The relationship of quantitative indicators sCD56 and sCD16 with the level of immunocompetent cells, cytokines, circulating immune complexes and cyclic nucleotides in practically healthy people living in the Arctic territory

Cover Page

Cite item

Full Text

Abstract

We studied the content of immunocompetent blood cells, phagocytic activity of neutrophils, concentrations of cytokines, circulating immune complexes and levels of cyclic nucleotides (cAMP and cGMP) of serum with different levels of soluble adhesion molecules NCAM (CD56) and immunoglobulin Fc-receptor III (CD16) in practically healthy people living in the Arctic territory. It was found that the increase in serum concentration of sCD56 and sCD16 in practically healthy adults of working age is associated with an increase in the content of cells with the corresponding membrane receptors. The increase in sCD56 concentration occurs with an increase in the content of NK cells (CD3-CD16+CD56+) and T-NK cells (CD3+CD16+CD56+). The increase in sCD16 level is accompanied by a decrease in the content of circulating in the blood lymphocytes predominantly T-helper cells (CD3+CD4+), cytotoxic T-lymphocytes (CD3+CD8+) and activated T-lymphocytes (CD3+HLADR+). Increased sCD56 concentrations were associated with increases in pro-inflammatory IL-1β, IL-6, TNF-α and anti-inflammatory IL-10. Concentrations of circulating immune complexes increased with increasing sCD16 and sCD56 content. The signal conduction activity increases with increasing content of CD16+ and CD56+ leukocytes of peripheral blood and sCD56+ leukocytes and shedding of these molecules occurs against the background of decreasing concentrations of cAMP and cGMP.

About the authors

A. V. Samodova

N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences

Author for correspondence.
Email: annapoletaeva2008@yandex.ru
Russian Federation, Ave. Nikolsky 20, Arkhangelsk, 163020

L. K. Dobrodeeva

N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences

Email: annapoletaeva2008@yandex.ru
Russian Federation, Ave. Nikolsky 20, Arkhangelsk, 163020

V. P. Patrakeeva

N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences

Email: annapoletaeva2008@yandex.ru
Russian Federation, Ave. Nikolsky 20, Arkhangelsk, 163020

