Abstract
Mono-ADP-ribosylation is the enzymatic transfer of ADP-ribose from NAD+ to acceptor proteins catalyzed by ADP-ribosyltransferases. Using m-aminophenylboronate affinity chromatography, 2D-gel electrophoresis, in-gel digestion and MALDI-TOF analysis we have identified eight in vitro ADP-ribosylated proteins in Streptomyces coelicolor, which can be classified into three categories: (i) secreted proteins; (ii) metabolic enzymes using NAD+/NADH or NADP+/NADPH as coenzymes; and (iii) other proteins. The secreted proteins could be classified into two functional categories: SCO2008 and SCO5477 encode members of the family
of periplasmic extracellular solute-binding proteins, and SCO6108 and SCO1968 are secreted hydrolases. Dehydrogenases are encoded by SCO4824 and SCO4771. The other targets are GlnA (glutamine synthetaseI., SCO2198) and SpaA (starvation-sensing protein encoded by SCO7629). SCO2008 protein and GlnA had been identified as ADP-ribosylated proteins in previous studies. With these results we provided experimental support for a previous suggestion that ADP-ribosylation may regulate membrane transport and localization of periplasmic proteins. Since ADP-ribosylation results in inactivation of the target protein, ADP-ribosylation of dehydrogenases might modulate crucial primary metabolic pathways in Streptomyces. Several of the proteins identified here could provide a strong connection between protein ADP-ribosylation and the regulation of morphological differentiation in S. coelicolor.
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- Heterologous overproduction of oviedomycin by refactoring biosynthetic gene cluster and metabolic engineering of host strain Streptomyces coelicolor
Boncheol Gu, Duck Gyun Kim, Do-Kyung Kim, Minji Kim, Hyun Uk Kim, Min-Kyu Oh
Microbial Cell Factories.2023;[Epub] CrossRef - Streptomyces coelicolor macrodomain hydrolase SCO6735 cleaves thymidine-linked ADP-ribosylation of DNA
Andrea Hloušek-Kasun, Petra Mikolčević, Johannes Gregor Matthias Rack, Callum Tromans-Coia, Marion Schuller, Gytis Jankevicius, Marija Matković, Branimir Bertoša, Ivan Ahel, Andreja Mikoč
Computational and Structural Biotechnology Journal.2022; 20: 4337. CrossRef - ADP-ribosylation systems in bacteria and viruses
Petra Mikolčević, Andrea Hloušek-Kasun, Ivan Ahel, Andreja Mikoč
Computational and Structural Biotechnology Journal.2021; 19: 2366. CrossRef - ADP‐ribosylation: new facets of an ancient modification
Luca Palazzo, Andreja Mikoč, Ivan Ahel
The FEBS Journal.2017; 284(18): 2932. CrossRef - Characterization of DNA Binding Sites of RokB, a ROK-Family Regulator from Streptomyces coelicolor Reveals the RokB Regulon
Paulina Bekiesch, Karl Forchhammer, Alexander Kristian Apel, Marie-Joelle Virolle
PLOS ONE.2016; 11(5): e0153249. CrossRef - Disruption of Macrodomain Protein SCO6735 Increases Antibiotic Production in Streptomyces coelicolor
Jasna Lalić, Melanija Posavec Marjanović, Luca Palazzo, Dragutin Perina, Igor Sabljić, Roko Žaja, Thomas Colby, Bruna Pleše, Mirna Halasz, Gytis Jankevicius, Giselda Bucca, Marijan Ahel, Ivan Matić, Helena Ćetković, Marija Luić, Andreja Mikoč, Ivan Ahel
Journal of Biological Chemistry.2016; 291(44): 23175. CrossRef - NAD+-specific glutamate dehydrogenase (EC.1.4.1.2) in Streptomyces coelicolor; in vivo characterization and the implication for nutrient-dependent secondary metabolism
Songhee H. Kim, Byung-Gee Kim
Applied Microbiology and Biotechnology.2016; 100(12): 5527. CrossRef - Macrodomains: Structure, Function, Evolution, and Catalytic Activities
Johannes Gregor Matthias Rack, Dragutin Perina, Ivan Ahel
Annual Review of Biochemistry.2016; 85(1): 431. CrossRef - Transcriptomic Analysis of Liquid Non-Sporulating Streptomyces coelicolor Cultures Demonstrates the Existence of a Complex Differentiation Comparable to That Occurring in Solid Sporulating Cultures
Paula Yagüe, Antonio Rodríguez-García, María Teresa López-García, Beatriz Rioseras, Juan Francisco Martín, Jesús Sánchez, Angel Manteca, Ken Mills
PLoS ONE.2014; 9(1): e86296. CrossRef - ADP-ribosylation of guanosine by SCO5461 protein secreted from Streptomyces coelicolor
Tsuyoshi Nakano, Yuko Matsushima-Hibiya, Masafumi Yamamoto, Azusa Takahashi-Nakaguchi, Hirokazu Fukuda, Masaya Ono, Takeji Takamura-Enya, Haruyasu Kinashi, Yukari Totsuka
Toxicon.2013; 63: 55. CrossRef - 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
Krisztina Szirák, Judit Keserű, Sándor Biró, Iván Schmelczer, György Barabás, András Penyige
Journal of Microbiology.2012; 50(3): 409. CrossRef