Disruption of macrodomain protein SCO6735 increases antibiotic production in streptomyces coelicolor

Journal of Biological Chemistry

Volumn 291, Issue 44, 2016, Pages 23175-23187

  Lalić, Jasna ^a   Marjanović, Melanija Posavec ^a   Palazzo, Luca ^b   Perina, Dragutin ^a   Sabljić, Igor ^a   Žaja, Roko ^a,b   Colby, Thomas ^c   Pleše, Bruna ^a   Halasz, Mirna ^a   Jankevicius, Gytis ^b   Bucca, Giselda ^d   Ahel, Marijan ^a   Matič, Ivan ^c   Četković, Helena ^a   Luić, Marija ^a   Mikoç, Andreja ^a   Ahel, Ivan ^b  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

^d UNIVERSITY OF BRIGHTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIA; CHEMICAL MODIFICATION; CRYSTAL STRUCTURE; HYDROLYSIS;

ADP-RIBOSYLATION; ANTIBIOTIC PRODUCTION; CELLULAR FUNCTION; CELLULAR PROCESS; PHYSICAL AND CHEMICAL PROPERTIES; POST-TRANSLATIONAL MODIFICATIONS; STREPTOMYCES COELICOLOR; STRUCTURAL DOMAINS;

PROTEINS;

BACTERIAL PROTEIN; SCO6735 PROTEIN; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSE; ANTIINFECTIVE AGENT;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DAMAGE; MOLECULAR PHYLOGENY; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN PROCESSING; SEQUENCE ALIGNMENT; STREPTOMYCES COELICOLOR; BIOSYNTHESIS; CHEMISTRY; GENETICS; METABOLISM;

ADENOSINE DIPHOSPHATE RIBOSE; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DNA DAMAGE; PROTEIN PROCESSING, POST-TRANSLATIONAL; STREPTOMYCES COELICOLOR;

EID: 84994036024     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.721894     Document Type: Article

References (76)

