Molecular basis for an attenuated cytoplasmic dsRNA response in human embryonic stem cells

Cell Cycle

Volumn 9, Issue 17, 2010, Pages 3552-3564

  Chen, Ling Ling ^a   Yang, Li ^a   Carmichael, Gordon G ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

dsRNA; Innate immunity; Interferon; Pluripotency; Stem cells

Indexed keywords

BETA INTERFERON; DOUBLE STRANDED RNA; OLIGOADENYLATE SYNTHETASE; PROTEIN KINASE R; RETINOIC ACID INDUCIBLE PROTEIN I; RIBONUCLEASE L; SYNTHETASE; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; EMBRYONIC STEM CELL; GENE CONTROL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

IPS; MAMMALIA;

EID: 77956417791     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.17.12792     Document Type: Article

References (87)

1. Wang Q, Carmichael GG. Effects of length and location on the cellular response to double-stranded RNA. Microbiol Mol Biol Rev 2004; 68:432-52. (Pubitemid 39238277)
2. Kumar M, Carmichael GG. Antisense RNA: Function and fate of duplex RNA in cells of higher eukaryotes. Microbiol Mol Biol Rev 1998; 62:1415-34. (Pubitemid 28558304)
3. Baulcombe D. RNA silencing. Trends Biochem Sci 2005; 30:290-3.
4. Filipowicz W. RNAi: The nuts and bolts of the RISC machine. Cell 2005; 122:17-20. (Pubitemid 40977936)
5. Bass BL. RNA editing by adenosine deaminases that act on RNA. Annu Rev Biochem 2002; 71:817-46.
6. Matsumoto M, Funami K, Oshiumi H, Seya T. Toll-like receptor 3: A link between toll-like receptor, interferon and viruses. Microbiol Immunol 2004; 48:147-54. (Pubitemid 38405076)
7. Meylan E, Tschopp J, Karin M. Intracellular pattern recognition receptors in the host response. Nature 2006; 442:39-44. (Pubitemid 44064203)
8. Gantier MP, Williams BR. The response of mammalian cells to double-stranded RNA. Cytokine Growth Factor Rev 2007; 18:363-71.
9. Uematsu S, Akira S. Toll-like receptors and type I interferons. J Biol Chem 2007; 282:15319-24.
10. Vercammen E, Staal J, Beyaert R. Sensing of viral infection and activation of innate immunity by toll-like receptor 3. Clin Microbiol Rev 2008; 21:13-25. (Pubitemid 351160008)
11. Kenny EF, O'Neill LAJ. Signalling adaptors used by Toll-like receptors: An update. Cytokine 2008; 43:342-9.
12. Seya T, Matsumoto M, Ebihara T, Oshiumi H. Functional evolution of the TICAM-1 pathway for extrinsic RNA sensing. Immunol Rev 2009; 227:44-53.
13. Nakhaei P, Genin P, Civas A, Hiscott J. RIG-I-like receptors: Sensing and responding to RNA virus infection. Semin Immunol 2009; 21:215-22.
14. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140:805-20.
15. McAllister CS, Samuel CE. The RNA-activated protein kinase enhances the induction of interferon-beta and apoptosis mediated by cytoplasmic RNA sensors. J Biol Chem 2009; 284:1644-51.
16. McAllister CS, Toth AM, Zhang P, Devaux P, Cattaneo R, Samuel CE. Mechanisms of protein kinase PKR-mediated amplification of beta interferon induction by C protein-deficient measles virus. J Virol 2010; 84:380-6.
17. Lemaire PA, Anderson E, Lary J, Cole JL. Mechanism of PKR Activation by dsRNA. J Mol Biol 2008; 381:351-60.
18. Samuel CE. Mechanism of interferon action: Phosphorylation of protein synthesis initiation factor eIF-2 in interferon-treated human cells by a ribosome-associated kinase processing site specificity similar to hemin-regulated rabbit reticulocyte kinase. Proc Natl Acad Sci USA 1979; 76:600-4.
19. Kumar A, Haque J, Lacoste J, Hiscott J, Williams BR. Double-stranded RNA-dependent protein kinase activates transcription factor NFkappaB by phosphorylating IkappaB. Proc Natl Acad Sci USA 1994; 91:6288-92. (Pubitemid 24200645)
20. Thanos D, Maniatis T. NFkappaB: A lesson in family values. Cell 1995; 80:529-32.
