Durable natural killer cell response after three doses of SARS-CoV-2 inactivated vaccine in HIV-infected individuals.


Journal

Chinese medical journal
ISSN: 2542-5641
Titre abrégé: Chin Med J (Engl)
Pays: China
ID NLM: 7513795

Informations de publication

Date de publication:
28 Nov 2023
Historique:
received: 29 05 2023
medline: 29 11 2023
pubmed: 29 11 2023
entrez: 29 11 2023
Statut: aheadofprint

Résumé

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccine can induce a potent cellular and humoral immune response to protect against SARS-CoV-2 infection. However, it was unknown whether SARS-CoV-2 vaccination can induce effective natural killer (NK) cell response in people living with human immunodeficiency virus (PLWH) and healthy individuals. Forty-seven PLWH and thirty healthy controls (HCs) inoculated with SARS-CoV-2 inactivated vaccine were enrolled from Beijing Youan Hospital in this study. The effect of SARS-CoV-2 vaccine on NK cell frequency, phenotype, and function in PLWH and HCs was evaluated by flow cytometry, and the response of NK cells to SARS-CoV-2 Omicron Spike (SARS-2-OS) protein stimulation was also evaluated. SARS-CoV-2 vaccine inoculation elicited activation and degranulation of NK cells in PLWH, which peaked at 2 weeks and then decreased to a minimum at 12 weeks after the third dose of vaccine. However, in vitro stimulation of the corresponding peripheral blood monocular cells from PLWH with SARS-2-OS protein did not upregulate the expression of the aforementioned markers. Additionally, the frequencies of NK cells expressing the activation markers CD25 and CD69 in PLWH were significantly lower than those in HCs at 0, 4 and 12 weeks, but the percentage of CD16+ NK cells in PLWH was significantly higher than that in HCs at 2, 4 and 12 weeks after the third dose of vaccine. Interestingly, the frequency of CD16+ NK cells was significantly negatively correlated with the proportion of CD107a+ NK cells in PLWH at each time point after the third dose. Similarly, this phenomenon was also observed in HCs at 0, 2, and 4 weeks after the third dose. Finally, regardless of whether NK cells were stimulated with SARS-2-OS or not, we did not observe any differences in the expression of NK cell degranulation markers between PLWH and HCs. SARS-CoV-2 vaccine elicited activation and degranulation of NK cells, indicating that the inoculation of SARS-CoV-2 vaccine enhances NK cell response.

Sections du résumé

BACKGROUND BACKGROUND
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccine can induce a potent cellular and humoral immune response to protect against SARS-CoV-2 infection. However, it was unknown whether SARS-CoV-2 vaccination can induce effective natural killer (NK) cell response in people living with human immunodeficiency virus (PLWH) and healthy individuals.
METHODS METHODS
Forty-seven PLWH and thirty healthy controls (HCs) inoculated with SARS-CoV-2 inactivated vaccine were enrolled from Beijing Youan Hospital in this study. The effect of SARS-CoV-2 vaccine on NK cell frequency, phenotype, and function in PLWH and HCs was evaluated by flow cytometry, and the response of NK cells to SARS-CoV-2 Omicron Spike (SARS-2-OS) protein stimulation was also evaluated.
RESULTS RESULTS
SARS-CoV-2 vaccine inoculation elicited activation and degranulation of NK cells in PLWH, which peaked at 2 weeks and then decreased to a minimum at 12 weeks after the third dose of vaccine. However, in vitro stimulation of the corresponding peripheral blood monocular cells from PLWH with SARS-2-OS protein did not upregulate the expression of the aforementioned markers. Additionally, the frequencies of NK cells expressing the activation markers CD25 and CD69 in PLWH were significantly lower than those in HCs at 0, 4 and 12 weeks, but the percentage of CD16+ NK cells in PLWH was significantly higher than that in HCs at 2, 4 and 12 weeks after the third dose of vaccine. Interestingly, the frequency of CD16+ NK cells was significantly negatively correlated with the proportion of CD107a+ NK cells in PLWH at each time point after the third dose. Similarly, this phenomenon was also observed in HCs at 0, 2, and 4 weeks after the third dose. Finally, regardless of whether NK cells were stimulated with SARS-2-OS or not, we did not observe any differences in the expression of NK cell degranulation markers between PLWH and HCs.
CONCLUSIONS CONCLUSIONS
SARS-CoV-2 vaccine elicited activation and degranulation of NK cells, indicating that the inoculation of SARS-CoV-2 vaccine enhances NK cell response.

Identifiants

pubmed: 38018259
doi: 10.1097/CM9.0000000000002947
pii: 00029330-990000000-00865
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2023 The Chinese Medical Association, produced by Wolters Kluwer, Inc. under the CC-BY-NC-ND license.

