Tumor interstitial fluid as modulator of cancer inflammation, thrombosis, immunity and angiogenesis

Anticancer Research

Volumn 32, Issue 2, 2012, Pages 405-414

  Baronzio, Gianfranco ^a   Schwartz, Laurent ^b   Kiselevsky, Mikhail ^c   Guais, Adeline ^d   Sanders, Edward ^d   Milanesi, Gloria ^e   Baronzio, Miriam ^a   Freitas, Isabel ^e  

^a Centro Medico Kines   (Italy)

^b RAYMOND POINCARÉ HOSPITAL   (France)

^c N N BLOKHIN RUSSIAN CANCER RESEARCH CENTER   (Russian Federation)

^d Biorebus   (France)

^e UNIVERSITY OF PAVIA   (Italy)

Author keywords

Angiogenesis; Chemotherapy; Immunotherapy; Inflammation; Nutritive function; Osmotic forces; Radiotherapy; Review; TIF; TIFP; Tumor blood flow

Indexed keywords

ALBUMIN; AQUAPORIN; CHOLESTEROL; CYTOKINE; DEXAMETHASONE; FIBRIN; FLUOROURACIL; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1; LACTIC ACID; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; VASCULOTROPIN;

ANGIOGENESIS; APOPTOSIS; BLOOD VESSEL PERMEABILITY; BREAST TUMOR; CANCER INVASION; CELL INFILTRATION; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CYTOPLASM VESICLE; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; EXOSOME; EXTRACELLULAR MATRIX; HUMAN; HYPOXIA; IMMUNITY; IMMUNOHISTOCHEMISTRY; INTERSTITIAL FLUID; LYMPH NODE METASTASIS; LYMPHATIC SYSTEM; METASTASIS; NONHUMAN; OSMOLARITY; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; THROMBOSIS; THYROID CARCINOMA; TUMOR GROWTH; TUMOR INTERSTITIAL FLUID; TUMOR MICROENVIRONMENT; TUMOR VOLUME;

ANIMALS; EXTRACELLULAR FLUID; HUMANS; INFLAMMATION; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; THROMBOSIS;

EID: 84856814073     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (125)

