Microparticles mediated cross-talk between tumoral and endothelial cells promote the constitution of a pro-metastatic vascular niche through Arf6 up regulation

Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449(7162):557–563. doi:10.1038/nature06188 Lis R, Touboul C, Mirshahi P, Ali F, Mathew S, Nolan DJ, Maleki M, Abdalla SA, Raynaud CM, Querleu D, Al-Azwani E, Malek J, Mirshahi M, Rafii A (2011) Tumor associated mesenchymal stem cells protects ovarian cancer cells from hyperthermia through CXCL12. Int J Cancer 128(3):715–725. doi:10.1002/ijc.25619 Pasquier J, Galas L, Boulange-Lecomte C, Rioult D, Bultelle F, Magal P, Webb G, Le Foll F (2012) Different modalities of intercellular membrane exchanges mediate cell-to-cell p-glycoprotein transfers in MCF-7 breast cancer cells. J Biol Chem 287(10):7374–7387. doi:10.1074/jbc.M111.312157 Pasquier J, Magal P, Boulange-Lecomte C, Webb G, Le Foll F (2011) Consequences of cell-to-cell P-glycoprotein transfer on acquired multidrug resistance in breast cancer: a cell population dynamics model. Biol Direct 6:5. doi:10.1186/1745-6150-6-5 Rafii A, Mirshahi P, Poupot M, Faussat AM, Simon A, Ducros E, Mery E, Couderc B, Lis R, Capdet J, Bergalet J, Querleu D, Dagonnet F, Fournie JJ, Marie JP, Pujade-Lauraine E, Favre G, Soria J, Mirshahi M (2008) Oncologic trogocytosis of an original stromal cells induces chemoresistance of ovarian tumours. PLoS One 3(12):e3894. doi:10.1371/journal.pone.0003894 Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, Garcia-Santos G, Ghajar C, Nitadori-Hoshino A, Hoffman C, Badal K, Garcia BA, Callahan MK, Yuan J, Martins VR, Skog J, Kaplan RN, Brady MS, Wolchok JD, Chapman PB, Kang Y, Bromberg J, Lyden D (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18(6):883–891. doi:10.1038/nm.2753 Thery C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9(8):581–593. doi:10.1038/nri2567 Thery C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2(8):569–579. doi:10.1038/nri855 Pan BT, Johnstone RM (1983) Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33(3):967–978 D’Souza-Schorey C, Clancy JW (2012) Tumor-derived microvesicles: shedding light on novel microenvironment modulators and prospective cancer biomarkers. Genes Dev 26(12):1287–1299. doi:10.1101/gad.192351.112 Eldh M, Ekstrom K, Valadi H, Sjostrand M, Olsson B, Jernas M, Lotvall J (2010) Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA. PLoS One 5(12):e15353. doi:10.1371/journal.pone.0015353 Pelchen-Matthews A, Raposo G, Marsh M (2004) Endosomes, exosomes and Trojan viruses. Trends Microbiol 12(7):310–316. doi:10.1016/j.tim.2004.05.004 Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, Flament C, Pouzieux S, Faure F, Tursz T, Angevin E, Amigorena S, Zitvogel L (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7(3):297–303. doi:10.1038/85438 Gong J, Jaiswal R, Mathys JM, Combes V, Grau GE, Bebawy M (2012) Microparticles and their emerging role in cancer multidrug resistance. Cancer Treat Rev 38(3):226–234. doi:10.1016/j.ctrv.2011.06.005 Bebawy M, Combes V, Lee E, Jaiswal R, Gong J, Bonhoure A, Grau GE (2009) Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia 23(9):1643–1649. doi:10.1038/leu.2009.76 Kawamoto T, Ohga N, Akiyama K, Hirata N, Kitahara S, Maishi N, Osawa