Movement of regulatory RNA between animal cells

Genesis

Volumn 53, Issue 7, 2015, Pages 395-416

  Jose, Antony M ^a  

^a University of Maryland   (United States)

Author keywords

C. elegans; Epigenetics; Exosomes; Hormones; Mobile RNA; Systemic RNAi

Indexed keywords

RNA; STEROID HORMONE; REGULATORY RNA SEQUENCE;

ANIMAL CELL; BASE PAIRING; BIOGENESIS; CAENORHABDITIS ELEGANS; CELL COMMUNICATION; CELL MEMBRANE; CELLULAR SECRETION; CYTOSOL; EXTRACELLULAR FLUID; GENE CONTROL; GENETIC MODEL; GERM CELL; HUMAN; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA TRANSPORT; ANIMAL; DROSOPHILA MELANOGASTER; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; REGULATORY RNA SEQUENCE;

ANIMALIA; CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CELL COMMUNICATION; DROSOPHILA MELANOGASTER; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA; RNA TRANSPORT;

EID: 84937736479     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22871     Document Type: Review

References (219)

1. Akay A, Sarkies P, Miska EA. 2015. E. coli OxyS non-coding RNA does not trigger RNAi in C. elegans. Sci Rep 5:9597.
2. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732-738.
3. Ambros V. 2011. MicroRNAs and developmental timing. Curr Opin Genet Dev 21:511-517.
4. Aronstein K, Pankiw T, Saldivar E. 2006. SID-I is implicated in systemic gene silencing in the honey bee. J Apiculture Res Bee World 45:20-24.
5. 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. 2011. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108:5003-5008.
6. Aucher A, Rudnicka D, Davis DM. 2013. MicroRNAs transfer from human macrophages to hepato-carcinoma cells and inhibit proliferation. J Immunol 191:6250-6260.
7. Backes S, Langlois RA, Schmid S, Varble A, Shim JV, Sachs D, tenOever BR. 2014. The Mammalian response to virus infection is independent of small RNA silencing. Cell Rep 8:114-125.
8. Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, Zimmermann P, David G. 2012. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14:677-685.
9. Banse SA, Hunter CP. 2012. Vampiric isolation of extracellular fluid from Caenorhabditis elegans. J Vis Exp 61:e3647.
10. Bayer-Santos E, Lima FM, Ruiz JC, Almeida IC, da Silveira JF. 2014. Characterization of the small RNA content of Trypanosoma cruzi extracellular vesicles. Mol Biochem Parasitol 193:71-74.
11. 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.
12. Belyi VA, Levine AJ, Skalka AM. 2010. Unexpected inheritance: Multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog. 6:e1001030.
13. Benkovics AH, Timmermans MC. 2014. Developmental patterning by gradients of mobile small RNAs. Curr Opin Genet Dev 27C:83-91.
14. Billi AC, Fischer SE, Kim JK. 2014. Endogenous RNAi pathways in C. elegans. WormBook 7:1-49.
15. Billy E, Brondani V, Zhang H, Muller U, Filipowicz W. 2001. Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. Proc Natl Acad Sci USA 98:14428-14433.
16. Blanchard D, Parameswaran P, Lopez-Molina J, Gent J, Saynuk JF, Fire A. 2011. On the nature of in vivo requirements for rde-4 in RNAi and developmental pathways in C. elegans. RNA Biol 8:458-467.
17. Bolukbasi MF, Mizrak A, Ozdener GB, Madlener S, Ströbel T, Erkan EP, Fan JB, Breakefield XO, Saydam O. 2012. miR-1289 and "Zipcode"-like Sequence Enrich mRNAs in Microvesicles. Mol Ther Nucleic Acids 1:e10.
18. Briese M, Esmaeili B, Johnson NM, Sattelle DB. 2006. pWormgatePro enables promoter-driven knockdown by hairpin RNA interference of muscle and neuronal gene products in Caenorhabditis elegans. Invert Neurosci 6:5-12.
19. Bronisz A, Wang Y, Nowicki MO, Peruzzi P, Ansari KI, Ogawa D, Balaj L, De Rienzo G, Mineo M, Nakano I, Ostrowski MC, Hochberg F, Weissleder R, Lawler SE, Chiocca EA, Godlewski J. 2014. Extracellular vesicles modulate the glioblastoma microenvironment via a tumor suppression signaling network directed by miR-1. Cancer Res 74:738-750.
20. Brunkard JO, Runkel AM, Zambryski PC. 2015. The cytosol must flow: Intercellular transport through plasmodesmata. Curr Opin Cell Biol 35:13-20.
21. Buck AH, Coakley G, Simbari F, McSorley HJ, Quintana JF, Le Bihan T, Kumar S, Abreu-Goodger C, Lear M, Harcus Y, Ceroni A, Babayan SA, Blaxter M, Ivens A, Maizels RM. 2014. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun 5:5488.
22. Calixto A, Chelur D, Topalidou I, Chen X, Chalfie M. 2010. Enhanced neuronal RNAi in C. elegans using SID-1. Nat Methods 7:554-559.
23. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN. 2010. Cell signaling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316-321.
24. Chauhan VM, Orsi G, Brown A, Pritchard DI, Aylott JW. 2013. Mapping the pharyngeal and intestinal pH of Caenorhabditis elegans and real-time luminal pH oscillations using extended dynamic range pH-sensitive nanosensors. ACS Nano 7:5577-5587.
25. Chen C, Lin BR, Hsu MY, Cheng CM. 2015. Paper-based Devices for Isolation and Characterization of Extracellular Vesicles. J Vis Exp 98:e52722.
26. Chen CC, Simard MJ, Tabara H, Brownell DR, McCollough JA, Mello CC. 2005. A member of the polymerase beta nucleotidyltransferase superfamily is required for RNA interference in C. elegans. Curr Biol 15:378-383.