Références

Björkström NK, Strunz B, Ljunggren HG. Natural killer cells in antiviral immunity. Nat Rev Immunol 2022;22:112–123. doi: 10.1038/s41577-021-00558-3.
doi: 10.1038/s41577-021-00558-3
COVID-19 weekly epidemiological update. World Health Organization 2023. Available from: https://covid19.who.int/. [Last Accessed on 2023 April 20]
Neely HR, Mazo IB, Gerlach C, von Andrian UH. Is there natural killer cell memory and can it be harnessed by vaccination? Natural killer cells in vaccination. Cold Spring Harb Perspect Biol 2018;10:a029488. doi: 10.1101/cshperspect.a029488.
doi: 10.1101/cshperspect.a029488
Wagstaffe HR, Mooney JP, Riley EM, Goodier MR. Vaccinating for natural killer cell effector functions. Clin Transl Immunology 2018;7:e1010. doi: 10.1002/cti2.1010.
doi: 10.1002/cti2.1010
Rydyznski CE, Waggoner SN. Boosting vaccine efficacy the natural (killer) way. Trends Immunol 2015;36:536–546. doi: 10.1016/j.it.2015.07.004.
doi: 10.1016/j.it.2015.07.004
Cox A, Cevik H, Feldman HA, Canaday LM, Lakes N, Waggoner SN. Targeting natural killer cells to enhance vaccine responses. Trends Pharmacol Sci 2021;42:789–801. doi: 10.1016/j.tips.2021.06.004.
doi: 10.1016/j.tips.2021.06.004
Wagstaffe HR, Clutterbuck EA, Bockstal V, Stoop JN, Luhn K, Douoguih M, et al. Ebola virus glycoprotein stimulates IL-18-dependent natural killer cell responses. J Clin Invest 2020;130:3936–3946. doi: 10.1172/JCI132438.
doi: 10.1172/JCI132438
Tarazona R, Casado JG, Delarosa O, Torre-Cisneros J, Villanueva JL, Sanchez B, et al. Selective depletion of CD56 (dim) NK cell subsets and maintenance of CD56 (bright) NK cells in treatment-naive HIV-1-seropositive individuals. J Clin Immunol 2002;22:176–183. doi: 10.1023/a:1015476114409.
doi: 10.1023/a:1015476114409
Frias M, Rivero-Juarez A, Gordon A, Camacho A, Cantisan S, Cuenca-Lopez F, et al. Persistence of pathological distribution of NK cells in HIV-infected patients with prolonged use of HAART and a sustained immune response. PLoS One 2015;10:e0121019. doi: 10.1371/journal.pone.0121019.
doi: 10.1371/journal.pone.0121019
Hong HS, Eberhard JM, Keudel P, Bollmann BA, Ballmaier M, Bhatnagar N, et al. HIV infection is associated with a preferential decline in less-differentiated CD56dim CD16+ NK cells. J Virol 2010;84:1183–1188. doi: 10.1128/JVI.01675-09.
doi: 10.1128/JVI.01675-09
Brunetta E, Fogli M, Varchetta S, Bozzo L, Hudspeth KL, Marcenaro E, et al. Chronic HIV-1 viremia reverses NKG2A/NKG2C ratio on natural killer cells in patients with human cytomegalovirus co-infection. AIDS 2010;24:27–34. doi: 10.1097/QAD.0b013e3283328d1f.
doi: 10.1097/QAD.0b013e3283328d1f
Ariyanto IA, Estiasari R, Edwar L, Makwana N, Lee S, Price P. Characterization of natural killer cells in HIV patients beginning therapy with a high burden of cytomegalovirus. Immunol Invest 2019;48:345–354. doi: 10.1080/08820139.2018.1538236.
doi: 10.1080/08820139.2018.1538236
Jost S, Quillay H, Reardon J, Peterson E, Simmons RP, Parry BA, et al. Changes in cytokine levels and NK cell activation associated with influenza. PLoS One 2011;6:e25060. doi: 10.1371/journal.pone.0025060.
doi: 10.1371/journal.pone.0025060
Marquardt N, Ivarsson MA, Blom K, Gonzalez VD, Braun M, Falconer K, et al. The human NK cell response to yellow fever virus 17D is primarily governed by NK cell differentiation independently of NK cell education. J Immunol 2015;195:3262–3272. doi: 10.4049/jimmunol.1401811.
doi: 10.4049/jimmunol.1401811
Goodier MR, Rodriguez-Galan A, Lusa C, Nielsen CM, Darboe A, Moldoveanu AL, et al. Influenza vaccination generates cytokine-induced memory-like NK cells: Impact of human cytomegalovirus infection. J Immunol 2016;197:313–325. doi: 10.4049/jimmunol.1502049.
doi: 10.4049/jimmunol.1502049
Albarran B, Goncalves L, Salmen S, Borges L, Fields H, Soyano A, et al. Profiles of NK, NKT cell activation and cytokine production following vaccination against hepatitis B. APMIS 2005;113:526–535. doi: 10.1111/j.1600-0463.2005.apm_191.x.
doi: 10.1111/j.1600-0463.2005.apm_191.x
Horowitz A, Behrens RH, Okell L, Fooks AR, Riley EM. NK cells as effectors of acquired immune responses: Effector CD4+ T cell-dependent activation of NK cells following vaccination. J Immunol 2010;185:2808–2818. doi: 10.4049/jimmunol.1000844.
doi: 10.4049/jimmunol.1000844
Myers JA, Miller JS. Exploring the NK cell platform for cancer immunotherapy. Nat Rev Clin Oncol 2021;18:85–100. doi: 10.1038/s41571-020-0426-7.
doi: 10.1038/s41571-020-0426-7
Goodier MR, Lusa C, Sherratt S, Rodriguez-Galan A, Behrens R, Riley EM. Sustained immune complex-mediated reduction in CD16 expression after vaccination regulates NK cell function. Front Immunol 2016;7:384. doi: 10.3389/fimmu.2016.00384.
doi: 10.3389/fimmu.2016.00384
Peruzzi G, Femnou L, Gil-Krzewska A, Borrego F, Weck J, Krzewski K, et al. Membrane-type 6 matrix metalloproteinase regulates the activation-induced downmodulation of CD16 in human primary NK cells. J Immunol 2013;191:1883–1894. doi: 10.4049/jimmunol.1300313.
doi: 10.4049/jimmunol.1300313
Romee R, Foley B, Lenvik T, Wang Y, Zhang B, Ankarlo D, et al. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood 2013;121:3599–3608. doi: 10.1182/blood-2012-04-425397.
doi: 10.1182/blood-2012-04-425397
Zhou Q, Gil-Krzewska A, Peruzzi G, Borrego F. Matrix metalloproteinases inhibition promotes the polyfunctionality of human natural killer cells in therapeutic antibody-based anti-tumour immunotherapy. Clin Exp Immunol 2013;173:131–139. doi: 10.1111/cei.12095.
doi: 10.1111/cei.12095
Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 2004;294:15–22. doi: 10.1016/j.jim.2004.08.008.
doi: 10.1016/j.jim.2004.08.008
Krzewski K, Gil-Krzewska A, Nguyen V, Peruzzi G, Coligan JE. LAMP1/CD107a is required for efficient perforin delivery to lytic granules and NK-cell cytotoxicity. Blood 2013;121:4672–4683. doi: 10.1182/blood-2012-08-453738.
doi: 10.1182/blood-2012-08-453738
Cuapio A, Boulouis C, Filipovic I, Wullimann D, Kammann T, Parrot T, et al. NK cell frequencies, function and correlates to vaccine outcome in BNT162b2 mRNA anti-SARS-CoV-2 vaccinated healthy and immunocompromised individuals. Mol Med 2022;28:20. doi: 10.1186/s10020-022-00443-2.
doi: 10.1186/s10020-022-00443-2

