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Cellular & Molecular Biology Letters logoLink to Cellular & Molecular Biology Letters
. 2009 Jun 25;14(4):636–656. doi: 10.2478/s11658-009-0018-0

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

Karin Schara 1,2, Vid Janša 1, Vid Šuštar 1, Drago Dolinar 1,2, Janez Ivan Pavlič 3,4, Maruša Lokar 4, Veronika Kralj-Iglič 1, Peter Veranič 5, Aleš Iglič 4,
PMCID: PMC6275886  PMID: 19554268

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.

Key words: Membrane nanostructures, Cell-to-cell communication, Microvesicles, Nanotubes, Trousseau syndrome, Heparin

Full Text

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Abbreviations used

cardiolipin

1,1′,2,2′-tetraoleoyl cardiolipin

FITC

fluorescein isothiocyanate

GPVs

giant phospholipid vesicles

HLA, -B, -C

human leukocyte antigens of class I

MHC

major histocompatibility complex

MVs

microvesicles

POPC

1-palmitoyl-2-oleoyl-snglycero-3-phosphocholine

Footnotes

The content of this Review was first presented in a shortened form at the 12th Mejbaum-Katzenellenbogen Seminar “Membrane Skeleton. Recent Advances and Future Research Directions”, June 15–18, 2008, Zakopane, Poland. Publication cost was partially covered by the organizers of this meeting.

