Home LiteratureArticle Details
PMID: 16870700 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Novel function of clathrin light chain in promoting endocytic vesicle formation.

Molecular biology of the cell ·Vol. 17 ·No. 10 ·2006-10-00 ·Pages 4343-52

Newpher TM, Idrissi FZ, Geli MI, Lemmon SK

Abstract

Clathrin-mediated endocytosis is a major pathway for uptake of lipid and protein cargo at the plasma membrane. The lattices of clathrin-coated pits and vesicles are comprised of triskelions, each consisting of three oligomerized heavy chains (HC) bound by a light chain (LC). In addition to binding HC, LC interacts with members of the Hip1/R family of endocytic proteins, including the budding yeast homologue, Sla2p. Here, using in vivo analysis in yeast, we provide novel insight into the role of this interaction. We find that overexpression of LC partially restores endocytosis to cells lacking clathrin HC. This suppression is dependent on the Sla2p binding region of LC. Using live cell imaging techniques to visualize endocytic vesicle formation, we find that the N-terminal Sla2p binding region of LC promotes the progression of arrested Sla2p patches that form in the absence of HC. We propose that LC binding to Sla2p positively regulates Sla2p for efficient endocytic vesicle formation.

MeSH Terms
Binding Sites Carrier Proteins/metabolism Clathrin Heavy Chains/genetics Clathrin Light Chains/genetics,physiology Clathrin-Coated Vesicles/physiology Cytoskeletal Proteins Models, Biological Saccharomyces cerevisiae/metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism,physiology Transport Vesicles/physiology
Chemicals
Carrier Proteins Clathrin Light Chains Cytoskeletal Proteins SLA2 protein, S cerevisiae Saccharomyces cerevisiae Proteins Clathrin Heavy Chains
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Newpher Thomas M
Department of Molecular and Cellular Pharmacology, University of Miami, Miami, FL 33101, USA.
Idrissi Fatima-Zahra
Geli Maria Isabel
Lemmon Sandra K
References (33)
33 references, click to expand
  1. An actin-binding protein of the Sla2/Huntingtin interacting protein 1 family is a novel component of clathrin-coated pits and vesicles.
    J Cell Biol. 1999 Dec 27;147(7):1503-18 PMID: 10613908
  2. Harnessing actin dynamics for clathrin-mediated endocytosis.
    Nat Rev Mol Cell Biol. 2006 Jun;7(6):404-14 PMID: 16723976
  3. Biological basket weaving: formation and function of clathrin-coated vesicles.
    Annu Rev Cell Dev Biol. 2001;17:517-68 PMID: 11687498
  4. HIP1 and HIP12 display differential binding to F-actin, AP2, and clathrin. Identification of a novel interaction with clathrin light chain.
    J Biol Chem. 2002 May 31;277(22):19897-904 PMID: 11889126
  5. Scd5p and clathrin function are important for cortical actin organization, endocytosis, and localization of sla2p in yeast.
    Mol Biol Cell. 2002 Aug;13(8):2607-25 PMID: 12181333
  6. Clathrin light and heavy chain interface: alpha-helix binding superhelix loops via critical tryptophans.
    EMBO J. 2002 Nov 15;21(22):6072-82 PMID: 12426379
  7. A pathway for association of receptors, adaptors, and actin during endocytic internalization.
    Cell. 2003 Nov 14;115(4):475-87 PMID: 14622601
  8. The Sla2p talin domain plays a role in endocytosis in Saccharomyces cerevisiae.
    Genetics. 2003 Dec;165(4):1661-74 PMID: 14704157
  9. HIP1 and HIP1r stabilize receptor tyrosine kinases and bind 3-phosphoinositides via epsin N-terminal homology domains.
    J Biol Chem. 2004 Apr 2;279(14):14294-306 PMID: 14732715
  10. Clathrin requirement for normal growth of yeast.
    Science. 1987 Oct 23;238(4826):504-9 PMID: 3116672
  11. Characterization of yeast clathrin and anticlathrin heavy-chain monoclonal antibodies.
    J Cell Biochem. 1988 Apr;36(4):329-40 PMID: 3288647
  12. Clathrin: a role in the intracellular retention of a Golgi membrane protein.
    Science. 1989 Sep 22;245(4924):1358-65 PMID: 2675311
