Quantitative and stoichiometric analysis of the microRNA content of exosomes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 41, 2014, Pages 14888-14893

  Chevillet, John R ^a   Kang, Qing ^a,b   Ruf, Ingrid K ^a   Briggs, Hilary A ^a   Vojtech, Lucia N ^d   Hughes, Sean M ^d   Cheng, Heather H ^a,d   Arroyo, Jason D ^a   Meredith, Emily K ^a   Gallichotte, Emily N ^a   Pogosova Agadjanyan, Era L ^a   Morrissey, Colm ^d   Stirewalt, Derek L ^a   Hladik, Florian ^a,d   Yu, Evan Y ^d   Higano, Celestia S ^a,d   Tewari, Muneesh ^a,b,c  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Circulating; Microvesicle

Indexed keywords

MICRORNA;

BIOLOGICAL MODEL; BLOOD; EXOSOME; GENE DOSAGE; GENETICS; HUMAN; NEOPLASM; TUMOR CELL LINE; ULTRASTRUCTURE;

CELL LINE, TUMOR; EXOSOMES; GENE DOSAGE; HUMANS; MICRORNAS; MODELS, BIOLOGICAL; NEOPLASMS;

EID: 84907906605     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1408301111     Document Type: Article

References (51)

1. Pan BT, Teng K, Wu C, Adam M, Johnstone RM (1985) Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 101(3):942-948.
2. Harding C, Heuser J, Stahl P (1984) Endocytosis and intracellular processing of transferrin and colloidal gold-transferrin in rat reticulocytes: Demonstration of a pathway for receptor shedding. Eur J Cell Biol 35(2):256-263.
3. Raposo G, Stoorvogel W (2013) Extracellular vesicles: Exosomes, microvesicles, and friends. J Cell Biol 200(4):373-383.
4. Valadi H, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9(6):654-659.
5. Kharaziha P, Ceder S, Li Q, Panaretakis T (2012) Tumor cell-derived exosomes: A message in a bottle. Biochim Biophys Acta 1826(1):103-111.
6. Hannafon BN, Ding WQ (2013) Intercellular communication by exosome-derived microRNAs in cancer. Int J Mol Sci 14(7):14240-14269.
7. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92-105.
8. Christianson HC, Svensson KJ, van Kuppevelt TH, Li JP, Belting M (2013) Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc Natl Acad Sci USA 110(43):17380-17385.
9. Huan J, et al. (2013) RNA trafficking by acute myelogenous leukemia exosomes. Cancer Res 73(2):918-929.
10. Montecalvo A, et al. (2012) Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119(3):756-766.
11. Kosaka N, et al. (2010) Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285(23):17442-17452.
12. Umezu T, Ohyashiki K, Kuroda M, Ohyashiki JH (2013) Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene 32(22):2747-2755.
13. Alvarez-Erviti L, et al. (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29(4):341-345.
14. Ohno S, et al. (2013) Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 21(1):185-191.
15. Ramachandran S, Palanisamy V (2012) Horizontal transfer of RNAs: Exosomes as mediators of intercellular communication. Wiley Interdiscip Rev RNA 3(2):286-293.
16. Stoorvogel W (2012) Functional transfer of microRNA by exosomes. Blood 119(3):646-648.
17. Leslie M (2013) Cell biology. NIH effort gambles on mysterious extracellular RNAs. Science 341(6149):947.
18. Sverdlov ED (2012) Amedeo Avogadro' s cry: What is 1 μg of exosomes? BioEssays 34(10):873-875.
19. Dragovic RA, et al. (2011) Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis. Nanomedicine (Lond Print) 7(6):780-788.
20. 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 3(2006):3.22.
21. Hessvik NP, Phuyal S, Brech A, Sandvig K, Llorente A (2012) Profiling of microRNAs in exosomes released from PC-3 prostate cancer cells. Biochim Biophys Acta 1819(11-12):1154-1163.
22. Bryant RJ, et al. (2012) Changes in circulating microRNA levels associated with prostate cancer. Br J Cancer 106(4):768-774.
23. Ogata-Kawata H, et al. (2014) Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS ONE 9(4):e92921.
24. Gajos-Michniewicz A, Duechler M, Czyz M (2014) MiRNA in melanoma-derived exosomes. Cancer Lett 347(1):29-37.