27. Chevillet JR, Kang Q, Ruf IK, Briggs HA, Vojtech LN, Hughes SM, Cheng HH, Arroyo JD, Meredith EK, Gallichotte EN, Pogosova-Agadjanyan EL, Morrissey C, Stirewalt DL, Hladik F, Yu EY, Higano CS, Tewari M. 2014. Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc Natl Acad Sci USA 111:14888-14893.
28. Chim SS, Shing TK, Hung EC, Leung TY, Lau TK, Chiu RW, Lo YM. 2008. Detection and characterization of placental microRNAs in maternal plasma. Clin Chem 54:482-490.
29. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC. 2009. Pattern formation via small RNA mobility. Genes Dev 23:549-554.
30. Chou S, Daugherty MD, Peterson SB, Biboy J, Yang Y, Jutras BL, Fritz-Laylin LK, Ferrin MA, Harding BN, Jacobs-Wagner C, Yang XF, Vollmer W, Malik HS, Mougous JD. 2015. Transferred interbacterial antagonism genes augment eukaryotic innate immune function. Nature 518:98-101.
31. Collino F, Deregibus MC, Bruno S, Sterpone L, Aghemo G, Viltono L, Tetta C, Camussi G. 2010. Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS One 5:e11803.
32. 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.
33. Cossetti C, Lugini L, Astrologo L, Saggio I, Fais S, Spadafora C. 2014. Soma-to-germline transmission of RNA in mice xenografted with human tumour cells: Possible transport by exosomes. PLoS One 9:e101629.
34. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, Martinson V, vanEngelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai J, Cui L, Hutchison SK, Simons JF, Egholm M, Pettis JS, Lipkin WI. 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283-287.
35. Crescitelli R, Lässer C, Szabó TG, Kittel A, Eldh M, Dianzani I, Buzás EI, Lötvall J. 2013. Distinct RNA profiles in subpopulations of extracellular vesicles: Apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles 2:20677.
36. Cullen BR, Cherry S, tenOever BR. 2013. Is RNA interference a physiologically relevant innate antiviral immune response in mammals? Cell Host Microbe 14:374-378.
37. Darwin C. 1868. Provisional hypothesis of pangenesis. The variation of animals and plants under domestication, Vol. 27. London: John Murray. pp 349-399.
38. Devanapally S, Ravikumar S, Jose AM. 2015. Double-stranded RNA made in C. elegans neurons can enter the germline and cause transgenerational gene silencing. Proc Natl Acad Sci USA 112:2133-2138.
39. Dias BG, Ressler KJ. 2014. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci 17:89-96.
40. Ding SW, Voinnet O. 2014. Antiviral RNA silencing in mammals: no news is not good news. Cell Rep 9:795-797.
41. Dunning Hotopp JC. 2011. Horizontal gene transfer between bacteria and animals. Trends Genet 27:157-163.
42. Dunning Hotopp JC, Clark ME, Oliveira DCSG, Foster JM, Fischer P, Munoz Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH. 2007. Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes. Science 317:1753-1756.
43. Duxbury MS, Ashley SW, Whang EE. 2005. RNA interference: A mammalian SID-1 homologue enhances siRNA uptake and gene silencing efficacy in human cells. Biochem Biophys Res Commun 331:459-463.
44. Dzitoyeva S, Dimitrijevic N, Manev, H. 2001. Intra-abdominal injection of double-stranded RNA into anesthetized adult Drosophila triggers RNA interference in the central nervous system. Mol Psychiatry 6:665-670.
45. Elhassan MO, Christie J, Duxbury MS. 2012. Homo sapiens systemic RNA interference-defective-1 transmembrane family member 1 (SIDT1) protein mediates contact-dependent small RNA transfer and microRNA-21-driven chemoresistance. J Biol Chem 287:5267-5277.
46. Extavour CG, Akam M. 2003. Mechanisms of germ cell specification across the metazoans: Epigenesis and preformation. Development 130:5869-5884.
47. Feinberg EH, Hunter CP. 2003. Transport of dsRNA into cells by the transmembrane protein SID-1. Science 301:1545-1547.
48. Feng S, Jacobsen SE, Reik W. 2010. Epigenetic reprogramming in plant and animal development. Science 330:622-627.
49. Fernandez-Calero T, Garcia-Silva R, Pena A, Robello C, Persson H, Rovira C, Naya H, Cayota A. 2015. Profiling of small RNA cargo of extracellular vesicles shed by Trypanosoma cruzi reveals a specific extracellular signature. Mol Biochem Parasitol 199:19-28.
50. Figliolini F, Cantaluppi V, De Lena M, Beltramo S, Romagnoli R, Salizzoni M, Melzi R, Nano R, Piemonti L, Tetta C, Biancone L, Camussi G. 2014. Isolation, characterization and potential role in beta cell-endothelium cross-talk of extracellular vesicles released from human pancreatic islets. PLoS One 9:e102521.
51. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811.
52. Fong MY, Zhou W, Liu L, Alontaga AY, Chandra M, Ashby J, Chow A, O'Connor ST, Li S, Chin AR, Somlo G, Palomares M, Li Z, Tremblay JR, Tsuyada A, Sun G, Reid MA, Wu X, Swiderski P, Ren X, Shi Y, Kong M, Zhong W, Chen Y, Wang SE. 2015. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat Cell Biol 17:183-194.
53. Frézal L, Félix MA. 2015. C. elegans outside the Petri dish. Elife 4:e05849.
54. Fukuda K, Watanabe T, Tokisue T, Tsujita T, Nishikawa S, Hasegawa T, Seya T, Matsumoto M. 2008. Modulation of double-stranded RNA recognition by the N-terminal histidine-rich region of the human toll-like receptor 3. J Biol Chem 283:22787-22794.
