Disseminated purulent peritonitis outcome affects NKT cell phenotype

封面

如何引用文章

全文:

详细

The aim of our study was to investigate the main characteristics of peripheral blood NKT cell phenotype in patients with disseminated purulent peritonitis (DPP) in dynamics of postoperative period, depending on the disease outcome. Fifty-two patients with acute surgical diseases and injuries of the abdominal organs complicated by DPP, and 68 healthy individuals in control group, were examined. Blood sampling was performed before surgery (preoperative period), as well as on the day 7, 14 and 21 of postoperative period. All patients with DPP were divided into two groups depending on disease outcome in postoperative period: patients with favorable disease outcome (n = 34); and patients with unfavorable outcome (n = 18). Study of the phenotype of blood NKT lymphocytes was performed by flow cytometry using direct immunofluorescence of whole peripheral blood samples with monoclonal antibodies. The low relative and absolute level of NKT cells was observed in DPP patients regardless of outcome disease in preoperative period. At the same time, the absolute level of NKT cells returned to normal only in patients with favorable DPP outcome and only by day 21 after surgery. Patients with favorable DPP outcome by the end of examination period had normalized quantity of mature NKT-lymphocytes and significantly decreased level of cytotoxic cells which was apparently associated with migration of such cell subsets to site of inflammation. A reduced level of non-classical (expressing CD8 marker) mature and cytokine-producing NKT cells was detected only in patients with favorable DPP outcome in preoperative period which returned to normal by the end of postoperative period. At the same time, patients with unfavorable disease outcome had reduced quantity of NKT cells of these subsets by day 21 of postoperative treatment. Patients with favorable outcome had high level of mature and cytotoxic CD11b+ NKT cells already in the preoperative period, while patients with unfavorable DPP outcome had increased level of cytotoxic CD11b+ NKT cells only by day 21 after surgery. The proportion of NKT cells expressing activation markers (CD28 and CD57) was reduced in patients in preoperative period that returned to normal immediately after surgery with favorable outcome, while it recovered with unfavorable outcome closer to the end of postoperative examination. The defined features of NKT cell phenotype in patients with unfavorable DPP outcome characterize disturbances in subset ratio and mechanisms of functioning of this cell fraction. This determines a need to develop immunotherapeutic methods aimed at stimulating immunoregulatory activity of NKT cells.

作者简介

Andrey Savchenko

Federal Research Center “Krasnoyarsk Science Center”, Siberian Branch of the Russian Academy of Sciences, Scientific Research Institute of Medical Problems of the North

Email: aasavchenko@yandex.ru

PhD, MD (Medicine), Professor, Head of the Laboratory of Cellular-Molecular Physiology and Pathology

俄罗斯联邦, Krasnoyarsk

Alexandr Borisov

Federal Research Center “Krasnoyarsk Science Center”, Siberian Branch of the Russian Academy of Sciences, Scientific Research Institute of Medical Problems of the North

Email: 2410454@mail.ru

PhD (Medicine), Leading Researcher, Laboratory of Cellular-Molecular Physiology and Pathology

俄罗斯联邦, Krasnoyarsk

Igor Kudryavtsev

I.P. Pavlov First St. Petersburg State Medical University, Russian Ministry of Health; Institute of Experimental Medicine

Email: igorek1981@yandex.ru

PhD (Biology), Head of the Cell Immunology Laboratory, Department of Immunology; Assistant Professor, Department of Immunology

俄罗斯联邦, 197376, St. Petersburg, Academician Pavlov str., 12; St. Petersburg

V. Belenjuk

Federal Research Center “Krasnoyarsk Science Center”, Siberian Branch of the Russian Academy of Sciences, Scientific Research Institute of Medical Problems of the North

