A Circular RNA Protects Dormant Hematopoietic Stem Cells from DNA Sensor cGAS-Mediated Exhaustion

Immunity

Volumn 48, Issue 4, 2018, Pages 688-701.e7

  Xia, Pengyan ^a   Wang, Shuo ^a   Ye, Buqing ^a   Du, Ying ^a   Li, Chong ^a   Xiong, Zhen ^a,b   Qu, Yuan ^a,b   Fan, Zusen ^a,b  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

cGAS; circular RNA; DNA recognition; HSC; self DNA; type I interferons

Indexed keywords

ALPHA INTERFERON RECEPTOR; BETA INTERFERON RECEPTOR; CD11B ANTIGEN; CIRCULAR RNA; CYCLIC GMP ADENOSINE PHOSPHATE SYNTHASE; GLYCOPROTEIN P 15095; INTERFERON; MESSENGER RNA; RECEPTOR TYPE TYROSINE PROTEIN PHOSPHATASE C; SYNTHETASE; UNCLASSIFIED DRUG; UNTRANSLATED RNA; MB21D1 PROTEIN, MOUSE; NUCLEOTIDYLTRANSFERASE; RNA; RNA, CIRCULAR; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BONE MARROW; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL SELF-RENEWAL; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE; CONFORMATION; CYTOLOGY; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE;

ANIMALS; BONE MARROW; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE; HEK293 CELLS; HEMATOPOIETIC STEM CELLS; HUMANS; INTERFERON TYPE I; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEIC ACID CONFORMATION; NUCLEOTIDYLTRANSFERASES; RNA; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 85044666197     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2018.03.016     Document Type: Article

References (53)