25. Tadokoro H, Umezu T, Ohyashiki K, Hirano T, Ohyashiki JH (2013) Exosomes derived from hypoxic leukemia cells enhance tube formation in endothelial cells. J Biol Chem 288(48):34343-34351.
26. Duijvesz D, Luider T, Bangma CH, Jenster G (2011) Exosomes as biomarker treasure chests for prostate cancer. Eur Urol 59(5):823-831.
27. Arroyo JD, et al. (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108(12):5003-5008.
28. Turchinovich A, Weiz L, Langheinz A, Burwinkel B (2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res 39(16):7223-7233.
29. Cheng L, Sharples RA, Scicluna BJ, Hill AF (2014) Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cellfree blood. J Extracell Vesicles, 10.3402/jec.v3.23743.
30. Mitchell PS, et al. (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105(30):10513-10518.
31. Cheng HH, et al. (2013) Circulating microRNA profiling identifies a subset of metastatic prostate cancer patients with evidence of cancer-associated hypoxia. PLoS ONE 8(7):e69239.
32. Momen-Heravi F, et al. (2013) Current methods for the isolation of extracellular vesicles. Biol Chem 394(10):1253-1262.
33. Witwer KW, et al. (2013) Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles, 10.3402/jev.v2i0.20360.
34. Redis RS, Calin S, Yang Y, You MJ, Calin GA (2012) Cell-to-cell miRNA transfer: From body homeostasis to therapy. Pharmacol Ther 136(2):169-174.
35. Filipe V, Hawe A, Jiskoot W (2010) Critical evaluation of Nanoparticle Tracking Analysis (NTA) by NanoSight for the measurement of nanoparticles and protein aggregates. Pharm Res 27(5):796-810.
36. Kroh EM, Parkin RK, Mitchell PS, Tewari M (2010) Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods 50(4):298-301.
37. Bustin SA, Nolan T (2004) Pitfalls of quantitative real-time reverse-transcription polymerase chain reaction. J Biomol Tech 15(3):155-166.
38. Hindson CM, et al. (2013) Absolute quantification by droplet digital PCR versus analog real-time PCR. Nat Methods 10(10):1003-1005.
39. Dingle TC, Sedlak RH, Cook L, Jerome KR (2013) Tolerance of droplet-digital PCR vs real-time quantitative PCR to inhibitory substances. Clin Chem 59(11):1670-1672.
40. Kalra H, et al. (2013) Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma. Proteomics 13(22):3354-3364.
41. Steinman RM, Brodie SE, Cohn ZA (1976) Membrane flow during pinocytosis. A stereologic analysis. J Cell Biol 68(3):665-687.
42. Fabbri M, et al. (2012) MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 109(31):E2110-E2116.
43. Park CK, et al. (2014) Extracellular microRNAs activate nociceptor neurons to elicit pain via TLR7 and TRPA1. Neuron 82(1):47-54.
44. Gagnon KT, Li L, Chu Y, Janowski BA, Corey DR (2014) RNAi factors are present and active in human cell nuclei. Cell Reports 6(1):211-221.
45. Skog J, et al. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10(12):1470-1476.
46. Morello M, et al. (2013) Large oncosomes mediate intercellular transfer of functional microRNA. Cell Cycle 12(22):3526-3536.
47. Delorme-Axford E, et al. (2013) Human placental trophoblasts confer viral resistance to recipient cells. Proc Natl Acad Sci USA 110(29):12048-12053.
48. Strobl H, et al. (1997) flt3 ligand in cooperation with transforming growth factorbeta1 potentiates in vitro development of Langerhans-type dendritic cells and allows single-cell dendritic cell cluster formation under serum-free conditions. Blood 90(4):1425-1434.
49. Gatti E, et al. (2000) Large-scale culture and selective maturation of human Langerhans cells from granulocyte colony-stimulating factor-mobilized CD34+ progenitors. J Immunol 164(7):3600-3607.
50. Lamparski HG, et al. (2002) Production and characterization of clinical grade exosomes derived from dendritic cells. J Immunol Methods 270(2):211-226.
51. Andrews PA, Velury S, Mann SC, Howell SB (1988) cis-Diamminedichloroplatinum(II) accumulation in sensitive and resistant human ovarian carcinoma cells. Cancer Res 48(1):68-73.