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

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.

Abbreviations

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

References

  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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google Scholar 

  4. Greenwalt, T.J. The how and why of exocytic vesicles. Transfusion 46 (2006) 143–152.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google Scholar 

  10. Huttner, W.B. and Schmidt, A.A. Membrane curvature: a case of endofeelin’. Trends Cell Biol. 12 (2002) 155–158.

    PubMed  Article  CAS  Google 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.

    Chapter  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google Scholar 

  17. Zimmerberg, J. and Kozlov, M.M. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7 (2006) 9–19.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  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. and Morgensternm, E. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J. 17 (2003) 476–478.

    PubMed  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.

    PubMed  CAS  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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  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.

    Article  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 71 (1974) 4457–4461.

    PubMed  Article  CAS  Google Scholar 

  36. Evans, E.A. Bending resistance and chemically induced moments in membrane bilayers. Biophys. J. 14 (1974) 923–931.

    PubMed  Article  CAS  Google 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.

    CAS  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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    Article  CAS  Google 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.

    PubMed  Article  CAS  Google Scholar 

  42. Singer, S.J. and Nicholson, G.L. The fluid mosaic model of the structure of cell membranes. Science 175 (1972) 720–731.

    PubMed  Article  CAS  Google Scholar 

  43. Isomaa, B., Hagerstrand, H. and Paatero, G. Shape transformations induced by amphiphiles in erythrocytes. Biochim. Biophys. Acta 899 (1987) 93–103.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Google 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.

    PubMed  Article  Google Scholar 

  50. Gerdes, H.H. and Carvalho, R.N. Intercellular transfer mediated by tunneling nanotubes. Curr. Opin. Cell Biol. 20 (2008) 470–475.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    Article  Google Scholar 

  54. Mitchison, T.J. Actin based motility on retraction fibers in mitotic PtK2 cells. Cell Motil. Cytoskeleton 22 (1992) 135–151.

    PubMed  Article  CAS  Google Scholar 

  55. Magin, T.M., Vijayaraj, P. and Leube, R.E. Structural and regulatory functions of keratins. Exp. Cell Res. 313 (2007) 2021–2032.

    PubMed  Article  CAS  Google Scholar 

  56. Watkins, S.C. and Salter, R.D. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 23 (2005) 309–318.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google Scholar 

  58. Simons, K. and Ikonen, E. Functional rafts in cell membranes. Nature 387 (1997) 569–572.

    PubMed  Article  CAS  Google Scholar 

  59. Brown, D.A. and London, E. Function of lipid rafts in biological membranes. Annu. Rev. Cell Biol. 14 (1998) 111–136.

    Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  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. and Simons, K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141 (1998) 929–942.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  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. 99 (1984) 2260–2267.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google Scholar 

  74. Salzer, U. and Prohaska, R. Segregation of lipid raft proteins during calcium-induced vesiculation of erythrocytes. Blood 101 (2003) 3751–3753.

    Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google Scholar 

  77. Harder, T. and Simons, K. Caveolae, DUGs, and the dynamcs of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9 (1997) 534–542.

    PubMed  Article  CAS  Google 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.

    Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google Scholar 

  85. Varki, A. Trousseau’s syndrome: multiple definitions and multiple mechanisms. Blood 110 (2007) 1723–1729.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google Scholar 

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Correspondence to Aleš Iglič.

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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.

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Schara, K., Janša, V., Šuštar, V. et al. Mechanisms for the formation of membranous nanostructures in cell-to-cell communication. Cell Mol Biol Lett 14, 636–656 (2009). https://doi.org/10.2478/s11658-009-0018-0

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  • DOI: https://doi.org/10.2478/s11658-009-0018-0

Key words

  • Membrane nanostructures
  • Cell-to-cell communication
  • Microvesicles
  • Nanotubes
  • Trousseau syndrome
  • Heparin