THE EFFECT OF STREPTOCOCCUS PYOGENES ARGININE DEIMINASE ON HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS PROLIFERATION AND ACTIVATION MARKERS EXPRESSION

Cover Page


Cite item

Full Text

Abstract

Arginine is an important nutrient involved in the regulation of homeostasis, vascular tone, as well as the development of infl ammation and immune response. Arginine defi ciency caused by bacterial arginine-deiminase can lead to endothelial dysfunction. In the present study, using the Supernatants of Destroyed Streptococcal Cells (SDSCs) of the original strain (S. pyogenes M49-16) and its isogenic mutant with the inactivated gene of arginine-deiminase ArcA (M49-16delArcA), the effect of arginine deiminase on the proliferative activity and expression of adhesion molecules on human umbilical vein endothelial cells (HUVEC) was evaluated. Cell distribution by cell cycle phases and expression of surface molecules were investigated by fl ow cytometry using monoclonal antibodies. It was shown that the original strain SDSC signifi cantly reduced the proliferative activity of HUVEC and increased the expression of adhesion molecules CD62P, ICAM-1 and tissue factor CD142. The SDSC of the mutant strain did not have any effect. In the presence of supernatants of both strains, the expression of VEGFR-2 receptor did not change. The results showed that streptococcal arginine deiminase promotes development of endothelial dysfunction, infl ammation, and coagulation.

About the authors

J. T. Mammedova

FSBSI “Institute of Experimental Medicine”;
St. Petersburg State Technological University (Technical University)

Author for correspondence.
Email: jennet_m@mail.ru

post-graduate student;

Junior scientific researcher, Dept. of immunology,

Saint-Petersburg

Russian Federation

L. A. Burova

FSBSI “Institute of Experimental Medicine”

Email: fake@neicon.ru

MD, Leading Researcher scientific researcher, Dept. of molecular microbiology,

Saint-Petersburg

Russian Federation

A. B. Malashicheva

FSBSI “Almazov National Medical Research Centre”;
St. Petersburg University

Email: fake@neicon.ru

PhD, Group Leader, Laboratory of Molecular Cardiology,

Associate Professor, Dept. of Embryology, Biological Faculty, 

Saint-Petersburg

Russian Federation

D. S. Semenova

FSBSI “Almazov National Medical Research Centre”;
St. Petersburg University

Email: fake@neicon.ru

post-graduate student of St.-Petersburg University, Laboratory Technician Researcher Laboratory of Molecular Cardiology, Federal Almazov Medical Research Centre,

Junior Researcher, Laboratory of Regenerative Biomedicine, Institute of Cytology, RAS,

Saint-Petersburg

Russian Federation

I. S. Freidlin

FSBSI “Institute of Experimental Medicine”;
Pavlov First Saint Petersburg State Medical University

Email: fake@neicon.ru
MD, corresponding member of RAS, Professor, Chief scientifi c researcher, Dept. of immunology, FSBSI “Institute of Experimental Medicine”, professor, Pavlov First Saint Petersburg State Medical University, Saint-Petersburg Russian Federation

E. A. Starikova

FSBSI “Institute of Experimental Medicine”;
Pavlov First Saint Petersburg State Medical University

Email: fake@neicon.ru
PhD, Senior scientifi c researcher, Dept. of immunology, FSBSI “Institute of Experimental Medicine”, assistant professor, Pavlov First Saint Petersburg State Medical University, Saint-Petersburg Russian Federation