References

  1. Abel A. V., Yang C., Thakar M. S., Malarkannan S. Natural killer development, maturation, and clinical utilization // Frontiers in Immunology. 2018. V. 9. P. 1869.doi: 10.3389/fimmu.2018.01869
  2. Aguilar O. A., Gonzalez-Hinojosa M. D. R, Arakawa-Hoyt J. S. et al. The CD16 and CD32b Fc-gamma receptors regulate antibody-mediated responses in mouse natural killer cells // J. Leukoc. Biol. 2023. V. 113. № 1. P. 27–40.doi: 10.1093/jleuko/qiac003
  3. Artyukhov V. G. Secondary messengers cAMP, Ca2+, NO – modulate the functional properties of lymphocytes under UV irradiation // Bulletin of Experimental Biology and Medicine. 2010. V. 12. P. 637–641.
  4. Ashman R. F. Accelerated loss and replacement of receptors on antigen-binding cells after immunization // Journal of Immunology. 1980. V. 124. P. 893–904.
  5. Ashman R. F. Immunological role of antigenbinding cell // Immunology Today. 1982. V. 3. P. 349–352.
  6. Balkwill F., Charles K., Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease // Cancer Cell. 2005. V. 7. № 3. P. 211–217.doi: 10.1016/j.ccr.2005.02.013
  7. Belchenko D. I. Functional system of non-lymphoid cells in erythrocyte clearance of circulating immune complexes // Immunology. 2013. V. 34. P. 88–90.
  8. Belchenko D. I., Krivosheina E. L. Exocytic lysis of erythrocytes by megakaryocytes in bone marrow erythroclastic clusters and autoregots in acute lymphoblastic leukemia. // Hematology and transfusiology. 1999. V. 44. № 5. P. 18–21.
  9. Brieva J. A., Villar L. M., Leoro G., Alvarez-Cermeño J.C., Roldán E., Gonzalez-Porqué P. Soluble HLA class I antigen secretion by normal lymphocytes: relationship with cell activation and effect of interferon-gamma // Clinical and Experimental Immunology. 1990. V. 82. № 2. P. 390–395.doi: 10.1111/j.1365-2249.1990.tb05459.x
  10. Burke S. D., Seaward A. V.C., Ramshaw H., Smith G. N., Virani S., Croy B. C., Lima P. D.A. Homing receptor expression is deviated on CD56+ blood lymphocytes during pregnancy in Type 1 diabetic women // PLoS One. 2015. V. 10. № 3. P. e0119526.doi: 10.1371/journal.pone.0119526
  11. Cai H., Kakiuchi-Kiyota S., Hendricks R., Zhong S., Liu L., Adedeji A. O., Chan P., Schutten M. M., Kamath A. V., Ovacik M. A. Nonclinical Pharmacokinetics, Pharmacodynamics, and Translational Model of RO7297089, A Novel Anti-BCMA/CD16A Bispecific Tetravalent Antibody for the Treatment of Multiple Myeloma // AAPS J. 2022. V. 24. № 6. P. 100.doi: 10.1208/s12248-022-00744-8
  12. Carville A., Evans T. I., Reeves R. K. Characterization of circulating natural killer cells in neotropical primates // PLoS. One. 2013. V. 8. № 11. P. e78793.doi: 10.1371/journal.pone.0078793
  13. Crinier A., Narni-Mancinelli E., Ugolini S., Vivier E. SnapShot; Natural Killer Cells // Cell. 2020. V. 180. № 6. P. 1280–1286.doi: 10.1016/j.cell.2020.02.029
  14. Dhus O., Bunk S., Aulock S., Hermann C. IL-10 release requires stronger toll-like receptors 4-triggering than TNF: a possible explanation for the selective effects of heterozygous TLR4 polymorphism Asp(299)Gly on IL-10 release // Immunology. 2008. V. 213. № 8. P. 621–627.doi: 10.1016/j.imbio.2008.03.001
  15. Euchner J., Sprissler J., Cathomen T. Natural Killer Cells Generated From Human Induced Pluripotent Stem Cells Mature to CD56brightCD16+NKp80+/-In-Vitro and Express KIR2DL2/DL3 and KIR3DL1 // Front Immunol. 2021. V. 4. № 12. P. 640672.doi: 10.3389/fimmu.2021.640672.
  16. Firsova M. V., Mendeleeva L. P., Kovrigina A. M., Savchenko V. G. Expression of adhesion molecule CD56 in tumor plasma cells in bone marrow as a prognostic factor in multiple myeloma // Clinical oncohematology. 2019. V. 12. № 4. P. 377–384.doi: 10.21320/2500-2139-2019-12-4-377-384
  17. Gardiner C. M. Killer cell immunoglobulin-like receptors on NK cell: the how, where and why // International Journal of Immunogenetics. 2008. V. 35. № 1. P. 1–8.doi: 10.1111/j.1744-313X.2007.00739.x
  18. Gong P., Metrebian F., Dulau-Florea A., Wang Z-X., Bajaj R., Gulati G., Peiper, S.C., Gong J. Z. Aberrant expression of CD56 on granulocytes and monocytes in myelo-proliferative neoplasm // Journal of Hematopathology. 2013. V. 6. № 3. P. 127–134.
