On the role of membrane anisotropy and BAR proteins in the stability of tubular membrane structures

Journal of Biomechanics

Volumn 45, Issue 2, 2012, Pages 231-238

  Kabaso, Doron ^a   Bobrovska, Nataliya ^a,b   Góźdź, Wojciech ^b   Gov, Nir ^c   Kralj Iglič, Veronika ^a   Veranič, Peter ^a   Iglič, Aleš ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b INSTITUTE OF PHYSICAL CHEMISTRY   (Poland)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Axisymmetric model; Curvature driven lateral segregation; Linear stability analysis; Membrane anisotropy; Membrane nanotubes

Indexed keywords

ACTIN FILAMENT; AXISYMMETRIC MODELS; CELL SURFACES; CURVATURE DRIVEN LATERAL SEGREGATION; HIGH DENSITY; ISOTROPIC BENDING; LINEAR STABILITY; NANO DOMAIN; RADIAL DIRECTION; SHORT TERM STABILITY; SPONTANEOUS CURVATURE; TUBULAR MEMBRANES;

ANISOTROPY; CELL MEMBRANES; LINEAR STABILITY ANALYSIS; MEMBRANES; NANOTUBES; SYSTEM STABILITY;

PROTEINS;

MEMBRANE PROTEIN; PROMININ; PROTEIN I BAR; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANISOTROPY; ARTICLE; MEMBRANE BIOLOGY; MEMBRANE STABILIZATION; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; STRUCTURE ANALYSIS; TUBULAR MEMBRANE STRUCTURE;

ACTIN CYTOSKELETON; ANIMALS; ANISOTROPY; ANTIGENS, CD; CELL MEMBRANE STRUCTURES; CYTOSKELETAL PROTEINS; GLYCOPROTEINS; HUMANS; MEMBRANE LIPIDS; MODELS, BIOLOGICAL; PEPTIDES; PROTEIN STRUCTURE, TERTIARY;

EID: 84455169435     PISSN: 00219290     EISSN: 18732380     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2011.10.039     Document Type: Article

References (50)