1. Barkauskaite, E., Jankevicius, G., and Ahel, I. (2015) Structures and mechanisms of enzymes employed in the synthesis and degradation of PARPdependent protein ADP-ribosylation. Mol. Cell 58, 935-946
2. Vyas, S., Matic, I., Uchima, L., Rood, J., Zaja, R., Hay, R. T., Ahel, I., and Chang, P. (2014) Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun. 5, 4426
3. Gibson, B. A., and Kraus, W. L. (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell Biol. 13, 411-424
4. Corda, D., and Di Girolamo, M. (2003) Functional aspects of protein mono-ADP-ribosylation. EMBO J. 22, 1953-1958
5. Hawse, W. F., and Wolberger, C. (2009) Structure-based mechanism of ADP-ribosylation by sirtuins. J. Biol. Chem. 284, 33654-33661
6. Slade, D., Dunstan, M. S., Barkauskaite, E., Weston, R., Lafite, P., Dixon, N., Ahel, M., Leys, D., and Ahel, I. (2011) The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 477, 616-620
7. Sharifi, R., Morra, R., Appel, C. D., Tallis, M., Chioza, B., Jankevicius, G., Simpson, M. A., Matic, I., Ozkan, E., Golia, B., Schellenberg, M. J., Weston, R., Williams, J. G., Rossi, M. N., Galehdari, H., et al. (2013) Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. EMBO J. 32, 1225-1237
8. Jankevicius, G., Hassler, M., Golia, B., Rybin, V., Zacharias, M., Timinszky, G., and Ladurner, A. G. (2013) A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nat. Struct. Mol. Biol. 20, 508-514
9. Rosenthal, F., Feijs, K. L., Frugier, E., Bonalli, M., Forst, A. H., Imhof, R., Winkler, H. C., Fischer, D., Caflisch, A., Hassa, P. O., L?scher, B., and Hottiger, M. O. (2013) Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nat. Struct. Mol. Biol. 20, 502-507
10. PMikoč, A., Ahel, J., Ćetković, H. T., Ẑaja, R., and Ahel, I. (2014) Distribution of protein poly(ADP-ribosyl)ation systems across all domains of life. DNA Repair 23, 4-16
11. Till, S., and Ladurner, A. G. (2009) Sensing NAD metabolites through macro domains. Front. Biosci. 14, 3246-3258
12. Rack, J. G., Perina, D., and Ahel, I. (2016) Macrodomains: structure, function, evolution, and catalytic activities. Annu. Rev. Biochem. 85, 2.1-2.24
13. Takada, T., Iida, K., and Moss, J. (1993) Cloning and site-directed mutagenesis of human ADP-ribosylarginine hydrolase. J. Biol. Chem. 268, 17837-17843
14. Koh, D. W., Lawler, A. M., Poitras, M. F., Sasaki, M., Wattler, S., Nehls, M. C., Stöger, T., Poirier, G. G., Dawson, V. L., and Dawson, T. M. (2004) Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc. Natl. Acad. Sci. U.S.A. 101, 17699-17704
15. Feijs, K. L., Forst, A. H., Verheugd, P., and Luscher, B. (2013) Macrodomain-containing proteins: regulating new intracellular functions of mono(ADP-ribosyl)ation. Nat. Rev. Mol. Cell Biol. 14, 542-542
16. Holbourn, K. P., Shone, C. C., and Acharya, K. R. (2006) A family of killer toxins: exploring the mechanism of ADP-ribosylating toxins. FEBS J. 273, 4579-4593
17. Moure, V. R., Costa, F. F., Cruz, L. M., Pedrosa, F. O., Souza, E. M., Li, X. D., Winkler, F., and Huergo, L. F. (2015) Regulation of nitrogenase by reversible mono-ADP-ribosylation. Curr. Top. Microbiol. Immunol. 384, 89-106
18. Eastman, D., and Dworkin, M. (1994) Endogenous ADP-ribosylation during development of the prokaryote Myxococcus xanthus. Microbiology 140, 3167-3176
19. Hildebrandt, K., Eastman, D., and Dworkin, M. (1997) ADP-ribosylation by the extracellular fibrils of Myxococcus xanthus. Mol. Microbiol. 23, 231-235
20. Serres, M. H., and Ensign, J. C. (1996) Endogenous ADP-ribosylation of proteins in Mycobacterium smegmatis. J. Bacteriol. 178, 6074-6077
21. Huh, J. W., Shima, J., and Ochi, K. (1996) ADP-ribosylation of proteins in Bacillus subtilis and its possible importance in sporulation. J. Bacteriol. 178, 4935-4941
22. Ochi, K., Penyige, A., and Barabas, G. (1992) The possible role of ADPribosylation in sporulation and streptomycin production by Streptomyces griseus. J. Gen. Microbiol. 138, 1745-1750
23. Penyige, A., Deák, E., Kálmánczhelyi, A., and Barabás, G. (1996) Evidence of a role for NAD ? -glycohydrolase and ADP-ribosyltransferase in growth and differentiation of Streptomyces griseus NRRL B-2682: inhibition by m-aminophenylboronic acid. Microbiology 142, 1937-1944
