Tracking miRNAs' footprints in tumor-microenvironment interactions: Insights and implications for targeted cancer therapy

Genes Chromosomes and Cancer

Volumn 54, Issue 6, 2015, Pages 335-352

  Nouraee, Nazila ^a   Mowla, Seyed Javad ^a   Calin, George A ^b  

^a TARBIAT MODARES UNIVERSITY   (Iran)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; ANTINEOPLASTIC AGENT;

ANGIOGENESIS; ARTICLE; CANCER ASSOCIATED FIBROBLAST; CANCER RESISTANCE; CANCER THERAPY; CARCINOGENESIS; EXOSOME; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; MOLECULARLY TARGETED THERAPY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; STROMA CELL; TUMOR CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; CANCER STEM CELL; DISEASE COURSE; INFLAMMATION; METABOLISM; NEOPLASMS; NEOVASCULARIZATION (PATHOLOGY);

ANTINEOPLASTIC AGENTS; CARCINOGENESIS; DISEASE PROGRESSION; EXOSOMES; EXTRACELLULAR MATRIX; HUMANS; INFLAMMATION; MICRORNAS; NEOPLASMS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; TUMOR MICROENVIRONMENT;

EID: 84928089576     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.22244     Document Type: Article

References (153)

1. Aprelikova O, Yu X, Palla J, Wei B, John S, Yi M, Stephens R, Simpson R, Risinger J, Jazaeri A, Niederhuber J. 2010. The role of miR-31 and its target gene SATB2 in cancer-associated fibroblasts. Cell Cycle 9:4387-4398.
2. Aprelikova O, Palla J, Hibler B, Yu X, Greer Y, Yi M, Stephens R, Maxwell G, Jazaeri A, Risinger J, Rubin J, Niederhuber J. 2013. Silencing of miR-148a in cancer-associated fibroblasts results in WNT10B-mediated stimulation of tumor cell motility. Oncogene 23:3246-3253.
3. Asangani I, Rasheed S, Nikolova D, Leupold J, Colburn N, Post S, Allgayer H. 2008. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27:2128-2136.
4. Atay S, Godwin A. 2014. Tumor-derived exosomes: A message delivery system for tumor progression. Commun Integr Biol 7:e28231.
5. Aushev V, Zborovskaya I, Laktionov K, Girard N, Cros M, Herceg Z, Krutovskikh V. 2013. Comparisons of microRNA patterns in plasma before and after tumor removal reveal new biomarkers of lung squamous cell carcinoma. PLoS One 8:e78649.
6. Ayala G, Tuxhorn J, Wheeler T, Frolov A, Scardino P, Ohori M, Wheeler M, Spitler J, Rowley D. 2003. Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer. Clin Cancer Res 9:4792-4801.
7. Bader A. 2012. miR-34-A microRNA replacement therapy is headed to the clinic. Front Genet 3:120.
8. Balkwill F. 2009. Tumour necrosis factor and cancer. Nat Rev Cancer 9:361-371.
9. Banerjee S, Xie N, Cui H, Tan Z, Yang S, Icyuz M, Abraham E, Liu G. 2013. MicroRNA let-7c regulates macrophage polarization. J Immunol 190:6542-6549.
10. Banyard J, Chung I, Wilson A, Vetter G, Bechec N, Bielenberg D, Zetter B. 2013. Regulation of epithelial plasticity by miR-424 and miR-200 in a new prostate cancer metastasis model. Sci Rep 3:3151.
11. Bergers G, Hanahan D. 2008. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 8:592-603.
12. Bobrie AC, Colombo M, Raposo G, Thery C. 2011. Exosome secretion: Molecular mechanisms and roles in immune responses. Traffic 12:1659-1668.
13. Bouchie A. 2013. First microRNA mimic enters clinic. Nat Biotechnol 31:577.
14. Bronisz A, Godlewski J, Wallace J, Merchant A, Nowicki M, Mathsyaraja H, Srinivasan R, Trimboli A, Martin C, Li F, Yu L, Fernandez S, Pecot T, Rosol T, Cory S, Hallett M, Park M, Piper M, Marsh C, Yee L, Jimenez R, Nuovo G, Lawler S, Chiocca E, Leone G, Ostrowski M. 2011. Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320. Nat Cell Biol 14:159-167.
