Growth-dependent release of carbohydrate metabolism-related and antioxidant enzymes from Staphylococcus aureus strain 6 as determined by proteomic analysis

Donenko,F. V.; Gruber,I. M.; Semenova,I. B.; Priyatkin,R. G.; Ziganshin,R. H.; Zaryadyeva,E. A.; Ignatova,O. M.; Kurbatova,E. A.; Kiselevsky,M. V.; Efferth,T.

doi:10.3892/etm.2011.346

Growth-dependent release of carbohydrate metabolism-related and antioxidant enzymes from Staphylococcus aureus strain 6 as determined by proteomic analysis

Authors:
- F. V. Donenko
- I. M. Gruber
- I. B. Semenova
- R. G. Priyatkin
- R. H. Ziganshin
- E. A. Zaryadyeva
- O. M. Ignatova
- E. A. Kurbatova
- M. V. Kiselevsky
- T. Efferth
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Affiliations: Cell Immunity Laboratory, N.N. Blokhin Russian Cancer Research Center, Russian Academy of Medical Science, Moscow 1115478, Russia, Mechnikov Research Institute for Vaccine and Sera, Russian Academy of Medical Science, Moscow 1115478, Russia, Shemyakin-Ovchinnikov Institute for Bioorganic Chemistry, Russian Academy of Science, Moscow, Russia, Department of Pharmaceutical Biology, Institute of Pharmaceutical Biology, University of Mainz, Mainz, Germany
Published online on: September 1, 2011 https://doi.org/10.3892/etm.2011.346
Pages: 1199-1204

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Abstract

Proteins released into the culture medium by Staphylococcus aureus (S. aureus) strain 6 were determined at the end of the exponential growth phase (4.5 h). Eleven proteins were identified by liquid chromatography coupled with mass spectrometry. Three proteins were predicted to have signal peptides indicating their extracellular localization. The other proteins were presumably located in the cytoplasm of the bacteria. Five out of the 11 proteins were involved in carbohydrate metabolism. Other intracellular proteins of S. aureus were not detected in the culture medium. This indicates that the release of these 11 proteins was specific and that unspecific protein release due to damaged or dying bacteria did not play a role. It is suggested that enzymes associated with carbohydrate metabolism may provide the energy necessary for the transition of bacteria from a resting to a proliferative state. Another enzyme released by S. aureus, superoxide dismutase, may catalyze redox reactions in this context. The production of other proteolytic enzymes and toxins may take place at later stages of bacterial growth. A cocktail of these 11 proteins was used for the immunization of mice. Indeed, vaccination with these proteins prolonged the survival times of mice upon infection with S. aureus strain 6. Therefore, these proteins may have implications for the development of novel strategies for the prevention and therapy of S. aureus infections.

