Broad role for YBX1 in defining the small noncoding RNA composition of exosomes

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

Volumn 114, Issue 43, 2017, Pages E8987-E8995

  Shurtleff, Matthew J ^a,b   Yao, Jun ^c   Qin, Yidan ^c   Nottingham, Ryan M ^c   Temoche Diaz, Morayma M ^b   Schekman, Randy ^a,d   Lambowitz, Alan M ^c  

^a University of California Berkeley   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD63 ANTIGEN; COMPLEMENTARY RNA; LONG UNTRANSLATED RNA; SMALL UNTRANSLATED RNA; TRANSFER RNA; Y BOX BINDING PROTEIN 1; DNA; YBX1 PROTEIN, HUMAN;

ARTICLE; CELL SELECTION; DNA CONTAMINATION; DNA MODIFICATION; EXOSOME; HEK293T CELL LINE; INTRON; PRIORITY JOURNAL; RNA EXTRACTION; SEQUENCE ANALYSIS; TERMINAL OLIGOPYRIMIDINE TRACT; THERMOSTABILITY; ULTRACENTRIFUGATION; ANIMAL; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; DNA; EXOSOMES; EXTRACELLULAR VESICLES; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; RNA, SMALL UNTRANSLATED; Y-BOX-BINDING PROTEIN 1;

EID: 85032000154     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1712108114     Document Type: Article

References (57)

