T helper cell subsets and related target cells in acute COVID-19
- Authors: Kudryavtsev I.V.1,2, Golovkin A.S.3, Totolian A.A.1,4
-
Affiliations:
- I.P. Pavlov First St. Petersburg State Medical University of the Ministry of Healthcare of Russian Federation
- Institute of Experimental Medicine
- V.A. Almazov National Medical Research Centre
- St. Petersburg Pasteur Institute
- Issue: Vol 12, No 3 (2022)
- Pages: 409-426
- Section: REVIEWS
- URL: https://bakhtiniada.ru/2220-7619/article/view/119036
- DOI: https://doi.org/10.15789/2220-7619-THC-1882
- ID: 119036
Cite item
Full Text
Abstract
Current review presents a brief overview of the immune system dysregulation during acute COVID-19 and illustrates the main alterations in peripheral blood CD4+ T-cell (Th) subsets as well as related target cells. Effects of dendritic cell dysfunction induced by SARS-CoV-2 exhibited decreased expression of cell-surface HLA-DR, CCR7 as well as co-stimulatory molecules CD80 and CD86, suggesting reduced antigen presentation, migratory and activation capacities of peripheral blood dendritic cells. SARS-CoV-2-specific Th cells could be detected as early as days 2–4 post-symptom onset, whereas the prolonged lack of SARS-CoV-2-specific Th cells was associated with severe and/or poor COVID-19 outcome. Firstly, in acute COVID-19 the frequency of Th1 cell was comparable with control levels, but several studies have reported about upregulated inhibitory immune checkpoint receptors and exhaustion-associated molecules (TIM3, PD-1, BTLA, TIGIT etc.) on circulating CD8+ T-cells and NK-cells, whereas the macrophage count was increased in bronchoalveolar lavage (BAL) samples. Next, type 2 immune responses are mediated mainly by Th2 cells, and several studies have revealed a skewing towards dominance of Th2 cell subset in peripheral blood samples from patients with acute COVID-19. Furthermore, the decrease of circulating main Th2 target cells — basophiles and eosinophils — were associated with severe COVID-19, whereas the lung tissue was enriched with mast cells and relevant mediators released during degranulation. Moreover, the frequency of peripheral blood Th17 cells was closely linked to COVID-19 severity, so that low level of Th17 cells was observed in patients with severe COVID-19, but in BAL the relative number of Th17 cells as well as the concentrations of relevant effector cytokines were dramatically increased. It was shown that severe COVID-19 patients vs. healthy control had higher relative numbers of neutrophils if compared, and the majority of patients with COVID-19 had increased frequency and absolute number of immature neutrophils with altered ROS production. Finally, the frequency of Tfh cells was decreased during acute COVID-19 infection. Elevated count of activated Tfh were found as well as the alterations in Tfh cell subsets characterized by decreased “regulatory” Tfh1 cell and increased “pro-inflammatory” Tfh2 as well as Tfh17 cell subsets were revealed. Descriptions of peripheral blood B cells during an acute SARS-CoV-2 infection werev reported as relative B cell lymphopenia with decreased frequency of “naïve” and memory B cell subsets, as well as increased level of CD27hiCD38hiCD24– plasma cell precursors and atypical CD21low B cells. Thus, the emerging evidence suggests that functional alterations occur in all Th cell subsets being linked with loss-of-functions of main Th cell subsets target cells. Furthermore, recovered individuals could suffer from long-term immune dysregulation and other persistent symptoms lasting for many months even after SARS-CoV-2 elimination, a condition referred to as post-acute COVID-19 syndrome.
Keywords
Full Text
##article.viewOnOriginalSite##About the authors
I. V. Kudryavtsev
I.P. Pavlov First St. Petersburg State Medical University of the Ministry of Healthcare of Russian Federation; Institute of Experimental Medicine
Author for correspondence.
Email: igorek1981@yandex.ru
PhD (Biology), Head of the Cell Immunology Laboratory, Department of Immunology, Assistant Professor, Department of Immunology
Russian Federation, St. Petersburg; St. PetersburgA. S. Golovkin
V.A. Almazov National Medical Research Centre
Email: golovkin_a@mail.ru
PhD, MD (Medicine), Head of a Research Group of Genetic Cell Engineering, Institute of Molecular Biology and Genetics
Russian Federation, St. PetersburgAreg A. Totolian
I.P. Pavlov First St. Petersburg State Medical University of the Ministry of Healthcare of Russian Federation; St. Petersburg Pasteur Institute
Email: totolian@pasteurorg.ru
RAS Full Member, PhD, MD (Medicine), Professor, Head of the Department of Immunology, Director
Russian Federation, St. Petersburg; St. PetersburgReferences
- Арсентьева Н.А., Любимова Н.Е., Бацунов О.К., Коробова З.Р., Станевич О.В., Лебедева А.А., Воробьев Е.А., Воробьева С.В., Куликов А.Н., Лиознов Д.А., Шарапова М.А., Певцов Д.Э., Тотолян А.А. Цитокины в плазме крови больных COVID-19 в острой фазе заболевания и фазе полного выздоровления // Медицинская иммунология. 2021. Т. 23, № 2. С. 311–326. [Arsentieva N.A., Liubimova N.E., Batsunov O.K., Korobova Z.R., Stanevich O.V., Lebedeva A.A., Vorobyov E.A., Vorobyova S.V., Kulikov A.N., Lioznov D.A., Sharapova M.A., Pevtcov D.E., Totolian A.A. Plasma cytokines in patients with COVID-19 during acute phase of the disease and following complete recovery. Meditsinskaya immunologiya = Medical Immunology (Russia), 2021, vol. 23, no. 2, pp. 311–326 (In Russ.)] doi: 10.15789/1563-0625-PCI-2312
