Cyclic (di)nucleotides: The common language shared by microbe and host

Current Opinion in Microbiology

Volumn 30, Issue , 2016, Pages 79-87

  Gao, Juyi ^a,b,c   Tao, Jianli ^a,b,c   Liang, Weili ^d   Jiang, Zhengfan ^a,b,c  

^a PEKING UNIVERSITY   (China)

^b Peking University   (China)

^c Tsinghua University   (China)

^d CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; CRYOPYRIN; CYCLIC AMP; CYCLIC GMP; CYCLIC NUCLEOTIDE; DINUCLEOTIDE; GUANOSINE PHOSPHATE; INTERLEUKIN 1BETA; PURINE NUCLEOTIDE; STING PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; ANTIBODY PRODUCTION; BACILLUS SUBTILIS; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BINDING SITE; ENZYME ACTIVITY; EUKARYOTE; GENE EXPRESSION; GEOBACTER SULFURREDUCENS; GLUCONACETOBACTER XYLINUS; HOST CELL; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; INNATE IMMUNITY; INTERFERON PRODUCTION; INTESTINAL SECRETION; INTRACELLULAR SIGNALING; MICROBIAL GROWTH; NEUROTRANSMISSION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROKARYOTE; PROTEIN DOMAIN; REVIEW; RIBOSWITCH; SECOND MESSENGER; STRESS; T LYMPHOCYTE ACTIVATION; TYPE III SECRETION SYSTEM; VIBRIO CHOLERAE; VIRUS PARTICLE; ANIMAL; BACTERIAL INFECTION; BACTERIUM; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; HUMANS; NUCLEOTIDES, CYCLIC; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION;

EID: 84957589057     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2015.12.005     Document Type: Review

References (84)

