Evolving Models for Assembling and Shaping Clathrin-coated Pits

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2020 Aug 10

PMID 32770195

Citations 30

Authors

Zhiming Chen

Sandra L Schmid

Affiliations

Soon will be listed here.

Abstract

Clathrin-mediated endocytosis occurs via the assembly of clathrin-coated pits (CCPs) that invaginate and pinch off to form clathrin-coated vesicles (CCVs). It is well known that adaptor protein 2 (AP2) complexes trigger clathrin assembly on the plasma membrane, and biochemical and structural studies have revealed the nature of these interactions. Numerous endocytic accessory proteins collaborate with clathrin and AP2 to drive CCV formation. However, many questions remain as to the molecular events involved in CCP initiation, stabilization, and curvature generation. Indeed, a plethora of recent evidence derived from cell perturbation, correlative light and EM tomography, live-cell imaging, modeling, and high-resolution structural analyses has revealed more complexity and promiscuity in the protein interactions driving CCP maturation than anticipated. After briefly reviewing the evidence supporting prevailing models, we integrate these new lines of evidence to develop a more dynamic and flexible model for how redundant, dynamic, and competing protein interactions can drive endocytic CCV formation and suggest new approaches to test emerging models.

Citing Articles

Clathrin-associated carriers enable recycling through a kiss-and-run mechanism.

Xu J, Liang Y, Li N, Dang S, Jiang A, Liu Y Nat Cell Biol. 2024; 26(10):1652-1668.

PMID: 39300312 DOI: 10.1038/s41556-024-01499-4.

Ubiquitin-driven protein condensation stabilizes clathrin-mediated endocytosis.

Yuan F, Gollapudi S, Day K, Ashby G, Sangani A, Malady B PNAS Nexus. 2024; 3(9):pgae342.

PMID: 39253396 PMC: 11382290. DOI: 10.1093/pnasnexus/pgae342.

Vesiculation pathways in clathrin-mediated endocytosis.

Wang X, Berro J, Ma R bioRxiv. 2024; .

PMID: 39185216 PMC: 11343097. DOI: 10.1101/2024.08.13.607731.

Diversity, Origin and Evolution of the ESCRT Systems.

Makarova K, Tobiasson V, Wolf Y, Lu Z, Liu Y, Zhang S bioRxiv. 2024; .

PMID: 38903064 PMC: 11188069. DOI: 10.1101/2024.02.06.579148.

Primary Human Breast Cancer-Associated Endothelial Cells Favor Interactions with Nanomedicines.

Wang L, Sheth V, Liu K, Panja P, Frickenstein A, He Y Adv Mater. 2024; 36(28):e2403986.

PMID: 38663008 PMC: 11239290. DOI: 10.1002/adma.202403986.

References

Haucke V, Kozlov M . Membrane remodeling in clathrin-mediated endocytosis. J Cell Sci. 2018; 131(17). DOI: 10.1242/jcs.216812. View

Pascolutti R, Algisi V, Conte A, Raimondi A, Pasham M, Upadhyayula S . Molecularly Distinct Clathrin-Coated Pits Differentially Impact EGFR Fate and Signaling. Cell Rep. 2019; 27(10):3049-3061.e6. PMC: 6581797. DOI: 10.1016/j.celrep.2019.05.017. View

Rosendale M, Van T, Grillo-Bosch D, Sposini S, Claverie L, Gauthereau I . Functional recruitment of dynamin requires multimeric interactions for efficient endocytosis. Nat Commun. 2019; 10(1):4462. PMC: 6773865. DOI: 10.1038/s41467-019-12434-9. View

Li P, Banjade S, Cheng H, Kim S, Chen B, Guo L . Phase transitions in the assembly of multivalent signalling proteins. Nature. 2012; 483(7389):336-40. PMC: 3343696. DOI: 10.1038/nature10879. View

Willox A, Sahraoui Y, Royle S . Non-specificity of Pitstop 2 in clathrin-mediated endocytosis. Biol Open. 2014; 3(5):326-31. PMC: 4021354. DOI: 10.1242/bio.20147955. View