- Иванова И.А., Омельченко Н.Д., Филиппенко А.В., Труфанова А.А., Носков А.К. Роль клеточного звена иммунитета в формировании иммунного ответа при коронавирусных инфекциях // Медицинская иммунология. 2021. Т. 23, № 6. С. 1229–1238. [Ivanova I.A., Omelchenko N.D., Filippenko A.V., Trufanova A.A., Noskov A.K. Role of the cellular immunity in the formation of the immune response in coronavirus infections. Meditsinskaya immunologiya = Medical Immunology (Russia), 2021, vol. 23, no. 6, pp. 1229–1238. (In Russ.)] doi: 10.15789/1563-0625-ROT-2302
- Кудрявцев И.В., Борисов А.Г., Васильева Е.В., Кробинец И.И., Савченко А.А., Серебрякова М.К., Тотолян Арег А. Фенотипическая характеристика цитотоксических Т-лимфоцитов: регуляторные и эффекторные молекулы // Медицинская иммунология. 2018. Т. 20, № 2. С. 227–240. [Kudryavtsev I.V., Borisov A.G., Vasilyeva E.V., Krobinets I.I., Savchenko A.A., Serebriakova M.K., Totolian Areg A. Phenotypic characterisation of peripheral blood cytotoxic T lymphocytes: regulatory and effector molecules. Meditsinskaya immunologiya = Medical Immunology (Russia), 2018, vol. 20, no. 2, pp. 227–240. (In Russ.)] doi: 10.15789/1563-0625-2018-2-227-240
- Кудрявцев И.В., Борисов А.Г., Кробинец И.И., Савченко А.А., Серебрякова М.К., Тотолян А.А. Хемокиновые рецепторы на Т-хелперах различного уровня дифференцировки: основные субпопуляции // Медицинская иммунология. 2016. Т. 18, № 3. С. 239–250. [Kudryavtsev I.V., Borisov A.G., Krobinets I.I., Savchenko A.A., Serebriakova M.K., Totolian A.A. Chemokine receptors at distinct differentiation stages of T-helpers from peripheral blood. Meditsinskaya immunologiya = Medical Immunology (Russia), 2016, vol. 18, no. 3, pp. 239-250. (In Russ.)]. doi: 10.15789/1563-0625-2016-3-239-250
- Лядова И.В., Стариков А.А. COVID-19 и вакцинация БЦЖ: есть ли связь? // Инфекция и иммунитет. 2020. Т. 10, № 3. С. 459–468. [Lyadova I.V., Starikov A.A. COVID-19 and BCG vaccine: is there a link? Infektsiya i immunitet = Russian Journal of Infection and Immunity, 2020, vol. 10, no. 3, pp. 459–468. (In Russ.)] doi: 10.15789/2220-7619-CAB-1472
- Смирнов В.С., Тотолян А.А. Врожденный иммунитет при коронавирусной инфекции // Инфекция и иммунитет. 2020. Т. 10, № 2. С. 259–268. [Smirnov V.S., Totolian A.A. Innate immunity in coronavirus infection. Infektsiya i immunitet = Russian Journal of Infection and Immunity, 2020, vol. 10, no. 2, pp. 259–268. (In Russ.)] doi: 10.15789/2220-7619-111-1440
- Afrin L.B., Weinstock L.B., Molderings G.J. Covid-19 hyperinflammation and post-Covid-19 illness may be rooted in mast cell activation syndrome. Int. J. Infect. Dis., 2020, vol. 100, pp. 327–332. doi: 10.1016/j.ijid.2020.09.016
- Alcorn J.F. IL-22 plays a critical role in maintaining epithelial integrity during pulmonary infection. Front. Immunol., 2020, vol. 11: 1160. doi: 10.3389/fimmu.2020.01160
- Amer S.A., Albeladi O.A., Elshabrawy A.M., Alsharief N.H., Alnakhli F.M., Almugathaui A.F., Almashahadi S.S., Dawood H.M., Malik M.B., Shah J., Aiash H. Role of neutrophil to lymphocyte ratio as a prognostic indicator for COVID-19. Health Sci. Rep., 2021, vol. 4, no. 4: e442. doi: 10.1002/hsr2.442
- Annunziato F., Romagnani C., Romagnani S. The 3 major types of innate and adaptive cell-mediated effector immunity. J. Allergy Clin. Immunol., 2015, vol. 135, no. 3, pp. 626–635. doi: 10.1016/j.jaci.2014.11.001
- Bakin E.A., Stanevich O.V., Chmelevsky M.P., Belash V.A., Belash A.A., Savateeva G.A., Bokinova V.A., Arsentieva N.A., Sayenko L.F., Korobenkov E.A., Lioznov D.A., Totolian A.A., Polushin Y.S., Kulikov A.N. A novel approach for COVID-19 patient condition tracking: from instant prediction to regular monitoring. Front. Med. (Lausanne), 2021, vol. 8: 744652. doi: 10.3389/fmed.2021.744652
- Bonecchi R., Bianchi G., Bordignon P.P., D’Ambrosio D., Lang R., Borsatti A., Sozzani S., Allavena P., Gray P.A., Mantovani A., Sinigaglia F. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med., 1998, vol. 187, no. 1, pp. 129–134. doi: 10.1084/jem.187.1.129
- Boppana S., Qin K., Files J.K., Russell R.M., Stoltz R., Bibollet-Ruche F., Bansal A., Erdmann N., Hahn B.H., Goepfert P.A. SARS-CoV-2-specific circulating T follicular helper cells correlate with neutralizing antibodies and increase during early convalescence. PLoS Pathog., 2021, vol. 17, no. 7: e1009761. doi: 10.1371/journal.ppat.1009761
- Braun J., Loyal L., Frentsch M., Wendisch D., Georg P., Kurth F., Hippenstiel S., Dingeldey M., Kruse B., Fauchere F., Baysal E., Mangold M., Henze L., Lauster R., Mall M.A., Beyer K., Röhmel J., Voigt S., Schmitz J., Miltenyi S., Demuth I., Müller M.A., Hocke A., Witzenrath M., Suttorp N., Kern F., Reimer U., Wenschuh H., Drosten C., Corman V.M., Giesecke-Thiel C., Sander L.E., Thiel A. SARS-CoV-2-reactive T cells in healthy donors and patients with COVID-19. Nature, 2020, vol. 587, no. 7833, pp. 270–274. doi: 10.1038/s41586-020-2598-9
- Byazrova M., Yusubalieva G., Spiridonova A., Efimov G., Mazurov D., Baranov K., Baklaushev V., Filatov A. Pattern of circulating SARS-CoV-2-specific antibody-secreting and memory B-cell generation in patients with acute COVID-19. Clin. Transl. Immunology, 2021, vol. 10, no. 2: e1245. doi: 10.1002/cti2.1245
- Cai H., Liu G., Zhong J., Zheng K., Xiao H., Li C., Song X., Li Y., Xu C., Wu H., He Z., Zhu Q. Immune checkpoints in viral infections. Viruses, 2020, vol. 12, no. 9: 1051. doi: 10.3390/v12091051