55. Gantier MP, Williams BR. 2007. The response of mammalian cells to double-stranded RNA. Cytokine Growth Factor Rev 18:363-371.
56. Gao J, Gu X, Mahuran DJ, Wang Z, Zhang H. 2013. Impaired glucose tolerance in a mouse model of sidt2 deficiency. PLoS One. 8:e66139.
57. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, Farinelli L, Miska E, Mansuy IM. 2014. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 17:667-669.
58. Garbian Y, Maori E, Kalev H, Shafir S, Sela I. 2012. Bidirectional transfer of RNAi between honey bee and Varroa destructor: Varroa gene silencing reduces Varroa population. PLoS Pathog 8:e1003035.
59. Goto A, Blandin S, Royet J, Reichhart JM, Levashina EA. 2003. Silencing of toll pathway components by direct injection of double-stranded RNA into Drosophila adult flies. Nucl Acids Res 31:6619-6623.
60. Greer EL, Maures TJ, Ucar D, Hauswirth AG, Mancini E, Lim JP, Benayoun BA, Shi Y, Brunet A. 2011. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479:365-371.
61. Grishok A. 2013. Biology and Mechanisms of Short RNAs in Caenorhabditis elegans. Adv Genet 83:1-69.
62. Guduric-Fuchs J, O'Connor A, Camp B, O'Neill CL, Medina RJ, Simpson DA. 2012. Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics 13:357.
63. Hammond SM. An overview of microRNAs. Adv Drug Deliv Rev, e-pub, 12 May 2015.
64. Han W, Sundaram P, Kenjale H, Grantham J, Timmons L. 2008. The Caenorhabditis elegans rsd-2 and rsd-6 genes are required for chromosome functions during exposure to unfavorable environments. Genetics 178:1875-1893.
65. Hansen EP, Kringel H, Williams AR, Nejsum P. Secretion of RNA-containing extracellular vesicles by the porcine whipworm, Trichuris suis. J Parasitol 101:336-340.
66. Harris KP, Tepass U. 2010. Cdc42 and vesicle trafficking in polarized cells. Traffic 11:1272-1279.
67. Hinas A, Wright AJ, Hunter CP. 2012. SID-5 is an endosome-associated protein required for efficient systemic RNAi in C. elegans. Curr Biol 22:1938-1943.
68. Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T, Oshida T, Ikuta K, Jern P, Gojobori T, Coffin JM, Tomonaga K. 2010. Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463:84-87.
69. Hosoda T, Zheng H, Cabral-da-Silva M, Sanada F, Ide-Iwata N, Ogórek B, Ferreira-Martins J, Arranto C, D'Amario D, del Monte F, Urbanek K, D'Alessandro DA, Michler RE, Anversa P, Rota M, Kajstura J, Leri A. 2011. Human cardiac stem cell differentiation is regulated by a mircrine mechanism. Circulation 123:1287-1296.
70. 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. 2008. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3:e3694.
71. Hunter W, Ellis J, Vanengelsdorp D, Hayes J, Westervelt D, Glick E, Williams M, Sela I, Maori E, Pettis J, Cox-Foster D, Paldi N. 2010. Large-scale field application of RNAi technology reducing Israeli acute paralysis virus disease in honey bees (Apis mellifera, Hymenoptera: Apidae). PLoS Pathog 6:e1001160.
72. Huvenne H, Smagghe G. 2010. Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: A review. J Insect Physiol 56:227-235.
73. Ismail N, Wang Y, Dakhlallah D, Moldovan L, Agarwal K, Batte K, Shah P, Wisler J, Eubank TD, Tridandapani S, Paulaitis ME, Piper MG, Marsh CB. 2013. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood 121:984-995.
74. Ivashuta S, Zhang Y, Wiggins BE, Ramaseshadri P, Segers GC, Johnson S, Meyer SE, Kerstetter RA, McNulty BC, Bolognesi R, Heck GR. 2015. Environmental RNAi in herbivorous insects. RNA 21:840-850.
75. Jialin G, Xuefan G, Huiwen Z. 2010. SID1 transmembrane family, member 2 (Sidt2): A novel lysosomal membrane protein. Biochem Biophys Res Commun 402:588-594.
76. Jose AM, Hunter CP. 2007. Transport of sequence-specific RNA interference information between cells. Annu Rev Genet 41:305-330.
77. Jose AM, Smith JJ, Hunter CP. 2009. Export of RNA silencing from C. elegans tissues does not require the RNA channel SID-1. Proc Natl Acad Sci USA 106:2283-2288.
78. Jose AM, Garcia GA, Hunter CP. 2011. Two classes of silencing RNAs move between Caenorhabditis elegans tissues. Nat Struct Mol Biol 18:1184-1188.
79. Jose AM, Kim YA, Leal-Ekman S, Hunter CP. 2012. Conserved tyrosine kinase promotes the import of silencing RNA into Caenorhabditis elegans cells. Proc Natl Acad Sci USA 109:14520-14525.
80. Juang BT, Gu C, Starnes L, Palladino F, Goga A, Kennedy S, L'Etoile ND. 2013. Endogenous nuclear RNAi mediates behavioral adaptation to odor. Cell 154:1010-1022.
81. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J. 2003. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231-237.
82. Katakowski M, Buller B, Wang X, Rogers T, Chopp M. 2010. Functional microRNA is transferred between glioma cells. Cancer Res 70:8259-8263.
83. Katoch R, Sethi A, Thakur N, Murdock LL. 2013. RNAi for insect control: Current perspective and future challenges. Appl Biochem Biotechnol 171:847-873.
84. Kim YK, Yeo J, Kim B, Ha M, Kim VN. 2012. Short structured RNAs with low GC content are selectively lost during extraction from a small number of cells. Mol Cell 46:893-895.
