Versatile modes of cellular regulation via cyclic dinucleotides

Nature Chemical Biology

Volumn 13, Issue 4, 2017, Pages 350-359

  Krasteva, Petya Violinova ^a,b   Sondermann, Holger ^c  

^a INSTITUT PASTEUR   (France)

^b INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC DINUCLEOTIDE; DINUCLEOTIDE; ION; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CYCLIC NUCLEOTIDE;

BACTERIAL SECRETION SYSTEM; ENZYME DEGRADATION; ENZYME SYNTHESIS; GENE; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STIMULATOR OF INTERFERON GENE; AMINO ACID SEQUENCE; ANIMAL; BACTERIUM; CHEMISTRY; EUKARYOTE; HUMAN; METABOLISM; MOLECULAR MODEL; PROKARYOTIC CELL; PROTEIN PROCESSING;

AMINO ACID SEQUENCE; ANIMALS; BACTERIA; EUKARYOTA; HUMANS; MODELS, MOLECULAR; NUCLEOTIDES, CYCLIC; PROKARYOTIC CELLS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 85016154450     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2337     Document Type: Review

References (100)

1. Ross, P. et al. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325, 279-281 (1987).
2. Weinhouse, H. et al. c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett. 416, 207-211 (1997).
3. Tal, R. et al. Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J. Bacteriol. 180, 4416-4425 (1998).
4. Paul, R. et al. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18, 715-727 (2004).
5. Christen, M., Christen, B., Folcher, M., Schauerte, A. & Jenal, U. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 280, 30829-30837 (2005).
6. Simm, R., Morr, M., Kader, A., Nimtz, M. & Romling, U. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol. 53, 1123-1134 (2004).
7. Hickman, J.W., Tifrea, D.F. & Harwood, C.S. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. USA 102, 14422-14427 (2005).
8. Hisert, K.B. et al. A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages: role of cyclic diGMP. Mol. Microbiol. 56, 1234-1245 (2005).
9. Tischler, A.D. & Camilli, A. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53, 857-869 (2004).
10. Galperin, M.Y., Nikolskaya, A.N. & Koonin, E.V. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203, 11-21 (2001).
11. Witte, G., Hartung, S., Buttner, K. & Hopfner, K.P. Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol. Cell 30, 167-178 (2008).
12. Bai, Y. et al. Cyclic di-AMP impairs potassium uptake mediated by a cyclic di-AMP binding protein in Streptococcus pneumoniae. J. Bacteriol. 196, 614-623 (2014).
13. Huynh, T.N. et al. An HD-domain phosphodiesterase mediates cooperative hydrolysis of c-di-AMP to affect bacterial growth and virulence. Proc. Natl. Acad. Sci. USA 112, E747-E756 (2015).
14. Mehne, F.M. et al. Cyclic di-AMP homeostasis in bacillus subtilis: both lack and high level accumulation of the nucleotide are detrimental for cell growth. J. Biol. Chem. 288, 2004-2017 (2013).
15. Zhang, L., Li, W. & He, Z.G. DarR, a TetR-like transcriptional factor, is a cyclic di-AMP-responsive repressor in Mycobacterium smegmatis. J. Biol. Chem. 288, 3085-3096 (2013).
16. Kaplan Zeevi, M. et al. Listeria monocytogenes multidrug resistance transporters and cyclic di-AMP, which contribute to type I interferon induction, play a role in cell wall stress. J. Bacteriol. 195, 5250-5261 (2013).
17. Sureka, K. et al. The cyclic dinucleotide c-di-AMP is an allosteric regulator of metabolic enzyme function. Cell 158, 1389-1401 (2014).
18. Corrigan, R.M. et al. Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc. Natl. Acad. Sci. USA 110, 9084-9089 (2013).
19. Moscoso, J.A. et al. Binding of cyclic di-AMP to the Staphylococcus aureus Sensor kinase KDPD occurs via the universal stress protein domain and downregulates the expression of the KDP potassium transporter. J. Bacteriol. 198, 98-110 (2015).
20. Davies, B.W., Bogard, R.W., Young, T.S. & Mekalanos, J.J. Coordinated regulation of accessory genetic elements produces cyclic di-nucleotides for V. cholerae virulence. Cell 149, 358-370 (2012).
21. Pei, J. & Grishin, N.V. GGDEF domain is homologous to adenylyl cyclase. Proteins 42, 210-216 (2001).
