Home LiteratureArticle Details
PMID: 21111236 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains.

Cell ·Vol. 143 ·No. 5 ·2010-11-24 ·Pages 761-73

Puthenveedu MA, Lauffer B, Temkin P, Vistein R, Carlton P, Thorn K, Taunton J, Weiner OD, Parton RG, von Zastrow M

Abstract

The functional consequences of signaling receptor endocytosis are determined by the endosomal sorting of receptors between degradation and recycling pathways. How receptors recycle efficiently, in a sequence-dependent manner that is distinct from bulk membrane recycling, is not known. Here, in live cells, we visualize the sorting of a prototypical sequence-dependent recycling receptor, the beta-2 adrenergic receptor, from bulk recycling proteins and the degrading delta-opioid receptor. Our results reveal a remarkable diversity in recycling routes at the level of individual endosomes, and indicate that sequence-dependent recycling is an active process mediated by distinct endosomal subdomains distinct from those mediating bulk recycling. We identify a specialized subset of tubular microdomains on endosomes, stabilized by a highly localized but dynamic actin machinery, that mediate this sorting, and provide evidence that these actin-stabilized domains provide the physical basis for a two-step kinetic and affinity-based model for protein sorting into the sequence-dependent recycling pathway.

MeSH Terms
Actins/metabolism Cell Line Cell Membrane/metabolism Cytoskeleton/metabolism Endosomes/metabolism Humans Kinetics Protein Structure, Tertiary Protein Transport Receptors, Adrenergic, beta-2/chemistry,metabolism Receptors, Opioid, delta/metabolism
Chemicals
Actins Receptors, Adrenergic, beta-2 Receptors, Opioid, delta
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Puthenveedu Manojkumar A
Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA, USA. map3@andrew.cmu.edu
Lauffer Benjamin
Temkin Paul
Vistein Rachel
Carlton Peter
Thorn Kurt
Taunton Jack
Weiner Orion D
Parton Robert G
von Zastrow Mark
References (57)
57 references, click to expand
  1. Regulating the actin cytoskeleton during vesicular transport.
    Curr Opin Cell Biol. 2002 Aug;14(4):428-33 PMID: 12383793
  2. ESCRT complexes and the biogenesis of multivesicular bodies.
    Curr Opin Cell Biol. 2008 Feb;20(1):4-11 PMID: 18222686
  3. Association of cortactin with dynamic actin in lamellipodia and on endosomal vesicles.
    J Cell Sci. 2000 Dec;113 Pt 24:4421-6 PMID: 11082035
  4. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis.
    Mol Biol Cell. 2005 Feb;16(2):964-75 PMID: 15601897
  5. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination.
    Biophys J. 2008 Jun;94(12):4957-70 PMID: 18326650
  6. Cooperation of phosphoinositides and BAR domain proteins in endosomal tubulation.
    Traffic. 2006 Nov;7(11):1539-50 PMID: 17010122
  7. Cortactin signalling and dynamic actin networks.
    Biochem J. 2004 Aug 15;382(Pt 1):13-25 PMID: 15186216
  8. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex.
    Dev Cell. 2009 Nov;17(5):712-23 PMID: 19922875
  9. The endocytic matrix.
    Nature. 2010 Jan 28;463(7280):464-73 PMID: 20110990
  10. SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment.
    Nat Cell Biol. 2007 Dec;9(12):1370-80 PMID: 17994011
  11. Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family.
    J Cell Biol. 1994 Sep;126(6):1445-53 PMID: 8089177
  12. Dysbindin promotes the post-endocytic sorting of G protein-coupled receptors to lysosomes.