15. Bruning U, Cerone L, Neufeld Z, Fitzpatrick S, Cheong A, Scholz C, Simpson D, Leonard M, Tambuwala M, Cummins E, Taylor C. 2011. MicroRNA-155 promotes resolution of hypoxia-inducible factor 1α activity during prolonged hypoxia. Mol Cell Biol 31:4087-4096.
16. Calin G, Croce C. 2006. MicroRNA signatures in human cancers. Nat Rev Cancer 6:857-866.
17. Castellana D, Zobairi F, Martinez M, Panaro M, Mitolo V, Freyssinet J, Kunzelmann C. 2009. Membrane microvesicles as actors in the establishment of a favorable prostatic tumoral niche: A role for activated fibroblasts and CX3CL1-CX3CR1 axis. Cancer Res 69:785-793.
18. Chan Y, Khanna S, Roy S, Sen C. 2011. miR-200b targets Ets-1 and is down-regulated by hypoxia to induce angiogenic response of endothelial cells. J Biol Chem 286:2047-2056.
19. Chen L, Li Y, Fu Y, Peng J, Mo M, Stamatakos M, Teal C, Brem R, Stojadinovic A, Grinkemeyer M, McCaffrey T, Man Y, Fu S. 2013. Role of deregulated microRNAs in breast cancer progression using FFPE tissue. PLoS One 8:e54213.
20. Cortez M, Valdecanas D, Zhang X, Zhan Y, Bhardwaj V, Calin G, Komaki R, Giri D, Quini C, Wolfe T, Peltier H, Bader A, Heymach J, Meyn R, Welsh J. 2014. Therapeutic delivery of miR-200c enhances radiosensitivity in lung cancer. Mol Ther 22:1494-1503.
21. De Paula D, Bentley M, Mahato R. 2007. Hydrophobization and bioconjugation for enhanced siRNA delivery and targeting. RNA 13:431-456.
22. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth E, Lee W, Enders G, Mendell J, Tikhonenko A. 2006. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38:1060-1065.
23. Donnem T, Fenton C, Lonvik K, Berg T, Eklo K, Andersen S, Stenvold H, Shibli K, Saad S, Bremnes R, Busund L. 2012. MicroRNA signatures in tumor tissue related to angiogenesis in non-small cell lung cancer. PLoS One 7:e29671.
24. Ellis L, Hicklin D. 2008. VEGF-targeted therapy: Mechanisms of anti-tumour activity. Nat Rev Cancer 8:579-591.
25. Elmen J, Lindow M, Schutz S, Lawrence M, Petri A, Obad S, Lindholm M, Hedtjarn M, Hansen H, Berger U, Gullans S, Kearney P, Sarnow P, Straarup E, Kauppinen S. 2008. LNA-mediated microRNA silencing in non-human primates. Nature 452:896-900.
26. Fabbri M. 2012. TLRs as miRNA receptors. Cancer Res 72:6333-6337.
27. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, Lovat F, Fadda P, Mao C, Nuovo G, Zanesi N, Crawford M, Ozer G, Wernicke D, Alder H, Caligiuri M, Nana-Sinkam P, Perrotti D, Croce C. 2012. microRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 109:E2110-E2116.
28. Ferrara N, Hillan K, Gerber H, Novotny W. 2004. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov 3:391-400.
29. Folini M, Gandellini P, Longoni N, Profumo V, Callari M, Pennati M, Colecchia M, Supino R, Veneroni S, Salvioni R, Valdagni R, Daidone M, Zaffaroni N. 2010. miR-21: An oncomir on strike in prostate cancer. Mol Cancer 9:12.
30. Gibbings D, Ciaudo C, Erhardt M, Voinnet O. 2009. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11:1143-1149.
31. Godfrey A, Xu Z, Weinberg C, Getts R, Wade P, DeRoo L, Sandler D, Taylor J. 2013. Serum microRNA expression as an early marker for breast cancer risk in prospectively collected samples from the Sister Study cohort. Breast Cancer Res 15:R42.
32. Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus M, Tetta C, Bussolati B, Camussi G. 2011. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 71:5346-5356.
33. Gregory P, Bert A, Paterson E, Barry S, Tsykin A, Farshid G, Vadas M, Khew-Goodall Y, Goodall G. 2008. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10:593-601.
34. Grivennikov S, Karin M. 2011. Inflammatory cytokines in cancer: Tumour necrosis factor and interleukin 6 take the stage. Ann Rheum Dis 70:i104-i108.
