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PMID: 18987335 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

LIM kinase 1 and cofilin regulate actin filament population required for dynamin-dependent apical carrier fission from the trans-Golgi network.

Molecular biology of the cell ·Vol. 20 ·No. 1 ·2009-01-00 ·Pages 438-51

Salvarezza SB, Deborde S, Schreiner R, Campagne F, Kessels MM, Qualmann B, Caceres A, Kreitzer G, Rodriguez-Boulan E

Abstract

The functions of the actin cytoskeleton in post-Golgi trafficking are still poorly understood. Here, we report the role of LIM Kinase 1 (LIMK1) and its substrate cofilin in the trafficking of apical and basolateral proteins in Madin-Darby canine kidney cells. Our data indicate that LIMK1 and cofilin organize a specialized population of actin filaments at the Golgi complex that is selectively required for the emergence of an apical cargo route to the plasma membrane (PM). Quantitative pulse-chase live imaging experiments showed that overexpression of kinase-dead LIMK1 (LIMK1-KD), or of LIMK1 small interfering RNA, or of an activated cofilin mutant (cofilin S3A), selectively slowed down the exit from the trans-Golgi network (TGN) of the apical PM marker p75-green fluorescent protein (GFP) but did not interfere with the apical PM marker glycosyl phosphatidylinositol-YFP or the basolateral PM marker neural cell adhesion molecule-GFP. High-resolution live imaging experiments of carrier formation and release by the TGN and analysis of peri-Golgi actin dynamics using photoactivatable GFP suggest a scenario in which TGN-localized LIMK1-cofilin regulate a population of actin filaments required for dynamin-syndapin-cortactin-dependent generation and/or fission of precursors to p75 transporters.

