An RNA-Based Fluorescent Biosensor for High-Throughput Analysis of the cGAS-cGAMP-STING Pathway

Cell Chemical Biology

Volumn 23, Issue 12, 2016, Pages 1539-1549

  Bose, Debojit ^a   Su, Yichi ^a   Marcus, Assaf ^a   Raulet, David H ^a   Hammond, Ming C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cGAMP; cGAS; cyclic AMP GMP; cyclic dinucleotide; cyclic GMP AMP; GEMM II; high throughput screen; riboswitch; Spinach aptamer; STING

Indexed keywords

CYCLIC AMP; CYCLIC GMP; RNA;

ARTICLE; AUTOIMMUNE DISEASE; BACILLUS HALODURANS; BIOSENSOR; CANCER IMMUNOTHERAPY; CELL LYSATE; CLOSTRIDIUM ACETOBUTYLICUM; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYMATIC ASSAY; ENZYME ACTIVITY; GENE; HIGH THROUGHPUT SCREENING; L929 CELL LINE; MAMMAL CELL; MICROORGANISM DETECTION; NEOPLASM; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RIBOSWITCH; RNA BASED FLUORESCENT BIOSENSOR; SIGNAL TRANSDUCTION; STIMULATOR OF INTERFERON GENE;

EID: 85006952437     PISSN: 24519456     EISSN: 24519448     Source Type: Journal    
DOI: 10.1016/j.chembiol.2016.10.014     Document Type: Article

References (60)