1. Baumgart T., Capraro B.R., Zhu C., Das S.L. Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annual Review of Physical Chemistry 2011, 62:483-506.
2. Corbeil D., Röper K., Fargeas C.A., Joester A., Huttner W.B. Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2001, 2:82-91.
3. Davis D.M., Sowinski S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nature Reviews Molecular Cell Biology 2008, 6:431-436.
4. Derényi I., Jülicher F., Prost J. Formation and interaction of membrane tubes. Physical Review Letters 2002, 88:238101.
5. Dubey G.P., Ben-Yehuda S. Intercellular nanotubes mediate bacterial communication. Cell 2011, 144:590-600.
6. Fischer T. Bending stiffness of lipid bilayers. III. Gaussian curvature. Journal de Physique II (France) 1992, 2:337-343.
7. Fošnarič M., Iglič A., May S. Influence of rigid inclusions on the bending elasticity of a lipid membrane. Physical Review E 2006, 174:051503.
8. Gerdes H.H., Bukoreshtiev N.V., Barroso J.F.V. Tunneling nanotubes: a new route for the exchange of components between animal cells. FEBS Letters 2007, 581:2194-2201.
9. Gimsa U., Iglič A., Fiedler S., Zwanzig M., Kralj-Iglič V.L., Jonas L., Gimsa J. Actin is not required for nanotubular protrusions of primary astrocytes grown on metal nano-lawn. Molecular Membrane Biology 2007, 24:243-255.
10. Góźdź W.T. Spontaneous curvature induced shape transformations of tubular polymersomes. Langmuir 2004, 20:7385-7391.
11. Góźdź W.T. Influence of spontaneous curvature and microtubules on the conformations of lipid vesicles. The Journal of Physical Chemistry B 2005, 109:21145-21149.
12. Góźdź W.T. The interface width of separated two-component lipid membranes. Journal of Physical Chemistry B 2006, 110:21981-21986.
13. Góźdź W.T. Shape transformation of lipid vesicles induced by diffusing macromolecules. Journal of Chemical Physics 2011, 134:024110.
14. Heath R.J.W., Install R.H. F-BAR domains: multifunctional regulators of membrane curvature. Journal of Cell Science 2008, 121:1951-1954.
15. Heinrich M.C., Capraro B.R., Tian A., Isas J.M., Langen R., Baumgart T. Quantifying membrane curvature generation of Drosophila amphiphysin N-BAR domains. The Journal of Physical Chemistry Letters 2010, 1:3401-3406.
16. Helfrich W. Elastic properties of lipid bilayers: theory and possible experiments. Zeitschrift für Naturforschung C 1973, 28:693-703.
17. Hurtig J., Chiu T., Onfelt B. Intercellular nanotubes: insights from imaging studies and beyond. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology 2010, 2:260-276.
18. Huttner H.B., Zimmerberg J. Implications of lipid microdomains for membrane curvature, budding and fission. Commentary Current Opinion Cell Biology 2001, 13:478-484.
19. Iglič A., Babnik B., Gimsa U., Kralj-Iglič V. On the role of membrane anisotropy in the beading transition of undulated tubular membrane structures. Journal of Physics A: Mathematical and General 2005, 38:8527-8536.
20. Iglič A., Hägerstrand H., Veranič P., Plemenitaš V., Kralj-Iglič V. Curvature induced accumulation of anisotropic membrane components 29 and raft formation in cylindrical membrane protrusions. Journal of Theoretical Biology 2006, 240:368-373.
21. Iglič A., Babnik B., Fošnarič M., Hägerstrand H., Kralj-Iglič V. On the role of anisotropy of membrane constituents in formation of a membrane neck during budding of multicomponent membrane. Journal of Biomechanics 2007, 40:579-585.
22. Iglič A., Lokar M., Babnik B., Slivnik T., Veranič P., Hägerstrand H., Kralj-Igličv V. Possible role of flexible red blood cell membrane nanodomains in the growth and stability of membrane nanotubes. Blood Cells, Molecules and Diseases 2007, 39:14-23.
23. Itoh T., Erdmann K.S., Roux A., Habermann B., Werner H., De Camilli P. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Developmental Cell 2005, 23:791-804.
24. Janich P., Corbeil D. GM1 and GM3 lipids highlight distinct lipid microdomains with the apical domain of epithelial cells. FEBS Letters 2007, 581:1783-1787.
25. Jorgačevski J., Fošnarič M., Vardjan N., Stenovec M., Potokar M., Kreft M., Kralj-Iglič V., Iglič A., Zorec R. Fusion pore stability of peptidergic vesicles. Molecular Membrane Biology 2010, 27:65-80.