MeSH Terms
Actin Depolymerizing Factors/genetics,metabolism Actins/metabolism Animals Biomarkers/metabolism Cell Line Cell Polarity Cytoskeleton/metabolism Dogs Dynamins/genetics,metabolism Golgi Apparatus/metabolism Isoenzymes/genetics,metabolism Lim Kinases/genetics,metabolism Models, Biological Neural Cell Adhesion Molecules/genetics,metabolism Protein Transport/physiology RNA, Small Interfering/genetics,metabolism Receptor, Nerve Growth Factor/genetics,metabolism Recombinant Fusion Proteins/genetics,metabolism trans-Golgi Network/metabolism
Chemicals
Actin Depolymerizing Factors Actins Biomarkers Isoenzymes Neural Cell Adhesion Molecules RNA, Small Interfering Receptor, Nerve Growth Factor Recombinant Fusion Proteins Lim Kinases Dynamins
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Salvarezza Susana B
Margaret Dyson Vision Research Institute and Department of Cell and Developmental Biology, HRH Prince Alwaleed Bin Talal Bin Abdulaziz Alsaud Institute for Computational Biomedicine, Weill Medical College of Cornell University, New York, NY 10065, USA.
Deborde Sylvie
Schreiner Ryan
Campagne Fabien
Kessels Michael M
Qualmann Britta
Caceres Alfredo
Kreitzer Geri
Rodriguez-Boulan Enrique
References (69)
69 references, click to expand
  1. Key components of the fission machinery are interchangeable.
    Nat Cell Biol. 2006 Dec;8(12):1376-82 PMID: 17086176
  2. 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
  3. Apical sorting by galectin-3-dependent glycoprotein clustering.
    Traffic. 2007 Apr;8(4):379-88 PMID: 17319896
  4. Lim kinases, regulators of actin dynamics.
    Int J Biochem Cell Biol. 2007;39(6):1071-6 PMID: 17188549
  5. Variable actin dynamics requirement for the exit of different cargo from the trans-Golgi network.
    FEBS Lett. 2007 Aug 7;581(20):3875-81 PMID: 17651738
  6. Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state.
    J Cell Biol. 2007 Sep 24;178(7):1251-64 PMID: 17875745
  7. Polarization-dependent selective transport to the apical membrane by KIF5B in MDCK cells.
    Dev Cell. 2007 Oct;13(4):511-22 PMID: 17925227
  8. Antibody to AP1B adaptor blocks biosynthetic and recycling routes of basolateral proteins at recycling endosomes.
    Mol Biol Cell. 2007 Dec;18(12):4872-84 PMID: 17881725
  9. Clathrin is a key regulator of basolateral polarity.
    Nature. 2008 Apr 10;452(7188):719-23 PMID: 18401403
  10. Isoform and splice-variant specific functions of dynamin-2 revealed by analysis of conditional knock-out cells.
    Mol Biol Cell. 2008 Dec;19(12):5347-59 PMID: 18923138
  11. Cytoskeletal changes regulated by the PAK4 serine/threonine kinase are mediated by LIM kinase 1 and cofilin.
    J Biol Chem. 2001 Aug 24;276(34):32115-21 PMID: 11413130
  12. KIFC3, a microtubule minus end-directed motor for the apical transport of annexin XIIIb-associated Triton-insoluble membranes.
    J Cell Biol. 2001 Oct 1;155(1):77-88 PMID: 11581287
  13. Regulation of protein transport from the Golgi complex to the endoplasmic reticulum by CDC42 and N-WASP.
    Mol Biol Cell. 2002 Mar;13(3):866-79 PMID: 11907268
  14. A photoactivatable GFP for selective photolabeling of proteins and cells.
    Science. 2002 Sep 13;297(5588):1873-7 PMID: 12228718
  15. Motoring around the Golgi.
    Nat Cell Biol. 2002 Oct;4(10):E236-42 PMID: 12360306
  16. Regulating the actin cytoskeleton during vesicular transport.
    Curr Opin Cell Biol. 2002 Aug;14(4):428-33 PMID: 12383793
  17. Three-dimensional analysis of post-Golgi carrier exocytosis in epithelial cells.
    Nat Cell Biol. 2003 Feb;5(2):126-36 PMID: 12545172
  18. Cortactin is a component of clathrin-coated pits and participates in receptor-mediated endocytosis.
    Mol Cell Biol. 2003 Mar;23(6):2162-70 PMID: 12612086
  19. Regulated portals of entry into the cell.
    Nature. 2003 Mar 6;422(6927):37-44 PMID: 12621426
  20. Signals for sorting of transmembrane proteins to endosomes and lysosomes.
    Annu Rev Biochem. 2003;72:395-447 PMID: 12651740
  21. Microtubule organization and function in epithelial cells.
    Traffic. 2004 Jan;5(1):1-9 PMID: 14675420
  22. Targeting of a tropomyosin isoform to short microfilaments associated with the Golgi complex.
    Mol Biol Cell. 2004 Jan;15(1):268-80 PMID: 14528022
  23. LIM kinase 1, a key regulator of actin dynamics, is widely expressed in embryonic and adult tissues.
    Exp Cell Res. 2004 Apr 1;294(2):392-405 PMID: 15023529
  24. A novel p75 neurotrophin receptor-related protein, NRH2, regulates nerve growth factor binding to the TrkA receptor.
    J Neurosci. 2004 Mar 17;24(11):2742-9 PMID: 15028767
  25. Cofilin promotes actin polymerization and defines the direction of cell motility.
    Science. 2004 Apr 30;304(5671):743-6 PMID: 15118165
  26. Caspase-mediated cleavage and activation of LIM-kinase 1 and its role in apoptotic membrane blebbing.
    Genes Cells. 2004 Jun;9(6):591-600 PMID: 15189451
  27. Actin dynamics coupled to clathrin-coated vesicle formation at the trans-Golgi network.
    J Cell Biol. 2004 Jun 21;165(6):781-8 PMID: 15210728
  28. LIMK1 regulates Golgi dynamics, traffic of Golgi-derived vesicles, and process extension in primary cultured neurons.
    Mol Biol Cell. 2004 Jul;15(7):3433-49 PMID: 15090620
  29. Dynamin GTPase domain mutants that differentially affect GTP binding, GTP hydrolysis, and clathrin-mediated endocytosis.
    J Biol Chem. 2004 Sep 24;279(39):40431-6 PMID: 15262989
  30. Association of Cdc42/N-WASP/Arp2/3 signaling pathway with Golgi membranes.
    Traffic. 2004 Nov;5(11):838-46 PMID: 15479449
  31. Mobility of microinjected rhodamine actin within living chicken gizzard cells determined by fluorescence photobleaching recovery.
