56. Sato K, Norris A, Sato M, Grant BD (2014) C. elegans as a model for membrane traffic. WormBook Apr 25:1-47.
57. Fares H, Greenwald I (2001) Genetic analysis of endocytosis in Caenorhabditis elegans: Coelomocyte uptake defective mutants. Genetics 159(1):133-145.
58. Fares H, Greenwald I (2001) Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat Genet 28(1):64-68.
59. Nicot AS, et al. (2006) The phosphoinositide kinase PIKfyve/Fab1p regulates terminal lysosome maturation in Caenorhabditis elegans. Mol Biol Cell 17(7):3062-3074.
60. Tsai J, Douglas MG (1996) A conserved HPD sequence of the J-domain is necessary for YDJ1 stimulation of Hsp70 ATPase activity at a site distinct from substrate binding. J Biol Chem 271(16):9347-9354.
61. Cheetham ME, Caplan AJ (1998) Structure, function and evolution of DnaJ: Conservation and adaptation of chaperone function. Cell Stress Chaperones 3(1):28-36.
62. Yan W, Craig EA (1999) The glycine-phenylalanine-rich region determines the specificity of the yeast Hsp40 Sis1. Mol Cell Biol 19(11):7751-7758.
63. Sato K, et al. (2009) Differential requirements for clathrin in receptor-mediated endocytosis and maintenance of synaptic vesicle pools. Proc Natl Acad Sci USA 106(4): 1139-1144.
64. Raiborg C, et al. (2002) Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol 4(5):394-398.
65. Raiborg C, Wesche J, Malerød L, Stenmark H (2006) Flat clathrin coats on endosomes mediate degradative protein sorting by scaffolding Hrs in dynamic microdomains. J Cell Sci 119::2414-2424.
66. Gleason RJ, Akintobi AM, Grant BD, Padgett RW (2014) BMP signaling requires retromer- dependent recycling of the type I receptor. Proc Natl Acad Sci USA 111(7): 2578-2583.
67. McGough IJ, Cullen PJ (2013) Clathrin is not required for SNX-BAR-retromer-mediated carrier formation. J Cell Sci 126(pt 1):45-52.
68. van de Linde S, et al. (2011) Direct stochastic optical reconstruction microscopy with standard fluorescent probes. Nat Protoc 6(7):991-1009.
69. Helmuth JA, Paul G, Sbalzarini IF (2010) Beyond co-localization: Inferring spatial interactions between sub-cellular structures from microscopy images. BMC Bioinformatics 11:372.
70. Shivanandan A, Radenovic A, Sbalzarini IF (2013) MosaicIA: An ImageJ/Fiji plugin for spatial pattern and interaction analysis. BMC Bioinformatics 14:349.
71. Gruenberg J (2001) The endocytic pathway: A mosaic of domains. Nat Rev Mol Cell Biol 2(10):721-730.
72. Puthenveedu MA, et al. (2010) Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143(5):761-773.
73. Hunt SD, Townley AK, Danson CM, Cullen PJ, Stephens DJ (2013) Microtubule motors mediate endosomal sorting by maintaining functional domain organization. J Cell Sci 126(pt 11):2493-2501.
74. Louvard D, et al. (1983) A monoclonal antibody to the heavy chain of clathrin. EMBO J 2(10):1655-1664.
75. Raposo G, Tenza D, Murphy DM, Berson JF, Marks MS (2001) Distinct protein sorting and localization to premelanosomes, melanosomes, and lysosomes in pigmented melanocytic cells. J Cell Biol 152(4):809-824.
76. van Meel E, Klumperman J (2014) TGN exit of the cation-independent mannose 6-phosphate receptor does not require acid hydrolase binding. Cell Logist 4(3):e954441.
77. Klumperman J, Raposo G (2014) The complex ultrastructure of the endolysosomal system. Cold Spring Harb Perspect Biol 6(10):a016857.
78. Raiborg C (2006) Hrs makes receptors silent: A key to endosomal protein sorting. Crit Rev Oncog 12(3-4):295-discussion 295-296.
79. van Niel G, et al. (2011) The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev Cell 21(4):708-721.
80. Mayers JR, et al. (2011) ESCRT-0 assembles as a heterotetrameric complex on membranes and binds multiple ubiquitinylated cargoes simultaneously. J Biol Chem 286(11):9636-9645.
81. Derivery E, Helfer E, Henriot V, Gautreau A (2012) Actin polymerization controls the organization of WASH domains at the surface of endosomes. PLoS One 7(6):e39774.
82. Derivery E, Gautreau A (2015) Quantitative analysis of endosome tubulation and microdomain organization mediated by the WASH complex. Methods Cell Biol 130: 215-234.
83. Chang HC, Hull M, Mellman I (2004) The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila. J Cell Biol 164(7):1055-1064.
84. Girard M, McPherson PS (2008) RME-8 regulates trafficking of the epidermal growth factor receptor. FEBS Lett 582(6):961-966.
85. Girard M, Poupon V, Blondeau F, McPherson PS (2005) The DnaJ-domain protein RME-8 functions in endosomal trafficking. J Biol Chem 280(48):40135-40143.
86. Raiborg C, Wesche J, Malerød L, Stenmark H (2006) Flat clathrin coats on endosomes mediate degradative protein sorting by scaffolding Hrs in dynamic microdomains. J Cell Sci 119(pt 12):2414-2424.
87. Seaman MNJ, Freeman CL (2014) Analysis of the Retromer complex-WASH complex interaction illuminates new avenues to explore in Parkinson disease. Commun Integr Bio l 7:e29483.
88. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71-94.
89. Timmons L, Fire A (1998) Specific interference by ingested dsRNA. Nature 395(6705): 854.
90. Kamath RS, Ahringer J (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30(4):313-321.
91. Dempsey GT, Vaughan JC, Chen KH, Bates M, Zhuang X (2011) Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat Methods 8(12):1027-1036.
92. Henriques R, et al. (2010) QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ. Nat Methods 7(5):339-340.
93. Frøkjaer-Jensen C, et al. (2008) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40(11):1375-1383.
94. Praitis V, Casey E, Collar D, Austin J (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157(3):1217-1226.
95. Schweinsberg PJ, Grant BD C. elegans gene transformation by microparticle bombardment. WormBook Dec 30:1-10.
96. Dickinson DJ, Ward JD, Reiner DJ, Goldstein B (2013) Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods 10(10):1028-1034.
97. Kim E, Sun L, Gabel CV, Fang-Yen C (2013) Long-term imaging of Caenorhabditis elegans using nanoparticle-mediated immobilization. PLoS One 8(1):e53419.