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The role of extracellular vesicles in phenotypic cancer transformation Cover

The role of extracellular vesicles in phenotypic cancer transformation

Open Access
|Jul 2013

References

  1. 1. Al-Nedawi K, Meehan B, Rak J. Microvesicles: messengers and mediators of tumor progression. Cell Cycle 2009; 8: 2014-18.10.4161/cc.8.13.898819535896
  2. 2. Rak J. Microparticles in cancer. Semin Thromb Hemost 2010; 36: 888-906.10.1055/s-0030-126704321049390
  3. 3. Pap E. The role of microvesicles in malignancies. Adv Exp Med Biol 2011; 714: 183-199.10.1007/978-94-007-0782-5_1021506015
  4. 4. Camussi G, Deregibus MC, Bruno S, Grange C, Fonsato V, Tetta C. Exosome/ microvesicle-mediated epigenetic reprogramming of cells. Am J Cancer Res 2011; 1: 98-110.
  5. 5. Veranic P, Lokar M, Schutz GJ, Weghuber J, Wieser S, Hagerstrand H, et al. Different types of cell-to-cell connections mediated by nanotubular structures. Biophys J 2008; 95: 4416-25.10.1529/biophysj.108.131375256792418658210
  6. 6. Sustar V, Bedina-Zavec A, Stukelj R, Frank M, Bobojevic G, Jansa R, et al. Nanoparticles isolated from blood: a reflection of vesiculability of blood cells during the isolation process. Int J Nanomedicine 2011; 6: 2737-48.
  7. 7. Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967; 13: 269-88.10.1111/j.1365-2141.1967.tb08741.x6025241
  8. 8. Junkar I, Sustar V, Frank M, Jansa V, Bedina Zavec A, Rozman B, et al. Blood and synovial microparticles as revealed by atomic force and scanning electron microscope. Open Autoimmun J 2009; 1: 50-58.10.2174/1876894600901010050
  9. 9. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci USA 2004; 101: 13368-73.10.1073/pnas.040345310151657315326289
  10. 10. Gonzales P, Pisitkun T, Knepper MA. Urinary exosomes: is there a future? Nephrol Dial Transplant 2008; 23: 1799-801.
  11. 11. Graves LE, Ariztia EV, Navari JR, Matzel HJ, Stack MS, Fishman DA. Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Res 2004; 64: 7045-9.10.1158/0008-5472.CAN-04-180015466198
  12. 12. Mrvar-Brecko A, Sustar V, Jansa V, Stukelj R, Jansa R, Mujagic E, et al. Isolated microvesicles from peripheral blood and body fluids as observed by scanning electron microscope. Blood Cells Mol Dis 2010; 44: 307-12.10.1016/j.bcmd.2010.02.00320199878
  13. 13. Skriner K, Adolph K, Jungblut PR, Burmester GR. Association of citrullinated proteins with synovial exosomes. Arthritis Rheum 2006; 54: 3809-14.10.1002/art.2227617133577
  14. 14. Bard MP, Hegmans JP, Hemmes A, Luider TM, Willemsen R, Severijnen LA, et al. Proteomic analysis of exosomes isolated from human malignant pleural effusions. Am J Respir Cell Mol Biol 2004; 31: 114-21.10.1165/rcmb.2003-0238OC14975938
  15. 15. Admyre C, Grunewald J, Thyberg J, Gripenback S, Tornling G, Eklund A, et al. Exosomes with major histocompatibility complex class II and costimulatory molecules are present in human BAL fluid. Eur Respir J 2003; 22: 578-583.10.1183/09031936.03.0004170314582906
  16. 16. Sullivan R, Saez F, Girouard J, Frenette G. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells MolDis 2005; 35: 1-10.10.1016/j.bcmd.2005.03.00515893944
  17. 17. Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, Norman M, et al. Exosomes with immune modulatory features are present in human breast milk. J Immunol 2007; 179: 1969-78.10.4049/jimmunol.179.3.196917641064
  18. 18. Taylor DD, Akyol S, Gercel-Taylor C. Pregnancy-associated exosomes and their modulation of T cell signaling. J Immunol 2006; 176: 1534-42.10.4049/jimmunol.176.3.153416424182