35. Hanke M, Hoefig K, Merz H, Feller A, Kausch I, Jocham D, Warnecke J, Sczakiel G. 2010. A robust methodology to study urine microRNA as tumor marker: MicroRNA-126 and microRNA-182 are related to urinary bladder cancer. Urol Oncol 28:655-661.
36. Hayata K, Iwahashi M, Ojima T, Katsuda M, Iida T, Nakamori M, Ueda K, Nakamura M, Miyazawa M, Tsuji T, Yamaue H. 2013. Inhibition of IL-17A in tumor microenvironment augments cytotoxicity of tumor-infiltrating lymphocytes in tumor-bearing Mice. PLoS One 8:e53131.
37. Hu S, Huang M, Li Z, Jia F, Ghosh Z, Lijkwan M, Fasanaro P, Sun N, Wang X, Martelli F, Robbins R, Wu J. 2010. MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation 122:S124-S131.
38. Hu S, Zhu W, Zhang L, Pei M, Liu M. 2014. MicroRNA-155 broadly orchestrates inflammation-induced changes of microRNA expression in breast cancer. Cell Res 24:254-257.
39. Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S, Egan D, Li A, Huang G, Klein-Szanto A, Gimotty P, Katsaros D, Coukos G, Zhang L, Pure E, Agami R. 2008. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol 10:202-210.
40. Huang X, Ding L, Bennewith K, Tong R, Welford S, Ang K, Story M, Le Q, Giaccia A. 2009. Hypoxia inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 35:856-867.
41. Huang X, Le Q, Giaccia A. 2010. miR-210, micromanager of the hypoxia pathway. Trends Mol Med 16:230-237.
42. Huang Y, Yuan J, Righi E, Kamoun W, Ancukiewicz M, Nezivar J, Santosuosso M, Martin J, Martin M, Vianello F, Leblanc P, Munn L, Huang P, Duda D, Fukumura D, Jain R, Poznansky M. 2012. Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc Natl Acad Sci USA 109:17561-17566.
43. Iliopoulos D, Jaeger S, Hirsch H, Bulyk M, Struhl K. 2010. STAT3 activation of miR-21 and miR-181b-1, via PTEN and CYLD, are part of the epigenetic switch linking inflammation to cancer. Mol Cell 39:493-506.
44. Ivey K, Muth A, Arnold J, King F, Yeh R, Fish J, Hsiao E, Schwartz R, Conklin B, Bernstein H, Srivastava D. 2008. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2:219-229.
45. Ivy S, Wick J, Kaufman B. 2009. An overview of small-molecule inhibitors of VEGFR signaling. Nat Rev Clin Oncol 6:569-579.
46. Jain R. 2005. Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 307:58-62.
47. Jakob P, Doerries C, Briand S, Mocharla P, Krankel N, Besler C, Mueller M, Manes C, Templin C, Baltes C, Rudin M, Adams H, Wolfrum M, Noll G, Ruschitzka F, Luscher T, Landmesser U. 2012. Loss of angiomiR-126 and 130a in angiogenic early outgrowth cells from patients with chronic heart failure: Role for impaired in vivo neovascularization and cardiac repair capacity. Circulation 126:2962-2975.
48. Joyce J, Pollard J. 2009. Microenvironmental regulation of metastasis. Nat Rev Cancer 9:239-252.
49. Kalluri R, Zeisberg M. 2006. Fibroblasts in cancer. Nat Rev Cancer 6:392-401.
50. Karin M. 2006. Nuclear factor-κB in cancer development and progression. Nature 441:43143-43146.
51. Kasinski A, Slack F. 2012. miRNA-34 prevents cancer initiation and progression in a therapeutically resistant K-ras and p53-induced mouse model of lung adenocarcinoma. Cancer Res 72:5576-5587.
52. Kent O, McCall M, Cornish T, Halushka M. 2014. Lessons from miR-143/145: The importance of cell-type localization of miRNAs. Nucleic Acids Res 42:7528-7538.
53. Kharaziha P, Rodriguez P, Li Q, Rundqvist H, Bjorklund A-C, Augsten M, Ullen A, Egevad L, Wiklund P, Nilsson S, Kroemer G, Grander D, Panaretakis T. 2012. Targeting of distinct signaling cascades and cancer-associated fibroblasts define the efficacy of Sorafenib against prostate cancer cells. Cell Death Dis 3:e262.
54. Klampfer L. 2011. Cytokines, inflammation and colon cancer. Curr Cancer Drug Targets 11:451-464.
55. Korpal M, Lee E, Hu G, Kang Y. 2008. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 283:14910-14914.
56. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. 2010. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285:17442-17452.
