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PMID: 18957512 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

The Rip11/Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling.

Journal of cell science ·Vol. 121 ·No. Pt 22 ·2008-11-15 ·Pages 3824-33

Schonteich E, Wilson GM, Burden J, Hopkins CR, Anderson K, Goldenring JR, Prekeris R

Abstract

Sorting and recycling of endocytosed proteins are required for proper cellular function and growth. Internalized receptors either follow a fast constitutive recycling pathway, returning to the cell surface directly from the early endosomes, or a slow pathway that involves transport via perinuclear recycling endosomes. Slow recycling pathways are thought to play a key role in directing recycling proteins to specific locations on cell surfaces, such as the leading edges of motile cells. These pathways are regulated by various Rab GTPases, such as Rab4 and Rab11. Here we characterize the role of Rip11/FIP5, a known Rab11-binding protein, in regulating endocytic recycling. We use a combination of electron and fluorescent microscopy with siRNA-based protein knockdown to show that Rip11/FIP5 is present at the peripheral endosomes, where it regulates the sorting of internalized receptors to a slow recycling pathway. We also identify kinesin II as a Rip11/FIP5-binding protein and show that it is required for directing endocytosed proteins into the same recycling pathway. Thus, we propose that the Rip11/FIP5-kinesin-II complex has a key role in the routing of internalized receptors through the perinuclear recycling endosomes.

