Skip to main content
Log in

Yersinia pseudotuberculosis Thermostable Toxin Dysregulates the Functional Activity of Two Types of Phagocytes in the Holothurian Eupentacta fraudatrix

  • CELL BIOLOGY
  • Published:
Biology Bulletin Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. 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.

    Article  CAS  PubMed  Google Scholar 

  2. Benoit, M., Desnues, B., and Mege, J.L., Macrophage polarization in bacterial infections, J. Immunol., 2008, vol. 181, pp. 3733–3739.

    Article  CAS  PubMed  Google Scholar 

  3. 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.

    Article  CAS  Google Scholar 

  4. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Brown, G.C., Reversible binding and inhibition of catalase by nitric oxide, J. Biochem., 1995, vol. 232, pp. 188–191.

    CAS  Google Scholar 

  6. 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.

  7. Chia, F.-S. and Xing, J., Echinoderm coelomocytes, Zool. Studies, 1996, vol. 35, pp. 231–254.

    Google Scholar 

  8. 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.

    Article  CAS  PubMed  Google Scholar 

  9. 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.

    Article  CAS  Google Scholar 

  10. 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.

    Article  CAS  Google Scholar 

  11. 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.

    Article  CAS  Google Scholar 

  12. 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.

    Article  CAS  Google Scholar 

  13. 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.

    CAS  Google Scholar 

  14. 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.

    Article  CAS  PubMed  Google Scholar 

  15. Fraternale, A., Brundu, S., and Magnani, M., Polarization and repolarization of macrophages, J. Clin. Cell. Immunol., 2015, vol. 6, pp. 2–12.

    Google Scholar 

  16. 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.

    CAS  PubMed  Google Scholar 

  17. He, C. and Carter, A.B., The metabolic prospective and redox regulation of macrophage polarization, J. Clin. Cell. Immunol., 2015, vol. 6. pii 371.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 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.

  19. 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.

    Article  CAS  PubMed  Google Scholar 

  20. 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.

  21. 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.

    Article  CAS  PubMed  Google Scholar 

  22. Mel’nikov, V.P., Test of nitro blue tetrazolium reduction by mononuclear phagocytes, Lab. Delo, 1991, no. 8, pp. 51–53.

  23. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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.

  27. 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.

    Article  CAS  PubMed  Google Scholar 

  28. 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.

    Google Scholar 

  29. 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.

    Article  CAS  PubMed  Google Scholar 

  30. 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.

  31. Timchenko, N.F., Nedashkovskaya, E.P., Dolmatova, L.S., and Somova-Isachkova, L.M., Toksiny Yersinia pseudotuberculosis (Yersinia pseudotuberculosis Toxins), Vladivostok: Primpoligrafkombinat, 2004.

    Google Scholar 

  32. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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.

  34. 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.

    Article  CAS  PubMed  Google Scholar 

  35. 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.

    CAS  Google Scholar 

  36. 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.

    Article  CAS  PubMed  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to L. S. Dolmatova.

Additional information

Translated by A. Panyushkina

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359019020043

Navigation