1. Zweifach BW: Microcirculation. Annu Rev Physiol 35: 117-150, 1973.
2. Schmid-Schönbein GW: Biomechanics of microcirculatory blood perfusion. Annu Rev Biomed Eng 1: 73-102, 1999.
3. Nagy JA, Benjamin L, Zeng H, Dvorak AM, Dvorak HF: Vascular permeability, vascular hyperpermeability and angiogenesis. Angiogenesis 11(2): 109-119, 2008.
4. Guyton AC: Interstitial fluid pressure-volume relationship and their regulation. In: Cellular and Respiratory Mass Transport Ciba Foundation; 4-24. G.Ew and Knight (eds.), 1969.
5. Michel CC and Curry FE: Microvascular permeability Physiol Rev 79(3): 703-761, 1999. (Pubitemid 29330172)
6. Bazzoni G and Dejana E: Pores in the sieve and channels in the wall: control of paracellular permeability by junctional proteins in endothelial cells. Microcirculation 8(3): 143-152, 2011.
7. Nagy JA, Brown LF, Senger DR, Lanir N, Van de Water L, Dvorak AM and Dvorak HF: Pathogenesis of tumor stromageneration: a critical role for leaky blood vessels and fibrin deposition. Biochim Biophys Acta 948(3): 305-326, 1989. (Pubitemid 19055388)
8. Dvorak HF, Senger DR and Dvorak AM: Fibrin as a component of the tumor stroma: origins and biological significance. Cancer Metastasis Rev 2(1): 41-73, 1983.
9. Majno G and Joris I: Disturbances of fluid exchange. In: Cell Tissue, and Disease. Majno G and Joris I (eds.). Oxford University Press, New York pp. 613-629, 2004.
10. McDonald DM and Foss AJ: Endothelial cells of tumor vessels: abnormal but not absent. Cancer Metastasis Rev 19: 109-120, 2000. (Pubitemid 32004700)
11. McDonald DM and Baluk P: Significance of blood vessel leakiness in cancer. Cancer Res 62: 5381-5385, 2002. (Pubitemid 35024617)
12. Dvorak AM and Feng D: The vesiculo-vacuolar organelle (VVO). A new endothelial cell permeability organelle. J Histochem Cytochem 49(4): 419-432, 2001.
13. Feng D, Nagy JA, Pyne K, Hammel I, Dvorak HF and Dvorak AM: Pathways of macromolecular extravasation across microvascular endothelium in response to VPF/VEGF and other vasoactive mediators. Microcirculation 6(1): 23-44, 1999. (Pubitemid 129672560)
14. Feng D, Nagy JA, Dvorak HF and Dvorak AM: Ultrastructural studies define soluble macromolecular, particulate, and cellular transendothelial cell pathways in venules, lymphatic vessels, and tumor-associated microvessels in man and animals. Microsc Res Tech 57(5): 289-326, 2002. (Pubitemid 34579214)
15. Armulik A, Abramsson A and Betsholtz C: Endothelial/pericyte interactions. Circ Res 97: 512-523, 2005. (Pubitemid 41361741)
16. Eming SA and Hubbell JA. Extracellular matrix in angiogenesis: dynamic structures with translational potential. Exp Dermatol 20(7): 605-613, 2011.
17. Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK and McDonald DM: Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 160(3): 985-1000, 2002. (Pubitemid 34224587)
18. Xian X, Håkansson J, Ståhlberg A, Lindblom P, Betsholtz C, Gerhardt H and Semb H: Pericytes limit tumor cell metastasis. J Clin Invest 116(3): 642-645, 12006.
19. Maeda H, Wu J, Sawa T, Matsumura Y and Hori K: Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release 65(1-2): 271-284, 2000. (Pubitemid 30122932)
20. Freitas I, Baronzio GF, Bono B, Griffini P, Bertone V, Sonzini N, Magrassi GR, Bonandrini L and Gerzeli G: Tumor interstitial fluid: misconsidered component of the internal milieu of a solid tumor. Anticancer Res 17(1A): 165-172, 1997. (Pubitemid 27116662)
21. Senger DR: Vascular endothelial growth factor: much more than an angiogenesis factor. Mol Biol Cell 21(3): 377-379, 2010.
22. Dvorak HF: Discovery of vascular permeability factor (VPF). Exp Cell Res 312(5): 522-526, 2006.