编辑信件的主要联系方式.
Email: dyh.88@mail.ru

Junior Researcher, Laboratory of Cellular-Molecular Physiology and Pathology

俄罗斯联邦, Krasnoyarsk

参考

  1. Акинфиева О.В., Бубнова Л.Н., Бессмельцев С.С. NKT-клетки: характерные свойства и функциональная значимость для регуляции иммунного ответа // Онкогематология. 2010. № 4. С. 39–47. [Akinfieva O.V., Bubnova L.N., Bessmeltsev S.S. NKT cells: characteristic properties and functional significance for the regulation of the immune response. Onkogematologiya = Oncohematology, 2010, no. 4, pp. 39–47. (In Russ.)]
  2. Беленюк В.Д., Савченко А.А., Борисов А.Г., Кудрявцев И.В. Особенности фенотипа В-лимфоцитов крови в зависимости от исхода распространенного гнойного перитонита // Инфекция и иммунитет. 2021. Т. 11, № 3. C. 454–462. [Belenjuk V.D., Savchenko A.A., Borisov A.G., Kudryavtsev I.V. Features of peripheral blood B-cell subset phenotype are associated with clinical outcome of widespread purulent peritonitis. Infektsiya i immunitet = Russian Journal of Infection and Immunity, 2021, vol. 11, no. 3, pp. 454–462. (In Russ.)] doi: 10.15789/2220-7619-CBC-1397
  3. Борисов Р.Н., Здзитовецкий Д.Э., Каспаров Э.В., Савченко А.А., Борисов С.А., Бердников Д.С., Говоруха Е.С., Болдырев П.Н. Типы реакции иммунной системы и их характеристика у больных распространенным гнойным перитонитом // Сибирское медицинское обозрение. 2019. № 5. С. 80–87. [Borisov R.N., Zdzitovetskii D.E., Kasparov E.V., Savchenko A.A., Borisov S.A., Berdnikov D.S., Govorukha E.S., Boldyrev P.N. Types of immune system reactions and their characteristic in patients with generalized purulent peritonitis. Sibirskoe meditsinskoe obozrenie = Siberian Medical Review, 2019, no. 5, pp. 80–87 (In Russ.)] doi: 10.20333/2500136-2019-5-80-87
  4. Кудрявцев И.В., Субботовская А.И. Опыт измерения параметров иммунного статуса с использованием шестицветного цитофлуориметрического анализа // Медицинская иммунология. 2015. Т. 17, № 1. С. 19–26. [Kudryavtsev I.V., Subbotovskaya A.I. Experience in measuring the parameters of the immune status using six-color cytofluorimetric analysis. Meditsinskaya immunologiya = Medical Immunology (Russia), 2015, vol. 17, no. 1, pp. 19–26. (In Russ.)] doi: 10.15789/1563-0625-2015-1-19-26
  5. Савченко А.А., Борисов А.Г., Черданцев Д.В., Первова О.В., Кудрявцев И.В., Гвоздев И.И., Мошев А.В. Особенности фенотипа и активности NAD(P)-зависимых дегидрогеназ нейтрофилов у больных распространенным гнойным перитонитом в прогнозе развития сепсиса // Инфекция и иммунитет. 2018. Т. 8, № 3. С. 369–376. [Savchenko А.А., Borisov A.G., Cherdancev D.V., Pervova O.V., Kudryavtsev I.V., Gvozdev I.I., Moshev A.V. Features of the phenotype and NAD(P)-dependent dehydrogenases activity in neutrophil by patients with widespread purulent peritonitis in prognosis for sepsis development. Infektsiya i immunitet = Russian Journal of Infection and Immunity, 2018, vol. 8, no. 3, pp. 369–376. (In Russ.)] doi: 10.15789/2220-7619-2018-3-369-376
  6. Табаков Д.В., Заботина Т.Н., Борунова А.А., Панчук И.О., Короткова О.В., Кадагидзе З.Г. Гетерогенность популяций NK и NKT-лимфоцитов у здоровых доноров // Медицинская иммунология. 2017. Т. 19, № 4. С. 401–408. [Tabakov D.V., Zabotina T.N., Borunova A.A., Panchuk I.O., Korotkova O.V., Kadagidze Z.G. Heterogeneity of NK and NKT lymphocyte populations in healthy donors. Meditsinskaya immunologiya = Medical Immunology (Russia), 2017, vol. 19, no. 4, pp. 401–408. (In Russ.)] doi: 10. 15789/1563-0625-2017-4-401-408
