Abstract—
The effect of a thermostable toxin of Yersinia pseudotuberculosis (in comparison with that of dexamethasone) on the functional activities of two types of phagocytes (P1 and P2) was studied in the holothurian Eupentacta fraudatrix. A high level of NO was shown to be a marker of intact P1 cells, while the high activity of arginase was a marker of P2 cells. The antioxidant defense in the P1 type was more pronounced than that of the P2 type. At the same time, the toxin inhibited the functional activity (generation of reactive oxygen species) of P1 phagocytes after 1 h of incubation and induced primarily the activity of P2 phagocytes, compared to that of P1 cells, after 24 h. In contrast to dexamethasone, which induced the transformation of the P1 phenotype into the P2 phenotype, the toxin promoted the mutual acquisition of the phenotype features by these two types of phagocytes. An analogy between the P1 and P2 phagocytes of the holothurian and M1 and M2 macrophages is discussed.
Similar content being viewed by others
REFERENCES
Almeida, P.E., Roque, N.R., Magalhães, K.G., Mattos, K.A., Teixeira, L., Maya-Monteiro, C., Almeida, C.J., Castro-Faria-Neto, H.C., Ryffel, B., Quesniaux, V.F., and Bozza, P.T., Differential TLR2 downstream signaling regulates lipid metabolism and cytokine production triggered by Mycobacterium bovis BCG infection, Biochim. Biophys. Acta, 2014, vol. 1841, pp. 97–107.
Benoit, M., Desnues, B., and Mege, J.L., Macrophage polarization in bacterial infections, J. Immunol., 2008, vol. 181, pp. 3733–3739.
Bradford, M.M., A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.
Break, T.J., Jun, S., Indramohan, M., Carr, K.D., Sieve, A.N., Dory, L., and Berg, R.E., Extracellular superoxide dismutase inhibits innate immune responses and clearance of an intracellular bacterial infection, J. Immunol., 2012, vol. 188, pp. 3342–3350.
Brown, G.C., Reversible binding and inhibition of catalase by nitric oxide, J. Biochem., 1995, vol. 232, pp. 188–191.
Chesnokova, N.P., Ponukalina, E.V., and Bizenkova, M.N., Molecular and cellular mechanisms of inactivation of free radicals in biological systems, Usp. Sovrem. Estestvoznan., 2006, no. 7, pp. 29–36.
Chia, F.-S. and Xing, J., Echinoderm coelomocytes, Zool. Studies, 1996, vol. 35, pp. 231–254.
Dobashi, K., Pahan, K., Chahal, A., and Singh, I., Modulation of endogenous antioxidant enzymes by nitric oxide in rat C6 glial cells, J. Neurochem., 1997, vol. 68, pp. 1896–1903.
Dolmatova, LS., Eliseikina, M.G., and Romashina, V.V., Antioxidant enzymatic activity of coelomocytes of the Far East sea cucumber Eupentacta fraudatrix, J. Evol. Biochem. Physiol., 2004, vol. 40, pp. 126–135.
Dolmatova, L.S., Eliseykina, M.G., Timchenko, N.F., Kovaleva, A.L., and Shitkova, O.A., Generation of reactive oxygen species in the different fractions of the coelomocytes of holothurian Eupentacta fraudatrix in response to the thermostable toxin of Yersinia pseudotuberculosis in vitro, Chinese J. Oceanol. Limnol., 2003, vol. 21, pp. 293–304.
Dolmatova, L.S. and Ulanova, O.A., Dexamethasone treatment in vitro resulted in different responces of two fractions of phagocytes of the holothurian Eupentacta fraudatrix, Rus. J. Mar. Biol., 2015, vol. 41, pp. 503–506.
Dolmatova, L.S. and Zaika, O.A., Apoptosis-modulating effect of prostaglandin E2 in coelomocytes of holothurian Eupentacta fraudatrix depends on the cell antioxidant enzyme status, Biol. Bull. (Moscow), 2007, vol. 34, no. 3, pp. 221–229.
Dotsenko, O.I., Dotsenko, V.A., and Mishchenko, A.M., Superoxide dismutase and catalase activity in erythrocytes and several tissues of mice under conditions of low-frequency vibrations, Fizika Zhivogo, 2010, vol. 18, pp. 107–113.
Elnekave, K., Siman-Tov, R., and Ankri, S., Consumption of L-arginine mediated by Entamoeba histolytica L-arginase (EhArg) inhibits amoebicidal activity and nitric oxide production by activated macrophages, Parasite Immunol., 2003, vol. 25, pp. 597–608.
Fraternale, A., Brundu, S., and Magnani, M., Polarization and repolarization of macrophages, J. Clin. Cell. Immunol., 2015, vol. 6, pp. 2–12.
Habig, W.H., Pabst, M.J., and Jackoby, W.B., Glutathione S-transferase. The first enzymatic step in mercapturic acid formation, J. Biol. Chem., 1974, vol. 249, pp. 7130–7139.
He, C. and Carter, A.B., The metabolic prospective and redox regulation of macrophage polarization, J. Clin. Cell. Immunol., 2015, vol. 6. pii 371.
Koren-Gluzer, M., Rosenblat, M., and Hayek, T., Paraoxonase 2 induces a phenotypic switch in macrophage polarization favoring an M2 anti-inflammatory state, Int. J. Endocrinol., 2015, vol. 2015. ID 915243.