1. Kalia D., Merey G., Nakayama S., Zheng Y., Zhou J., Luo Y., Guo M., Roembke B.T., Sintim H.O. Nucleotide, c-di-GMP, c-di-AMP, cGMP, cAMP, (p)ppGpp signaling in bacteria and implications in pathogenesis. Chem Soc Rev 2013, 42:305-341.
2. Wu J., Chen Z.J. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 2014, 32:461-488.
3. Romling U., Galperin M.Y., Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 2013, 77:1-52.
4. Danilchanka O., Mekalanos J.J. Cyclic dinucleotides and the innate immune response. Cell 2013, 154:962-970.
5. Dey B., Bishai W.R. Crosstalk between Mycobacterium tuberculosis and the host cell. Semin Immunol 2014, 26:486-496.
6. 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 2008, 30:167-178.
7. Witte C.E., Whiteley A.T., Burke T.P., Sauer J.D., Portnoy D.A., Woodward J.J. Cyclic di-AMP is critical for Listeria monocytogenes growth, cell wall homeostasis, and establishment of infection. Mbio 2013, 4.
8. Mehne F.M.P., Gunka K., Eilers H., Herzberg C., Kaever V., Stulke J. Cyclic Di-AMP homeostasis in Bacillus subtilis both lack and high level accumulation of the nucleotide are detrimental for cell growth. J Biol Chem 2013, 288:2004-2017.
9. Luo Y., Helmann J.D. Analysis of the role of Bacillus subtilis sM in ss-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. Mol Microbiol 2012, 83:623-639.
10. 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 2010, 328:1703-1705.
11. Sauer J.D., Sotelo-Troha K., von Moltke J., Monroe K.M., Rae C.S., Brubaker S.W., Hyodo M., Hayakawa Y., Woodward J.J., Portnoy D.A., 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 2011, 79:688-694.
12. 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 2011, 478:515-518.
13. Parvatiyar K., Zhang Z., Teles R.M., Ouyang S., Jiang Y., Iyer S.S., Zaver S.A., Schenk M., Zeng S., Zhong W., et al. The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat Immunol 2012, 13:1155-1161.
14. Ross P., Weinhouse H., Aloni Y., Michaeli D., Weinbergerohana P., Mayer R., Braun S., Devroom E., Vandermarel G.A., Vanboom J.H., et al. Regulation of cellulose synthesis in Acetobacter-xylinum by cyclic diguanylic acid. Nature 1987, 325:279-281.
15. Romling U., Simm R. Prevailing concepts of c-di-GMP signaling. Contrib Microbiol 2009, 16:161-181.
16. Chen Z.H., Schaap P. The prokaryote messenger c-di-GMP triggers stalk cell differentiation in Dictyostelium. Nature 2012, 488:680-683.
17. 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 2004, 53:1123-1134.
18. Tischler A.D., Camilli A. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 2004, 53:857-869.
19. Ogunniyi A.D., Paton J.C., Kirby A.C., McCullers J.A., Cook J., Hyodo M., Hayakawa Y., Karaolis D.K. c-di-GMP is an effective immunomodulator and vaccine adjuvant against pneumococcal infection. Vaccine 2008, 26:4676-4685.
20. Ebensen T., Libanova R., Schulze K., Yevsa T., Morr M., Guzman C.A. Bis-(3',5')-cyclic dimeric adenosine monophosphate: strong Th1/Th2/Th17 promoting mucosal adjuvant. Vaccine 2011, 29:5210-5220.
21. Blaauboer S.M., Mansouri S., Tucker H.R., Wang H.L., Gabrielle V.D., Jin L. The mucosal adjuvant cyclic di-GMP enhances antigen uptake and selectively activates pinocytosis-efficient cells in vivo. Elife 2015, 4.
22. 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 2015, 216:149-157.
23. Wang Z.L., Celis E. STING activator c-di-GMP enhances the anti-tumor effects of peptide vaccines in melanoma-bearing mice. Cancer Immunol Immunother 2015, 64:1057-1066.
24. 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 2012, 19:728-730.
25. Ouyang S., Song X., Wang Y., Ru H., Shaw N., Jiang Y., Niu F., Zhu Y., Qiu W., Parvatiyar K., et al. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 2012, 36:1073-1086.
26. Shang G., Zhu D., Li N., Zhang J., Zhu C., Lu D., Liu C., Yu Q., Zhao Y., Xu S., et al. Crystal structures of STING protein reveal basis for recognition of cyclic di-GMP. Nat Struct Mol Biol 2012, 19:725-727.
27. 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 2012, 19:722-724.
28. Yin Q., Tian Y., Kabaleeswaran V., Jiang X., Tu D., Eck M.J., Chen Z.J., Wu H. Cyclic di-GMP sensing via the innate immune signaling protein STING. Mol Cell 2012, 46:735-745.
29. Kranzusch P.J., Wilson S.C., Lee A.S., Berger J.M., Doudna J.A., Vance R.E. Ancient origin of cGAS-STING reveals mechanism of universal 2',3'-cGAMP signaling. Mol Cell 2015, 59:891-903.
30. Chin K.H., Tu Z.L., Su Y.C., Yu Y.J., Chen H.C., Lo Y.C., Chen C.P., Barber G.N., Chuah M.L., Liang Z.X., et al. Novel c-di-GMP recognition modes of the mouse innate immune adaptor protein STING. Acta Crystallogr D Biol Crystallogr 2013, 69:352-366.