- Chen G., Wu D., Guo W., Cao Y., Huang D., Wang H., Wang T., Zhang X., Chen H., Yu H., Zhang X., Zhang M., Wu S., Song J., Chen T., Han M., Li S., Luo X., Zhao J., Ning Q. Clinical and immunological features of severe and moderate coronavirus disease 2019. J. Clin. Invest., 2020, vol. 130, no. 5, pp. 2620–2629. doi: 10.1172/JCI137244
- Chevrier S., Zurbuchen Y., Cervia C., Adamo S., Raeber M.E., de Souza N., Sivapatham S., Jacobs A., Bachli E., Rudiger A., Stüssi-Helbling M., Huber L.C., Schaer D.J., Nilsson J., Boyman O., Bodenmiller B. A distinct innate immune signature marks progression from mild to severe COVID-19. Cell Rep. Med., 2020, vol. 2, no. 1: 100166. doi: 10.1016/j.xcrm.2020.100166
- Chua R.L., Lukassen S., Trump S., Hennig B.P., Wendisch D., Pott F., Debnath O., Thürmann L., Kurth F., Völker M.T., Kazmierski J., Timmermann B., Twardziok S., Schneider S., Machleidt F., Müller-Redetzky H., Maier M., Krannich A., Schmidt S., Balzer F., Liebig J., Loske J., Suttorp N., Eils J., Ishaque N., Liebert U.G., von Kalle C., Hocke A., Witzenrath M., Goffinet C., Drosten C., Laudi S., Lehmann I., Conrad C., Sander L.E., Eils R. COVID-19 severity correlates with airway epithelium-immune cell interactions identified by single-cell analysis. Nat. Biotechnol., 2020, vol. 38, no. 8, pp. 970–979. doi: 10.1038/s41587-020-0602-4
- Collin M., Bigley V. Human dendritic cell subsets: an update. Immunology, 2018, vol. 154, pp. 3–20. doi: 10.1111/imm.12888
- Cortés-Vieyra R., Gutiérrez-Castellanos S., Álvarez-Aguilar C., Baizabal-Aguirre V.M., Nuñez-Anita R.E., Rocha-López A.G., Gómez-García A. Behavior of eosinophil counts in recovered and deceased COVID-19 patients over the course of the disease. Viruses, 2021 vol. 13, no. 9: 1675. doi: 10.3390/v13091675
- Crotty S. T follicular helper cell biology: a decade of discovery and diseases. Immunity, 2019, vol. 50, no. 5, pp. 1132–1148. doi: 10.1016/j.immuni.2019.04.011
- De Biasi S., Meschiari M., Gibellini L., Bellinazzi C., Borella R., Fidanza L., Gozzi L., Iannone A., Lo Tartaro D., Mattioli M., Paolini A., Menozzi M., Milić J., Franceschi G., Fantini R., Tonelli R., Sita M., Sarti M., Trenti T., Brugioni L., Cicchetti L., Facchinetti F., Pietrangelo A., Clini E., Girardis M., Guaraldi G., Mussini C., Cossarizza A. Marked T cell activation, senescence, exhaustion and skewing towards TH17 in patients with COVID-19 pneumonia. Nat. Commun., 2020, vol. 11, no. 1: 3434. doi: 10.1038/s41467-020-17292-4
- Demaria O., Carvelli J., Batista L., Thibult M.L., Morel A., André P., Morel Y., Vély F., Vivier E. Identification of druggable inhibitory immune checkpoints on natural killer cells in COVID-19. Cell Mol. Immunol., 2020, vol. 17, no. 9, pp. 995–997. doi: 10.1038/s41423-020-0493-9
- Dewanjee S., Kandimalla R., Kalra R.S., Valupadas C., Vallamkondu J., Kolli V., Dey Ray S., Reddy A.P., Reddy P.H. COVID-19 and rheumatoid arthritis crosstalk: emerging association, therapeutic options and challenges. Cells, 2021, vol. 10, no. 12: 3291. doi: 10.3390/cells10123291
- Durand M., Walter T., Pirnay T., Naessens T., Gueguen P., Goudot C., Lameiras S., Chang Q., Talaei N., Ornatsky O., Vassilevskaia T., Baulande S., Amigorena S., Segura E. Human lymphoid organ cDC2 and macrophages play complementary roles in T follicular helper responses. J. Exp. Med., 2019, vol. 216, no. 7, pp. 1561–1581. doi: 10.1084/jem.20181994
- Eberl G. Immunity by equilibrium. Nat. Rev. Immunol., 2016, vol. 16, no. 8, pp. 524–532. doi: 10.1038/nri.2016.75
- Gebremeskel S., Schanin J., Coyle K.M., Butuci M., Luu T., Brock E.C., Xu A., Wong A., Leung J., Korver W., Morin R.D., Schleimer R.P., Bochner B.S., Youngblood B.A. Mast cell and eosinophil activation are associated with COVID-19 and TLR-mediated viral inflammation: implications for an anti-siglec-8 antibody. Front. Immunol., 2021, vol. 12: 650331. doi: 10.3389/fimmu.2021.650331
- Giamarellos-Bourboulis E.J., Netea M.G., Rovina N., Akinosoglou K., Antoniadou A., Antonakos N., Damoraki G., Gkavogianni T., Adami M.E., Katsaounou P., Ntaganou M., Kyriakopoulou M., Dimopoulos G., Koutsodimitropoulos I., Velissaris D., Koufargyris P., Karageorgos A., Katrini K., Lekakis V., Lupse M., Kotsaki A., Renieris G., Theodoulou D., Panou V., Koukaki E., Koulouris N., Gogos C., Koutsoukou A. Complex immune dysregulation in COVID-19 patients with severe respiratory failure. Cell Host Microbe, 2020, vol. 27, no. 6, pp. 992–1000.e3. doi: 10.1016/j.chom.2020.04.009
- Gil-Etayo F.J., Suàrez-Fernández P., Cabrera-Marante O., Arroyo D., Garcinuño S., Naranjo L., Pleguezuelo D.E., Allende L.M., Mancebo E., Lalueza A., Díaz-Simón R., Paz-Artal E., Serrano A. T-helper cell subset response is a determining factor in COVID-19 progression. Front. Cell Infect. Microbiol., 2021, vol. 11: 624483. doi: 10.3389/fcimb.2021.624483
- Golovkin A., Kalinina O., Bezrukikh V., Aquino A., Zaikova E., Karonova T., Melnik O., Vasilieva E., Kudryavtsev I. Imbalanced immune response of T-cell and B-cell subsets in patients with moderate and severe COVID-19. Viruses, 2021, vol. 13, no. 10: 1966. doi: 10.3390/v13101966
- Gong F., Dai Y., Zheng T., Cheng L., Zhao D., Wang H., Liu M., Pei H., Jin T., Yu D., Zhou P. Peripheral CD4+ T cell subsets and antibody response in COVID-19 convalescent individuals. J. Clin. Invest., 2020, vol. 130, no. 12, pp. 6588–6599. doi: 10.1172/JCI141054
