Regulation of Membrane-Shape Transitions Induced by I-BAR Domains

Biophysical Journal

Volumn 109, Issue 2, 2015, Pages 298-307

  Chen, Zhiming ^a   Shi, Zheng ^a   Baumgart, Tobias ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2-OLEOYLPHOSPHATIDYLCHOLINE; DIOLEOYL PHOSPHATIDYLETHANOLAMINE; LIPOSOME; MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE;

ANIMAL; CELL MEMBRANE; CELL SURFACE; CHEMISTRY; CONFOCAL MICROSCOPY; DIMERIZATION; HUMAN; METABOLISM; MOUSE; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY; SURFACE TENSION;

ANIMALS; CELL MEMBRANE; CELL SURFACE EXTENSIONS; DIMERIZATION; HUMANS; MEMBRANE PROTEINS; MICE; MICROSCOPY, CONFOCAL; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY; SURFACE TENSION; UNILAMELLAR LIPOSOMES;

EID: 84937550246     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.06.010     Document Type: Article

References (56)

1. J. Zimmerberg, and M.M. Kozlov How proteins produce cellular membrane curvature Nat. Rev. Mol. Cell Biol. 7 2006 9 19
2. A. Frost, V.M. Unger, and P. De Camilli The BAR domain superfamily: membrane-molding macromolecules Cell 137 2009 191 196
3. J.L. Gallop, and C.C. Jao H.T. McMahon Mechanism of endophilin N-BAR domain-mediated membrane curvature EMBO J. 25 2006 2898 2910
4. B.R. Capraro, and Z. Shi T. Baumgart Kinetics of endophilin N-BAR domain dimerization and membrane interactions J. Biol. Chem. 288 2013 12533 12543
5. S.H. Lee, and F. Kerff R. Dominguez Structural basis for the actin-binding function of missing-in-metastasis Structure 15 2007 145 155
6. T.H. Millard, and G. Bompard K. Fütterer Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53 EMBO J. 24 2005 240 250
7. Z. Chen, and K. Chang T. Baumgart Intradimer/intermolecular interactions suggest autoinhibition mechanism in endophilin A1 J. Am. Chem. Soc. 136 2014 4557 4564
8. P.K. Mattila, and A. Pykäläinen P. Lappalainen Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism J. Cell Biol. 176 2007 953 964
9. C. Mim, and H. Cui V.M. Unger Structural basis of membrane bending by the N-BAR protein endophilin Cell 149 2012 137 145
10. J. Saarikangas, and H. Zhao P. Lappalainen Molecular mechanisms of membrane deformation by I-BAR domain proteins Curr. Biol. 19 2009 95 107
11. L.M. Machesky, and S.A. Johnston MIM: a multifunctional scaffold protein J. Mol. Med. 85 2007 569 576
12. G. Bompard, and S.J. Sharp L.M. Machesky Involvement of Rac in actin cytoskeleton rearrangements induced by MIM-B J. Cell Sci. 118 2005 5393 5403
13. Y.G. Lee, and J.A. Macoska K.J. Pienta MIM, a potential metastasis suppressor gene in bladder cancer Neoplasia 4 2002 291 294
14. A. Yamagishi, and M. Masuda N. Mochizuki A novel actin bundling/filopodium-forming domain conserved in insulin receptor tyrosine kinase substrate p53 and missing in metastasis protein J. Biol. Chem. 279 2004 14929 14936
15. S. Suetsugu, and K. Murayama S. Yokoyama The RAC binding domain/IRSp53-MIM homology domain of IRSp53 induces RAC-dependent membrane deformation J. Biol. Chem. 281 2006 35347 35358
16. G. Scita, and S. Confalonieri S. Suetsugu IRSp53: crossing the road of membrane and actin dynamics in the formation of membrane protrusions Trends Cell Biol. 18 2008 52 60
17. P.K. Mattila, and M. Salminen P. Lappalainen Mouse MIM, a tissue-specific regulator of cytoskeletal dynamics, interacts with ATP-actin monomers through its C-terminal WH2 domain J. Biol. Chem. 278 2003 8452 8459
18. H. Nakagawa, and H. Miki J.V. Small IRSp53 is colocalised with WAVE2 at the tips of protruding lamellipodia and filopodia independently of Mena J. Cell Sci. 116 2003 2577 2583
19. S. Suetsugu The proposed functions of membrane curvatures mediated by the BAR domain superfamily proteins J. Biochem. 148 2010 1 12
20. H. Zhao, A. Pykäläinen, and P. Lappalainen I-BAR domain proteins: linking actin and plasma membrane dynamics Curr. Opin. Cell Biol. 23 2011 14 21
21. P.K. Mattila, and P. Lappalainen Filopodia: molecular architecture and cellular functions Nat. Rev. Mol. Cell Biol. 9 2008 446 454
22. H.T. McMahon, and E. Boucrot Molecular mechanism and physiological functions of clathrin-mediated endocytosis Nat. Rev. Mol. Cell Biol. 12 2011 517 533
23. C.E. Morris, and U. Homann Cell surface area regulation and membrane tension J. Membr. Biol. 179 2001 79 102
24. A. Pietuch, and B.R. Brückner A. Janshoff Elastic properties of cells in the context of confluent cell monolayers: impact of tension and surface area regulation Soft Matter 9 2013 11490 11502
25. Y. Schweitzer, and A.D. Lieber M.M. Kozlov Theoretical analysis of membrane tension in moving cells Biophys. J. 106 2014 84 92
