Home LiteratureArticle Details
PMID: 14709721 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Mechanism of recruiting Sec6/8 (exocyst) complex to the apical junctional complex during polarization of epithelial cells.

Journal of cell science ·Vol. 117 ·No. Pt 4 ·2004-02-01 ·Pages 559-70

Yeaman C, Grindstaff KK, Nelson WJ

Abstract

Sec6/8 (exocyst) complex regulates vesicle delivery and polarized membrane growth in a variety of cells, but mechanisms regulating Sec6/8 localization are unknown. In epithelial cells, Sec6/8 complex is recruited to cell-cell contacts with a mixture of junctional proteins, but then sorts out to the apex of the lateral membrane with components of tight junction and nectin complexes. Sec6/8 complex fractionates in a high molecular mass complex with tight junction proteins and a portion of E-cadherin, and co-immunoprecipitates with cell surface-labeled E-cadherin and nectin-2alpha. Recruitment of Sec6/8 complex to cell-cell contacts can be achieved in fibroblasts when E-cadherin and nectin-2alpha are co-expressed. These results support a model in which localized recruitment of Sec6/8 complex to the plasma membrane by specific cell-cell adhesion complexes defines a site for vesicle delivery and polarized membrane growth during development of epithelial cell polarity.

MeSH Terms
Animals Carrier Proteins/metabolism Cell Adhesion/physiology Cell Adhesion Molecules/isolation & purification,physiology Cell Line Cell Polarity/physiology Dogs Epithelial Cells/physiology Intracellular Membranes/physiology Kidney/cytology Macromolecular Substances
Chemicals
Carrier Proteins Cell Adhesion Molecules Macromolecular Substances
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Yeaman Charles
Department of Molecular and Cellular Physiology, Beckman Center for Molecular and Genetic Medicine, Stanford University School of Medicine, Stanford, CA 94305-5345, USA. [email protected]
Grindstaff Kent K
Nelson W James
References (65)
65 references, click to expand
  1. Nectin/PRR: an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein.
    J Cell Biol. 1999 May 3;145(3):539-49 PMID: 10225955
  2. Yeast homologues of tomosyn and lethal giant larvae function in exocytosis and are associated with the plasma membrane SNARE, Sec9.
    J Cell Biol. 1999 Jul 12;146(1):125-40 PMID: 10402465
  3. Sec1p binds to SNARE complexes and concentrates at sites of secretion.
    J Cell Biol. 1999 Jul 26;146(2):333-44 PMID: 10427089
  4. Neuronal polarity: controlling the sorting and diffusion of membrane components.
    Neuron. 1999 Aug;23(4):637-40 PMID: 10482229
  5. VAP-33 localizes to both an intracellular vesicle population and with occludin at the tight junction.
    J Cell Sci. 1999 Nov;112 ( Pt 21):3723-32 PMID: 10523508
  6. Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein.
    Nat Cell Biol. 2000 Feb;2(2):125-7 PMID: 10655593
  7. Membrane fusion and exocytosis.
    Annu Rev Biochem. 1999;68:863-911 PMID: 10872468
  8. Membrane traffic in polarized epithelial cells.
    Curr Opin Cell Biol. 2000 Aug;12(4):483-90 PMID: 10873817
  9. Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo.
    J Cell Biol. 2000 Aug 21;150(4):849-60 PMID: 10953008
  10. The mammalian Sec6/8 complex interacts with Ca(2+) signaling complexes and regulates their activity.
    J Cell Biol. 2000 Sep 4;150(5):1101-12 PMID: 10973998
  11. Two cell adhesion molecules, nectin and cadherin, interact through their cytoplasmic domain-associated proteins.
    J Cell Biol. 2000 Sep 4;150(5):1161-76 PMID: 10974003
  12. Exocyst is involved in cystogenesis and tubulogenesis and acts by modulating synthesis and delivery of basolateral plasma membrane and secretory proteins.
    Mol Biol Cell. 2000 Dec;11(12):4259-75 PMID: 11102522
  13. Spatial regulation of the exocyst complex by Rho1 GTPase.
    Nat Cell Biol. 2001 Apr;3(4):353-60 PMID: 11283608
  14. The exocyst complex associates with microtubules to mediate vesicle targeting and neurite outgrowth.
    J Neurosci. 2001 Jun 1;21(11):3839-48 PMID: 11356872
