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PMID: 17485489 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

v-SNARE cellubrevin is required for basolateral sorting of AP-1B-dependent cargo in polarized epithelial cells.

The Journal of cell biology ·Vol. 177 ·No. 3 ·2007-05-07 ·Pages 477-88

Fields IC, Shteyn E, Pypaert M, Proux-Gillardeaux V, Kang RS, Galli T, Fölsch H

Abstract

The epithelial cell-specific adaptor complex AP-1B is crucial for correct delivery of many transmembrane proteins from recycling endosomes to the basolateral plasma membrane. Subsequently, membrane fusion is dependent on the formation of complexes between SNARE proteins located at the target membrane and on transport vesicles. Although the t-SNARE syntaxin 4 has been localized to the basolateral membrane, the v-SNARE operative in the AP-1B pathway remained unknown. We show that the ubiquitously expressed v-SNARE cellubrevin localizes to the basolateral membrane and to recycling endosomes, where it colocalizes with AP-1B. Furthermore, we demonstrate that cellubrevin coimmunoprecipitates preferentially with syntaxin 4, implicating this v-SNARE in basolateral fusion events. Cleavage of cellubrevin with tetanus neurotoxin (TeNT) results in scattering of AP-1B localization and missorting of AP-1B-dependent cargos, such as transferrin receptor and a truncated low-density lipoprotein receptor, LDLR-CT27. These data suggest that cellubrevin and AP-1B cooperate in basolateral membrane trafficking.