31. Zhang H., Han M.-J., Tao J., Ye Z.-Y., Du X.-X., Deng M.-J., Zhang X.-Y., Li L.-F., Jiang Z.-F., Su X.-D. Rat and human STINGs profile similarly towards anticancer/antiviral compounds. Sci Rep 2015, 5:18035.
32. 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 2013, 339:826-830.
33. 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 2013, 339:786-791.
34. 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 2012, 149:358-370.
35. 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 U S A 2015, 112:5383-5388.
36. Nelson J.W., Sudarsan N., Phillips G.E., Stav S., Lunse C.E., McCown P.J., Breaker R.R. Control of bacterial exoelectrogenesis by c-AMP-GMP. Proc Natl Acad Sci U S A 2015, 112:5389-5394.
37. 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 2013, 51:226-235.
38. 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 2013, 153:1094-1107.
39. 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 2013, 341:1390-1394.
40. Watson R.O., Manzanillo P.S., Cox J.S. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 2012, 150:803-815.
41. Collins A.C., Cai H., Li T., Franco L.H., Li X.D., Nair V.R., Scharn C.R., Stamm C.E., Levine B., Chen Z.J., et al. Cyclic GMP-AMP synthase is an innate immune DNA sensor for Mycobacterium tuberculosis. Cell Host Microbe 2015, 17:820-828.
42. 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 2015, 17:811-819.
43. Ablasser A., Schmid-Burgk J.L., Hemmerling I., Horvath G.L., Schmidt T., Latz E., Hornung V. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 2013, 503:530-534.
44. Bridgeman A., Maelfait J., Davenne T., Partridge T., Peng Y., Mayer A., Dong T., Kaever V., Borrow P., Rehwinkel J. Viruses transfer the antiviral second messenger cGAMP between cells. Science 2015, 349:1228-1232.
45. Gentili M., Kowal J., Tkach M., Satoh T., Lahaye X., Conrad C., Boyron M., Lombard B., Durand S., Kroemer G., et al. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science 2015, 349:1232-1236.
46. Vojtova J., Kamanova J., Sebo P. Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr Opin Microbiol 2006, 9:69-75.
47. Turk B.E. Manipulation of host signalling pathways by anthrax toxins. Biochem J 2007, 402:405-417.
48. 2+ and cAMP. Nature 2012, 492:123-127.
49. Windham P.F., Tinsley H.N. cGMP signaling as a target for the prevention and treatment of breast cancer. Semin Cancer Biol 2015, 31:106-110.
50. Ochoa C.D., Alexeyev M., Pastukh V., Balczon R., Stevens T. Pseudomonas aeruginosa exotoxin Y is a promiscuous cyclase that increases endothelial tau phosphorylation and permeability. J Biol Chem 2012, 287:25407-25418.
51. Beckert U., Wolter S., Hartwig C., Bahre H., Kaever V., Ladant D., Frank D.W., Seifert R. ExoY from Pseudomonas aeruginosa is a nucleotidyl cyclase with preference for cGMP and cUMP formation. Biochem Biophys Res Commun 2014, 450:870-874.
52. Engel J., Balachandran P. Role of Pseudomonas aeruginosa type III effectors in disease. Curr Opin Microbiol 2009, 12:61-66.
53. Franchi L., Stoolman J., Kanneganti T.D., Verma A., Rarnphal R., Nunez G. Critical role for Ipaf in Pseudomonas aeruginosa-induced caspase-1 activation. Eur J Immunol 2007, 37:3030-3039.
54. Xayarath B., Freitag N.E. Uncovering the nonessential nature of an essential second messenger. Cell Host Microbe 2015, 17:731-732.
55. Schaap P. Cyclic di-nucleotide signaling enters the eukaryote domain. IUBMB Life 2013, 65:897-903.
56. Bai Y., Yang J., Eisele L.E., Underwood A.J., Koestler B.J., Waters C.M., Metzger D.W., Bai G. Two DHH subfamily 1 proteins in Streptococcus pneumoniae possess cyclic di-AMP phosphodiesterase activity and affect bacterial growth and virulence. J Bacteriol 2013, 195:5123-5132.
57. Gao P., Patel D.J. V-cGAPs: attenuators of 3'3'-cGAMP signaling. Cell Res 2015, 25:529-530.
58. Aravind L., Koonin E.V. A novel family of predicted phosphoesterases includes Drosophila prune protein and bacterial RecJ exonuclease. Trends Biochem Sci 1998, 23:17-19.
59. Corrigan R.M., Grundling A. Cyclic di-AMP: another second messenger enters the fray. Nat Rev Microbiol 2013, 11:513-524.
60. Orr M.W., Donaldson G.P., Severin G.B., Wang J., Sintim H.O., Waters C.M., Lee V.T. Oligoribonuclease is the primary degradative enzyme for pGpG in Pseudomonas aeruginosa that is required for cyclic-di-GMP turnover. Proc Natl Acad Sci U S A 2015, 112:E5048-E5057.