  7. Хайдуков С.В., Байдун Л.А., Зурочка А.В., Тотолян Арег А. Стандартизованная технология «Исследование субпопуляционного состава лимфоцитов периферической крови с применением проточных цитофлюориметров анализаторов» (проект) // Медицинская иммунология. 2012. Т. 14, № 3. С. 255–268. [Khaydukov S.V., Baydun L.A., Zurochka A.V., Totolian Areg A. Standardized technology «Research of lymphocytes subpopulation composition in peripheral blood using flow cytometry analyzers» (Draft). Meditsinskaya immunologiya = Medical Immunology (Russia), 2012, vol. 14, no. 3, pp. 255–268. (In Russ.)] doi: 10.15789/1563-0625-2012-3-255-268
  8. Almeida J.S., Couceiro P., López-Sejas N., Alves V., Růžičková L., Tarazona R., Solana R., Freitas-Tavares P., Santos-Rosa M., Rodrigues-Santos P. NKT-like (CD3+CD56+) cells in chronic myeloid leukemia patients treated with tyrosine kinase inhibitors. Front. Immunol., 2019, vol. 10, pp. 2493. doi: 10.3389/fimmu. 2019.02493
  9. Bae E.A., Seo H., Kim I.K., Jeon I., Kang C.Y. Roles of NKT cells in cancer immunotherapy. Arch. Pharm. Res., 2019, vol. 42, no. 7, pp. 543–548. doi: 10.1007/s12272-019-01139-8
  10. Bendelac A., Savage P.B., Teyton L. The biology of NKT cells. Annu. Rev. Immunol., 2007, vol. 25, pp. 297–336. doi: 10.1146/annurev. immunol.25.022106. 141711
  11. Brailey P.M., Lebrusant-Fernandez M., Barral P. NKT cells and the regulation of intestinal immunity: a two-way street. FEBS J., 2020, vol. 287, no. 9, pp. 1686–1699. doi: 10.1111/febs.15238
  12. Cairo C., Webb T.J. Effective barriers: the role of NKT cells and innate lymphoid cells in the gut. J. Immunol., 2022, vol. 208, no. 2, pp. 235–246. doi: 10.4049/jimmunol. 2100799
  13. Ceeraz S., Thompson C.R., Beatson R., Choy E.H. Harnessing CD8+CD28– regulatory T cells as a tool to treat autoimmune disease. Cells, 2021, vol. 10, no. 11, pp. 2973. doi: 10.3390/cells10112973
  14. Chen Y., Tian Z. Innate lymphocytes: pathogenesis and therapeutic targets of liver diseases and cancer. Cell. Mol. Immunol., 2021, vol. 18, no. 1, pp. 57–72. doi: 10.1038/s41423-020-00561-z
  15. Cichoż-Lach H., Grywalska E., Michalak A., Kowalik A., Mielnik M., Roliński J. Deviations in peripheral blood cell populations are associated with the stage of primary biliary cholangitis and presence of itching. Arch. Immunol. Ther. Exp. (Warsz), 2018, vol. 66, no. 6, pp. 443–452. doi: 10.1007/s00005-018-0515-9
  16. De Andrés C., Fernández-Paredes L., Tejera-Alhambra M., Alonso B., Ramos-Medina R., Sánchez-Ramón S. Activation of blood CD3+CD56+CD8+ T cells during pregnancy and multiple sclerosis. Front. Immunol., 2017, vol. 8, pp. 196. doi: 10.3389/fimmu. 2017.00196
  17. Farrington L.A., Callaway P.C., Vance H.M., Baskevitch K., Lutz E., Warrier L., McIntyre T.I., Budker R., Jagannathan P., Nankya F., Musinguzi K., Nalubega M., Sikyomu E., Naluwu K., Arinaitwe E., Dorsey G., Kamya M.R., Feeney M.E. Opsonized antigen activates Vδ2+ T cells via CD16/FCγRIIIa in individuals with chronic malaria exposure. PLoS Pathog., 2020, vol. 16, no. 10: e1008997. doi: 10.1371/journal.ppat. 1008997
  18. Ferrari L., Martelli P., Saleri R., De Angelis E., Ferrarini G., Cavalli V., Passeri B., Bazzoli G., Ogno G., Magliani W., Borghetti P. An engineered anti-idiotypic antibody-derived killer peptide (KP) early activates swine inflammatory monocytes, CD3+CD16+ natural killer T cells and CD4+CD8α+ double positive CD8β+ cytotoxic T lymphocytes associated with TNF-α and IFN-γ secretion. Comp. Immunol. Microbiol. Infect. Dis., 2020, vol. 72, pp. 101523. doi: 10.1016/j.cimid. 2020.101523