  19. 19. Asea A, Jean-Pierre C, Kaur P, Rao P, Linhares IM, Skupski D, et al. Heat shock protein-containing exosomes in mid-trimester amniotic fluids. JReprod Immunol 2008; 79: 12-7.10.1016/j.jri.2008.06.00118715652
  20. 20. Perkumas KM, Hoffman EA, McKay BS, Allingham RR, Stamer WD. Myocilin-associated exosomes in human ocular samples. Exp Eye Res 2007; 84: 209-12.10.1016/j.exer.2006.09.020178010717094967
  21. 21. Ogawa Y, Kanai-Azuma M, Akimoto Y, Kawakami H, Yanoshita R. Exosomelike vesicles with dipeptidyl peptidase IV in human saliva. Biol Pharm Bull 2008; 31: 1059-62.10.1248/bpb.31.105918520029
  22. 22. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006; 20:1487-95.10.1038/sj.leu.240429616791265
  23. 23. van der Vos KE, Balaj L, Skog J, Breakefield XO. Brain Tumor Microvesicles: Insights into Intercellular Communication in the Nervous System. Cell MolNeurobiol 2011; 31: 949-59.10.1007/s10571-011-9697-y370217221553248
  24. 24. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10: 1470-U1209.10.1038/ncb1800
  25. 25. Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez-Curtis L, Machalinski B, Ratajczak J, et al. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 2005; 113: 752-60.10.1002/ijc.20657
  26. 26. Safaei R, Larson BJ, Cheng TC, Gibson MA, Otani S, Naerdemann W, et al. Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol Cancer Ther 2005; 4: 1595-604.10.1158/1535-7163.MCT-05-0102
  27. 27. Shedden K, Xie XT, Chandaroy P, Chang YT, Rosania GR. Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles. Cancer Res 2003; 63: 4331-7.
  28. 28. Hakulinen J, Junnikkala S, Sorsa T, Meri S. Complement inhibitor membrane cofactor protein (MCP; CD46) is constitutively shed from cancer cell membranes in vesicles and converted by a metalloproteinase to a functionally active soluble form. Eur J Immunol 2004; 34: 2620-9.10.1002/eji.200424969
  29. 29. Valenti R, Huber V, Filipazzi P, Pilla L, Sovena G, Villa A, et al. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res 2006; 66: 9290-8.10.1158/0008-5472.CAN-06-1819
  30. 30. Abid Hussein MN, Boing AN, Sturk A, Hau CM, Nieuwland R. Inhibition of microparticle release triggers endothelial cell apoptosis and detachment. Thromb Haemost 2007; 98: 1096-107.10.1160/TH05-04-0231
  31. 31. Kim HK, Song KS, Park YS, Kang YH, Lee YJ, Lee KR, et al. Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur J Cancer 2003; 39: 184-91.10.1016/S0959-8049(02)00596-8
  32. 32. Jansa R, Sustar V, Frank M, Susanj P, Bester J, Mancek-Keber M, et al. 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: 124-32.10.1016/j.bcmd.2008.01.00918387323
  33. 33. Baran J, Baj-Krzyworzeka M, Weglarczyk K, Szatanek R, Zembala M, Barbasz J, et al. Circulating tumour-derived microvesicles in plasma of gastric cancer patients. Cancer Immunol Immunother 2010; 59: 841-50.10.1007/s00262-009-0808-220043223
  34. 34. Lipowsky R. The conformation of membranes. Nature 1991; 349: 475-81.10.1038/349475a01992351
  35. 35. Kralj-Iglic V, Babnik B, Gauger DR, May S, Iglic A. Quadrupolar ordering of phospholipid molecules in narrow necks of phospholipid vesicles. J StatPhys 2006; 125: 727-52.10.1007/s10955-006-9051-9
  36. 36. Hagerstrand H, Isomaa B. Morphological characterization of exovesicles and endovesicles released from human erythrocytes following treatment with amphiphiles. Biochim Biophys Acta 1992; 1109: 117-26.10.1016/0005-2736(92)90074-V
  37. 37. Black PH. Shedding from Normal and Cancer-Cell Surfaces. New Engl J Med 1980; 303: 1415-6.10.1056/NEJM198012113032411
  38. 38. Kralj-Iglic V, Batista U, Hägerstrand H, Iglic A, Majhenc J, Sok M. On mechanisms of cell plasma membrane vesiculation. Radiol Oncol 1998; 32: 119-23.