T, Yamamoto K, Kondoh M, Shindoh M, Hida Y, Hida K (2012) Tumor-derived microvesicles induce proangiogenic phenotype in endothelial cells via endocytosis. PLoS One 7(3):e34045. doi:10.1371/journal.pone.0034045 Svensson KJ, Kucharzewska P, Christianson HC, Skold S, Lofstedt T, Johansson MC, Morgelin M, Bengzon J, Ruf W, Belting M (2011) Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2-mediated heparin-binding EGF signaling in endothelial cells. Proc Natl Acad Sci U S A 108(32):13147–13152. doi:10.1073/pnas.1104261108 Li XB, Zhang ZR, Schluesener HJ, Xu SQ (2006) Role of exosomes in immune regulation. J Cell Mol Med 10(2):364–375 Pap E (2011) The role of microvesicles in malignancies. Adv Exp Med Biol 714:183–199. doi:10.1007/978-94-007-0782-5_10 Muralidharan-Chari V, Clancy JW, Sedgwick A, D’Souza-Schorey C (2010) Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 123(Pt 10):1603–1611. doi:10.1242/jcs.064386 Folkman J (2006) Angiogenesis. Ann Rev Med 57:1–18. doi:10.1146/annurev.med.57.121304.131306 Jayson GC, Hicklin DJ, Ellis LM (2012) Antiangiogenic therapy–evolving view based on clinical trial results. Nat Rev Clin Oncol 9(5):297–303. doi:10.1038/nrclinonc.2012.8 Rapisarda A, Melillo G (2012) Overcoming disappointing results with antiangiogenic therapy by targeting hypoxia. Nat Rev Clin Oncol 9(7):378–390. doi:10.1038/nrclinonc.2012.64 Ebos JM, Kerbel RS (2011) Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat Rev Clin Oncol 8(4):210–221. doi:10.1038/nrclinonc.2011.21 Sitohy B, Nagy JA, Dvorak HF (2012) Anti-VEGF/VEGFR therapy for cancer: reassessing the target. Cancer Res 72(8):1909–1914. doi:10.1158/0008-5472.CAN-11-3406 Ding BS, Nolan DJ, Guo P, Babazadeh AO, Cao Z, Rosenwaks Z, Crystal RG, Simons M, Sato TN, Worgall S, Shido K, Rabbany SY, Rafii S (2011) Endothelial-derived angiocrine signals induce and sustain regenerative lung alveolarization. Cell 147(3):539–553. doi:10.1016/j.cell.2011.10.003 Maretzky T, Evers A, Zhou W, Swendeman SL, Wong PM, Rafii S, Reiss K, Blobel CP (2011) Migration of growth factor-stimulated epithelial and endothelial cells depends on EGFR transactivation by ADAM17. Nat Commun 2:229. doi:10.1038/ncomms1232 Pasquier J, Guerrouahen BS, Al Thawadi H, Ghiabi P, Maleki M, Abu-Kaoud N, Jacob A, Mirshahi M, Galas L, Rafii S, Le Foll F, Rafii A (2013) Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J Transl Med 11:94. doi:10.1186/1479-5876-11-94 Pasquier J, Rafii A (2013) Role of the microenvironment in ovarian cancer stem cell maintenance. Biomed Res Int 2013:630782. doi:10.1155/2013/630782 Folkman J (2001) Angiogenesis-dependent diseases. Semin Oncol 28(6):536–542 Nguyen M, Watanabe H, Budson AE, Richie JP, Hayes DF, Folkman J (1994) Elevated levels of an angiogenic peptide, basic fibroblast growth factor, in the urine of patients with a wide spectrum of cancers. J Nat Cancer Inst 86(5):356–361 Rak JW, Hegmann EJ, Lu C, Kerbel RS (1994) Progressive loss of sensitivity to endothelium-derived growth inhibitors expressed by human melanoma cells during disease progression. J Cell Physiol 159(2):245–255. doi:10.1002/jcp.1041590208 Lu J, Ye X, Fan F, Xia L, Bhattacharya R, Bellister S, Tozzi F, Sceusi E, Zhou Y, Tachibana I, Maru DM, Hawke DH, Rak J, Mani SA, Zweidler-McKay