- Gosain R., Abdou Y., Singh A., Rana N., Puzanov I., Ernstoff M.S. COVID-19 and cancer: a comprehensive review. Curr. Oncol. Rep., 2020, vol. 22, no. 5, pp. 53. doi: 10.1007/s11912-020-00934-7
- Grifoni A., Sidney J., Vita R., Peters B., Crotty S., Weiskopf D., Sette A. SARS-CoV-2 human T cell epitopes: adaptive immune response against COVID-19. Cell Host Microbe, 2021, vol. 29, no. 7, pp. 1076–1092. doi: 10.1016/j.chom.2021.05.010
- Grifoni A., Weiskopf D., Ramirez S.I., Mateus J., Dan J.M., Moderbacher C.R., Rawlings S.A., Sutherland A., Premkumar L., Jadi R.S., Marrama D., de Silva A.M., Frazier A., Carlin A.F., Greenbaum J.A., Peters B., Krammer F., Smith D.M., Crotty S., Sette A. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell, 2020, vol. 181, no. 7, pp. 1489–1501.e15. doi: 10.1016/j.cell.2020.05.015
- Guilliams M., Ginhoux F., Jakubzick C., Naik S.H., Onai N., Schraml B.U., Segura E., Tussiwand R., Yona S. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat. Rev. Immunol., 2014, vol. 14, no. 8, pp. 571–578. doi: 10.1038/nri3712
- Guizani I., Fourti N., Zidi W., Feki M., Allal-Elasmi M. SARS-CoV-2 and pathological matrix remodeling mediators. Inflamm. Res., 2021, vol. 70, no. 8, pp. 847–858. doi: 10.1007/s00011–021-01487-6
- Gutiérrez-Bautista J.F., Rodriguez-Nicolas A., Rosales-Castillo A., Jiménez P., Garrido F., Anderson P., Ruiz-Cabello F., López-Ruz M.Á. Negative clinical evolution in COVID-19 patients is frequently accompanied with an increased proportion of undifferentiated Th cells and a strong underrepresentation of the Th1 subset. Front. Immunol., 2020, vol. 11: 596553. doi: 10.3389/fimmu.2020.596553
- Hou H., Zhang Y., Tang G., Luo Y., Liu W., Cheng C., Jiang Y., Xiong Z., Wu S., Sun Z., Xu S., Fan X., Wang F. Immunologic memory to SARS-CoV-2 in convalescent COVID-19 patients at 1 year postinfection. J. Allergy Clin. Immunol., 2021, vol. 148, no. 6, pp. 1481–1492.e2. doi: 10.1016/j.jaci.2021.09.008
- Hou Y., Zhao J., Martin W., Kallianpur A., Chung M.K., Jehi L., Sharifi N., Erzurum S., Eng C., Cheng F. New insights into genetic susceptibility of COVID-19: an ACE2 and TMPRSS2 polymorphism analysis. BMC Med., 2020, vol. 18, no. 1: 216. doi: 10.1186/s12916–020-01673-z
- Hume D.A., Irvine K.M., Pridans C. The mononuclear phagocyte system: the relationship between monocytes and macrophages. Trends Immunol., 2019, vol. 40, no. 2, pp. 98–112. doi: 10.1016/j.it.2018.11.007
- Iwamura A.P.D., Tavares da Silva M.R., Hümmelgen A.L., Soeiro Pereira P.V., Falcai A., Grumach A.S., Goudouris E., Neto A.C., Prando C. Immunity and inflammatory biomarkers in COVID-19: a systematic review. Rev. Med. Virol., 2021, vol. 31, no. 4: e2199. doi: 10.1002/rmv.2199
- Izcovich A., Ragusa M.A., Tortosa F., Lavena Marzio M.A., Agnoletti C., Bengolea A., Ceirano A., Espinosa F., Saavedra E., Sanguine V., Tassara A., Cid C., Catalano H.N., Agarwal A., Foroutan F., Rada G. Prognostic factors for severity and mortality in patients infected with COVID-19: a systematic review. PLoS One, 2020, vol. 15, no. 11: e0241955. doi: 10.1371/journal.pone.0241955
- Jennings G., Monaghan A., Xue F., Mockler D., Romero-Ortuño R. A systematic review of persistent symptoms and residual abnormal functioning following acute COVID-19: ongoing symptomatic phase vs. post-COVID-19 syndrome. J. Clin. Med., 2021, vol. 10, no. 24: 5913. doi: 10.3390/jcm10245913
- Jiang Y., Wei X., Guan J., Qin S., Wang Z., Lu H., Qian J., Wu L., Chen Y., Chen Y., Lin X. COVID-19 pneumonia: CD8+ T and NK cells are decreased in number but compensatory increased in cytotoxic potential. Clin. Immunol., 2020, vol. 218: 108516. doi: 10.1016/j.clim.2020.108516
- Juno J.A., Tan H.X., Lee W.S., Reynaldi A., Kelly H.G., Wragg K., Esterbauer R., Kent H.E., Batten C.J., Mordant F.L., Gherardin N.A., Pymm P., Dietrich M.H., Scott N.E., Tham W.H., Godfrey D.I., Subbarao K., Davenport M.P., Kent S.J., Wheatley A.K. Humoral and circulating follicular helper T cell responses in recovered patients with COVID-19. Nat. Med., 2020, vol. 26, no. 9, pp. 1428–1434. doi: 10.1038/s41591–020-0995-0
- Kalfaoglu B., Almeida-Santos J., Tye C.A., Satou Y., Ono M. T-cell hyperactivation and paralysis in severe COVID-19 infection revealed by single-cell analysis. Front. Immunol., 2020, vol. 11: 589380. doi: 10.3389/fimmu.2020.589380
- Kanannejad Z., Alyasin S., Esmaeilzadeh H., Nabavizadeh H., Amin R. Asthma and COVID-19 pandemic: focused on the eosinophil count and ACE2 expression. Eur. Ann. Allergy Clin. Immunol., 2021. doi: 10.23822/EurAnnACI.1764–1489.233
- Kaneko N., Kuo H.H., Boucau J., Farmer J.R., Allard-Chamard H., Mahajan V.S., Piechocka-Trocha A., Lefteri K., Osborn M., Bals J., Bartsch Y.C., Bonheur N., Caradonna T.M., Chevalier J., Chowdhury F., Diefenbach T.J., Einkauf K., Fallon J., Feldman J., Finn K.K., Garcia-Broncano P., Hartana C.A., Hauser B.M., Jiang C., Kaplonek P., Karpell M., Koscher E.C., Lian X., Liu H., Liu J., Ly N.L., Michell A.R., Rassadkina Y., Seiger K., Sessa L., Shin S., Singh N., Sun W., Sun X., Ticheli H.J., Waring M.T., Zhu A.L., Alter G., Li J.Z., Lingwood D., Schmidt A.G., Lichterfeld M., Walker B.D., Yu X.G., Padera R.F.Jr., Pillai S.; Massachusetts Consortium on Pathogen Readiness Specimen Working Group. Loss of Bcl-6-expressing T follicular helper cells and germinal centers in COVID-19. Cell, 2020, vol. 183, no. 1, pp. 143–157.e13. doi: 10.1016/j.cell.2020.08.025
