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1 Department of Oncology Rehabilitation, Shenzhen Luohu People's Hospital, the 3rd Affiliated Hospital of Shenzhen University, Shenzhen, China.

2 Medical Laboratory of Shenzhen LuoHu People's Hospital, Shenzhen, China.

3 Department of Hepatobiliary & Pancreatic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital & Shenzhen Hospital, China.

4 Department of Pancreatic and Gastric Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China.

Weiran Li et al.

Bioengineered .

2021 Dec .

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1 Department of Oncology Rehabilitation, Shenzhen Luohu People's Hospital, the 3rd Affiliated Hospital of Shenzhen University, Shenzhen, China.

2 Medical Laboratory of Shenzhen LuoHu People's Hospital, Shenzhen, China.

3 Department of Hepatobiliary & Pancreatic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital & Shenzhen Hospital, China.

4 Department of Pancreatic and Gastric Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China.

Aging-related phenotype, cell expansion, and cell cycle analysis of NK cells. (a-e) The human NK cells treated with calcitriol or rapamycin for 72 h showed the following cell biomarkers: natural killer group 2 member A (NKG2A), cluster of differentiation 16 (CD16), T cell immunoglobulin and mucin domain-containing protein 3 (TIM3) programmed cell death-1 (PD-1), and killer immunoglobulin-like receptor (KIR), which were related to aging. 50 nM rapamycin (RAPA) was used as the positive control. n = 3 for each group. *P < 0.05 and **P < 0.01 were compared with the negative control (NC) group. (f) NK cells (right) isolated from human peripheral blood mononuclear cells (PBMCs, left) by Magnetic bead sorting. (g) Cell proliferation analysis measured by cell counting kit 8 (CCK8). (h) Effect of calcitriol or rapamycin on the cell cycle in sorted NK cells after treatment for 72 h. *P < 0.05, ●P < 0.05, and #P < 0.05 indicated the significant differences in the G1, S, and G2 phases, respectively. All the groups were compared with NC, respectively. n = 3. (i) The percentage of T cell immunoglobulin and immunoreceptor tyrosine-based inhibitory motif (ITIM) domain (TIGIT)-positive NK cells after treatment with calcitriol or rapamycin for 72 h. *P < 0.05 and **P < 0.01 were compared with NC. n = 3
Effects of calcitriol on the functions of NK cells. (a) Analysis of the cytokine released by the calcitriol-treated NK cells in 48 h. (b) Fluorescence-activated cell sorting (FACS) results showed dead K562 cells labeled by 3,3′-dioctadecyl-oxacarbocyanine (DIO) and propidium iodide (PI). K562 cells were co-cultured with different ratios of calcitriol-treated NK cells for 4 h. (c) FACS analysis of dead K562 cells in NK-killing assays. (d) The degranulation effects of treated NK cells in killing assays. n = 3 for each group. *P < 0.05 and **P < 0.01 were compared with NC
The anti-aging effects of calcitriol on NK cells. (a) The expression of the vitamin D receptor (VDR), sirtuin 1 (SIRT1), SIRT1-∆Exon8, and protein kinase R-like endoplasmic reticulum kinase (pERK) in NK cells was detected by western blotting analysis after treatment with calcitriol for 48 h. Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) was used as the loading control. Bar diagram illustrating the western blotting results (n = 3). *P < 0.05 and **P < 0.01 were compared with NC (n = 3). (b) Dosage mortality curve of NK cells after treatment with hydrogen peroxide (H 2 O 2 ) for 24 h. (c) Percentage of TIM3 cells exhibiting high expression after treatment with 100 μM H 2 O 2 for 24 h. (d) The senescence-associated β-galactosidase staining and analysis results. The senescent cells were stained in blue and indicated by red arrows. Scale bar, 50 μm. (e) NK cells were stained with Hoechst and Chloromethyl-X-Rosamine (CMXRos) to determine the cell location and mitochondrial membrane potential. The aging and apoptotic cells were Hoechst + CMXRos − and indicated by white arrows. Scale bar, 50 μm. Statistical analysis showed relative fluorescence intensity. *P < 0.05 and **P < 0.01 were compared with H 2 O 2 group in figures C, D, and E (n = 3)
The anti-apoptotic effects of calcitriol on NK cells. (a) Anti-apoptotic effects of calcitriol in H 2 O 2 -induced injury. FACS analysis showed the percentage of apoptotic NK cells after treatment with 100 μM H 2 O 2 for 24 h. (b) The expression levels of caspase-3 p20 and caspase-3 p17 in NK cells were detected by western blotting analysis after treatment with 100 μM H 2 O 2 for 24 h. GAPDH was used as the loading control. Bar diagram illustrating the western blotting results (n = 3). *P < 0.05 was compared with the H 2 O 2 group

Olson KC, Kulling Larkin PM, Signorelli R, Hamele CE, Olson TL, Conaway MR, Feith DJ, Loughran TP Jr.
Olson KC, et al.
Cytokine. 2018 Nov;111:551-562. doi: 10.1016/j.cyto.2018.09.016. Epub 2018 Nov 17.
Cytokine. 2018.

