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Cellular and Molecular Biology Letters

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Volume 14, Issue 4 (Dec 2009)

Mechanisms for the formation of membranous nanostructures in cell-to-cell communication

Karin Schara
  • Laboratory of Clinical Biophysics, Institute of Biophysics, Faculty of Medicine, University of Ljubljana, Lipičeva 2, SI-1000, Ljubljana, Slovenia
  • University Medical Centre Ljubljana, Zaloška 9, SI-1000, Ljubljana, Slovenia
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/ Vid Janša
  • Laboratory of Clinical Biophysics, Institute of Biophysics, Faculty of Medicine, University of Ljubljana, Lipičeva 2, SI-1000, Ljubljana, Slovenia
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/ Vid Šuštar
  • Laboratory of Clinical Biophysics, Institute of Biophysics, Faculty of Medicine, University of Ljubljana, Lipičeva 2, SI-1000, Ljubljana, Slovenia
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/ Drago Dolinar
  • Laboratory of Clinical Biophysics, Institute of Biophysics, Faculty of Medicine, University of Ljubljana, Lipičeva 2, SI-1000, Ljubljana, Slovenia
  • University Medical Centre Ljubljana, Zaloška 9, SI-1000, Ljubljana, Slovenia
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/ Janez Pavlič
  • Faculty of Health Studies, University of Ljubljana, Poljanska 26a, SI-1000, Ljubljana, Slovenia
  • Laboratory of Physics, Faculty of Electrical Engineering, University of Ljubljana, Tržaška 25, SI-1000, Ljubljana, Slovenia
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/ Maruša Lokar
  • Laboratory of Physics, Faculty of Electrical Engineering, University of Ljubljana, Tržaška 25, SI-1000, Ljubljana, Slovenia
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/ Veronika Kralj-Iglič
  • Laboratory of Clinical Biophysics, Institute of Biophysics, Faculty of Medicine, University of Ljubljana, Lipičeva 2, SI-1000, Ljubljana, Slovenia
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/ Peter Veranič
  • Institute of Cell Biology, Faculty of Medicine, University of Ljubljana, Lipičeva 2, SI-1000, Ljubljana, Slovenia
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/ Aleš Iglič
  • Laboratory of Physics, Faculty of Electrical Engineering, University of Ljubljana, Tržaška 25, SI-1000, Ljubljana, Slovenia
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Published Online: 2009-09-10 | DOI: https://doi.org/10.2478/s11658-009-0018-0

Abstract

Cells interact by exchanging material and information. Two methods of cell-to-cell communication are by means of microvesicles and by means of nanotubes. Both microvesicles and nanotubes derive from the cell membrane and are able to transport the contents of the inner solution. In this review, we describe two physical mechanisms involved in the formation of microvesicles and nanotubes: curvature-mediated lateral redistribution of membrane components with the formation of membrane nanodomains; and plasmamediated attractive forces between membranes. These mechanisms are clinically relevant since they can be affected by drugs. In particular, the underlying mechanism of heparin’s role as an anticoagulant and tumor suppressor is the suppression of microvesicluation due to plasma-mediated attractive interaction between membranes.

Keywords: Membrane nanostructures; Cell-to-cell communication; Microvesicles; Nanotubes; Trousseau syndrome; Heparin

  • [1] Taylor, D.D., Gercel-Taylor, C., Jiang, C.G. and Black, P.H. Characterization of plasma membrane shedding from murine melanoma cells. Int. J. Cancer 41 (1988) 629–635. http://dx.doi.org/10.1002/ijc.2910410425CrossrefGoogle Scholar

  • [2] Distler, J.H., Pisetsky, D.S., Huber, L.C., Kalden, J.R., Gay, S. and Distler, O. Microparticles as regulators of inflammation: novel players of cellular crosstalk in the rheumatic diseases. Arthritis Rheum. 52 (2005) 3337–3348. http://dx.doi.org/10.1002/art.21350CrossrefGoogle Scholar

  • [3] Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A. and Ratajczak, M.Z. Membrane-derived microvesicles (MV): important and underappreciated mediators of cell to cell communication. Leukemia 20 (2006) 1487–1495. http://dx.doi.org/10.1038/sj.leu.2404296CrossrefGoogle Scholar