References

  1. Cusumano Z. T., Watson M. E. Jr., Caparon M. G.. Streptococcus pyogenes arginine and citrulline catabolism promotes infection and modulates innate immunity. Infection and Immunity 2014, 82(1), 233–242.
  2. Gallego P., Planell R., Benach J., Querol E., PerezPons J. A., Reverter D. Structural characterization of the enzymes composing the arginine deiminase pathway in Mycoplasma penetrans. PLoS One 2012, 7(10), e47886.
  3. Starikova E. A., Sokolov A. V., Vlasenko A. Y., Burova L. A., Freidlin I. S., Vasilyev V. B. Biochemical and biological activity of arginine deiminase from Streptococcus pyogenes M22. Biochemistry and Cell Biology 2016, 94(2), 129–37.
  4. Morris S. M. Jr. Arginine metabolism: boundaries of our knowledge. Journal of Nutrition 2007, 137(6), 1602S-1609S.
  5. Saxton R. A., Sabatini D. M. mTOR signaling in Growth, Metabolism, and Disease. Cell 2017, 168(6), 960–976.
  6. Laplante M., Sabatini D. M. mTOR signaling in growth control and disease. Cell 2012, 149(2), 274–293.
  7. Danese S., Dejana E., Fiocchi C. Immune Regulation by Microvascular Endothelial Cells: Directing Innate and Adaptive Immunity, Coagulation, and Infl ammation. Journal of Immunology 2007, 178(10), 6017–6022.
  8. Bochenek M. L., Schütz E., Schäfer K. Endothelial cell senescence and thrombosis: Ageing clots. Thrombosis Research 2016, 147, 36–45.
  9. Старикова Э. А., Карасева А. Б., Бурова Л. А., Суворов А. Н., Соколов А. В., Васильев В. Б., Фрейдлин И. С. Pоль аргининдеиминазы Streptococcus pyogenes M49-16 в ингибиции пролиферации эндотелиальных клеток человека линии EA.hy926. Медицинская иммунология 2016, 18(6), 555–562.
  10. Baudin B., Bruneel A., Bosselut N., Vaubourdolle M. A protocol for isolation and culture of human umbilical vein endothelial cells. Nature Protocols 2007, 2, 481–485.
  11. O’Reilly F. M., Casper K. A., Otto K. B., Sexton S. A., Swerlick R. A. Regulation of tissue factor in microvascular dermal endothelial cells. Journal of Investigative Dermatology 2003, 120(3), 489–494.
  12. Kratzer A., Chu H. W., Salys J., Moumen Z., Leberl M., Bowler R., Cool C., Zamora M., Taraseviciene-Stewart L. Endothelial cell adhesion molecule CD146: implications for its role in the pathogenesis of COPD. Journal of Pathology 2013, 230(4), 388–398.
  13. Rosenthal M. D., Carrott P. W., Patel J., Kiraly L., Martindale R. G. Parenteral or Enteral Arginine Supplementation Safety and Efficacy. Journal of Nutrition 2016, 146(12), 2594S-2600S 14. Breitenstein A., Tanner F. C., Lüscher T. F. Tissue Factor and Cardiovascular Disease. Circulation Journal 2010, 7 (1), 3.
  14. Sakai A., Kume N., Nishi E., Tanoue K., Miyasaka M., Kita T. P-selectin and vascular cell adhesion molecule-1 are focally expressed in aortas of hypercholesterolemic rabbits before intimal accumulation of macrophages and T lymphocytes. Arteriosclerosis, Thrombosis, and Vascular Biology 1997; 17, 310–316.
  15. Davies M. J., Gordon J. L., Gearing A. J., Pigott R., Woolf N., Katz D., Kyriakopoulos A. The expression of the adhesion molecules ICAM-1, VCAM-1, PECAM, and E-selectin in human atherosclerosis. Journal of Pathology 1993, 171, 223–229.
  16. Adams M. R., Jessup W., Hailstones D., Celermajer D. S. L-arginine reduces human monocyte adhesion to vascular endothelium and endothelial expression of cell adhesion molecules. Circulation 1997, 95(3), 662–668.
  17. Yang Y., Loscalzo J. Regulation of tissue factor expression in human microvascular endothelial cells by nitric oxide. Circulation 2000, 101, 2144–2148
  18. Romero M., Jiménez R., Sánchez M., López-Sepúlveda R., Zarzuelo M. J., O’Valle F., Zarzuelo A., PérezVizcaíno F., Duarte J. Quercetin inhibits vascular superoxide production induced by endothelin-1: Role of NADPH oxidase, uncoupled eNOS and PKC. Atherosclerosis 2009, 202, 58–67.