    PLoS One. 2010 Feb 19;5(2):e9325 PMID: 20174469
  13. Delivery of ligands from sorting endosomes to late endosomes occurs by maturation of sorting endosomes.
    J Cell Biol. 1992 Apr;117(2):301-10 PMID: 1560027
  14. G protein-coupled receptor sorting to endosomes and lysosomes.
    Annu Rev Pharmacol Toxicol. 2008;48:601-29 PMID: 17995450
  15. Cargo-mediated regulation of a rapid Rab4-dependent recycling pathway.
    Mol Biol Cell. 2009 Jun;20(11):2774-84 PMID: 19369423
  16. Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited to sites of clathrin-mediated endocytosis in cultured fibroblasts.
    Eur J Cell Biol. 2004 Feb;83(1):13-8 PMID: 15085951
  17. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins.
    Nature. 1998 Jul 9;394(6689):192-5 PMID: 9671304
  18. A FAM21-containing WASH complex regulates retromer-dependent sorting.
    Dev Cell. 2009 Nov;17(5):699-711 PMID: 19922874
  19. Concentric zones of active RhoA and Cdc42 around single cell wounds.
    J Cell Biol. 2005 Jan 31;168(3):429-39 PMID: 15684032
  20. The association of NHERF adaptor proteins with g protein-coupled receptors and receptor tyrosine kinases.
    Annu Rev Physiol. 2006;68:491-505 PMID: 16460281
  21. Analysis of the role of p200-containing vesicles in post-Golgi traffic.
    Mol Biol Cell. 1996 Jun;7(6):961-74 PMID: 8817001
  22. Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex.
    Biochem J. 2004 May 15;380(Pt 1):1-17 PMID: 15040784
  23. NHERF-1 and the cytoskeleton regulate the traffic and membrane dynamics of G protein-coupled receptors.
    J Biol Chem. 2007 Aug 24;282(34):25076-87 PMID: 17599914
  24. Regulation of actin filament assembly by Arp2/3 complex and formins.
    Annu Rev Biophys Biomol Struct. 2007;36:451-77 PMID: 17477841
  25. A novel sorting sequence in the beta2-adrenergic receptor switches recycling from default to the Hrs-dependent mechanism.
    J Biol Chem. 2007 Feb 2;282(5):3095-104 PMID: 17138565
  26. Distinct modes of regulated receptor insertion to the somatodendritic plasma membrane.
    Nat Neurosci. 2006 May;9(5):622-7 PMID: 16604070
  27. Regulation of GPCRs by endocytic membrane trafficking and its potential implications.
    Annu Rev Pharmacol Toxicol. 2008;48:537-68 PMID: 18184106
  28. Endosomal sorting and signalling: an emerging role for sorting nexins.
    Nat Rev Mol Cell Biol. 2008 Jul;9(7):574-82 PMID: 18523436
  29. Sequestration and recycling of beta 2-adrenergic receptors permit receptor resensitization.
    Mol Pharmacol. 1995 Apr;47(4):666-76 PMID: 7723728
  30. Dynamics of endocytic vesicle creation.
    Dev Cell. 2005 Nov;9(5):581-92 PMID: 16256734
  31. Intracellular membrane traffic: pathways, carriers, and sorting devices.
    Methods Enzymol. 1983;98:1-13 PMID: 6422205
  32. Coronins: the return of the crown.
    Trends Cell Biol. 2006 Aug;16(8):421-6 PMID: 16806932
  33. Dynamin2 and cortactin regulate actin assembly and filament organization.
    Curr Biol. 2002 Oct 29;12(21):1852-7 PMID: 12419186
  34. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor.
    Nature. 1999 Sep 16;401(6750):286-90 PMID: 10499588
  35. Organizing the cell cortex: the role of ERM proteins.
    Nat Rev Mol Cell Biol. 2010 Apr;11(4):276-87 PMID: 20308985
  36. Recycling receptors: the round-trip itinerary of migrant membrane proteins.
    Cell. 1983 Mar;32(3):663-7 PMID: 6299572
  37. Engineered protein connectivity to actin mimics PDZ-dependent recycling of G protein-coupled receptors but not its regulation by Hrs.