23. Vaupel P: Hypoxia and aggressive tumor phenotype: implications for therapy and prognosis. Oncologist 13(Suppl 3): 21-26, 2008.
24. Vaupel P: The role of hypoxia-induced factors in tumor progression. Oncologist 9(Suppl 5): 10-17, 2004.
25. Vaupel P and Harrison L: Tumor hypoxia: causative factors, compensatory mechanisms, and cellular response. Oncologist 9(Suppl 5): 4-9, 2004. (Pubitemid 39658340)
26. Baronzio G, Freitas I and Kwaan HC: Tumor microenvironment and hemorheological abnormalities. Semin Thromb Hemost 29(5): 489-497, 2003. (Pubitemid 37352649)
27. Jain RK: Integrative pathophysiology of solid tumors: role in detection and treatment. Cancer J Sci Am 4(Suppl 1): S48-57, 1998.
28. Semenza GL: Tumor metabolism: cancer cells give and take lactate. J Clin Invest 118(12): 3930-3942, 2008.
29. Gullino PM: The internal milieu of tumors Prog Exp Tumor Res 8: 1-25, 1966.
30. Gullino PM, Clark SH and Grantham FH: The interstitial fluid of solid tumors. Cancer Res 24: 780-794, 1964.
31. Butler TP, Grantham FH and Gullino PM: Bulk transfer of fluid in the interstitial compartment of mammary tumors. Cancer Res 35(11): 3084-3088, 1975.
32. Gullino PM: Extracellular compartments of solid tumors. In: Cancer: A Comprehensive Treatise. Vol 3. Becker FF (ed). Plenum Press New York, pp. 327-354, 1975.
33. Sylven B and Bois I: Protein content and enzymatic assays of interstitial fluid from some normal tissues and transplanted mouse tumors. Cancer Res 20: 831-836, 1960.
34. Ziche M, Jones J and Gullino PM: Role of prostaglandin E1 and copper in angiogenesis. J Natl Cancer Inst 69(2): 475-482, 1982.
35. Gullino PM: Prostaglandins and gangliosides of tumor microenvironment: their role in angiogenesis. Acta Oncologica 34: 439-441, 1995.
36. Alessandri G, Raju KS and Gullino PM: Interaction of gangliosides with fibronectin in the mobilization of capillary endothelium. Possible influence on the growth of metastasis. Invasion Metastasis 6(3): 145-165, 1986. (Pubitemid 16000053)
37. Ziehe M, Alessandri G and Gullino PM: Gangliosides promote the angiogenic response. Lab Invest 61(6): 629-634, 1989. (Pubitemid 20027690)
38. Gullino PM, Grantham FH and Clark SH: The collagen content of transplanted tumors. Cancer Res 22: 1031-1037, 1962.
39. Rutkowski JM and Swartz MA: A driving force for change: interstitial flow as a morphoregulator. Trends Cell Biol 17(1): 44-50, 2007. (Pubitemid 46027589)
40. Arteaga-Solis E, Gayraud B and Ramirez F: Elastic and collagenous networks in vascular diseases. Cell Struct Funct 25(2): 69-72, 2000. (Pubitemid 30453803)
41. Celis JE, Gromov P, Cabezon T, Moreira JM, Ambartsumian N, Sandelin K, Rank F and Gromova I: Proteomic characterization of the interstitial fluid perfusing the breast tumor microenvironment: a novel resource for biomarker and therapeutic target discovery. Mol Cell Proteomics 3(4): 327-344, 2004. (Pubitemid 38702087)
42. Alexander H, Stegner AL, Wagner-Mann C, Du Bois GC, Alexander S and Sauter ER: Proteomic analysis to identify breast cancer biomarkers in nipple aspirate fluid. Clin Cancer Res 10(22): 7500-7510, 2004. (Pubitemid 39557511)
43. Wiig H, Tenstad O, Iversen PO, Kalluri R and Bjerkvig R: Interstitial fluid: the overlooked component of the tumor microenvironment? Fibrogenesis Tissue Repair 23;3(1): 12,2010.
44. Roh HD, Boucher Y, Kainicki S, Buchsbaum R, Bloomer WD and Jain RK: Interstitial hypertension in carcinoma of uterine cervix in patients: possible correlation with tumor oxygenation and radiation response. Cancer Res 51(24): 6695-6698, 1991.