  • [4] Greenwalt, T.J. The how and why of exocytic vesicles. Transfusion 46 (2006) 143–152. http://dx.doi.org/10.1111/j.1537-2995.2006.00692.xCrossrefGoogle Scholar

  • [5] del Conde, I., Shrimpton, C.N., Thiagarajan, P. and Lopez, J.A. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 106 (2005) 1604–1611. http://dx.doi.org/10.1182/blood-2004-03-1095CrossrefGoogle Scholar

  • [6] Sprong, H., van der Sluijs, P. and Meer, G. How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2 (2001) 504–513. http://dx.doi.org/10.1038/35080071CrossrefGoogle Scholar

  • [7] Rustom, A., Saffrich, R., Marković, I., Walther, P. and Gerdes, H.H. Nanotubular highways for intercellular organelle transport. Science 303 (2004) 1007–1010. http://dx.doi.org/10.1126/science.1093133CrossrefGoogle Scholar

  • [8] Iglič, A., Fošnarič, M., Hägerstrand, H. and Kralj-Iglič, V. Coupling between vesicle shape and the non-homogeneous lateral distribution of membrane constituents in Golgi bodies. FEBS Lett. 574 (2004) 9–12. http://dx.doi.org/10.1016/j.febslet.2004.07.085CrossrefGoogle Scholar

  • [9] Veranič, P., Lokar, M., Schütz, G. J., Weghuber, J., Wieser, S., Hägerstrand, H., Kralj-Iglič, V. and Iglič, A. Different types of cell-to-cell connections mediated by nanotubular structures. Biophys. J. 95 (2008) 4416–4425. http://dx.doi.org/10.1529/biophysj.108.131375CrossrefGoogle Scholar

  • [10] Huttner, W.B. and Schmidt, A.A. Membrane curvature: a case of endofeelin’. Trends Cell Biol. 12 (2002) 155–158. http://dx.doi.org/10.1016/S0962-8924(02)02252-3CrossrefGoogle Scholar

  • [11] Sens, P. and Turner, M.S. The forces that shape caveolae. in: Lipid rafts and caveolae (Fielding, C.J., Ed.), Wiley-VCH Verlag, Weinheim, 2006, 25–44. http://dx.doi.org/10.1002/3527608079.ch2Google Scholar

  • [12] Staneva, G., Seigneuret, M., Koumanov, K., Trugnan, G. and Angelova, M.I. Detergents induce raft-like domains budding and fission from giant unilamellar heterogeneous vesicles. A direct microscopy observation. Chem. Phys. Lipids 136 (2005) 55–66. http://dx.doi.org/10.1016/j.chemphyslip.2005.03.007CrossrefGoogle Scholar

  • [13] Iglič, A., Babnik, B., Bohinc, K., Fosnarič, M. Hägerstrand, H. and Kralj-Iglič, V. On the role of anisotropy of membrane constituents in formation of a membrane neck during budding of a multicomponent membrane. J. Biomech. 40 (2007) 579–585. http://dx.doi.org/10.1016/j.jbiomech.2006.02.006CrossrefGoogle Scholar

  • [14] Janich, P. and Corbeil, D. GM1 and GM3 gangliosides highlight distinc lipid microdomains with the apical domain of epithelial cells. FEBS Lett. 581 (2007) 1783–1787. http://dx.doi.org/10.1016/j.febslet.2007.03.065Google Scholar

  • [15] Hägerstrand, H., Mrówczyñska, L., Salzer, U., Prohaska, R., Michelsen, K., Kralj-Iglič, V. and Iglič, A. Curvature-dependent lateral distribution of raft markers in the human erythrocyte membrane. Mol. Membr. Biol. 23 (2006) 277–288. http://dx.doi.org/10.1080/09687860600682536CrossrefGoogle Scholar

  • [16] Holopainen, J.M., Angelova, M.I. and Kinnunen, P.K.J. Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys. J. 78 (2000) 830–838. http://dx.doi.org/10.1016/S0006-3495(00)76640-9CrossrefGoogle Scholar

  • [17] Zimmerberg, J. and Kozlov, M.M. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7 (2006) 9–19. http://dx.doi.org/10.1038/nrm1784CrossrefGoogle Scholar

  • [18] Huttner, W.B. and Zimmerberg, J. Implications of lipid microdomains for membrane curvature, budding and fission. Commentary. Curr. Opin. Cell Biol. 13 (2001) 478–484. http://dx.doi.org/10.1016/S0955-0674(00)00239-8CrossrefGoogle Scholar