61. Cohen D., Mechold U., Nevenzal H., Yarmiyhu Y., Randall T.E., Bay D.C., Rich J.D., Parsek M.R., Kaever V., Harrison J.J., et al. Oligoribonuclease is a central feature of cyclic diguanylate signaling in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 2015, 112:11359-11364.
62. Wigren E., Liang Z.X., Romling U. Finally! The structural secrets of a HD-GYP phosphodiesterase revealed. Mol Microbiol 2014, 91:1-5.
63. Ryan R.P., Dow J.M. Intermolecular interactions between HD-GYP and GGDEF domain proteins mediate virulence-related signal transduction in Xanthomonas campestris. Virulence 2010, 1:404-408.
64. Kranzusch P.J., Lee A.S., Wilson S.C., Solovykh M.S., Vance R.E., Berger J.M., Doudna J.A. Structure-guided reprogramming of human cGAS dinucleotide linkage specificity. Cell 2014, 158:1011-1021.
65. Ming Z., Wang W., Xie Y., Ding P., Chen Y., Jin D., Sun Y., Xia B., Yan L., Lou Z. Crystal structure of the novel di-nucleotide cyclase from Vibrio cholerae (DncV) responsible for synthesizing a hybrid cyclic GMP-AMP. Cell Res 2014, 24:1270-1273.
66. Zhu D., Wang L., Shang G., Liu X., Zhu J., Lu D., Wang L., Kan B., Zhang J.R., Xiang Y. Structural biochemistry of a Vibrio cholerae dinucleotide cyclase reveals cyclase activity regulation by folates. Mol Cell 2014, 55:931-937.
67. Gao J., Tao J., Liang W., Zhao M., Du X., Cui S., Duan H., Kan B., Su X., Jiang Z. Identification and characterization of phosphodiesterases that specifically degrade 3'3'-cyclic GMP-AMP. Cell Res 2015, 25:539-550.
68. Li L., Yin Q., Kuss P., Maliga Z., Millan J.L., Wu H., Mitchison T.J. Hydrolysis of 2'3'-cGAMP by ENPP1 and design of nonhydrolyzable analogs. Nat Chem Biol 2014, 10:1043-1048.
69. Stefan C., Jansen S., Bollen M. NPP-type ectophosphodiesterases: unity in diversity. Trends Biochem Sci 2005, 30:542-550.
70. Korekane H., Park J.Y., Matsumoto A., Nakajima K., Takamatsu S., Ohtsubo K., Miyamoto Y., Hanashima S., Kanekiyo K., Kitazume S., et al. Identification of ectonucleotide pyrophosphatase/phosphodiesterase 3 (ENPP3) as a regulator of N-acetylglucosaminyltransferase GnT-IX (GnT-Vb). J Biol Chem 2013, 288:27912-27926.
71. Baker D.A., Kelly J.M. Structure, function and evolution of microbial adenylyl and guanylyl cyclases. Mol Microbiol 2004, 52:1229-1242.
72. Beste K.Y., Spangler C.M., Burhenne H., Koch K.W., Shen Y., Tang W.J., Kaever V., Seifert R. Nucleotidyl cyclase activity of particulate guanylyl cyclase A: comparison with particulate guanylyl cyclases E and F, soluble guanylyl cyclase and bacterial adenylyl cyclases CyaA and edema factor. PLoS One 2013, 8:e70223.
73. An S.Q., Chin K.H., Febrer M., McCarthy Y., Yang J.G., Liu C.L., Swarbreck D., Rogers J., Maxwell Dow J., Chou S.H., et al. A cyclic GMP-dependent signalling pathway regulates bacterial phytopathogenesis. EMBO J 2013, 32:2430-2438.
74. Marden J.N., Dong Q.A., Roychowdhury S., Berleman J.E., Bauer C.E. Cyclic GMP controls Rhodospirillum centenum cyst development. Mol Microbiol 2011, 79:600-615.
75. Ryu M.H., Youn H., Kang I.H., Gomelsky M. Identification of bacterial guanylate cyclases. Proteins 2015, 83:799-804.
76. Guo Y.L., Seebacher T., Kurz U., Linder J.U., Schultz J.E. Adenylyl cyclase Rv1625c of Mycobacterium tuberculosis: a progenitor of mammalian adenylyl cyclases. EMBO J 2001, 20:3667-3675.
77. Potter L.R. Guanylyl cyclase structure, function and regulation. Cell Signal 2011, 23:1921-1926.
78. Omori K., Kotera J. Overview of PDEs and their regulation. Circ Res 2007, 100:309-327.
79. Richter W. 3',5' Cyclic nucleotide phosphodiesterases class III: members, structure, and catalytic mechanism. Proteins 2002, 46:278-286.
80. Shenoy A.R., Capuder M., Draskovic P., Lamba D., Visweswariah S.S., Podobnik M. Structural and biochemical analysis of the Rv0805 cyclic nucleotide phosphodiesterase from Mycobacterium tuberculosis. J Mol Biol 2007, 365:211-225.
81. Berthet J., Rall T.W., Sutherland E.W. The relationship of epinephrine and glucagon to liver phosphorylase. IV. Effect of epinephrine and glucagon on the reactivation of phosphorylase in liver homogenates. J Biol Chem 1957, 224:463-475.
82. Makman R.S., Sutherland E.W. Adenosine 3',5'-phosphate in Escherichia coli. J Biol Chem 1965, 240:1309-1314.
83. Ashman D.F., Lipton R., Melicow M.M., Price T.D. Isolation of adenosine 3,5-monophosphate and guanosine 3,5-monophosphate from rat urine. Biochem Biophys Res Commun 1963, 11:330-334.
84. Bernlohr R.W., Haddox M.K., Goldberg N.D. Cyclic guanosine 3':5'-monophosphate in Escherichia coli and Bacillus lichenformis. J Biol Chem 1974, 249:4329-4331.