CoChat
Sign Up
Cited by 20Cellular transport and secretionProtein Kinase Regulation and GTPase SignalingCaveolin-1 and cellular processes

A novel tribasic Golgi export signal directs cargo protein interaction with activated Rab11 and AP-1–dependent Golgi–plasma membrane trafficking

Open access
Parmar, Hirendrasinh B., Duncan, Roy·2016·Molecular Biology of the Cell
DOI 10.1091/mbc.e15-12-0845PMC PMC4831885
Open this paper in CoChat — free account

Abstract

The reovirus fusion–associated small transmembrane (FAST) proteins comprise a unique family of viral membrane fusion proteins dedicated to inducing cell–cell fusion. We recently reported that a polybasic motif (PBM) in the cytosolic tail of reptilian reovirus p14 FAST protein functions as a novel tribasic Golgi export signal. Using coimmunoprecipitation and fluorescence resonance energy transfer (FRET) assays, we now show the PBM directs interaction of p14 with GTP-Rab11. Overexpression of dominant-negative Rab11 and RNA interference knockdown of endogenous Rab11 inhibited p14 plasma membrane trafficking and resulted in p14 accumulation in the Golgi complex. This is the first example of Golgi export to the plasma membrane that is dependent on the interaction of membrane protein cargo with activated Rab11. RNA interference and immunofluorescence microscopy further revealed that p14 Golgi export is dependent on AP-1 (but not AP-3 or AP-4) and that Rab11 and AP-1 both colocalize with p14 at the TGN. Together these results imply the PBM mediates interactions of p14 with activated Rab11 at the TGN, resulting in p14 sorting into AP1-coated vesicles for anterograde TGN–plasma membrane transport.

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 · 10.1091/mbc.e15-12-0845

Cites

Statistics

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?

Self-check

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

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

Cites

No references could be resolved yet.