P, Ellis LM (2013) Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 23(2):171–185. doi:10.1016/j.ccr.2012.12.021 Antonyak MA, Li B, Boroughs LK, Johnson JL, Druso JE, Bryant KL, Holowka DA, Cerione RA (2011) Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc Natl Acad Sci U S A 108(12):4852–4857. doi:10.1073/pnas.1017667108 Katsuno Y, Lamouille S, Derynck R (2013) TGF-beta signaling and epithelial-mesenchymal transition in cancer progression. Curr Opin Oncol 25(1):76–84. doi:10.1097/CCO.0b013e32835b6371 Weng L, Enomoto A, Ishida-Takagishi M, Asai N, Takahashi M (2010) Girding for migratory cues: roles of the Akt substrate Girdin in cancer progression and angiogenesis. Cancer Sci 101(4):836–842. doi:10.1111/j.1349-7006.2009.01487.x Garnier D, Magnus N, Lee TH, Bentley V, Meehan B, Milsom C, Montermini L, Kislinger T, Rak J (2012) Cancer cells induced to express mesenchymal phenotype release exosome-like extracellular vesicles carrying tissue factor. J Biol Chem 287(52):43565–43572. doi:10.1074/jbc.M112.401760 Seandel M, Butler JM, Kobayashi H, Hooper AT, White IA, Zhang F, Vertes EL, Kobayashi M, Zhang Y, Shmelkov SV, Hackett NR, Rabbany S, Boyer JL, Rafii S (2008) Generation of a functional and durable vascular niche by the adenoviral E4ORF1 gene. Proc Natl Acad Sci U S A 105(49):19288–19293. doi:10.1073/pnas.0805980105 Muralidharan-Chari V, Clancy J, Plou C, Romao M, Chavrier P, Raposo G, D’Souza-Schorey C (2009) ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Current Biol: CB 19(22):1875–1885. doi:10.1016/j.cub.2009.09.059 Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, Seabra MC, Darchen F, Amigorena S, Moita LF, Thery C (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12(1):19–30. doi:10.1038/ncb2000, sup pp 11-13 Bianco F, Perrotta C, Novellino L, Francolini M, Riganti L, Menna E, Saglietti L, Schuchman EH, Furlan R, Clementi E, Matteoli M, Verderio C (2009) Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J 28(8):1043–1054. doi:10.1038/emboj.2009.45 Tysnes BB (2010) Tumor-initiating and -propagating cells: cells that we would like to identify and control. Neoplasia 12(7):506–515 Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100(7):3983–3988. doi:10.1073/pnas.0530291100 Bapat SA, Mali AM, Koppikar CB, Kurrey NK (2005) Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 65(8):3025–3029. doi:10.1158/0008-5472.CAN-04-3931 Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J (2009) Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci U S A 106(10):3794–3799. doi:10.1073/pnas.0804543106 Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringner M, Morgelin M, Bourseau-Guilmain E, Bengzon J, Belting M (2013) Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci U S A 110(18):7312–7317. doi:10.1073/pnas.1220998110 Corrado C, Flugy AM, Taverna S, Raimondo S, Guggino G, Karmali R, De Leo G, Alessandro R (2012) Carboxyamidotriazole-orotate inhibits the growth of imatinib-resistant chronic myeloid leukaemia cells and modulates exosomes-stimulated angiogenesis. PLoS One 7(8):e42310. doi:10.1371/journal.pone.0042310 Park JO, Choi DY, Choi DS, Kim HJ, Kang JW, Jung JH, Lee JH, Kim J, Freeman MR, Lee KY, Gho YS, Kim KP (2013) Identification and characterization of proteins isolated