Circulating miRNAs in cancer: From detection to therapy

Journal of Hematology and Oncology

Volumn 7, Issue 1, 2014, Pages

  Wang, Wen Tao ^a   Chen, Yue Qin ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; TUMOR MARKER;

BODY FLUID; CANCER CELL; CANCER DIAGNOSIS; CANCER GROWTH; CANCER PATIENT; CANCER STAGING; CANCER THERAPY; CARCINOGENESIS; CELL COMMUNICATION; EXOSOME; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NEXT GENERATION SEQUENCING; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; BLOOD; GENETICS; NEOPLASM; PROGNOSIS;

ANIMALS; BIOMARKERS, TUMOR; HUMANS; MICRORNAS; NEOPLASMS; PROGNOSIS; TUMOR MICROENVIRONMENT;

EID: 84922194380     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/s13045-014-0086-0     Document Type: Review

References (99)

1. Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
2. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G: The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
3. Lytle JR, Yario TA, Steitz JA: Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR. Proc Natl Acad Sci U S A 2007, 104:9667-9672.
4. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, Da PI, Gunsalus KC, Stoffel M, Rajewsky N: Combinatorial microRNA target predictions. Nat Genet 2005, 37:495-500.
5. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, Diehn M, Liu H, Panula SP, Chiao E, Dirbas FM, Somlo G, Pera RA, Lao K, Clarke MF: Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 2009, 138:592-603.
6. Popovic R, Riesbeck LE, Velu CS, Chaubey A, Zhang J, Achille NJ, Erfurth FE, Eaton K, Lu J, Grimes HL, Chen J, Rowley JD, Zeleznik-Le NJ: Regulation of mir-196b by MLL and its overexpression by MLL fusions contributes to immortalization. Blood 2009, 113:3314-3322.
7. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, Yatabe Y, Kawahara K, Sekido Y, Takahashi T: A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005, 65:9628-9632.
8. Hassan O, Ahmad A, Sethi S, Sarkar FH: Recent updates on the role of microRNAs in prostate cancer. J Hematol Oncol 2012, 5:9.
9. Akao Y, Nakagawa Y, Hirata I, Iio A, Itoh T, Kojima K, Nakashima R, Kitade Y, Naoe T: Role of anti-oncomirs miR-143 and.145 in human colorectal tumors. Cancer Gene Ther 2010, 17:398-408.
10. Pan Q, Chegini N: MicroRNA signature and regulatory functions in the endometrium during normal and disease states. Semin Reprod Med 2008, 26:479-493.
11. Chim SS, Shing TK, Hung EC, Leung TY, Lau TK, Chiu RW, Lo YM: Detection and characterization of placental microRNAs in maternal plasma. Clin Chem 2008, 54:482-490.
12. Gutwein P, Stoeck A, Riedle S, Gast D, Runz S, Condon TP, Marme A, Phong MC, Linderkamp O, Skorokhod A, Altevogt P: Cleavage of L1 in exosomes and apoptotic membrane vesicles released from ovarian carcinoma cells. Clin Cancer Res 2005, 11:2492-2501.
13. Lodes MJ, Caraballo M, Suciu D, Munro S, Kumar A, Anderson B: Detection of cancer with serum miRNAs on an oligonucleotide microarray. PLoS One 2009, 4:e6229.
14. Lawrie CH, Gal S, Dunlop HM, Pushkaran B, Liggins AP, Pulford K, Banham AH, Pezzella F, Boultwood J, Wainscoat JS, Hatton CS, Harris AL: Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 2008, 141:672-675.
15. Huan J, Hornick NI, Shurtleff MJ, Skinner AM, Goloviznina NA, Roberts CJ, Kurre P: RNA trafficking by acute myelogenous leukemia exosomes. Cancer Res 2013, 73:918-929.
16. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, Tait JF, Tewari M: Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A 2011, 108:5003-5008.
17. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O: Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 2009, 11:1143-1149.
18. Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, Xiao T, Schafer J, Lee ML, Schmittgen TD, Nana-Sinkam SP, Jarjoura D, Marsh CB: Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 2008, 3:e3694.
19. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X, Sun Q, Wang K, Ba Y, Wang Q, Wang D, Yang J, Liu P, Xu T, Yan Q, Zhang J, Zen K, Zhang CY: Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010, 39:133-144.
20. Hergenreider E, Heydt S, Treguer K, Boettger T, Horrevoets AJ, Zeiher AM, Scheffer MP, Frangakis AS, Yin X, Mayr M, Braun T, Urbich C, Boon RA, Dimmeler S: Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 2012, 14:249-256.
21. Chen WX, Cai YQ, Lv MM, Chen L, Zhong SL, Ma TF, Zhao JH, Tang JH: Exosomes from docetaxel-resistant breast cancer cells alter chemosensitivity by delivering microRNAs. Tumour Biol 2014, 10:9649-9659.
22. Wang WT, Zhao YN, Yan JX, Weng MY, Wang Y, Chen YQ, Hong SJ: Differentially expressed microRNAs in the serum of cervical squamous cell carcinoma patients before and after surgery. J Hematol Oncol 2014, 7:6.
23. Ji F, Yang B, Peng X, Ding H, You H, Tien P: Circulating microRNAs in hepatitis B virus-infected patients. J Viral Hepat 2011, 18:e242.e251.
24. Kroh EM, Parkin RK, Mitchell PS, Tewari M: Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods 2010, 50:298-301.
25. Plieskatt JL, Rinaldi G, Feng Y, Levine PH, Easley S, Martinez E, Hashmi S, Sadeghi N, Brindley PJ, Bethony JM, Mulvenna JP: Methods and matrices: approaches to identifying miRNAs for nasopharyngeal carcinoma. J Transl Med 2014, 12:3.
26. McDonald JS, Milosevic D, Reddi HV, Grebe SK, Algeciras-Schimnich A: Analysis of circulating microRNA: preanalytical and analytical challenges. Clin Chem 2011, 57:833-840.
27. Zeng CW, Chen ZH, Zhang XJ, Han BW, Lin KY, Li XJ, Wei PP, Zhang H, Li Y, Chen YQ: MIR125B1 represses the degradation of the PML-RARA oncoprotein by an autophagy-lysosomal pathway in acute promyelocytic leukemia. Autophagy 2014, 10:1726-1737.
28. Kuwabara Y, Ono K, Horie T, Nishi H, Nagao K, Kinoshita M, Watanabe S, Baba O, Kojima Y, Shizuta S, Imai M, Tamura T, Kita T, Kimura T: Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate myocardial damage. Circ Cardiovasc Genet 2011, 4:446-454.
29. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M: Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A 2008, 105:10513-10518.
30. Wulfken LM, Moritz R, Ohlmann C, Holdenrieder S, Jung V, Becker F, Herrmann E, Walgenbach-Brunagel G, von Ruecker A, Muller SC, Ellinger J: MicroRNAs in renal cell carcinoma: diagnostic implications of serum miR-1233 levels. PLoS One 2011, 6:e25787.
31. Flavia Pichiorri PARC: Circulating Mir-16 and Mir-25 As New Prognosticators For Multiple Myeloma [abstract]. Blood 2013, 122:s1853.
32. Filkova M, Aradi B, Senolt L, Ospelt C, Vettori S, Mann H, Filer A, Raza K, Buckley CD, Snow M, Vencovsky J, Pavelka K, Michel BA, Gay RE, Gay S, Jungel A: Association of circulating miR-223 and miR-16 with disease activity in patients with early rheumatoid arthritis. Ann Rheum Dis 2013, 10:1898-1904.
33. Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, Weber M, Hamm CW, Roxe T, Muller-Ardogan M, Bonauer A, Zeiher AM, Dimmeler S: Circulating microRNAs in patients with coronary artery disease. Circ Res 2010, 107:677-684.