- Kang C.K., Han G.C., Kim M., Kim G., Shin H.M., Song K.H., Choe P.G., Park W.B., Kim E.S., Kim H.B., Kim N.J., Kim H.R., Oh M.D. Aberrant hyperactivation of cytotoxic T-cell as a potential determinant of COVID-19 severity. Int. J. Infect. Dis., 2020, vol. 97, pp. 313–321. doi: 10.1016/j.ijid.2020.05.106
- Kempuraj D., Selvakumar G.P., Ahmed M.E., Raikwar S.P., Thangavel R., Khan A., Zaheer S.A., Iyer S.S., Burton C., James D., Zaheer A. COVID-19, mast cells, cytokine storm, psychological stress, and neuroinflammation. Neuroscientist, 2020, vol. 26, no. 5–6, pp. 402–414. doi: 10.1177/1073858420941476
- Kimura H., Francisco D., Conway M., Martinez F.D., Vercelli D., Polverino F., Billheimer D., Kraft M. Type 2 inflammation modulates ACE2 and TMPRSS2 in airway epithelial cells. J. Allergy Clin. Immunol., 2020, vol. 146, no. 1, pp. 80–88.e8. doi: 10.1016/j.jaci.2020.05.004
- Koutsakos M., Lee W.S., Wheatley A.K., Kent S.J., Juno J.A. T follicular helper cells in the humoral immune response to SARS-CoV-2 infection and vaccination. J. Leukoc. Biol., 2022, vol. 111, no. 2, pp. 355–365. doi: 10.1002/JLB.5MR0821-464R
- Kudryavtsev I., Kalinina O., Bezrukikh V., Melnik O., Golovkin A. The significance of phenotyping and quantification of plasma extracellular vesicles levels using high-sensitivity flow cytometry during COVID-19 treatment. Viruses, 2021, vol. 13, no. 5: 767. doi: 10.3390/v13050767
- Kudryavtsev I.V., Arsentieva N.A., Batsunov O.K., Korobova Z.R., Khamitova I.V., Isakov D.V., Kuznetsova R.N., Rubinstein A.A., Stanevich O.V., Lebedeva A.A., Vorobyov E.A., Vorobyova S.V., Kulikov A.N., Sharapova M.A., Pevtcov D.E., Totolian A.A. Alterations in B cell and follicular T-helper cell subsets in patients with acute COVID-19 and COVID-19 convalescents. Curr. Issues Mol. Biol., 2022, vol. 44, no. 1, pp. 194–205. doi: 10.3390/cimb44010014
- Kunal S., Madan M., Tarke C., Gautam D.K., Kinkar J.S., Gupta K., Agarwal R., Mittal S., Sharma S.M. Emerging spectrum of post-COVID-19 syndrome. Postgrad. Med. J., 2021. doi: 10.1136/postgradmedj-2020-139585
- Kuri-Cervantes L., Pampena M.B., Meng W., Rosenfeld A.M., Ittner C.A.G., Weisman A.R., Agyekum R.S., Mathew D., Baxter A.E., Vella L.A., Kuthuru O., Apostolidis S.A., Bershaw L., Dougherty J., Greenplate A.R., Pattekar A., Kim J., Han N., Gouma S., Weirick M.E., Arevalo C.P., Bolton M.J., Goodwin E.C., Anderson E.M., Hensley S.E., Jones T.K., Mangalmurti N.S., Luning Prak E.T., Wherry E.J., Meyer N.J., Betts M.R. Comprehensive mapping of immune perturbations associated with severe COVID-19. Sci. Immunol., 2020, vol. 5, no. 49: eabd7114. doi: 10.1126/sciimmunol.abd7114
- Kvedaraite E., Hertwig L., Sinha I., Ponzetta A., Hed Myrberg I., Lourda M., Dzidic M., Akber M., Klingström J., Folkesson E., Muvva J.R., Chen P., Gredmark-Russ S., Brighenti S., Norrby-Teglund A., Eriksson L.I., Rooyackers O., Aleman S., Strålin K., Ljunggren H.G., Ginhoux F., Björkström N.K., Henter J.I., Svensson M., Karolinska K.I.K. COVID-19 Study Group. Major alterations in the mononuclear phagocyte landscape associated with COVID-19 severity. Proc. Natl. Acad. Sci. USA, 2021, vol. 118, no. 6: e2018587118. doi: 10.1073/pnas.2018587118
- Laing A.G., Lorenc A., Del Molino Del Barrio I., Das A., Fish M., Monin L., Muñoz-Ruiz M., McKenzie D.R., Hayday T.S., Francos-Quijorna I., Kamdar S., Joseph M., Davies D., Davis R., Jennings A., Zlatareva I., Vantourout P., Wu Y., Sofra V., Cano F., Greco M., Theodoridis E., Freedman J.D., Gee S., Chan J.N.E., Ryan S., Bugallo-Blanco E., Peterson P., Kisand K., Haljasmägi L., Chadli L., Moingeon P., Martinez L., Merrick B., Bisnauthsing K., Brooks K., Ibrahim M.A.A., Mason J., Lopez Gomez F., Babalola K., Abdul-Jawad S., Cason J., Mant C., Seow J., Graham C., Doores K.J., Di Rosa F., Edgeworth J., Shankar-Hari M., Hayday A.C. A dynamic COVID-19 immune signature includes associations with poor prognosis. Nat. Med., 2020, vol. 26, no. 10, pp. 1623–1635. doi: 10.1038/s41591-020-1038-6
- Lau D., Lan L.Y., Andrews S.F., Henry C., Rojas K.T., Neu K.E., Huang M., Huang Y., DeKosky B., Palm A.E., Ippolito G.C., Georgiou G., Wilson P.C. Low CD21 expression defines a population of recent germinal center graduates primed for plasma cell differentiation. Sci. Immunol., 2017, vol. 2, no. 7: eaai8153. doi: 10.1126/sciimmunol.aai8153
- Leng Z., Zhu R., Hou W., Feng Y., Yang Y., Han Q., Shan G., Meng F., Du D., Wang S., Fan J., Wang W., Deng L., Shi H., Li H., Hu Z., Zhang F., Gao J., Liu H., Li X., Zhao Y., Yin K., He X., Gao Z., Wang Y., Yang B., Jin R., Stambler I., Lim L.W., Su H., Moskalev A., Cano A., Chakrabarti S., Min K.J., Ellison-Hughes G., Caruso C., Jin K., Zhao R.C. Transplantation of ACE2– mesenchymal stem cells improves the outcome of patients with COVID-19 pneumonia. Aging Dis., 2020, vol. 11, no. 2, pp. 216–228. doi: 10.14336/AD.2020.0228
- Li Q., Ding X., Xia G., Chen H.G., Chen F., Geng Z., Xu L., Lei S., Pan A., Wang L., Wang Z. Eosinopenia and elevated C-reactive protein facilitate triage of COVID-19 patients in fever clinic: a retrospective case-control study. EClinicalMedicine, 2020, vol. 23: 100375. doi: 10.1016/j.eclinm.2020.100375
- Liao M., Liu Y., Yuan J., Wen Y., Xu G., Zhao J., Cheng L., Li J., Wang X., Wang F., Liu L., Amit I., Zhang S., Zhang Z. Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19. Nat. Med., 2020, vol. 26, pp. 842–844. doi: 10.1038/s41591–020-0901-9