  39. 39. Kralj-Iglic V, Veranic P. Curvature-Induced Sorting of Bilayer Membrane Constituents and Formation of Membrane Rafts. In: A. Leitmannova Liu, editor. Advances in planar lipid bilayers and liposomes, Vol. 5, Elsevier; 2007. p. 129-49.10.1016/S1554-4516(06)05005-8
  40. 40. Kralj-Iglic V, Iglic A, Hagerstrand H, Peterlin P. Stable tubular microexovesicles of the erythrocyte membrane induced by dimeric amphiphiles. PhysRev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 2000; 61: 4230-4.10.1103/PhysRevE.61.4230
  41. 41. Sheetz MP, Singer SJ. Biological-membranes as bilayer couples - molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci USA 1974; 71: 4457-61.10.1073/pnas.71.11.4457
  42. 42. Helfrich W. Blocked lipid exchange in bilayers and its possible influence on the shape of vesicles. Z. Naturforsch. 1974; 29c: 510.10.1515/znc-1974-9-1010
  43. 43. Evans EA. Bending resistance and chemically induced moments in membrane bilayers. Biophys J 1974; 14: 923-31.10.1016/S0006-3495(74)85959-X
  44. 44. Kralj-Iglic V. Stability of membranous nanostructures: a possible key mechanism in cancer progression. Int J Nanomedicine 2012; 7: 3579-96.10.2147/IJN.S29076341420422888223
  45. 45. Zachowski A, Devaux PF. Transmembrane movements of lipids. Experientia 1990; 46: 644-5610.1007/BF019397032193828
  46. 46. Sims PJ, Wiedmer T. Unraveling the mysteries of phospholipid scrambling. Thromb Haemost 2001; 86: 266-75.10.1055/s-0037-1616224
  47. 47. Wydro P, Hac-Wydro K. Thermodynamic description of the interactions between lipids in ternary Langmuir monolayers: the study of cholesterol distribution in membranes. J Phys Chem B 2007; 111: 2495-502.10.1021/jp066950+
  48. 48. Pap E, Pallinger E, Pasztoi M, Falus A. Highlights of a new type of intercellular communication: microvesicle-based information transfer. InflammRes 2009; 58: 1-8.10.1007/s00011-008-8210-7
  49. 49. van Meer G. Dynamic transbilayer lipid asymmetry. Csh Perspect Biol 2011; 3.10.1101/cshperspect.a004671
  50. 50. Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes/ microvesicles as a mechanism of cell-to-cell communication. Kidney Int2010; 78: 838-48.10.1038/ki.2010.278
  51. 51. Davizon P, Lopez JA. Microparticles and thrombotic disease. Curr OpinHematol 2009; 16: 334-41.10.1097/MOH.0b013e32832ea49c
  52. 52. Mrówczyńska L, Salzer U, Iglič A, Hägerstrand H. Curvature factor and membrane solubilisation, with particular reference to membrane rafts. CellBiol Int, 2011; 35: 991-5.10.1042/CBI20100786
  53. 53. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997; 387: 569-72.10.1038/42408
  54. 54. Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Bi 1998; 14: 111-36.10.1146/annurev.cellbio.14.1.111
  55. 55. Ikonen E. Roles of lipid rafts in membrane transport. Curr Opin Cell Biol 2001; 13: 470-7.10.1016/S0955-0674(00)00238-6
  56. 56. Flaumenhaft R. Formation and fate of platelet microparticles. Blood CellsMol Dis 2006; 36: 182-7.10.1016/j.bcmd.2005.12.019
  57. 57. Huttner WB, Zimmerberg J. Implications of lipid microdomains for membrane curvature, budding and fission. Curr Opin Cell Biol 2001; 13: 478-84.10.1016/S0955-0674(00)00239-8
  58. 58. Schmidt A, Wolde M, Thiele C, Fest W, Kratzin H, Podtelejnikov AV, et al. Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 1999; 401: 133-41.10.1038/4361310490020
  59. 59. Kozlov MM. Fission of biological membranes: interplay between dynamin and lipids. Traffic 2001; 2: 51-65.10.1034/j.1600-0854.2001.020107.x11208168
  60. 60. Heijnen HFG, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: Microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999; 94: 3791-9.10.1182/blood.V94.11.3791