  • [19] Iglič, A., Hägerstrand, H., Veranič, P., Plemenitaš, A. and Kralj-Iglič, V. Curvature induced accumulation of anisotropic membrane components and raft formation in cylindrical membrane protrusions. J. Theor. Biol. 240 (2006) 368–373. http://dx.doi.org/10.1016/j.jtbi.2005.09.020CrossrefGoogle Scholar

  • [20] Fošnarič, M., Iglič, A., Slivnik, T. and Kralj-Iglič, V. Flexible membrane inclusions and membrane inclusions induced by rigid globular proteins. in: Advances in planar lipid bilayers and liposomes (Leitmannova Liu, A., Ed.), vol. 7, Elsevier, 2008, 143–168. Google Scholar

  • [21] Müller, I., Klocke, A., Alex, M., Kotzsch, M., Luther, T. and Morgensternm, E. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J. 17 (2003) 476–478. Google Scholar

  • [22] Sims, P.J., Wiedmer, T., Esmon, C.T., Weiss, H.J. and Shattil, S.J. Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane. Studies in Scott syndrome: an isolated defect in platelet procoagulant activity. J. Biol. Chem. 264 (1989) 17049–17057. Google Scholar

  • [23] Martínez, M.C., Tesse, A., Zobairi, F. and Andriantsitohaina, R. Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am. J. Physiol. Heart Circ. Physiol. 288 (2005) H1004–H1009. http://dx.doi.org/10.1152/ajpheart.00842.2004CrossrefGoogle Scholar

  • [24] Whiteside, T.L. Tumour-derived exosomes or microvesicles: another mechanism of tumour escape from the host immune system? Br. J. Cancer 92 (2005) 209–211. http://dx.doi.org/10.1038/sj.bjc.6602360CrossrefGoogle Scholar

  • [25] Cerri, C., Chimenti, D., Conti, I., Neri, T., Paggiaro, P. and Celi, A. Monocyte/macrophage-derived microparticles up-regulate inflammatory mediator synthesis by human airway epithelial cells. J. Immunol. 177 (2006) 1975–1980. Google Scholar

  • [26] Diamant, M., Tushuizen, M.E., Sturk, A. and Nieuwland, R. Cellular microparticles: new players in the field of vascular disease? Eur. J. Clin. Invest. 34 (2004) 392–401. http://dx.doi.org/10.1111/j.1365-2362.2004.01355.xCrossrefGoogle Scholar

  • [27] Janowska-Wieczorek, A., Marquez-Curtis, L.A., Wysoczynski, M. and Ratajczak, M.Z. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion 46 (2006) 1199–1209. http://dx.doi.org/10.1111/j.1537-2995.2006.00871.xCrossrefGoogle Scholar

  • [28] Janša, R., Šuštar, V., Frank, M., Sušan, P., Bešter, J., Manèek-Keber, M., Kržan, M. and Iglič A. Number of microvesicles in peripheral blood and ability of plasma to induce adhesion between phospholipid membranes in 19 patients with gastrointestinal diseases. Blood Cells Mol. Dis. 41 (2008) 124–132. http://dx.doi.org/10.1016/j.bcmd.2008.01.009CrossrefGoogle Scholar

  • [29] Coltel, N., Combes, V., Wassmer, S.C., Chimini, G. and Grau, G.E. Cell vesiculation and immunopathology: implications in cerebral malaria. Microbes Infect. 8 (2006) 2305–2316. http://dx.doi.org/10.1016/j.micinf.2006.04.006CrossrefGoogle Scholar

  • [30] Berckmans, R.J., Nieuwland, R., Tak, P.P., Böing, A.N., Romijn, F.P. and Kraan, M.C. Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII-dependent mechanism. Arthritis Rheum. 46 (2002) 2857–2866. http://dx.doi.org/10.1002/art.10587CrossrefGoogle Scholar

  • [31] Brogan, P.A., Shah, V., Brachet, C., Harnden, A., Mant, D. and Klein, N. Endothelial and platelet microparticles in vasculitis of the young. Arthritis Rheum. 50 (2004) 927–936. http://dx.doi.org/10.1002/art.20199CrossrefGoogle Scholar

