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Article Open Access

Adropin attenuates pancreatitis‑associated lung injury through PPARγ phosphorylation‑related macrophage polarization

  • Authors:
    • Fadian Ding
    • Guozhong Liu
    • Feng Gao
    • Zhou Zheng
    • Yupu Hong
    • Youting Chen
    • Shangeng Weng

  • View Affiliations / Copyright

    Affiliations: Department of Hepatopancreatobiliary Surgery, The First Affiliated Hospital of Fujian Medical University, Fuzhou, Fujian 350004, P.R. China, Department of Pathology, The First Affiliated Hospital of Fujian Medical University, Fuzhou, Fujian 350004, P.R. China, Institute of Abdominal Surgery, The First Affiliated Hospital of Fujian Medical University, Fuzhou, Fujian 350004, P.R. China
    Copyright: © Ding et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 95
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    Published online on: August 28, 2023
       https://doi.org/10.3892/ijmm.2023.5298
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Abstract

Acute pancreatitis (AP)‑associated lung injury (ALI) is a critical complication of AP. Adropin is a regulatory protein of immune metabolism. The present study aimed to explore the immunomodulatory effects of adropin on AP‑ALI. For this purpose, serum samples of patients with AP were collected and the expression levels of serum adropin were detected using ELISA. Animal models of AP and adropin knockout (Adro‑KO) were constructed, and adropin expression in serum and lung tissues was investigated. The levels of fibrosis and apoptosis were evaluated using hematoxylin and eosin staining, Masson's staining and immunohistochemistry of in lung tissue. M1/M2 type macrophages in the lungs were detected using immunofluorescence staining, western blot analysis and reverse transcription‑quantitative PCR. As shown by the results, adropin expression was decreased in AP. In the Adro‑KO + L‑arginine (L‑Arg) group, macrophage infiltration, fibrosis and apoptosis were increased. The expression of peroxisome proliferator‑ activated receptor γ (PPARγ) was downregulated, and the macrophages exhibited a trend towards M1 polarization in the Adro‑KO + L‑Arg group. Adropin exogenous supplement attenuated the levels of fibrosis and apoptosis in the model of AP. Adropin exogenous supplement also increased PPARγ expression by the regulation of the phosphorylation levels, which was associated with M2 macrophage polarization. On the whole, the findings of the present study suggest that adropin promotes the M2 polarization of lung macrophages and reduces the severity of AP‑ALI by regulating the function of PPARγ through the regulation of its phosphorylation level.
View Figures

Figure 1

Adropin expression in AP-associated lung injury. (A) Adropin protein expression in serum in patients with AP. (B) Adropin protein expression in serum in the WT + L-Arg group. (C) Serum amylase level in the WT + L-Arg group. (D) Enho mRNA expression in the lung tissue in the WT + L-Arg group. (E) Adropin protein expression in lung tissue in the WT + L-Arg group determined using immunofluorescence. (F) Hematoxylin and eosin staining of pancreatic tissue in the WT + L-Arg group. (G) The adropin protein expression in lung tissue was measured using western blotting. (H) Quantitative analysis of adropin expression determined using immunofluorescence in panel E. (I) Quantitative analysis of the western blots in panel G. *P<0.05 and **P<0.01. AP, acute pancreatitis; L-Arg, L-arginine; NS, normal saline; Enho, energy homeostasis-associated gene.

Figure 2

Results reveal severe acute pancreatitis-associated lung injury in the Adro-KO + L-Arg group. (A) H&E, Masson's staining and immunohistochemistry of lung tissue in the Adro-KO + L-Arg group. (B) Western blot analysis of lung tissue in the Adro-KO + L-Arg group. (C) TUNEL staining of lung tissue in the Adro-KO + L-Arg group. (D) Quantitative analysis of TUNEL staining shown in panel C (n≥8). (E) Quantitative analysis of Masson's staining shown in panel A (n≥7). (F) Quantitative analysis of immunohistochemistry (TGF-β; n≥3). (G) Quantitative analysis of immunohistochemistry (CD68; n≥5). (H) Quantitative analysis of the western blots (caspase-3; n=9). (I) Quantitative analysis of the western blots (PARP1; n=9). *P<0.05 and ***P<0.001. L-Arg, L-arginine; H&E, hematoxylin and eosin; Adro-KO, adropin knockout; NS, normal saline.

Figure 3

Excessive M1 macrophage polarization is observed in the Adro-KO + L-Arg group. (A) Western blot analysis of lung tissue form the Adro-KO + L-Arg group. (B) Co-expression of CD68 and iNOS in lung tissue in L-Arg group determined using immunofluorescence. (C) Co-expression of CD68 and CD206 of lung tissue in the L-Arg group determined using immunofluorescence. (D) iNOS mRNA level in lung tissue from the Adro-KO + L-Arg group (n≥8). (E) CD68 mRNA level in lung tissue from the Adro-KO + L-Arg group (n≥7). (F) CD163 mRNA level in lung tissue from the Adro-KO + L-Arg group (n≥8). (G) Arg-1 mRNA level in lung tissue from the Adro-KO + L-Arg group (n≥8). (H) Quantitative analysis of immunofluorescence (CD68 + iNOS) staining (n≥5). (I) Quantitative analysis of immunofluorescence (CD68; CD206) staining in macrophages (n≥9). (J) Quantitative analysis of the western blots (PPARγ; n≥6); (K) Quantitative analysis of the western blots (PPARγ Ser273; n≥6). (L) Quantitative analysis of the western blots (PPARγ Ser112; n≥6). *P<0.05. L-Arg, L-arginine; NS, normal saline; Adro-KO, adropin knockout; iNOS, inducible nitric oxide synthase.

