Identification, activity and disulfide connectivity of C-di- GMP regulating proteins in Mycobacterium tuberculosis

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Gupta, Kajal ^a   Kumar, Prasun ^a   Chatterji, Dipankar ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BIS (3',5') CYCLIC DIMERIC GUANOSINE MONOPHOSPHATE; CYCLIC GMP; CYSTEINE; DIGUANYLATE CYCLASE; IODOACETAMIDE; PHOSPHODIESTERASE; UNCLASSIFIED DRUG; BIS(3',5') CYCLIC DIGUANYLIC ACID; BIS(3',5')-CYCLIC DIGUANYLIC ACID; DISULFIDE; DRUG DERIVATIVE; ESCHERICHIA COLI PROTEIN; LYASE;

ALKYLATION; AMINO ACID ANALYSIS; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVITY; IN VITRO STUDY; MASS SPECTROMETRY; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN STABILITY; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; ENZYMOLOGY; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MICROBIAL VIABILITY; MUTATION; PROTEIN TERTIARY STRUCTURE; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BLOTTING, WESTERN; CIRCULAR DICHROISM; CYCLIC GMP; CYSTEINE; DISULFIDES; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; MICROBIAL VIABILITY; MODELS, MOLECULAR; MUTATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORUS-OXYGEN LYASES; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 78649800745     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015072     Document Type: Article

References (60)

1. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Ann Rev Microbiol 55: 165-99.
2. Redfield JR (2002) Is quorum sensing a side effect of diffusion sensing? Trends in Microbiol 10: 365-70.
3. Tamayo R, Pratt JT, Camilli A (2007) Roles of cyclic diguanlylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61: 131-48.
4. Jenal U (2004) Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr Opin Micorbiol: 185-91.
5. Guo YL, Seebacher T, Kurz U, Linder JU, Schultz JE (2001) Adenylyl cyclase Rv1625c of Mycobacterium tuberculosis: a progenitor of mammalian adenylyl cyclases. EMBO J 20: 3667-75.
6. Avarbock A, Avarbock D, The JS, Buckstein M, Wang Z, et al. (2005) Functional regulation of the opposing (p)ppGpp synthethase/hydrolase activities of RelMtb from Mycobacterium tuberculosis. Biochem 44: 9913-23. 20.
7. Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, et al. (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325: 279-81.
8. Weinhouse H, Sapir S, Amikam D, Shilo V, Volman G, et al. (1997) C-di GMPbinding protein, anew factor regulatory cellulose synthesis in Acetobacter xylinum. FEBS Lett 416: 207-11.
9. Jenal U, Malone J (2006) Mechanisms of Cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40: 385-07.
10. Sudarshan N, Lee ER, Weinberg Z, Moy RH, Kim JN, et al. (2008) Riboswitches in Eubacteria sense the second messenger cyclic di-GMP. Science 321: 411-13.
11. Ryan RP, Yvonne F, Jean FL, Lisa CC, Stephen S, et al. (2006) Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci USA 103: 6712-17.
12. Ryjenkow 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: 1972-78.
13. Galperin MY (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: Bacterial IQ, extroverts and introverts. BMC Micorobiol, doi:10.1186/1471-2180-5-35.
14. Regine H (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Micorbiol, 7: 263-73.
15. Tischler AD, Camilli A (2005) Cyclic Diguanylate regulates Vibrio cholerae Virulence gene expression. Infect Immun 73: 5873-82.
16. Hisert KB, MacCoss M, Shiloh MU, Darwin KH, Singh S (2005) A glutamatealanine- leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defense and killing of macrophages: role of cyclic di GMP. Mol Microbiol 56: 1234-45.
17. Kumar M, Chatterji D (2008) C-di-GMP a second messenger required for long term survival, but not for biofilm formation in Mycobacterium smegmatis. Micorbiol 154: 2942-55.
18. Römling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57: 629-39.
19. Pesavento C, Hengge R (2009) Bacterial nucleotide-based second messengers. Curr Opin Micorbiol 12: 1-7.
20. Simm R, Morr M, Kadar A, Nimtz M, Romling U (2004) GGDEF and EAL domains inversely regulate cyclic-di-GMP levels and transition from sensibility to motility. Mol Micorbiol 53: 1123-34.
21. Hisert KB, MacCoss M, Shiloh MU, Darwin KH, Singh S, et al. (2005) A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defense and killing of macrophages: role of cyclic di GMP. Mol Microbiol 56: 1234-45.
22. Kulesekara H, Lee V, Brencic A, Liberati N, Urbach J (2006) Analysis of Pseudomonas aeruginosa Diguanylate Cyclases and Phosphodiesterases Reveals a Role for Bis-(39-59)- Cyclic-GMP in Virulence. Proc Natl Acad Sci USA 103: 2839-44. 22.
23. Holland LM, Sinéad TO'D, Ryjenkov DA, Gomelsky L, Slater SR, et al. (2008) A Staphylococcal GGDEF domain protein regulates biofilm formation independently of cyclic dimeric GMP. J Bacteriol 190: 5178-89.
24. Shang F, Xue T, Sun H, Xing L, Zhang S (2009) The Staphylococcus aureus GGDEF domain-containing protein, GdpS, influences protein A gene expression in a cyclic diguanylic acid-independent manner. Infect Immun 77: 2849-56.
25. Dutton RJ, Boyd D, Berkem M, Beckwith J (2008) Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc Natl Acad Sci USA 105: 11933-38.
26. Gorman JJ, Wallis TP, Pitt JJ (2002) Protein disulfide bond determination by Mass Spectrometry. Mass Spectrom Rev 21: 183-216.
27. Wu J, Watson JT (1997) A novel methodology for assignment of disulfide bond pairings in protein. Protein Sci 6: 391-95.
28. Yen T-Y, Joshi RK, Hui Y, Seto NOL, Palcic MM, et al. (2000) Characterization of cysteine residues and disulfide bonds in proteins by liquid chromatography/electrospray ionization tandem mass spectrometry. J Mass Spectrom 35: 990-02.
29. Lu CH, Chen YC, Yu CS, Hwang JK (2007) Predicting disulfide connectivity patterns. Proteins: Structure Function and Bioinformatics 67: 262-270.
30. Bernardez Clark ED, Schwartz E, Rudolph R (1999) Inhibition of aggregation side reactions during in vitro protein folding. Methods Enzymol 309: 217-36.
31. Takagi T, Kubo K (1997) Sodium dodecyl sulfate-protein polypeptide complexes in 8M urea with special reference to sodium dodecyl sulfatepolyacrylamide gel electrophoresis. Biochem Biophys Acta 578: 68-75.
32. Paul R, Weiser S, Amiot NC, Chan C, Schirmer T (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Gen Dev 18: 715-27.
33. Boeckmann B, Bairoch A, Apweiler R, Blatter MC, Estreicher A, et al. (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL. Nucl Acids Res 31: 365-370.
34. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
35. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25: 3389-3402.
36. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. ClustalW and ClustalX version 2. Bioinformatics 2007 23(21): 2947-2948.
37. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The protein data bank. Nucl Acids Res 28: 235-242.
38. Sali A, Blundell TL (1993) Comparative protein modeling by satisfaction of spatial restrains. J Mol Biol 234: 779-815.
39. Kelley LA, Sternberg MJE (2009) Protein structure prediction on the web: a case study using the Phyre server. Nature Protocols 4: 363-371.
40. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE (2005) GROMACS: fast, flexible, and free. J Comput Chem 26: 1701-18.
41. Jorgensen WL, Tirado-Rives J (1988) The OPLS Force Field for Proteins. Energy minimizations for crystals of cyclic peptides and crambin. J Am Chem Soc 110: 1657-1666.
42. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK - a program to check the stereochemical quality of protein structures. J Ap Cryst 26: 283-291.
43. Eisenberg D, Lüthy R, Bowie JU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277: 396-404.
44. Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucl Acids Res 35: W407-W410.
45. The PyMOL Molecular Graphics System, Version 1.2r3pre, Schrödinger, LLC.
46. Finn RD, Mistry J, Tate J, Coggill C, Heger A, et al. (2010) The Pfam protein families database. Nucl Acids Res Database Issue 38: D211-222.
47. Deng WP, Nickoloff JA (1992) Site directed mutagenesis of virtually any plasmid by eliminating a unique site. Anal Biochem 200: 81-88.
48. Barik S (1996) Site directed mutagenesis in vitro by megaprimer PCR. Methods Mol Biol 57: 203-15.
49. Steen H, Mann M (2004) The ABC's (and XYZ's) of peptide sequencing. Nat Rev Cell Biol 5: 699-11.
50. Mormaan M, Eble J, Schwoppe C, Mesters R, Berdel W (2008) Fragmentation of intra peptide and inter peptide disulfide bonds of proteolytic peptides by nano ESI collision induced dissociation. Anal Bioannal Chem 392: 831-838.
51. 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.
52. Rao F, Yang Y, Qi Y, Liang ZX (2008) Catalytic mechanism of cyclic di-GMPspecific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J Bacteriol 190: 3622-3631.
53. Heinig M, Frishman D (2004) STRIDE: a Web server for secondary structure assignment known atomic coordinates of proteins. Nucl Acids Res 32: W500-2.
54. McDonald IK, Thornton JM (1994) Satisfying Hydrogen Bonding Potential in Proteins. JMB 238: 777-793.
55. Collaborative Computational Project, Number 4 (1994) "The CCP4 Suite: Programs for Protein Crystallography". Acta Cryst D50: 760-763.
56. Tal R, Wong HC, Calhoon R, Gelfand D, Fear AL etal(1998) Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinus; genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180: 4416-25.
57. Salona C, Garcia B, Latasa C, Arana-Toldea A, Zorraquiano V, et al. (2009) Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-di-GMP signaling network in Salmonella. Proc Natl Acad Sci USA 106: 7997-02.
58. Kulasekara H, Lee V, Brencic A, Liberation N, Urbach J, et al. (2006) Analysis of Pseudomonas aeruginosa, diguanylate cyclases and phosphodiesterase reveals a role forbis-(39-59)-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103: 2839-44.
59. Tarutina M, Ryienkov DA, Gomelsky M (2006) An unorthodox bacteriophytochrome from Rhodobacter sphaeroides involved in turnover of the second messenger c-di-GMP. J Biol Chem 281: 34751-58.
60. Ferreira RB, Antunes LC, Greenberg EP, McCarter LL (2008) Vibrio parahaemolyticus ScrC modulates c-di-GMP regualtion of gene expression relevant to growth on surfaces. J Bacteriol 2008; 190: 851-60.