from microvesicles derived from human lung cancer pleural effusions. Proteomics 13(14):2125–2134. doi:10.1002/pmic.201200323 Raimondo F, Morosi L, Chinello C, Magni F, Pitto M (2011) Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery. Proteomics 11(4):709–720. doi:10.1002/pmic.201000422 Chlebowski A, Lubas M, Jensen TH, Dziembowski A (2013) RNA decay machines: the exosome. Biochim Biophys Acta 1829(6–7):552–560. doi:10.1016/j.bbagrm.2013.01.006 Hogan MC, Johnson KL, Zenka RM, Cristine Charlesworth M, Madden BJ, Mahoney DW, Oberg AL, Huang BQ, Leontovich AA, Nesbitt LL, Bakeberg JL, McCormick DJ, Robert Bergen H, Ward CJ (2013) Subfractionation, characterization, and in-depth proteomic analysis of glomerular membrane vesicles in human urine. Kidney Int. doi:10.1038/ki.2013.422 Inal JM, Kosgodage U, Azam S, Stratton D, Antwi-Baffour S, Lange S (2013) Blood/plasma secretome and microvesicles. Biochim Biophys Acta 1834(11):2317–2325. doi:10.1016/j.bbapap.2013.04.005 Chaput N, Thery C (2011) Exosomes: immune properties and potential clinical implementations. Sem Immunopathol 33(5):419–440. doi:10.1007/s00281-010-0233-9 Ji H, Greening DW, Barnes TW, Lim JW, Tauro BJ, Rai A, Xu R, Adda C, Mathivanan S, Zhao W, Xue Y, Xu T, Zhu HJ, Simpson RJ (2013) Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics 13(10–11):1672–1686. doi:10.1002/pmic.201200562 Tauro BJ, Greening DW, Mathias RA, Mathivanan S, Ji H, Simpson RJ (2013) Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids. Mol Cell Proteomics : MCP 12(3):587–598. doi:10.1074/mcp.M112.021303 Taraboletti G, D’Ascenzo S, Giusti I, Marchetti D, Borsotti P, 2Millimaggi D, Giavazzi R, Pavan A, Dolo V (2006) Bioavailability of VEGF in tumor-shed vesicles depends on vesicle burst induced by acidic pH. Neoplasia 8(2):96–103. doi:10.1593/neo.05583 Martin D, Galisteo R, Gutkind JS (2009) CXCL8/IL8 stimulates vascular endothelial growth factor (VEGF) expression and the autocrine activation of VEGFR2 in endothelial cells by activating NFkappaB through the CBM (Carma3/Bcl10/Malt1) complex. J Biol Chem 284(10):6038–6042. doi:10.1074/jbc.C800207200 Matte I, Lane D, Laplante C, Rancourt C, Piche A (2012) Profiling of cytokines in human epithelial ovarian cancer ascites. Am J Cancer Res 2(5):566–580 Wang Y, Xu RC, Zhang XL, Niu XL, Qu Y, Li LZ, Meng XY (2012) Interleukin-8 secretion by ovarian cancer cells increases anchorage-independent growth, proliferation, angiogenic potential, adhesion and invasion. Cytokine+ 59(1):145–155. doi:10.1016/j.cyto.2012.04.013 Andrae J, Gallini R, Betsholtz C (2008) Role of platelet-derived growth factors in physiology and medicine. Genes Dev 22(10):1276–1312. doi:10.1101/gad.1653708 Machens HG, Morgan JR, Berthiaume F, Stefanovich P, Siemers F, Krapohl B, Berger A, Mailander P (2002) Platelet-derived growth factor-AA-mediated functional angiogenesis in the rat epigastric island flap after genetic modification of fibroblasts is ischemia dependent. Surgery 131(4):393–400 Zhang J, Cao R, Zhang Y, Jia T, Cao Y, Wahlberg E (2009) Differential roles of PDGFR-alpha and PDGFR-beta in angiogenesis and vessel stability. FASEB J : Off Pub Fed Am Soc Exp Biol 23(1):153–163. doi:10.1096/fj.08-113860 Li S, Hu GF (2012) Emerging role of angiogenin in stress