  19. Glaser K., Kern D., Speer C. P., Schlegel N., Schwab M., Thome U. H., Härtel C., Wright C. J. Imbalanced Inflammatory Responses in Preterm and Term Cord Blood Monocytes and Expansion of the CD14+CD16+ Subset upon Toll-like Receptor Stimulation // Int. J. Mol. Sci. 2023. V. 24. № 5. P. 4919.doi: 10.3390/ijms24054919
  20. Justo G. A., Bitencourt M. A., Pasquini R., Castelo-Branco M.T.L., Almeida-Oliveira A., Diamond H. R., Rumjanek V. M. Immune status of Fanconi anemia patients: decrease in T CD8 and CD56dim CD16+ NK lymphocytes // Ann Hematol. 2014. V. 93. № 5. P. 761–767.doi: 10.1007/s00277-013-1953-4
  21. Kanda N., Watanabe S. Intracellular 3ʺ5ʺ-adenosine cyclic monophosphate level regulates house dust milte-induced interleukin-13 production by T-cells from mite-sensitive patients with atopic dermatitis // Journal of Investigative Dermatology. 2001. V. 116. № 1. P. 3–11.doi: 10.1046/j.1523-1747.2001.01196.x
  22. Krug U., Krug F., Cuatrecasas P. Emergence of insulin receptors on human lymphocytes during in vitro transformation. Proceedings of the National Academy of Sciences. U.S.A. 1972. V. 69. № 9. P. 2604–2608.doi: 10.1073/pnas.69.9.2604
  23. Kussick S. J., Wood B. L. Using 4-color flow cytometry to identify abnormal myeloid populations // Archives of Pathology & Laboratory Medicine. 2003. V. 127. № 9. P. 1140–1147.doi: 10.5858/2003-127-1140-UCFCTI
  24. Kuwahara A., Nagai K., Nakanishi T., Kumagai I., Asano R. Functional Domain Order of an Anti-EGFR × Anti-CD16 Bispecific Diabody Involving NK Cell Activation // Int. J. Mol. Sci. 2020. V. 21. № 23. P. 8914.doi: 10.3390/ijms21238914
  25. Lanier L. L., Le A. M., Civin C. I., Loken M. R., Phillips J. H. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes // J. Immunol. 1986. V. 136. № 12. P. 4480–4486.
  26. Lemke M. M., Theisen R. M., Bozich E. R., McLean M.R., Lee C. Y., Lopez E., Rerks-Ngarm S., Pitisuttithum P., Nitayaphan S., Kratochvil S., Wines B. D., Hogarth P. M., Kent S. J., Chung A. W., Arnold K. B. A Quantitative approach to unravel the role of host genetics in IgG-FcγR complex formation after vaccination // Front. Immunol. 2022. V. 13. P. 820148.doi: 10.3389/fimmu.2022.820148
  27. Li T., Gao N, Cui W., Zhao L., Pan L. Natural killer cells and their function in Takayasu’s arteritis // Clin. Exp. Rheumatol. 2020. V. 124. № 2. P. 84–90.
  28. Lebedev O. E., Krutetskaya Z., Krutetskaya N. I. The role of the adenylate cyclase system of regulation of Ca++ signals induced by purineergic agonists inhibitors of endoplasmic Ca-ATPases in rat peritoneal macrophages. Mater. 2nd Congress of Biophysicists of Russia: M, 1999. 333 p.
  29. Loor F. Plasma membrane and cell cortex interactions in lymphocyte functions // Advances in Immunology. 1980. V. 30. № 1. P. 120.doi: 10.1016/s0065-2776(08)60194-7
  30. Lu J., Marian K. D., Mold K., Du Clos T. W., Sun P. D. Pentraxins and Fc-receptors // Immunological Reviews. 2012. V. 250. № 1. P. 230–238.doi: 10.1111/j.1600-065X.2012.01162.x
  31. Mareeva T., Martinez-Hacktrt E., Sykulev Y. Haw a T cell receptor-like antibody recognizes major histocompatibility complex-bound peptide // Journal of Biological Chemistry. 2008. V. 283. № 43. P. 29053–29059.doi: 10.1074/jbc.M804996200
  32. Masuda M., Morimoto T., Kobatake S., Nishimura N., Nakamoto K., Dong X. H., Komiyama Y., Ogawa R., Takahashi H. Measurement of soluble Fcg receptor type IIIa derived from macrophages in plasma: increase in patients with rheumatoid arthritis // Clin. Exp. Immunol. 2003. V. 132. № 3. P. 477–484.doi: 10.1046/j.1365-2249.2003.02168.x
  33. Masuda M., Takahashi H. Increase of soluble Fc gamma RIIIa derived from macrophages in plasma from patients with atherosclerosis // Rinsho Byori. 2002. V. 50. № 5. P. 502–505.
  34. Meza Guzman L. G., Keating N., Nicholson S. E. Natural killer cells: tumor, surveillance and signaling // Cancers. 2020. V. 12. № 4. P. 952.doi: 10.3390/cancers12040952
  35. Melsen J. E., Themeli M., van Ostaijen-Ten Dam M. M., van Beelen E., Lugthart G., Hoeben R. C., Marco W Schilham M., Mikkers H. M. Protocol for Isolation, Stimulation and Functional Profiling of Primary and iPSC-derived Human NK Cells // Bio Protoc. 2020. V. 10. № 23. P. e3845.doi: 10.21769/BioProtoc.3845.