45. Boucher Y, Kirkwood JM, Opacic D, Desantis M and Jain RK: Interstitial hypertension in superficial metastatic melanomas in humans. Cancer Res 51(24): 6691-6694, 1991.
46. Gutmann R, Leunig M, Feyh J, Goetz AE, Messmer K, Kastenbauer E and Jain RK: Interstitial hypertension in head and neck tumors in patients: correlation with tumor size. Cancer Res 52(7): 1993-1995, 1992.
47. Less JR, Posner MC, Boucher Y, Borochovitz D, Wolmark N and Jain RK: Interstitial hypertension in human breast and colorectal tumors. Cancer Res 52(22): 6371-6374, 1992.
48. Curti BD, Urba WJ, Alvord WG, Janik JE, Smith JW 2nd, Madara K and Longo DL: Interstitial pressure of subcutaneous nodules in melanoma and lymphoma patients: changes during treatment. Cancer Res 53(10 Suppl): 2204-2207, 1993. (Pubitemid 23156799)
49. Nathanson SD and Nelson L: Interstitial fluid pressure in breast cancer, benign breast conditions, and breast parenchyma. Ann Surg Oncol 1(4): 333-338, 1994.
50. Milosevic M, Fyles A and Hill R: Interstitial fluid pressure in cervical cancer: guide to targeted therapy. Am J Clin Oncol 24(5): 516-521, 2001. (Pubitemid 32959113)
51. Wiig H, Tveit E, Hultborn R, Reed RK and Weiss L: Interstitial fluid pressure in DMBA-induced rat mammary tumours. Scand J Clin Lab Invest 42(2): 159-164, 1982. (Pubitemid 12124734)
52. Wiig H and Gadeholt G: Interstitial fluid pressure and hemodynamics in a sarcoma implanted in the rat tail. Microvasc Res 29(2): 176-189, 1985. (Pubitemid 15108032)
53. Roh HD, Boucher Y, Kalnicki S, Buchsbaum R, Bloomer WD and Jain RK: Interstitial hypertension in carcinoma of uterine cervix in patients: possible correlation with tumor oxygenation and radiation response. Cancer Res 51(24): 6695-6698, 1991.
54. Milosevic M, Fyles A, Hedley D and Hill R: The human tumor microenvironment: invasive (needle) measurement of oxygen and interstitial fluid pressure. Semin Radiat Oncol 14(3): 249-258, 2004. (Pubitemid 38903229)
55. Lunt SJ, Kalliomaki TM, Brown A, Yang VX, Milosevic M and Hill RP: Interstitial fluid pressure, vascularity and metastasis in ectopic, orthotopic and spontaneous tumours. BM C Cancer 7:8: 2-16, 2008.
56. Nathan SS, Huvos AG, Casas-Ganem JE, Yang R, Linkov I, Sowers R, DiResta GR, Gorlick R and Healey JH: Tumor interstitial fluid pressure may regulate angiogenic factors in osteosarcoma. J Orthop Res 26(11): 1520-1525, 2008.
57. Swartz MA and Fleury ME: Interstitial flow and its effects in soft tissues. Annu Rev Biomed Eng 9: 229-256, 2007. (Pubitemid 350246657)
58. Jain RK: Physiological barriers to delivery of monoclonal antibodies and other macromolecules in tumors. Cancer Res 50(3 Suppl): 814s-819s, 1990.
59. Jain RK: Barriers to drug delivery in solid tumors. Sci Am 271(1): 58-65, 1994.
60. Lee CM and Tannock IF: The distribution of the therapeutic monoclonal antibodies cetuximab and trastuzumab within solid tumors. BMC Cancer 3(10): 255-266, 2010.
61. Roh HD, Boucher Y, Kalnicki S, Buchsbaum R, Bloomer WD, Jain RK: Interstitial hypertension in carcinoma of uterine cervix in patients: possible correlation with tumor oxygenation and radiation response. Cancer Res 51(24): 6695-6698, 1991.
62. Salnikov AV, Iversen VV, Koisti M, Sundberg C, Johansson L, Stuhr LB, Sjöquist M, Ahlström H, Reed RK and Rubin K: Lowering of tumor interstitial fluid pressure specifically augments efficacy of chemotherapy. FASEB J 17(12): 1756-1758, 2003.
63. Yuan F, Leunig M, Huang SK, Berk DA, Papahadjopoulos D and Jain RK: Microvascular permeability and interstitial penetration of sterically stabilized (stealth) liposomes in a human tumor xenograft. Cancer Res 54(13): 3352-3356, 1994. (Pubitemid 24225946)