1. Colombo M, Raposo G, Théry C (2014) Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 30: 255-289.
2. Bobrie A, Colombo M, Krumeich S, Raposo G, Théry C (2012) Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation. J Extracell Vesicles 1:18397.
3. Gould SJ, Raposo G (2013) As we wait: Coping with an imperfect nomenclature for extracellular vesicles. J Extracell Vesicles 2:20389.
4. Booth AM, et al. (2006) Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J Cell Biol 172:923-935.
5. Skog J, et al. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470-1476.
6. Ratajczak J, et al. (2006) Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20:847-856.
7. Valadi H, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654-659.
8. Mitchell PS, et al. (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105:10513-10518.
9. Kosaka N, et al. (2010) Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285:17442-17452.
10. Meckes DG, Jr, et al. (2010) Human tumor virus utilizes exosomes for intercellular communication. Proc Natl Acad Sci USA 107:20370-20375.
11. Pegtel DM, et al. (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107:6328-6333.
12. Squadrito ML, et al. (2014) Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep 8:1432-1446.
13. Ridder K, et al. (2014) Extracellular vesicle-mediated transfer of genetic information between the hematopoietic system and the brain in response to inflammation. PLoS Biol 12:e1001874.
14. Zomer A, et al. (2015) In vivo imaging reveals extracellular vesicle-mediated phenocopying of metastatic behavior. Cell 161:1046-1057.
15. Bellingham SA, Coleman BM, Hill AF (2012) Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res 40:10937-10949.
16. Nolte-'t Hoen EN, et al. (2012) Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res 40:9272-9285.
17. Ogawa Y, Taketomi Y, Murakami M, Tsujimoto M, Yanoshita R (2013) Small RNA transcriptomes of two types of exosomes in human whole saliva determined by next generation sequencing. Biol Pharm Bull 36:66-75.
18. Batagov AO, Kuznetsov VA, Kurochkin IV (2011) Identification of nucleotide patterns enriched in secreted RNAs as putative cis-acting elements targeting them to exosome nano-vesicles. BMC Genomics 12(Suppl 3):S18.
19. Vojtech L, et al. (2014) Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res 42: 7290-7304.
20. Qin Y, et al. (2016) High-throughput sequencing of human plasma RNA by using thermostable group II intron reverse transcriptases. RNA 22:111-128.
21. 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: 5003-5008.
22. Cha DJ, et al. (2015) KRAS-dependent sorting of miRNA to exosomes. Elife 4:e07197.
23. McKenzie AJ, et al. (2016) KRAS-MEK signaling controls Ago2 sorting into exosomes. Cell Rep 15:978-987.
24. Shurtleff MJ, Temoche-Diaz MM, Karfilis KV, Ri S, Schekman R (2016) Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction. Elife 5:e19276.
25. Villarroya-Beltri C, et al. (2013) Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4:2980.
26. Santangelo L, et al. (2016) The RNA-binding protein SYNCRIP is a component of the hepatocyte exosomal machinery controlling microRNA sorting. Cell Rep 17:799-808.
27. Mukherjee K, et al. (2016) Reversible HuR-microRNA binding controls extracellular export of miR-122 and augments stress response. EMBO Rep 17:1184-1203.
28. Mohr S, et al. (2013) Thermostable group II intron reverse transcriptase fusion proteins and their use in cDNA synthesis and next-generation RNA sequencing. RNA 19: 958-970.
29. Wu DC, Lambowitz AM (2017) Facile single-stranded DNA sequencing of human plasma DNA via thermostable group II intron reverse transcriptase template switching. Sci Rep 7:8421.
30. Nottingham RM, et al. (2016) RNA-seq of human reference RNA samples using a thermostable group II intron reverse transcriptase. RNA 22:597-613.
31. Katibah GE, et al. (2014) Broad and adaptable RNA structure recognition by the human interferon-induced tetratricopeptide repeat protein IFIT5. Proc Natl Acad Sci USA 111:12025-12030.
32. Eckwahl MJ, Sim S, Smith D, Telesnitsky A, Wolin SL (2015) A retrovirus packages nascent host noncoding RNAs from a novel surveillance pathway. Genes Dev 29: 646-657.
33. Eckwahl MJ, et al. (2016) Analysis of the human immunodeficiency virus-1 RNA packageome. RNA 22:1228-1238.
34. Dhahbi JM, et al. (2013) 5'-YRNA fragments derived by processing of transcripts from specific YRNA genes and pseudogenes are abundant in human serum and plasma. Physiol Genomics 45:990-998.
35. Kumar P, Kuscu C, Dutta A (2016) Biogenesis and function of transfer RNA-related fragments (tRFs). Trends Biochem Sci 41:679-689.
36. Tosar JP, et al. (2015) Assessment of small RNA sorting into different extracellular fractions revealed by high-throughput sequencing of breast cell lines. Nucleic Acids Res 43:5601-5616.
37. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262:9412-9420.
38. Avni D, Biberman Y, Meyuhas O (1997) The 5' terminal oligopyrimidine tract confers translational control on TOP mRNAs in a cell type- and sequence context-dependent manner. Nucleic Acids Res 25:995-1001.
39. Avni D, Shama S, Loreni F, Meyuhas O (1994) Vertebrate mRNAs with a 5'-terminal pyrimidine tract are candidates for translational repression in quiescent cells: Characterization of the translational cis-regulatory element. Mol Cell Biol 14:3822-3833.
40. Damgaard CK, Lykke-Andersen J (2011) Translational coregulation of 5'TOP mRNAs by TIA-1 and TIAR. Genes Dev 25:2057-2068.
41. Iadevaia V, Caldarola S, Tino E, Amaldi F, Loreni F (2008) All translation elongation factors and the e, f, and h subunits of translation initiation factor 3 are encoded by 5'-terminal oligopyrimidine (TOP) mRNAs. RNA 14:1730-1736.
42. Lässer C, et al. (2017) Two distinct extracellular RNA signatures released by a single cell type identified by microarray and next-generation sequencing. RNA Biol 14: 58-72.
43. Guzman N, et al. (2015) Breast cancer-specific miR signature unique to extracellular vesicles includes "microRNA-like" tRNA fragments. Mol Cancer Res 13:891-901.
44. Wang F, et al. (2013) Regulated capture by exosomes of mRNAs for cytoplasmic tRNA synthetases. J Biol Chem 288:29223-29228.
45. Lo WS, et al. (2014) Human tRNA synthetase catalytic nulls with diverse functions. Science 345:328-332.
46. Blenkiron C, Hurley DG, Fitzgerald S, Print CG, Lasham A (2013) Links between the oncoprotein YB-1 and small non-coding RNAs in breast cancer. PLoS One 8:e80171.
47. Goodarzi H, et al. (2015) Endogenous tRNA-derived fragments suppress breast cancer progression via YBX1 displacement. Cell 161:790-802.
48. Liu TT, et al. (2015) Noncoding RNAs that associate with YB-1 alter proliferation in prostate cancer cells. RNA 21:1159-1172.
49. Lyons SM, Achorn C, Kedersha NL, Anderson PJ, Ivanov P (2016) YB-1 regulates tiRNAinduced stress granule formation but not translational repression. Nucleic Acids Res 44:6949-6960.
50. Lyabin DN, Eliseeva IA, Ovchinnikov LP (2014) YB-1 protein: Functions and regulation. Wiley Interdiscip Rev RNA 5:95-110.
51. Somasekharan SP, et al. (2015) YB-1 regulates stress granule formation and tumor progression by translationally activating G3BP1. J Cell Biol 208:913-929.
52. Lin Y, Protter DS, Rosen MK, Parker R (2015) Formation and maturation of phaseseparated liquid droplets by RNA-binding proteins. Mol Cell 60:208-219.
53. Chakrabortty SK, Prakash A, Nechooshtan G, Hearn S, Gingeras TR (2015) Extracellular vesicle-mediated transfer of processed and functional RNY5 RNA. RNA 21:1966-1979.
54. Lasda E, Parker R (2016) Circular RNAs co-precipitate with extracellular vesicles: A possible mechanism for circRNA clearance. PLoS One 11:e0148407.
55. Nabet BY, et al. (2017) Exosome RNA unshielding couples stromal activation to pattern recognition receptor signaling in cancer. Cell 170:352-366.e13.
56. Lasham A, Print CG, Woolley AG, Dunn SE, Braithwaite AW (2013) YB-1: Oncoprotein, prognostic marker and therapeutic target? Biochem J 449:11-23.
57. Meyuhas O, Kahan T (2015) The race to decipher the top secrets of TOP mRNAs. Biochim Biophys Acta 1849:801-811.