MeSH Terms
Adaptor Protein Complex 1/genetics,metabolism Adaptor Protein Complex beta Subunits/genetics,metabolism Animals Cell Line Cell Membrane/metabolism Cell Polarity/drug effects,physiology Dogs Endosomes/metabolism Epithelial Cells/cytology,metabolism Humans Membrane Fusion/drug effects,physiology Metalloendopeptidases/pharmacology Protein Transport/drug effects,physiology Qa-SNARE Proteins/genetics,metabolism Receptors, LDL/metabolism SNARE Proteins/genetics,metabolism Tetanus Toxin/pharmacology Vesicle-Associated Membrane Protein 3/genetics,metabolism
Chemicals
AP1B1 protein, human Adaptor Protein Complex 1 Adaptor Protein Complex beta Subunits Qa-SNARE Proteins Receptors, LDL SNARE Proteins Tetanus Toxin VAMP3 protein, human Vesicle-Associated Membrane Protein 3 tetanospasmin Metalloendopeptidases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Fields Ian C
Department of Biochemistry, Molecular Biology and Cell Biology, Northwestern University, Evanston, IL 60208, USA.
Shteyn Elina
Pypaert Marc
Proux-Gillardeaux Véronique
Kang Richard S
Galli Thierry
Fölsch Heike
References (58)
58 references, click to expand
  1. The building blocks for basolateral vesicles in polarized epithelial cells.
    Trends Cell Biol. 2005 Apr;15(4):222-8 PMID: 15817379
  2. Organization of vesicular trafficking in epithelia.
    Nat Rev Mol Cell Biol. 2005 Mar;6(3):233-47 PMID: 15738988
  3. Transcytosis of NgCAM in epithelial cells reflects differential signal recognition on the endocytic and secretory pathways.
    J Cell Biol. 2005 Aug 15;170(4):595-605 PMID: 16087710
  4. The role of syntaxins in the specificity of vesicle targeting in polarized epithelial cells.
    Mol Biol Cell. 2005 Dec;16(12):5784-92 PMID: 16207812
  5. Syntaxins 3 and 4 are concentrated in separate clusters on the plasma membrane before the establishment of cell polarity.
    Mol Biol Cell. 2006 Feb;17(2):977-89 PMID: 16339081
  6. Apical targeting of syntaxin 3 is essential for epithelial cell polarity.
    J Cell Biol. 2006 Jun 19;173(6):937-48 PMID: 16785322
  7. The exocyst defrocked, a framework of rods revealed.
    Nat Struct Mol Biol. 2006 Jul;13(7):577-81 PMID: 16826234
  8. SNAREs--engines for membrane fusion.
    Nat Rev Mol Cell Biol. 2006 Sep;7(9):631-43 PMID: 16912714
  9. AP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells.
    Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1564-9 PMID: 17244703
  10. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells.
    Cell. 1999 Oct 15;99(2):189-98 PMID: 10535737
  11. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells.
    J Cell Biol. 2001 Feb 5;152(3):595-606 PMID: 11157985
  12. SNARE protein trafficking in polarized MDCK cells.
    Traffic. 2000 Jul;1(7):553-60 PMID: 11208143
  13. Adaptor-related proteins.
    Curr Opin Cell Biol. 2001 Aug;13(4):444-53 PMID: 11454451
  14. Adaptins: the final recount.
    Mol Biol Cell. 2001 Oct;12(10):2907-20 PMID: 11598180
  15. Biological basket weaving: formation and function of clathrin-coated vesicles.
    Annu Rev Cell Dev Biol. 2001;17:517-68 PMID: 11687498
  16. The Di-leucine motif of vesicle-associated membrane protein 4 is required for its localization and AP-1 binding.
    J Biol Chem. 2001 Dec 28;276(52):49183-7 PMID: 11598115
  17. AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells.
    Nat Cell Biol. 2002 Feb;4(2):154-9 PMID: 11802162
  18. 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 U S A. 2002 May 14;99(10):6755-60 PMID: 11997454
  19. Differential recognition of tyrosine-based basolateral signals by AP-1B subunit mu1B in polarized epithelial cells.
    Mol Biol Cell. 2002 Jul;13(7):2374-82 PMID: 12134076
  20. The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane.
    Nat Cell Biol. 2002 Aug;4(8):605-9 PMID: 12105417
  21. SNARE expression and localization in renal epithelial cells suggest mechanism for variability of trafficking phenotypes.
    Am J Physiol Renal Physiol. 2002 Nov;283(5):F1111-22 PMID: 12372788
  22. Three-dimensional analysis of post-Golgi carrier exocytosis in epithelial cells.
    Nat Cell Biol. 2003 Feb;5(2):126-36 PMID: 12545172
  23. Polarized epithelial membrane traffic: conservation and plasticity.
    Nat Cell Biol. 2003 Apr;5(4):287-93 PMID: 12669082
  24. Adaptation of core mechanisms to generate cell polarity.
    Nature. 2003 Apr 17;422(6933):766-74 PMID: 12700771
  25. A dual mechanism controlling the localization and function of exocytic v-SNAREs.
    Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):9011-6 PMID: 12853575
  26. Signals for sorting of transmembrane proteins to endosomes and lysosomes.
    Annu Rev Biochem. 2003;72:395-447 PMID: 12651740
  27. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection.
    J Cell Biol. 2003 Oct 27;163(2):203-8 PMID: 14581447