    Cell. 1982 Jul;29(3):835-45 PMID: 6891291
  32. N-glycans as apical sorting signals in epithelial cells.
    Nature. 1995 Nov 2;378(6552):96-8 PMID: 7477300
  33. Mammalian Cdc42 is a brefeldin A-sensitive component of the Golgi apparatus.
    J Biol Chem. 1996 Oct 25;271(43):26850-4 PMID: 8900167
  34. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility.
    J Cell Biol. 1997 Mar 24;136(6):1307-22 PMID: 9087445
  35. Cdc42 controls secretory and endocytic transport to the basolateral plasma membrane of MDCK cells.
    Nat Cell Biol. 1999 May;1(1):8-13 PMID: 10559857
  36. Proteins of the ADF/cofilin family: essential regulators of actin dynamics.
    Annu Rev Cell Dev Biol. 1999;15:185-230 PMID: 10611961
  37. Cofilin phosphorylation and actin cytoskeletal dynamics regulated by rho- and Cdc42-activated LIM-kinase 2.
    J Cell Biol. 1999 Dec 27;147(7):1519-32 PMID: 10613909
  38. 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
  39. Syndapin isoforms participate in receptor-mediated endocytosis and actin organization.
    J Cell Biol. 2000 Mar 6;148(5):1047-62 PMID: 10704453
  40. Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3.
    Curr Biol. 2000 Mar 23;10(6):311-20 PMID: 10744973
  41. Disruption of Golgi structure and function in mammalian cells expressing a mutant dynamin.
    J Cell Sci. 2000 Jun;113 ( Pt 11):1993-2002 PMID: 10806110
  42. Molecular links between endocytosis and the actin cytoskeleton.
    J Cell Biol. 2000 Sep 4;150(5):F111-6 PMID: 10974009
  43. cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network.
    EMBO J. 2001 May 1;20(9):2171-9 PMID: 11331583
  44. Cytoplasmic dynein regulation by subunit heterogeneity and its role in apical transport.
    J Cell Biol. 2001 Jun 25;153(7):1499-509 PMID: 11425878
  45. Functional rafts in cell membranes.
    Nature. 1997 Jun 5;387(6633):569-72 PMID: 9177342
  46. Cofilin promotes rapid actin filament turnover in vivo.
    Nature. 1997 Jul 3;388(6637):78-82 PMID: 9214506
  47. The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells.
    J Cell Biol. 1997 Nov 17;139(4):929-40 PMID: 9362511
  48. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase.
    Nature. 1998 Jun 25;393(6687):805-9 PMID: 9655397
  49. PAK4, a novel effector for Cdc42Hs, is implicated in the reorganization of the actin cytoskeleton and in the formation of filopodia.
    EMBO J. 1998 Nov 16;17(22):6527-40 PMID: 9822598
  50. Measuring actin dynamics in endothelial cells.
    Microsc Res Tech. 1998 Dec 1;43(5):385-94 PMID: 9858336
  51. New anti-actin drugs in the study of the organization and function of the actin cytoskeleton.
    Microsc Res Tech. 1999 Oct 1;47(1):18-37 PMID: 10506759
  52. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis.
    Mol Biol Cell. 2005 Feb;16(2):964-75 PMID: 15601897
  53. Organization of vesicular trafficking in epithelia.
    Nat Rev Mol Cell Biol. 2005 Mar;6(3):233-47 PMID: 15738988
  54. Actin and Arf1-dependent recruitment of a cortactin-dynamin complex to the Golgi regulates post-Golgi transport.
    Nat Cell Biol. 2005 May;7(5):483-92 PMID: 15821732
  55. Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells.
    J Cell Biol. 2005 May 9;169(3):491-501 PMID: 15883199
  56. Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells.
    Cell. 2005 May 20;121(4):593-606 PMID: 15907472
  57. CtBP3/BARS drives membrane fission in dynamin-independent transport pathways.
    Nat Cell Biol. 2005 Jun;7(6):570-80 PMID: 15880102
  58. LIM kinase 1 coordinates microtubule stability and actin polymerization in human endothelial cells.
    J Biol Chem. 2005 Jul 15;280(28):26533-42 PMID: 15897190
  59. Evolving endosomes: how many varieties and why?
    Curr Opin Cell Biol. 2005 Aug;17(4):423-34 PMID: 15975780
  60. A modular design for the clathrin- and actin-mediated endocytosis machinery.
    Cell. 2005 Oct 21;123(2):305-20 PMID: 16239147
  61. Deconstructing the cadherin-catenin-actin complex.
    Cell. 2005 Dec 2;123(5):889-901 PMID: 16325582
  62. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins.
    Dev Cell. 2005 Dec;9(6):791-804 PMID: 16326391
  63. Requirement for galectin-3 in apical protein sorting.
    Curr Biol. 2006 Feb 21;16(4):408-14 PMID: 16488876
  64. Par-3 mediates the inhibition of LIM kinase 2 to regulate cofilin phosphorylation and tight junction assembly.
    J Cell Biol. 2006 Feb 27;172(5):671-8 PMID: 16505165
  65. Actin dynamics at the Golgi complex in mammalian cells.
    Curr Opin Cell Biol. 2006 Apr;18(2):168-78 PMID: 16488588
  66. Complexes of syndapin II with dynamin II promote vesicle formation at the trans-Golgi network.
    J Cell Sci. 2006 Apr 15;119(Pt 8):1504-16 PMID: 16551695
  67. LIM kinase 2 is widely expressed in all tissues.
    J Histochem Cytochem. 2006 May;54(5):487-501 PMID: 16399995
  68. Phosphatidylinositol 5-kinase stimulates apical biosynthetic delivery via an Arp2/3-dependent mechanism.
    J Biol Chem. 2006 Jun 2;281(22):15376-84 PMID: 16601114
  69. Vesicle formation at the plasma membrane and trans-Golgi network: the same but different.
    Science. 2006 Sep 15;313(5793):1591-4 PMID: 16973870
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
DOI
10.1091/mbc.e08-08-0891
Published
2009-01-00
Epub
2008-00-05
Pages
438-51
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC2613098
Subset
IM
Grants
NEI NIH HHS · R01 EY008538 · United States
NIGMS NIH HHS · R01 GM034107 · United States
NEI NIH HHS · EY-08538 · United States
NIGMS NIH HHS · GM-34107 · United States
External Links
PubMed source DOI: 10.1091/mbc.e08-08-0891 PMC Full Text View journal details
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