References

  • 1.Taylor D.D., Gercel-Taylor C., Jiang C.G., Black P.H. Characterization of plasma membrane shedding from murine melanoma cells. Int. J. Cancer. 1988;41:629–635. doi: 10.1002/ijc.2910410425. [DOI] [PubMed] [Google Scholar]
  • 2.Distler J.H., Pisetsky D.S., Huber L.C., Kalden J.R., Gay S., Distler O. Microparticles as regulators of inflammation: novel players of cellular crosstalk in the rheumatic diseases. Arthritis Rheum. 2005;52:3337–3348. doi: 10.1002/art.21350. [DOI] [PubMed] [Google Scholar]
  • 3.Ratajczak J., Wysoczynski M., Hayek F., Janowska-Wieczorek A., Ratajczak M.Z. Membrane-derived microvesicles (MV): important and underappreciated mediators of cell to cell communication. Leukemia. 2006;20:1487–1495. doi: 10.1038/sj.leu.2404296. [DOI] [PubMed] [Google Scholar]
  • 4.Greenwalt T.J. The how and why of exocytic vesicles. Transfusion. 2006;46:143–152. doi: 10.1111/j.1537-2995.2006.00692.x. [DOI] [PubMed] [Google Scholar]
  • 5.del Conde I., Shrimpton C.N., Thiagarajan P., Lopez J.A. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood. 2005;106:1604–1611. doi: 10.1182/blood-2004-03-1095. [DOI] [PubMed] [Google Scholar]
  • 6.Sprong H., van der Sluijs P., Meer G. How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2001;2:504–513. doi: 10.1038/35080071. [DOI] [PubMed] [Google Scholar]
  • 7.Rustom A., Saffrich R., Marković I., Walther P., Gerdes H.H. Nanotubular highways for intercellular organelle transport. Science. 2004;303:1007–1010. doi: 10.1126/science.1093133. [DOI] [PubMed] [Google Scholar]
  • 8.Iglič A., Fošnarič M., Hägerstrand H., Kralj-Iglič V. Coupling between vesicle shape and the non-homogeneous lateral distribution of membrane constituents in Golgi bodies. FEBS Lett. 2004;574:9–12. doi: 10.1016/j.febslet.2004.07.085. [DOI] [PubMed] [Google Scholar]
  • 9.Veranič P., Lokar M., Schütz G. J., Weghuber J., Wieser S., Hägerstrand H., Kralj-Iglič V., Iglič A. Different types of cell-to-cell connections mediated by nanotubular structures. Biophys. J. 2008;95:4416–4425. doi: 10.1529/biophysj.108.131375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Huttner W.B., Schmidt A.A. Membrane curvature: a case of endofeelin’. Trends Cell Biol. 2002;12:155–158. doi: 10.1016/S0962-8924(02)02252-3. [DOI] [PubMed] [Google Scholar]
  • 11.Sens P., Turner M.S. The forces that shape caveolae. In: Fielding C.J., editor. Lipid rafts and caveolae. Wiley-VCH Verlag: Weinheim; 2006. pp. 25–44. [Google Scholar]
  • 12.Staneva G., Seigneuret M., Koumanov K., Trugnan G., Angelova M.I. Detergents induce raft-like domains budding and fission from giant unilamellar heterogeneous vesicles. A direct microscopy observation. Chem. Phys. Lipids. 2005;136:55–66. doi: 10.1016/j.chemphyslip.2005.03.007. [DOI] [PubMed] [Google Scholar]
  • 13.Iglič A., Babnik B., Bohinc K., Fosnarič M., Hägerstrand H., 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. 2007;40:579–585. doi: 10.1016/j.jbiomech.2006.02.006. [DOI] [PubMed] [Google Scholar]
  • 14.Janich P., Corbeil D. GM1 and GM3 gangliosides highlight distinc lipid microdomains with the apical domain of epithelial cells. FEBS Lett. 2007;581:1783–1787. doi: 10.1016/j.febslet.2007.03.065. [DOI] [PubMed] [Google Scholar]
  • 15.Hägerstrand H., Mrówczyñska L., Salzer U., Prohaska R., Michelsen K., Kralj-Iglič V., Iglič A. Curvature-dependent lateral distribution of raft markers in the human erythrocyte membrane. Mol. Membr. Biol. 2006;23:277–288. doi: 10.1080/09687860600682536. [DOI] [PubMed] [Google Scholar]
  • 16.Holopainen J.M., Angelova M.I., Kinnunen P.K.J. Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys. J. 2000;78:830–838. doi: 10.1016/S0006-3495(00)76640-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Zimmerberg J., Kozlov M.M. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 2006;7:9–19. doi: 10.1038/nrm1784. [DOI] [PubMed] [Google Scholar]