26. Kabaso D., Shlomovitz R., Auth T., Lew V.L., Gov N.S. Curling and local shape changes of red blood cell membranes driven by cytoskeletal reorganization. Biophysical Journal 2010, 99:808-816.
27. Kabaso D., Shlomovitz R., Schloen K., Stradal T., Gov N.S. Theoretical model for cellular shapes driven by protrusive and adhesive forces. PLoS Computational Biology 2011, 7:1-13.
28. Kabaso D., Gongadze E., Elter P., van Rienen K.U., Gimsa J., Iglič A. Attachment of rod-like (BAR) and membrane shape. Mini-Reviews in Medicinal Chemistry 2011, 11:272-282.
29. Kralj-Iglič V., Heinrich V., Svetina S., Zeks B. Free energy of closed membrane with anisotropic inclusions. The European Physical Journal B 1999, 10:5-8.
30. Kralj-Iglič V., Iglič A., Gomišček G., Sevšek F., Arrigler V., Hägerstrand H. Microtubes and nanotubes of a phospholipid bilayer membrane. Journal of Physics A: Mathematical and General 2002, 35:1533-1549.
31. Lokar M., Iglič A., Veranič P. Protruding membrane nanotubes: attachement of tubular protrusions to adajacent cells by several anchoring junctions. Protoplasma 2010, 246:81-87.
32. Mattila P.K., Pykalainen A., Saarikangas J., Paavilainen V.O., Vihinen H., Jokitalo E., Lappalainen P. Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. Journal of Cell Biology 2007, 176:953-964.
33. Miao L., Fourcade B., Rao M., Wortis M., Zia R.K.P. Equilibrium budding and vesiculation in the curvature model of fluid lipid vesicles. Physical Review E 1991, 43:6843-6856.
34. Millard T.H., Bompard G., Heung M.Y., Dafforn T.R., Scott D.J., Machesky L.M., Futterer K. Structural basis of Filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. The EMBO Journal 2005, 24:240-250.
35. Perutkova Š., Kralj-Iglič V., Frank M., Iglič A. Mechanical stability of membrane nanotubular protrusions influenced by attachment of flexible rod-like proteins. Journal of Biomechanics 2010, 43:1612-1617.
36. Risselada H.J., Marrink S.J., Müller M. Curvature-dependent elastic properties of liquid-ordered domains result in inverted domain sorting on uniaxially compressed vesicles. Physical Review Letters 2011, 106:148102.
37. Rituper B., Davletov B., Zorec R. Lipid-protein interactions in exocytotic release of hormones and neurotransmitters. Clinical Lipidology 2010, 5:747-761.
38. Röper K., Corbeil D., Huttner W.B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nature Cell Biology 2000, 2:582-592.
39. Rustom A., Saffrich R., Markovic I., Walther P., Gerdes H. Nanotubular highways for intercellular organelle transport. Science 2004, 303:1007-1010.
40. Saarikangas J., Zhao H., Pykäläinen A., Laurinmäki P., Mattila P.K., Kinnunen P.K., Butcher S.J., Lappalainen P. Molecular mechanisms of membrane deformation by I-BAR domain proteins. Current Biology 2009, 19:95-107.
41. Scita G., Confalonieri S., Lappalainen P., Suetsugu S. Irsp53: crossing the road of membrane and actin dynamics in the formation of membrane protrusions. Trends in Cell Biology 2008, 18:52-60.
42. Shimada A., Niwa H., Tsujita K., Suetsugu S., Nitta K., et al. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 2007, 129:761-772.
43. Shlomovitz R., Gov N.S. Physical model of contractile ring initiation in dividing cells. Biophysical Journal 2008, 94:1155-1168.
44. Sorre B., Callan-Jones A., Manneville J.B., Nassoy P., Joanny J.-F., Prost J., Goud B., Bassereau P. Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:5622-5626.
45. Tian A., Baumgart T. Sorting of lipids and proteins in membrane curvature gradients. Biophysical Journal 2009, 96:2676-2688.
46. Veksler A., Gov N.S. Phase transitions of the coupled membrane-cytoskeleton modify cellular shape. Biophysical Journal 2007, 93:3798-3810.
47. Veranič P., Lokar M., Schuetz G.J., Weghuber J., Wieser S., Hagerstrand H., Kralj-Iglič V., Iglič A. Different types of cell-to-cell connections mediated by nanotubular structures. Biophysical Journal 2008, 95:4416-4425.
48. Weigmann A., Corbeil D., Hellwig A., Huttner W.B. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 1997, 74:12425-12430.
49. Yang C., Hoelzle M., Disanza A., Scita G., Svitkina T. Coordination of membrane and actin cytoskeleton dynamics during filopodia protrusion. PLoS One 2009, 4:e5678.
50. Zhao H., Pykäläinen A., Lappalainen P. I-BAR domain proteins: linking actin and plasma membrane dynamics. Current Opinion in Cell Biology 2010, 23:1-8.