  15. The brain exocyst complex interacts with RalA in a GTP-dependent manner: identification of a novel mammalian Sec3 gene and a second Sec15 gene.
    J Biol Chem. 2001 Aug 10;276(32):29792-7 PMID: 11406615
  16. The Sec6/8 complex in mammalian cells: characterization of mammalian Sec3, subunit interactions, and expression of subunits in polarized cells.
    Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9648-53 PMID: 11493706
  17. Sec6/8 complexes on trans-Golgi network and plasma membrane regulate late stages of exocytosis in mammalian cells.
    J Cell Biol. 2001 Nov 12;155(4):593-604 PMID: 11696560
  18. Cdc42 interacts with the exocyst and regulates polarized secretion.
    J Biol Chem. 2001 Dec 14;276(50):46745-50 PMID: 11595741
  19. Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast.
    Mol Biol Cell. 2001 Dec;12(12):4129-38 PMID: 11739806
  20. The exocyst is a Ral effector complex.
    Nat Cell Biol. 2002 Jan;4(1):66-72 PMID: 11740492
  21. The exocyst complex binds the small GTPase RalA to mediate filopodia formation.
    Nat Cell Biol. 2002 Jan;4(1):73-8 PMID: 11744922
  22. Mammalian homolog of Drosophila tumor suppressor lethal (2) giant larvae interacts with basolateral exocytic machinery in Madin-Darby canine kidney cells.
    Mol Biol Cell. 2002 Jan;13(1):158-68 PMID: 11809830
  23. Biochemical and structural definition of the l-afadin- and actin-binding sites of alpha-catenin.
    J Biol Chem. 2002 May 24;277(21):18868-74 PMID: 11907041
  24. aPKC kinase activity is required for the asymmetric differentiation of the premature junctional complex during epithelial cell polarization.
    J Cell Sci. 2002 Sep 15;115(Pt 18):3565-73 PMID: 12186943
  25. 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
  26. Regulating the actin cytoskeleton during vesicular transport.
    Curr Opin Cell Biol. 2002 Aug;14(4):428-33 PMID: 12383793
  27. Three-dimensional analysis of post-Golgi carrier exocytosis in epithelial cells.
    Nat Cell Biol. 2003 Feb;5(2):126-36 PMID: 12545172
  28. The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin.
    Nature. 2003 Apr 10;422(6932):629-33 PMID: 12687004
  29. Ultracentrifugation-based approaches to study regulation of Sec6/8 (exocyst) complex function during development of epithelial cell polarity.
    Methods. 2003 Jul;30(3):198-206 PMID: 12798134
  30. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  31. Apical membrane aminopeptidase appears at site of cell-cell contact in cultured kidney epithelial cells.
    Proc Natl Acad Sci U S A. 1980 Jul;77(7):4132-6 PMID: 6933462
  32. Formation of the apical pole of epithelial (Madin-Darby canine kidney) cells: polarity of an apical protein is independent of tight junctions while segregation of a basolateral marker requires cell-cell interactions.
    J Cell Biol. 1987 Apr;104(4):905-16 PMID: 3558485
  33. Ankyrin binding to (Na+ + K+)ATPase and implications for the organization of membrane domains in polarized cells.
    Nature. 1987 Aug 6-12;328(6130):533-6 PMID: 3039371
  34. Experimentally induced alteration in the polarity of developing neurons.
    Nature. 1987 Nov 19-25;330(6145):254-6 PMID: 3313064
  35. Kinetics of desmosome assembly in Madin-Darby canine kidney epithelial cells: temporal and spatial regulation of desmoplakin organization and stabilization upon cell-cell contact. I. Biochemical analysis.
    J Cell Biol. 1988 Mar;106(3):677-85 PMID: 3346322
  36. Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH.
    J Cell Biol. 1989 Mar;108(3):855-64 PMID: 2921284
  37. Biogenetic pathways of plasma membrane proteins in Caco-2, a human intestinal epithelial cell line.
    J Cell Biol. 1990 Oct;111(4):1351-61 PMID: 1976637
  38. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane.
    J Cell Biol. 1993 Oct;123(1):35-45 PMID: 8408203
  39. A small rab GTPase is distributed in cytoplasmic vesicles in non polarized cells but colocalizes with the tight junction marker ZO-1 in polarized epithelial cells.
    J Cell Biol. 1994 Jan;124(1-2):101-15 PMID: 8294494
  40. Expression and polarized targeting of a rab3 isoform in epithelial cells.