34. Zeng X, Xiang J, Wu M, Xiong W, Tang H, Deng M, Li X, Liao Q, Su B, Luo Z, Zhou Y, Zhou M, Zeng Z, Li X, Shen S, Shuai C, Li G, Fang J, Peng S: Circulating miR-17, miR-20a, miR-29c, and miR-223 combined as non-invasive biomarkers in nasopharyngeal carcinoma. PLoS One 2012, 7:e46367.
35. Yun JJ, Heisler LE, Hwang II, Wilkins O, Lau SK, Hyrcza M, Jayabalasingham B, Jin J, McLaurin J, Tsao MS, der SD: Genomic DNA functions as a universal external standard in quantitative real-time PCR. Nucleic Acids Res 2006, 34:e85.
36. Whelan JA, Russell NB, Whelan MA: A method for the absolute quantification of cDNA using real-time PCR. J Immunol Methods 2003, 278:261-269.
37. Wang WT, Zhao YN, Han BW, Hong SJ, Chen YQ: Circulating microRNAs identified in a genome-wide serum microRNA expression analysis as noninvasive biomarkers for endometriosis. J Clin Endocrinol Metab 2013, 98:281-289.
38. Chen Y, Gelfond JA, McManus LM, Shireman PK: Reproducibility of quantitative RT-PCR array in miRNA expression profiling and comparison with microarray analysis. BMC Genomics 2009, 10:407.
39. Ho SL, Chan HM, Wong RN, Li HW: Self-assembling protein platform for direct quantification of circulating microRNAs in serum with total internal reflection fluorescence microscopy. Anal Chim Acta 2014, 823:61-68.
40. Lusi EA, Passamano M, Guarascio P, Scarpa A, Schiavo L: Innovative electrochemical approach for an early detection of microRNAs. Anal Chem 2009, 81:2819-2822.
41. Redova M, Sana J, Slaby O: Circulating miRNAs as new blood-based biomarkers for solid cancers. Future Oncol 2013, 9:387-402.
42. Pu XX, Huang GL, Guo HQ, Guo CC, Li H, Ye S, Ling S, Jiang L, Tian Y, Lin TY: Circulating miR-221 directly amplified from plasma is a potential diagnostic and prognostic marker of colorectal cancer and is correlated with p53 expression. J Gastroenterol Hepatol 2010, 25:1674-1680.
43. Yang Q, Lu J, Wang S, Li H, Ge Q, Lu Z: Application of next-generation sequencing technology to profile the circulating microRNAs in the serum of preeclampsia versus normal pregnant women. Clin Chim Acta 2011, 412:2167-2173.
44. Schuster SC: Next-generation sequencing transforms today's biology. Nat Methods 2008, 5:16-18.
45. Han Y, Chen J, Zhao X, Liang C, Wang Y, Sun L, Jiang Z, Zhang Z, Yang R, Chen J, Li Z, Tang A, Li X, Ye J, Guan Z, Gui Y, Cai Z: MicroRNA expression signatures of bladder cancer revealed by deep sequencing. PLoS One 2011, 6:e18286.
46. Wach S, Nolte E, Szczyrba J, Stohr R, Hartmann A, Orntoft T, Dyrskjot L, Eltze E, Wieland W, Keck B, Ekici AB, Grasser F, Wullich B: MicroRNA profiles of prostate carcinoma detected by multiplatform microRNA screening. Int J Cancer 2012, 130:611-621.
47. Ryu S, Joshi N, McDonnell K, Woo J, Choi H, Gao D, McCombie WR, Mittal V: Discovery of novel human breast cancer microRNAs from deep sequencing data by analysis of pri-microRNA secondary structures. PLoS One 2011, 6:e16403.
48. Zhou J, Yu L, Gao X, Hu J, Wang J, Dai Z, Wang JF, Zhang Z, Lu S, Huang X, Wang Z, Qiu S, Wang X, Yang G, Sun H, Tang Z, Wu Y, Zhu H, Fan J: Plasma microRNA panel to diagnose hepatitis B virus-related hepatocellular carcinoma. J Clin Oncol 2011, 29:4781-4788.
49. Roth C, Rack B, Muller V, Janni W, Pantel K, Schwarzenbach H: Circulating microRNAs as blood-based markers for patients with primary and metastatic breast cancer. Breast Cancer Res 2010, 12:R90.
