Minimal mesoscale model for protein-mediated vesiculation in clathrin-dependent endocytosis

PLoS Computational Biology

Volumn 6, Issue 9, 2010, Pages

  Agrawal, Neeraj J ^a   Nukpezah, Jonathan ^a   Radhakrishnan, Ravi ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; MACHINERY; MAMMALS; MEMBRANES; MOLECULAR BIOLOGY; PROTEINS;

CELLULAR FUNCTION; CLATHRIN-DEPENDENT ENDOCYTOSIS; CLATHRINS; ENDOCYTIC MACHINERY; ENDOCYTIC PATHWAYS; EUKARYOTIC CELLS; EXTRACELLULAR; MESO-SCALE MODELING; PROTEIN-MEMBRANE INTERACTIONS; REGULATORY PROCESS;

PROBABILITY DISTRIBUTIONS;

CLATHRIN; EPSIN;

ARTICLE; BINDING SITE; CALCULATION; CELL MATURATION; CELL SIZE; CELL STRUCTURE; CELL TYPE; CONTROLLED STUDY; ENDOCYTOSIS; MATHEMATICAL MODEL; MINIMAL MESOSCALE MODEL; NERVE CELL; PROBABILITY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

EUKARYOTA; MAMMALIA; MIRIDAE;

EID: 78049436709     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000926     Document Type: Article

References (50)