85. Kizana E, Cingolani E, Marbán E. 2009. Non-cell-autonomous effects of vector-expressed regulatory RNAs in mammalian heart cells. Gene Ther 16:1163-1168.
86. Kobayashi I, Tsukioka H, Kômoto N, Uchino K, Sezutsu H, Tamura T, Kusakabe T, Tomita S. 2012. SID-1 protein of Caenorhabditis elegans mediates uptake of dsRNA into Bombyx cells. Insect Biochem Mol Biol 42:148-154.
87. Koppers-Lalic D, Hackenberg M, Bijnsdorp IV, van Eijndhoven MA, Sadek P, Sie D, Zini N, Middeldorp JM, Ylstra B, de Menezes RX, Würdinger T, Meijer GA, Pegtel DM. 2014. Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep 8:1649-1658.
88. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. 2010a. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285:17442-17452.
89. Kosaka N, Izumi H, Sekine K, Ochiya T. 2010b. microRNA as a new immune-regulatory agent in breast milk. Silence 1:7.
90. Labreuche Y, Veloso A, de la Vega E, Gross PS, Chapman RW, Browdy CL, Warr GW. 2010. Non-specific activation of antiviral immunity and induction of RNA interference may engage the same pathway in the Pacific white leg shrimp Litopenaeus vannamei. Dev Comp Immunol 34:1209-1218.
91. Lee JK, Park SR, Jung BK, Jeon YK, Lee YS, Kim MK, Kim YG, Jang JY, Kim CW. 2013. Exosomes derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells. PLoS One 8:e84256.
92. Lee YS, Pressman S, Andress AP, Kim K, White JL, Cassidy JJ, Li X, Lubell K, Lim do H, Cho IS, Nakahara K, Preall JB, Bellare P, Sontheimer EJ, Carthew RW. 2009. Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 11:1150-1156.
93. Lee RC, Hammell CM, Ambros V. 2006. Interacting endogenous and exogenous RNAi pathways in Caenorhabditis elegans. RNA 12:589-597.
94. Leslie M. 2013. NIH effort gambles on mysterious extracellular RNAs. Science 341:947.
95. Li W, Koutmou KS, Leahy DJ, Li M. Systemic RNA Interference Deficiency-1 (SID-1) extracellular domain selectively binds long double-stranded RNA and is required for RNA transport by SID-1. J Biol Chem, e-pub, 11 Jun 2015.
96. Li Y, Lu J, Han Y, Fan X, Ding SW. 2013. RNA interference functions as an antiviral immunity mechanism in mammals. Science 342:231-234.
97. Lim PK, Bliss SA, Patel SA, Taborga M, Dave MA, Gregory LA, Greco SJ, Bryan M, Patel PS, Rameshwar P. 2011. Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res 71:1550-1560.
98. Liu H, Wang X, Wang HD, Wu J, Ren J, Meng L, Wu Q, Dong H, Wu J, Kao TY, Ge Q, Wu ZX, Yuh CH, Shan G. 2012. Escherichia coli noncoding RNAs can affect gene expression and physiology of Caenorhabditis elegans. Nat Commun 3:1073.
99. Liu L, Botos I, Wang Y, Leonard JN, Shiloach J, Segal DM, Davies DR. 2008. Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 320:379-381.
100. Long OS, Benson JA, Kwak JH, Luke CJ, Gosai SJ, O'Reilly LP, Wang Y, Li J, Vetica AC, Miedel MT, Stolz DB, Watkins SC, Züchner S, Perlmutter DH, Silverman GA, Pak SC. 2014. A C. elegans model of human α1-antitrypsin deficiency links components of the RNAi pathway to misfolded protein turnover. Hum Mol Genet 23:5109-5122.
101. Lu R, Maduro M, Li F, Li HW, Broitman-Maduro G, Li WX, Ding, SW. 2005. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436:1040-1043.
102. Luo Y, Wang X, Yu D, Kang L. 2012. The SID-1 double-stranded RNA transporter is not required for systemic RNAi in the migratory locust. RNA Biol 9:663-671.
103. Ma S, Chang J, Wang X, Liu Y, Zhang J, Lu W, Gao J, Shi R, Zhao P, Xia Q. 2014. CRISPR/Cas9 mediated multiplex genome editing and heritable mutagenesis of BmKu70 in Bombyx mori. Sci Rep 4:4489.
104. Maillard PV, Ciaudo C, Marchais A, Li Y, Jay F, Ding SW, Voinnet O. 2013. Antiviral RNA interference in mammalian cells. Science 342:235-238.
105. Maori E, Paldi N, Shafir S, Kalev H, Tsur E, Glick E, Sela I. 2009. IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion. Insect Mol Biol 18:55-60.
106. Mayoral JG, Hussain M, Joubert DA, Iturbe-Ormaetxe I, O'Neill SL, Asgari S. 2014. Wolbachia small noncoding RNAs and their role in cross-kingdom communications. Proc Natl Acad Sci USA 111:18721-18726.
107. McEwan DL, Weisman AS, Hunter CP. 2012. Uptake of extracellular doublestranded RNA by SID-2. Mol Cell 47:746-754.
108. Metcalf JA, Funkhouser-Jones LJ, Brileya K, Reysenbach AL, Bordenstein SR. 2014. Antibacterial gene transfer across the tree of life. Elife 3:e04266.
109. Miller SC, Brown SJ, Tomoyasu Y. 2008. Larval RNAi in Drosophila? Dev Genes Evol 218:505-510.
110. Miller SC, Miyata K, Brown SJ, Tomoyasu Y. 2012. Dissecting systemic RNA interference in the red flour beetle Tribolium castaneum: Parameters affecting the efficiency of RNAi. PloS One 7:e47431.
111. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A, Sanchez-Madrid F. 2011. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2:282.
112. Miyashima S, Koi S, Hashimoto T, Nakajima K. 2011. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138:2303-2313.
