Zholobak N. М.

ON THE MECHANISMS OF ANTIBACTERIAL AND PROBIOTIC EFFECT OF COLLOIDAL (NANO-SIZED) CERIUM DIOXIDE


About the author:

Zholobak N. М.

Heading:

LITERATURE REVIEWS

Type of article:

Scentific article

Annotation:

In this paper, we summarize the current data on biosecurity of nanocrystalline cerium dioxide (CeO2 NP) for environmental microorganisms, and on the probiotic effect of CeO2 NP. We analyze the possible ways of the interaction of nanoparticles with the bacterial cell, which provide the means of their probiotic and antibacterial action. The analysis of the probiotic and antibacterial action of CeO2 NP shows that gram-positive microorganisms are more susceptible to nanoparticles than gram-negative. It is related to different permeability and other functions of the bacterial wall of these two groups of microorganisms. The phosphoenolpyruvate: carbohydrate phosphotransferase system (PTS) plays a major role in the transportation of nutrients through the membrane. It provides selective transportation for glucose, fructose, and other carbohydrates in phosphorized form. PTS is one of the first systems of the cell that react on the contact with CeO2 NP. I. e., CeO2 NP can actively change the processes of the nutrients transportation. We concluded that the way CeO2 NP influence the metabolism of microorganisms depends on the ways they receive carbon and energy: auto/heterotrophs, photo/chemotrophs. These properties are mostly defined by the PTS of the bacteria, which serves as a regulator of the processes of consumption of carbon, nitrogen, and phosphates, influences chemotaxis, potassium transportation, and virulence of some pathogenic microorganisms. Signal transmission in the described regulatory processes depends on the phosphorylation of PTS components. It depends, in turn, on the substrates availability. Consequently, the selectivity of CeO2 NP's action on pathogenic and semi-pathogenic microorganisms can be easily explained. The microorganism’s quality of being pathogenic or semi-pathogenic to human is linked to auxotrophy – inability to synthesize carbohydrates, amino acids, and other grow factors (purines, pyrimidines, lipids, vitamins, ferroporphyrins, etc.), evolutional adaptation to receiving it from the environment or the host organism. Cerium has chemical values that resemble calcium. E.g., the ability to make phosphate-containing compounds. Thus, CeO2 NP can change the catalytic properties of phosphate anions when binding with them. Moreover, the dynamic of adsorption of phosphate on cerium oxide accorded with the classical model and can be described by the second-order kinetic equation. It means that CeO2 NP can affect the phosphate-mediated and phosphate-related metabolic intracellular processes, and can demonstrate the phosphatase activity. We found a correlation between the antibacterial action of CeO2 NP and the role of PTS in the sugars transportation for different groups of microorganisms. This correlation supports the idea that antibacterial effects of CeO2 NP depend on inhibition of bacteria’s PTS. Indeed, the maximal antibacterial effect of CeO2 NP is found for bacterias, for which PTS plays the key role in the sugars transportation. On the other hand, the probiotic effect of CeO2 NP can also be predicted basing on the activity of PTS in different groups of microorganisms. This system is typical for obligate and facultative anaerobes and is absent for aerobic bacteria. For bacteria that can synthesize sugars, and which live in aerobic condition, the nanoparticles have probiotic action by reducing the toxic effect of ROS that are actively produced in these conditions. Summarizing, we found out that the result of the interaction between CeO2 NP and microorganisms depends on physicochemical properties of the nanoparticles, and it is realized through the response of the bacterial cell. This response is influenced by the complex of cascade reactions that depends on the presence or absence of the outer membrane (gram-positive/negative bacteria), the features of the nutrients transportation system (the role of phosphotransferase system), the characteristics of the intracellular metabolism (hyperproduction of peroxides), and genetic activity. Basing on the mentioned properties, it is possible to predict the result of the interaction between the CeO2 NP and a microorganism.