Auteurs

Xiaodong Yang (X)

Beijing Key Laboratory for HIV/AIDS Research, Sino-French Joint Laboratory for Research on Humoral Immune Response to HIV Infection, Clinical and Research Center for Infectious Diseases, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Xiuwen Wang (X)

Beijing Key Laboratory for HIV/AIDS Research, Sino-French Joint Laboratory for Research on Humoral Immune Response to HIV Infection, Clinical and Research Center for Infectious Diseases, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Xin Zhang (X)

Beijing Key Laboratory for HIV/AIDS Research, Sino-French Joint Laboratory for Research on Humoral Immune Response to HIV Infection, Clinical and Research Center for Infectious Diseases, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Haifeng Ding (H)

National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China.

Hu Wang (H)

Beijing Key Laboratory for HIV/AIDS Research, Sino-French Joint Laboratory for Research on Humoral Immune Response to HIV Infection, Clinical and Research Center for Infectious Diseases, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Tao Huang (T)

Tian Yuan Studio, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Guanghui Zhang (G)

Tian Yuan Studio, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Junyi Duan (J)

Tian Yuan Studio, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Wei Xia (W)

Beijing Key Laboratory for HIV/AIDS Research, Sino-French Joint Laboratory for Research on Humoral Immune Response to HIV Infection, Clinical and Research Center for Infectious Diseases, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Bin Su (B)

Beijing Key Laboratory for HIV/AIDS Research, Sino-French Joint Laboratory for Research on Humoral Immune Response to HIV Infection, Clinical and Research Center for Infectious Diseases, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Cong Jin (C)

National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China.

Hao Wu (H)

Beijing Key Laboratory for HIV/AIDS Research, Sino-French Joint Laboratory for Research on Humoral Immune Response to HIV Infection, Clinical and Research Center for Infectious Diseases, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Tong Zhang (T)

Beijing Key Laboratory for HIV/AIDS Research, Sino-French Joint Laboratory for Research on Humoral Immune Response to HIV Infection, Clinical and Research Center for Infectious Diseases, Beijing Youan Hospital, Capital Medical University, Beijing 100069, China.

Classifications MeSH