64. Lunt SJ, Fyles A, Hill RP, Milosevic M: Interstitial fluid pressure in tumors: therapeutic barrier and biomarker of angiogenesis. Future Oncol 4(6): 793-802, 2008.
65. Yuan F: Transvascular drug delivery in solid tumors. Semin Radiat Oncol 8(3): 164-175, 1998.
66. Truskey GA, Yuan F and Katz DF: Transport Phenomena in Biological Systems. Part II Chapter 9; Pearson, Prentice, Hall, ed, Upper Saddle River, New Jersey pp. 427-447, 2004.
67. Jeyaseelan K, Sepramaniam S, Armugam A, Wintour EM: Aquaporins: a promising target for drug development. Expert Opin Ther Targets 10(6): 889-909, 2006. (Pubitemid 44816751)
68. Verkman AS, Hara-Chikuma M and Papadopoulos MC: Aquaporins - new players in cancer biology. J Mol Med 86(5): 523-529, 2008.
69. Hobbs SK, Monsky WL, Yuan F, Roberts WG, Griffith L, Torchilin VP and Jain RK: Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc Natl Acad Sci USA 95(8): 4607-4612, 1998. (Pubitemid 28207960)
70. Wiig H, Gyenge C, Iversen PO, Gullberg D and Tenstad O: The role of the extracellular matrix in tissue distribution of macromolecules in normal and pathological tissues: potential therapeutic consequences. Microcirculation 15(4): 283-296, 2008. (Pubitemid 351903344)
71. Wiig H, Gyenge CC and Tenstad O: The interstitial distribution of macromolecules in rat tumours is influenced by the negatively charged matrix components. J Physiol 567(Pt 2): 557-567, 2005. (Pubitemid 41301051)
72. Dreher MR, Liu W, Michelich CR et al: Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers. J Natl Cancer Inst 98(5): 335-344, 2006. (Pubitemid 43338213)
73. Swabb EA, Wei J and Gullino PM: Diffusion and convection in normal and neoplastic tissues. Cancer Res 34(10): 2814-2822, 1974.
74. Netti P and Jain RK: Interstitial transport in solid tumors. In: Cancer Modeling and Simulation. Preziosi L (ed.). CRC press, Boca Raton pp. 51-74, 2003.
75. Stuhr LE, Salnikov AV, Iversen VV, Salvesen G, Rubin K and Reed RK: High-dose, short-term, anti-inflammatory treatment with dexamethasone reduces growth and augments the effects of 5-fluorouracil on dimethyl-alpha- benzanthracene-induced mammary tumors in rats. Scand J Clin Lab Invest 66(6): 477-486, 2006. (Pubitemid 44454444)
76. Navalitloha Y, Schwartz ES, Groothuis EN, Allen CV, Levy RM and Groothuis DR: Therapeutic implications of tumor interstitial fluid pressure in subcutaneous RG-2 tumors. Neuro Oncol 8(3): 227-233, 2006. (Pubitemid 46542647)
77. Netti PA, Berk DA, Swartz MA et al: Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 60(9): 2497-2503, 2000. (Pubitemid 30262444)
78. Oldberg A, Kalamajski S, Salnikov AV, Stuhr L, Mörgelin M, Reed RK, Heldin NE and Rubin K: Collagen-binding proteoglycan fibromodulin can determine stroma matrix structure and fluid balance in experimental carcinoma. Proc Natl Acad Sci USA 104(35): 13966-13971, 2007. (Pubitemid 350003321)
79. Jacobson A, Salnikov A, Lammerts E, Roswall P, Sundberg C, Heldin P, Rubin K and Heldin NE: Hyaluronan content in experimental carcinoma is not correlated to interstitial fluid pressure. Biochem Biophys Res Commun 305(4): 1017-1023, 2003. (Pubitemid 36597865)
80. Heldin CH, Rubin K, Pietras K and Ostman A: High interstitial fluid pressure - an obstacle in cancer therapy. Nat Rev Cancer 4(10): 806-813, 2004. (Pubitemid 39331152)
81. Semenza GL: Tumor metabolism: cancer cells give and take lactate. J Clin Invest 118(12): 3930-3942, 2008.
82. Sonveaux P, Végran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN, De Saedeleer CJ, Kennedy KM, Diepart C, Jordan BF, Kelley MJ, Gallez B, Wahl ML, Feron O and Dewhirst MW: Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 118(12): 3835-3837, 2008.