response and cell survival under adverse conditions. J Cell Physiol 227(7):2822–2826. doi:10.1002/jcp.23051 Tello-Montoliu A, Patel JV, Lip GY (2006) Angiogenin: a review of the pathophysiology and potential clinical applications. J Thromb Haemos : JTH 4(9):1864–1874. doi:10.1111/j.1538-7836.2006.01995.x Kishimoto K, Liu S, Tsuji T, Olson KA, Hu GF (2005) Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis. Oncogene 24(3):445–456. doi:10.1038/sj.onc.1208223 Campo L, Turley H, Han C, Pezzella F, Gatter KC, Harris AL, Fox SB (2005) Angiogenin is up-regulated in the nucleus and cytoplasm in human primary breast carcinoma and is associated with markers of hypoxia but not survival. J Pathol 205(5):585–591. doi:10.1002/path.1740 Larsen AK, Ouaret D, El Ouadrani K, Petitprez A (2011) Targeting EGFR and VEGF(R) pathway cross-talk in tumor survival and angiogenesis. Pharmacol Ther 131(1):80–90. doi:10.1016/j.pharmthera.2011.03.012 Young K, Conley B, Romero D, Tweedie E, O’Neill C, Pinz I, Brogan L, Lindner V, Liaw L, Vary CP (2012) BMP9 regulates endoglin-dependent chemokine responses in endothelial cells. Blood 120(20):4263–4273. doi:10.1182/blood-2012-07-440784 Lv LH, Wan YL, Lin Y, Zhang W, Yang M, Li GL, Lin HM, Shang CZ, Chen YJ, Min J (2012) Anticancer drugs cause release of exosomes with heat shock proteins from human hepatocellular carcinoma cells that elicit effective natural killer cell antitumor responses in vitro. J Biol Chem 287(19):15874–15885. doi:10.1074/jbc.M112.340588 Corcoran C, Rani S, O’Brien K, O’Neill A, Prencipe M, Sheikh R, Webb G, McDermott R, Watson W, Crown J, O’Driscoll L (2012) Docetaxel-resistance in prostate cancer: evaluating associated phenotypic changes and potential for resistance transfer via exosomes. PLoS One 7(12):e50999. doi:10.1371/journal.pone.0050999 Azmi AS, Bao B, Sarkar FH (2013) Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev. doi:10.1007/s10555-013-9441-9 Jaiswal R, Luk F, Dalla PV, Grau GE, Bebawy M (2013) Breast cancer-derived microparticles display tissue selectivity in the transfer of resistance proteins to cells. PLoS One 8(4):e61515. doi:10.1371/journal.pone.0061515 Press JZ, Reyes M, Pitteri SJ, Pennil C, Garcia R, Goff BA, Hanash SM, Swisher EM (2012) Microparticles from ovarian carcinomas are shed into ascites and promote cell migration. Int J Gynecol Cancer : Off J Int Gynecol Cancer Soc 22(4):546–552. doi:10.1097/IGC.0b013e318241d9b9 Galindo-Hernandez O, Villegas-Comonfort S, Candanedo F, Gonzalez-Vazquez MC, Chavez-Ocana S, Jimenez-Villanueva X, Sierra-Martinez M, Salazar EP (2013) Elevated concentration of microvesicles isolated from peripheral blood in breast cancer patients. Arch Med Res 44(3):208–214. doi:10.1016/j.arcmed.2013.03.002 Thery C, Amigorena S, Raposo G, Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3:Unit 3 22. doi:10.1002/0471143030.cb0322s30 Touboul C, Lis R, Al Farsi H, Raynaud CM, Warfa M, Althawadi H, Mery E, Mirshahi M, Rafii A (2013) Mesenchymal stem cells enhance ovarian cancer cell infiltration through IL6 secretion in an amniochorionic membrane based 3D model. J Transl Med 11:28. doi:10.1186/1479-5876-11-28 Benelli R, Albini A (1999) In vitro models of angiogenesis: the use of Matrigel. Int J Biol Markers 14(4):243–246