  • [32] Combes, V., Simon, A.C., Grau, G.E., Arnoux, D., Camoin, L. and Sabatier, F. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J. Clin. Invest. 104 (1999) 93–102. http://dx.doi.org/10.1172/JCI4985CrossrefGoogle Scholar

  • [33] Dignat-George, F., Camoin-Jau, L., Sabatier, F., Arnoux, D., Anfosso, F. and Bardin, N. Endothelial microparticles: a potential contribution to the thrombotic complications of the antiphospholipid syndrome. Thromb. Haemost. 91 (2004) 667–673. Google Scholar

  • [34] Morel, O., Jesel, L., Freyssinet, J.M. and Toti, F. Elevated levels of procoagulant microparticles in a patient with myocardial infarction, antiphospholipid antibodies and multifocal cardiac thrombosis. Thromb. J. 3 (2005) 15/1–5. http://dx.doi.org/10.1186/1477-9560-3-15CrossrefGoogle Scholar

  • [35] Sheetz, M.P., Singer, S.J. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA 71 (1974) 4457–4461. http://dx.doi.org/10.1073/pnas.71.11.4457CrossrefGoogle Scholar

  • [36] Evans, E.A. Bending resistance and chemically induced moments in membrane bilayers. Biophys. J. 14 (1974) 923–931. http://dx.doi.org/10.1016/S0006-3495(74)85959-XCrossrefGoogle Scholar

  • [37] Helfrich, W. Blocked lipid exchange in bilayers and its possible influence on the shape of vesicles. Z. Naturforsch [c] 29 (1974) 510–515. Google Scholar

  • [38] Urbanija, J., Tomšič, N., Lokar, M., Ambrožič, A. and Čučnik, S., Rozman, B., Kandušer, M., Iglič, A. and Kralj-Iglič, V. Coalescence of phospholipid membranes as a possible origin of anticoagulant effect of serum proteins. Chem. Phys. Lipids 150 (2007) 49–57. http://dx.doi.org/10.1016/j.chemphyslip.2007.06.216CrossrefGoogle Scholar

  • [39] Urbanija, J., Babnik, B., Frank, M., Tomšič, N., Rozman, B., Kralj-Iglič, V. and Iglič, A. Attachment of β2-glycoprotein I to negatively charged liposomes may prevent the release of daughter vesicles from the parent membrane. Eur. Biophys. J. 37 (2008) 1085–1095. http://dx.doi.org/10.1007/s00249-007-0252-1CrossrefGoogle Scholar

  • [40] Laradji, M., and Kumar, P.B.S. Dynamics of domain growth in selfassembled fluid vesicles. Phys. Rev. Lett. 93 (2004) 198105/1–4. http://dx.doi.org/10.1103/PhysRevLett.93.198105CrossrefGoogle Scholar

  • [41] Diamant, M., Nieuwland, R., Pablo, R.F., Sturk, A., Smit, W. and Radder, J.K. Elevated numbers of tissue-factor exposed in microparticles correlate with components of the metabolic syndrome in uncomplicated type 2 diabetes mellitus. Circulation 106 (2002) 2442–2447. http://dx.doi.org/10.1161/01.CIR.0000036596.59665.C6CrossrefGoogle Scholar

  • [42] Singer, S.J. and Nicholson, G.L. The fluid mosaic model of the structure of cell membranes. Science 175 (1972) 720–731. http://dx.doi.org/10.1126/science.175.4023.720CrossrefGoogle Scholar

  • [43] Isomaa, B., Hagerstrand, H. and Paatero, G. Shape transformations induced by amphiphiles in erythrocytes. Biochim. Biophys. Acta 899 (1987) 93–103. http://dx.doi.org/10.1016/0005-2736(87)90243-4CrossrefGoogle Scholar

  • [44] Hagerstrand, H. and Isomaa, B. Morphological characterization of exovesicles and endovesicles released from human erythrocytes following treatment with amphiphiles. Biochim. Biophys. Acta 1109 (1992) 117–126. http://dx.doi.org/10.1016/0005-2736(92)90074-VCrossrefGoogle Scholar

  • [45] Kralj-Iglič, V., Iglič, A., Hagerstrand, H. and Peterlin, P. Stable tabular microexovesicles of the erythrocyte membrane induced by dimeric amphiphiles. Phys. Rev. E 61 (2000) 4230–4234. http://dx.doi.org/10.1103/PhysRevE.61.4230CrossrefGoogle Scholar