83. Stehle G, Sinn H, Wunder A, Hermann H, Schrenk, DL, Stewart JCM, Hartung G, Maier-Borst W and Heene DL: Plasma protein (albumin) catabolism by the tumor itself - implications for tumor metabolism and the genesis of cachexia. Crit Rev Oncol Hematol 26(2): 77-100, 1997. (Pubitemid 27362424)
84. Roberts WG and Palade GE: Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res 57(4): 765-772, 1997. (Pubitemid 27085664)
85. Feng D, Nagy JA, Dvorak AM and Dvorak HF: Different pathways of macromolecule extravasation from hyperpermeable tumor vessels. Microvasc Res 59(1): 24-37, 2000. (Pubitemid 30073135)
86. Kohn S, Nagy JA, Dvorak HF and Dvorak AM: Pathways of macromolecular tracer transport across venules and small veins. Structural basis for the hyperpermeability of tumor blood vessels. Lab Invest 67(5): 596-607, 1992.
87. Hashizume H, Baluk P, Morikawa S, McLean JW, Thurston G, Roberge S, Jain RK and McDonald DM: Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 156(4): 1363-1380, 2000. (Pubitemid 30660013)
88. Jain RK: Transport of molecules across tumor vasculature. Cancer Metastasis Rev 6(4): 559-593, 1987.
89. Fogh-Andersen N, Bjerrum PJ, Siggaard-Andersen O.: Ionic binding, net charge, and Donnan effect of human serum albumin as a function of pH. Clin Chem 39(1): 48-52, 1993. (Pubitemid 23034955)
90. Roche M, Rondeau P, Singh NR, Tarnus E and Bourdon E: The antioxidant properties of serum albumin. FEBS Lett 582(13): 1783-7, 2008.
91. Nicholson JP, Wolmarans MR and Park GR: The role of albumin in critical illness. Br J Anaesth 85(4): 599-610, 2000.
92. Schwartz L, Guais A, Pooya M and Abolhassani M: Is inflammation a consequence of extracellular hyperosmolarity? J Inflamm 23: 6-16, 2009.
93. Basu A and Haldar S: The relationship between BCL2, BAX and p53: consequences for cell cycle progression and cell death. Mol Hum Reprod 4(12): 1099-1109, 1998. (Pubitemid 28552792)
94. Maquart FX, Bellon G, Pasco S and Monboisse JC: Matrikines in the regulation of extracellular matrix degradation. Biochimie 87(3-4): 353-360, 2005. (Pubitemid 40387614)
95. Bellon G, Martiny L and Robinet A: Matrix metalloproteinases and matrikines in angiogenesis. Crit Rev Oncol Hematol 49(3): 203-20, 2004. (Pubitemid 38251353)
96. Aharon A and Brenner B: Microparticles, thrombosis and cancer. Best Pract Res Clin Haematol 22(1): 61-69, 2009.
97. Iero M, Valenti R, Huber V, Filipazzi P, Parmiani G, Fais S and Rivoltini L: Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 15(1): 80-88, 2008. (Pubitemid 350286175)
98. Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, Morice P, Pomel C, Lhomme C, Escudier B, Le Chevalier T, Tursz T, Amigorena S, Raposo G, Angevin E and Zitvogel L: Malignant effusions and immunogenic tumour-derived exosomes. Lancet 360: 295-305, 2002. (Pubitemid 34874721)
99. Bard MP, Hegmans JP, Hemmes A, Luider TM, Willemsen R, Severijnen LA, van Meerbeeck JP, Burgers SA, Hoogsteden HC and Lambrecht BN: Proteomic analysis of exosomes isolated from human malignant pleural effusions. Am J Respir Cell Mol Biol 31(1): 114-121, 2004. (Pubitemid 38888047)
100. Runz S, Keller S, Rupp C, Stoeck A, Issa Y, Koensgen D, Mustea A, Sehouli J, Kristiansen G and Altevogt P: Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol Dec 107(3): 563-571, 2007.
101. Cocucci E, Racchetti G and Meldolesi J: Shedding microvesicles: artefacts no more. Trends Cell Bio 19(2): 43-51, 2009.
102. Al-Nedawi K, Meehan B and Rak J: Microvesicles: messengers and mediators of tumor progression. Cell Cycle 8(13): 2014-2018, 2009.