21. Kumar A, Yang YL, Flati V, Der S, Kadereit S, Deb A, et al. Deficient cytokine signaling in mouse embryo fibroblasts with a targeted deletion in the PKR gene: Role of IRF-1 and NFkappaB. EMBO J 1997; 16:406-16. (Pubitemid 27049396)
22. Williams BR. Signal integration via PKR. Sci STKE 2001; 2.
23. Kerr IM, Brown RE. pppA2′p5′A2′p5′A: An inhibitor of protein synthesis synthesized with an enzyme fraction from interferon-treated cells. Proc Natl Acad Sci USA 1978; 75:256-60.
24. Minks MA, West DK, Benvin S, Greene JJ, Ts'o PO, Baglioni C. Activation of 2′,5′-oligo(A) polymerase and protein kinase of interferon-treated HeLa cells by 2′-O-methylated poly (inosinic acid). Poly(cytidylic acid), Correlations with interferon-inducing activity. J Biol Chem 1980; 255:6403-7. (Pubitemid 11229425)
25. Dong B, Silverman RH. 2-5A-dependent RNase molecules dimerize during activation by 2-5A. J Biol Chem 1995; 270:4133-7.
26. Li XL, Blackford JA, Hassel BA. RNase L mediates the antiviral effect of interferon through a selective reduction in viral RNA during encephalomyocarditis virus infection. J Virol 1998; 72:2752-9.
27. Iordanov MS, Paranjape JM, Zhou A, Wong J, Williams BR, Meurs EF, et al. Activation of p38 mitogen-activated protein kinase and c-Jun NH(2)-terminal kinase by double-stranded RNA and encephalomyocarditis virus: involvement of RNase L, protein kinase R and alternative pathways. Mol Cell Biol 2000; 20:617-27.
28. Matsumoto M, Funami K, Tanabe M, Oshiumi H, Shingai M, Seto Y, et al. Subcellular localization of Toll-like receptor 3 in human dendritic cells. J Immunol 2003; 171:3154-62. (Pubitemid 37093540)
29. Itoh K, Watanabe A, Funami K, Seya T, Matsumoto M. The clathrin-mediated endocytic pathway participates in dsRNA-induced IFNbeta production. J Immunol 2008; 181:5522-9.
30. Matsumoto M, Kikkawa S, Kohase M, Miyake K, Seya T. Establishment of a monoclonal antibody against human Toll-like receptor 3 that blocks double-stranded RNA-mediated signaling. Biochem Biophys Res Commun 2002; 293:1364-9. (Pubitemid 34681026)
31. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 2003; 4:161-7. (Pubitemid 36193018)
32. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, et al. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 2003; 4:491-6. (Pubitemid 36592443)
33. Jiang Z, Mak TW, Sen G, Li X. Toll-like receptor 3-mediated activation of NFkappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFNbeta. Proc Natl Acad Sci USA 2004; 101:3533-8. (Pubitemid 38338230)
34. Meylan E, Burns K, Hofmann K, Blanchetau V, Martinon F, Kelliher M, et al. RIP1 is an essential meidator of Toll-like receptor 3-induced NFkappaB activation. Nat Immunol 2004; 5:503-7. (Pubitemid 38660462)
35. Matsumoto M, Seya T. TLR3: Interferon induction by double-stranded RNA including poly(I:C). Adv Drug Deliv Rev 2008; 60:805-12.
36. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, et al. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003; 301:640-3.
37. Takada E, Okahira S, Sasai M, Funami K, Seya T, Matsumoto M. C-terminal LRRs of human Toll-like receptor 3 control receptor dimerization and signal transmission. Mol Immunol 2007; 44:3633-40. (Pubitemid 46817673)
38. Leonard JN, Ghirlando R, Askins J, Bell JK, Margulies DH, Davies DR, et al. The TLR3 signaling complex forms by cooperative receptor dimerization. Proc Natl Acad Sci USA 2008; 105:258-63.
39. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5:730-7. (Pubitemid 39023305)
40. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 2006; 314:997-1001. (Pubitemid 44749946)
41. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, et al. 5′-Triphosphate RNA is the ligand for RIG-I. Science 2006; 314:994-7.
42. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, Matsushita K, et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 2008; 205:1601-10. (Pubitemid 351962024)
43. Baum A, Garcia-Sastre A. Induction of type I interferon by RNA viruses: Cellular receptors and their substrates. Amino Acids 2009.
44. Zhong B, Yang Y, Li S, Wang YY, Li Y, Diao F, et al. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 2008; 29:538-50.
45. Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008; 455:674-8.
46. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, et al. IPS-1, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat Immunol 2005; 6:981-8. (Pubitemid 41486182)
47. Seth RB, Sun L, Ea CK, Chen ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NFkappaB and IRF 3. Cell 2005; 122:669-82. (Pubitemid 41242633)
48. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005; 437:1167-72. (Pubitemid 41509355)
49. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB. VISA is an adapter protein required for virus-triggered IFNbeta signaling. Mol Cell 2005; 19:727-40. (Pubitemid 41316668)
50. Kumar H, Kawai T, Kato H, Sato S, Takahashi K, Coban C, et al. Essential role of IPS-1 in innate immune responses against RNA viruses. J Exp Med 2006; 203:1795-803. (Pubitemid 44036284)
51. Sun Q, Sun L, Liu HH, Chen X, Seth RB, Forman J, et al. The specific and essential role of MAVS in antiviral innate immune responses. Immunity 2006; 24:633-42. (Pubitemid 43728147)
52. Okabe Y, Sano T, Nagata S. Regulation of the innate immune response by threonine-phosphatase of Eyes absent. Nature 2009; 460:520-4.
53. Johnsen IB, Nguyen TT, Ringdal M, Tryggestad AM, Bakke O, Lien E, et al. Toll-like receptor 3 associates with c-Src tyrosine kinase on endosomes to initiate antiviral signaling. EMBO J 2006; 25:3335-46. (Pubitemid 44141791)
54. Funami K, Sasai M, Ohba Y, Oshiumi H, Seya T, Matsumoto M. Spatiotemporal mobilization of Toll/IL-1 receptor domain-containing adaptor molecule-1 in response to dsRNA. J Immunol 2007; 179:6867-72.
55. Chen LL, Carmichael GG. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: Functional role of a nuclear noncoding RNA. Mol Cell 2009; 35:467-78.
56. Schlee M, Hartmann E, Coch C, Wimmenauer V, Janke M, Barchet W, et al. Approaching the RNA ligand for RIG-I? Immunol Rev 2009; 227:66-74.
57. Wianny F, Zernicka-Goetz M. Specific interference with gene function by double-stranded RNA in early mouse development. Nat Cell Biol 2000; 2:70-5.
58. Svoboda P, Stein P, Hayashi H, Schultz RM. Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development 2000; 127:4147-56.
59. Svoboda P, Stein P, Schultz RM. RNAi in mouse oocytes and preimplantation embryos: effectiveness of hairpin dsRNA. Biochem Biophys Res Commun 2001; 287:1099-104. (Pubitemid 32980565)
60. Billy E, Brondani V, Zhang H, Muller U, Filipowicz W. Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. Proc Natl Acad Sci USA 2001; 98:14428-33. (Pubitemid 33121408)
61. Yang S, Tutton S, Pierce E, Yoon K. Specific double-stranded RNA interference in undifferentiated mouse embryonic stem cells. Mol Cell Biol 2001; 21:7807-16. (Pubitemid 32988789)
62. Thomis DC, Samuel CE. Mechanism of interferon action: characterization of the intermolecular autophosphorylation of PKR, the interferon-inducible, RNA-dependent protein kinase. J Virol 1995; 69:5195-8.
63. Zhang F, Romano PR, Nagamura-Inoue T, Tian B, Dever TE, Mathews MB, et al. Binding of double-stranded RNA to protein kinase PKR is required for dimerization and promotes critical autophosphorylation events in the activation loop. J Biol Chem 2001; 276:24946-58.
