Free extracellular miRNA functionally targets cells by transfecting exosomes from their companion cells

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Bryniarski, Krzysztof ^a,b   Ptak, Wlodzimierz ^b   Martin, Emilia ^b   Nazimek, Katarzyna ^b   Szczepanik, Marian ^b   Sanak, Marek ^b   Askenase, Philip W ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 150; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; ANTIBODY; MIRN150 MICRORNA, MOUSE; TLR3 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; BINDING AFFINITY; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SELECTION; CELL TRANSFER; CELL VIABILITY; CELLULAR SECRETION; CONTACT SENSITIZATION; CONTROLLED STUDY; EXOSOME; GENETIC TRANSFECTION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; RNA TRANSPORT; SIGNAL TRANSDUCTION; SUPPRESSOR CELL; T CELL DEPLETION; ANIMAL; C57BL MOUSE; CELL LINE; GENETICS; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; LYMPHOCYTE ACTIVATION; METABOLISM;

MUS;

ANIMALS; ANTIBODIES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; EXOSOMES; HUMANS; LYMPHOCYTE ACTIVATION; MICE, INBRED C57BL; MICRORNAS; TOLL-LIKE RECEPTOR 3; TRANSFECTION;

EID: 84928818473     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122991     Document Type: Article

References (46)

1. Askenase PW, Tsuji RF (2000) B-1 B cell IgM antibody initiates T cell elicitation of contact sensitivity. Curr Top Microbiol Immunol 252: 171-177. PMID: 11125474
2. Ptak W, Ptak M, Rosenstein RW, Gershon RK (1982) Interactions between molecules (subfactors) released by different T cell sets that yield a complete factor with biological (suppressive) activity. Proc Natl Acad Sci USA 79: 2375-2378. PMID: 6980420
3. Szczepanik M, Akahira-Azuma M, Bryniarski K, Tsuji RF, Kawikova I, Ptak W, et al. (2003) B-1 B cells mediate required early T cell recruitment to elicit protein-induced delayed-type hypersensitivity. J Immunol 171: 6225-6235. PMID: 14634139
4. Lasser C (2015) Exosomes in diagnostic and therapeutic applications: biomarker, vaccine and RNA interference delivery vehicle. Expert Opin Biol Ther 15: 103-117. doi: 10.1517/14712598.2015.977250 PMID: 25363342
5. Bryniarski K, Ptak W, Jayakumar A, Pullmann K, Caplan M, Chairoungdua A, et al. (2013) Antigen-specific, antibody-coated, exosome-like nanovesicles deliver suppressor T-cell microRNA-150 to effector T cells to inhibit contact sensitivity. J Allergy Clin Immunol 132: 170-181. doi: 10.1016/j.jaci.2013.04.048 PMID: 23727037
6. Kerfoot S, Szczepanik M, Tung J, Askenase P (2008) Identification of initiator B-cells, a novel subset of activation induced deaminase (AID)-dependent B-1-like cells that mediate initiation of contact sensitivity. J Immunol. 181:1717-1727. PMID: 18641308
7. Askenase PW, Szczepanik M, Itakura A, Kiener C, Campos RA (2004) Extravascular T-cell recruitment requires initiation begun by Valpha14+ NKT cells and B-1 B cells. Trends Immunol 25: 441-449. PMID: 15275644
8. Thery C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581-593. doi: 10.1038/nri2567 PMID: 19498381
9. Thery C, Amigorena S, Raposo G, Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. In: Current Protocols in Cell Biology, Chapter 3: Unit 3 22. doi: 10.1002/0471143030.cb0322s30
10. Raposo G, Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200: 373-383. doi: 10.1083/jcb.201211138 PMID: 23420871
11. Thery C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2: 569-579. PMID: 12154376
12. Redegeld FA, van der Heijden MV, Kool M, Heijdra BM, Garssen J, Kraneveld AD, et al. (2002) Immunoglobulin-free light chains elicit immediate hypersensitivity-like responses. Nat Med 8: 694-701. PMID: 12068287
13. Paliwal V, Tsuji RF, Szczepanik M, Kawikova I, Campos RA, Kneilling M, et al. (2002) Subunits of IgM reconstitute defective contact sensitivity in B-1 cell-deficient xid mice: kappa light chains recruit T cells independent of complement. J Immunol 169: 4113-4123. PMID: 12370339
14. Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, et al. (2007) MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131: 146-159. PMID: 17923094
15. Hussein K, Theophile K, Busche G, Schlegelberger B, Gohring G, Kreipe H, et al. (2010) Significant inverse correlation of microRNA-150/MYB and microRNA-222/p27 in myelodysplastic syndrome. Leuk Res 34: 328-334. doi: 10.1016/j.leukres.2009.06.014 PMID: 19615744
16. Bezman NA, Chakraborty T, Bender T, Lanier LL (2011) MiR-150 regulates the development of NK and iNKT cells. J Exp Med 208:2717-2731. doi: 10.1084/jem.20111386 PMID: 22124110
17. Ghisi M, Corradin A, Basso K, Frasson C, Serafin V, Mukherjee S, et al. (2011) Modulation of microRNA expression in human T-cell development: targeting of NOTCH3 by miR-150. Blood 117: 7053-7062. doi: 10.1182/blood-2010-12-326629 PMID: 21551231
18. Zheng Q, Zhou L, Mi QS (2012) MicroRNA miR-150 is involved in Valpha14 invariant NKT cell development and function. J Immunol 188: 2118-26. doi: 10.4049/jimmunol.1103342 PMID: 22287707