1. Schmid EM, McMahon HT (2007) Integrating molecular and network biology to decode endocytosis. Nature 448: 883-888.
2. Deserno M, Bickel T (2003) Wrapping of a spherical colloid by a fluid membrane. Europhys Lett 62: 767-773.
3. Deserno M (2004) Elastic deformation of a fluid membrane upon colloid binding. Phys Rev E 69: 031903.
4. Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, et al. (2008) Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc Natl Acad Sci U S A 105: 14265-14270.
5. Edwards DA, Gooch KJ, Zhang I, McKinley GH, Langer R (1996) The nucleation of receptor-mediated endocytosis. Proc Natl Acad Sci U S A 93: 1786-1791.
6. Teis D, Huber LA (2003) The odd couple: signal transduction and endocytosis. Cell Mol Life Sci 60: 2020-2033.
7. Marsh M (2001) Endocytosis Hames BD, Glover DM, eds. New York: Oxford university Press.
8. Kirchhausen T (2000) Three ways to make a vesicle. Nat Rev Mol Cell Biol 1: 187-198.
9. Liu J, Kaksonen M, Drubin DG, Oster G (2006) Endocytic vesicle scission by lipid phase boundary forces. Proc Natl Acad Sci USA 103: 10277-10282.
10. Reynwar BJ, Illya G, Harmandaris VA, Muller MM, Kremer K, et al. (2007) Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447: 461-464.
11. Agrawal NJ, Weinstein J, Radhakrishnan R (2008) Landscape of Finite- Temperature Equilibrium Behavior of Curvature Inducing Proteins on a Bilayer Membrane Explored using a Linearized Elastic Free Energy Model. Mol Phys 106: 1913-1923.
12. Ford MGJ, Mills IG, Vallis Y, Praefcke GJK, Evans PR, et al. (2002) Curvature of clathrin coated pits driven by Epsin. Nature 419: 361-366.
13. Praefcke GJ, Ford MG, Schmid EM, Olesen LE, Gallop JL, et al. (2004) Evolving nature of the AP2 alpha-appendage hub during clathrin-coated vesicle endocytosis. Embo J 23: 4371-4383.
14. Kaksonen M, Toret CP, Drubin DG (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7: 404-414.
15. Hinrichsen L, Meyerhoiz A, Groos S, Ungewickell EJ (2006) Bending a membrane: How clathrin affects budding. Proc Natl Acad Sci USA 103: 8715-8720.
16. Merrifield CJ, Perrais D, Zenisek D (2005) Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121: 593-606.
17. Motley A, Bright NA, Seaman MNJ, Robinson MS (2003) Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 162: 909-918.
18. Hinrichsen L, Harborth J, Andrees L, Weber K, Ungewickell EJ (2003) Effect of Clathrin Heavy Chain- and {alpha}-Adaptin-specific Small Inhibitory RNAs on Endocytic Accessory Proteins and Receptor Trafficking in HeLa Cells. J Biol Chem 278: 45160-45170.
19. Jakobsson J, Gad H, Andersson F, Low P, Shupliakov O, et al. (2008) Role of epsin 1 in synaptic vesicle endocytosis. Proc Natl Acad Sci U S A. pp 6445-6450.
20. Saffarian S, Cocucci E, Kirchhausen T (2009) Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 7: e1000191.
21. Liu J, Sun Y, Drubin DG, Oster GF (2009) The Mechanochemistry of Endocytosis. Plos Biol 7: e1000204.
22. Kohyama T, Kroll DM, Gompper G (2003) Budding of crystalline domains in fluid membranes. Phys Rev E Stat Nonlin Soft Matter Phys 68: 061905.
23. Frese RN, Pamies JC, Olsen JD, Bahatyrova S, van der Weij-de Wit CD, et al. (2008) Protein Shape and Crowding Drive Domain Formation and Curvature in Biological Membranes. Biophys J 94: 640-647.
24. Lundmark R, Carlsson SR (2010) Driving membrane curvature in clathrindependent and clathrin-independent endocytosis. Semin Cell Dev Biol 21: 363-370.
25. Ehrlich M, Boll W, van Oijen A, Hariharan R, Chandran K, et al. (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118: 591-605.
26. Zhang C-Z, Wang Z-G (2008) Nucleation of membrane adhesions. Phys Rev E 77: 021906.
27. Boal DH (2002) Mechanics of the cell. Cambridge: Cambridge University Press.
28. Keen JH (1987) Clathrin assembly proteins: affinity purification and a model for coat assembly. J Cell Biol 105: 1989-1998.
29. Nossal R (2001) Energetics of clathrin basket assembly. Traffic 2: 138-147.
30. Edeling MA, Smith C, Owen D (2006) Life of a clathrin coat: insights from clathrin and AP structures. Nat Rev Mol Cell Biol 7: 32-44.
31. McLaughlin S, Wang J, Gambhir A, Murray D (2002) PIP2 AND PROTEINS: Interactions, Organization, and Information Flow. Annu Rev Biophys Biomol Struct 31: 151-175.
32. Seifert U (1997) Configurations of fluid membranes and vesicles. Advances in Physics 46: 13-137.
33. Lennon EM, Katsov K, Fredrickson GH (2008) Free Energy Evaluation in Field-Theoretic Polymer Simulations. Phys Rev Lett 101: 138302.
34. Lee S-JE, Hori Y, Groves JT, Dustin ML, Chakraborty AK (2002) The synapse assembly model. Trends Immunol 23: 500-502.
35. Blood PD, Voth GA (2006) Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations. Proc Natl Acad Sci USA 103: 15068-15072.
36. Arkhipov A, Yin Y, Schulten K (2009) Membrane-bending mechanism of amphiphysin N-BAR domains. Biophys J 97: 2727-2735.
37. Seifert U, Berndl K, Lipowsky R (1991) Shape transformations of vesicles: Phase diagram for spontaneous- curvature and bilayer-coupling models. Phys Rev A 44: 1182.
38. Safran SA (1999) Curvature elasticity of thin films. Adv Phys 48: 395-448.
39. Helfrich W (1973) Elastic Properties of Lipid Bilayers - Theory and Possible Experiments. Z Naturforsch C 28: 693-703.
40. Hoffman JD (1992) Numerical methods for engineers and scientists. New York: McGraw-Hill.
41. Agrawal NJ, Radhakrishnan R (2009) Calculation of free energies in fluid membranes subject to heterogeneous curvature fields. Phys Rev E 80: 011925.
42. Grafmuller A, Shillcock J, Lipowsky R (2007) Pathway of membrane fusion with two tension-dependent energy barriers. Phys Rev Lett 98: 218101.
43. Chandler DE, Gumbart J, Stack JD, Chipot C, Schulten K (2009) Membrane curvature induced by aggregates of LH2s and monomeric LH1s. Biophys J 97: 2978-2984.
44. Cui H, Ayton GS, Voth GA (2009) Membrane binding by the endophilin NBAR domain. Biophys J 97: 2746-2753.
45. Weinstein J, Radhakrishnan R (2006) A coarse-grained methodology for simulating interfacial dynamics in complex fluids: application to protein mediated membrane processes. Mol Phys 104: 3653-3666.
46. Goulian M, Bruinsma R, Pincus P (1993) Long-range forces in heterogeneous fluid membranes. Europhys Lett 22: 145-150.
47. Kim KS, Neu J, Oster G (1998) Curvature-mediated interactions between membrane proteins. Biophys J 75: 2274-2291.
48. Park J-M, Lubensky TC (1996) Interactions between Membrane Inclusions on Fluctuating Membranes. J Phys I France I 7: 1217.
49. Smith CJ, Grigorieff N, Pearse BMF (1998) Clathrin coats at 21 angstrom resolution: a cellular assembly designed to recycle multiple membrane receptors. Embo J 17: 4943-4953.
50. Duijneveldt JSV, Frenkel D (1992) Computer simulation study of free energy barriers during crystal nucleation. J Chem Phys 96: 4655.