Research works printed but not linked: 72

  1. Aloisi AL Bucci C Rab GTPases-cargo direct interactions: fine modulators of intracellular trafficking Histol Histopathol 2013 28 839 849 23558751
  2. Ang AL Taguchi T Francis S Folsch H Murrells LJ Pypaert M Warren G Mellman I Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells J Cell Biol 2004 167 531 543 15534004 PMC2172492
  3. Bankaitis VA Garcia-Mata R Mousley CJ Golgi membrane dynamics and lipid metabolism Curr Biol 2012 22 R414 424 22625862 PMC4059015
  4. Barr FA Review series: Rab GTPases and membrane identity: causal or inconsequential J Cell Biol 2013 202 191 199 23878272 PMC3718981
  5. Boutilier J Duncan R The reovirus fusion-associated small transmembrane (FAST) proteins: virus-encoded cellular fusogens Curr Top Membr 2011 68 107 140 21771497
  6. Brewer CB Roth MG A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin J Cell Biol 1991 114 413 421 1860878 PMC2289095
  7. Cancino J Torrealba C Soza A Yuseff MI Gravotta D Henklein P Rodriguez-Boulan E Gonzalez A Antibody to AP1B adaptor blocks biosynthetic and recycling routes of basolateral proteins at recycling endosomes Mol Biol Cell 2007 18 4872 4884 17881725 PMC2096610
  8. Caswell PT Spence HJ Parsons M White DP Clark K Cheng KW Mills GB Humphries MJ Messent AJ Anderson KI Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments Dev Cell 2007 13 496 510 17925226
  9. Chen W Feng Y Chen D Wandinger-Ness A Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor Mol Biol Cell 1998 9 3241 3257 9802909 PMC25617
  10. Cheng SB Filardo EJ Trans-Golgi network (TGN) as a regulatory node for beta1-adrenergic receptor (beta1AR) down-modulation and recycling J Biol Chem 2012 287 14178 14191 22378779 PMC3340205
  11. Cheng SB Quinn JA Graeber CT Filardo EJ Down-modulation of the G-protein-coupled estrogen receptor, GPER, from the cell surface occurs via a trans-Golgi-proteasome pathway J Biol Chem 2011 286 22441 22455 21540189 PMC3121390
  12. Ciechonska M Key T Duncan R Efficient reovirus- and measles virus-mediated pore expansion during syncytium formation is dependent on annexin A1 and intracellular calcium J Virol 2014 88 6137 6147 24648446 PMC4093853
  13. Corcoran JA Clancy EK Duncan R Homomultimerization of the reovirus p14 fusion-associated small transmembrane protein during transit through the ER-Golgi complex secretory pathway J Gen Virol 2011a 92 162 166 20861318
  14. Corcoran JA Clancy EK Duncan R Homomultimerization of the reovirus p14 fusion-associated small transmembrane protein during transit through the ER-Golgi complex secretory pathway J Gen Virol 2011b 92 162 166 20861318
  15. Corcoran JA Duncan R Reptilian reovirus utilizes a small type III protein with an external myristylated amino terminus to mediate cell-cell fusion J Virol 2004 78 4342 4351 15047847 PMC374291
  16. Donaldson JG Jackson CL ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 2011 12 362 375 PMC3245550 21587297
  17. Dong C Yang L Zhang X Gu H Lam ML Claycomb WC Xia H Wu G Rab8 interacts with distinct motifs in alpha2B- and beta2-adrenergic receptors and differentially modulates their transport J Biol Chem 2010 285 20369 20380 20424170 PMC2888448
  18. Feige JN Sage D Wahli W Desvergne B Gelman L PixFRET, an ImageJ plug-in for FRET calculation that can accommodate variations in spectral bleed-throughs Microsc Res Tech 2005 68 51 58 16208719
  19. Folsch H Mattila PE Weisz OA Taking the scenic route: biosynthetic traffic to the plasma membrane in polarized epithelial cells Traffic 2009 10 972 981 19453969 PMC2786770
  20. Futter CE Connolly CN Cutler DF Hopkins CR Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface J Biol Chem 1995 270 10999 11003 7738042
  21. Giraudo CG Maccioni HJ Endoplasmic reticulum export of glycosyltransferases depends on interaction of a cytoplasmic dibasic motif with Sar1 Mol Biol Cell 2003 14 3753 3766 12972562 PMC196565
  22. Goldenring JR Shen KR Vaughan HD Modlin IM Identification of a small GTP-binding protein, Rab25, expressed in the gastrointestinal mucosa, kidney, and lung J Biol Chem 1993 268 18419 18422 8360141
  23. Guo X Mattera R Ren X Chen Y Retamal C Gonzalez A Bonifacino JS The adaptor protein-1 mu1B subunit expands the repertoire of basolateral sorting signal recognition in epithelial cells Dev Cell 2013 27 353 366 24229647 PMC3992434
  24. Hamelin E Theriault C Laroche G Parent JL The intracellular trafficking of the G protein-coupled receptor TPbeta depends on a direct interaction with Rab11 J Biol Chem 2005 280 36195 36205 16126723
  25. Hammad MM Kuang YQ Morse A Dupre DJ Rab1 interacts directly with the beta2-adrenergic receptor to regulate receptor anterograde trafficking Biol Chem 2012 393 541 546 22628317
  26. Hirst J Irving C Borner GH Adaptor protein complexes AP-4 and AP-5: new players in endosomal trafficking and progressive spastic paraplegia Traffic 2013 14 153 164 23167973
  27. Honing S Sandoval IV von Figura K A di-leucine-based motif in the cytoplasmic tail of LIMP-II and tyrosinase mediates selective binding of AP-3 EMBO J 1998 17 1304 1314 9482728 PMC1170479
  28. Hunziker W Fumey C A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells EMBO J 1994 13 2963 2969 8039492 PMC395183
  29. Hunziker W Harter C Matter K Mellman I Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant Cell 1991 66 907 920 1909606
  30. Hutagalung AH Novick PJ Role of Rab GTPases in membrane traffic and cell physiology Physiol Rev 2011 91 119 149 21248164 PMC3710122
  31. Jia R Xu F Qian J Yao Y Miao C Zheng YM Liu SL Guo F Geng Y Identification of an endocytic signal essential for the antiviral action of IFITM3 Cell Microbiol 2014 16 1080 1093 24521078 PMC4065222
  32. Kelly EE Horgan CP McCaffrey MW Rab11 proteins in health and disease Biochem Soc Trans 2012 40 1360 1367 23176481
  33. Key T Duncan R A compact, multifunctional fusion module directs cholesterol-dependent homomultimerization and syncytiogenic efficiency of reovirus p10 FAST proteins PLoS Pathog 2014 10 e1004023 24651689 PMC3961370
  34. Kikuchi A Yamashita T Kawata M Yamamoto K Ikeda K Tanimoto T Takai Y Purification and characterization of a novel GTP-binding protein with a molecular weight of 24,000 from bovine brain membranes J Biol Chem 1988 263 2897 2904 3125171
  35. Knodler A Feng S Zhang J Zhang X Das A Peranen J Guo W Coordination of Rab8 and Rab11 in primary ciliogenesis Proc Natl Acad Sci USA 2010 107 6346 6351 20308558 PMC2851980
  36. Lai F Stubbs L Artzt K Molecular analysis of mouse Rab11b: a new type of mammalian YPT/Rab protein Genomics 1994 22 610 616 8001972