50. Zhu C, Ren C, Han J, Ding Y, Du J, Dai N, Dai J, Ma H, Hu Z, Shen H, Xu Y, Jin G: A five-microRNA panel in plasma was identified as potential biomarker for early detection of gastric cancer. Br J Cancer 2014, 110:2291-2299.
51. Wang LG, Gu J: Serum microRNA-29a is a promising novel marker for early detection of colorectal liver metastasis. Cancer Epidemiol 2012, 36:e61-e67.
52. Rocci A, Hofmeister CC, Geyer S, Stiff A, Gambella M, Cascione L, Guan J, Benson DM, Efebera YA, Talabere T, Dirisala V, Smith EM, Omede P, Isaia G, De Luca L, Rossi D, Gentili S, Uccello G, Consiglio J, Ria R, Benevolo G, Bringhen S, Callea V, Weiss B, Ferro A, Magarotto V, Alder H, Byrd JC, Boccadoro M, Marcucci G, et al: Circulating miRNA markers show promise as new prognosticators for multiple myeloma. Leukemia 2014, 28:1922-1926.
53. Summerer I, Niyazi M, Unger K, Pitea A, Zangen V, Hess J, Atkinson MJ, Belka C, Moertl S, Zitzelsberger H: Changes in circulating microRNAs after radiochemotherapy in head and neck cancer patients. Radiat Oncol 2013, 8:296.
54. Gezer U, Keskin S, Igci A, Tukenmez M, Tiryakioglu D, Cetinkaya M, Disci R, Dalay N, Eralp Y: Abundant circulating microRNAs in breast cancer patients fluctuate considerably during neoadjuvant chemotherapy. Oncol Lett 2014, 8:845-848.
55. Su TH, Liu CH, Liu CJ, Chen CL, Ting TT, Tseng TC, Chen PJ, Kao JH, Chen DS: Serum microRNA-122 level correlates with virologic responses to pegylated interferon therapy in chronic hepatitis C. Proc Natl Acad Sci U S A 2013, 110:7844-7849.
56. Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J, Amigorena S: Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001, 166:7309-7318.
57. Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, Coscia C, Iessi E, Logozzi M, Molinari A, Colone M, Tatti M, Sargiacomo M, Fais S: Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 2009, 284:34211-34222.
58. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WJ, Carter BS, Krichevsky AM, Breakefield XO: Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008, 10:1470-1476.
59. Segura E, Guerin C, Hogg N, Amigorena S, Thery C: CD8+ dendritic cells use LFA-1 to capture MHC-peptide complexes from exosomes in vivo. J Immunol 2007, 179:1489-1496.
60. Morelli AE, Larregina AT, Shufesky WJ, Sullivan ML, Stolz DB, Papworth GD, Zahorchak AF, Logar AJ, Wang Z, Watkins SC, Falo LJ, Thomson AW: Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 2004, 104:3257-3266.
61. Fitzner D, Schnaars M, van Rossum D, Krishnamoorthy G, Dibaj P, Bakhti M, Regen T, Hanisch UK, Simons M: Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J Cell Sci 2011, 124:447-458.
62. 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, 9:654-659.
63. Vojtech L, Woo S, Hughes S, Levy C, Ballweber L, Sauteraud RP, Strobl J, Westerberg K, Gottardo R, Tewari M, Hladik F: Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res 2014, 42:7290-7304.
64. Noah Hornick BSJH: Hypoxia regulates exosomal microrna content, trafficking and function of key elements in the AML microenvironment [abstract]. Blood 2013, 122:s742.
65. Yang M, Chen J, Su F, Yu B, Su F, Lin L, Liu Y, Huang JD, Song E: Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 2011, 10:117.
66. Niu Z, Goodyear SM, Rao S, Wu X, Tobias JW, Avarbock MR, Brinster RL: MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 2011, 108:12740-12745.
67. Taverna S, Amodeo V, Saieva L, Russo A, Giallombardo M, De Leo G, Alessandro R: Exosomal shuttling of miR-126 in endothelial cells modulates adhesive and migratory abilities of chronic myelogenous leukemia cells. Mol Cancer 2014, 13:169.
68. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT: MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011, 13:423-433.
69. Wang K, Zhang S, Weber J, Baxter D, Galas DJ: Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res 2010, 38:7248-7259.
70. Turchinovich A, Weiz L, Langheinz A, Burwinkel B: Characterization of extracellular circulating microRNA. Nucleic Acids Res 2011, 39:7223-7233.
71. Turchinovich A, Weiz L, Burwinkel B: Isolation of circulating microRNA associated with RNA-binding protein. Methods Mol Biol 2013, 1024:97-107.
72. Wu S, Yu W, Qu X, Wang R, Xu J, Zhang Q, Xu J, Li J, Chen L: Argonaute 2 promotes myeloma angiogenesis via microRNA dysregulation. J Hematol Oncol 2014, 7:40.
73. Zhang L, Hou D, Chen X, Li D, Zhu L, Zhang Y, Li J, Bian Z, Liang X, Cai X, Yin Y, Wang C, Zhang T, Zhu D, Zhang D, Xu J, Chen Q, Ba Y, Liu J, Wang Q, Chen J, Wang J, Wang M, Zhang Q, Zhang J, Zen K, Zhang CY: Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res 2012, 22:107-126.
74. Lukasik A, Zielenkiewicz P: In silico identification of plant miRNAs in mammalian breast milk exosomes-a small step forward? PLoS One 2014, 9:e99963.
75. Witwer KW, McAlexander MA, Queen SE, Adams RJ: Real-time quantitative PCR and droplet digital PCR for plant miRNAs in mammalian blood provide little evidence for general uptake of dietary miRNAs: limited evidence for general uptake of dietary plant xenomiRs. RNA Biol 2013, 10:1080-1086.
76. Liang GFZYSB: Assessing the survival of exogenous plant microRNA in mice. Food Sci Nutr 2014, 2:380-388.
77. Valeri N, Braconi C, Gasparini P, Murgia C, Lampis A, Paulus-Hock V, Hart JR, Ueno L, Grivennikov SI, Lovat F, Paone A, Cascione L, Sumani KM, Veronese A, Fabbri M, Carasi S, Alder H, Lanza G, Gafa' R, Moyer MP, Ridgway RA, Cordero J, Nuovo GJ, Frankel WL, Rugge M, Fassan M, Groden J, Vogt PK, Karin M, Sansom OJ, et al: MicroRNA-135b promotes cancer progression by acting as a downstream effector of oncogenic pathways in colon cancer. Cancer Cell 2014, 25:469-483.
78. Uchino K, Takeshita F, Takahashi RU, Kosaka N, Fujiwara K, Naruoka H, Sonoke S, Yano J, Sasaki H, Nozawa S, Yoshiike M, Kitajima K, Chikaraishi T, Ochiya T: Therapeutic effects of microRNA-582-5p and-3p on the inhibition of bladder cancer progression. Mol Ther 2013, 21:610-619.
79. Sun YM, Lin KY, Chen YQ: Diverse functions of miR-125 family in different cell contexts. J Hematol Oncol 2013, 6:6.
80. Guan Y, Yao H, Zheng Z, Qiu G, Sun K: MiR-125b targets BCL3 and suppresses ovarian cancer proliferation. Int J Cancer 2011, 128:2274-2283.
81. Huang L, Luo J, Cai Q, Pan Q, Zeng H, Guo Z, Dong W, Huang J, Lin T: MicroRNA-125b suppresses the development of bladder cancer by targeting E2F3. Int J Cancer 2011, 128:1758-1769.
82. Li W, Duan R, Kooy F, Sherman SL, Zhou W, Jin P: Germline mutation of microRNA-125a is associated with breast cancer. J Med Genet 2009, 46:358-360.
83. Bloomston M, Frankel WL, Petrocca F, Volinia S, Alder H, Hagan JP, Liu CG, Bhatt D, Taccioli C, Croce CM: MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 2007, 297:1901-1908.