22. Chan, C. et al. Structural basis of activity and allosteric control of diguanylate cyclase. Proc. Natl. Acad. Sci. USA 101, 17084-17089 (2004).
23. Dahlstrom, K.M., Giglio, K.M., Sondermann, H. & O'Toole, G.A. The inhibitory site of a diguanylate cyclase is a necessary element for interaction and signaling with an effector protein. J. Bacteriol. 198, 1595-1603 (2016).
24. Barends, T.R. et al. Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459, 1015-1018 (2009).
25. Bellini, D. et al. Crystal structure of an HD-GYP domain cyclic-di-GMP phosphodiesterase reveals an enzyme with a novel trinuclear catalytic iron centre. Mol. Microbiol. 91, 26-38 (2014).
26. Stelitano, V. et al. C-di-GMP hydrolysis by Pseudomonas aeruginosa HD-GYP phosphodiesterases: analysis of the reaction mechanism and novel roles for pGpG. PLoS One 8, e74920 (2013).
27. Cohen, D. et al. Oligoribonuclease is a central feature of cyclic diguanylate signaling in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 112, 11359-11364 (2015).
28. Orr, M.W. et al. Oligoribonuclease is the primary degradative enzyme for pGpG in Pseudomonas aeruginosa that is required for cyclic-di-GMP turnover. Proc. Natl. Acad. Sci. USA 112, E5048-E5057 (2015).
29. Galperin, M.Y. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol. 5, 35 (2005).
30. Corrigan, R.M. & Grundling, A. Cyclic di-AMP: another second messenger enters the fray. Nat. Rev. Microbiol. 11, 513-524 (2013).
31. Rao, F. et al. YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity. J. Biol. Chem. 285, 473-482 (2010).
32. Kranzusch, P.J. et al. Structure-guided reprogramming of human cGAS dinucleotide linkage specificity. Cell 158, 1011-1021 (2014).
33. Zhu, D. et al. Structural biochemistry of a Vibrio cholerae dinucleotide cyclase reveals cyclase activity regulation by folates. Mol. Cell 55, 931-937 (2014).
34. Hallberg, Z.F. et al. Hybrid promiscuous (Hypr) GGDEF enzymes produce cyclic AMP-GMP (3′, 3′-cGAMP). Proc. Natl. Acad. Sci. USA 113, 1790-1795 (2016).
35. Navarro, M.V., De, N., Bae, N., Wang, Q. & Sondermann, H. Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 17, 1104-1116 (2009).
36. Navarro, M.V. et al. Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol. 9, e1000588 (2011).
37. Ozaki, S. et al. Activation and polar sequestration of PopA, a c-di-GMP effector protein involved in Caulobacter crescentus cell cycle control. Mol. Microbiol. 94, 580-594 (2014).
38. Lee, V.T. et al. A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol. Microbiol. 65, 1474-1484 (2007).
39. Amikam, D. & Galperin, M.Y. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22, 3-6 (2006).
40. Hickman, J.W. & Harwood, C.S. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 69, 376-389 (2008).
41. Krasteva, P.V. et al. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327, 866-868 (2010).
42. Srivastava, D., Harris, R.C. & Waters, C.M. Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae. J. Bacteriol. 193, 6331-6341 (2011).
43. Duvel, J. et al. A chemical proteomics approach to identify c-di-GMP binding proteins in Pseudomonas aeruginosa. J. Microbiol. Methods 88, 229-236 (2012).
44. Nesper, J., Reinders, A., Glatter, T., Schmidt, A. & Jenal, U. A novel capture compound for the identification and analysis of cyclic di-GMP binding proteins. J. Proteomics 75, 4874-4878 (2012).
45. Roelofs, K.G., Wang, J., Sintim, H.O. & Lee, V.T. Differential radial capillary action of ligand assay for high-throughput detection of protein-metabolite interactions. Proc. Natl. Acad. Sci. USA 108, 15528-15533 (2011).
46. Roelofs, K.G. et al. Systematic identification of cyclic-di-GMP binding proteins in Vibrio cholerae reveals a novel class of cyclic-di-GMP-binding ATPases associated with type II secretion systems. PLoS Pathog. 11, e1005232 (2015).
47. Newell, P.D., Boyd, C.D., Sondermann, H. & O'Toole, G.A. A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol. 9, e1000587 (2011).