  37. Lock JG Stow JL Rab11 in recycling endosomes regulates the sorting and basolateral transport of E-cadherin Mol Biol Cell 2005 16 1744 1755 15689490 PMC1073657
  38. Mardones GA Burgos PV Lin Y Kloer DP Magadan JG Hurley JH Bonifacino JS Structural basis for the recognition of tyrosine-based sorting signals by the mu3A subunit of the AP-3 adaptor complex J Biol Chem 2013 288 9563 9571 23404500 PMC3611023
  39. McDonold CM Fromme JC Four GTPases differentially regulate the Sec7 Arf-GEF to direct traffic at the trans-golgi network Dev Cell 2014 30 759 767 25220393 PMC4182139
  40. McEwen DP Schumacher SM Li Q Benson MD Iniguez-Lluhi JA Van Genderen KM Martens JR Rab-GTPase-dependent endocytic recycling of Kv1.5 in atrial myocytes J Biol Chem 2007 282 29612 29620 17673464
  41. Mellman I Nelson WJ Coordinated protein sorting, targeting and distribution in polarized cells. Nat Rev Mol Cell Biol 2008 9 833 845 PMC3369829 18946473
  42. Nishimura N Plutner H Hahn K Balch WE The delta subunit of AP-3 is required for efficient transport of VSV-G from the trans-Golgi network to the cell surface Proc Natl Acad Sci USA 2002 99 6755 6760 11997454 PMC124475
  43. Ohno H Clathrin-associated adaptor protein complexes J Cell Sci 2006 119 3719 3721 16959901
  44. Ohno H Stewart J Fournier MC Bosshart H Rhee I Miyatake S Saito T Gallusser A Kirchhausen T Bonifacino JS Interaction of tyrosine-based sorting signals with clathrin-associated proteins Science 1995 269 1872 1875 7569928
  45. Parent A Hamelin E Germain P Parent JL Rab11 regulates the recycling of the beta2-adrenergic receptor through a direct interaction Biochem J 2009 418 163 172 18983266
  46. Park SY Guo X Adaptor protein complexes and intracellular transport Biosci Rep 2014 34 PMC4114066 24975939
  47. Parmar HB Barry C Duncan R Polybasic trafficking signal mediates golgi export, ER retention or ER export and retrieval based on membrane-proximity PLoS One 2014a 9 e94194 24714640 PMC3979892
  48. Parmar HB Barry C Kai F Duncan R Golgi complex-plasma membrane trafficking directed by an autonomous, tribasic Golgi export signal Mol Biol Cell 2014b 25 866 878 24451258 PMC3952855
  49. Pellinen T Arjonen A Vuoriluoto K Kallio K Fransen JA Ivaska J Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins J Cell Biol 2006 173 767 780 16754960 PMC2063892
  50. Pfeffer SR Rab GTPase regulation of membrane identity Curr Opin Cell Biol 2013 25 414 419 23639309 PMC3729790
  51. Popova NV Deyev IE Petrenko AG Clathrin-mediated endocytosis and adaptor proteins Acta Naturae 2013 5 62 73 24307937 PMC3848845
  52. Rajasekaran AK Humphrey JS Wagner M Miesenbock G Le Bivic A Bonifacino JS Rodriguez-Boulan E TGN38 recycles basolaterally in polarized Madin-Darby canine kidney cells Mol Biol Cell 1994 5 1093 1103 7865877 PMC301133
  53. Ren X Farias GG Canagarajah BJ Bonifacino JS Hurley JH Structural basis for recruitment and activation of the AP-1 clathrin adaptor complex by Arf1 Cell 2013 152 755 767 23415225 PMC3913725
  54. Robinson MS Sahlender DA Foster SD Rapid inactivation of proteins by rapamycin-induced rerouting to mitochondria Dev Cell 2010 18 324 331 20159602 PMC2845799
  55. Rodriguez-Boulan E Kreitzer G Musch A Organization of vesicular trafficking in epithelia Nat Rev Mol Cell Biol 2005 6 233 247 15738988
  56. Rzomp KA Scholtes LD Briggs BJ Whittaker GR Scidmore MA Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner Infect Immun 2003 71 5855 5870 14500507 PMC201052
  57. Sakurada K Uchida K Yamaguchi K Aisaka K Ito S Ohmori T Takeyama Y Ueda T Hori Y Ohyanagi H Molecular cloning and characterization of a ras p21-like GTP-binding protein (24KG) from rat liver Biochem Biophys Res Commun 1991 177 1224 1232 1711847
  58. Santiago-Tirado FH Bretscher A Membrane-trafficking sorting hubs: cooperation between PI4P and small GTPases at the trans-Golgi network Trends Cell Biol 2011 21 515 525 21764313 PMC3164296
  59. Schindelin J Arganda-Carreras I Frise E Kaynig V Longair M Pietzsch T Preibisch S Rueden C Saalfeld S Schmid B Fiji: an open-source platform for biological-image analysis Nat Methods 2012 9 676 682 22743772 PMC3855844
  60. Somsel Rodman J Wandinger-Ness A Rab GTPases coordinate endocytosis J Cell Sci 2000 113 183 192 10633070
  61. Sekar RB Periasamy A Fluorescence resonance energy transfer (FRET) microscopy imaging of live cell protein localizations J Cell Biol 2003 160 629 633 12615908 PMC2173363
  62. Stenmark H (Rab GTPases as coordinators of vesicle traffic Nat Rev Mol Cell Biol 2009 10 513 525 19603039
  63. Takahashi M Ishiko T Kamohara H Hidaka H Ikeda O Ogawa M Baba H Curcumin (1,7-bis(4-hydroxy-3-methoxyphenyl)-1,6-heptadiene-3,5-dione) blocks the chemotaxis of neutrophils by inhibiting signal transduction through IL-8 receptors Mediators Inflamm 2007 2007 10767 17710245 PMC1940327
  64. Top D de Antueno R Salsman J Corcoran J Mader J Hoskin D Touhami A Jericho MH Duncan R Liposome reconstitution of a minimal protein-mediated membrane fusion machine EMBO J 2005 24 2980 2988 16079913 PMC1201348
  65. van de Graaf SF Chang Q Mensenkamp AR Hoenderop JG Bindels RJ Direct interaction with Rab11a targets the epithelial Ca2+ channels TRPV5 and TRPV6 to the plasma membrane Mol Cell Biol 2006 26 303 312 16354700 PMC1317621
  66. Vicinanza M D’Angelo G Di Campli A De Matteis MA Function and dysfunction of the PI system in membrane trafficking EMBO J 2008 27 2457 2470 18784754 PMC2536629
  67. Wang YJ Wang J Sun HQ Martinez M Sun YX Macia E Kirchhausen T Albanesi JP Roth MG Yin HL Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi Cell 2003 114 299 310 12914695
  68. Welz T Wellbourne-Wood J Kerkhoff E Orchestration of cell surface proteins by Rab11 Trends Cell Biol 2014 24 407 415 24675420
  69. Wikstrom K Reid HM Hill M English KA O’Keeffe MB Kimbembe CC Kinsella BT Recycling of the human prostacyclin receptor is regulated through a direct interaction with Rab11a GTPase Cell Signal 2008 20 2332 2346 18832025
  70. Wilson C Venditti R Rega LR Colanzi A D’Angelo G De Matteis MA The Golgi apparatus: an organelle with multiple complex functions Biochem J 2011 433 1 9 21158737
  71. Wilson GM Fielding AB Simon GC Yu X Andrews PD Hames RS Frey AM Peden AA Gould GW Prekeris R The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis Mol Biol Cell 2005 16 849 860 15601896 PMC545916
  72. Zimmermann R Eyrisch S Ahmad M Helms V Protein translocation across the ER membrane Biochim Biophys Acta 2011 1808 912 924 20599535