- Liu J., Li S., Liu J., Liang B., Wang X., Wang H., Li W., Tong Q., Yi J., Zhao L., Xiong L., Guo C., Tian J., Luo J., Yao J., Pang R., Shen H., Peng C., Liu T., Zhang Q., Wu J., Xu L., Lu S., Wang B., Weng Z., Han C., Zhu H., Zhou R., Zhou H., Chen X., Ye P., Zhu B., Wang L., Zhou W., He S., He Y., Jie S., Wei P., Zhang J., Lu Y., Wang W., Zhang L., Li L., Zhou F., Wang J., Dittmer U., Lu M., Hu Y., Yang D., Zheng X. Longitudinal characteristics of lymphocyte responses and cytokine profiles in the peripheral blood of SARS-CoV-2 infected patients. EBioMedicine, 2020, vol. 55: 102763. doi: 10.1016/j.ebiom.2020.102763
- Malkova A., Kudlay D., Kudryavtsev I., Starshinova A., Yablonskiy P., Shoenfeld Y. Immunogenetic predictors of severe COVID-19. Vaccines (Basel), 2021, vol. 9, no. 3: 211. doi: 10.3390/vaccines9030211
- Malkova A., Kudryavtsev I., Starshinova A., Kudlay D., Zinchenko Y., Glushkova A., Yablonskiy P., Shoenfeld Y. Post COVID-19 syndrome in patients with asymptomatic/mild form. Pathogens, 2021, vol. 10, no. 11: 1408. doi: 10.3390/pathogens10111408
- Mann E.R., Menon M., Knight S.B., Konkel J.E., Jagger C., Shaw T.N., Krishnan S., Rattray M., Ustianowski A., Bakerly N.D., Dark P., Lord G., Simpson A., Felton T., Ho L.P.; NIHR Respiratory TRC, Feldmann M., CIRCO, Grainger J.R., Hussell T. Longitudinal immune profiling reveals key myeloid signatures associated with COVID-19. Sci Immunol., 2020, vol. 5, no. 51: eabd6197. doi: 10.1126/sciimmunol.abd6197
- Martín-Sánchez E., Garcés J.J., Maia C., Inogés S., López-Díaz de Cerio A., Carmona-Torre F., Marin-Oto M., Alegre F., Molano E., Fernandez-Alonso M., Perez C., Botta C., Zabaleta A., Alcaide A.B., Landecho M.F., Rua M., Pérez-Warnisher T., Blanco L., Sarvide S., Vilas-Zornoza A., Alignani D., Moreno C., Pineda I., Sogbe M., Argemi J., Paiva B., Yuste J.R. Immunological biomarkers of fatal COVID-19: a study of 868 patients. Front. Immunol., 2021, vol. 12: 659018. doi: 10.3389/fimmu.2021.659018
- Mathew D., Giles J.R., Baxter A.E., Oldridge D.A., Greenplate A.R., Wu J.E., Alanio C., Kuri-Cervantes L., Pampena M.B., D’Andrea K., Manne S., Chen Z., Huang Y.J., Reilly J.P., Weisman A.R., Ittner C.A.G., Kuthuru O., Dougherty J., Nzingha K., Han N., Kim J., Pattekar A., Goodwin E.C., Anderson E.M., Weirick M.E., Gouma S., Arevalo C.P., Bolton M.J., Chen F., Lacey S.F., Ramage H., Cherry S., Hensley S.E., Apostolidis S.A., Huang A.C., Vella L.A., UPenn COVID Processing Unit, Betts M.R., Meyer N.J., Wherry E.J. Deep immune profiling of COVID-19 patients reveals distinct immunotypes with therapeutic implications. Science, 2020, vol. 369, no. 6508: eabc8511. doi: 10.1126/science.abc8511
- Maucourant C., Filipovic I., Ponzetta A., Aleman S., Cornillet M., Hertwig L., Strunz B., Lentini A., Reinius B., Brownlie D., Cuapio A., Ask E.H., Hull R.M., Haroun-Izquierdo A., Schaffer M., Klingström J., Folkesson E., Buggert M., Sandberg J.K., Eriksson L.I., Rooyackers O., Ljunggren H.G., Malmberg K.J., Michaёlsson J., Marquardt N., Hammer Q., Strålin K., Björkström N.K.; Karolinska COVID-19 Study Group. Natural killer cell immunotypes related to COVID-19 disease severity. Sci. Immunol., 2020, vol. 5, no. 50: eabd6832. doi: 10.1126/sciimmunol.abd6832
- Morita R., Schmitt N., Bentebibel S.E., Ranganathan R., Bourdery L., Zurawski G., Foucat E., Dullaers M., Oh S., Sabzghabaei N., Lavecchio E.M., Punaro M., Pascual V., Banchereau J., Ueno H. Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity, 2011, vol. 34, no. 1, pp. 108–121. doi: 10.1016/j.immuni.2010.12.012
- Motta Junior J.D.S., Miggiolaro A.F.R.D.S., Nagashima S., de Paula C.B.V., Baena C.P., Scharfstein J., de Noronha L. Mast cells in alveolar septa of COVID-19 patients: a pathogenic pathway that may link interstitial edema to immunothrombosis. Front. Immunol., 2020, vol. 11: 574862. doi: 10.3389/fimmu
- Mylvaganam R.J., Bailey J.I., Sznajder J.I., Sala M.A.; Northwestern Comprehensive COVID Center Consortium. Recovering from a pandemic: pulmonary fibrosis after SARS-CoV-2 infection. Eur Respir Rev., 2021, vol. 30, no. 162: 210194. doi: 10.1183/16000617.0194-2021.73
- Nair A.P., Soliman A., Al Masalamani M.A., De Sanctis V., Nashwan A.J., Sasi S., Ali E.A., Hassan O.A., Iqbal F.M., Yassin M.A. Clinical outcome of eosinophilia in patients with COVID-19: a controlled study. Acta Biomed., 2020, vol. 91, no. 4: e2020165. doi: 10.23750/abm.v91i4.10564
- Neidleman J., Luo X., Frouard J., Xie G., Gill G., Stein E.S., McGregor M., Ma T., George A.F., Kosters A., Greene W.C., Vasquez J., Ghosn E., Lee S., Roan N.R. SARS-CoV-2-specific T cells exhibit phenotypic features of helper function, lack of terminal differentiation, and high proliferation potential. Cell Rep. Med., 2020, vol. 1, no. 6: 100081. doi: 10.1016/j.xcrm.2020.100081
- Ni L., Ye F., Cheng M.L., Feng Y., Deng Y.Q., Zhao H., Wei P., Ge J., Gou M., Li X., Sun L., Cao T., Wang P., Zhou C., Zhang R., Liang P., Guo H., Wang X., Qin C.F., Chen F., Dong C. Detection of SARS-CoV-2-specific humoral and cellular immunity in COVID-19 convalescent individuals. Immunity, 2020, vol. 52, no. 6, pp. 971–977.e3. doi: 10.1016/j.immuni.2020.04.023
- Patente T.A., Pinho M.P., Oliveira A.A., Evangelista G.C.M., Bergami-Santos P.C., Barbuto J.A.M. Human dendritic cells: their heterogeneity and clinical application potential in cancer immunotherapy. Front. Immunol., 2019, vol. 9: 3176. doi: 10.3389/fimmu.2018.03176
