The Library

Theoretical model for the formation of caveolae and similar membrane invaginations

Tools

Sens, Pierre and Turner, Matthew S. . (2004) Theoretical model for the formation of caveolae and similar membrane invaginations. Biophysical Journal, Vol.86 (No.4). pp. 2049-2057. ISSN 0006-3495

Preview

PDF
WRAP_sens_theorecical_model.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader
Download (175Kb)

Official URL: http://dx.doi.org/10.1016/S0006-3495(04)74266-6

Abstract

We study a physical model for the formation of bud-like invaginations on fluid lipid membranes under tension, and apply this model to caveolae formation. We demonstrate that budding can be driven by membrane-bound proteins, provided that they exert asymmetric forces on the membrane that give rise to bending moments. In particular, caveolae formation does not necessarily require forces to be applied by the cytoskeleton. Our theoretical model is able to explain several features observed experimentally in caveolae, where proteins in the caveolin family are known to play a crucial role in the formation of caveolae buds. These include 1), the formation of caveolae buds with sizes in the 100-nm range and 2), that certain N- and C-termini deletion mutants result in vesicles that are an order-of-magnitude larger. Finally, we discuss the possible origin of the morphological striations that are observed on the surfaces of the caveolae.

Item Type:	Journal Article
Subjects:	Q Science > QR Microbiology
Divisions:	Faculty of Science > Physics
Library of Congress Subject Headings (LCSH):	Cell membranes -- Formation, Cell receptors, Proteins, Lipid membranes
Journal or Publication Title:	Biophysical Journal
Publisher:	Biophysical Society
ISSN:	0006-3495
Date:	April 2004
Volume:	Vol.86
Number:	No.4
Page Range:	pp. 2049-2057
Identification Number:	10.1016/S0006-3495(04)74266-6
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Royal Society (Great Britain)
References:	Abramowitz and Stegun, 1984 M. Abramowitz and I.A. Stegun, Pocketbook of Mathematical Functions, Verlag Harri Deutsch, Frankfurt, Germany (1984). Alberts et al., 1994 B. Alberts, D. Bray, J. Lewis, M. Raff, K. Roberts and J. Watson, Molecular Biology of the Cell, Garland, New York (1994). Bickel et al., 2001 T. Bickel, C. Jeppesen and C.M. Marques, Local entropic effects of polymers grafted to soft interfaces, Eur. Phys. J. E. 4 (2001), pp. 33–43. Breidenich et al., 2000 M. Breidenich, R.R. Netz and R. Lipowsky, The shape of polymer-decorated membranes, Europhys. Lett. 49 (2000), pp. 431–437. Daoud and Cotton, 1982 M. Daoud and J.P. Cotton, Star-shaped polymers, J. Phys. I (Fr.). 43 (1982), pp. 531–538. de Gennes, 1991 P.G. de Gennes, Scaling Concepts in Polymer Physics, Cornell University Press, Ithaca, NY (1991). Evans et al., 2003 A. Evans, M.S. Turner and P. Sens, Interactions between proteins bound to biomembranes, Phys. Rev. E. 67 (2003), p. 041907. Evans and Rawicz, 1990 E. Evans and W. Rawicz, Entropy-driven tension and bending elasticity in condensed-fluid membranes, Phys. Rev. Lett. 64 (1990), pp. 2094–2097. Fielding and Fielding, 2000 C.J. Fielding and P.E. Fielding, Cholesterol and caveolae: structural and functional relationships, Biochim. Biophys. Acta 1529 (2000), pp. 210–222. Gilbert et al., 1999 A. Gilbert, J.P. Paccaud, M. Foti, G. Porcheron, J. Balz and J.L. Carpentier, Direct demonstration of the endocytic function of caveolae by a cell-free assay, J. Cell Sci. 112 (1999), pp. 1101–1110. Goulian, 1996 M. Goulian, Inclusions in membranes, Curr. Opin. Colloid Int. 1 (1996), pp. 358–361. Hiergeist et al., 1996 C. Hiergeist, V.A. Indrani and R. Lipowsky, Membranes with anchored polymers at the adsorption transition, Europhys. Lett. 36 (1996), pp. 491–496. Jülicher and Lipowsky, 1996 F. Jülicher and R. Lipowsky, Shape transformations of vesicles with intramembrane domains, Phys. Rev. E. 53 (1996), pp. 2670–2683. Kim and Sung, 1999 Y.W. Kim and W. Sung, Vesicular budding induced by a long and flexible polymer, Europhys. Lett. 47 (1999), pp. 292–297. Kurzchalia and Parton, 1999 T.V. Kurzchalia and R.G. Parton, Membrane microdomains and caveolae, Curr. Opin. Cell Biol. 11 (1999), pp. 424–431. Lasic et al., 2001 D.D. Lasic, R. Joannic, B.C. Keller, P.M. Frederik and L. Auvray, Spontaneous vesiculation, Adv. Colloid Interface Sci. 89–90 (2001), pp. 337–349. Li et al., 1998 S. Li, F. Galbiati, D. Volonté, M. Sargiacomo, J.A. Engelman, K. Das, P.E. Scherer and M.P. Lisanti, Mutational analysis of caveolin-induced vesicle formation. Expression of caveolin-1 recruits caveolin-2 to caveolae membranes, FEBS Lett. 434 (1998), pp. 127–134. Leibler, 1986 S. Leibler, Curvature instability in membranes, J. Phys. I (Fr.). 