Korhonen, R., Lahti, A., Hamalainen, M., Kankaanranta, H., and Moilanen, E., Dexamethasone inhibits inducible nitric-oxide synthase expression and nitric oxide production by destabilizing mRNA in lipopolysaccharide-treated macrophages, Mol. Pharmacol., 2002, vol. 62, pp. 698–704.
Kovalev, N.N., Pivnenko, T.N., and Kim, G.N., Analysis of the market of biologically active products from the commercial holothurians (Echinodermata: Holothuroidea): raw materials and technologies, Ryb. Khoz., 2016, no. 2, pp. 112–116.
Kraaij, M.D., van der Kooij, S.W., Reinders, M.E., Koekkoek, K., Rabelink, T.J., van Kooten, C., and Gelderman, K.A., Dexamethasone increases ROS production and T cell suppressive capacity by anti-inflammatory macrophages, Mol. Immunol., 2011, vol. 49, pp. 549–557.
Mel’nikov, V.P., Test of nitro blue tetrazolium reduction by mononuclear phagocytes, Lab. Delo, 1991, no. 8, pp. 51–53.
Mendoza-Coronel, E. and Ortega, E., Macrophage polarization modulates FcγR- and CD13-mediated phagocytosis and reactive oxygen species production, independently of receptor membrane, Front. Immunol., 2017, vol. 8, p. 303.
Merriman, J.A., Klingelhutz, A.J., Diekema, D.J., and Leung, D.Y., Novel Staphylococcus aureus secreted protein alters keratinocyte proliferation and elicits a proinflammatory response in vitro and in vivo, Biochemistry, 2015, vol. 54, pp. 4855–4862.
Nguyen, G.T., Green, E.R., and Mecsas, J., Neutrophils to the ROScue: mechanisms of NADPH oxidase activation and bacterial resistance, Front. Cell. Infect. Microbiol., 2017, vol. 7, p. 373.
Oboh, G., Ademiluyi, A.O., Ademosun, A.O., Olasehinde, T.A., Oyeleye, S.I., Boligon, A.A., and Athayde, M.L., Phenolic extract from Moringa oleifera leaves inhibits key enzymes linked to erectile dysfunction and oxidative stress in rats’ penile tissues, Biochem. Res. Int., 2015, vol. 2015. ID 175950.
Rast, J.P. and Messier-Solek, C., Marine invertebrate genome sequences and our evolving understanding of animal immunity, Biol. Bull., 2008, vol. 214, pp. 274–283.
Sarbaeva, N.N., Ponomareva, Yu.V., and Milyakova, M.N., Macrophages. Diversity of phenotypes and functions, interaction with foreign materials, Geny i Kletki, 2016, vol. 11, no. 1, pp. 9–17.
Smith, L.C. and Davidson, E.H., The echinoid immune system and the phylogenetic occurrence of immune mechanisms in deuterostomes, Immunol. Today, 1992, vol. 13, pp. 356–362.
Tan, H., Wang, N., Li, S., Hong, M., Wang, X., and Feng, Y., The reactive oxygen species in macrophage polarization: reflecting its dual role in progression and treatment of human diseases, Oxid. Med. Cell Longev., 2016. ID 2795090.
Timchenko, N.F., Nedashkovskaya, E.P., Dolmatova, L.S., and Somova-Isachkova, L.M., Toksiny Yersinia pseudotuberculosis (Yersinia pseudotuberculosis Toxins), Vladivostok: Primpoligrafkombinat, 2004.
Torika, N., Asraf, K., Danon, A.A., Apte, R.N., and Fleisher-Berkovich, S., Telmisartan modulates glial activation: in vitro and in vivo studies, PLoS One, 2016, vol. 11. e0155823.
Trav’es, P.G., Luque, A., and Hortelano, S., Macrophages, inflammation, and tumor suppressors: ARF, a new player in the game, Mediators Inflamm., 2012. ID 568783.
Tsai, H.C. and Wu, R., Cholera toxin directly enhances IL-17a production from human CD4+ T cells, J. Immunol., 2013, vol. 191, pp. 4095–4102.
Zemskov, V.M., Barsukov, A.A., Gnatenko, D.A., Shishkina, N.S., Kulikova, A.N., and Kozlova, M.N., Fundamental and applied aspects of the analysis of the oxygen metabolism of phagocytic cells, Usp. Sovrem. Biol., 2013, vol. 133, pp. 469–480.
Zheng, W., Umitsu, M., Jagan, I., Tran, C.W., Ishiyama, N., BeGora, M., Araki, K., Ohashi, P.S., Ikura, M., and Muthuswamy, S.K., An interaction between Scribble and the NADPH oxidase complex controls M1 macrophage polarization and function, Nat. Cell Biol., 2016, vol. 18, pp. 1244–1252.
COMPLIANCE WITH ETHICAL STANDARDS
Conflict of interests. The authors declare that they have no conflict of interest.
Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated by A. Panyushkina
Rights and permissions
About this article
Cite this article
Dolmatova, L.S., Ulanova, O.A. & Timchenko, N.F. Yersinia pseudotuberculosis Thermostable Toxin Dysregulates the Functional Activity of Two Types of Phagocytes in the Holothurian Eupentacta fraudatrix. Biol Bull Russ Acad Sci 46, 117–127 (2019). https://doi.org/10.1134/S1062359019020043
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1062359019020043