  61. 61. Pap E, Pallinger E, Falus A. The role of membrane vesicles in tumorigenesis. Crit Rev Oncol Hematol 2011; 79: 213-23.10.1016/j.critrevonc.2010.07.01520884225
  62. 62. Di Vizio D, Kim J, Hager MH, Morello M, Yang W, Lafargue CJ, et al. Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res 2009; 69: 5601-9.10.1158/0008-5472.CAN-08-3860285387619549916
  63. 63. Del Conde I, Shrimpton CN, Thiagarajan P, Lopez JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005; 106: 1604-11.10.1182/blood-2004-03-109515741221
  64. 64. Kharaziha P, Ceder S, Li Q, Panaretakis T. Tumor cell-derived exosomes: A message in a bottle. Biochim Biophys Acta 2012; 1826: 103-11.10.1016/j.bbcan.2012.03.00622503823
  65. 65. Miyanishi M, Tada K, Koike M, Uchiyama Y, Kitamura T, Nagata S. Identification of Tim4 as a phosphatidylserine receptor. Nature 2007; 450: 435-9.10.1038/nature0630717960135
  66. 66. Segura E, Nicco C, Lombard B, Veron P, Raposo G, Batteux F, et al. ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood 2005; 106: 216-23.10.1182/blood-2005-01-022015790784
  67. 67. Feng D, Zhao WL, Ye YY, Bai XC, Liu RQ, Chang LF, et al. Cellular Internalization of exosomes occurs through phagocytosis. Traffic 2010; 11: 675-87.10.1111/j.1600-0854.2010.01041.x20136776
  68. 68. Teissier E, Pecheur EI. Lipids as modulators of membrane fusion mediated by viral fusion proteins. Eur Biophys J 2007; 36: 887-99.10.1007/s00249-007-0201-z708011517882414
  69. 69. Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. JBiol Chem 2009; 284: 34211-22.10.1074/jbc.M109.041152279719119801663
  70. 70. Escrevente C, Keller S, Altevogt P, Costa J. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 2011; 11: 108.10.1186/1471-2407-11-108307294921439085
  71. 71. Taraboletti G, D’Ascenzo S, Giusti I, Marchetti D, Borsotti P, Millimaggi D, et al. Bioavailability of VEGF in tumor-shed vesicles depends on vesicle burst induced by acidic pH. Neoplasia 2006; 8: 96-103.10.1593/neo.05583157851216611402
  72. 72. Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol 2009; 19: 43-51.10.1016/j.tcb.2008.11.00319144520
  73. 73. Rak J, Guha A. Extracellular vesicles - vehicles that spread cancer genes. Bioessays 2012; 34: 489-97.10.1002/bies.20110016922442051
  74. 74. Lee TH, D’Asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J. Microvesicles as mediators of intercellular communication in cancer - the emerging science of cellular ‘debris’. Semin Immunopathol 2011; 33: 455-67.10.1007/s00281-011-0250-321318413
  75. 75. Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008; 10: 619-24.10.1038/ncb172518425114
  76. 76. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno- Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012; 18: 883-91.10.1038/nm.2753
  77. 77. Sidhu SS, Mengistab AT, Tauscher AN, LaVail J, Basbaum C. The microvesicle as a vehicle for EMMPRIN in tumor-stromal interactions. Oncogene 2004; 23: 956-963.10.1038/sj.onc.1207070
  78. 78. McCready J, Sims JD, Chan D, Jay DG. Secretion of extracellular hsp90alpha via exosomes increases cancer cell motility: a role for plasminogen activation. BMC Cancer 2010; 10: 294.10.1186/1471-2407-10-294
  79. 79. Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, Morice P. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002; 360: 295-305. 10.1016/S0140-6736(02)09552-1
  80. 80. Koga K, Matsumoto K, Akiyoshi T, Kubo M, Yamanaka N, Tasaki A, et al. Purification, characterization and biological significance of tumor-derived exosomes. Anticancer Res 2005; 25: 3703-7.