  • 18.Huttner W.B., Zimmerberg J. Implications of lipid microdomains for membrane curvature, budding and fission. Commentary. Curr. Opin. Cell Biol. 2001;13:478–484. doi: 10.1016/S0955-0674(00)00239-8. [DOI] [PubMed] [Google Scholar]
  • 19.Iglič A., Hägerstrand H., Veranič P., Plemenitaš A., Kralj-Iglič V. Curvature induced accumulation of anisotropic membrane components and raft formation in cylindrical membrane protrusions. J. Theor. Biol. 2006;240:368–373. doi: 10.1016/j.jtbi.2005.09.020. [DOI] [PubMed] [Google 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.
  • 21.Müller I., Klocke A., Alex M., Kotzsch M., Luther T., Morgensternm E. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J. 2003;17:476–478. doi: 10.1096/fj.02-0574fje. [DOI] [PubMed] [Google Scholar]
  • 22.Sims P.J., Wiedmer T., Esmon C.T., Weiss H.J., 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. 1989;264:17049–17057. [PubMed] [Google Scholar]
  • 23.Martínez M.C., Tesse A., Zobairi F., Andriantsitohaina R. Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am. J. Physiol. Heart Circ. Physiol. 2005;288:H1004–H1009. doi: 10.1152/ajpheart.00842.2004. [DOI] [PubMed] [Google Scholar]
  • 24.Whiteside T.L. Tumour-derived exosomes or microvesicles: another mechanism of tumour escape from the host immune system? Br. J. Cancer. 2005;92:209–211. doi: 10.1038/sj.bjc.6602360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Cerri C., Chimenti D., Conti I., Neri T., Paggiaro P., Celi A. Monocyte/macrophage-derived microparticles up-regulate inflammatory mediator synthesis by human airway epithelial cells. J. Immunol. 2006;177:1975–1980. doi: 10.4049/jimmunol.177.3.1975. [DOI] [PubMed] [Google Scholar]
  • 26.Diamant M., Tushuizen M.E., Sturk A., Nieuwland R. Cellular microparticles: new players in the field of vascular disease? Eur. J. Clin. Invest. 2004;34:392–401. doi: 10.1111/j.1365-2362.2004.01355.x. [DOI] [PubMed] [Google Scholar]
  • 27.Janowska-Wieczorek A., Marquez-Curtis L.A., Wysoczynski M., Ratajczak M.Z. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion. 2006;46:1199–1209. doi: 10.1111/j.1537-2995.2006.00871.x. [DOI] [PubMed] [Google Scholar]
  • 28.Janša R., Šuštar V., Frank M., Sušan P., Bešter J., Manèek-Keber M., Kržan M., 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. 2008;41:124–132. doi: 10.1016/j.bcmd.2008.01.009. [DOI] [PubMed] [Google Scholar]
  • 29.Coltel N., Combes V., Wassmer S.C., Chimini G., Grau G.E. Cell vesiculation and immunopathology: implications in cerebral malaria. Microbes Infect. 2006;8:2305–2316. doi: 10.1016/j.micinf.2006.04.006. [DOI] [PubMed] [Google Scholar]
  • 30.Berckmans R.J., Nieuwland R., Tak P.P., Böing A.N., Romijn F.P., Kraan M.C. Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII-dependent mechanism. Arthritis Rheum. 2002;46:2857–2866. doi: 10.1002/art.10587. [DOI] [PubMed] [Google Scholar]
  • 31.Brogan P.A., Shah V., Brachet C., Harnden A., Mant D., Klein N. Endothelial and platelet microparticles in vasculitis of the young. Arthritis Rheum. 2004;50:927–936. doi: 10.1002/art.20199. [DOI] [PubMed] [Google Scholar]
  • 32.Combes V., Simon A.C., Grau G.E., Arnoux D., Camoin L., Sabatier F. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J. Clin. Invest. 1999;104:93–102. doi: 10.1172/JCI4985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Dignat-George F., Camoin-Jau L., Sabatier F., Arnoux D., Anfosso F., Bardin N. Endothelial microparticles: a potential contribution to the thrombotic complications of the antiphospholipid syndrome. Thromb. Haemost. 2004;91:667–673. doi: 10.1160/TH03-07-0487. [DOI] [PubMed] [Google Scholar]