Zhuo Y, Ilangovan U, Schirf V, Demeler B, Sousa R, Hinck A . Dynamic interactions between clathrin and locally structured elements in a disordered protein mediate clathrin lattice assembly. J Mol Biol. 2010; 404(2):274-90. PMC: 2981644. DOI: 10.1016/j.jmb.2010.09.044. View

Praefcke G, Ford M, Schmid E, Olesen L, Gallop J, Peak-Chew S . Evolving nature of the AP2 alpha-appendage hub during clathrin-coated vesicle endocytosis. EMBO J. 2004; 23(22):4371-83. PMC: 526462. DOI: 10.1038/sj.emboj.7600445. View

Liu Y, Lukiyanchuk V, Schmid S . Common membrane trafficking defects of disease-associated dynamin 2 mutations. Traffic. 2011; 12(11):1620-33. PMC: 3188678. DOI: 10.1111/j.1600-0854.2011.01250.x. View

Kumar G, Sain A . Shape transitions during clathrin-induced endocytosis. Phys Rev E. 2017; 94(6-1):062404. DOI: 10.1103/PhysRevE.94.062404. View

10.

Sochacki K, Taraska J . From Flat to Curved Clathrin: Controlling a Plastic Ratchet. Trends Cell Biol. 2019; 29(3):241-256. DOI: 10.1016/j.tcb.2018.12.002. View

11.

Smith C, Grigorieff N, Pearse B . Clathrin coats at 21 A resolution: a cellular assembly designed to recycle multiple membrane receptors. EMBO J. 1998; 17(17):4943-53. PMC: 1170823. DOI: 10.1093/emboj/17.17.4943. View

12.

Avinoam O, Schorb M, Beese C, Briggs J, Kaksonen M . ENDOCYTOSIS. Endocytic sites mature by continuous bending and remodeling of the clathrin coat. Science. 2015; 348(6241):1369-72. DOI: 10.1126/science.aaa9555. View

13.

Lemmon S, Traub L . Getting in touch with the clathrin terminal domain. Traffic. 2012; 13(4):511-9. PMC: 3330156. DOI: 10.1111/j.1600-0854.2011.01321.x. View

14.

Reis C, Chen P, Srinivasan S, Aguet F, Mettlen M, Schmid S . Crosstalk between Akt/GSK3β signaling and dynamin-1 regulates clathrin-mediated endocytosis. EMBO J. 2015; 34(16):2132-46. PMC: 4557666. DOI: 10.15252/embj.201591518. View

15.

Elbaum-Garfinkle S, Kim Y, Szczepaniak K, Chen C, Eckmann C, Myong S . The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. Proc Natl Acad Sci U S A. 2015; 112(23):7189-94. PMC: 4466716. DOI: 10.1073/pnas.1504822112. View

16.

McMahon H, Boucrot E . Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol. 2011; 12(8):517-33. DOI: 10.1038/nrm3151. View

17.

Kanaseki T, Kadota K . The "vesicle in a basket". A morphological study of the coated vesicle isolated from the nerve endings of the guinea pig brain, with special reference to the mechanism of membrane movements. J Cell Biol. 1969; 42(1):202-20. PMC: 2107565. DOI: 10.1083/jcb.42.1.202. View

18.

Sidhu S, Fairbrother W, Deshayes K . Exploring protein-protein interactions with phage display. Chembiochem. 2003; 4(1):14-25. DOI: 10.1002/cbic.200390008. View

19.

Bassereau P, Jin R, Baumgart T, Deserno M, Dimova R, Frolov V . The 2018 biomembrane curvature and remodeling roadmap. J Phys D Appl Phys. 2019; 51(34). PMC: 6333427. DOI: 10.1088/1361-6463/aacb98. View

20.

Mettlen M, Danuser G . Imaging and modeling the dynamics of clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol. 2014; 6(12):a017038. PMC: 4292148. DOI: 10.1101/cshperspect.a017038. View