  81. 81. Dinger ME, Mercer TR, Mattick JS. RNAs as extracellular signaling molecules. J Mol Endocrinol 2008; 40: 151-9.10.1677/JME-07-016018372404
  82. 82. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001; 294: 853-8.10.1126/science.106492111679670
  83. 83. Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 2006; 6: 259-69.10.1038/nrc184016557279
  84. 84. Tsui NB, Ng EK, Lo YM. Stability of endogenous and added RNA in blood specimens, serum, and plasma. Clin Chem 2002; 48: 1647-53.10.1093/clinchem/48.10.1647
  85. 85. Tsui NB, Ng EK, Lo YM. Molecular analysis of circulating RNA in plasma. Methods Mol Biol 2006; 336: 123-34.10.1385/1-59745-074-X:123
  86. 86. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosomemediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9: 654-9.10.1038/ncb159617486113
  87. 87. Hong BS, Cho JH, Kim H, Choi EJ, Rho S, Kim J, et al. Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells. BMC Genomics 2009; 10: 556.10.1186/1471-2164-10-556278858519930720
  88. 88. Baj-Krzyworzeka M, Szatanek R, Weglarczyk K, Baran J, Urbanowicz B, Branski P, et al. Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes. Cancer Immunol Immunother 2006; 55: 808-18.10.1007/s00262-005-0075-916283305
  89. 89. Kogure T, Lin WL, Yan IK, Braconi C, Patel T. Intercellular nanovesiclemediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011; 54: 1237-48.10.1002/hep.24504331036221721029
  90. 90. Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoSOne 2010; 5: e13247.10.1371/journal.pone.0013247295191220949044
  91. 91. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008; 110:13-21.10.1016/j.ygyno.2008.04.03318589210
  92. 92. Bergsmedh A, Szeles A, Henriksson M, Bratt A, Folkman MJ, Spetz AL, et al. Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc NatlAcad Sci USA 2001; 98: 6407-11.10.1073/pnas.1011299983348111353826
  93. 93. Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2011; 2: 180.10.1038/ncomms1180304068321285958
  94. 94. Desler C, Marcker ML, Singh KK, Rasmussen LJ. The importance of mitochondrial DNA in aging and cancer. J Aging Res 2011; 2011: 407536.10.4061/2011/407536309256021584235
  95. 95. Guescini M, Genedani S, Stocchi V, Agnati LF. Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J Neural Transm 2010; 117: 1-4.10.1007/s00702-009-0288-819680595
  96. 96. Bannert N, Kurth R. Retroelements and the human genome: new perspectives on an old relation. Proc Natl Acad Sci USA 2004; 101: 14572-9.10.1073/pnas.040483810152198615310846
  97. 97. Cordaux R, Batzer MA. The impact of retrotransposons on human genome evolution. Nat Rev Genet 2009; 10: 691-703.10.1038/nrg2640
  98. 98. Wiemels JL, Hofmann J, Kang M, Selzer R, Green R, Zhou M, et al. Chromosome 12p deletions in TEL-AML1 childhood acute lymphoblastic leukemia are associated with retrotransposon elements and occur postnatally. Cancer Res 2008; 68: 9935-44.10.1158/0008-5472.CAN-08-2139
  99. 99. Bretscher MS. Membrane structure: some general principles. Science 1973; 181: 622-9.10.1126/science.181.4100.622
  100. 100. Dahiya R, Boyle B, Goldberg BC, Yoon WH, Konety B, Chen K, et al. Metastasis-associated alterations in phospholipids and fatty acids of human prostatic adenocarcinoma cell lines. Biochem Cell Biol 1992; 70: 548-54.10.1139/o92-085
  101. 101. Kim CW, Lee HM, Lee TH, Kang C, Kleinman HK, Gho YS. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res 2002; 62: 6312-7.