  • 34.Morel O., Jesel L., Freyssinet J.M., Toti F. Elevated levels of procoagulant microparticles in a patient with myocardial infarction, antiphospholipid antibodies and multifocal cardiac thrombosis. Thromb. J. 2005;3:15/1–5. doi: 10.1186/1477-9560-3-15. [DOI] [PMC free article] [PubMed] [Google 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. 1974;71:4457–4461. doi: 10.1073/pnas.71.11.4457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Evans E.A. Bending resistance and chemically induced moments in membrane bilayers. Biophys. J. 1974;14:923–931. doi: 10.1016/S0006-3495(74)85959-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Helfrich W. Blocked lipid exchange in bilayers and its possible influence on the shape of vesicles. Z. Naturforsch [c] 1974;29:510–515. doi: 10.1515/znc-1974-9-1010. [DOI] [PubMed] [Google Scholar]
  • 38.Urbanija J., Tomšič N., Lokar M., Ambrožič A., Čučnik S., Rozman B., Kandušer M., Iglič A., Kralj-Iglič V. Coalescence of phospholipid membranes as a possible origin of anticoagulant effect of serum proteins. Chem. Phys. Lipids. 2007;150:49–57. doi: 10.1016/j.chemphyslip.2007.06.216. [DOI] [PubMed] [Google Scholar]
  • 39.Urbanija J., Babnik B., Frank M., Tomšič N., Rozman B., Kralj-Iglič V., 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. 2008;37:1085–1095. doi: 10.1007/s00249-007-0252-1. [DOI] [PubMed] [Google Scholar]
  • 40.Laradji M., Kumar P.B.S. Dynamics of domain growth in selfassembled fluid vesicles. Phys. Rev. Lett. 2004;93:198105/1–4. doi: 10.1103/PhysRevLett.93.198105. [DOI] [PubMed] [Google Scholar]
  • 41.Diamant M., Nieuwland R., Pablo R.F., Sturk A., Smit W., 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. 2002;106:2442–2447. doi: 10.1161/01.CIR.0000036596.59665.C6. [DOI] [PubMed] [Google Scholar]
  • 42.Singer S.J., Nicholson G.L. The fluid mosaic model of the structure of cell membranes. Science. 1972;175:720–731. doi: 10.1126/science.175.4023.720. [DOI] [PubMed] [Google Scholar]
  • 43.Isomaa B., Hagerstrand H., Paatero G. Shape transformations induced by amphiphiles in erythrocytes. Biochim. Biophys. Acta. 1987;899:93–103. doi: 10.1016/0005-2736(87)90243-4. [DOI] [PubMed] [Google Scholar]
  • 44.Hagerstrand H., Isomaa B. Morphological characterization of exovesicles and endovesicles released from human erythrocytes following treatment with amphiphiles. Biochim. Biophys. Acta. 1992;1109:117–126. doi: 10.1016/0005-2736(92)90074-V. [DOI] [PubMed] [Google Scholar]
  • 45.Kralj-Iglič V., Iglič A., Hagerstrand H., Peterlin P. Stable tabular microexovesicles of the erythrocyte membrane induced by dimeric amphiphiles. Phys. Rev. E. 2000;61:4230–4234. doi: 10.1103/PhysRevE.61.4230. [DOI] [PubMed] [Google Scholar]
  • 46.Kralj-Iglič V., Hagerstrand H., Bobrowska-Hagerstrand M., Iglič A. Hypothesis on nanostructures of cell and phospholipid membranes as cell infrastructure. Med. Razgl. 2005;44:155–169. [Google Scholar]
  • 47.Urbanija J., Bohinc K., Bellen A., Maset S., Iglič A., Kralj-Iglič V., Sunil Kumar P.B. Attraction between negatively charged surfaces mediated by spherical counterions with quadrupolar charge distribution. J. Chem. Phys. 2008;129:105101. doi: 10.1063/1.2972980. [DOI] [PubMed] [Google Scholar]
  • 48.Önfelt B., Nedvetzki S., Yanagi K., Davis D.M. Cutting edge: Membrane nanotubes connect immune cells. J. Immunol. 2004;173:1511–1513. doi: 10.4049/jimmunol.173.3.1511. [DOI] [PubMed] [Google Scholar]
  • 49.Vidulescu C., Clejan S., O’Connor K.C. Vesicle traffic through intercellular bridges in DU 145 human prostate cancer cells. J. Cell Mol. Med. 2004;8:388–396. doi: 10.1111/j.1582-4934.2004.tb00328.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Gerdes H.H., Carvalho R.N. Intercellular transfer mediated by tunneling nanotubes. Curr. Opin. Cell Biol. 2008;20:470–475. doi: 10.1016/j.ceb.2008.03.005. [DOI] [PubMed] [Google Scholar]