  • [46] Kralj-Iglič, V., Hagerstrand, H., Bobrowska-Hagerstrand, M. and Iglič, A. Hypothesis on nanostructures of cell and phospholipid membranes as cell infrastructure. Med. Razgl. 44 (2005) 155–169. Google Scholar

  • [47] Urbanija, J., Bohinc, K., Bellen, A., Maset, S., Iglič, A., Kralj-Iglič, V. and Sunil Kumar, P.B. Attraction between negatively charged surfaces mediated by spherical counterions with quadrupolar charge distribution. J. Chem. Phys. 129 (2008) 105101. http://dx.doi.org/10.1063/1.2972980CrossrefGoogle Scholar

  • [48] Önfelt, B., Nedvetzki, S., Yanagi, K. and Davis, D.M. Cutting edge: Membrane nanotubes connect immune cells. J. Immunol. 173 (2004) 1511–1513. CrossrefGoogle Scholar

  • [49] Vidulescu, C., Clejan, S. and O’Connor, K.C. Vesicle traffic through intercellular bridges in DU 145 human prostate cancer cells. J. Cell Mol. Med. 8 (2004) 388–396. http://dx.doi.org/10.1111/j.1582-4934.2004.tb00328.xCrossrefGoogle Scholar

  • [50] Gerdes, H.H. and Carvalho, R.N. Intercellular transfer mediated by tunneling nanotubes. Curr. Opin. Cell Biol. 20 (2008) 470–475. http://dx.doi.org/10.1016/j.ceb.2008.03.005CrossrefGoogle Scholar

  • [51] Gurke, S., Barroso, J.F. and Gerdes, H.H. The art of cellular communication: tunneling nanotubes bridge the divide. Histochem. Cell Biol. 129 (2008) 539–550. http://dx.doi.org/10.1007/s00418-008-0412-0CrossrefGoogle Scholar

  • [52] Davis, D.M. and Sowinski. S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nat. Rev. Mol. Cell Biol. 9 (2008) 431–436. http://dx.doi.org/10.1038/nrm2399CrossrefGoogle Scholar

  • [53] Sherer, N.M. and Mothes, W. Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis. Trends Cell Biol. 9 (2008) 414–420. http://dx.doi.org/10.1016/j.tcb.2008.07.003CrossrefGoogle Scholar

  • [54] Mitchison, T.J. Actin based motility on retraction fibers in mitotic PtK2 cells. Cell Motil. Cytoskeleton 22 (1992) 135–151. http://dx.doi.org/10.1002/cm.970220207CrossrefGoogle Scholar

  • [55] Magin, T.M., Vijayaraj, P. and Leube, R.E. Structural and regulatory functions of keratins. Exp. Cell Res. 313 (2007) 2021–2032. http://dx.doi.org/10.1016/j.yexcr.2007.03.005CrossrefGoogle Scholar

  • [56] Watkins, S.C. and Salter, R.D. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 23 (2005) 309–318. http://dx.doi.org/10.1016/j.immuni.2005.08.009CrossrefGoogle Scholar

  • [57] Vignjevic, D., Kojima, S., Aratyn, Y., Danciu, O., Svitkina, T. and Borisy, G.G. Role of fascin in filopodial protrusion. J. Cell Biol. 174 (2006) 863–875. http://dx.doi.org/10.1083/jcb.200603013CrossrefGoogle Scholar

  • [58] Simons, K. and Ikonen, E. Functional rafts in cell membranes. Nature 387 (1997) 569–572. http://dx.doi.org/10.1038/42408CrossrefGoogle Scholar

  • [59] Brown, D.A. and London, E. Function of lipid rafts in biological membranes. Annu. Rev. Cell Biol. 14 (1998) 111–136. http://dx.doi.org/10.1146/annurev.cellbio.14.1.111CrossrefGoogle Scholar

  • [60] Causeret, M., Taulet, N., Comunale, F., Favard, C. and Gauthier-Rouvière, C. N-cadherin association with lipid rafts regulates its dynamic assembly at cell-cell junctions in C2C12 myoblasts. Mol. Biol. Cell. 16 (2005) 2168–2180. http://dx.doi.org/10.1091/mbc.E04-09-0829CrossrefGoogle Scholar