  102. 102. McGarry LJ, Thompson D. Retrospective database analysis of the prevention of venous thromboembolism with low-molecular-weight heparin in acutely III medical inpatients in community practice. Clin Ther 2004; 26: 419-30.10.1016/S0149-2918(04)90038-0
  103. 103. Smorenburg SM, Hettiarachchi RJ, Vink R, Buller HR. The effects of unfractionated heparin on survival in patients with malignancy-a systematic review. Thromb Haemost 1999; 82: 1600-4.10.1055/s-0037-1614885
  104. 104. Stevenson JL, Choi SH, Wahrenbrock M, Varki A, Varki NM. Heparin effects in metastasis and Trouseeau syndrome: anticoagulation is not the primary mechanism. Haem Rep 2005; 1: 59-60.
  105. 105. Sustar V, Jansa R, Frank M, Hagerstrand H, Krzan M, Iglic A et al. Suppression of membrane microvesiculation - a possible anticoagulant and anti-tumor progression effect of heparin. Blood Cells Mol Dis 2009; 42: 223-7.10.1016/j.bcmd.2009.01.01219261492
  106. 106. Urbanija J, Tomsic N, Lokar M, Ambrozic A, Cucnik S, Rozman B, et al. Coalescence of phospholipid membranes as a possible origin of anticoagulant effect of serum proteins. Chem Phys Lipids 2007; 150: 49-57.10.1016/j.chemphyslip.2007.06.21617662972
  107. 107. Urbanija J, Babnik B, Frank M, Tomsic N, Rozman B, Kralj-Iglic V, et al. Attachment of beta 2-glycoprotein I to negatively charged liposomes may prevent the release of daughter vesicles from the parent membrane. EurBiophys J 2008; 37: 1085-95.
  108. 108. May S, Iglič A, Reščič J, Maset S., Bohinc K. Bridging like-charged macroions through long divalent rod-like ions. J Phys Chem B 2008; 112: 1685-92.10.1021/jp073355e18205341
  109. 109. Velikonja A, Perutkova Š, Gongadze E, Kramar P, Polak A, Maček-Lebar A, Iglič A. Monovalent ions and water dipoles in contact with dipolar zwitterionic lipid headroups - theory and MD simulations, Int J Mol Sci 2013; 14: 2846-61.
  110. 110. Gongadze E, Iglič A. Excluded volume effect of counterions and water dipoles near a highly charged surface due to a rotationally averaged Boltzmann factor for water dipoles. Gen Phys Biophys 2013; 21: 143-5..10.4149/gpb_201301423531844
  111. 111. Ambrožič A, Čučnik S, Tomšič N, Urbanija J, Lokar M, Babnik B et al. Interaction of giant phospholipid vesicles containing cardiolipin and cholesterol with beta 2-glycoprotein-I and anti-beta2-glycoprotein-I antibodies. Autoimmun Rev 2006; 6: 10-5.10.1016/j.autrev.2006.03.00117110310
DOI: https://doi.org/10.2478/raon-2013-0037 | Journal eISSN: 1581-3207 | Journal ISSN: 1318-2099
Language: English
Page range: 197 - 205
Published on: Jul 30, 2013
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2013 Eva Ogorevc, Veronika Kralj-Iglic, Peter Veranic, published by Association of Radiology and Oncology
This work is licensed under the Creative Commons License.