    J Biol Chem. 2009 Jan 23;284(4):2448-58 PMID: 19001361
  38. pH-induced microtubule-dependent redistribution of late endosomes in neuronal and epithelial cells.
    J Cell Biol. 1991 Apr;113(2):261-74 PMID: 2010463
  39. Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape.
    J Cell Biol. 2000 Oct 2;151(1):187-98 PMID: 11018064
  40. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process.
    J Cell Biol. 1993 Jun;121(6):1257-69 PMID: 8509447
  41. WASH and the Arp2/3 complex regulate endosome shape and trafficking.
    Cytoskeleton (Hoboken). 2010 Mar;67(3):193-206 PMID: 20175130
  42. Type I PDZ ligands are sufficient to promote rapid recycling of G Protein-coupled receptors independent of binding to N-ethylmaleimide-sensitive factor.
    J Biol Chem. 2005 Feb 4;280(5):3305-13 PMID: 15548537
  43. Biogenesis and function of multivesicular bodies.
    Annu Rev Cell Dev Biol. 2007;23:519-47 PMID: 17506697
  44. Endocytic recycling.
    Nat Rev Mol Cell Biol. 2004 Feb;5(2):121-32 PMID: 15040445
  45. Myocyte adrenoceptor signaling pathways.
    Science. 2003 Jun 6;300(5625):1530-2 PMID: 12791980
  46. A modular design for the clathrin- and actin-mediated endocytosis machinery.
    Cell. 2005 Oct 21;123(2):305-20 PMID: 16239147
  47. Modulation of postendocytic sorting of G protein-coupled receptors.
    Science. 2002 Jul 26;297(5581):615-20 PMID: 12142540
  48. Endocytosis and the recycling of plasma membrane.
    J Cell Biol. 1983 Jan;96(1):1-27 PMID: 6298247
  49. ESCRTing proteins in the endocytic pathway.
    Trends Biochem Sci. 2007 Dec;32(12):561-73 PMID: 17988873
  50. Essential role of Hrs in a recycling mechanism mediating functional resensitization of cell signaling.
    EMBO J. 2005 Jul 6;24(13):2265-83 PMID: 15944737
  51. Rab proteins as membrane organizers.
    Nat Rev Mol Cell Biol. 2001 Feb;2(2):107-17 PMID: 11252952
  52. The emerging shape of the ESCRT machinery.
    Nat Rev Mol Cell Biol. 2007 May;8(5):355-68 PMID: 17450176
  53. Endocytosis and signalling: intertwining molecular networks.
    Nat Rev Mol Cell Biol. 2009 Sep;10(9):609-22 PMID: 19696798
  54. Cargo regulates clathrin-coated pit dynamics.
    Cell. 2006 Oct 6;127(1):113-24 PMID: 17018281
  55. Actin in the endocytic pathway: from yeast to mammals.
    FEBS Lett. 2008 Jun 18;582(14):2112-9 PMID: 18420037
  56. Mechanisms of beta-adrenergic receptor desensitization and resensitization.
    Adv Pharmacol. 1998;42:416-20 PMID: 9327928
  57. Cortactin branches out: roles in regulating protrusive actin dynamics.
    Cell Motil Cytoskeleton. 2008 Sep;65(9):687-707 PMID: 18615630
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
DOI
10.1016/j.cell.2010.10.003
Email
map3@andrew.cmu.edu
Published
2010-11-24
Pages
761-73
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC3058345
Subset
IM
Grants
NIDA NIH HHS · R37 DA010711 · United States
NIDA NIH HHS · K99 DA024698 · United States
NIGMS NIH HHS · R01 GM084040 · United States
NIDA NIH HHS · R00 DA024698-02 · United States
NIDA NIH HHS · R29 DA010711 · United States
NIDA NIH HHS · R00 DA024698 · United States
NIDA NIH HHS · R01 DA010711 · United States
NIDA NIH HHS · K99/R00 DA024698 · United States
NIGMS NIH HHS · R01 GM084040-03 · United States
Corrections
CommentIn
PMID: 21179055
External Links
PubMed source DOI: 10.1016/j.cell.2010.10.003 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2