  • [61] Laidler, P., Gil, D., Pituch-Noworolska, A., Ciołczyk, D., Ksiazek, D., Przybyło, M. and Lityńska, A. Expression of beta1-integrins and N-cadherin in bladder cancer and melanoma cell lines. Acta Biochim. Pol. 47 (2000) 1159–1170. Google Scholar

  • [62] Sowinski, S., Jolly, C., Berninghausen, O., Purbhoo, M.A., Chauveau, A., K.hler, K., Oddos, S., Eissmann, P., Brodsky, F.M., Hopkins, C., Önfelt, B., Sattentau, Q. and Davis, D.M. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10 (2008) 211–219. http://dx.doi.org/10.1038/ncb1682CrossrefGoogle Scholar

  • [63] Koyanagi, M., Brandes, R.P., Haendeler, J., Zeiher, A.M. and Dimmeler, S. Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: a novel mechanism for cell fate changes? Circ. Res. 96 (2005) 1039–1041. http://dx.doi.org/10.1161/01.RES.0000168650.23479.0cCrossrefGoogle Scholar

  • [64] Kralj-Iglič, V. and Veranič, P. Curvature-induced sorting of bilayer membrane constituents and formation of membrane rafts. in: Advances in planar lipid bilayers and liposomes (Leitmannova Liu, A., Ed.), vol. 5, Elsevier, 2006, 129–149. Google Scholar

  • [65] Harder, T., Scheiffele, P., Verkade, P. and Simons, K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141 (1998) 929–942. http://dx.doi.org/10.1083/jcb.141.4.929CrossrefGoogle Scholar

  • [66] Neumann-Giesen, C., Falkenbach, B., Beicht, P., Claasen, S., Lüers, G., Stuermer, C.A., Herzog, V. and Tikkanen, R. Membrane and raft association of reggie-1/flotilin-2: role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem. J. 378 (2004) 509–518. http://dx.doi.org/10.1042/BJ20031100CrossrefGoogle Scholar

  • [67] Corbeil, D., Röper, K., Fargeas, C.A., Joester, A. and Huttner, W.B. Prominin: A story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2 (2001) 82–91. http://dx.doi.org/10.1034/j.1600-0854.2001.020202.xCrossrefGoogle Scholar

  • [68] Röper, K., Corbeil, D. and Huttner, W.B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nat. Cell Biol. 2 (2000) 582–592. http://dx.doi.org/10.1038/35023524CrossrefGoogle Scholar

  • [69] Rajendran, L., Masilamani, M., Solomon, S., Tikkanen, R., Stuermer, C.A., Plattner, H. and Illges, H. Asymmetric localization of flotillins/reggies in preaseembled platforms confers inherent polarity to hematopoietic cells. Proc. Natl. Acad. Sci. USA 100 (2003) 8241–8246. http://dx.doi.org/10.1073/pnas.1331629100CrossrefGoogle Scholar

  • [70] Hägerstrand, H. and Mrówczyñska, L. Pathching of ganglioside(M1) in human erythrocytes — distribution of CD47 and CD59 in patched and curved membrane. Mol. Membr. Biol. 25 (2008) 258–265. http://dx.doi.org/10.1080/09687680802043638CrossrefGoogle Scholar

  • [71] Kuypers, F.A., Roelofsen, B., Berendsen, W., Op den Kamp, J.A.F., van Deenen, L.L.M. Shape changes in human erythrocytes induced by replacement of the native phosphatidiylcholine with species contatinig various fatty acids. J. Cell. Biol. 99 (1984) 2260–2267. http://dx.doi.org/10.1083/jcb.99.6.2260CrossrefGoogle Scholar

  • [72] Iglič, A., Lokar, M., Babnik, B., Slivnik, T., Veranič, P., Hägerstrand H and Kralj-Iglič, V. Possible role of flexible red blood cell membrane nanodomains in the growth and stability of membrane nanotubes. Blood Cells Mol. Dis. 39 (2007) 14–23. http://dx.doi.org/10.1016/j.bcmd.2007.02.013CrossrefGoogle Scholar

  • [73] Samuel, B.U., Mohandas, N., Harrison, T., McManus, H., Rosse, W., Reid, M. and Haldar, K. The role of cholesterol and glycosylphosphatidylinositolanchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J. Biol. Chem. 276 (2001) 29319–29329. http://dx.doi.org/10.1074/jbc.M101268200CrossrefGoogle Scholar