- Picchianti Diamanti A., Rosado M.M., Nicastri E., Sesti G., Pioli C., Laganà B. Severe acute respiratory syndrome coronavirus-2 infection and autoimmunity 1 year later: the era of vaccines. Front. Immunol., 2021, vol. 12: 708848. doi: 10.3389/fimmu.2021.708848
- Qeadan F., Chehade M., Tingey B., Egbert J., Dellon E.S., Peterson K.A. Patients with eosinophilic gastrointestinal disorders have lower in-hospital mortality rates related to COVID-19. J. Allergy Clin. Immunol Pract., 2021, vol. 9, no. 12, pp. 4473–4476.e4. doi: 10.1016/j.jaip.2021.09.022
- Rodriguez L., Pekkarinen P.T., Lakshmikanth T., Tan Z., Consiglio C.R., Pou C., Chen Y., Mugabo C.H., Nguyen N.A., Nowlan K., Strandin T., Levanov L., Mikes J., Wang J., Kantele A., Hepojoki J., Vapalahti O., Heinonen S., Kekäläinen E., Brodin P. Systems-level immunomonitoring from acute to recovery phase of severe COVID-19. Cell Rep. Med., 2020, vol. 1, no. 5: 100078. doi: 10.1016/j.xcrm.2020.100078
- Rydyznski Moderbacher C., Ramirez S.I., Dan J.M., Grifoni A., Hastie K.M., Weiskopf D., Belanger S., Abbott R.K., Kim C., Choi J., Kato Y., Crotty E.G., Kim C., Rawlings S.A., Mateus J., Tse L.P.V., Frazier A., Baric R., Peters B., Greenbaum J., Ollmann Saphire E., Smith D.M., Sette A., Crotty S. Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell, 2020, vol. 183, no. 4, pp. 996–1012.e19. doi: 10.1016/j.cell.2020.09.038
- Santa Cruz A., Mendes-Frias A., Oliveira A.I., Dias L., Matos A.R., Carvalho A., Capela C., Pedrosa J., Castro A.G., Silvestre R. Interleukin-6 is a biomarker for the development of fatal severe acute respiratory syndrome coronavirus 2 pneumonia. Front. Immunol., 2021, vol. 12: 613422. doi: 10.3389/fimmu.2021.613422
- Sattler A., Angermair S., Stockmann H., Heim K.M., Khadzhynov D., Treskatsch S., Halleck F., Kreis M.E., Kotsch K. SARS-CoV-2-specific T cell responses and correlations with COVID-19 patient predisposition. J. Clin. Invest., 2020, vol. 130, no. 12, pp. 6477–6489. doi: 10.1172/JCI140965
- Schultheiß C., Paschold L., Simnica D., Mohme M., Willscher E., von Wenserski L., Scholz R., Wieters I., Dahlke C., Tolosa E., Sedding D.G., Ciesek S., Addo M., Binder M. Next-generation sequencing of T and B cell receptor repertoires from COVID-19 patients showed signatures associated with severity of disease. Immunity, 2020, vol. 53, no. 2, pp. 442–455.e4. doi: 10.1016/j.immuni.2020.06.024
- Sekine T., Perez-Potti A., Rivera-Ballesteros O., Stralin K., Gorin J.B., Olsson A., Llewellyn-Lacey S., Kamal H., Bogdanovic G., Muschiol S., Wullimann D.J., Kammann T., Emgård J., Parrot T., Folkesson E.; Karolinska COVID-19 Study Group, Rooyackers O., Eriksson L.I., Henter J.I., Sönnerborg A., Allander T., Albert J., Nielsen M., Klingström J., Gredmark-Russ S., Björkström N.K., Sandberg J.K., Price D.A., Ljunggren H.G., Aleman S., Buggert M. Robust T cell immunity in convalescent individuals with asymptomatic or mild COVID-19. Cell, 2020, vol. 183, no. 1, pp. 158–168.e14. doi: 10.1016/j.cell.2020.08.017
- Shibabaw T. Inflammatory cytokine: IL-17A signaling pathway in patients present with COVID-19 and current treatment strategy. J. Inflamm. Res., 2020, vol. 13, pp. 673–680. doi: 10.2147/JIR.S278335
- Silvin A., Chapuis N., Dunsmore G., Goubet A.G., Dubuisson A., Derosa L., Almire C., Hénon C., Kosmider O., Droin N., Rameau P., Catelain C., Alfaro A., Dussiau C., Friedrich C., Sourdeau E., Marin N., Szwebel T.A., Cantin D., Mouthon L., Borderie D., Deloger M., Bredel D., Mouraud S., Drubay D., Andrieu M., Lhonneur A.S., Saada V., Stoclin A., Willekens C., Pommeret F., Griscelli F., Ng L.G., Zhang Z., Bost P., Amit I., Barlesi F., Marabelle A., Pène F., Gachot B., André F., Zitvogel L., Ginhoux F., Fontenay M., Solary E. Elevated calprotectin and abnormal myeloid cell subsets discriminate severe from mild COVID-19. Cell, 2020, vol. 182, no. 6, pp. 1401–1418.e18. doi: 10.1016/j.cell.2020.08.002
- Spoerl S., Kremer A.N., Aigner M., Eisenhauer N., Koch P., Meretuk L., Löffler P., Tenbusch M., Maier C., Überla K., Heinzerling L., Frey B., Lutzny-Geier G., Winkler T.H., Krönke G., Vetter M., Bruns H., Neurath M.F., Mackensen A., Kremer A.E., Völkl S. Upregulation of CCR4 in activated CD8+ T cells indicates enhanced lung homing in patients with severe acute SARS-CoV-2 infection. Eur. J. Immunol., 2021, vol. 51, no. 6, pp. 1436–1448. doi: 10.1002/eji.202049135
- Tan A.T., Linster M., Tan C.W., Le Bert N., Chia W.N., Kunasegaran K., Zhuang Y., Tham C.Y.L., Chia A., Smith G.J.D., Young B., Kalimuddin S., Low J.G.H., Lye D., Wang L.F., Bertoletti A. Early induction of functional SARS-CoV-2-specific T cells associates with rapid viral clearance and mild disease in COVID-19 patients. Cell Rep., 2021, vol. 34, no. 6: 108728. doi: 10.1016/j.celrep.2021.108728
- Tong X., Cheng A., Yuan X., Zhong X., Wang H., Zhou W., Xu X., Li Y. Characteristics of peripheral white blood cells in COVID-19 patients revealed by a retrospective cohort study. BMC Infect. Dis., 2021, vol. 21, no. 1: 1236. doi: 10.1186/s12879-021-06899-7
- Van Eeden C., Khan L., Osman M.S., Cohen Tervaert J.W. Natural killer cell dysfunction and its role in COVID-19. Int. J. Mol. Sci., 2020, vol. 21, no. 17: 6351. doi: 10.3390/ijms21176351
