Cyclic-di-GMP signaling in the Gram-positive pathogen Clostridium difficile

Current Genetics

Volumn 61, Issue 4, 2015, Pages 497-502

  Bordeleau, Eric ^a,b   Burrus, Vincent ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Biofilm; Clostridium difficile; Cyclic di GMP; Motility; Riboswitch; Toxins

Indexed keywords

CARRIER PROTEIN; CYCLIC DIGUANOSINE MONOPHOSPHATE; CYCLIC GMP; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIAL TOXIN; BIS(3',5')-CYCLIC DIGUANYLIC ACID; ENTEROTOXIN; RIBOSWITCH; TCDA PROTEIN, CLOSTRIDIUM DIFFICILE; TOXB PROTEIN, CLOSTRIDIUM DIFFICILE;

LIFE CYCLE; NONHUMAN; PEPTOCLOSTRIDIUM DIFFICILE; PHENOTYPE; PRIORITY JOURNAL; REVIEW; RIBOSWITCH; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; BIOFILM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PATHOGENICITY; SECOND MESSENGER; VIRULENCE;

BACTERIAL PROTEINS; BACTERIAL TOXINS; BIOFILMS; CLOSTRIDIUM DIFFICILE; CYCLIC GMP; ENTEROTOXINS; GENE EXPRESSION REGULATION, BACTERIAL; PHENOTYPE; RIBOSWITCH; SECOND MESSENGER SYSTEMS; VIRULENCE;

EID: 84944512750     PISSN: 01728083     EISSN: 14320983     Source Type: Journal    
DOI: 10.1007/s00294-015-0484-z     Document Type: Review

References (59)