47 (1986), pp. 507–516. Leibler and Andelman, 1987 S. Leibler and D. Andelman, Ordered and curved meso-structures in membranes and amphiphilic films, J. Phys. I (Fr.). 48 (1987), pp. 2013–2018. View Record in Scopus \| Cited By in Scopus (84) Lipowsky, 1997 R. Lipowsky, Flexible membranes with anchored polymers, Colloids Surf. A. 128 (1997), pp. 255–264. Lisanti et al., 1994 M.P. Lisanti, P.E. Scherer, J. Vidugiriene, Z.L. Tang, A. Hermanowskivosatka, Y.H. Tu, R.F. Cook and M. Sargiacomo, Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease, J. Cell Biol. 126 (1994), pp. 111–126. Mashl and Bruinsma, 1998 R.J. Mashl and R.F. Bruinsma, Spontaneous curvature theory of clathrin-coated membranes, Biophys. J. 74 (1998), pp. 2862–2875. Morris and Homann, 2001 C.E. Morris and U. Homann, Cell surface area regulation and membrane tension, J. Membr. Biol. 179 (2001), pp. 79–102. Mouritsen and Andersen, 1998 O.G. Mouritsen and O.S. Andersen, In Search of a New Biomembrane Model, Biologiske Skrifter, Copenhagen, Denmark (1998). Nicolas, 2002 Nicolas, A. 2002. Polyméres greffés sur une membrane: quelques aspects théoriques. Oh et al., 1998 P. Oh, D.P. McIntosh and J.E. Schnitzer, Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium, J. Cell Biol. 141 (1998), pp. 101–114. Park et al., 2000 H. Park, Y.M. Go, R. Darji, J.W. Choi, M.P. Lisanti, M.C. Maland and H. Jo, Caveolin-1 regulates shear stress-dependent activation of extracellular signal-regulated kinase, Am. J. Physiol. Heart Circ. Physiol. 278 (2000), pp. 1285–1293. Rothberg et al., 1992 K.G. Rothberg, J.E. Heuser, W.C. Donzell, Y.S. Ying, J.R. Glenney and R.G. Anderson, Caveolin, a protein component of caveolae membrane coats, Cell 68 (1992), pp. 673–682. Safran, 1994 S.A. Safran, Statistical Thermodynamics of Surfaces, Interfaces and Membranes, Perseus, Cambridge, MA (1994). Sarasij and Rao, 2002 R. Sarasij and M. Rao, Tilt texture domains on a membrane and chirality induced budding, Phys. Rev. Lett. 88 (2002), p. 088101. Sargiacomo et al., 1995 M. Sargiacomo, P.E. Scherer, Z.L. Tang, E. Kübler, K.S. Song, M.C. Sanders and M.P. Lisanti, Oligomeric structure of caveolin: implications for caveolae membrane organization, Proc. Natl. Acad. Sci. USA 92 (1995), pp. 9407–9411. Schlegel et al., 1998 A. Schlegel, D. Volonté, J.A. Engelman, F. Galbiati, P. Mehta, X.L. Zhang, P.E. Scherer and M.P. Lisanti, Crowded little caves: structure and function of caveolae, Cell. Signal 10 (1998), pp. 457–463. Schlegel and Lisanti, 2000 A. Schlegel and M.P. Lisanti, A molecular dissection of caveolin-1 membrane attachment and oligomerization. Two separate regions of the caveolin-1 C-terminal domain mediate membrane binding and oligomer/oligomer interactions in vivo, J. Biol. Chem. 275 (2000), pp. 21605–21617. Schlegel and Lisanti, 2001 A. Schlegel and M.P. Lisanti, Caveolae and their coat proteins, the caveolins: from electron microscopic novelty to biological launching pad, J. Cell Physiol. 186 (2001), pp. 329–337. Sear et al., 1999 R.P. Sear, S.W. Chung, G. Markovich, W.M. Gelbart and J.R. Heath, Spontaneous patterning of quantum dots at the air-water interface, Phys. Rev. E. 59 (1999), pp. R6255–R6258. Sear and Gelbart, 1999 R.P. Sear and W.M. Gelbart, Microphase separation versus the vapor-liquid transition in systems of spherical particles, J. Chem. Phys. 110 (1999), pp. 4582–4588. Seifert, 1993 U. Seifert, Curvature-induced lateral phase segregation in two-component vesicles, Phys. Rev. Lett. 70 (1993), pp. 1335–1338. Sheetz and Dai, 1996 M.P. Sheetz and J.W. Dai, Modulation of membrane dynamics and cell motility by membrane tension, Trends Cell Biol. 6 (1996), pp. 85–89. Song and Waugh, 1993 J. Song and R.E. Waugh, Bending rigidity of SOPC membranes containing cholesterol, Biophys. J. 64 (1993), pp. 1967–1970. Stahlhut et al., 2000 M. Stahlhut, K. Sandvig and B. van Deurs, Caveolae: uniform structures with multiple functions in signaling, cell growth, and cancer, Exp. Cell Res. 261 (2000), pp. 111–118. Takei and Haucke, 2001 K. Takei and V. Haucke, Clathrin-mediated endocytosis: membrane factors pull the trigger, Trends Cell Biol. 11 (2001), pp. 385–391. Westermann et al., 1999 M. Westermann, H. Leutbecher and H.W. Meyer, Membrane structure of caveolae and isolated caveolin-rich vesicles, Histochem. Cell Biol. 111 (1999), pp. 71–81.
URI:	http://wrap.warwick.ac.uk/id/eprint/911