113. Mlotshwa S, Voinnet O, Mette MF, Matzke M, Vaucheret H, Ding SW, Pruss G, Vance VB. 2002. RNA silencing and the mobile silencing signal. Plant Cell 14:S289-301.
114. Mochizuki K, Fine NA, Fujisawa T, Gorovsky MA. 2002. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell 110:689-699.
115. Mon H, Kobayashi I, Ohkubo S, Tomita S, Lee J, Sezutsu H, Tamura T, Kusakabe T. 2012. Effective RNA interference in cultured silkworm cells mediated by overexpression of Caenorhabditis elegans SID-1. RNA Biol 9:40-46.
116. Mon H, Li Z, Kobayashi I, Tomita S, Lee J, Sezutsu H, Tamura T, Kusakabe T. 2013. Soaking RNAi in Bombyx mori BmN4-SID1 cells arrests cell cycle progression. J Insect Sci 13:155.
117. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z, Milosevic J, Tkacheva OA, Divito SJ, Jordan R, Lyons-Weiler J, Watkins SC, Morelli AE. 2012. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119:756-766.
118. Morales CR, Lefrancois S, Chennathukuzhi V, El-Alfy M, Wu X, Yang J, Gerton GL, Hecht NB. 2002. A TB-RBP and Ter ATPase complex accompanies specific mRNAs from nuclei through the nuclear pores and into intercellular bridges in mouse male germ cells. Dev Biol 246:480-494.
119. Morel L, Regan M, Higashimori H, Ng SK, Esau C, Vidensky S, Rothstein J, Yang Y. 2013. Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1. J Biol Chem 288:7105-7116.
120. Njock MS, Cheng HS, Dang LT, Nazari-Jahantigh M, Lau AC, Boudreau E, Roufaiel M, Cybulsky MI, Schober A, Fish JE. 2015. Endothelial cells suppress monocyte activation through secretion of extracellular vesicles containing antiinflammatory microRNAs. Blood 125:3202-3212.
121. Nolte-'t Hoen EN, Buermans HP, Waasdorp M, Stoorvogel W, Wauben MH, 't Hoen PA. 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.
122. Nowacki M, Vijayan V, Zhou Y, Schotanus K, Doak TG, Landweber LF. 2008. RNA-mediated epigenetic programming of a genome-rearrangement pathway. Nature 451:153-158.
123. Nuez I, Felix MA. 2012. Evolution of susceptibility to ingested doublestranded RNAs in Caenorhabditis nematodes. PloS One 7:e29811.
124. 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.
125. Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M, Demesa-Arévalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada JP. 2010. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628-632.
126. Ostenfeld MS, Jeppesen DK, Laurberg JR, Boysen AT, Bramsen JB, Primdal-Bengtson B, Hendrix A, Lamy P, Dagnaes-Hansen F, Rasmussen MH, Bui KH, Fristrup N, Christensen EI, Nordentoft I, Morth JP, Jensen JB, Pedersen JS, Beck M, Theodorescu D, Borre M, Howard KA, Dyrskjøt L, Ørntoft TF. 2014. Cellular disposal of miR23b by RAB27-dependent exosome release is linked to acquisition of metastatic properties. Cancer Res 74:5758-5771.
127. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, Seabra MC, Darchen F, Amigorena S, Moita LF, Thery C. 2010. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12:19-30.
128. Parker GS, Eckert DM, Bass BL. 2006. RDE-4 preferentially binds long dsRNA and its dimerization is necessary for cleavage of dsRNA to siRNA. RNA 12:807-818.
129. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Gruijl TD, Würdinger T, Middeldorp JM. 2010. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107:6328-6333.
130. Pei J, Millay DP, Olson EN, Grishin NV. 2011. CREST-a large and diverse superfamily of putative transmembrane hydrolases. Biol Direct 6:37.
131. Petruk S, Sedkov Y, Riley KM, Hodgson J, Schweisguth F, Hirose S, Jaynes JB, Brock HW, Mazo A. 2006. Transcription of bxd noncoding RNAs promoted by trithorax represses Ubx in cis by transcriptional interference. Cell 127:1209-1221.
132. Phillips CM, Montgomery TA, Breen PC, Ruvkun G. 2012. MUT-16 promotes formation of perinuclear mutator foci required for RNA silencing in the C. elegans germline. Genes Dev 26:1433-1444.
133. Plasterk RH. 2002. RNA silencing: The genome's immune system. Science 296:1263-1265.
134. Pope SM, Lässer C. 2013. Toxoplasma gondii infection of fibroblasts causes the production of exosome-like vesicles containing a unique array of mRNA and miRNA transcripts compared to serum starvation. J Extracell Vesicles 2:22484.
135. Posadas DM, Carthew RW. 2014. MicroRNAs and their roles in developmental canalization. Curr Opin Genet Dev 27:1-6.
136. Pratt AJ, Rambo RP, Lau PW, MacRae IJ. 2012. Preparation and characterization of the extracellular domain of human Sid-1. PLoS One 7:e33607.
137. Pyott DE, Molnar A. 2015. Going mobile: Non-cell-autonomous small RNAs shape the genetic landscape of plants. Plant Biotechnol J 13:306-318.
138. Rajasethupathy P, Antonov I, Sheridan R, Frey S, Sander C, Tuschl T, Kandel ER. 2012. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell. 149(3): 693-707.
139. Rechavi O, Erlich Y, Amram H, Flomenblit L, Karginov FV, Goldstein I, Hannon GJ, Kloog Y. 2009. Cell contact-dependent acquisition of cellular and viral nonautonomously encoded small RNAs. Genes Dev 23:1971-1979.
140. Rechavi O, Minevich G, Hobert O. 2011. Transgenerational inheritance of an acquired small RNA-based antiviral response in C. elegans. Cell 147:1248-1256.