84. Shi XB, Xue L, Yang J, Ma AH, Zhao J, Xu M, Tepper CG, Evans CP, Kung HJ, DeVere WR: An androgen-regulated miRNA suppresses Bak1 expression and induces androgen-independent growth of prostate cancer cells. Proc Natl Acad Sci U S A 2007, 104:19983-19988.
85. Nelson PT, Baldwin DA, Kloosterman WP, Kauppinen S, Plasterk RH, Mourelatos Z: RAKE and LNA-ISH reveal microRNA expression and localization in archival human brain. RNA 2006, 12:187-191.
86. Redis RS, Calin S, Yang Y, You MJ, Calin GA: Cell-to-cell miRNA transfer: from body homeostasis to therapy. Pharmacol Ther 2012, 136:169-174.
87. Chen Y, Gao DY, Huang L: In vivo delivery of miRNAs for cancer therapy: Challenges and strategies. Adv Drug Deliv Rev 2014, in press.
88. Kleger A, Perkhofer L, Seufferlein T: Smarter drugs emerging in pancreatic cancer therapy. Ann Oncol 2014, 25:1260-1270.
89. Castelli DD, Terreno E, Cabella C, Chaabane L, Lanzardo S, Tei L, Visigalli M, Aime S: Evidence for in vivo macrophage mediated tumor uptake of paramagnetic/fluorescent liposomes. NMR Biomed 2009, 22:1084-1092.
90. Inoue T, Sugimoto M, Sakurai T, Saito R, Futaki N, Hashimoto Y, Honma Y, Arai I, Nakaike S: Modulation of scratching behavior by silencing an endogenous cyclooxygenase-1 gene in the skin through the administration of siRNA. J Gene Med 2007, 9:994-1001.
91. Zheng D, Giljohann DA, Chen DL, Massich MD, Wang XQ, Iordanov H, Mirkin CA, Paller AS: Topical delivery of siRNA-based spherical nucleic acid nanoparticle conjugates for gene regulation. Proc Natl Acad Sci U S A 2012, 109:11975-11980.
92. Wang H, Chiu M, Xie Z, Chiu M, Liu Z, Chen P, Liu S, Byrd JC, Muthusamy N, Garzon R, Croce CM, Marcucci G, Chan KK: Synthetic microRNA cassette dosing: pharmacokinetics, tissue distribution and bioactivity. Mol Pharm 2012, 9:1638-1644.
93. Karlsen TA, Brinchmann JE: Liposome delivery of microRNA-145 to mesenchymal stem cells leads to immunological off-target effects mediated by RIG-I. Mol Ther 2013, 21:1169-1181.
94. Neuzillet C, Tijeras-Raballand A, Cros J, Faivre S, Hammel P, Raymond E: Stromal expression of SPARC in pancreatic adenocarcinoma. Cancer Metastasis Rev 2013, 32:585-602.
95. Neesse A, Frese KK, Chan DS, Bapiro TE, Howat WJ, Richards FM, Ellenrieder V, Jodrell DI, Tuveson DA: SPARC independent drug delivery and antitumour effects of nab-paclitaxel in genetically engineered mice. Gut 2014, 63:974-983.
96. Bananis E, Murray JW, Stockert RJ, Satir P, Wolkoff AW: Microtubule and motor-dependent endocytic vesicle sorting in vitro. J Cell Biol 2000, 151:179-186.
97. Bomsel M, Parton R, Kuznetsov SA, Schroer TA, Gruenberg J: Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells. Cell 1990, 62:719-731.
98. Takatsu H, Katoh Y, Ueda T, Waguri S, Murayama T, Takahashi S, Shin HW, Nakayama K: Mitosis-coupled, microtubule-dependent clustering of endosomal vesicles around centrosomes. Cell Struct Funct 2013, 38:31-41.
99. Stehbens SJ, Paszek M, Pemble H, Ettinger A, Gierke S, Wittmann T: CLASPs link focal-adhesion-associated microtubule capture to localized exocytosis and adhesion site turnover. Nat Cell Biol 2014, 16:561-573.