  13. Analysis of clathrin light chain-heavy chain interactions using truncated mutants of rat liver light chain LCB3.
    J Biol Chem. 1990 Mar 5;265(7):3661-8 PMID: 2406259
  14. Yeast endocytosis assays.
    Methods Enzymol. 1991;194:697-710 PMID: 2005817
  15. Bovine brain clathrin light chains impede heavy chain assembly in vitro.
    J Biol Chem. 1991 Jul 5;266(19):12710-4 PMID: 2061336
  16. Suppressors of clathrin deficiency: overexpression of ubiquitin rescues lethal strains of clathrin-deficient Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Jan;13(1):521-32 PMID: 8380227
  17. Regulation of clathrin assembly and trimerization defined using recombinant triskelion hubs.
    Cell. 1995 Oct 20;83(2):257-67 PMID: 7585943
  18. The light chain subunit is required for clathrin function in Saccharomyces cerevisiae.
    J Biol Chem. 1996 Dec 20;271(51):33123-30 PMID: 8955161
  19. Novel functions of clathrin light chains: clathrin heavy chain trimerization is defective in light chain-deficient yeast.
    J Cell Sci. 1997 Apr;110 ( Pt 7):899-910 PMID: 9133677
  20. The I/LWEQ module: a conserved sequence that signifies F-actin binding in functionally diverse proteins from yeast to mammals.
    Proc Natl Acad Sci U S A. 1997 May 27;94(11):5679-84 PMID: 9159132
  21. Clathrin self-assembly is regulated by three light-chain residues controlling the formation of critical salt bridges.
    EMBO J. 1998 Aug 10;17(5):1297-303 PMID: 9482727
  22. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  23. Sla2p is associated with the yeast cortical actin cytoskeleton via redundant localization signals.
    Mol Biol Cell. 1999 Jul;10(7):2265-83 PMID: 10397764
  24. Molecular model for a complete clathrin lattice from electron cryomicroscopy.
    Nature. 2004 Dec 2;432(7017):573-9 PMID: 15502812
  25. Intrasteric inhibition mediates the interaction of the I/LWEQ module proteins Talin1, Talin2, Hip1, and Hip12 with actin.
    Biochemistry. 2004 Dec 14;43(49):15418-28 PMID: 15581353
  26. Interaction of Sla2p's ANTH domain with PtdIns(4,5)P2 is important for actin-dependent endocytic internalization.
    Mol Biol Cell. 2005 Feb;16(2):717-30 PMID: 15574875
  27. Huntingtin-interacting protein 1 (Hip1) and Hip1-related protein (Hip1R) bind the conserved sequence of clathrin light chains and thereby influence clathrin assembly in vitro and actin distribution in vivo.
    J Biol Chem. 2005 Feb 18;280(7):6109-17 PMID: 15533940
  28. Huntingtin interacting protein 1 (HIP1) regulates clathrin assembly through direct binding to the regulatory region of the clathrin light chain.
    J Biol Chem. 2005 Feb 18;280(7):6101-8 PMID: 15533941
  29. In vivo dynamics of clathrin and its adaptor-dependent recruitment to the actin-based endocytic machinery in yeast.
    Dev Cell. 2005 Jul;9(1):87-98 PMID: 15992543
  30. A modular design for the clathrin- and actin-mediated endocytosis machinery.
    Cell. 2005 Oct 21;123(2):305-20 PMID: 16239147
  31. Spatial dynamics of receptor-mediated endocytic trafficking in budding yeast revealed by using fluorescent alpha-factor derivatives.
    Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5793-8 PMID: 16574772
  32. Clathrin is important for normal actin dynamics and progression of Sla2p-containing patches during endocytosis in yeast.
    Traffic. 2006 May;7(5):574-88 PMID: 16643280
  33. The actin-binding protein Hip1R associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro.
    J Cell Biol. 2001 Sep 17;154(6):1209-23 PMID: 11564758
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2006-10-00
Epub
2006-00-26
Pages
4343-52
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1635359
Subset
IM
Grants
NIGMS NIH HHS · R01 GM055796 · United States
NIGMS NIH HHS · T32 GM008056 · United States
NIGMS NIH HHS · R01 GM55796 · United States
NIGMS NIH HHS · T32 GM08056-20 · 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: product@genelibs.com