1. Ablasser, A., Goldeck, M., Cavlar, T., Deimling, T., Witte, G., Röhl, I., Hopfner, K.P., Ludwig, J., Hornung, V., cGAS produces a 2′-5′-linked cyclic dinucleotide second messenger that activates STING. Nature 498 (2013), 380–384.
2. Bruns, I., Lucas, D., Pinho, S., Ahmed, J., Lambert, M.P., Kunisaki, Y., Scheiermann, C., Schiff, L., Poncz, M., Bergman, A., Frenette, P.S., Megakaryocytes regulate hematopoietic stem cell quiescence through CXCL4 secretion. Nat. Med. 20 (2014), 1315–1320.
3. Chen, L.L., The biogenesis and emerging roles of circular RNAs. Nat. Rev. Mol. Cell Biol. 17 (2016), 205–211.
4. Chen, Q., Sun, L., Chen, Z.J., Regulation and function of the cGAS-STING pathway of cytosolic DNA sensing. Nat. Immunol. 17 (2016), 1142–1149.
5. Chuikov, S., Levi, B.P., Smith, M.L., Morrison, S.J., Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress. Nat. Cell Biol. 12 (2010), 999–1006.
6. Civril, F., Deimling, T., de Oliveira Mann, C.C., Ablasser, A., Moldt, M., Witte, G., Hornung, V., Hopfner, K.P., Structural mechanism of cytosolic DNA sensing by cGAS. Nature 498 (2013), 332–337.
7. Conn, S.J., Pillman, K.A., Toubia, J., Conn, V.M., Salmanidis, M., Phillips, C.A., Roslan, S., Schreiber, A.W., Gregory, P.A., Goodall, G.J., The RNA binding protein quaking regulates formation of circRNAs. Cell 160 (2015), 1125–1134.
8. Crow, Y.J., Hayward, B.E., Parmar, R., Robins, P., Leitch, A., Ali, M., Black, D.N., van Bokhoven, H., Brunner, H.G., Hamel, B.C., et al. Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 cause Aicardi-Goutières syndrome at the AGS1 locus. Nat. Genet. 38 (2006), 917–920.
9. Essers, M.A., Offner, S., Blanco-Bose, W.E., Waibler, Z., Kalinke, U., Duchosal, M.A., Trumpp, A., IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458 (2009), 904–908.
10. Gall, A., Treuting, P., Elkon, K.B., Loo, Y.M., Gale, M. Jr., Barber, G.N., Stetson, D.B., Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease. Immunity 36 (2012), 120–131.
11. Gao, D., Wu, J., Wu, Y.T., Du, F., Aroh, C., Yan, N., Sun, L., Chen, Z.J., Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341 (2013), 903–906.
12. Gao, P., Ascano, M., Wu, Y., Barchet, W., Gaffney, B.L., Zillinger, T., Serganov, A.A., Liu, Y., Jones, R.A., Hartmann, G., et al. Cyclic [G(2′,5′)pA(3′,5′)p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase. Cell 153 (2013), 1094–1107.
13. Gao, D., Li, T., Li, X.D., Chen, X., Li, Q.Z., Wight-Carter, M., Chen, Z.J., Activation of cyclic GMP-AMP synthase by self-DNA causes autoimmune diseases. Proc. Natl. Acad. Sci. USA 112 (2015), E5699–E5705.
14. Gruber, A.R., Lorenz, R., Bernhart, S.H., Neuböck, R., Hofacker, I.L., The Vienna RNA websuite. Nucleic Acids Res., 36, 2008 W70-4.
15. Guarnerio, J., Bezzi, M., Jeong, J.C., Paffenholz, S.V., Berry, K., Naldini, M.M., Lo-Coco, F., Tay, Y., Beck, A.H., Pandolfi, P.P., Oncogenic role of fusion-circRNAs derived from cancer-associated chromosomal translocations. Cell 165 (2016), 289–302.
16. Hansen, T.B., Jensen, T.I., Clausen, B.H., Bramsen, J.B., Finsen, B., Damgaard, C.K., Kjems, J., Natural RNA circles function as efficient microRNA sponges. Nature 495 (2013), 384–388.
17. Hock, H., Hamblen, M.J., Rooke, H.M., Schindler, J.W., Saleque, S., Fujiwara, Y., Orkin, S.H., Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature 431 (2004), 1002–1007.
18. Hornung, V., Hartmann, R., Ablasser, A., Hopfner, K.P., OAS proteins and cGAS: unifying concepts in sensing and responding to cytosolic nucleic acids. Nat. Rev. Immunol. 14 (2014), 521–528.
19. Hu, M.M., Yang, Q., Xie, X.Q., Liao, C.Y., Lin, H., Liu, T.T., Yin, L., Shu, H.B., Sumoylation promotes the stability of the DNA sensor cGAS and the adaptor STING to regulate the kinetics of response to DNA virus. Immunity 45 (2016), 555–569.
20. Ivanova, N.B., Dimos, J.T., Schaniel, C., Hackney, J.A., Moore, K.A., Lemischka, I.R., A stem cell molecular signature. Science 298 (2002), 601–604.
21. Li, X., Shu, C., Yi, G., Chaton, C.T., Shelton, C.L., Diao, J., Zuo, X., Kao, C.C., Herr, A.B., Li, P., Cyclic GMP-AMP synthase is activated by double-stranded DNA-induced oligomerization. Immunity 39 (2013), 1019–1031.
22. Li, X.D., Wu, J., Gao, D., Wang, H., Sun, L., Chen, Z.J., Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341 (2013), 1390–1394.
23. Li, Z., Huang, C., Bao, C., Chen, L., Lin, M., Wang, X., Zhong, G., Yu, B., Hu, W., Dai, L., et al. Exon-intron circular RNAs regulate transcription in the nucleus. Nat. Struct. Mol. Biol. 22 (2015), 256–264.
24. Mankan, A.K., Schmidt, T., Chauhan, D., Goldeck, M., Höning, K., Gaidt, M., Kubarenko, A.V., Andreeva, L., Hopfner, K.P., Hornung, V., Cytosolic RNA:DNA hybrids activate the cGAS-STING axis. EMBO J. 33 (2014), 2937–2946.
25. Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S.D., Gregersen, L.H., Munschauer, M., et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495 (2013), 333–338.
26. Petkovic, S., Müller, S., RNA circularization strategies in vivo and in vitro. Nucleic Acids Res. 43 (2015), 2454–2465.
27. Pronk, C.J., Veiby, O.P., Bryder, D., Jacobsen, S.E., Tumor necrosis factor restricts hematopoietic stem cell activity in mice: involvement of two distinct receptors. J. Exp. Med. 208 (2011), 1563–1570.