141. Rechavi O, Houri-Ze'evi L, Anava S, Goh WS, Kerk SY, Hannon GJ, Hobert O. 2014. Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell 158:277-287.
142. Remy JJ. 2010. Stable inheritance of an acquired behavior in Caenorhabditis elegans. Curr Biol 20:R877-878.
143. Ren R, Xu X, Lin T, Weng S, Liang H, Huang M, Dong C, Luo Y, He J. 2011. Cloning, characterization, and biological function analysis of the SidT2 gene from Siniperca chuatsi. Dev Comp Immunol 35:692-701.
144. Robalino J, Bartlett T, Shepard E, Prior S, Jaramillo G, Scura E, Chapman RW, Gross PS, Browdy CL, Warr GW. 2005. Double-stranded RNA induces sequence-specific antiviral silencing in addition to nonspecific immunity in a marine shrimp: convergence of RNA interference and innate immunity in the invertebrate antiviral response? J Virol 79:13561-13571.
145. Roberts TC, Godfrey C, McClorey G, Vader P, Briggs D, Gardiner C, Aoki Y, Sargent I, Morgan JE, Wood MJ. 2013. Extracellular microRNAs are dynamic non-vesicular biomarkers of muscle turnover. Nucleic Acids Res 41:9500-9513.
146. Roignant JY, Carre C, Mugat B, Szymczak D, Lepesant JA, Antoniewski C. 2003. Absence of transitive and systemic pathways allows cell-specific and isoform specific RNAi in Drosophila. RNA 9:299-308.
147. Rouhana L, Weiss JA, Forsthoefel DJ, Lee H, King RS, Inoue T, Shibata N, Agata K, Newmark PA. 2013. RNA interference by feeding in vitro-synthesized double-stranded RNA to planarians: Ethodology and dynamics. Dev Dyn 242:718-730.
148. Sakaguchi A, Sarkies P, Simon M, Doebley AL, Goldstein LD, Hedges A, Ikegami K, Alvares SM, Yang L, LaRocque JR, Hall J, Miska EA, Ahmed S. 2014. Caenorhabditis elegans RSD-2 and RSD-6 promote germ cell immortality by maintaining small interfering RNA populations. Proc Natl Acad Sci USA 111:E4323-4331.
149. Saleh MC, van Rij RP, Hekele A, Gillis A, Foley E, O'Farrell PH, Andino, R. 2006. The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat Cell Biol 8:793-802.
150. Saleh MC, Tassetto M, van Rij RP, Goic B, Gausson V, Berry B, Jacquier C, Antoniewski C, Andino R. 2009. Antiviral immunity in Drosophila requires systemic RNA interference spread. Nature 458:346-350.
151. Sánchez-Alvarado A, Newmark PA. 1999. Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc Natl Acad Sci USA 96:5049-5054.
152. Schott D, Yanai I, Hunter CP. 2014. Natural RNA interference directs a heritable response to the environment. Sci Rep 4:7387.
153. Schott DH, Cureton DK, Whelan SP, Hunter CP. 2005. An antiviral role for the RNA interference machinery in Caenorhabditis elegans. Proc Natl Acad Sci USA 102:18420-18424.
154. Scott JG, Michel K, Bartholomay LC, Siegfried BD, Hunter WB, Smagghe G, Zhu KY, Douglas AE. 2013. Towards the elements of successful insect RNAi. J Insect Physiol 59:1212-1221.
155. Sheth U, Pitt J, Dennis S, Priess JR. 2010. Perinuclear P granules are the principal sites of mRNA export in adult C. elegans germ cells. Development 137:1305-1314.
156. Shih JD, Hunter CP. 2011. SID-1 is a dsRNA-selective dsRNA-gated channel. RNA 17:1057-1065.
157. Shih JD, Fitzgerald MC, Sutherlin M, Hunter CP. 2009. The SID-1 double-stranded RNA transporter is not selective for dsRNA length. RNA 15:384-390.
158. Shreve JT, Shukle RH, Subramanyam S, Johnson AJ, Schemerhorn BJ, Williams CE, Stuart JJ. 2013. A genome-wide survey of small interfering RNA and microRNA pathway genes in a galling insect. J Insect Physiol 59:367-376.
159. Singh PP, Li L, Schorey JS. 2015. Exosomal RNA from mycobacterium tuberculosis-infected cells is functional in recipient macrophages. Traffic 16:555-571.
160. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO. 2008. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10:1470-1476.
161. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, Martienssen RA. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461-472.
162. Smardon A, Spoerke JM, Stacey SC, Klein ME, Mackin N, Maine EM. 2000. EGO-1 is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans. Curr Biol 10:169-178.
163. Sorrentino S. 1998. Human extracellular ribonucleases: multiplicity, molecular diversity and catalytic properties of the major RNase types. Cell Mol Life Sci 54:785-794.
164. Squadrito ML, Baer C, Burdet F, Maderna C, Gilfillan GD, Lyle R, Ibberson M, De Palma M. 2014. Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep 8:1432-1446.
165. Steele EJ. 1981. Somatic Selection and Adaptive Evolution: On the Inheritance of Acquired Characters. Williams-Wallace, 2nd ed. Toronto: University of Chicago Press.
166. Stein P, Svoboda P, Anger M, Schultz RM. 2003. RNAi: Mammalian oocytes do it without RNA-dependent RNA polymerase. RNA 9:187-192.
167. Sterken MG, Snoek LB, Bosman KJ, Daamen J, Riksen JA, Bakker J, Pijlman GP, Kammenga JE. 2014. A heritable antiviral RNAi response limits Orsay virus infection in Caenorhabditis elegans N2. PLoS One 9:e89760.
168. Svoboda P, Stein P, Hayashi H, Schultz RM. 2000. Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development 127:4147-4156.