    J Cell Biol. 1994 May;125(3):583-94 PMID: 8175882
  41. Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly.
    J Cell Biol. 1994 Jun;125(6):1327-40 PMID: 8207061
  42. Implications of the SNARE hypothesis for intracellular membrane topology and dynamics.
    Curr Biol. 1994 Mar 1;4(3):220-33 PMID: 7922327
  43. Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis.
    Cell. 1994 Oct 21;79(2):245-58 PMID: 7954793
  44. 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
  45. Preferential addition of newly synthesized membrane protein at axonal growth cones.
    Nature. 1995 Jun 15;375(6532):592-4 PMID: 7791876
  46. Epidermal growth factor induces tyrosine phosphorylation and reorganization of the tight junction protein ZO-1 in A431 cells.
    J Cell Sci. 1995 Apr;108 ( Pt 4):1735-42 PMID: 7542259
  47. Mechanism for transition from initial to stable cell-cell adhesion: kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay.
    J Cell Biol. 1996 Jul;134(2):549-57 PMID: 8707837
  48. Differential localization of syntaxin isoforms in polarized Madin-Darby canine kidney cells.
    Mol Biol Cell. 1996 Dec;7(12):2007-18 PMID: 8970161
  49. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae.
    EMBO J. 1996 Dec 2;15(23):6483-94 PMID: 8978675
  50. The mammalian brain rsec6/8 complex.
    Neuron. 1996 Dec;17(6):1209-19 PMID: 8982167
  51. Mouse homolog of poliovirus receptor-related gene 2 product, mPRR2, mediates homophilic cell aggregation.
    Exp Cell Res. 1997 Sep 15;235(2):374-84 PMID: 9299162
  52. Afadin: A novel actin filament-binding protein with one PDZ domain localized at cadherin-based cell-to-cell adherens junction.
    J Cell Biol. 1997 Oct 20;139(2):517-28 PMID: 9334353
  53. The Ras target AF-6 interacts with ZO-1 and serves as a peripheral component of tight junctions in epithelial cells.
    J Cell Biol. 1997 Nov 3;139(3):785-95 PMID: 9348294
  54. Post-Golgi biosynthetic trafficking.
    J Cell Sci. 1997 Dec;110 ( Pt 24):3001-9 PMID: 9365270
  55. Identification of four distinct pools of catenins in mammalian cells and transformation-dependent changes in catenin distributions among these pools.
    J Biol Chem. 1997 Nov 21;272(47):29652-62 PMID: 9368032
  56. Subunit structure of the mammalian exocyst complex.
    Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14438-43 PMID: 9405631
  57. The secretory protein Sec8 is required for paraxial mesoderm formation in the mouse.
    Dev Biol. 1997 Dec 15;192(2):364-74 PMID: 9441674
  58. A role for CAP, a novel, multifunctional Src homology 3 domain-containing protein in formation of actin stress fibers and focal adhesions.
    J Biol Chem. 1998 Feb 13;273(7):4073-80 PMID: 9461600
  59. Sec3p is a spatial landmark for polarized secretion in budding yeast.
    Cell. 1998 Feb 20;92(4):559-71 PMID: 9491896
  60. Apiconuclear organization of microtubules does not specify protein delivery from the trans-Golgi network to different membrane domains in polarized epithelial cells.
    Mol Biol Cell. 1998 Mar;9(3):685-99 PMID: 9487135
  61. 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
  62. Subunit composition, protein interactions, and structures of the mammalian brain sec6/8 complex and septin filaments.
    Neuron. 1998 Jun;20(6):1111-22 PMID: 9655500
  63. Spatial regulation of exocytosis: lessons from yeast.
    J Cell Biol. 1998 Aug 10;142(3):609-12 PMID: 9700152
  64. The sec6/8 complex is located at neurite outgrowth and axonal synapse-assembly domains.
    J Neurosci. 1999 Feb 15;19(4):1324-34 PMID: 9952410
  65. Differential behavior of E-cadherin and occludin in their colocalization with ZO-1 during the establishment of epithelial cell polarity.
    J Cell Physiol. 1999 May;179(2):115-25 PMID: 10199550
Article Info
Journal
Journal of cell science
Abbr.
J Cell Sci
ISSN
0021-9533
Published
2004-02-01
Epub
2004-00-06
Pages
559-70
Language
English
Region
England
NLM ID
0052457
PMCID
PMC3368615
Subset
IM
Grants
NIGMS NIH HHS · R01 GM035527 · United States
NIGMS NIH HHS · GM35227 · United States
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: [email protected]