48. Cooley, R.B. et al. Cyclic di-GMP-regulated periplasmic proteolysis of a Pseudomonas aeruginosa type Vb secretion system substrate. J. Bacteriol. 198, 66-76 (2015).
49. Chatterjee, D. et al. Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMP. eLife 3, e03650 (2014).
50. Giardina, G. et al. Investigating the allosteric regulation of YfiN from Pseudomonas aeruginosa: clues from the structure of the catalytic domain. PLoS One 8, e81324 (2013).
51. Malone, J.G. et al. The YfiBNR signal transduction mechanism reveals novel targets for the evolution of persistent Pseudomonas aeruginosa in cystic fibrosis airways. PLoS Pathog. 8, e1002760 (2012).
52. Srivastava, D., Hsieh, M.L., Khataokar, A., Neiditch, M.B. & Waters, C.M. Cyclic di-GMP inhibits Vibrio cholerae motility by repressing induction of transcription and inducing extracellular polysaccharide production. Mol. Microbiol. 90, 1262-1276 (2013).
53. Tschowri, N. et al. Tetrameric c-di-GMP mediates effective transcription factor dimerization to control Streptomyces development. Cell 158, 1136-1147 (2014).
54. Chin, K.H. et al. The cAMP receptor-like protein CLP is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris. J. Mol. Biol. 396, 646-662 (2010).
55. Li, W. & He, Z.G. LtmA, a novel cyclic di-GMP-responsive activator, broadly regulates the expression of lipid transport and metabolism genes in Mycobacterium smegmatis. Nucleic Acids Res. 40, 11292-11307 (2012).
56. Shikuma, N.J., Fong, J.C. & Yildiz, F.H. Cellular levels and binding of c-di-GMP control subcellular localization and activity of the Vibrio cholerae transcriptional regulator VpsT. PLoS Pathog. 8, e1002719 (2012).
57. Baraquet, C. & Harwood, C.S. Cyclic diguanosine monophosphate represses bacterial flagella synthesis by interacting with the Walker A motif of the enhancer-binding protein FleQ. Proc. Natl. Acad. Sci. USA 110, 18478-18483 (2013).
58. Baraquet, C., Murakami, K., Parsek, M.R. & Harwood, C.S. The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP. Nucleic Acids Res. 40, 7207-7218 (2012).
59. Matsuyama, B.Y. et al. Mechanistic insights into c-di-GMP-dependent control of the biofilm regulator FleQ from Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 113, E209-E218 (2016).
60. Lauriano, C.M., Ghosh, C., Correa, N.E. & Klose, K.E. The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J. Bacteriol. 186, 4864-4874 (2004).
61. den Hengst, C.D. et al. Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth. Mol. Microbiol. 78, 361-379 (2010).
62. Vieira-Pires, R.S., Szollosi, A. & Morais-Cabral, J.H. The structure of the KtrAB potassium transporter. Nature 496, 323-328 (2013).
63. Kim, H. et al. Structural studies of potassium transport protein KtrA regulator of conductance of K+ (RCK) C domain in complex with cyclic diadenosine monophosphate (c-di-AMP). J. Biol. Chem. 290, 16393-16402 (2015).
64. Lolicato, M. et al. Cyclic dinucleotides bind the C-linker of HCN4 to control channel cAMP responsiveness. Nat. Chem. Biol. 10, 457-462 (2014).
65. Costa, T.R. et al. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 13, 343-359 (2015).
66. Trampari, E. et al. Bacterial rotary export ATPases are allosterically regulated by the nucleotide second messenger cyclic-di-GMP. J. Biol. Chem. 290, 24470-24483 (2015).
67. Wang, Y.C. et al. Nucleotide binding by the widespread high-affinity cyclic di-GMP receptor MshEN domain. Nat. Commun. 7, 12481 (2016).
68. Whitney, J.C. & Howell, P.L. Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria. Trends Microbiol. 21, 63-72 (2013).
69. McNamara, J.T., Morgan, J.L. & Zimmer, J. A molecular description of cellulose biosynthesis. Annu. Rev. Biochem. 84, 895-921 (2015).
70. Fang, X. et al. GIL, a new c-di-GMP-binding protein domain involved in regulation of cellulose synthesis in enterobacteria. Mol. Microbiol. 93, 439-452 (2014).
71. Li, Z., Chen, J.H., Hao, Y. & Nair, S.K. Structures of the PelD cyclic diguanylate effector involved in pellicle formation in Pseudomonas aeruginosa PAO1. J. Biol. Chem. 287, 30191-30204 (2012).