26. A.D. Lieber, and S. Yehudai-Resheff K. Keren Membrane tension in rapidly moving cells is determined by cytoskeletal forces Curr. Biol. 23 2013 1409 1417
27. S. Watanabe, and B.R. Rost E.M. Jorgensen Ultrafast endocytosis at mouse hippocampal synapses Nature 504 2013 242 247
28. J. Dai, and M.P. Sheetz Regulation of endocytosis, exocytosis, and shape by membrane tension Cold Spring Harb. Symp. Quant. Biol. 60 1995 567 571
29. N.C. Gauthier, and M.A. Fardin M.P. Sheetz Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading Proc. Natl. Acad. Sci. USA 108 2011 14467 14472
30. S. Boulant, and C. Kural T. Kirchhausen Actin dynamics counteract membrane tension during clathrin-mediated endocytosis Nat. Cell Biol. 13 2011 1124 1131
31. T.A. Masters, and B. Pontes N.C. Gauthier Plasma membrane tension orchestrates membrane trafficking, cytoskeletal remodeling, and biochemical signaling during phagocytosis Proc. Natl. Acad. Sci. USA 110 2013 11875 11880
32. S. Sukharev, and F. Sachs Molecular force transduction by ion channels: diversity and unifying principles J. Cell Sci. 125 2012 3075 3083
33. K. Keren, and Z. Pincus J.A. Theriot Mechanism of shape determination in motile cells Nature 453 2008 475 480
34. A. Diz-Muñoz, D.A. Fletcher, and O.D. Weiner Use the force: membrane tension as an organizer of cell shape and motility Trends Cell Biol. 23 2013 47 53
35. Z. Shi, and T. Baumgart Membrane tension and peripheral protein density mediate membrane shape transitions Nat. Commun. 6 2015 5974
36. S. Leibler Curvature instability in membranes J. Phys. 47 1986 507 516
37. F. Divet, G. Danker, and C. Misbah Fluctuations and instability of a biological membrane induced by interaction with macromolecules Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72 2005 041901
38. L. Limozin, and E. Sackmann Polymorphism of cross-linked actin networks in giant vesicles Phys. Rev. Lett. 89 2002 168103
39. L. Limozin, M. Bärmann, and E. Sackmann On the organization of self-assembled actin networks in giant vesicles Eur. Phys. J. E Soft Matter 10 2003 319 330
40. A.P. Liu, and D.L. Richmond D.A. Fletcher Membrane-induced bundling of actin filaments Nat. Phys. 4 2008 789 793
41. J.C. Stachowiak, and E.M. Schmid C.C. Hayden Membrane bending by protein-protein crowding Nat. Cell Biol. 14 2012 944 949
42. A. Tian, and T. Baumgart Sorting of lipids and proteins in membrane curvature gradients Biophys. J. 96 2009 2676 2688
43. Z. Shi, and T. Baumgart Dynamics and instabilities of lipid bilayer membrane shapes Adv. Colloid Interface Sci. 208 2014 76 88
44. B. Sorre, and A. Callan-Jones A. Roux Nature of curvature coupling of amphiphysin with membranes depends on its bound density Proc. Natl. Acad. Sci. USA 109 2012 173 178
45. J.W. Cahn, and J.E. Hilliard Free energy of a nonuniform system. 1. Interfacial free energy J. Chem. Phys. 28 1958 258 267
46. N. Ben-Tal, and B. Honig S. McLaughlin Electrostatic binding of proteins to membranes. Theoretical predictions and experimental results with charybdotoxin and phospholipid vesicles Biophys. J. 73 1997 1717 1727
47. T. Baumgart, and B.R. Capraro S.L. Das Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids Annu. Rev. Phys. Chem. 62 2011 483 506
48. H.F. Renard, and M. Simunovic L. Johannes Endophilin-A2 functions in membrane scission in clathrin-independent endocytosis Nature 517 2015 493 496
49. E. Boucrot, and A.P. Ferreira H.T. McMahon Endophilin marks and controls a clathrin-independent endocytic pathway Nature 517 2015 460 465
50. C. Zhu, S.L. Das, and T. Baumgart Nonlinear sorting, curvature generation, and crowding of endophilin N-BAR on tubular membranes Biophys. J. 102 2012 1837 1845
51. P.D. Blood, R.D. Swenson, and G.A. Voth Factors influencing local membrane curvature induction by N-BAR domains as revealed by molecular dynamics simulations Biophys. J. 95 2008 1866 1876
52. C. Yang, and M. Hoelzle T. Svitkina Coordination of membrane and actin cytoskeleton dynamics during filopodia protrusion PLoS ONE 4 2009 e5678
53. D.J. Kast, and C. Yang R. Dominguez Mechanism of IRSp53 inhibition and combinatorial activation by Cdc42 and downstream effectors Nat. Struct. Mol. Biol. 21 2014 413 422
54. E. Boucrot, and A. Pick M.M. Kozlov Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains Cell 149 2012 124 136
55. B.R. Capraro, and Y. Yoon T. Baumgart Curvature sensing by the epsin N-terminal homology domain measured on cylindrical lipid membrane tethers J. Am. Chem. Soc. 132 2010 1200 1201
56. W.T. Hsieh, and C.J. Hsu T. Baumgart Curvature sorting of peripheral proteins on solid-supported wavy membranes Langmuir 28 2012 12838 12843