28. Riddell, J., Gazit, R., Garrison, B.S., Guo, G., Saadatpour, A., Mandal, P.K., Ebina, W., Volchkov, P., Yuan, G.C., Orkin, S.H., Rossi, D.J., Reprogramming committed murine blood cells to induced hematopoietic stem cells with defined factors. Cell 157 (2014), 549–564.
29. Rongvaux, A., Jackson, R., Harman, C.C., Li, T., West, A.P., de Zoete, M.R., Wu, Y., Yordy, B., Lakhani, S.A., Kuan, C.Y., et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell 159 (2014), 1563–1577.
30. Rossi, L., Lin, K.K., Boles, N.C., Yang, L., King, K.Y., Jeong, M., Mayle, A., Goodell, M.A., Less is more: unveiling the functional core of hematopoietic stem cells through knockout mice. Cell Stem Cell 11 (2012), 302–317.
31. Salzman, J., Chen, R.E., Olsen, M.N., Wang, P.L., Brown, P.O., Cell-type specific features of circular RNA expression. PLoS Genet., 9, 2013, e1003777.
32. Sato, T., Onai, N., Yoshihara, H., Arai, F., Suda, T., Ohteki, T., Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat. Med. 15 (2009), 696–700.
33. Schoggins, J.W., MacDuff, D.A., Imanaka, N., Gainey, M.D., Shrestha, B., Eitson, J.L., Mar, K.B., Richardson, R.B., Ratushny, A.V., Litvak, V., et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505 (2014), 691–695.
34. Seo, G.J., Yang, A., Tan, B., Kim, S., Liang, Q., Choi, Y., Yuan, W., Feng, P., Park, H.S., Jung, J.U., Akt kinase-mediated checkpoint of cGAS DNA sensing pathway. Cell Rep. 13 (2015), 440–449.
35. Sun, L., Wu, J., Du, F., Chen, X., Chen, Z.J., Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339 (2013), 786–791.
36. Vicens, Q., Westhof, E., Biogenesis of circular RNAs. Cell 159 (2014), 13–14.
37. Wang, S., Xia, P., Ye, B., Huang, G., Liu, J., Fan, Z., Transient activation of autophagy via Sox2-mediated suppression of mTOR is an important early step in reprogramming to pluripotency. Cell Stem Cell 13 (2013), 617–625.
38. Wassermann, R., Gulen, M.F., Sala, C., Perin, S.G., Lou, Y., Rybniker, J., Schmid-Burgk, J.L., Schmidt, T., Hornung, V., Cole, S.T., Ablasser, A., Mycobacterium tuberculosis differentially activates cGAS- and inflammasome-dependent intracellular immune responses through ESX-1. Cell Host Microbe 17 (2015), 799–810.
39. White, M.J., McArthur, K., Metcalf, D., Lane, R.M., Cambier, J.C., Herold, M.J., van Delft, M.F., Bedoui, S., Lessene, G., Ritchie, M.E., et al. Apoptotic caspases suppress mtDNA-induced STING-mediated type I IFN production. Cell 159 (2014), 1549–1562.
40. Wilson, A., Murphy, M.J., Oskarsson, T., Kaloulis, K., Bettess, M.D., Oser, G.M., Pasche, A.C., Knabenhans, C., Macdonald, H.R., Trumpp, A., c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 18 (2004), 2747–2763.
41. Wilson, A., Laurenti, E., Oser, G., van der Wath, R.C., Blanco-Bose, W., Jaworski, M., Offner, S., Dunant, C.F., Eshkind, L., Bockamp, E., et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135 (2008), 1118–1129.
42. Wu, J., Sun, L., Chen, X., Du, F., Shi, H., Chen, C., Chen, Z.J., Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339 (2013), 826–830.
43. Xia, P., Wang, S., Huang, G., Du, Y., Zhu, P., Li, M., Fan, Z., RNF2 is recruited by WASH to ubiquitinate AMBRA1 leading to downregulation of autophagy. Cell Res. 24 (2014), 943–958.
44. Xia, P., Wang, S., Huang, G., Zhu, P., Li, M., Ye, B., Du, Y., Fan, Z., WASH is required for the differentiation commitment of hematopoietic stem cells in a c-Myc-dependent manner. J. Exp. Med. 211 (2014), 2119–2134.
45. Xia, P., Wang, S., Ye, B., Du, Y., Huang, G., Zhu, P., Fan, Z., Sox2 functions as a sequence-specific DNA sensor in neutrophils to initiate innate immunity against microbial infection. Nat. Immunol. 16 (2015), 366–375.
46. Xia, P., Wang, S., Gao, P., Gao, G., Fan, Z., DNA sensor cGAS-mediated immune recognition. Protein Cell 7 (2016), 777–791.
47. Xia, P., Ye, B., Wang, S., Zhu, X., Du, Y., Xiong, Z., Tian, Y., Fan, Z., Glutamylation of the DNA sensor cGAS regulates its binding and synthase activity in antiviral immunity. Nat. Immunol. 17 (2016), 369–378.
48. Yang, Y.G., Lindahl, T., Barnes, D.E., Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease. Cell 131 (2007), 873–886.
49. Yoh, S.M., Schneider, M., Seifried, J., Soonthornvacharin, S., Akleh, R.E., Olivieri, K.C., De Jesus, P.D., Ruan, C., de Castro, E., Ruiz, P.A., et al. PQBP1 is a proximal sensor of the cGAS-dependent innate response to HIV-1. Cell 161 (2015), 1293–1305.
50. Zhang, J., Grindley, J.C., Yin, T., Jayasinghe, S., He, X.C., Ross, J.T., Haug, J.S., Rupp, D., Porter-Westpfahl, K.S., Wiedemann, L.M., et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441 (2006), 518–522.
51. Zhang, Y., Zhang, X.O., Chen, T., Xiang, J.F., Yin, Q.F., Xing, Y.H., Zhu, S., Yang, L., Chen, L.L., Circular intronic long noncoding RNAs. Mol. Cell 51 (2013), 792–806.
52. Zhang, X.O., Wang, H.B., Zhang, Y., Lu, X., Chen, L.L., Yang, L., Complementary sequence-mediated exon circularization. Cell 159 (2014), 134–147.
53. Zhou, F., Li, X., Wang, W., Zhu, P., Zhou, J., He, W., Ding, M., Xiong, F., Zheng, X., Li, Z., et al. Tracing haematopoietic stem cell formation at single-cell resolution. Nature 533 (2016), 487–492.