169. tenOever BR. 2014. Response to Voinnet et al. Cell Rep 9:798-799.
170. Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H, Kanginakudru S, Albrechtsen M, An C, Aymeric JL, Barthel A, Bebas P, Bitra K, Bravo A, Chevalier F, Collinge DP, Crava CM, de Maagd RA, Duvic B, Erlandson M, Faye I, Felföldi G, Fujiwara H, Futahashi R, Gandhe AS, Gatehouse HS, Gatehouse LN, Giebultowicz JM, Gómez I, Grimmelikhuijzen CJ, Groot AT, Hauser F, Heckel DG, Hegedus DD, Hrycaj S, Huang L, Hull JJ, Iatrou K, Iga M, Kanost MR, Kotwica J, Li C, Li J, Liu J, Lundmark M, Matsumoto S, Meyering-Vos M, Millichap PJ, Monteiro A, Mrinal N, Niimi T, Nowara D, Ohnishi A, Oostra V, Ozaki K, Papakonstantinou M, Popadic A, Rajam MV, Saenko S, Simpson RM, Soberón M, Strand MR, Tomita S, Toprak U, Wang P, Wee CW, Whyard S, Zhang W, Nagaraju J, Ffrench-Constant RH, Herrero S, Gordon K, Swevers L, Smagghe G. 2011. RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57:231-245.
171. Tijsterman M, May RC, Simmer F, Okihara KL, Plasterk RH. 2004. Genes required for systemic RNA interference in Caenorhabditis elegans. Curr Biol 14:111-116.
172. Timmons L, Fire A. 1998. Specific interference by ingested dsRNA. Nature 395:854.
173. Timmons L, Tabara H, Mello CC, Fire AZ. 2003. Inducible systemic RNA silencing in Caenorhabditis elegans. Mol Biol Cell 14:2972-2983.
174. Tominaga N, Kosaka N, Ono M, Katsuda T, Yoshioka Y, Tamura K, Lötvall J, Nakagama H, Ochiya T. 2015. Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier. Nat Commun 6:6716.
175. Tomoyasu Y, Miller SC, Tomita S, Schoppmeier M, Grossmann D, Bucher G. 2008. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Gen Biol 9:R10.
176. Tosar JP, Gámbaro F, Sanguinetti J, Bonilla B, Witwer KW, Cayota A. 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.
177. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brügger B, Simons M. 2008. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319:1244-1247.
178. Tsang SY, Moore JC, Huizen RV, Chan CW, Li RA. 2007. Ectopic expression of systemic RNA interference defective protein in embryonic stem cells. Biochem Biophys Res Commun 357:480-486.
179. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. 2011. Characterization of extracellular circulating microRNA. Nucleic Acids Res 39:7223-7233.
180. Ulvila J, Parikka M, Kleino A, Sormunen R, Ezekowitz RA, Kocks C, Ramet M. 2006. Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J Biol Chem 281:14370-14375.
181. Umezu T, Tadokoro H, Azuma K, Yoshizawa S, Ohyashiki K, Ohyashiki JH. 2014. Exosomal miR-135b shed from hypoxic multiple myeloma cells enhances angiogenesis by targeting factor-inhibiting HIF-1. Blood 124:3748-3757.
182. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654-659.
183. Valdes VJ, Athie A, Salinas LS, Navarro RE, Vaca L. 2012. CUP-1 is a novel protein involved in dietary cholesterol uptake in Caenorhabditis elegans. PLoS One 7:e33962.
184. Valiunas V, Polosina YY, Miller H, Potapova IA, Valiuniene L, Doronin S, Mathias RT, Robinson RB, Rosen MR, Cohen IS, Brink PR. 2005. Connexin-specific cell-to-cell transfer of short interfering RNA by gap junctions. J Physiol 568(Pt 2):459-468.
185. Viaud S, Ploix S, Lapierre V, Théry C, Commere PH, Tramalloni D, Gorrichon K, Virault-Rocroy P, Tursz T, Lantz O, Zitvogel L, Chaput N. 2011. Updated technology to produce highly immunogenic dendritic cell-derived exosomes of clinical grade: A critical role of interferon-γ. J Immunother 34:65-75.
186. 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.
187. Villarroya-Beltri C, Gutiérrez-Vázquez C, Sánchez-Cabo F, Pérez-Hernández D, Vázquez J, Martin-Cofreces N, Martinez-Herrera DJ, Pascual-Montano A, Mittelbrunn M, Sánchez-Madrid F. 2013. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4:2980.
188. Vojtech L, Woo S, Hughes S, Levy C, Ballweber L, Sauteraud RP, Strobl J, Westerberg K, Gottardo R, Tewari M, Hladik F. 2014. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res 42:7290-7304.
189. Vyas N, Walvekar A, Tate D, Lakshmanan V, Bansal D, Lo Cicero A, Raposo G, Palakodeti D, Dhawan J. 2014. Vertebrate Hedgehog is secreted on two types of extracellular vesicles with different signaling properties. Sci Rep 4:7357.
190. Wang H, Gong L, Qi J, Hu M, Zhong G, Gong L. 2014. Molecular cloning and characterization of a SID-1-like gene in Plutella xylostella. Arch Insect Biochem Physiol 87:164-176.
191. 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.
192. Whyard S, Singh AD, Wong S. 2009. Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem Mol Biol 39:824-832.
193. Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I, Huang HD, Jin H. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118-123.
194. Weismann A. 1883. On Heredity. In: Poulton EB, Schonland S, Shipley AE, editors. Essays on heredity and kindred biological problems, Vol. 4. Oxford: Clarendon. pp 67-106.
195. Whangbo JS, Hunter CP. 2008. Environmental RNA interference. Trends Genet 24:297-305.
196. Wilkins C, Dishongh R, Moore SC, Whitt MA, Chow M, Machaca K. 2005. RNA interference is an antiviral defence mechanism in Caenorhabditis elegans. Nature 436:1044-1047.