  • 51.Gurke S., Barroso J.F., Gerdes H.H. The art of cellular communication: tunneling nanotubes bridge the divide. Histochem. Cell Biol. 2008;129:539–550. doi: 10.1007/s00418-008-0412-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Davis D.M., Sowinski S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nat. Rev. Mol. Cell Biol. 2008;9:431–436. doi: 10.1038/nrm2399. [DOI] [PubMed] [Google Scholar]
  • 53.Sherer N.M., Mothes W. Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis. Trends Cell Biol. 2008;9:414–420. doi: 10.1016/j.tcb.2008.07.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Mitchison T.J. Actin based motility on retraction fibers in mitotic PtK2 cells. Cell Motil. Cytoskeleton. 1992;22:135–151. doi: 10.1002/cm.970220207. [DOI] [PubMed] [Google Scholar]
  • 55.Magin T.M., Vijayaraj P., Leube R.E. Structural and regulatory functions of keratins. Exp. Cell Res. 2007;313:2021–2032. doi: 10.1016/j.yexcr.2007.03.005. [DOI] [PubMed] [Google Scholar]
  • 56.Watkins S.C., Salter R.D. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity. 2005;23:309–318. doi: 10.1016/j.immuni.2005.08.009. [DOI] [PubMed] [Google Scholar]
  • 57.Vignjevic D., Kojima S., Aratyn Y., Danciu O., Svitkina T., Borisy G.G. Role of fascin in filopodial protrusion. J. Cell Biol. 2006;174:863–875. doi: 10.1083/jcb.200603013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 1997;387:569–572. doi: 10.1038/42408. [DOI] [PubMed] [Google Scholar]
  • 59.Brown D.A., London E. Function of lipid rafts in biological membranes. Annu. Rev. Cell Biol. 1998;14:111–136. doi: 10.1146/annurev.cellbio.14.1.111. [DOI] [PubMed] [Google Scholar]
  • 60.Causeret M., Taulet N., Comunale F., Favard C., Gauthier-Rouvière C. N-cadherin association with lipid rafts regulates its dynamic assembly at cell-cell junctions in C2C12 myoblasts. Mol. Biol. Cell. 2005;16:2168–2180. doi: 10.1091/mbc.E04-09-0829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Laidler P., Gil D., Pituch-Noworolska A., Ciołczyk D., Ksiazek D., Przybyło M., Lityńska A. Expression of beta1-integrins and N-cadherin in bladder cancer and melanoma cell lines. Acta Biochim. Pol. 2000;47:1159–1170. [PubMed] [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., Davis D.M. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 2008;10:211–219. doi: 10.1038/ncb1682. [DOI] [PubMed] [Google Scholar]
  • 63.Koyanagi M., Brandes R.P., Haendeler J., Zeiher A.M., Dimmeler S. Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: a novel mechanism for cell fate changes? Circ. Res. 2005;96:1039–1041. doi: 10.1161/01.RES.0000168650.23479.0c. [DOI] [PubMed] [Google 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.
  • 65.Harder T., Scheiffele P., Verkade P., Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 1998;141:929–942. doi: 10.1083/jcb.141.4.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Neumann-Giesen C., Falkenbach B., Beicht P., Claasen S., Lüers G., Stuermer C.A., Herzog V., 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. 2004;378:509–518. doi: 10.1042/BJ20031100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67.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. doi: 10.1034/j.1600-0854.2001.020202.x. [DOI] [PubMed] [Google Scholar]
  • 68.Röper K., Corbeil D., Huttner W.B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nat. Cell Biol. 2000;2:582–592. doi: 10.1038/35023524. [DOI] [PubMed] [Google Scholar]