64. Xu RH, Chen X, Li DS, Li R, Addicks GC, Glennon C, et al. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 2002; 20:1261-4. (Pubitemid 35462493)
65. Xu RH, Peck RM, Li DS, Feng X, Ludwig T, Thomson JA. Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods 2005; 2:185-90. (Pubitemid 41122125)
66. Zeng H, Park JW, Guo M, Lin G, Crandall L, Compton T, et al. Lack of ABCG2 expression and side population properties in human pluripotent stem cells. Stem Cells 2009; 27:2435-45.
67. Bonin M, Oberstrass J, Lukacs N, Ewert K, Oesterschulze E, Kassing R, et al. Determination of preferential binding sites for anti-dsRNA antibodies on double-stranded RNA by scanning force microscopy. RNA 2000; 6:563-70. (Pubitemid 30212234)
68. Balagopal V, Parker R. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr Opin Cell Biol 2009; 21:403-8.
69. Anderson P, Kedersha N. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 2009; 10:430-6.
70. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441:101-5.
71. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, Flavell RA, et al. Essential role of mda-5 in type I IFN responses to polyriboinosinic: polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci USA 2006; 103:8459-64. (Pubitemid 43838477)
72. Zhang Z, Carmichael GG. The fate of dsRNA in the nucleus. A p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell 2001; 106:465-75.
73. Aravin AA, Hannon GJ, Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 2007; 318:761-4. (Pubitemid 351411762)
74. Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R. Mouse ES cells express endogenous shRNAs, siRNAs and other Microprocessor-independent, Dicerdependent small RNAs. Genes Dev 2008; 22:2773-85.
75. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008; 453:539-43. (Pubitemid 351733315)
76. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, et al. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008; 453:534-8. (Pubitemid 351733314)
77. Qi J, Yu JY, Shcherbata HR, Mathieu J, Wang AJ, Seal S, et al. microRNAs regulate human embryonic stem cell division. Cell Cycle 2009; 8:3729-41.
78. Shalgi R, Brosh R, Oren M, Pilpel Y, Rotter V. Coupling transcriptional and post-transcriptional miRNA regulation in the control of cell fate. Aging 2009; 1:762-70.
79. Barroso-del Jesus A, Lucena-Aguilar G, Menendez P. The miR-302-367 cluster as a potential stemness regulator in ESCs. Cell Cycle 2009; 8:394-8.
80. Burke DC, Graham CF, Lehman JM. Appearance of interferon inducibility and sensitivity during differentiation of murine teratocarcinoma cells in vitro. Cell 1978; 13:243-8.
81. Barlow DP, Randle BJ, Burke DC. Interferon synthesis in the early post-implantation mouse embryo. Differentiation 1984; 27:229-35.
82. Francis MK, Lehman JM. Control of beta-interferon expression in murine embryonal carcinoma F9 cells. Mol Cell Biol 1989; 9:3553-6.
83. Harada H, Willison K, Sakakibara J, Miyamoto M, Fujita T, Taniguchi T. Absence of the type I IFN system in EC cells: transcriptional activator (IRF-1) and repressor (IRF-2) genes are developmentally regulated. Cell 1990; 63:303-12.
84. Krause D, Silverman RH, Jacobsen H, Leisy SA, Dieffenbach CW, Friedman RM. Regulation of ppp(A2'p)nA-dependent RNase levels during interferon treatment and cell differentiation. Eur J Biochem 1985; 146:611-8.
85. Kalvakolanu DV, Sen GC. Differentiation-dependent activation of interferon-stimulated gene factors and transcription factor NFkappaB in mouse embryonal carcinoma cells. Proc Natl Acad Sci USA 1993; 90:3167-71.
86. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-72. (Pubitemid 350138099)
87. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10:25.