1. Abel S, Bucher T, Nicollier M, Hug I, Kaever V, Abel Zur Wiesch P, Jenal U (2013) Bi-modal distribution of the second messenger c-di-GMP controls cell fate and asymmetry during the caulobacter cell cycle. PLoS Genet 9:e1003744
2. Amikam D, Galperin MY (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3–6
3. Aubry A, Hussack G, Chen W, KuoLee R, Twine SM, Fulton KM, Foote S, Carrillo CD, Tanha J, Logan SM (2012) Modulation of toxin production by the flagellar regulon in Clostridium difficile. Infect Immun 80:3521–3532
4. Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackermann M, Kaever V, Sourjik V, Roth V, Jenal U (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141:107–116
5. Bordeleau E, Brouillette E, Robichaud N, Burrus V (2010) Beyond antibiotic resistance: integrating conjugative elements of the SXT/R391 family that encode novel diguanylate cyclases participate to c-di-GMP signalling in Vibrio cholerae. Environ Microbiol 12:510–523
6. Bordeleau E, Fortier LC, Malouin F, Burrus V (2011) c-di-GMP turn-over in Clostridium difficile is controlled by a plethora of diguanylate cyclases and phosphodiesterases. PLoS Genet 7:e1002039
7. Bordeleau E, Purcell EB, Lafontaine DA, Fortier LC, Tamayo R, Burrus V (2015) Cyclic Di-GMP Riboswitch-Regulated Type IV Pili Contribute to Aggregation of Clostridium difficile. J Bacteriol 197:819–832
8. Breaker RR (2012) Riboswitches and the RNA world. Cold Spring Harb Perspect Biol 4
9. Burke KE, Lamont JT (2014) Clostridium difficile infection: a worldwide disease. Gut Liver 8:1–6
10. Buskila AA, Kannaiah S, Amster-Choder O (2014) RNA localization in bacteria. RNA Biol 11:1051–1060
11. Cafardi V, Biagini M, Martinelli M, Leuzzi R, Rubino JT, Cantini F, Norais N, Scarselli M, Serruto D, Unnikrishnan M (2013) Identification of a novel zinc metalloprotease through a global analysis of Clostridium difficile extracellular proteins. PLoS One 8:e81306
12. Chen Y, Chai Y, Guo JH, Losick R (2012) Evidence for cyclic Di-GMP-mediated signaling in Bacillus subtilis. J Bacteriol 194:5080–5090
13. Chen LH, Koseoglu VK, Guvener ZT, Myers-Morales T, Reed JM, D’Orazio SE, Miller KW, Gomelsky M (2014) Cyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes. PLoS Pathog 10:e1004301
14. Duerig A, Abel S, Folcher M, Nicollier M, Schwede T, Amiot N, Giese B, Jenal U (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23:93–104
15. El Meouche I, Peltier J, Monot M, Soutourina O, Pestel-Caron M, Dupuy B, Pons JL (2013) Characterization of the SigD regulon of C. difficile and its positive control of toxin production through the regulation of tcdR. PLoS One 8:e83748
16. Fang X, Gomelsky M (2010) A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol 76:1295–1305
17. Galperin MY, Higdon R, Kolker E (2010) Interplay of heritage and habitat in the distribution of bacterial signal transduction systems. Mol BioSyst 6:721–728
18. Gao X, Mukherjee S, Matthews PM, Hammad LA, Kearns DB, Dann CE 3rd (2013) Functional characterization of core components of the Bacillus subtilis cyclic-di-GMP signaling pathway. J Bacteriol 195:4782–4792
19. Gerding DN, Lessa FC (2015) The epidemiology of clostridium difficile infection inside and outside health care institutions. Infect Dis Clin North Am 29:37–50
20. Giltner CL, Nguyen Y, Burrows LL (2012) Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev 76:740–772
21. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273
22. Hensbergen PJ, Klychnikov OI, Bakker D, van Winden VJ, Ras N, Kemp AC, Cordfunke RA, Dragan I, Deelder AM, Kuijper EJ, Corver J, Drijfhout JW, van Leeuwen HC (2014) A novel secreted metalloprotease (CD2830) from Clostridium difficile cleaves specific proline sequences in LPXTG cell surface proteins. Mol Cell Proteomics. doi:10.1074/mcp.M1113.034728 (in press)
23. Hisert KB, MacCoss M, Shiloh MU, Darwin KH, Singh S, Jones RA, Ehrt S, Zhang Z, Gaffney BL, Gandotra S, Holden DW, Murray D, Nathan C (2005) 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
24. Holland LM, O’Donnell ST, Ryjenkov DA, Gomelsky L, Slater SR, Fey PD, Gomelsky M, O’Gara JP (2008) A staphylococcal GGDEF domain protein regulates biofilm formation independently of cyclic dimeric GMP. J Bacteriol 190:5178–5189
25. Hull TD, Ryu MH, Sullivan MJ, Johnson RC, Klena NT, Geiger RM, Gomelsky M, Bennett JA (2012) Cyclic Di-GMP phosphodiesterases RmdA and RmdB are involved in regulating colony morphology and development in Streptomyces coelicolor. J Bacteriol 194:4642–4651
26. Krasteva PV, Fong JC, Shikuma NJ, Beyhan S, Navarro MV, Yildiz FH, Sondermann H (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327:866–868
27. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Ausubel FM, Lory S (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci 103:2839–2844
28. Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR (2010) An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329:845–848