  19. Gao Y.L., Yao Y., Zhang X., Chen F., Meng X.L., Chen X.S., Wang C.L., Liu Y.C., Tian X., Shou S.T., Chai Y.F. Regulatory T cells: angels or demons in the pathophysiology of sepsis? Front. Immunol., 2022, vol. 13, pp. 829210. doi: 10.3389/fimmu. 2022.829210
  20. González-Osuna L., Sierra-Cristancho A., Cafferata E.A., Melgar-Rodríguez S., Rojas C., Carvajal P., Cortez C., Vernal R. Senescent CD4+CD28– T lymphocytes as a potential driver of Th17/Treg imbalance and alveolar bone resorption during periodontitis. Int. J. Mol. Sci., 2022, vol. 23, no. 5, pp. 2543. doi: 10.3390/ ijms23052543
  21. Goswami M., Sharma D., Khan N.M., Checker R., Sandur S.K., Jawali N. Antioxidant supplementation enhances bacterial peritonitis in mice by inhibiting phagocytosis. J. Med. Microbiol., 2014, vol. 63, pt 3, pp. 355–366. doi: 10.1099/jmm.0.067173-0
  22. Hu J., Yi B., Zhang H. Influence of climatic factors on single-center peritoneal dialysis-associated peritonitis. Zhong Nan Da Xue Xue Bao Yi Xue Ban, 2022, vol. 47, no. 5, pp. 639–649. doi: 10.11817/j.issn.1672-7347.2022.210506
  23. Huang H., Liu Y., Ouyang X., Wang H., Zhang Y. Identification of a peptide targeting CD56. Immunobiology, 2020, vol. 225, no. 4: 151982. doi: 10.1016/j.imbio. 2020.151982
  24. Ibidapo-Obe O., Stengel S., Köse-Vogel N., Quickert S., Reuken P.A., Busch M., Bauer M., Stallmach A., Bruns T. Mucosal-associated invariant T cells redistribute to the peritoneal cavity during spontaneous bacterial peritonitis and contribute to peritoneal inflammation. Cell. Mol. Gastroenterol. Hepatol., 2020, vol. 9, no. 4, pp. 661–677. doi: 10.1016/j.jcmgh. 2020.01.003
  25. Kabanov D.S., Grachev S.V., Prokhorenko I.R. Monoclonal antibody to CD14, TLR4, or CD11b: impact of epitope and isotype specificity on ROS generation by human granulocytes and monocytes. Oxid. Med. Cell. Longev., 2020, vol. 2020: 5708692. doi: 10.1155/2020/5708692
  26. Khan S.Q., Khan I., Gupta V. CD11b activity modulates pathogenesis of lupus nephritis. Front. Med. (Lausanne), 2018, vol. 5: 52. doi: 10.3389/fmed. 2018.00052
  27. Kumar V.V., Verma A., Thakur D.S., Somashekar U., Kothari R., Sharma D. Prophylactic mesh placement in emergency midline laparotomy for intestinal perforation peritonitis: an appeal for caution. Trop. Doct., 2022, vol. 23: e494755221110831. doi: 10.1177/ 00494755221110831
  28. Lotte R., Courdurié A., Gaudart A., Emery A., Chevalier A., Tran A., Payen M., Ruimy R. Spontaneous bacterial peritonitis: the incremental value of a fast and direct bacterial identification from ascitic fluids inoculated in blood culture bottles by MALDI-TOF MS for a better management of patients. Microorganisms, 2022, vol. 10, no. 6: 1188. doi: 10.3390/ microorganisms 10061188
  29. Lu Y., Li Y., Zhou W., Ding B., Yu Q. Regulatory T cells regulate the distribution of natural killer T cells through CD39 signal transduction in asthma. Hum. Cell., 2019, vol. 32, no. 2, pp. 141–149. doi: 10.1007/s13577-018-00226-0
  30. Ngiow S.F., Young A. Re-education of the tumor microenvironment with targeted therapies and immunotherapies. Front. Immunol., 2020, vol. 11: 1633. doi: 10.3389/fimmu. 2020.01633