197. Winston WM, Molodowitch C, Hunter CP. 2002. Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295:2456-2459.
198. Winston WM, Sutherlin M, Wright AJ, Feinberg EH, Hunter CP. 2007. Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc Natl Acad Sci USA 104:10565-10570.
199. Witwer KW, Hirschi KD. 2014. Transfer and functional consequences of dietary microRNAs in vertebrates: Concepts in search of corroboration. Bioessays 36:394-406.
200. Witwer KW, Buzás EI, Bemis LT, Bora A, Lässer C, Lötvall J, Nolte-'t Hoen EN, Piper MG, Sivaraman S, Skog J, Théry C, Wauben MH, Hochberg F. 2013. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2:20360.
201. Wolfrum C, Shi S, Jayaprakash KN, Jayaraman M, Wang G, Pandey RK, Rajeev KG, Nakayama T, Charrise K, Ndungo EM, Zimmermann T, Koteliansky V, Manoharan M, Stoffel M. 2007. Mechanisms and optimization of in vivo delivery of lipophilic siRNAs. Nat Biotechnol 25:1149-1157.
202. Xiao D, Gao X, Xu J, Liang X, Li Q, Yao J, Zhu KY. 2015. Clathrin-dependent endocytosis plays a predominant role in cellular uptake of double-stranded RNA in the red flour beetle. Insect Biochem Mol Biol 60:68-77.
203. Xu J, Mon H, Kusakabe T, Li Z, Zhu L, Iiyama K, Masuda A, Mitsudome T, Lee JM. 2013a. Establishment of a soaking RNA interference and Bombyx mori nucleopolyhedrovirus (BmNPV)-hypersensitive cell line using Bme21 cell. Appl Microbiol Biotechnol 97:10435-10444.
204. Xu J, Nagata Y, Mon H, Li Z, Zhu L, Iiyama K, Kusakabe T, Lee JM. 2013b. Soaking RNAi-mediated modification of Sf9 cells for baculovirus expression system by ectopic expression of Caenorhabditis elegans SID-1. Appl Microbiol Biotechnol 97:5921-5931.
205. Xu J, Yoshimura K, Mon H, Li Z, Zhu L, Iiyama K, Kusakabe T, Lee JM. 2014. Establishment of Caenorhabditis elegans SID-1-dependent DNA delivery system in cultured silkworm cells. Mol Biotechnol 56:193-198.
206. Xu HJ, Chen T, Ma XF, Xue J, Pan PL, Zhang XC, Cheng JA, Zhang CX. 2013c. Genome-wide screening for components of small interfering RNA (siRNA) and micro-RNA (miRNA) pathways in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Mol Biol 22:635-647.
207. Yáñez-Mó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, Colás E, Cordeiro-da Silva A, Fais S, Falcon-Perez JM, Ghobrial IM, Giebel B, Gimona M, Graner M, Gursel I, Gursel M, Heegaard NH, Hendrix A, Kierulf P, Kokubun K, Kosanovic M, Kralj-Iglic V, Krämer-Albers EM, Laitinen S, Lässer C, Lener T, Ligeti E, Linē A, Lipps G, Llorente A, Lötvall J, Manček-Keber M, Marcilla A, Mittelbrunn M, Nazarenko I, Nolte-'t Hoen EN, Nyman TA, O'Driscoll L, Olivan M, Oliveira C, Pállinger É, Del Portillo HA, Reventós J, Rigau M, Rohde E, Sammar M, Sánchez-Madrid F, Santarém N, Schallmoser K, Ostenfeld MS, Stoorvogel W, Stukelj R, Van der Grein SG, Vasconcelos MH, Wauben MH, De Wever O. 2015. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 4:27066.
208. Yang H, Vallandingham J, Shiu P, Li H, Hunter CP, Mak HY. 2014. The DEAD box helicase RDE-12 promotes amplification of RNAi in cytoplasmic foci in C. elegans. Curr Biol 24:832-838.
209. Yigit E, Batista PJ, Bei Y, Pang KM, Chen CC, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ, Mello CC. 2006. Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127:747-757.
210. Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, Akhmedov NB, Farber DB. 2009. Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One 4:e4722.
211. Zayas RM, Hernandez A, Habermann B, Wang Y, Stary JM, Newmark PA. 2005. The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: Analysis of ESTs from the hermaphroditic strain. Proc Natl Acad Sci USA 102:18491-18496.
212. Zhang C, Montgomery TA, Fischer SEJ, Garcia SMDA, Riedel CG, Fahlgren N, Sullivan CM, Carrington JC, Ruvkun G. 2012a. The Caenorhabditis elegans RDE-10/RDE-11 complex regulates RNAi by promoting secondary siRNA amplification. Curr Biol 22:881-890.
213. Zhang H, Fire AZ. 2010. Cell autonomous specification of temporal identity by Caenorhabditis elegans microRNA lin-4. Dev Biol 344:603-610.
214. Zhang J, Khan SA, Hasse C, Ruf S, Heckel DG, Bock R. 2015. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science. 347:991-994.
215. 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 C-Y. 2012b. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res 22:107-126.
216. Zhang Y, Wiggins BE, Lawrence C, Petrick J, Ivashuta S, Heck G. 2012c. Analysis of plant-derived miRNAs in animal small RNA datasets. BMC Genomics 13:381.
217. 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. 2010. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39:133-144.
218. Zhuang JJ, Hunter CP. 2012. The Influence of Competition Among C. elegans Small RNA Pathways on Development. Genes (Basel). 3:671-685.
219. Zhuang JJ, Banse SA, Hunter CP. 2013. The nuclear argonaute NRDE-3 contributes to transitive RNAi in Caenorhabditis elegans. Genetics 194:117-131.