PMID: 30455079
Free PMC article.

Marampon F, Gravina GL, Festuccia C, Popov VM, Colapietro A, Sanità P, Musio D, De Felice F, Lenzi A, Jannini EA, Di Cesare E, Tombolini V.
Marampon F, et al.
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Bold A, et al.
Immunobiology. 2022 Nov;227(6):152286. doi: 10.1016/j.imbio.2022.152286. Epub 2022 Sep 29.
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Hazeldine J, Lord JM.
Hazeldine J, et al.
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Hodge G, Hodge S, Liu H, Nguyen P, Holmes-Liew CL, Holmes M.
Hodge G, et al.
Transplantation. 2019 Nov;103(11):2255-2263. doi: 10.1097/TP.0000000000002817.
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Li Y, Zhao L, Qi W.
Li Y, et al.
Bioengineered. 2022 Feb;13(2):3877-3895. doi: 10.1080/21655979.2022.2027172.
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Zhang X, Zhang H, Gong J, Yu H, Wu D, Hou J, Li M, Sun X.
Zhang X, et al.
Bioengineered. 2022 Feb;13(2):3724-3738. doi: 10.1080/21655979.2022.2029066.
Bioengineered. 2022.

PMID: 35105283
Free PMC article.

This work was financially supported by the Shenzhen Science and Technology Innovation Committee (JCYJ20170412155231633), Shenzhen Key Medical Discipline Construction Fund (No. SZXK062), and the Sanming Project of Medicine in Shenzhen (No. SZSM202011010);Shenzhen Science and Technology Innovation Committee [JCYJ20170412155231633];Shenzhen Key Medical Discipline Construction Fund [No. SZXK062];Sanming Project of Medicine in Shenzhen [No. SZSM202011010].

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Vitamin D is widely considered to have a regulatory effect on the immune system. Some clinical investigations have shown that the demand for vitamin D increases with age. Calcitriol is the biologically active form of vitamin D. However, its effect on human natural killer (NK) cells remains unclear. Therefore, in this study, we investigated the anti-aging and immunomodulatory effects of calcitriol on NK cells using a series of immunological methods to explore its important role in innate immunity. We found that calcitriol reversed the expression of aging-related biomarkers in NK cells and inhibited their expansion by maintaining these cells in the G1 phase, without any apoptosis and exhaustion. Calcitriol repressed the release of inflammation-related cytokines, such as interleukin-5 (IL-5), interleukin-13 (IL-13), interferon-gamma (IFN-γ), and tumor necrosis factor-alpha (TNF-α). The degranulation of NK cells was downregulated by calcitriol when these cells were co-cultured with K562 tumor cells. We also found that calcitriol upregulated the aging-related sirtuin 1- protein/kinase R-like endoplasmic reticulum kinase (SIRT1/pERK) pathway and SIRT1-deltaExon8 (SIRT1-∆Exon8) expression by activating the vitamin D receptor (VDR). Moreover, calcitriol could be a potential negative regulator of NK cell apoptosis and mitochondrial inactivation which caused by oxidative stress. Thus, calcitriol exhibits anti-aging effects on human NK cells in vitro by activating the SIRT1-PERK axis and resisting oxidative senescence.

Keywords:

Calcitriol; SIRT1-∆Exon8; anti-aging; nk cells; oxidative senescence.

All authors approved the submission of this manuscript. The authors declare that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.
Aging-related phenotype, cell expansion, and…
Aging-related phenotype, cell expansion, and cell cycle analysis of NK cells. (a-e) The…
Effects of calcitriol on the functions of NK cells. (a) Analysis of the…
The anti-aging effects of calcitriol…
The anti-aging effects of calcitriol on NK cells. (a) The expression of the…
The anti-apoptotic effects of calcitriol…
The anti-apoptotic effects of calcitriol on NK cells. (a) Anti-apoptotic effects of calcitriol…

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