MeSH Terms
Adaptor Proteins, Signal Transducing Carrier Proteins/genetics,metabolism Endocytosis Endosomes/genetics,metabolism HeLa Cells Humans Kinesins/genetics,metabolism Mitochondrial Proteins/genetics,metabolism Protein Binding Protein Transport
Chemicals
Adaptor Proteins, Signal Transducing Carrier Proteins KIF3A protein, human KIF3B protein, human Mitochondrial Proteins RAB11FIP5 protein, human Kinesins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Schonteich Eric
Department of Cellular and Developmental Biology, School of Medicine, University of Colorado Health Sciences Center, 12801 E. 17th Avenue, Aurora, CO 80045, USA.
Wilson Gayle M
Burden Jemima
Hopkins Colin R
Anderson Keith
Goldenring James R
Prekeris Rytis
References (58)
58 references, click to expand
  1. Sec15 is an effector for the Rab11 GTPase in mammalian cells.
    J Biol Chem. 2004 Oct 8;279(41):43027-34 PMID: 15292201
  2. Molecular characterization of Rab11 interactions with members of the family of Rab11-interacting proteins.
    J Biol Chem. 2004 Aug 6;279(32):33430-7 PMID: 15173169
  3. Rab11 regulates recycling through the pericentriolar recycling endosome.
    J Cell Biol. 1996 Nov;135(4):913-24 PMID: 8922376
  4. Enhancement of the recycling and activation of beta-adrenergic receptor by Rab4 GTPase in cardiac myocytes.
    J Biol Chem. 2006 Apr 21;281(16):11097-103 PMID: 16484224
  5. Structural basis for Rab11-mediated recruitment of FIP3 to recycling endosomes.
    J Mol Biol. 2006 Nov 24;364(2):121-35 PMID: 17007872
  6. Identification of a link between the tumour suppressor APC and the kinesin superfamily.
    Nat Cell Biol. 2002 Apr;4(4):323-7 PMID: 11912492
  7. The leaden gene product is required with Rab27a to recruit myosin Va to melanosomes in melanocytes.
    Traffic. 2002 Mar;3(3):193-202 PMID: 11886590
  8. A role for the spectrin superfamily member Syne-1 and kinesin II in cytokinesis.
    J Cell Sci. 2004 Feb 1;117(Pt 4):619-29 PMID: 14709720
  9. Class I FIPs, Rab11-binding proteins that regulate endocytic sorting and recycling.
    Methods Enzymol. 2005;403:512-25 PMID: 16473616
  10. Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis.
    EMBO J. 2005 Oct 5;24(19):3389-99 PMID: 16148947
  11. Regulation of vesicle trafficking in madin-darby canine kidney cells by Rab11a and Rab25.
    J Biol Chem. 2000 Sep 15;275(37):29138-46 PMID: 10869360
  12. Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport.
    Mol Biol Cell. 2006 Jan;17 (1):163-77 PMID: 16251358
  13. Identification and characterization of a family of Rab11-interacting proteins.
    J Biol Chem. 2001 Oct 19;276(42):39067-75 PMID: 11495908
  14. Arfophilin is a common target of both class II and class III ADP-ribosylation factors.
    Biochemistry. 2001 Sep 11;40(36):10846-52 PMID: 11535061
  15. Structural basis for Rab11-dependent membrane recruitment of a family of Rab11-interacting protein 3 (FIP3)/Arfophilin-1.
    Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15416-21 PMID: 17030804
  16. Rab proteins, connecting transport and vesicle fusion.
    Traffic. 2005 Dec;6(12 ):1070-7 PMID: 16262719
  17. From sorting endosomes to exocytosis: association of Rab4 and Rab11 GTPases with the Fc receptor, FcRn, during recycling.
    Mol Biol Cell. 2005 Apr;16(4):2028-38 PMID: 15689494
  18. Novel heterotrimeric kinesin-related protein purified from sea urchin eggs.
    Nature. 1993 Nov 18;366(6452):268-70 PMID: 8232586
  19. Rab27a is an essential component of melanosome receptor for myosin Va.
    Mol Biol Cell. 2002 May;13(5):1735-49 PMID: 12006666
  20. Photoreceptor localization of the KIF3A and KIF3B subunits of the heterotrimeric microtubule motor kinesin II in vertebrate retina.
    Exp Eye Res. 1999 Nov;69(5):491-503 PMID: 10548469
  21. The subapical compartment: a traffic center in membrane polarity development.
    J Cell Sci. 2004 May 1;117(Pt 11):2183-92 PMID: 15126620
  22. Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease.
    Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5286-91 PMID: 12672950
  23. Insulin-induced GLUT4 translocation involves protein kinase C-lambda-mediated functional coupling between Rab4 and the motor protein kinesin.
    Mol Cell Biol. 2003 Jul;23 (14 ):4892-900 PMID: 12832475
  24. Completion of cytokinesis in C. elegans requires a brefeldin A-sensitive membrane accumulation at the cleavage furrow apex.
    Curr Biol. 2001 May 15;11(10):735-46 PMID: 11378383
  25. Myosin V, Rab11, and dRip11 direct apical secretion and cellular morphogenesis in developing Drosophila photoreceptors.
    J Cell Biol. 2007 May 21;177(4):659-69 PMID: 17517962
  26. Rabs and their effectors: achieving specificity in membrane traffic.
    Proc Natl Acad Sci U S A. 2006 Aug 8;103(32):11821-7 PMID: 16882731
  27. Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells.