24. Shima, J., Penyige, A., and Ochi, K. (1996) Changes in patterns of ADPribosylated proteins during differentiation of Streptomyces coelicolor A3(2) and its developmental mutants. J. Bacteriol. 178, 3785-3790
25. Penyige, A., Keseru, J., Fazakas, F., Schmelczer, I., Szirák, K., Barabás, G., and Birá, S. (2009) Analysis and identification of ADP-ribosylated proteins of Streptomyces coelicolor M145. J. Microbiol. 47, 549-556
26. Penyige, A., Vargha, G., Ensign, J. C., and Barabás, G. (1992) The possible role of ADP ribosylation in physiological regulation of sporulation in Streptomyces griseus. Gene 115, 181-185
27. Pallen, M. J., Lam, A. C., Loman, N. J., and McBride, A. (2001) An abundance of bacterial ADP-ribosyltransferases: implications for the origin of exotoxins and their human homologues. Trends Microbiol. 9, 302-307
28. Nakano, T., Matsushima-Hibiya, Y., Yamamoto, M., Takahashi-Nakaguchi, A., Fukuda, H., Ono, M., Takamura-Enya, T., Kinashi, H., and Totsuka, Y. (2013) ADP-ribosylation of guanosine by SCO5461 protein secreted from Streptomyces coelicolor. Toxicon 63, 55-63
29. Ahel, D., Horejsí, Z. , Wiechens, N. , Polo, S. E. , Garcia-Wilson, E. , Ahel, I., Flynn, H., Skehel, M., West, S. C., Jackson, S. P., Owen-Hughes, T., and Boulton, S. J. (2009) Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325, 1240-1243
30. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D 60, 2256-2268
31. Peterson, F. C., Chen, D., Lytle, B. L., Rossi, M. N., Ahel, I., Denu, J. M., and Volkman, B. F. (2011) Orphan macrodomain protein (human C6orf130) is an O-acyl-ADP-ribose deacylase: solution structure and catalytic properties. J. Biol. Chem. 286, 35955-35965
32. Ahel, I., Vujaklija, D., Mikoc, A., and Gamulin, V. (2002) Transcriptional analysis of the recA gene in Streptomyces rimosus: identification of the new type of promoter. FEMS Microbiol. Lett. 209, 133-137
33. Gamulin, V., Cetkovic, H., and Ahel, I. (2004) Identification of a promoter motif regulating the major DNA damage response mechanism of Mycobacterium tuberculosis. FEMS Microbiol. Lett. 238, 57-63
34. Gust, B., Challis, G. L., Fowler, K., Kieser, T., and Chater, K. F. (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. U.S.A. 100, 1541-1546
35. Malpartida, F., and Hopwood, D. A. (1986) Physical and genetic characterization of the gene cluster for the antibiotic actinorhodin in Streptomyces coelicolor A3(2). Mol. Gen. Genet. 205, 66-73
36. Liu, G., Chater, K. F., Chandra, G., Niu, G., and Tan, H. (2013) Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol. Mol. Biol. Rev. 77, 112-143
37. Szirák, K. , Keseru, J. , Biró, S. , Schmelczer, I., Barabás, G., and Penyige, A. (2012) Disruption of SCO5461 gene coding for a mono-ADP-ribosyltransferase enzyme produces a conditional pleiotropic phenotype affecting morphological differentiation and antibiotic production in Streptomyces coelicolor. J. Microbiol. 50, 409- 418
38. Barkauskaite, E., Jankevicius, G., Ladurner, A. G., Ahel, I., and Timinszky, G. (2013) The recognition and removal of cellular poly(ADP-ribose) signals. FEBS J. 280, 3491-3507
39. Liu, Y., Zhou, J., Omelchenko, M. V., Beliaev, A. S., Venkateswaran, A., Stair, J., Wu, L., Thompson, D. K., Xu, D., Rogozin, I. B., Gaidamakova, E. K., Zhai, M., Makarova, K. S., Koonin, E. V., and Daly, M. J. (2003) Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc. Natl. Acad. Sci. U.S.A. 100, 4191-4196
40. Kim, T., Lee, J., and Kim, K. S. (2013) Escherichia coli YmdB regulates biofilm formation independently of its role as an RNase III modulator. BMC Microbiol. 13, 266
41. Sugawara, K., Dohmae, N., Kasai, K., Saido-Sakanaka, H., Okamoto, S., Takio, K., and Ochi, K. (2002) Isolation and identification of novel ADPribosylated proteins from Streptomyces coelicolor A3(2). Biosci. Biotechnol. Biochem. 66, 2292-2296
42. Aguiar, R. C., Takeyama, K., He, C., Kreinbrink, K., and Shipp, M. A. (2005) B-aggressive lymphoma family proteins have unique domains that modulate transcription and exhibit poly(ADP-ribose) polymerase activity. J. Biol. Chem. 280, 33756-33765
43. Kustatscher, G., Hothorn, M., Pugieux, C., Scheffzek, K., and Ladurner, A. G. (2005) Splicing regulates NAD metabolite binding to histone macroH2A. Nat. Struct. Mol. Biol. 12, 624-625
44. Tallis, M., Morra, R., Barkauskaite, E., and Ahel, I. (2014) Poly(ADP-ribosyl)ation in regulation of chromatin structure and the DNA damage response. Chromosoma 123, 79-90
45. Golia, B., Singh, H. R., and Timinszky, G. (2015) Poly-ADP-ribosylation signaling during DNA damage repair. Front. Biosci. (Landmark) 20, 440-457
46. Stallings, C. L., Chu, L., Li, L. X., and Glickman, M. S. (2011) Catalytic and non-catalytic roles for the mono-ADP-ribosyltransferase Arr in the mycobacterial DNA damage response. PLoS One 6, e21807
47. Stonesifer, J., and Baltz, R. H. (1985) Mutagenic DNA repair in Streptomyces. Proc. Natl. Acad. Sci. U.S.A. 82, 1180-1183
48. Baltz, R. H., and Stonesifer, J. (1985) Mutagenic and error-free DNA repair in Streptomyces. Mol. Gen. Genet. 200, 351-355
49. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F., and Hopwood, D. A. (2000) Practical Streptomyces Genetics, John Innes Foundation, Norwich, UK
50. Pigac, J., and Schrempf, H. (1995) A simple and rapid method of transformation of Streptomyces rimosus R6 and other streptomycetes by electroporation. Appl. Environ. Microbiol. 61, 352-356
51. Redenbach, M., Kieser, H. M., Denapaite, D., Eichner, A., Cullum, J., Kinashi, H., and Hopwood, D. A. (1996) A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol. Microbiol. 21, 77-96
52. Gregory, M. A., Till, R., and Smith, M. C. (2003) Integration site for Streptomyces phage phi BT1 and development of site-specific integrating vectors. J. Bacteriol. 185, 5320-5323
53. Xiao, Y. H., and Pei, Y. (2011) Asymmetric overlap extension PCR method for site-directed mutagenesis. Methods Mol. Biol. 687, 277-282
54. Lambrecht, M. J., Brichacek, M., Barkauskaite, E., Ariza, A., Ahel, I., and Hergenrother, P. J. (2015) Synthesis of dimeric ADP-ribose and its structure with human poly(ADP-ribose) glycohydrolase. J. Am. Chem. Soc. 137, 3558-3564
55. Palazzo, L., Daniels, C. M., Nettleship, J. E., Rahman, N., McPherson, R. L., Ong, S. E., Kato, K., Nureki, O., Leung, A. K., and Ahel, I. (2016) ENPP1 processes protein ADP-ribosylation in vitro. FEBS J. 10.1111/febs.13811
56. Coze, F., Gilard, F., Tcherkez, G., Virolle, M. J., and Guyonvarch, A. (2013) Carbon-flux distribution within Streptomyces coelicolor metabolism: a comparison between the actinorhodin-producing strain M145 and its non-producing derivative M1146. PLoS One 8, e84151
57. Pfaffl, M. W. (2004) Quantification strategies in real-time PCR. In A-Z of quantitative PCR (Bustin, S. A., ed) pp. 87-112, International University Line, La Jolla, CA
58. Simon, P. (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19, 1439-1440
59. Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
60. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729
61. Abascal, F., Zardoya, R., and Posada, D. (2005) ProtTest: selection of bestfit models of protein evolution. Bioinformatics 21, 2104-2105
62. Posada, D., and Crandall, K. A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817-818
63. Whelan, S., and Goldman, N. (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691-699
64. Ronquist, F., and Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574
65. Simossis, V. A., and Heringa, J. (2005) PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Nucleic Acids Res. 33, W289-W294
66. Kabsch, W. (2010) XDS. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
67. Evans, P. R., and Murshudov, G. N. (2013) How good are my data and what is the resolution? Acta Crystallogr. D Biol. Crystallogr. 69, 1204-1214
68. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
69. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025
70. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., and Sternberg, M. J. (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845- 858
71. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
72. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
73. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
74. Palazzo, L., Thomas, B., Jemth, A. S., Colby, T., Leidecker, O., Feijs, K. L., Zaja, R., Loseva, O., Puigvert, J. C., Matic, I., Helleday, T., and Ahel, I. (2015) Processing of protein ADP-ribosylation by Nudix hydrolases. Biochem. J. 468, 293-301
75. Wiśniewski, J. R., Zougman, A., Nagaraj, N., and Mann, M. (2009) Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362
76. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372