Tags:

cerium dioxide nanoparticles (CeO2 NP), probiotic effect, antibacterial effect, phosphotransferase system, the mechanism of the action

Bibliography:

  • 1. Бабенко Л.П. Вплив наночастинок діоксиду церію на різні фізіологічні групи мікроорганізмів / Л.П. Бабенко, Л.А. Данкевич, Н.М. Жолобак [та ін.] // Наук. записки Терноп. нац. пед. ун-ту. Сер. Біол. – 2014. – № 3. – С. 45-51.
  • 2. Болдырев А.А. Биохимия мембран / Под ред. А.А. Болдырева. Кн. 1. Введение в биохимию мембран. – М.: Высш. школа. – 1986. – 112 с.
  • 3. Борисов Л.Б. Медицинская микробиология, вирусология, иммунология. Гл. 4. Физиология и биохимия микроорганизмов (бактерий) / Л.Б. Борисов. — М.: ООО «МИА» – 2005. – С. 46-67.
  • 4. Грецкий И.А. Photobacterium phosphoreum – объект для изучения биологических эффектов наночастиц диоксида церия / И.А. Грецкий, Н.М. Жолобак, А.Б. Щербаков [и др.] // Живые и биокосные системы. – 2016. – 15 (электронный ресурс – в печати).
  • 5. Жолобак Н.М. Антибактеріальні ефекти колоїдного (нанорозмірного) діоксиду церію / Н.М. Жолобак // Вісник проблем біології і медицини. – 2015. – Вип. 3, Том 2 (123). – С. 23-28.
  • 6. Жолобак Н.М. Ефективність застосування наночастинок колоїдного церію та L. bulgaricus у мишей / Н.М. Жолобак, Т.К. Журавська, І.І. Качмарська [та ін.] // Матеріали конф. «Довкілля та здоров’я», 14-16 квітня 2009, Тернопіль. – С. 32.
  • 7. Иванов В.К. Нанокристаллический диоксид церия: свойства, получение, применение / В.К. Иванов, А.Б. Щербаков, А.Е. Баранчиков, В.В. Козик. – Томск: Изд-во Том. ун-та, 2013. – 287 с.
  • 8. Лущак В.І. Оксидативний стрес у мікроорганізмів / В.І.Лущак // XII з’їзд товариства мікробіологів України ім. С.М. Виноградського, 25-30 травня 2009 р., Ужгород. Тези доп. – Ужгород : Патент, 2009. – С. 17.
  • 9. Щербаков А.Б. Нанокристаллический диоксид церия: перспективный материал для биомедицинского применения / А.Б. Щербаков, В.К. Иванов, Н.М. Жолобак [и др.] // Биофизика. — 2011. — Т. 56 (6). Р. 995-1015.
  • 10. Archibald F.S. Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria / F.S. Archibald, I. Fridovich // J. Bacteriol. – 1981. – Vol. 146, № 3. – P. 928-936.
  • 11. Babenko L.P. Antibacterial activity of cerium colloids against opportunistic microorganisms in vitro / L.P. Babenko, N.M. Zholobak, A.B. Shcherbakov [et al.] // Мікробіол. журн. — 2012. — 74 (3). — Р. 54-62.
  • 12. Babu K.S. Cytotoxicity and antibacterial activity of gold-supported cerium oxide nanoparticles / K.S. Babu, M. Anandkumar, T.Y. Tsai [et al.] // Int. J. Nanomedicine. – 2014. – Vol. 9. – P. 5515-5531.
  • 13. Beliaev A.S. Global transcriptome analysis of Shewanella oneidensis MR-1 exposed to different terminal electron acceptors / A.S. Beliaev, D.M. Klingeman, J.A. Klappenbach [et al.] // J. Bacteriol. – 2005. – Vol. 187. – P. 7138-7145.
  • 14. Celardo I. Pharmacological potential of cerium oxide nanoparticles / I. Celardo, J.Z. Pedersen, E. Traversa [et al.] // Nanoscale. – 2011. – Vol. 3 (4). – P. 1411-1420.
  • 15. Deutscher J. The bacterial phosphoenolpyruvate: carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions / J. Deutscher, F.M.D. Aké, M. Derkaoui [et al.] // MMBR. – 2014. — Vol. 78 (2). – P. 231-256.