1. Ablasser, A., Goldeck, M., Cavlar, T., Deimling, T., Witte, G., Rohl, 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. Ahn, J., Gutman, D., Saijo, S., Barber, G.N., STING manifests self DNA-dependent inflammatory disease. Proc. Natl. Acad. Sci. USA 109 (2012), 19386–19391.
3. Ahn, J., Ruiz, P., Barber, G.N., Intrinsic self-DNA triggers inflammatory disease dependent on STING. J. Immunol. 193 (2014), 4634–4642.
4. Ahn, J., Konno, H., Barber, G.N., Diverse roles of STING-dependent signaling on the development of cancer. Oncogene 34 (2015), 5302–5308.
5. An, J., Woodward, J.J., Sasaki, T., Minie, M., Elkon, K.B., Cutting edge: antimalarial drugs inhibit IFN-beta production through blockade of cyclic GMP-AMP synthase-DNA interaction. J. Immunol. 194 (2015), 4089–4093.
6. Baird, J.R., Friedman, D., Cottam, B., Dubensky, T.W. Jr., Kanne, D.B., Bambina, S., Bahjat, K., Crittenden, M.R., Gough, M.J., Radiotherapy combined with novel STING-targeting oligonucleotides results in regression of established tumors. Cancer Res. 76 (2016), 50–61.
7. Barker, J.R., Koestler, B.J., Carpenter, V.K., Burdette, D.L., Waters, C.M., Vance, R.E., Valdivia, R.H., STING-dependent recognition of cyclic di-AMP mediates type I interferon responses during Chlamydia trachomatis infection. MBio, 4, 2013 e00018-13.
8. Boer, D.R., Canals, A., Coll, M., DNA-binding drugs caught in action: the latest 3D pictures of drug-DNA complexes. Dalton Trans., 2009, 399–414.
9. Burdette, D.L., Monroe, K.M., Sotelo-Troha, K., Iwig, J.S., Eckert, B., Hyodo, M., Hayakawa, Y., Vance, R.E., STING is a direct innate immune sensor of cyclic di-GMP. Nature 478 (2011), 515–518.
10. Burhenne, H., Kaever, V., Quantification of cyclic dinucleotides by reversed-phase LC-MS/MS. Methods Mol. Biol. 1016 (2013), 27–37.
11. Chandra, D., Quispe-Tintaya, W., Jahangir, A., Asafu-Adjei, D., Ramos, I., Sintim, H.O., Zhou, J., Hayakawa, Y., Karaolis, D.K., Gravekamp, C., STING ligand c-di-GMP improves cancer vaccination against metastatic breast cancer. Cancer Immunol. Res. 2 (2014), 901–910.
12. Corrales, L., Gajewski, T.F., Molecular pathways: targeting the stimulator of interferon genes (STING) in the immunotherapy of cancer. Clin. Cancer Res. 21 (2015), 4774–4779.
13. Corrales, L., Glickman, L.H., McWhirter, S.M., Kanne, D.B., Sivick, K.E., Katibah, G.E., Woo, S.R., Lemmens, E., Banda, T., Leong, J.J., et al. Direct activation of STING in the tumor microenvironment leads to potent and systemic tumor regression and immunity. Cell Rep. 11 (2015), 1018–1030.
14. Curran, E., Corrales, L., Kline, J., Targeting the innate immune system as immunotherapy for acute myeloid leukemia. Front. Oncol., 5, 2015, 83.
15. Demaria, O., De Gassart, A., Coso, S., Gestermann, N., Di Domizio, J., Flatz, L., Gaide, O., Michielin, O., Hwu, P., Petrova, T.V., et al. STING activation of tumor endothelial cells initiates spontaneous and therapeutic antitumor immunity. Proc. Natl. Acad. Sci. USA 112 (2015), 15408–15413.
16. Deng, L., Liang, H., Xu, M., Yang, X., Burnette, B., Arina, A., Li, X.D., Mauceri, H., Beckett, M., Darga, T., et al. STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity 41 (2014), 843–852.
17. Diner, E.J., Burdette, D.L., Wilson, S.C., Monroe, K.M., Kellenberger, C.A., Hyodo, M., Hayakawa, Y., Hammond, M.C., Vance, R.E., The innate immune DNA sensor cGAS produces a noncanonical cyclic dinucleotide that activates human STING. Cell Rep. 3 (2013), 1355–1361.
18. Downey, C.M., Aghaei, M., Schwendener, R.A., Jirik, F.R., DMXAA causes tumor site-specific vascular disruption in murine non-small cell lung cancer, and like the endogenous non-canonical cyclic dinucleotide STING agonist, 2′3′-cGAMP, induces M2 macrophage repolarization. PLoS One, 9, 2014, e99988.
19. 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.
20. 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.
21. 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.
22. Hansen, K., Prabakaran, T., Laustsen, A., Jorgensen, S.E., Rahbaek, S.H., Jensen, S.B., Nielsen, R., Leber, J.H., Decker, T., Horan, K.A., et al. Listeria monocytogenes induces IFNbeta expression through an IFI16-, cGAS- and STING-dependent pathway. EMBO J. 33 (2014), 1654–1666.
23. Herzner, A.M., Hagmann, C.A., Goldeck, M., Wolter, S., Kubler, K., Wittmann, S., Gramberg, T., Andreeva, L., Hopfner, K.P., Mertens, C., et al. Sequence-specific activation of the DNA sensor cGAS by Y-form DNA structures as found in primary HIV-1 cDNA. Nat. Immunol. 16 (2015), 1025–1033.
24. Hossain, M., Giri, P., Kumar, G.S., DNA intercalation by quinacrine and methylene blue: a comparative binding and thermodynamic characterization study. DNA Cell Biol 27 (2008), 81–90.
25. Ishikawa, H., Barber, G.N., STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455 (2008), 674–678.
26. Kellenberger, C.A., Hammond, M.C., In vitro analysis of riboswitch-Spinach aptamer fusions as metabolite-sensing fluorescent biosensors. Methods Enzymol. 550 (2015), 147–172.
27. Kellenberger, C.A., Wilson, S.C., Sales-Lee, J., Hammond, M.C., RNA-based fluorescent biosensors for live cell imaging of second messengers cyclic di-GMP and cyclic AMP-GMP. J. Am. Chem. Soc. 135 (2013), 4906–4909.
28. Kellenberger, C.A., Wilson, S.C., Hickey, S.F., Gonzalez, T.L., Su, Y., Hallberg, Z.F., Brewer, T.F., Iavarone, A.T., Carlson, H.K., Hsieh, Y.F., et al. GEMM-I riboswitches from Geobacter sense the bacterial second messenger cyclic AMP-GMP. Proc. Natl. Acad. Sci. USA 112 (2015), 5383–5388.