72. Whitney, J.C. et al. Structure of the cytoplasmic region of PelD, a degenerate diguanylate cyclase receptor that regulates exopolysaccharide production in Pseudomonas aeruginosa. J. Biol. Chem. 287, 23582-23593 (2012).
73. Steiner, S., Lori, C., Boehm, A. & Jenal, U. Allosteric activation of exopolysaccharide synthesis through cyclic di-GMP-stimulated protein-protein interaction. EMBO J. 32, 354-368 (2013).
74. Woodward, J.J., Iavarone, A.T. & Portnoy, D.A. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328, 1703-1705 (2010).
75. Sun, J., Deng, Z. & Yan, A. Bacterial multidrug efflux pumps: mechanisms, physiology and pharmacological exploitations. Biochem. Biophys. Res. Commun. 453, 254-267 (2014).
76. Chen, Z.H. & Schaap, P. The prokaryote messenger c-di-GMP triggers stalk cell differentiation in Dictyostelium. Nature 488, 680-683 (2012).
77. Gentili, M. et al. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science 349, 1232-1236 (2015).
78. Bridgeman, A. et al. Viruses transfer the antiviral second messenger cGAMP between cells. Science 349, 1228-1232 (2015).
79. Ablasser, A. et al. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 503, 530-534 (2013).
80. Chen, Q. et al. Carcinoma-astrocyte gap junctions promote brain metastasis by cGAMP transfer. Nature 533, 493-498 (2016).
81. Li, L. et al. Hydrolysis of 23′-cGAMP by ENPP1 and design of nonhydrolyzable analogs. Nat. Chem. Biol. 10, 1043-1048 (2014).
82. Sauer, J.D. et al. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect. Immun. 79, 688-694 (2011).
83. Burdette, D.L. et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 478, 515-518 (2011).
84. Diner, E.J. et al. The innate immune DNA sensor cGAS produces a noncanonical cyclic dinucleotide that activates human STING. Cell Rep. 3, 1355-1361 (2013).
85. 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, 786-791 (2013).
86. Wu, J. et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339, 826-830 (2013).
87. Ablasser, A. et al. cGAS produces a 2′-5′-linked cyclic dinucleotide second messenger that activates STING. Nature 498, 380-384 (2013).
88. Ouyang, S. et al. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 36, 1073-1086 (2012).
89. Shu, C., Yi, G., Watts, T., Kao, C.C. & Li, P. Structure of STING bound to cyclic di-GMP reveals the mechanism of cyclic dinucleotide recognition by the immune system. Nat. Struct. Mol. Biol. 19, 722-724 (2012).
90. Huang, Y.H., Liu, X.Y., Du, X.X., Jiang, Z.F. & Su, X.D. The structural basis for the sensing and binding of cyclic di-GMP by STING. Nat. Struct. Mol. Biol. 19, 728-730 (2012).
91. Shang, G. et al. Crystal structures of STING protein reveal basis for recognition of cyclic di-GMP. Nat. Struct. Mol. Biol. 19, 725-727 (2012).
92. Zhang, X. et al. Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol. Cell 51, 226-235 (2013).
93. Chin, K.H. et al. Novel c-di-GMP recognition modes of the mouse innate immune adaptor protein STING. Acta Crystallogr. D Biol. Crystallogr. 69, 352-366 (2013).
94. Kranzusch, P.J. et al. Ancient origin of cGAS-STING reveals mechanism of universal 2′,3′ cGAMP signaling. Mol. Cell 59, 891-903 (2015).
95. Yin, Q. et al. Cyclic di-GMP sensing via the innate immune signaling protein STING. Mol. Cell 46, 735-745 (2012).
96. Gao, P. 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, 1094-1107 (2013).
97. Zhang, L. et al. NLRC3, a member of the NLR family of proteins, is a negative regulator of innate immune signaling induced by the DNA sensor STING. Immunity 40, 329-341 (2014).
98. Mohite, B.V. & Patil, S.V. A novel biomaterial: bacterial cellulose and its new era applications. Biotechnol. Appl. Biochem. 61, 101-110 (2014).
99. Opoku-Temeng, C., Zhou, J., Zheng, Y., Su, J. & Sintim, H.O. Cyclic dinucleotide (c-di-GMP, c-di-AMP, and cGAMP) signalings have come of age to be inhibited by small molecules. Chem. Commun. (Camb.) 52, 9327-9342 (2016).
100. Gravekamp, C. & Chandra, D. Targeting STING pathways for the treatment of cancer. OncoImmunology 4, e988463 (2015).