  • 16. Garcia-Saucedo C. Low toxicity of CeO2 NP to the yeast Saccharomices cerevisiae / C. Garcia-Saucedo // J. of Hazardous Materials. – 2011. – Vol. 192. – P. 1572-1579.
  • 17. Gupta R.S. What are archaebacteria: life’s third domain or monoderm prokaryotes related to Gram-positive bacteria? A new proposal for the classification of prokaryotic organisms / R.S. Gupta // Molecular Microbiology. – 1998. – Vol. 29 (3). – P. 695-707.
  • 18. Gupta R.S. Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria and eukaryotes / R.S. Gupta // Microbiol. Mol. Biol. Rev. – 1998. – Vol. 62. – P. 1435-1491.
  • 19. http://en.wikipedia.org/wiki/Pseudomonas#Use_as_bioremediation_agents
  • 20. Ivanov V.K. Synthesis and thermal stability of nanocrystalline ceria sols stabilized by citric and polyacrylic acids / V.K. Ivanov, J.S. Polezhaeva, A.S. Shaporev [et al.] // Rus. J. Inorg. Chem. — 2010. — 55. Р. 328.
  • 21. Kroth Т. Einfluss von Seltenen Erden auf die scheinbare Verdaulichkeit der Rohnährstoffe bei wachsenden Ratten / Т. Kroth. — Inaugural-Dissertation zur Erlangung der tiermedizinischen Doktorwürde der Tierärztlichen Fakultät der Ludwig-Maximilians-Universität München, 2011. – 97 р.
  • 22. Kuchma M.H. Phosphate ester hydrolysis of biologically relevant molecules by cerium oxide nanoparticles / M.H. Kuchma, C.B. Komanski, J. Colon [et al.] // Nanomedicine: Nanotech. Biol. Med. – 2010. – Vol. 6. – P. 738-744.
  • 23. Lal P. Exopolysaccharide analysis of biofilm-forming Candida albicans / P. Lal, D. Sharma, P. Pruthi [et al.] // Journal of applied microbiology. – 2010. – Vol. 109 (1). – P. 128-136.
  • 24. Li B. Adsorption kinetics of phosphate on ceria-based adsorbent / B. Li, H.B. Wang, Y. Yuan // Advanced Materials Research. – 2013. – Vols. 726-731. – P. 1668-1672.
  • 25. Marty-Teysset C. Increased production of hydrogen peroxide by Lactobacillus delbrueckii subsp. bulgaricus upon aeration: Involvement of an NADH oxidase in oxidative stress / C. Marty-Teysset, F. de la Torre, J.R. Garel // Appl. Environ. Microbiol. – 2000. – Vol. 66, № 1. – P. 262-267.
  • 26. Najam-ul-Haqa M. Versatile nanocomposites in phosphoproteomics: A review / M. Najam-ul-Haqa, F. Jabeena, D. Hussaina [et al.] // Analytica Chimica Acta. – 2012. – Vol. 747. – P. 7-18.
  • 27. Nicholls D.G. Bioenergetics: An Introduction to the Chemiosmotic Theory / D.G. Nicholls. – Acad. Press: London, New York, Paris, 1982. – 190 р.
  • 28. Rameech N.McC. Inhibition of Nanoceria’s Catalytic Activity due to Ce3+ Site-Specific Interaction with Phosphate Ions / N.McC. Rameech, P. Mendez, S. Barkam [et al.] // J. Phys. Chem. C. – 2014. – Vol. 118 (33). – P. 18992-19006.
  • 29. Rose J. Interactions between manufactured nanoparticles and individual cells / J. Rose, M. Auffan, O. Zeyons [et al.] // Geochimica et Cosmochimica Acta Suppl. Goldschmidt Conference Abstracts. – 2006. – V. 70. – Р. 539.
  • 30. Santos C.L. Nanomaterials with Antimicrobial Properties: Applications in Health Sciences / C.L. Santos, A.J.R. Albuquerque, F.C. Sampaio [et al.] // In: Microbial pathogens and strategies for combating them: science, technology and education. Publisher: Formatex Research Center. Editor: A. Méndez-Vilas. – 2013. – Vol. 1. – P. 143-154.