29. Kobayashi, H., Kobayashi, C.I., Nakamura-Ishizu, A., Karigane, D., Haeno, H., Yamamoto, K.N., Sato, T., Ohteki, T., Hayakawa, Y., Barber, G.N., et al. Bacterial c-di-GMP affects hematopoietic stem/progenitors and their niches through STING. Cell Rep. 11 (2015), 71–84.
30. Kranzusch, P.J., Lee, A.S., Berger, J.M., Doudna, J.A., Structure of human cGAS reveals a conserved family of second-messenger enzymes in innate immunity. Cell Rep. 3 (2013), 1362–1368.
31. Lee, E.R., Baker, J.L., Weinberg, Z., Sudarsan, N., Breaker, R.R., An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329 (2010), 845–848.
32. LePecq, J.B., Paoletti, C., A fluorescent complex between ethidium bromide and nucleic acids. Physical-chemical characterization. J. Mol. Biol. 27 (1967), 87–106.
33. 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.
34. Li, T., Cheng, H., Yuan, H., Xu, Q., Shu, C., Zhang, Y., Xu, P., Tan, J., Rui, Y., Li, P., et al. Antitumor activity of cGAMP via stimulation of cGAS-cGAMP-STING-IRF3 mediated innate immune response. Sci. Rep., 6, 2016, 19049.
35. Ma, Z., Damania, B., The cGAS-STING defense pathway and its counteraction by viruses. Cell Host Microbe 19 (2016), 150–158.
36. Nakamura, T., Miyabe, H., Hyodo, M., Sato, Y., Hayakawa, Y., Harashima, H., Liposomes loaded with a STING pathway ligand, cyclic di-GMP, enhance cancer immunotherapy against metastatic melanoma. J. Control. Release 216 (2015), 149–157.
37. Paijo, J., Doring, M., Spanier, J., Grabski, E., Nooruzzaman, M., Schmidt, T., Witte, G., Messerle, M., Hornung, V., Kaever, V., et al. cGAS senses human cytomegalovirus and induces type I interferon responses in human monocyte-derived cells. PLoS Pathog., 12, 2016, e1005546.
38. Ren, A., Wang, X.C., Kellenberger, C.A., Rajashankar, K.R., Jones, R.A., Hammond, M.C., Patel, D.J., Structural basis for molecular discrimination by a 3′,3′-cGAMP sensing riboswitch. Cell Rep. 11 (2015), 1–12.
39. Shanahan, C.A., Gaffney, B.L., Jones, R.A., Strobel, S.A., Differential analogue binding by two classes of c-di-GMP riboswitches. J. Am. Chem. Soc. 133 (2011), 15578–15592.
40. Shrivastav, M., Niewold, T.B., Nucleic acid sensors and type I interferon production in systemic lupus erythematosus. Front. Immunol., 4, 2013, 319.
41. Sinha, R., Hossain, M., Kumar, G.S., RNA targeting by DNA binding drugs: structural, conformational and energetic aspects of the binding of quinacrine and DAPI to A-form and H(L)-form of poly(rC).poly(rG). Biochim. Biophys. Acta 1770 (2007), 1636–1650.
42. Smith, K.D., Shanahan, C.A., Moore, E.L., Simon, A.C., Strobel, S.A., Structural basis of differential ligand recognition by two classes of bis-(3′-5′)-cyclic dimeric guanosine monophosphate-binding riboswitches. Proc. Natl. Acad. Sci. USA 108 (2011), 7757–7762.
43. Song, W., Strack, R.L., Svensen, N., Jaffrey, S.R., Plug-and-play fluorophores extend the spectral properties of Spinach. J. Am. Chem. Soc. 136 (2014), 1198–1201.
44. Su, Y., Hickey, S.F., Keyser, S.G., Hammond, M.C., In vitro and in vivo enzyme activity screening via RNA-based fluorescent biosensors for S-adenosyl-l-homocysteine (SAH). J. Am. Chem. Soc. 138 (2016), 7040–7047.
45. 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.
46. Svensen, N., Jaffrey, S.R., Fluorescent RNA aptamers as a tool to study RNA-modifying enzymes. Cell Chem Biol. 23 (2016), 415–425.
47. Wang, X.C., Stephen, C.W., Hammond, M.C., Next-generation RNA-based fluorescent biosensors enable anaerobic detection of cyclic di-GMP. Nucleic Acids Res., 44, 2016, e139.
48. Waters, C.M., Methods for cyclic di-GMP detection. Wolfe, A.J., Visick, K.L., (eds.) The Second Messenger Cyclic Di-GMP, 2010, ASM Press, 68–75.
49. Watson, R.O., Bell, S.L., MacDuff, D.A., Kimmey, J.M., Diner, E.J., Olivas, J., Vance, R.E., Stallings, C.L., Virgin, H.W., Cox, J.S., The cytosolic sensor cGAS detects mycobacterium tuberculosis DNA to induce type I interferons and activate autophagy. Cell Host Microbe 17 (2015), 811–819.
50. Wheate, N.J., Brodie, C.R., Collins, J.G., Kemp, S., Aldrich-Wright, J.R., DNA intercalators in cancer therapy: organic and inorganic drugs and their spectroscopic tools of analysis. Mini Rev. Med. Chem. 7 (2007), 627–648.
51. 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.
52. Wilson, S.C., Cohen, D.T., Wang, X.C., Hammond, M.C., A neutral pH thermal hydrolysis method for quantification of structured RNAs. RNA 20 (2014), 1153–1160.
53. Woo, S.R., Fuertes, M.B., Corrales, L., Spranger, S., Furdyna, M.J., Leung, M.Y., Duggan, R., Wang, Y., Barber, G.N., Fitzgerald, K.A., et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity 41 (2014), 830–842.
54. Woo, S.R., Corrales, L., Gajewski, T.F., Innate immune recognition of cancer. Annu. Rev. Immunol. 33 (2015), 445–474.
55. Woo, S.R., Corrales, L., Gajewski, T.F., The STING pathway and the T cell-inflamed tumor microenvironment. Trends Immunol. 36 (2015), 250–256.
56. 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.
57. Wu, M.C., Lowe, P.T., Robinson, C.J., Vincent, H.A., Dixon, N., Leigh, J., Micklefield, J., Rational re-engineering of a transcriptional silencing PreQ1 riboswitch. J. Am. Chem. Soc. 137 (2015), 9015–9021.
58. Zhang, J.H., Chung, T.D., Oldenburg, K.R., A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen. 4 (1999), 67–73.
59. Zhang, X., Shi, H., Wu, J., Zhang, X., Sun, L., Chen, C., Chen, Z.J., Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol. Cell 51 (2013), 226–235.
60. Zhang, H., Tang, K., Zhang, Y., Ma, R., Ma, J., Li, Y., Luo, S., Liang, X., Ji, T., Gu, Z., et al. Cell-free tumor microparticle vaccines stimulate dendritic cells via cGAS/STING signaling. Cancer Immunol. Res. 3 (2015), 196–205.