19. Nazimek K, Nowak B, Marcinkiewicz J, Ptak M, Ptak W, Bryniarski K (2014) Enhanced generation of reactive oxygen intermediates by suppressor T cell-derived exosome-treated macrophages. Folia Med Cracov 54: 37-52. PMID: 25556365
20. EL Andaloussi S, Mager I, Breakefield XO, Wood MJ (2013) Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov 12: 347-357. doi: 10.1038/nrd3978 PMID: 23584393
21. Ohno S, Ishikawa A, Kuroda M (2013) Roles of exosomes and microvesicles in disease pathogenesis. Adv Drug Deliv Rev 65: 398-401. doi: 10.1016/j.addr.2012.07.019 PMID: 22981801
22. Ptak W, Rozycka D, Rewicka M (1980) Induction of suppressor cells and cells producing antigen-specific suppressor factors by haptens bound to self carriers. Immunobiology 156: 400-409. PMID: 6154643
23. Ferreri NR, Herzog WR, Askenase PW (1993) Inhibition of IL-2-dependent proliferation by a prostaglandin-dependent suppressor factor. J Immunol 150: 2102-2111. PMID: 8450204
24. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159. PMID: 2440339
25. England T E, Bruce AG, Uhlenbeck OC (1980) Specific labeling of 3′ termini of RNA with T4 RNA ligase. Methods Enzymol 65: 65-74. PMID: 6154874
26. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. (2011) Argonaute 2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108: 5003-5008. doi: 10.1073/pnas.1019055108 PMID: 21383194
27. Li L, Zhu D, Huang L, Zhang J, Bian Z, Chen X, et al. (2012) Argonaute 2 complexes selectively protect the circulating microRNAs in cell-secreted microvesicles. PLoS One 7: e46957. doi: 10.1371/journal. pone.0046957 PMID: 23077538
28. Turchinovich A, Burwinkel B (2012) Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma. RNA Biol 9: 1066-1075. doi: 10.4161/rna.21083 PMID: 22858679
29. Vickers KC, Remaley AT (2012) Lipid-based carriers of microRNAs and intercellular communication. Curr Opin Lipidol 23: 91-97. doi: 10.1097/MOL.0b013e328350a425 PMID: 22418571
30. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 13: 423-433. doi: 10.1038/ncb2210 PMID: 21423178
31. Hutchinson AT, Jones DR, Raison RL (2012) The ability to interact with cell membranes suggests possible biological roles for free light chain. Immunol Lett 142: 75-77. doi: 10.1016/j.imlet.2011.10.013 PMID: 22138405
32. Bryniarski K, Ptak W, Nazimek K, Askenase PW. (2014) Passive transfection of antigen-specific exosomes with immunoregulatory miRNA-150 to suppress contact sensitivity. Centr Eur J Immunol 39 (Suppl. 1): 20.
33. Turchinovich A, Weiz L, Burwinkel B (2012) Extracellular miRNAs: the mystery of their origin and function. Trends Biochem Sci 37: 460-465. doi: 10.1016/j.tibs.2012.08.003 PMID: 22944280
34. Turchinovich A, Weiz L, Langheinz A, Burwinkel B (2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res 39: 7223-7233. doi: 10.1093/nar/gkr254 PMID: 21609964
35. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, et al. (2008) Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18: 997-1006. doi: 10.1038/cr.2008.282 PMID: 18766170
36. Wang K, Zhang S,Weber J, Baxter D, Galas DJ (2010) Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res 38: 7248-7259. doi: 10.1093/nar/gkq601 PMID: 20615901
37. Schwarzenbach H, Nishida N, Calin GA, Pantel K (2014) Clinical relevance of circulating cell-free micro-RNAs in cancer. Nat Rev Clin Oncol 11: 145-156. doi: 10.1038/nrclinonc.2014.5 PMID: 24492836
38. Sheinerman KS, Tsivinsky VG, Umansky SR (2013) Analysis of organ-enriched microRNAs in plasma as an approach to development of Universal Screening Test: feasibility study. J Transl Med 11: 304. doi: 10.1186/1479-5876-11-304 PMID: 24330742
39. Liang H, Gong F, Zhang S, Zhang CY, Zen K, Chen X (2014) The origin, function, and diagnostic potential of extracellular microRNAs in human body fluids. Wiley Interdiscip Rev RNA 5: 285-300. doi: 10.1002/wrna.1208 PMID: 24259376
40. Xu L, Qi X, Duan S, Xie Y, Ren X, Chen G, et al. (2014) MicroRNAs: potential biomarkers for disease diagnosis. Biomed Mater Eng 24: 3917-3925. doi: 10.3233/BME-141223 PMID: 25227110
41. Chen X, Liang H, Zhang J, Zen K, Zhang CY (2012) Horizontal transfer of microRNAs: molecular mechanisms and clinical applications. Protein Cell 3: 28-37. doi: 10.1007/s13238-012-2003-z PMID: 22314808
42. Boon RA, Vickers KC (2013) Intercellular transport of microRNAs. Arterioscler Thromb Vasc Biol 33: 186-192. doi: 10.1161/ATVBAHA.112.300139 PMID: 23325475
43. Turchinovich A, Samatov TR, Tonevitsky AG, Burwinkel B (2013) Circulating miRNAs: cell-cell communication function? Front Genet 4: 119. doi: 10.3389/fgene.2013.00119 PMID: 23825476
44. Zhuang X, Xiang X, Grizzle W, Sun D, Zhang S, Axtell RC, et al. (2011) Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther 19: 1769-1779. doi: 10.1038/mt.2011.164 PMID: 21915101
45. Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29: 341-345. doi: 10.1038/nbt.1807 PMID: 21423189
46. Ptak W, Nazimek K, Askenase PW, Bryniarski K (2015) From mysterious supernatant entity to miRNA-150 in antigen-specific exosomes: a history of a hapten-specific T suppressor factor. Arch Immunol Ther Exp (in press) doi: 10.1007/s00005-015-0331-4