103. Morel O, Morel N, Freyssinet JM and Toti F: Platelet microparticles and vascular cells interactions: a checkpoint between the haemostatic and thrombotic responses. Platelets 19(1): 9-23, 2008. (Pubitemid 351171554)
104. Nazarenko I, Rana S, Baumann A, McAlear J, Hellwig A, Trendelenburg M, Lochnit G, Preissner KT and Zöller M: Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 70(4): 1668-1678, 2010.
105. Kim CW, Lee HM, Lee TH, Kang C, Kleinman HK and Gho YS: Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res 62(21): 6312-6317, 2002. (Pubitemid 35244486)
106. Al-Nedawi K, Meehan B, Kerbel RS, Allison AC and Rak J: Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci USA 106(10): 3794-3799, 2009.
107. Hood JL, Pan H, Lanza GM and Wickline SA: Paracrine induction of endothelium by tumor exosomes. Lab Invest 89: 1317-1328, 2009.
108. Stewart TJ and Abrams SI: How tumours escape mass destruction. Oncogene 27(45): 5894-5903, 2008.
109. Whiteside TL: Immune responses to malignancies. J Allergy Clin Immunol 125(2 Suppl 2): S272-283, 2010.
110. Valenti R, Huber V, Iero M, Filipazzi P, Parmiani G and Rivoltini L: Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res 67(7): 2912-2915, 2007. (Pubitemid 46724823)
111. Xiang X, Poliakov A, Liu C, Liu Y, Deng ZB, Wang J, Cheng Z, Shah SV, Wang GJ, Zhang L, Grizzle WE, Mobley J and Zhang HG: Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer 124(11): 2621-2633, 2009.
112. Szajnik M, Czystowska M, Szczepanski MJ, Mandapathil M and Whiteside TL: Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T-cells (Treg). PLoS One 5(7): e11469-11482, 2010.
113. Clayton A, Mitchell JP, Court J, Linnane S, Mason MD and Tabi Z: Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol 180(11): 7249-7258, 2008.
114. + T-cell apoptosis. Blood Cells Mol Dis 35(2): 169-173, 2005.
115. Zeelenberg IS, Ostrowski M, Krumeich S, Bobrie A, Jancic C, Boissonnas A, Delcayre A, Le Pecq JB, Combadière B, Amigorena S and Théry C: Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res 68(4): 1228-1235, 2008. (Pubitemid 351272243)
116. Chaput N, Andre F, Schartz NE, Flament C, Angevin E, Escudier B and Zitvogel L: Exosomes and anti-tumour immunotherapy. Bull Cancer 90(8-9): 695-698, 2003. (Pubitemid 37239072)
117. Butler TP and Gullino PM: Quantitation of cell shedding into efferent blood of mammary adenocarcinoma. Cancer Res 35(3): 512-516, 1975.
118. Schenck M, Ruebben H and Gulbins E: Molecular aspects of lymph node metastasis. Urologe A 48(1): 6-11, 2009.
119. Boardman KC and Swartz MA: Interstitial flow as a guide for lymphangiogenesis. Circ Res 92(7): 801-808, 2003. (Pubitemid 36457646)
120. Leu AJ, Berk DA, Lymboussaki A, Alitalo K and Jain RK: Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation. Cancer Res 60(16): 4324-4327, 2000. (Pubitemid 32103603)
121. Qian CN, Berghuis B, Tsarfaty G, Bruch M, Kort EJ, Ditlev J, Tsarfaty I, Hudson E, Jackson DG, Petillo D, Chen J, Resau JH and Teh BT: Preparing the 'soil': the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells. Cancer Res 66(21): 10365-10376, 2006. (Pubitemid 44799756)
122. Karpanen T and Alitalo K: Molecular biology and pathology of lymphangiogenesis. Annu Rev Pathol 3: 367-397, 2008. (Pubitemid 351488286)
123. Lee RT: Lessons from lymph. Flow-guided vessel formation. Circ Res 92: 701-703, 2003.
124. Helm CL, Fleury ME, Zisch AH, Boschetti F and Swartz MA: Synergy between interstitial flow and VEGF directs capillary morphogenesis in vitro through a gradient amplification mechanism. Proc Natl Acad Sci USA 102(44): 15779-15784, 2005. (Pubitemid 41552819)
125. Cao Y: Why and how do tumors stimulate lymphangiogenesis? Lymphat Res Biol 6(3-4): 145-148, 2008.