57. Kosaka N, Iguchi H, Hagiwara K, Yoshioka Y, Takeshita F, Ochiya T. 2013. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J Biol Chem 288:10849-10859.
58. Kredo-Russo S, Hornstein E. 2011. MicroRNA knock down by cholesterol-conjugated antisense oligos in mouse organ culture. Methods Mol Biol 732:89-97.
59. Kulshreshtha R, Ferracin M, Wojcik S, Garzon R, Alder H, Agosto-Perez F, Davuluri R, Liu C, Croce C, Negrini M, Calin G, Ivan M. 2007. A microRNA signature of hypoxia. Mol Cell Biol 27:1859-1867.
60. Lee J, Park S, Jung B, Jeon Y, Lee Y, Kim M, Kim Y, Jang J, Kim C. 2013. Exosomes derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells. PLoS One 8:e84256.
61. Lehmann S, Kruger C, Park B, Derkow K, Rosenberger K, Baumgart J, Trimbuch T, Eom G, Hinz M, Kaul D, Habbel P, Kalin R, Franzoni E, Rybak A, Nguyen D, Veh R, Ninnemann O, Peters O, Nitsch R, Heppner F, Golenbock D, Schott E, Ploegh H, Wulczyn F, Lehnardt S. 2012. An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat Neurosci 15:827-835.
62. Lei Z, Li B, Yang Z, Fang H, Zhang G, Feng Z, Huang B. 2009. Regulation of HIF-1α and VEGF by miR-20b tunes tumor cells to adapt to the alteration of oxygen concentration. PLoS One 4:e7629.
63. Li N, Fu H, Tie Y, Hu Z, Kong W, Wu Y, Zheng X. 2009. miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett 275:44-53.
64. Li Q, Zhang D, Wang Y, Sun P, Hou X, Larner J, Xiong W, Mi J. 2013. miR-21/Smad 7 signaling determines TGF-β1-induced CAF formation. Sci Rep 3:2038.
65. Litz J, Krystal G. 2006. Imatinib inhibits c-Kit-induced hypoxia-inducible factor-1α activity and vascular endothelial growth factor expression in small cell lung cancer cells. Mol Cancer Ther 5:1415-1422.
66. Liu L, Li C, Chen Q, Jing Y, Carpenter R, Jiang Y, Kung H, Lai L, Jiang B. 2011. miR-21 induced angiogenesis through AKT and ERK activation and HIF-1α expression. PLoS One 6:e19139.
67. Loayza-Puch F, Yoshida Y, Matsuzaki T, Takahashi C, Kitayama H, Noda M. 2010. Hypoxia and RAS-signaling pathways converge on, and cooperatively downregulate, the RECK tumor-suppressor protein through microRNAs. Oncogene 29:2638-2648.
68. Loffler D, Brocke-Heidrich K, Pfeifer G, Stocsits C, Hackermuller J, Kretzschmar A, Burger R, Gramatzki M, Blumert C, Bauer K, Cvijic H, Ullmann A, Stadler P, Horn F. 2007. Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 110:1330-1333.
69. Lou Y, Guo F, Liu F, Gao F, Zhang P, Niu X, Guo S, Yin J, Wang Y, Deng Z. 2012. miR-210 activates notch signaling pathway in angiogenesis induced by cerebral ischemia. Mol Cell Biochem 370:45-51.
70. Lu Z, Liu M, Stribinskis V, Klinge C, Ramos K, Colburn N, Li Y. 2008. MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene 27:4373-4379.
71. Luedde T. 2010. MicroRNA-151 and its hosting gene FAK (focal adhesion kinase) regulate tumor cell migration and spreading of hepatocellular carcinoma. Hepatology 52:1164-1166.
72. Ma L, Teruya-Feldstein J, Weinberg R. 2007. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449:682-688.
73. Madhusudan S, Muthuramalingam S, Braybrooke J, Wilner S, Kaur K, Han C, Hoare S, Balkwill F, Ganesan T. 2005. Study of etanercept, a tumor necrosis factor-α inhibitor, in recurrent ovarian cancer. J Clin Oncol 23:5950-5959.
74. Maia M, DeVriese A, Janssens T, Moons M, Lories R, Tavernier J, Conway E. 2011. CD248 facilitates tumor growth via its cytoplasmic domain. BMC Cancer 11:162.