Figure 4

Adropin exogenous supplement attenuates severe acute pancreatitis-associated lung injury. (A) Immunohistochemistry of lung tissue from the Adroko + L-Arg + Adro(34−76)group. (B) Western blot analysis of lung tissue from the Adro-KO + L-Arg + Adro(34−76) group. (C) TUNEL staining of lung tissue from the Adro-KO + L-Arg + Adro(34−76) group. (D) Quantitative analysis of immunohistochemistry for MPO (n≥4). (E) Quantitative analysis of immunohistochemistry for CD68 (n≥4). (F) Quantitative analysis of immunohistochemistry for caspase-3 (n≥5). (G) Quantitative analysis of immunohistochemistry for PARP1 (n≥3). (H) Quantitative analysis of the western blots (caspase-3) (n≥5). (I) Quantitative analysis of the western blots (PARP1) (n≥6). (J) Quantitative analysis of TUNEL staining from panel C (n≥5). *P<0.05, **P<0.01 and ***P<0.001. L-Arg, L-arginine; Adro-KO, adropin knockout; NS, normal saline; MPO, myeloperoxidase.

Figure 5

Adropin exogenous supplement induces M2 macrophage polarization. (A) Western blot analysis of lung tissue from the Adro-KO + L-Arg + Adro(34−76) group. (B) Quantitative analysis of the western blots (PPARγ, PPARγ Ser112, PPARγ Ser273) (n≥5). (C) Co-expression of CD68 and iNOS in lung tissue from the Adro-KO + L-Arg+Adro(34−76) group. (D) Co-expression of CD68 and iNOS in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group. (E) Ratio of CD68/DAPI of lung in Adro-KO+ L-Arg+Adro(34−76) group(n≥3); (F) The ratio of iNOS/DAPI in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group (n≥3). (G) Ratio of iNOS/CD68 in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group (n≥3). (H) Ratio of CD68/DAPI in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group (n≥3). (I) Ratio of CD206/DAPI in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group (n≥3). (J) Ratio of CD206/CD68 in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group (n≥3). (K) CD163 mRNA level in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group (n≥6). (L) Arg-1 mRNA level in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group (n≥6). (M) iNOS mRNA level in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group (n≥6). (N) CD86 mRNA level level in lung tissue from the Adro-KO + L-Arg + Adro(34−76) group (n≥6). *P<0.05 and ***P<0.001. L-Arg, L-arginine; Adro-KO, adropin knockout; NS, normal saline; iNOS, inducible nitric oxide synthase; Arg-1, arginase 1.
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Copy and paste a formatted citation
Spandidos Publications style
Ding F, Liu G, Gao F, Zheng Z, Hong Y, Chen Y and Weng S: Adropin attenuates pancreatitis‑associated lung injury through PPARγ phosphorylation‑related macrophage polarization. Int J Mol Med 52: 95, 2023.
APA
Ding, F., Liu, G., Gao, F., Zheng, Z., Hong, Y., Chen, Y., & Weng, S. (2023). Adropin attenuates pancreatitis‑associated lung injury through PPARγ phosphorylation‑related macrophage polarization. International Journal of Molecular Medicine, 52, 95. https://doi.org/10.3892/ijmm.2023.5298
MLA
Ding, F., Liu, G., Gao, F., Zheng, Z., Hong, Y., Chen, Y., Weng, S."Adropin attenuates pancreatitis‑associated lung injury through PPARγ phosphorylation‑related macrophage polarization". International Journal of Molecular Medicine 52.4 (2023): 95.
Chicago
Ding, F., Liu, G., Gao, F., Zheng, Z., Hong, Y., Chen, Y., Weng, S."Adropin attenuates pancreatitis‑associated lung injury through PPARγ phosphorylation‑related macrophage polarization". International Journal of Molecular Medicine 52, no. 4 (2023): 95. https://doi.org/10.3892/ijmm.2023.5298
Copy and paste a formatted citation
x
Spandidos Publications style
Ding F, Liu G, Gao F, Zheng Z, Hong Y, Chen Y and Weng S: Adropin attenuates pancreatitis‑associated lung injury through PPARγ phosphorylation‑related macrophage polarization. Int J Mol Med 52: 95, 2023.
APA
Ding, F., Liu, G., Gao, F., Zheng, Z., Hong, Y., Chen, Y., & Weng, S. (2023). Adropin attenuates pancreatitis‑associated lung injury through PPARγ phosphorylation‑related macrophage polarization. International Journal of Molecular Medicine, 52, 95. https://doi.org/10.3892/ijmm.2023.5298
MLA
Ding, F., Liu, G., Gao, F., Zheng, Z., Hong, Y., Chen, Y., Weng, S."Adropin attenuates pancreatitis‑associated lung injury through PPARγ phosphorylation‑related macrophage polarization". International Journal of Molecular Medicine 52.4 (2023): 95.
Chicago
Ding, F., Liu, G., Gao, F., Zheng, Z., Hong, Y., Chen, Y., Weng, S."Adropin attenuates pancreatitis‑associated lung injury through PPARγ phosphorylation‑related macrophage polarization". International Journal of Molecular Medicine 52, no. 4 (2023): 95. https://doi.org/10.3892/ijmm.2023.5298
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