  19. Kim S. R., Bae Y. H., Bae S. K., Choi K. S., Yoon K. H., Koo T. H., Jang H. O., Yun I., Kim K. W., Kwon Y. G., Yoo M. A., Bae M. K. Visfatin enhances ICAM-1 and VCAM-1 expression through ROS-dependent NFkappaB activation in endothelial cells. Biochimica et Biophysica Acta 2008, 1783 (5), 886–895.
  20. Patel H., Chen J., Kavdia M. Induced peroxidase and cytoprotective enzyme expressions support adaptation of HUVECs to sustain subsequent H2O2 exposure. Microvascular Research 2016, 103, 1–10.
  21. Ceriello A., Novials A., Ortega E., La S. L., Pujadas G., Testa R., Bonfi gli A. R., Esposito K., Giugliano D. Evidence that hyperglycemia after recovery from hypoglycemia worsens endothelial function and increases oxidative stress and inflammation in healthy control subjects and subjects with type 1 diabetes. Diabetes 2012, 61, 2993–2997.
  22. Nappo F., Esposito K., Cioffi M., Giugliano G., Molinari A. M., Paolisso G., Marfella R., Giugliano D. Postprandial endothelial activation in healthy subjects and in type 2 diabetic patients: role of fat and carbohydrate meals. Journal of the American College of Cardiology 2002, 39, 1145–1150.
  23. Huo Y., Ley K. Adhesion molecules and atherogenesis. Acta Physiologica Scandinavica 2001, 173, 35–43.
  24. Krieglstein C. F., Granger D. N. Adhesion molecules and their roles in vascular disease. American Journal of Hypertension 2001, 14, 44S-54S.
  25. Blann A. D., Nadar S. K., Lip G. Y.H. The adhesion molecule P-selectin and cardiovascular disease. European Heart Journal 2003, 24(24), 2166–2179.
  26. Park I. S., Kang S. W., Shin Y. J., Chae K. Y., Park M. O., Kim M. Y., Wheatley D. N., Min B. H. Arginine deiminase: a potential inhibitor of angiogenesis and tumour growth. British Journal of Cancer2003, 89(5), 907–914.
  27. Beloussow K., Wang L., Wu J., Ann D., Shen W. C. Recombinant arginine deiminase as a potential antiangiogenic agent. Cancer Letters 2002, 183(2), 155–162.
  28. Cтарикова Э. А., Маммедова Дж.Т., Бурова Л. А., Соколов А. В., Васильев В. Б., Фрейдлин И. С. Влияние аргининдеиминазы Streptococcus pyogenes на миграционную активность и структуру цитоскелета эндотелиальных клеток человека. Медицинская Иммунология 2017, 19(5), 521–528.
  29. Старикова Э. А., Лебедева А. М., Бурова Л. А., Фрейдлин И. С. Изменение функциональной активности эндотелиальных клеток под влиянием лизата S. pyogenes. Цитология 2012, 54, (1) 49–57.
  30. Маммедова Дж.Т., Старикова Э. А., Бурова Л. А., Малашичева А. Б., Семёнова Д. С., Фрейдлин И. С. Влияние аргининдеиминазы S. pyogenes на пролиферативную и миграционную активность эндотелиальных клеток вены пупочного канатика человека// Цитокины и воспаление 2017, 3, 48– 51.
  31. Shibuya M. Vascular endothelial growth factor (VEGF)-Receptor2: its biological functions, major signaling pathway, and specific ligand VEGF-E. Endothelium 2006, 13(2), 63–69.
  32. Grillo M. A., Colombatto S. Arginine revisited: minireview article. Amino Acids 2004, 26(4), 345–51.
  33. Grillo M. A., Colombatto S. Metabolism and function in animal tissues of agmatine, a biogenic amine formed from arginine. Amino Acids 2004, 26(1), 3–8.
  34. Förstermann U., Li H. Therapeutic effect of enhancing endothelial nitric oxide synthase (eNOS) expression and preventing eNOS uncoupling. British Journal of Pharmacology 2011, 164(2), 213–23.
  35. Kwon, Y.T., Kashina, A.S., Davydov, I.V., Hu, R.G., An, J.Y., Seo, J.W., Du, F., Varshavsky, A. An essential role of N-terminal arginylation in cardiovascular development. Science 2002, 297(5578), 96–99.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2019 Mammedova J.T., Burova L.A., Malashicheva A.B., Semenova D.S., Freidlin I.S., Starikova E.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № 77 - 11525 от 04.01.2002.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies