Home LiteratureArticle Details
PMID: 20890297 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

A molecular network for de novo generation of the apical surface and lumen.

Nature cell biology ·Vol. 12 ·No. 11 ·2010-11-00 ·Pages 1035-45

Bryant DM, Datta A, Rodríguez-Fraticelli AE, Peränen J, Martín-Belmonte F, Mostov KE

Abstract

To form epithelial organs cells must polarize and generate de novo an apical domain and lumen. Epithelial polarization is regulated by polarity complexes that are hypothesized to direct downstream events, such as polarized membrane traffic, although this interconnection is not well understood. We have found that Rab11a regulates apical traffic and lumen formation through the Rab guanine nucleotide exchange factor (GEF), Rabin8, and its target, Rab8a. Rab8a and Rab11a function through the exocyst to target Par3 to the apical surface, and control apical Cdc42 activation through the Cdc42 GEF, Tuba. These components assemble at a transient apical membrane initiation site to form the lumen. This Rab11a-directed network directs Cdc42-dependent apical exocytosis during lumen formation, revealing an interaction between the machineries of vesicular transport and polarization.

MeSH Terms
Animals Annexin A2/metabolism Cell Membrane/metabolism Cell Polarity/physiology Dogs Epithelial Cells/cytology,metabolism Germinal Center Kinases Models, Biological Morphogenesis Protein Serine-Threonine Kinases/metabolism cdc42 GTP-Binding Protein/metabolism rab GTP-Binding Proteins/metabolism
Chemicals
Annexin A2 Germinal Center Kinases Protein Serine-Threonine Kinases rab11 protein cdc42 GTP-Binding Protein rab GTP-Binding Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Bryant David M
Department of Anatomy, University of California, San Francisco, CA 94143-2140, USA.
Datta Anirban
Rodríguez-Fraticelli Alejo E
Peränen Johan
Martín-Belmonte Fernando
Mostov Keith E
References (53)
53 references, click to expand
  1. Cdc42 and vesicle trafficking in polarized cells.
    Traffic. 2010 Oct;11(10):1272-9 PMID: 20633244
  2. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis.
    J Cell Biol. 2008 Nov 17;183(4):625-33 PMID: 19001128
  3. Formation of cysts by alveolar type II cells in three-dimensional culture reveals a novel mechanism for epithelial morphogenesis.
    Mol Biol Cell. 2007 May;18(5):1693-700 PMID: 17332496
  4. The PAR proteins: fundamental players in animal cell polarization.
    Dev Cell. 2007 Nov;13(5):609-622 PMID: 17981131
  5. Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein block its transport to the cell surface.
    EMBO J. 1986 May;5(5):931-41 PMID: 3013626
  6. Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells.
    J Cell Biol. 2005 Jan 17;168(2):303-13 PMID: 15642748
  7. Coordination of Rab8 and Rab11 in primary ciliogenesis.
    Proc Natl Acad Sci U S A. 2010 Apr 6;107(14):6346-51 PMID: 20308558
  8. The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro.
    Mol Biol Cell. 2009 May;20(10):2522-9 PMID: 19297529
  9. 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
  10. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic.
    Nat Cell Biol. 2007 Sep;9(9):1066-73 PMID: 17704769
  11. ROCK-mediated contractility, tight junctions and channels contribute to the conversion of a preapical patch into apical surface during isochoric lumen initiation.
    J Cell Sci. 2008 Nov 1;121(Pt 21):3649-63 PMID: 18946028
  12. Par3 functions in the biogenesis of the primary cilium in polarized epithelial cells.
    J Cell Biol. 2007 Dec 17;179(6):1133-40 PMID: 18070914
  13. Three-dimensional analysis of post-Golgi carrier exocytosis in epithelial cells.
    Nat Cell Biol. 2003 Feb;5(2):126-36 PMID: 12545172
  14. From cells to organs: building polarized tissue.
    Nat Rev Mol Cell Biol. 2008 Nov;9(11):887-901 PMID: 18946477
  15. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42.
    Nat Cell Biol. 2000 Aug;2(8):531-9 PMID: 10934474
  16. Asymmetric coiled-coil structure with Guanine nucleotide exchange activity.
    Structure. 2007 Feb;15(2):245-52 PMID: 17292842
  17. Rac1 is required for reorientation of polarity and lumen formation through a PI 3-kinase-dependent pathway.
    Am J Physiol Renal Physiol. 2007 Nov;293(5):F1633-40 PMID: 17804488
  18. aPKC phosphorylation of Bazooka defines the apical/lateral border in Drosophila epithelial cells.
    Cell. 2010 Apr 30;141(3):509-23 PMID: 20434988
  19. Definition of distinct compartments in polarized Madin-Darby canine kidney (MDCK) cells for membrane-volume sorting, polarized sorting and apical recycling.
    Traffic. 2000 Feb;1(2):124-40 PMID: 11208093
  20. LGN regulates mitotic spindle orientation during epithelial morphogenesis.
    J Cell Biol. 2010 Apr 19;189(2):275-88 PMID: 20385777
  21. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42.
    Cell. 2007 Jan 26;128(2):383-97 PMID: 17254974
  22. Localization of GFP-tagged concentrative nucleoside transporters in a renal polarized epithelial cell line.
    Am J Physiol Renal Physiol. 2001 May;280(5):F879-85 PMID: 11292631
  23. Membrane traffic in cytokinesis.
    Biochem Soc Trans. 2005 Dec;33(Pt 6):1290-4 PMID: 16246101
  24. Tube morphogenesis: making and shaping biological tubes.
    Cell. 2003 Jan 10;112(1):19-28 PMID: 12526790
  25. Exocytosis of vacuolar apical compartment (VAC) in Madin-Darby canine kidney epithelial cells: cAMP is involved as second messenger.
    Exp Cell Res. 1993 Mar;205(1):171-8 PMID: 7681007
  26. Organogenesis: molecular mechanisms of tubulogenesis.
    Nat Rev Genet. 2002 Jul;3(7):513-23 PMID: 12094229
  27. Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea.
    Nat Cell Biol. 2008 Aug;10(8):964-70 PMID: 18641639
  28. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen.
    Cell. 2006 Mar 24;124(6):1283-98 PMID: 16564017
  29. Functional dissection of Rab GTPases involved in primary cilium formation.
    J Cell Biol. 2007 Jul 30;178(3):363-9 PMID: 17646400
  30. Crumbs/DaPKC-dependent apical exclusion of Bazooka promotes photoreceptor polarity remodeling.
    Curr Biol. 2010 Jun 22;20(12):1065-74 PMID: 20493700
  31. Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast.
    J Cell Biol. 2002 Jun 10;157(6):1005-15 PMID: 12045183
  32. The annexin 2/S100A10 complex controls the distribution of transferrin receptor-containing recycling endosomes.
    Mol Biol Cell. 2003 Dec;14(12):4896-908 PMID: 13679511
  33. Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells.
    Mol Biol Cell. 2007 Oct;18(10):3978-92 PMID: 17686995
  34. Tuba, a Cdc42 GEF, is required for polarized spindle orientation during epithelial cyst formation.
    J Cell Biol. 2010 May 17;189(4):661-9 PMID: 20479467
  35. Annexin 2 has a dual role as regulator and effector of v-Src in cell transformation.
    J Biol Chem. 2009 Apr 10;284(15):10202-10 PMID: 19193640
  36. Genetic control of single lumen formation in the zebrafish gut.
    Nat Cell Biol. 2007 Aug;9(8):954-60 PMID: 17632505
  37. Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis.
    Am J Physiol Cell Physiol. 2008 Aug;295(2):C545-56 PMID: 18579802
  38. RAB-11 permissively regulates spindle alignment by modulating metaphase microtubule dynamics in Caenorhabditis elegans early embryos.
    Mol Biol Cell. 2008 Jun;19(6):2553-65 PMID: 18385514
  39. Rab GTPases as coordinators of vesicle traffic.
    Nat Rev Mol Cell Biol. 2009 Aug;10(8):513-25 PMID: 19603039
  40. 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
  41. A Rab8-specific GDP/GTP exchange factor is involved in actin remodeling and polarized membrane transport.
    Mol Biol Cell. 2002 Sep;13(9):3268-80 PMID: 12221131
  42. Trafficking of Crumbs3 during cytokinesis is crucial for lumen formation.
    Mol Biol Cell. 2009 Nov;20(22):4652-63 PMID: 19776356
  43. The exocyst complex in polarized exocytosis.
    Curr Opin Cell Biol. 2009 Aug;21(4):537-42 PMID: 19473826
  44. Final stages of cytokinesis and midbody ring formation are controlled by BRUCE.
    Cell. 2008 Mar 7;132(5):832-45 PMID: 18329369
  45. Positional cloning of heart and soul reveals multiple roles for PKC lambda in zebrafish organogenesis.
    Curr Biol. 2001 Oct 2;11(19):1492-502 PMID: 11591316
  46. The Cdc42 GEF Intersectin 2 controls mitotic spindle orientation to form the lumen during epithelial morphogenesis.
    J Cell Biol. 2010 May 17;189(4):725-38 PMID: 20479469
  47. RalA and the exocyst complex influence neuronal polarity through PAR-3 and aPKC.
    J Cell Sci. 2009 May 15;122(Pt 10):1499-506 PMID: 19383721
  48. Determinants of apical membrane formation and distribution in multicellular epithelial MDCK cysts.
    Am J Physiol. 1994 Aug;267(2 Pt 1):C473-81 PMID: 8074182
  49. Polarity and endocytosis: reciprocal regulation.
    Trends Cell Biol. 2010 Aug;20(8):445-52 PMID: 20493706
  50. Liver progenitor cells fold up a cell monolayer into a double-layered structure during tubular morphogenesis.
    Mol Biol Cell. 2009 May;20(9):2486-94 PMID: 19297530
  51. A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11400-6 PMID: 8876147
  52. Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo.
    Nat Struct Mol Biol. 2005 Oct;12(10):879-85 PMID: 16155582
  53. Generation of single and double knockdowns in polarized epithelial cells by retrovirus-mediated RNA interference.
    Proc Natl Acad Sci U S A. 2004 Apr 6;101(14):4912-7 PMID: 15051873
Article Info
Journal
Nature cell biology
Abbr.
Nat Cell Biol
ISSN
1476-4679
DOI
10.1038/ncb2106
Published
2010-11-00
Epub
2010-00-03
Pages
1035-45
Language
English
Region
England
NLM ID
100890575
PMCID
PMC2975675
Subset
IM
Grants
NIAID NIH HHS · P01AI53194 · United States
NIDDK NIH HHS · R01 DK074398-04 · United States
NIAID NIH HHS · P01 AI053194 · United States
NIDDK NIH HHS · R01DK074398 · United States
NIAID NIH HHS · R01AI25144 · United States
NIAID NIH HHS · R01 AI025144 · United States
NIDDK NIH HHS · R01 DK067153 · United States
NIDDK NIH HHS · R01 DK067153-05 · United States
NIDDK NIH HHS · R01 DK074398 · United States
Corrections
CommentIn
PMID: 21045801
CommentIn
PMID: 25373773
External Links
PubMed source DOI: 10.1038/ncb2106 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: [email protected]

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