    Mol Biol Cell. 1999 Jan;10 (1):47-61 PMID: 9880326
  28. Protein kinase A, which regulates intracellular transport, forms complexes with molecular motors on organelles.
    Curr Biol. 2004 Oct 26;14 (20):1877-81 PMID: 15498498
  29. Two binding partners cooperate to activate the molecular motor Kinesin-1.
    J Cell Biol. 2007 Jan 1;176(1):11-7 PMID: 17200414
  30. Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein.
    J Biol Chem. 2002 Apr 5;277(14 ):12190-9 PMID: 11786538
  31. Rabs, Rips, FIPs, and endocytic membrane traffic.
    ScientificWorldJournal. 2003 Sep 15;3:870-80 PMID: 14532427
  32. Endocytosis and molecular sorting.
    Annu Rev Cell Dev Biol. 1996;12:575-625 PMID: 8970738
  33. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway.
    Cell. 1992 Sep 4;70(5):729-40 PMID: 1516131
  34. Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling.
    J Biol Chem. 2002 Dec 27;277(52):50415-21 PMID: 12393859
  35. Arfophilins are dual Arf/Rab 11 binding proteins that regulate recycling endosome distribution and are related to Drosophila nuclear fallout.
    Mol Biol Cell. 2003 Jul;14 (7):2908-20 PMID: 12857874
  36. Identification of an organelle receptor for myosin-Va.
    Nat Cell Biol. 2002 Apr;4(4):271-8 PMID: 11887186
  37. A Role of myosin Vb and Rab11-FIP2 in the aquaporin-2 shuttle.
    Traffic. 2007 Feb;8(2):110-23 PMID: 17156409
  38. Slac2-a/melanophilin, the missing link between Rab27 and myosin Va: implications of a tripartite protein complex for melanosome transport.
    J Biol Chem. 2002 Apr 5;277(14 ):12432-6 PMID: 11856727
  39. Endocytic recycling.
    Nat Rev Mol Cell Biol. 2004 Feb;5(2):121-32 PMID: 15040445
  40. Kinesin-2 is a motor for late endosomes and lysosomes.
    Traffic. 2005 Dec;6(12):1114-24 PMID: 16262723
  41. Microtubule-dependent movement of late endocytic vesicles in vitro: requirements for Dynein and Kinesin.
    Mol Biol Cell. 2004 Aug;15(8):3688-97 PMID: 15181154
  42. Membrane dynamics in endocytosis.
    Cell. 1996 Jan 12;84(1):13-21 PMID: 8548817
  43. Myosin vb is associated with plasma membrane recycling systems.
    Mol Biol Cell. 2001 Jun;12 (6):1843-57 PMID: 11408590
  44. Role of the kinesin-2 family protein, KIF3, during mitosis.
    J Biol Chem. 2006 Feb 17;281(7):4094-9 PMID: 16298999
  45. The RCP-Rab11 complex regulates endocytic protein sorting.
    Mol Biol Cell. 2004 Aug;15(8):3530-41 PMID: 15181150
  46. Hypoxia stimulates carcinoma invasion by stabilizing microtubules and promoting the Rab11 trafficking of the alpha6beta4 integrin.
    Cancer Res. 2005 Apr 1;65(7):2761-9 PMID: 15805276
  47. Stimulation-dependent recycling of integrin beta1 regulated by ARF6 and Rab11.
    Traffic. 2004 Jan;5(1):20-36 PMID: 14675422
  48. Isolation of a sea urchin egg kinesin-related protein using peptide antibodies.
    J Cell Sci. 1992 Feb;101 ( Pt 2):291-301 PMID: 1629246
  49. Crystal structure of rab11 in complex with rab11 family interacting protein 2.
    Structure. 2006 Aug;14 (8):1273-83 PMID: 16905101
  50. The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis.
    Mol Biol Cell. 2005 Feb;16(2):849-60 PMID: 15601896
  51. Comparative proteomics of clathrin-coated vesicles.
    J Cell Biol. 2006 Nov 20;175(4):571-8 PMID: 17116749
  52. Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis.
    Curr Biol. 2003 Oct 28;13(21):1848-57 PMID: 14588240
  53. Kinesin superfamily protein 3 (KIF3) motor transports fodrin-associating vesicles important for neurite building.
    J Cell Biol. 2000 Mar 20;148(6):1255-65 PMID: 10725338
  54. Powering membrane traffic in endocytosis and recycling.
    Nat Rev Mol Cell Biol. 2006 Dec;7(12):897-908 PMID: 17139330
  55. In polarized MDCK cells basolateral vesicles arise from clathrin-gamma-adaptin-coated domains on endosomal tubules.
    J Cell Biol. 1998 May 4;141(3):611-23 PMID: 9566963
  56. A Rab11/Rip11 protein complex regulates apical membrane trafficking via recycling endosomes.
    Mol Cell. 2000 Dec;6(6):1437-48 PMID: 11163216
  57. Identification of a novel Rab11/25 binding domain present in Eferin and Rip proteins.
    J Biol Chem. 2001 Oct 19;276(42):38966-70 PMID: 11481332
  58. Formation of mutually exclusive Rab11 complexes with members of the family of Rab11-interacting proteins regulates Rab11 endocytic targeting and function.
    J Biol Chem. 2002 Dec 13;277(50):49003-10 PMID: 12376546
Article Info
Journal
Journal of cell science
Abbr.
J Cell Sci
ISSN
0021-9533
Published
2008-11-15
Epub
2008-00-28
Pages
3824-33
Language
English
Region
England
NLM ID
0052457
PMCID
PMC4365997
Subset
IM
Grants
NIDDK NIH HHS · R01 DK064380 · United States
NIDDK NIH HHS · R01 DK070856 · United States
NIDDK NIH HHS · R01DK-064380 · United States
NIDDK NIH HHS · R01DK-070856 · United States
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