  31. Nilsson J., Hörnberg M., Schmidt-Christensen A., Linde K., Nilsson M., Carlus M., Erttmann S.F., Mayans S., Holmberg D. NKT cells promote both type 1 and type 2 inflammatory responses in a mouse model of liver fibrosis. Sci. Rep., 2020, vol. 10, no. 1: 21778. doi: 10.1038/s41598-020-78688-2
  32. Noma H., Eshima K., Satoh M., Iwabuchi K. Differential dependence on nuclear factor-κB-inducing kinase among natural killer T-cell subsets in their development. Immunology, 2015, vol. 146, no. 1, pp. 89–99. doi: 10.1111/imm.12484
  33. Pinson J., Tuech J.J., Ouaissi M., Mathonnet M., Mauvais F., Houivet E., Lacroix E., Rondeaux J., Sabbagh C., Bridoux V. Role of protective stoma after primary anastomosis for generalized peritonitis due to perforated diverticulitis-DIVERTI 2 (a prospective multicenter randomized trial): rationale and design (nct04604730). BMC Surg., 2022, vol. 22, no. 1: 191. doi: 10.1186/s12893-022-01589-w
  34. Rajabaleyan P., Michelsen J., Tange Holst U., Möller S., Toft P., Luxhøi J., Buyukuslu M., Bohm A.M., Borly L., Sandblom G., Kobborg M., Aagaard Poulsen K., Schou Løve U., Ovesen S., Grant Sølling C., Mørch Søndergaard B., Lund Lomholt M., Ritz Møller D., Qvist N., Bremholm Ellebæk M.; VACOR study group. Vacuum-assisted closure versus on-demand relaparotomy in patients with secondary peritonitis-the VACOR trial: protocol for a randomised controlled trial. World J. Emerg. Surg., 2022, vol. 17, no. 1: 25. doi: 10.1186/s13017-022-00427-x
  35. Senpuku H., Miyazaki H., Yoshihara A., Yoneda S., Narisawa N., Kawarai T., Nakagawa N., Miyachi M., Tada A., Yoshida G., Shimada M., Ohashi M., Nishimuta M., Kimura Y., Yoshitake Y. CD56(dim)CD16(high) and CD56(bright)CD16(–) cell percentages associated with maximum knee extensor strength and incidence of death in elderly. Springerplus, 2016, vol. 5: 244. doi: 10.1186/s40064-016-1884-3
  36. Shen H., Gu C., Liang T., Liu H., Guo F., Liu X. Unveiling the heterogeneity of NKT cells in the liver through single cell RNA sequencing. Sci. Rep., 2020, vol. 10, no. 1: 19453. doi: 10.1038/s41598-020-76659-1
  37. Shissler S.C., Singh N.J., Webb T.J. Thymic resident NKT cell subsets show differential requirements for CD28 co-stimulation during antigenic activation. Sci. Rep., 2020, vol. 10, no. 1: 8218. doi: 10.1038/s41598-020-65129-3
  38. Stengel S., Quickert S., Lutz P., Ibidapo-Obe O., Steube A., Köse-Vogel N., Yarbakht M., Reuken P.A., Busch M., Brandt A., Bergheim I., Deshmukh S.D., Stallmach A., Bruns T. Peritoneal level of CD206 associates with mortality and an inflammatory macrophage phenotype in patients with decompensated cirrhosis and spontaneous bacterial peritonitis. Gastroenterology, 2020, vol. 158, no. 6, pp. 1745–1761. doi: 10.1053/j.gastro. 2020.01.029
  39. Terabe M., Berzofsky J.A. Tissue-specific roles of NKT cells in tumor immunity. Front. Immunol., 2018, vol. 9: 1838. doi: 10.3389/fimmu. 2018.01838
  40. Vogt S., Mattner J. NKT cells contribute to the control of microbial infections. Front. Cell. Infect. Microbiol., 2021, vol. 11: 718350. doi: 10.3389/fcimb. 2021.718350
  41. Yang L., Liu S., Zhang Q., Jia S., Qiu C., Jin Z. Overexpression of ascitic interleukin-35 induces CD8+ T cell exhaustion in liver cirrhotic patients with spontaneous bacterial peritonitis. Int. Immunopharmacol., 2022, vol. 108: 108729. doi: 10.1016/j.intimp. 2022.108729

补充文件

附件文件
动作
1. JATS XML
下载

版权所有 © Savchenko A.A., Borisov A.G., Kudryavtsev I.V., Belenjuk V.D., 2022

Creative Commons License
此作品已接受知识共享署名 4.0国际许可协议的许可
##common.cookie##