75. Marcus M, Leonard J. 2013. FedExosomes: Engineering therapeutic biological nanoparticles that truly deliver. Pharmaceuticals (Basel) 6:659-680.
76. Michor F, Liphardt J, Ferrari M, Widom J. 2011. What does physics have to do with cancer? Nat Rev Cancer 11:657-670.
77. Mitra A, Zillhardt M, Hua Y, Tiwari P, Murmann A, Peter M, Lengyel E. 2012. MicroRNAs reprogram normal fibroblasts into cancer-associated fibroblasts in ovarian cancer. Cancer Discov 2:1100-1108.
78. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez C, Sanchez-Cabo F, Gonzalez M, Bernad A, Sanchez-Madrid F. 2011. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2:282.
79. Momen-Heravi F, Bala S, Bukong T, Szabo G. 2014. Exosome-mediated delivery of functionally active miRNA-155 inhibitor to macrophages. Nanomedicine 10:1517-1527.
80. Montecalvo A, Larregina A, Shufesky W, Stolz D, Sullivan M, Karlsson J, Baty C, Gibson G, Erdos G, Wang Z, Milosevic J, Tkacheva O, Divito S, Jordan R, Lyons-Weiler J, Watkins S, Morelli A. 2012. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119:756-766.
81. Munoz J, Bliss S, Greco S, Ramkissoon S, Ligon K, Rameshwar P. 2013. Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Mol Ther Nucleic Acids 2:e126.
82. Musumeci M, Coppola V, Addario A, Patrizii M, Maugeri-Sacca M, Memeo L, Colarossi C, Francescangeli F, Biffoni M, Collura D, Giacobbe A, D'Urso L, Falchi M, Venneri M, Muto G, De Maria R, Bonci D. 2011. Control of tumor and microenvironment cross-talk by miR-15a and miR-16 in prostate cancer. Oncogene 30:4231-4242.
83. Nagel R, le Sage C, Diosdado B, van der Waal M, Oude Vrielink J, Bolijn A, Meijer GA, Agami R. 2008. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 68:5795-5802.
84. Nishida N, Nagahara M, Sato T, Mimori K, Sudo T, Tanaka F, Shibata K, Ishii H, Sugihara K, Doki Y, Mori M. 2012. Microarray analysis of colorectal cancer stromal tissue reveals upregulation of two oncogenic miRNA clusters. Clin Cancer Res 18:3054-3070.
85. Nouraee N, Van Roosbroeck K, Vasei M, Semnani S, Samaei N, Naghshvar F, Omidi A, Calin G, Mowla SJ. 2013. Expression, tissue distribution and function of miR-21 in esophageal squamous cell carcinoma. PLoS One 8:e73009.
86. Ohno S, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, Fujita K, Mizutani T, Ohgi T, Ochiya T, Gotoh N, Kuroda M. 2013. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 21:185-191.
87. Papagiannakopoulos T, Shapiro A, Kosik K. 2008. MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 68:8164-8172.
88. Paranjape T, Slack F, Weidhaas J. 2009. MicroRNAs: Tools for cancer diagnostics. Gut 58:1546-1554.
89. Park S, Lee J, Ha M, Nam J, Kim V. 2009. miR-29 miRNAs activate p53 by targeting p85α and CDC42. Nat Struct Mol Biol 16:23-29.
90. Pegtel D, Cosmopoulos K, Thorley-Lawson D, van Eijndhoven M, Hopmans E, Lindenberg J, de Gruijl T, Wurdinger T, Middeldorp J. 2010. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107:6328-6333.
91. Pencheva N, Tran H, Buss C, Huh D, Drobnjak M, Busam K, Tavazoie S. 2012. Convergent multi-miRNA targeting of ApoE drives LRP1/LRP8-dependent melanoma metastasis and angiogenesis. Cell 151:1068-1082.
92. Plummer P, Freeman R, Taft R, Vider J, Sax M, Umer B, Gao D, Johns C, Mattick J, Wilton S, Ferro V, McMillan N, Swarbrick A, Mittal V, Mellick A. 2013. MicroRNAs regulate tumor angiogenesis modulated by endothelial progenitor cells. Cancer Res 73:341-352.
93. Png K, Halberg N, Yoshida M, Tavazoie S. 2011. A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells. Nature 481:190-194.
94. Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, Rainaldi G. 2006. MicroRNAs modulate the angiogenic properties of HUVECs. Blood 108:3068-3071.
95. Rana S, Malinowska K, Zoller M. 2013. Exosomal tumor microRNA modulates premetastatic organ cells. Neoplasia 15:281-295.