29. Massie JP, Reynolds EL, Koestler BJ, Cong JP, Agostoni M, Waters CM (2012) Quantification of high-specificity cyclic diguanylate signaling. Proc Natl Acad Sci 109:12746–12751
30. McKee RW, Mangalea MR, Purcell EB, Borchardt EK, Tamayo R (2013) The second messenger cyclic Di-GMP regulates clostridium difficile toxin production by controlling expression of sigD. J Bacteriol 195:5174–5185
31. Melville S, Craig L (2013) Type IV pili in Gram-positive bacteria. Microbiol Mol Biol Rev 77:323–341
32. Montero Llopis P, Jackson AF, Sliusarenko O, Surovtsev I, Heinritz J, Emonet T, Jacobs-Wagner C (2010) Spatial organization of the flow of genetic information in bacteria. Nature 466:77–81
33. Navarro MV, Newell PD, Krasteva PV, Chatterjee D, Madden DR, O’Toole GA, Sondermann H (2011) Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol 9:e1000588
34. Nevo-Dinur K, Nussbaum-Shochat A, Ben-Yehuda S, Amster-Choder O (2011) Translation-independent localization of mRNA in E. coli. Science 331:1081–1084
35. Newell PD, Monds RD, O’Toole GA (2009) LapD is a bis-(3′,5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc Natl Acad Sci 106:3461–3466
36. Newell PD, Boyd CD, Sondermann H, O’Toole GA (2011) A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol 9:e1000587
37. Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM (2010) The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a “backstop brake” mechanism. Mol Cell 38:128–139
38. Proft T, Baker EN (2009) Pili in Gram-negative and Gram-positive bacteria–structure, assembly and their role in disease. Cell Mol Life Sci 66:613–635
39. Purcell EB, McKee RW, McBride SM, Waters CM, Tamayo R (2012) Cyclic diguanylate inversely regulates motility and aggregation in Clostridium difficile. J Bacteriol 194:3307–3316
40. Romling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57:629–639
41. Romling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52
42. Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, Mayer R, Braun S, de Vroom E, van der Marel GA, van Boom JH, Benziman M (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279–281
43. Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, Zhang LH, Heeb S, Camara M, Williams P, Dow JM (2006) Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci 103:6712–6717
44. Ryan RP, Fouhy Y, Lucey JF, Jiang BL, He YQ, Feng JX, Tang JL, Dow JM (2007) Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol Microbiol 63:429–442
45. Ryjenkov DA, Tarutina M, Moskvin OV, Gomelsky M (2005) Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol 187:1792–1798
46. Schmidt AJ, Ryjenkov DA, Gomelsky M (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 187:4774–4781
47. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeno-Tarraga AM, Wang H, Holden MT, Wright A, Churcher C, Quail MA, Baker S, Bason N, Brooks K, Chillingworth T, Cronin A, Davis P, Dowd L, Fraser A, Feltwell T, Hance Z, Holroyd S, Jagels K, Moule S, Mungall K, Price C, Rabbinowitsch E, Sharp S, Simmonds M, Stevens K, Unwin L, Whithead S, Dupuy B, Dougan G, Barrell B, Parkhill J (2006) The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38:779–786
48. Serganov A, Nudler E (2013) A decade of riboswitches. Cell 152:17–24
49. Seshasayee AS, Fraser GM, Luscombe NM (2010) Comparative genomics of cyclic-di-GMP signalling in bacteria: post-translational regulation and catalytic activity. Nucleic Acids Res 38:5970–5981
50. Shang F, Xue T, Sun H, Xing L, Zhang S, Yang Z, Zhang L, Sun B (2009) The Staphylococcus aureus GGDEF domain-containing protein, GdpS, influences protein A gene expression in a cyclic diguanylic acid-independent manner. Infect Immun 77:2849–2856
51. Shen A (2012) Clostridium difficile toxins: mediators of inflammation. J Innate Immun 4:149–158
52. Soutourina OA, Monot M, Boudry P, Saujet L, Pichon C, Sismeiro O, Semenova E, Severinov K, Le Bouguenec C, Coppee JY, Dupuy B, Martin-Verstraete I (2013) Genome-wide identification of regulatory RNAs in the human pathogen Clostridium difficile. PLoS Genet 9:e1003493
53. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, Breaker RR (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411–413
54. Tamayo R, Tischler AD, Camilli A (2005) The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J Biol Chem 280:33324–33330
55. Tischler AD, Camilli A (2005) Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun 73:5873–5882
56. Tulli L, Marchi S, Petracca R, Shaw HA, Fairweather NF, Scarselli M, Soriani M, Leuzzi R (2013) CbpA: a novel surface exposed adhesin of Clostridium difficile targeting human collagen. Cell Microbiol 15:1674–1687
57. Vedantam G, Clark A, Chu M, McQuade R, Mallozzi M, Viswanathan VK (2012) Clostridium difficile infection: toxins and non-toxin virulence factors, and their contributions to disease establishment and host response. Gut Microbes 3:121–134
58. Voth DE, Ballard JD (2005) Clostridium difficile toxins: mechanism of action and role in disease. Clin Microbiol Rev 18:247–263
59. Yutin N, Galperin MY (2013) A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ Microbiol 15:2631–2641