Cited by

Sorted by citations

Authors
Parmar, H. B., & Duncan, R.
Affiliations
Dalhousie University (CA)
Corresponding author
Duncan, Roy
ORCID
Duncan, Roy
Venue
Molecular Biology of the Cell
Publisher
American Society for Cell Biology (ASCB)
Published
2016-04-15
Volume
27
Issue
8
Pages
1320-1331
ISSN
  • 1059-1524 (ISSN-L)
  • 1939-4586
DOI
10.1091/mbc.e15-12-0845
PMC
PMC4831885
OpenAlex
W2334764705
Cited by
20
References
0
Citations by year
2025: 1 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 3 · 2020: 2 · 2019: 6 · 2018: 3 · 2016: 1
FWCI
2.28
Type
journal article
Language
en
Open access
Licence
cc-by-nc-sa
Locations
  • Molecular Biology of the Cell (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • Dalhousie University
  • Natural Sciences and Engineering Research Council of Canada
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
Keywords
Rab11, polybasic motif, AP-1, anterograde transport, coated vesicles, Golgi apparatus, cell-cell fusion
MeSH terms
rab11 GTP-Binding Proteins, Cell Membrane, Golgi Apparatus, Guanosine Triphosphate, HeLa Cells, Humans, Viral Proteins, Coated Vesicles, Transcription Factor AP-1, rab GTP-Binding Proteins, Protein Transport, Protein Sorting Signals, Protein Interaction Domains and Motifs

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