96. Ratner M. 2004. Genentech discloses safety concerns over Avastin. Nat Biotechnol 22:1198.
97. Renthal N, Chen C, Williams K, Gerard R, Prange-Kiel J, Mendelson C. 2010. miR-200 family and targets, ZEB1 and ZEB2, modulate uterine quiescence and contractility during pregnancy and labor. Proc Natl Acad Sci USA 107:20828-20833.
98. Roma-Rodrigues C, Fernandes A, Baptista P. 2014. Exosome in tumour microenvironment: Overview of the crosstalk between normal and cancer cells. Biomed Res Int 2014:179486.
99. Ryu J, Hong S, Karikari C, Hruban R, Goggins M, Maitra A. 2010. Aberrant microRNA-155 expression is an early event in the multistep progression of pancreatic adenocarcinoma. Pancreatology 10:66-73.
100. Schetter A, Harris C. 2011. Alterations of microRNAs contribute to colon carcinogenesis. Semin Oncol 38:734-742.
101. Schetter A, Nguyen G, Bowman E, Mathe E, Yuen S, Hawkes J, Croce C, Leung S, Harris C. 2009. Association of inflammation-related and microRNA gene expression with cancer-specific mortality of colon adenocarcinoma. Clin Cancer Res 15:5878.
102. Schmid M, Varner J. 2010. Myeloid cells in the tumor microenvironment: Modulation of tumor angiogenesis and tumor inflammation. J Oncol 2010:201026.
103. Schmitt M, Margue C, Behrmann I, Kreis S. 2013. MiRNA-29: A microRNA family with tumor-suppressing and immune-modulating properties. Curr Mol Med 13:572-585.
104. Schwarzenbach H, Hoon D, Pantel K. 2011. Cell-free nucleic acids as biomarkers in cancer patients. Nat Rev Cancer 11:426-437.
105. Shen X, Fang J, Lv X, Pei Z, Wang Y, Jiang S, Ding K. 2011. Heparin impairs angiogenesis through inhibition of microRNA-10b. J Biol Chem 286:26616-26627.
106. Shen G, Li X, Jia Y, Piazza G, Xi Y. 2013. Hypoxia-regulated microRNAs in human cancer. Acta Pharmacol Sin 34:336-341.
107. Shimbo K, Miyaki S, Ishitobi H, Kato Y, Kubo T, Shimose S, Ochi M. 2014. Exosome-formed synthetic microRNA-143 is transferred to osteosarcoma cells and inhibits their migration. Biochem Biophys Res Commun 445:381-387.
108. Soon P, Kiaris H. 2013. MicroRNAs in the tumour microenvironment: Big role for small players. Endocr Relat Cancer 20:R257-R267.
109. Squadrito M, Pucci F, Magri L, Moi D, Gilfillan G, Ranghetti A, Casazza A, Mazzone M, Lyle R, Naldini L, De Palma M. 2012. miR-511-3p modulates genetic programs of tumor-associated macrophages. Cell Rep 1:141-154.
110. Stoorvogel W. 2012. Functional transfer of microRNA by exosomes. Blood 119:646-648.
111. Suarez Y, Fernandez-Hernando C, Pober J, Sessa W. 2007. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 100:1164-1173.
112. Swartz M, Lund A. 2012. Lymphatic and interstitial flow in the tumour microenvironment: Linking mechanobiology with immunity. Nat Rev Cancer 12:210-219.
113. Swartz M, Iida N, Roberts E, Sangaletti S, Wong M, Yull F, Coussens L, DeClerck Y. 2012. Tumor microenvironment complexity: Emerging roles in cancer therapy. Cancer Res 72:2473-2480.
114. Tabet F, Vickers K, Cuesta Torres L, Wiese C, Shoucri B, Lambert G, Catherinet C, Prado-Lourenco L, Levin M, Thacker S, Sethupathy P, Barter P, Remaley A, Rye K. 2014. HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells. Nat Commun 5:3292.
115. Tadokoro H, Umezu T, Ohyashiki K, Hirano T, Ohyashiki J. 2013. Exosomes derived from hypoxic leukemia cells enhance tube formation in endothelial cells. J Biol Chem 288:34343-34351.
116. Taganov K, Boldin M, Chang K, Baltimore D. 2006. NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 103:12481-12486.