  • [74] Salzer, U. and Prohaska, R. Segregation of lipid raft proteins during calcium-induced vesiculation of erythrocytes. Blood 101 (2003) 3751–3753. http://dx.doi.org/10.1182/blood-2002-12-3708CrossrefGoogle Scholar

  • [75] Salzer, U., Hinterdorfer, P., Hunger, U., Borken, C. and Prohaska, R. Ca2+- dependent vesicle release from erythrocytes involves stomatin-specific lipid rafts, aynexin (annexin VII), and sorcin. Blood 99 (2002) 2569–2577. http://dx.doi.org/10.1182/blood.V99.7.2569Google Scholar

  • [76] Sens, P. and Turner, M.S. Theoretical model for the formation of caveolae and similar membrane invaginations. Biophys. J. 86 (2004) 2049–2057. http://dx.doi.org/10.1016/S0006-3495(04)74266-6CrossrefGoogle Scholar

  • [77] Harder, T. and Simons, K. Caveolae, DUGs, and the dynamcs of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9 (1997) 534–542. http://dx.doi.org/10.1016/S0955-0674(97)80030-0CrossrefGoogle Scholar

  • [78] Brown, D.A. and London, E. Structure and origin of ordered lipid domains in biological membranes. J. Membrane Biol. 164 (1998) 103–114. http://dx.doi.org/10.1007/s002329900397CrossrefGoogle Scholar

  • [79] Wang, Y., Thiele, C. and Huttner, W.B. Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic 1 (2000) 952–962. http://dx.doi.org/10.1034/j.1600-0854.2000.011205.xCrossrefGoogle Scholar

  • [80] Thiele, C., Hannah, M.J., Fahrenholz, F. and Huttner, W.B. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2 (2000) 42–49. http://dx.doi.org/10.1038/71366CrossrefGoogle Scholar

  • [81] Roelofsen, B., Kuypers, F.A., Op den Kamp, J.A.F. and Deenen, L.L.M. Influence of phosphatidylcholine molecular species composition on stability of the erythrocyte membrane. Biochem. Soc. Trans. 17 (1989) 284–286. CrossrefGoogle Scholar

  • [82] Gimsa, U., Iglič, A., Fiedler, S., Zwanzig, M., Kralj-Iglič, V., Jonas, L. and Gimsa, J. Actin is not required for nanotubular protrusions of primary astrocytes grown on metal nano-lawn. Mol. Membr. Biol. 24 (2007) 243–255. http://dx.doi.org/10.1080/09687860601141730CrossrefGoogle Scholar

  • [83] Wang, W., Yang, L. and Huang, H.W. Evidence of cholesterol accumulated in high curvature regions: Implication to the curvature elastic energy for lipid mixtures. Biophys. J. 92 (2007) 2819–2830. http://dx.doi.org/10.1529/biophysj.106.097923CrossrefGoogle Scholar

  • [84] Frank, M., Manèek-Keber, M., Kržan, M., Sodin-Šemrl, S., Jerala, R., Iglič, A., Rozman, B. and Kralj-Iglič, V. Prevention of microvesiculation by adhesion of buds to the mother cell membrane — a possible anticoagulant effect of healthy donor plasma. Autoimmun. Rev. 7 (2008) 240–245. http://dx.doi.org/10.1016/j.autrev.2007.11.015CrossrefGoogle Scholar

  • [85] Varki, A. Trousseau’s syndrome: multiple definitions and multiple mechanisms. Blood 110 (2007) 1723–1729. http://dx.doi.org/10.1182/blood-2006-10-053736CrossrefGoogle Scholar

  • [86] Borsig, L. Non-anticoagulant effects of heparin in carcinoma metastasis and Trousseau’s syndrome. Pathophysiol. Haemost. Thromb. 33 suppl 1 (2003) 64–66. http://dx.doi.org/10.1159/000073298CrossrefGoogle Scholar

About the article

Published Online: 2009-09-10

Published in Print: 2009-12-01


Citation Information: Cellular and Molecular Biology Letters, ISSN (Online) 1689-1392, DOI: https://doi.org/10.2478/s11658-009-0018-0.

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© 2009 University of Wrocław, Poland. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

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