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1	Trishin AV, Donenko FV, Kurbatova EA, Voyushin KE, Kiselevsky MV, Egorova NB, Gruber IM, Semenova IB and Semenov BF: Protective activity of secreted proteins of Streptococcus pneumoniae and Klebsiella pneumoniae. Zh Microbiol. 4:46–50. 2008.PubMed/NCBI
2	Jones RC, Deck J, Edmondson RD and Hart ME: Relative quantitative comparisons of the extracellular protein profiles of Staphylococcus aureus UAMS-1 and its sarA, agr, and sarA agr regulatory mutants using 1D-PAGE and nanocapillary LC coupled with tandem MS. J Bacteriol. 190:5265–5278. 2008.PubMed/NCBI
3	Burlak C, Hammer CH, Robinson MA, Whitney AR, McGavin MJ, Kreiswirth BN and Deleo FR: Global analysis of community-associated methicillin-resistant Staphylococcus aureus exoproteins reveals molecules produced in vitro and during infection. Cell Microbiol. 9:1172–1190. 2007. View Article : Google Scholar : PubMed/NCBI
4	Sibbald MJ, Ziebandt AK, Engelmann S, Hecker M, de Jong A, Harmsen HJ, Raangs GC, Stokroos I, Arends JP, Dubois JY and van Dijl JM: Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol Mol Biol Rev. 70:755–788. 2006. View Article : Google Scholar : PubMed/NCBI
5	Egorova NB and Korzaya LI: The effect of repeated administration of staphylococcal immune preparations on the development of local staphylococcal infection in mice. J Hyg Epidemiol Microbiol Immunol. 27:203–210. 1983.PubMed/NCBI
6	Kuzmenko OM, Zlygostev SA, Mikhaylova NA, Gruber IM, Akhmatova NK, Kurbatova EA and Cherkasova LS: Characteristics of antigenic complexes of Staphylococcus aureus vaccine strains obtained in different cultivation conditions. Zh Microbiol. 2:51–54. 2010.PubMed/NCBI
7	Donenko FV, Sitdikova SM, Syrtsev AV, Gradyushko AT, Kiselevsky MV, Serebryakova MV and Efferth T: Hemoglobin-associated proteins isolated from blood serum of Ehrlich carcinoma-bearing mice. Int J Oncol. 32:885–893. 2008.PubMed/NCBI
8	Laemmli UK: Cleavage of structural proteins during the assembly of head of bacteriophage T4. Nature. 227:680–685. 1970. View Article : Google Scholar : PubMed/NCBI
9	Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem. 72:248–254. 1976. View Article : Google Scholar : PubMed/NCBI
10	Gardy JL, Laird MR, Chen F, Rey S, Walsh CJ, Ester M and Brinkman FSL: PSORTb v. 2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics. 21:617–623. 2005. View Article : Google Scholar
11	The UniProt Consortium: The universal protein resource (UniProt). Nucleic Acids Res. 35:D193–D197. 2007.
12	Hattori M, Miyakawa S, Ohama Y, Kawamura H, Yoshida T, To-o K, Kuriki T and Takahashi K: Reduced immunogenicity of beta-lactoglobulin by conjugation with acidic oligosaccharides. J Agric Food Chem. 52:4546–4553. 2004. View Article : Google Scholar : PubMed/NCBI
13	Clements MO, Watson SP and Foster SJ: Characterisation of the major superoxide dismutase of Staphylococcus aureus and its role in starvation survival, stress resistance, and pathogenicity. J Bacteriol. 181:3898–3903. 1999.PubMed/NCBI
14	Nakano M, Kawano Y, Kawagish M, Hasegawa T, Iinuma Y and Oht M: Two-dimensional analysis of exoproteins of methicillin-resistant Staphylococcus aureus (MRSA) for possible epidemiological applications. Microbiol Immunol. 46:11–22. 2002. View Article : Google Scholar : PubMed/NCBI
15	Du Plessis EM, Theron J, Joubert L, Lotter T and Watson TG: Characterization of a phosphatase secreted by Staphylococcus aureus strain 154, a new member of the bacterial class C family of nonspecific acid phosphatases. Syst Appl Microbiol. 25:21–30. 2002.PubMed/NCBI
16	Alexeyev MF and Winkler HH: Complete replacement of basic amino acid residues with cysteines in Rickettsia prowazekii ATP/ADP translocase. Biochim Biophys Acta. 1565:1362002. View Article : Google Scholar : PubMed/NCBI
17	Ziebandt AK, Becher D, Ohlsen K, Hacker J, Hecker M and Engelmann S: The influence of agr and sigmaB in growth phase dependent regulation of virulence factors in Staphylococcus aureus. Proteomics. 4:3034–3047. 2004. View Article : Google Scholar : PubMed/NCBI
18	Mohan V, Unnikrishnan R, Thomas N, Bhansali A, Wangnoo SK and Thomas K: Pneumococcal infections and immunization in diabetic patients. J Postgrad Med. 57:78–81. 2011. View Article : Google Scholar : PubMed/NCBI
19	Abdullah ZS, Khan MU, Kodali SK and Javaid A: Pyomyositis mimicking osteomyelitis detected by SPET/CT. Hell J Nucl Med. 13:277–279. 2010.PubMed/NCBI
20	King JT, Goulet JL, Perkal MF and Rosenthal RA: Glycemic control and infections in patients with diabetes undergoing noncardiac surgery. Ann Surg. 253:158–165. 2011. View Article : Google Scholar : PubMed/NCBI
21	Heiden MGV, Plas DR, Rathmell JC, Harris MH and Thompson CB: Growth factors can influence cell growth and survival though effects on glucose metabolism. Mol Cell Biol. 21:5899–5912. 2001. View Article : Google Scholar : PubMed/NCBI