117. Taguchi A, Yanagisawa K, Tanaka M, Cao K, Matsuyama Y, Goto H, Takahashi T. 2008. Identification of hypoxia-inducible factor-1α as a novel target for miR-17-92 microRNA cluster. Cancer Res 68:5540-5545.
118. Tellez C, Juri D, Do K, Bernauer A, Thomas C, Damiani L, Tessema M, Leng S, Belinsky S. 2011. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res 71:3087-3097.
119. Tian T, Zhu Y, Zhou Y, Liang G, Wang Y, Hu F, Xiao Z. 2014. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem 289:22258-22267.
120. Tili E, Michaille J. 2011. Resveratrol, microRNAs, inflammation, and cancer. J Nucleic Acids 2011:102431.
121. Tili E, Michaille J, Cimino A, Costinean S, Dumitru C, Adair B, Fabbri M, Alder H, Liu C, Calin G, Croce C. 2007. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-α stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol 179:5082-5089.
122. Tili E, Croce C, Michaille J. 2009. miR-155: On the crosstalk between inflammation and cancer. Int Rev Immunol 28:264-284.
123. Tili E, Michaille J, Adair B, Alder H, Limagne E, Taccioli CF, Ferracin M, Delmas D, Latruffe N, Croce C. 2010. Resveratrol decreases the levels of miR-155 by upregulating miR-663, a microRNA targeting JunB and JunD. Carcinogenesis 31:1561-1566.
124. Tili E, Michaille J, Wernicke D, Alder H, Costinean S, Volinia S, Croce C. 2011. Mutator activity induced by microRNA-155 (miR-155) links inflammation and cancer. Proc Natl Acad Sci USA 108:4908-4913.
125. Trotta R, Chen L, Ciarlariello D, Josyula S, Mao C, Costinean S, Yu L, Butchar J, Tridandapani S, Croce C, Caligiuri M. 2012. miR-155 regulates IFN-γ production in natural killer cells. Blood 119:3478-3485.
126. Urbich C, Kaluza D, Fromel T, Knau A, Bennewitz K, Boon R, Bonauer A, Doebele C, Boeckel J, Hergenreider E, Zeiher A, Kroll J, Fleming I, Dimmeler S. 2011. MicroRNA-27a/b controls endothelial cell repulsion and angiogenesis by targeting semaphorin 6A. Blood 119:1607-1616.
127. Valastyan S, Chang A, Benaich N, Reinhardt F, Weinberg R. 2010. Concurrent suppression of integrin α5, radixin, and RhoA phenocopies the effects of miR-31 on metastasis. Cancer Res 70:5147-5154.
128. Valencia K, Luis-Ravelo D, Bovy N, Anton I, Martínez-Canarias S, Zandueta C, Ormazabal C, Struman I, Tabruyn S, Rebmann V, De Las Rivas J, Guruceaga E, Bandres E, Lecanda F. 2014. miRNA cargo within exosome-like vesicle transfer influences metastatic bone colonization. Mol Oncol 8:689-703.
129. van Balkom B, de Jong O, Smits M, Brummelman J, den Ouden K, de Bree P, van Eijndhoven M, Pegtel D, Stoorvogel W, Wurdinger T, Verhaar M. 2013. Endothelial cells require miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood 121:3997-4006.
130. Vickers K, Palmisano B, Shoucri B, Shamburek R, Remaley A. 2011. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 13:423-433.
131. Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, Martinez-Herrera D, Pascual-Montano A, Mittelbrunn M, Sanchez-Madrid F. 2013. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4:2980.
132. Vire E, Curtis C, Davalos V, Git A, Robson S, Villanueva A, Vidal A, Barbieri I, Aparicio S, Esteller M, Caldas C, Kouzarides T. 2014. The breast cancer oncogene EMSY represses transcription of antimetastatic microRNA miR-31. Mol Cell 53:806-818.
133. Wang W, Lotze M. 2014. Good things come in small packages: Exosomes, immunity and cancer. Cancer Gene Ther 21:139-141.
134. Wang S, Aurora A, Johnson B, Qi X, McAnally J, Hill J, Richardson J, Bassel-Duby R, Olson E. 2008. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell 15:261-271.
135. Whyte S, Pandor A, Stevenson M, Rees A. 2010. Bevacizumab in combination with fluoropyrimidine-based chemotherapy for the first-line treatment of metastatic colorectal cancer. Health Technol Assess 14:47-53.
136. Wu F, Yang Z, Li G. 2009. Role of specific microRNAs for endothelial function and angiogenesis. Biochem Biophys Res Commun 386:549.
