The Monomeric Clathrin Assembly Protein, AP180, Regulates Contractile Vacuole Size in Dictyostelium Discoideum

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2006 Oct 20

PMID 17050736

Citations 17

Authors

Irene Stavrou

Theresa J OHalloran

Affiliations

Soon will be listed here.

Abstract

AP180, one of many assembly proteins and adaptors for clathrin, stimulates the assembly of clathrin lattices on membranes, but its unique contribution to clathrin function remains elusive. In this study we identified the Dictyostelium discoideum ortholog of the adaptor protein AP180 and characterized a mutant strain carrying a deletion in this gene. Imaging GFP-labeled AP180 showed that it localized to punctae at the plasma membrane, the contractile vacuole, and the cytoplasm and associated with clathrin. AP180 null cells did not display defects characteristic of clathrin mutants and continued to localize clathrin punctae on their plasma membrane and within the cytoplasm. However, like clathrin mutants, AP180 mutants, were osmosensitive. When immersed in water, AP180 null cells formed abnormally large contractile vacuoles. Furthermore, the cycle of expansion and contraction for contractile vacuoles in AP80 null cells was twice as long as that of wild-type cells. Taken together, our results suggest that AP180 plays a unique role as a regulator of contractile vacuole morphology and activity in Dictyostelium.

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References

Zhang B, Koh Y, Beckstead R, Budnik V, Ganetzky B, Bellen H . Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron. 1999; 21(6):1465-75. DOI: 10.1016/s0896-6273(00)80664-9. View

De Beer T, Carter R, Sorkin A, Overduin M . Structure and Asn-Pro-Phe binding pocket of the Eps15 homology domain. Science. 1998; 281(5381):1357-60. DOI: 10.1126/science.281.5381.1357. View

Damer C, OHalloran T . Spatially regulated recruitment of clathrin to the plasma membrane during capping and cell translocation. Mol Biol Cell. 2000; 11(6):2151-9. PMC: 14909. DOI: 10.1091/mbc.11.6.2151. View

Kay B, Yamabhai M, Wendland B, Emr S . Identification of a novel domain shared by putative components of the endocytic and cytoskeletal machinery. Protein Sci. 1999; 8(2):435-8. PMC: 2144257. DOI: 10.1110/ps.8.2.435. View

Owen D, Vallis Y, Noble M, Hunter J, Dafforn T, Evans P . A structural explanation for the binding of multiple ligands by the alpha-adaptin appendage domain. Cell. 1999; 97(6):805-15. DOI: 10.1016/s0092-8674(00)80791-6. View

Nonet M, Holgado A, Brewer F, Serpe C, Norbeck B, Holleran J . UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol Biol Cell. 1999; 10(7):2343-60. PMC: 25452. DOI: 10.1091/mbc.10.7.2343. View

Huang K, Dhondt K, Riezman H, Lemmon S . Clathrin functions in the absence of heterotetrameric adaptors and AP180-related proteins in yeast. EMBO J. 1999; 18(14):3897-908. PMC: 1171466. DOI: 10.1093/emboj/18.14.3897. View

Hao W, Luo Z, Zheng L, Prasad K, Lafer E . AP180 and AP-2 interact directly in a complex that cooperatively assembles clathrin. J Biol Chem. 1999; 274(32):22785-94. DOI: 10.1074/jbc.274.32.22785. View

Traub L, Downs M, Westrich J, Fremont D . Crystal structure of the alpha appendage of AP-2 reveals a recruitment platform for clathrin-coat assembly. Proc Natl Acad Sci U S A. 1999; 96(16):8907-12. PMC: 17706. DOI: 10.1073/pnas.96.16.8907. View

10.

Tebar F, Bohlander S, Sorkin A . Clathrin assembly lymphoid myeloid leukemia (CALM) protein: localization in endocytic-coated pits, interactions with clathrin, and the impact of overexpression on clathrin-mediated traffic. Mol Biol Cell. 1999; 10(8):2687-702. PMC: 25500. DOI: 10.1091/mbc.10.8.2687. View

11.

Bao H, Daniels R, Macleod G, Charlton M, Atwood H, Zhang B . AP180 maintains the distribution of synaptic and vesicle proteins in the nerve terminal and indirectly regulates the efficacy of Ca2+-triggered exocytosis. J Neurophysiol. 2005; 94(3):1888-903. DOI: 10.1152/jn.00080.2005. View

12.

Meyerholz A, Hinrichsen L, Groos S, Esk P, Brandes G, Ungewickell E . Effect of clathrin assembly lymphoid myeloid leukemia protein depletion on clathrin coat formation. Traffic. 2005; 6(12):1225-34. DOI: 10.1111/j.1600-0854.2005.00355.x. View

13.

Gabriel D, Hacker U, Kohler J, Schwartz J, Westphal M, Gerisch G . The contractile vacuole network of Dictyostelium as a distinct organelle: its dynamics visualized by a GFP marker protein. J Cell Sci. 1999; 112 ( Pt 22):3995-4005. DOI: 10.1242/jcs.112.22.3995. View

14.

Kirchhausen T . Adaptors for clathrin-mediated traffic. Annu Rev Cell Dev Biol. 1999; 15:705-32. DOI: 10.1146/annurev.cellbio.15.1.705. View

15.

ter Haar E, Harrison S, Kirchhausen T . Peptide-in-groove interactions link target proteins to the beta-propeller of clathrin. Proc Natl Acad Sci U S A. 2000; 97(3):1096-100. PMC: 15533. DOI: 10.1073/pnas.97.3.1096. View

16.

Owen D, Vallis Y, Pearse B, McMahon H, Evans P . The structure and function of the beta 2-adaptin appendage domain. EMBO J. 2000; 19(16):4216-27. PMC: 302036. DOI: 10.1093/emboj/19.16.4216. View

17.

Levi S, Polyakov M, Egelhoff T . Green fluorescent protein and epitope tag fusion vectors for Dictyostelium discoideum. Plasmid. 2000; 44(3):231-8. DOI: 10.1006/plas.2000.1487. View

18.

Morgan J, Prasad K, Hao W, Augustine G, Lafer E . A conserved clathrin assembly motif essential for synaptic vesicle endocytosis. J Neurosci. 2000; 20(23):8667-76. PMC: 6773056. View

19.

Ford M, Pearse B, Higgins M, Vallis Y, Owen D, Gibson A . Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science. 2001; 291(5506):1051-5. DOI: 10.1126/science.291.5506.1051. View

20.

Mao Y, Chen J, Maynard J, Zhang B, Quiocho F . A novel all helix fold of the AP180 amino-terminal domain for phosphoinositide binding and clathrin assembly in synaptic vesicle endocytosis. Cell. 2001; 104(3):433-40. DOI: 10.1016/s0092-8674(01)00230-6. View