  • 69.Rajendran L., Masilamani M., Solomon S., Tikkanen R., Stuermer C.A., Plattner H., Illges H. Asymmetric localization of flotillins/reggies in preaseembled platforms confers inherent polarity to hematopoietic cells. Proc. Natl. Acad. Sci. USA. 2003;100:8241–8246. doi: 10.1073/pnas.1331629100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Hägerstrand H., Mrówczyñska L. Pathching of ganglioside(M1) in human erythrocytes — distribution of CD47 and CD59 in patched and curved membrane. Mol. Membr. Biol. 2008;25:258–265. doi: 10.1080/09687680802043638. [DOI] [PubMed] [Google 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. 1984;99:2260–2267. doi: 10.1083/jcb.99.6.2260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Iglič A., Lokar M., Babnik B., Slivnik T., Veranič P., Hägerstrand H., Kralj-Iglič V. Possible role of flexible red blood cell membrane nanodomains in the growth and stability of membrane nanotubes. Blood Cells Mol. Dis. 2007;39:14–23. doi: 10.1016/j.bcmd.2007.02.013. [DOI] [PubMed] [Google Scholar]
  • 73.Samuel B.U., Mohandas N., Harrison T., McManus H., Rosse W., Reid M., Haldar K. The role of cholesterol and glycosylphosphatidylinositolanchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J. Biol. Chem. 2001;276:29319–29329. doi: 10.1074/jbc.M101268200. [DOI] [PubMed] [Google Scholar]
  • 74.Salzer U., Prohaska R. Segregation of lipid raft proteins during calcium-induced vesiculation of erythrocytes. Blood. 2003;101:3751–3753. doi: 10.1182/blood-2002-12-3708. [DOI] [PubMed] [Google Scholar]
  • 75.Salzer U., Hinterdorfer P., Hunger U., Borken C., Prohaska R. Ca2+- dependent vesicle release from erythrocytes involves stomatin-specific lipid rafts, aynexin (annexin VII), and sorcin. Blood. 2002;99:2569–2577. doi: 10.1182/blood.V99.7.2569. [DOI] [PubMed] [Google Scholar]
  • 76.Sens P., Turner M.S. Theoretical model for the formation of caveolae and similar membrane invaginations. Biophys. J. 2004;86:2049–2057. doi: 10.1016/S0006-3495(04)74266-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Harder T., Simons K. Caveolae, DUGs, and the dynamcs of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 1997;9:534–542. doi: 10.1016/S0955-0674(97)80030-0. [DOI] [PubMed] [Google Scholar]
  • 78.Brown D.A., London E. Structure and origin of ordered lipid domains in biological membranes. J. Membrane Biol. 1998;164:103–114. doi: 10.1007/s002329900397. [DOI] [PubMed] [Google Scholar]
  • 79.Wang Y., Thiele C., Huttner W.B. Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic. 2000;1:952–962. doi: 10.1034/j.1600-0854.2000.011205.x. [DOI] [PubMed] [Google Scholar]
  • 80.Thiele C., Hannah M.J., Fahrenholz F., Huttner W.B. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2000;2:42–49. doi: 10.1038/71366. [DOI] [PubMed] [Google Scholar]
  • 81.Roelofsen B., Kuypers F.A., Op den Kamp J.A.F., Deenen L.L.M. Influence of phosphatidylcholine molecular species composition on stability of the erythrocyte membrane. Biochem. Soc. Trans. 1989;17:284–286. doi: 10.1042/bst0170284. [DOI] [PubMed] [Google Scholar]
  • 82.Gimsa U., Iglič A., Fiedler S., Zwanzig M., Kralj-Iglič V., Jonas L., Gimsa J. Actin is not required for nanotubular protrusions of primary astrocytes grown on metal nano-lawn. Mol. Membr. Biol. 2007;24:243–255. doi: 10.1080/09687860601141730. [DOI] [PubMed] [Google Scholar]
  • 83.Wang W., Yang L., Huang H.W. Evidence of cholesterol accumulated in high curvature regions: Implication to the curvature elastic energy for lipid mixtures. Biophys. J. 2007;92:2819–2830. doi: 10.1529/biophysj.106.097923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 84.Frank M., Manèek-Keber M., Kržan M., Sodin-Šemrl S., Jerala R., Iglič A., Rozman B., 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. 2008;7:240–245. doi: 10.1016/j.autrev.2007.11.015. [DOI] [PubMed] [Google Scholar]
  • 85.Varki A. Trousseau’s syndrome: multiple definitions and multiple mechanisms. Blood. 2007;110:1723–1729. doi: 10.1182/blood-2006-10-053736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 86.Borsig L. Non-anticoagulant effects of heparin in carcinoma metastasis and Trousseau’s syndrome. Pathophysiol. Haemost. Thromb. 2003;33(suppl1):64–66. doi: 10.1159/000073298. [DOI] [PubMed] [Google Scholar]

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