- Varchetta S., Mele D., Oliviero B., Mantovani S., Ludovisi S., Cerino A., Bruno R., Castelli A., Mosconi M., Vecchia M., Roda S., Sachs M., Klersy C., Mondelli M.U. Unique immunological profile in patients with COVID-19. Cell Mol. Immunol., 2020, vol. 18, no. 3, pp. 604–612. doi: 10.1038/s41423-020-00557-9
- Vinuesa C.G., Linterman M.A., Yu D., MacLennan I.C. Follicular helper T cells. Annu Rev. Immunol., 2016, vol. 34, pp. 335–368. doi: 10.1146/annurev-immunol-041015-055605
- Vitte J., Diallo A.B., Boumaza A., Lopez A., Michel M., Allardet-Servent J., Mezouar S., Sereme Y., Busnel J.M., Miloud T., Malergue F., Morange P.E., Halfon P., Olive D., Leone M., Mege J.L. A granulocytic signature identifies COVID-19 and its severity. J. Infect. Dis., 2020, vol. 222, no. 12, pp. 1985–1996. doi: 10.1093/infdis/jiaa591
- Wang F., Nie J., Wang H., Zhao Q., Xiong Y., Deng L., Song S., Ma Z., Mo P., Zhang Y. Characteristics of peripheral lymphocyte subset alteration in COVID-19 pneumonia. J. Infect. Dis., 2020, vol. 221, no. 11, pp. 1762–1769. doi: 10.1093/infdis/jiaa150
- Weiskopf D., Schmitz K.S., Raadsen M.P., Grifoni A., Okba N.M.A., Endeman H., van den Akker J.P.C., Molenkamp R., Koopmans M.P.G., van Gorp E.C.M., Haagmans B.L., de Swart R.L., Sette A., de Vries R.D. Phenotype and kinetics of SARS-CoV-2-specific T cells in COVID-19 patients with acute respiratory distress syndrome. Sci. Immunol., 2020, vol. 5, no. 48: eabd2071. doi: 10.1126/sciimmunol.abd2071
- Wilk A.J., Rustagi A., Zhao N.Q., Roque J., Martínez-Colón G.J., McKechnie J.L., Ivison G.T., Ranganath T., Vergara R., Hollis T., Simpson L.J., Grant P., Subramanian A., Rogers A.J., Blish C.A. A single-cell atlas of the peripheral immune response in patients with severe COVID-19. Nat. Med., 2020, vol. 26, no. 7, pp. 1070–1076. doi: 10.1038/s41591-020-0944-y
- Winheim E., Rinke L., Lutz K., Reischer A., Leutbecher A., Wolfram L., Rausch L., Kranich J., Wratil P.R., Huber J.E., Baumjohann D., Rothenfusser S., Schubert B., Hilgendorff A., Hellmuth J.C., Scherer C., Muenchhoff M., von Bergwelt-Baildon M., Stark K., Straub T., Brocker T., Keppler O.T., Subklewe M., Krug A.B. Impaired function and delayed regeneration of dendritic cells in COVID-19. PLoS Pathog., 2021, vol. 17, no. 10: e1009742. doi: 10.1371/journal.ppat.1009742
- Woodruff M.C., Ramonell R.P., Nguyen D.C., Cashman K.S., Saini A.S., Haddad N.S., Ley A.M., Kyu S., Howell J.C., Ozturk T., Lee S., Suryadevara N., Case J.B., Bugrovsky R., Chen W., Estrada J., Morrison-Porter A., Derrico A., Anam F.A., Sharma M., Wu H.M., Le S.N., Jenks S.A., Tipton C.M., Staitieh B., Daiss J.L., Ghosn E., Diamond M.S., Carnahan R.H., Crowe J.E. Jr., Hu W.T., Lee F.E., Sanz I. Extrafollicular B cell responses correlate with neutralizing antibodies and morbidity in COVID-19. Nat. Immunol., 2020, vol. 21, no. 12, pp. 1506–1516. doi: 10.1038/s41590-020-00814-z
- Xie G., Ding F., Han L., Yin D., Lu H., Zhang M. The role of peripheral blood eosinophil counts in COVID-19 patients. Allergy, 2021, vol. 76, no. 2, pp. 471–482. doi: 10.1111/all.14465
- Yan B., Yang J., Xie Y., Tang X. Relationship between blood eosinophil levels and COVID-19 mortality. World Allergy Organ J., 2021, vol. 14, no. 3: 100521. doi: 10.1016/j.waojou.2021.100521
- Yao C., Bora S.A., Parimon T., Zaman T., Friedman O.A., Palatinus J.A., Surapaneni N.S., Matusov Y.P., Chiang G.C., Kassar A.G., Patel N., Green C.E.R., Aziz A.W., Suri H., Suda J., Lopez A.A., Martins G.A., Stripp B.R., Gharib S.A., Goodridge H.S., Chen P. Cell-type-specific immune dysregulation in severely ill COVID-19 patients. Cell Rep., 2021, vol. 34, no. 13: 108943. doi: 10.1016/j.celrep.2021.108943
- Youdi H., Bing Z., Shan Z., Xiaoqian W., Renxi W. Chemokine-expressing Th1 and treg cells are increased in the lung of patients with COVID-19. SSRN Electronic Journal, 2020. doi: 10.2139/ssrn.3629437
- Zhao Q., Yuan Y., Zhang J., Li J., Li W., Guo K., Wang Y., Chen J., Yan W., Wang B., Jing N., Ma B., Zhang Q. Early predictors of severe COVID-19 among hospitalized patients. J. Clin. Lab. Anal., 2021, pp. e24177. doi: 10.1002/jcla.24177
- Zhao Y., Kilian C., Turner J.E., Bosurgi L., Roedl K., Bartsch P., Gnirck A.C., Cortesi F., Schultheiß C., Hellmig M., Enk L.U.B., Hausmann F., Borchers A., Wong M.N., Paust H.J., Siracusa F., Scheibel N., Herrmann M., Rosati E., Bacher P., Kylies D., Jarczak D., Lütgehetmann M., Pfefferle S., Steurer S., Zur-Wiesch J.S., Puelles V.G., Sperhake J.P., Addo M.M., Lohse A.W., Binder M., Huber S., Huber T.B., Kluge S., Bonn S., Panzer U., Gagliani N., Krebs C.F. Clonal expansion and activation of tissue-resident memory-like Th17 cells expressing GM-CSF in the lungs of severe COVID-19 patients. Sci. Immunol., 2021, vol. 6, no. 56: eabf6692. doi: 10.1126/sciimmunol.abf6692
- Zheng M., Gao Y., Wang G., Song G., Liu S., Sun D., Xu Y., Tian Z. Functional exhaustion of antiviral lymphocytes in COVID-19 patients. Cell Mol. Immunol., 2020, vol. 17, no. 5, pp. 533–535. doi: 10.1038/s41423-020-0402-2
- Zhou R., To K.K., Wong Y.C., Liu L., Zhou B., Li X., Huang H., Mo Y., Luk T.Y., Lau T.T., Yeung P., Chan W.M., Wu A.K., Lung K.C., Tsang O.T., Leung W.S., Hung I.F., Yuen K.Y., Chen Z. Acute SARS-CoV-2 infection impairs dendritic cell and T cell responses. Immunity, 2020, vol. 53, no. 4, pp. 864–877.e5. doi: 10.1016/j.immuni.2020.07.026
- Zhu X., Zhu J. CD4 T helper cell subsets and related human immunological disorders. Int. J. Mol. Sci., 2020, vol. 21, no. 21: 8011. doi: 10.3390/ijms21218011
Supplementary files