137. Wu D, Wang Y, Fan L, Luo H, Han B, Sun L, Wang X, Zhang J, Cao L, Wang X, You Y, Liu N. 2011. MicroRNA-7 regulates glioblastoma cell invasion via targeting focal adhesion kinase expression. Chin Med J 124:2616-2621.
138. Xiao J, Lin H, Luo X, Luo X, Wang Z. 2011. miR-605 joins p53 network to form a p53:miR-605:Mdm2 positive feedback loop in response to stress. EMBO J 30:524-532.
139. Yan G, Xu S, Tan Z, Liu L, He Q. 2011. Global identification of miR-373-regulated genes in breast cancer by quantitative proteomics. Proteomics 11:912-920.
140. Yan X, Jia Y, Chen L, Zeng Q, Zhou J, Fu C, Chen H, Yuan H, Li Z, Shi L, Xu Y, Wang J, Zhang X, He L, Zhai C, Yue W, Pei X. 2013. Hepatocellular carcinoma-associated mesenchymal stem cells promote hepatocarcinoma progression: Role of the S100A4-miR155-SOCS1-MMP9 axis. Hepatology 57:2274-2286.
141. Yang C, Yue J, Fan M, Pfeffer L. 2010. Interferon induces miR-21 through a STAT3-dependent pathway as a suppressive negative feedback on interferon-induced apoptosis. Cancer Res 70:8108-8116.
142. Yang M, Chen J, Su F, Yu B, Su F, Lin L, Liu Y, Huang J, Song E. 2011. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 10:117.
143. Yang J, Zhang Z, Chen C, Liu Y, Si Q, Chuang T, Li N, Gomez-Cabrero A, Reisfeld R, Xiang R, Luo Y. 2014a. MicroRNA-19a-3p inhibits breast cancer progression and metastasis by inducing macrophage polarization through downregulated expression of Fra-1 proto-oncogene. Oncogene 33:3014-3023.
144. Yang T, Yang X, Chen X, Wang X, Hua J, Zhou D, Zhou B, Song Z. 2014b. MicroRNA-106b in cancer-associated fibroblasts from gastric cancer 4 promotes cell migration and invasion by targeting PTEN. FEBS Lett 588:2162-2169.
145. Yang X, Zhang X, Fu M, Weichselbaum R, Gajewski T, Guo Y, Fu Y. 2014c. Targeting the tumor microenvironment with interferon-β bridges innate and adaptive immune responses. Cancer Cell 25:37-48.
146. Yao Q, Cao S, Li C, Mengesha A, Kong B, Wei M. 2011. Micro-RNA-21 regulates TGF-β-induced myofibroblast differentiation by targeting PDCD4 in tumor-stroma interaction. Int J Cancer 128:1783-1792.
147. Zeng L, He X, Wang Y, Tang Y, Zheng C, Cai H, Liu J, Wang Y, Fu Y, Yang G. 2014. MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain. Gene Therapy 21:37-43.
148. Zhang B, Pan X, Cobb G, Anderson T. 2007. microRNAs as oncogenes and tumor suppressors. Dev Biol 302:1-12.
149. Zhang Y, Wang Z, Gemeinhart R. 2013. Progress in microRNA delivery. J Control Release 172:962-974.
150. Zhang J, Zeng C, Xu L, Gong J, Fang J, Zhuang S. 2014. MicroRNA-148a suppresses the epithelial-mesenchymal transition and metastasis of hepatoma cells by targeting Met/Snail signaling. Oncogene 33:4069-4076.
151. Zhou Q, Gallagher R, Ufret-Vincenty R, Li X, Olson E, Wang S. 2011. Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23-27-24 clusters. Proc Natl Acad Sci USA 108:8287-8292.
152. Zhou W, Fong M, Min Y, Somlo G, Liu L, Palomares M, Yu Y, Chow A, O'Connor S, Chin A, Yen Y, Wang Y, Marcusson E, Chu P, Wu J, Wu X, Li AX, Li Z, Gao H, Ren X, Boldin MP, Lin PC, Wang SE. 2014. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell 25:501-515.
153. Zuo Z, Calin GA, de Paula HM, Medeiros LJ, Fernandez MH, Shimizu M, Garcia-Manero G, Bueso-Ramos CE. 2011. Circulating microRNAs let-7a and miR-16 predict progression-free survival and overall survival in patients with myelodysplastic syndrome. Blood 118:413-415.