  36. Michel T., Poli A., Cuapio A., Briquemont B., Iserentant G., Ollert M., Zimmer J. Human CD56bright NK Cells: An Update // J. Immunol. 2016. V. 196. № 7. P. 2923–2931.doi: 10.4049/jimmunol.1502570.
  37. Novikov V. V. Soluble differentiation molecules in inflammatory processes (The second life of proteins) / Nizhny Novgorod: Gladkova O. V. “Publishing Salon”, 2022. 212 p.
  38. Palmer M. J., Mahajan V. S., Chen J., Irvine D. J., Lauffenburger D. A. Signaling thresholds govern heterogeneity in IL-7-receptor-mediated responses of naive CD8+ T-cells // Immunol. And cell Biol. 2011. V. 89. № 5. P. 581–594.doi: 10.1038/icb.2011.5
  39. Pukhteeva I. V., Gerasimovich N. V., Rybachenok D. S. Functioning of the cyclic nucleotide system under extracellular exposure to physiologically active substances // Journal of the Belarusian State University. Ecology. 2017. V. 1. P. 40–45.
  40. Riley C. R., Hansen M., Brimnes M. K., Hasselbalch H. C., Bjerrum O. B., Straten P. T., Svane I. M., Jensen M. K. Expansion of circulating CD56bright natural killer cells in patients with JAK2-positive chronic myeloproliferative neoplasms during treatment with interferon-α // Eur J. Haematol. 2015. V. 94. № 3. P. 227–234.doi: 10.1111/ejh.12420
  41. Saito L. M., Ortiz R. C., Amôr N. G., Lopes N. M., Buzo R. F., Garlet G. P., Rodini C. O. NK cells and the profile of inflammatory cytokines in the peripheral blood of patients with advanced carcinomas // Cytokine. 2024. V. 174. P. 156455.doi: 10.1016/j.cyto.2023.156455
  42. Samodova A. V., Dobrodeeva L. K. The correlation between the pool of free adhesion molecule receptors and the activity of the immune system in the Murmansk oblast residents // Human Physiology. 2019. V. 45. № 1. P. 90–97.doi: 10.1134/S0362119718060105
  43. Selvaraj R. J., Sbarra A. J., Thomas G. B., Cetrulo C. L., Mitchell G. W. A microtechnique for studying chemiluminescence response of phagocytes using whole blood and its application to the evaluation of phagocytes in pregnancy // Journal of the Reticuloendothelial Society. 1982. V. 31. № 1. P. 3–16.
  44. Shevchenko A. S. Changes in adenylate cyclase activity in megakaryocytes and platelets of irradiated sheep // Radiobiology. 1990. V. 30. № 3. P. 308–311.
  45. Starikova E. A., Kiseleva E. P., Freidlin I. S. Heterogeneity of mononuclear phagocytes: subpopulations and plasticity // Successes of modern biology. 2005. V. 125. № 5. P. 466–477.
  46. Stockmeyer B., Beyer T., Neuhuber W., Repp R., Kalden J. R., Valerius T., Herrmann M. Polymorphonuclear granulocytes induced antibody-dependent apoptosis in human breast cancer cells // Journal of Immunology. 2003. V. 171. № 10. P. 5124–5133.doi: 10.4049/jimmunol.171.10.5124
  47. Tasken K., Skokka A. J. The molecular machinery for c AMP-dependent immunomodulation in T-cells // Biochemical Society Transactions. 2006. V. 34. P. 476–479.doi: 10.1042/BST0340476
  48. Teale J. M., Liu F.-T., Katz D. H. A clonal analysis of the IgE response and its implication with regard to isotope commitment // J. Exp. Med. 1981. Vol. 153. № 4. P. 783–792.doi: 10.1084/jem.153.4.783
  49. Theofilopoulus A. N., Dixon F. J. Immune complexes in human diseases: a review // Am. J. Phathol. 1980. V. 100. № 2. P. 529–594.
  50. Watanabe A., Togi M., Koya T., Taniguchi M., Sakamoto T., Iwabuchi K., Jr T. K., Shimodaira S. Identification of CD56dim subpopulation marked with high expression of GZMB/PRF1/PI-9 in CD56+ interferon-α-induced dendritic cells // Genes Cells. 2021. V. 26. № 5. P. 313–327.doi: 10.1111/gtc.12844
  51. Werner K., Schwede F., Genieser H.-G., Geiger J., Butt E. Quantification of cAMP and cGMP analogs in intact cells: pitfalls in enzyme immunoassays for cyclic nucleotides // Naunyn-Schmiedeberg’s Archives of Pharmacology. 2011. V. 384. № 2. 169–176.doi: 10.1007/s00210-011-0662-6
  52. Wilke C. M., Wei S., Wang L., Kryczek I., Kao J., Zou W. Dual biological effects of the cytokines interleukin-10 and interferon-γ // Immunol. and Immunother. 2011. V. 60. № 11. P. 1529–1541.doi: 10.1007/s00262-011-1104-5
  53. Yurieva O. V., Dubrovina V. I. The role of cyclic nucleotide signaling systems in the regulation of immuno- and pathogenesis // Bulletin of the VSNC SB RAMS. 2012. V. 2. № 84. P. 159–163.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Russian Academy of Sciences