  • 31. Shcherbakov A.B. Advances and prospects of using nanocrystalline ceria in cancer theranostics / A.B. Shcherbakov, N.M. Zholobak, N.Ya. Spivak & V.K. Ivanov // Russian Journal of Inorganic Chemistry. — 12/2014, 59 (13). — Р. 1556-1575.
  • 32. Shcherbakov A.B. Advances and prospects of using nanocrystalline ceria in prolongation of lifespan and healthy aging / A.B. Shcherbakov, N.M. Zholobak, N.Ya. Spivak & V.K. Ivanov // Russian Journal of Inorganic Chemistry. — 12/2015, 60 (13). — Р. 1595-1625.
  • 33. Shcherbakov A.B. Cerium fluoride nanoparticles protect cells against oxidative stress / A.B. Shcherbakov, N.M. Zholobak, A.E. Baranchikov [et al.] // Materials Science and Engineering C. — 2015. — Vol. 50. — P. 151-159.
  • 34. Shcherbakov A.B. Nanocrystalline ceria based materials – Perspectives for biomedical application / A.B. Shcherbakov, V.K. Ivanov, N.M. Zholobak [et al.] // Biophysics. – 2011. – Vol. 56, Iss. 6. – P. 987-1004.
  • 35. Singh S. A phosphate-dependent shift in redox state of cerium oxide nanoparticles and its effects on catalytic properties / S. Singh, T. Dosani, A.S. Karakoti [et al.] // Biomaterials. – 2011. – Vol. 32 (28). – P. 6745-6753.
  • 36. Sobek J.M. Effects of the rare earth cerium on Escherichia coli / J.M. Sobek, D.E. Talburt // J. Bacteriol. — 1968. — 95 (1). — Р. 47-51.
  • 37. Sung W.-T. Transformation and fate of nanoscale ZnO, Ag, and CeO2 in different aquatic environments / W.-T. Sung. — Dept. Environmental Engineering, 2012 – 115 p.
  • 38. Zeyons O. Direct and indirect CeO2 nanoparticles toxicity for Escherichia coli and Synechocystis / O. Zeyons, A. Thill, F. Chauvat F. [et al.] // Nanotoxicology. – 2009. – Vol. 3 (4). – P. 284-295.
  • 39. Zholobak N.M. Antiviral effectivity of ceria colloid solutions / N.M. Zholobak, A.B. Shcherbakov, V.K. Ivanov [et al.] // Antiviral Research, Twenty-Fourth International Conference on Antiviral Research, Sofia, Bulgaria, May 2011. — V. 90, Iss. 2. — P. A67.
  • 40. Zholobak N.M. Direct monitoring of the interaction between ROS and cerium dioxide nanoparticles in living cells / N.M. Zholobak, A.B. Shcherbakov, E.O. Vitukova [et al.] // Royal Society of Chemistry Adv. – 2014. – № 4. – Р. 51703-51710.
  • 41. Zholobak N.M. Interaction of nanoceria with microorganisms / N. Zholobak, V. Ivanov, A. Scherbakov // In book: Nanobiomaterials in Antimicrobial Therapy, Chapter: 12, Publisher: Elsevier. — Р. 419-450.
  • 42. Zholobak N.M. Panthenol-stabilized cerium dioxide nanoparticles for cosmeceutic formulations against ROS-induced and UV-induced damage / N.M. Zholobak, A.B. Sherbakov, O.S. Bogorad-Kobelska [et al.] // Journal of Photochemistry and Photobiology B: Biology. — 2014. — V. 130. — Р. 102-108.
  • 43. Zholobak N.M. UV-shielding property, photocatalytic activity and photocytotoxicity of ceria colloid solutions / N.M. Zholobak, V.K. Ivanov, A.B. Shcherbakov [et al.] // J. Photochem. Photobiol. B. — 2011. — V. 102. — P. 32-38.

Publication of the article:

«Bulletin of problems biology and medicine» Issue 1 part 2 (127), 2016 year, 9-15 pages, index UDK 546.655.3-4+544.773:615.281.9