  28. The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells.
    J Cell Biol. 2003 Oct 27;163(2):339-50 PMID: 14581456
  29. The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains.
    J Cell Biol. 2003 Oct 27;163(2):351-62 PMID: 14581457
  30. The mechanisms of vesicle budding and fusion.
    Cell. 2004 Jan 23;116(2):153-66 PMID: 14744428
  31. Adaptor protein complexes as the key regulators of protein sorting in the post-Golgi network.
    Cell Struct Funct. 2003 Oct;28(5):419-29 PMID: 14745134
  32. Specific interaction between SNAREs and epsin N-terminal homology (ENTH) domains of epsin-related proteins in trans-Golgi network to endosome transport.
    J Biol Chem. 2004 Feb 6;279(6):4175-9 PMID: 14630930
  33. Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants.
    Cell. 1992 Nov 27;71(5):741-53 PMID: 1423629
  34. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin.
    Nature. 1992 Oct 29;359(6398):832-5 PMID: 1331807
  35. Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon a tyrosine.
    J Biol Chem. 1993 Feb 15;268(5):3313-20 PMID: 8381425
  36. TGN38 is maintained in the trans-Golgi network by a tyrosine-containing motif in the cytoplasmic domain.
    EMBO J. 1993 May;12(5):2219-28 PMID: 8491209
  37. Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein.
    Nature. 1993 Jul 22;364(6435):346-9 PMID: 8332193
  38. Cleavage of members of the synaptobrevin/VAMP family by types D and F botulinal neurotoxins and tetanus toxin.
    J Biol Chem. 1994 Apr 29;269(17):12764-72 PMID: 8175689
  39. Expression of the synaptic vesicle proteins VAMPs/synaptobrevins 1 and 2 in non-neural tissues.
    J Biol Chem. 1994 Jun 3;269(22):15403-6 PMID: 8195178
  40. Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells.
    J Cell Biol. 1994 Jun;125(5):1015-24 PMID: 8195285
  41. Structural requirements and sequence motifs for polarized sorting and endocytosis of LDL and Fc receptors in MDCK cells.
    J Cell Biol. 1994 Aug;126(4):991-1004 PMID: 8051216
  42. Different requirements for NSF, SNAP, and Rab proteins in apical and basolateral transport in MDCK cells.
    Cell. 1995 May 19;81(4):571-80 PMID: 7758111
  43. VAMP/synaptobrevin isoforms 1 and 2 are widely and differentially expressed in nonneuronal tissues.
    J Cell Biol. 1996 Jan;132(1-2):167-79 PMID: 8567721
  44. Identification of a novel syntaxin- and synaptobrevin/VAMP-binding protein, SNAP-23, expressed in non-neuronal tissues.
    J Biol Chem. 1996 Jun 7;271(23):13300-3 PMID: 8663154
  45. Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9559-64 PMID: 8790369
  46. Differential localization of syntaxin isoforms in polarized Madin-Darby canine kidney cells.
    Mol Biol Cell. 1996 Dec;7(12):2007-18 PMID: 8970161
  47. Mutational analysis of VAMP domains implicated in Ca2+-induced insulin exocytosis.
    EMBO J. 1996 Dec 16;15(24):6951-9 PMID: 9003771
  48. Structural requirements for basolateral sorting of the human transferrin receptor in the biosynthetic and endocytic pathways of Madin-Darby canine kidney cells.
    J Cell Biol. 1997 Jun 16;137(6):1255-64 PMID: 9182660
  49. A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells.
    Mol Biol Cell. 1998 Jun;9(6):1437-48 PMID: 9614185
  50. Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells.
    Cell. 1998 May 29;93(5):731-40 PMID: 9630218
  51. The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells.
    J Cell Biol. 1998 Jun 29;141(7):1503-13 PMID: 9647644
  52. Tyrosine-based membrane protein sorting signals are differentially interpreted by polarized Madin-Darby canine kidney and LLC-PK1 epithelial cells.
    J Biol Chem. 1998 Oct 9;273(41):26862-9 PMID: 9756932
  53. Dual-color visualization of trans-Golgi network to plasma membrane traffic along microtubules in living cells.
    J Cell Sci. 1999 Jan;112 ( Pt 1):21-33 PMID: 9841901
  54. Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3734-8 PMID: 10097106
  55. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells.
    J Cell Biol. 2004 Nov 8;167(3):531-43 PMID: 15534004
  56. EpsinR is an adaptor for the SNARE protein Vti1b.
    Mol Biol Cell. 2004 Dec;15(12):5593-602 PMID: 15371541
  57. Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane.
    J Cell Sci. 2004 Dec 1;117(Pt 25):5955-64 PMID: 15564373
  58. Tetanus neurotoxin-mediated cleavage of cellubrevin impairs epithelial cell migration and integrin-dependent cell adhesion.
    Proc Natl Acad Sci U S A. 2005 May 3;102(18):6362-7 PMID: 15851685
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2007-05-07
Pages
477-88
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2034334
Subset
IM
Grants
NIGMS NIH HHS · R01 GM070736 · United States
NIGMS NIH HHS · T32 GM008061 · United States
NIGMS NIH HHS · GM070736 · United States
NIGMS NIH HHS · GM8061 · United States
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