Effect of tumor-associated neutrophil releasing APRIL on proliferation of pancreatic cancer cells_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LIANG Lizhou ^1,2 , DENG Zhenfeng ^1,2 , JIN Zongrui ² , WU Guolin ² , XU Banghao ² , GUO Ya ² , WANG Jilong ² ,  WEN Zhang ²

1. Guangxi Medical University, Nanning 530021, R. P. China;
2. Department of Hepatobiliary Surgery, the First Affiliated Hospital of Guangxi Medical University, Nanning 530021, R. P. China;

Corresponding?author：

WEN Zhang, Email: wenzgxmu@163.com

Keywords：

pancreatic cancer; tumor associated neutrophil; a proliferation-inducing ligand; tumor proliferation; tumor progression

DOI：

10.7507/1007-9424.201911060

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To study the effect of tumor associated neutrophil (TAN) releasing a proliferation-inducing ligand (APRIL) on the proliferation of pancreatic cancer cells in microenvironment.Methods ① The expressions of APRIL in neutrophils (differentiated by HL-60 cell) and TAN cells were detected by use ELISA. ② The expressions of APRIL receptors B cell maturation antigen (BCMA) and trans-membrane activator and CAML interactor (TACI) in pancreatic cancer cell line PANC-1 were confirmed by use Western blotting. ③ Pancreatic cancer PANC-1 cells were co-cultured with TAN, and divided into a PANC-1 control group (referred to as the control group), a PANC-1+TAN treatment group (referred to as the PANC-1+TAN group), PANC-1+TAN+APRIL antibody treatment group (referred to as PANC-1+TAN+APRIL group), and PANC-1+rtificial recombinant APRIL protein (rAPRIL) treatment group (referred to as PANC-1+rAPRIL group). The CCK8 method was used to determine TAN release of APRIL on PANC-1 effect of cell proliferation activity.Results ① The APRIL content in the culture medium of TAN cell group was higher than that of neutrophil group [(556.20±84.38) pg/mL vs. (377.17±57.07) pg/mL, P=0.038]. ② PANC-1 cells express the receptors BCMA and TACI of APRIL. ③ PANC-1 cell activity of PANC-1+TAN group and PANC-1+rAPRIL group [(126.80±1.42)%, (168.95±12.54)%] were significantly higher than the control group [(100 ± 0.00)%, P<0.05, P<0.001], the activity of PANC-1 cells in the PANC-1+TAN group was significantly higher than that in the PANC-1+TAN+APRIL group [(86.29 ± 12.20)%, P=0.003] and significantly lower than that of PANC-1+rAPRIL group (P=0.002), the activity of PANC-1 cells in PANC-1+rAPRIL group was significantly higher than that in PANC-1+TAN+APRIL antibody group (P<0.001).Conclusion In the microenvironment of pancreatic cancer, the release of APRIL from TAN increases, which promotes the proliferative activity of PANC-1 in pancreatic cancer cells, which provides a new idea for the mechanism research and treatment of pancreatic cancer progression.

Citation： LIANG Lizhou, DENG Zhenfeng, JIN Zongrui, WU Guolin, XU Banghao, GUO Ya, WANG Jilong, WEN Zhang. Effect of tumor-associated neutrophil releasing APRIL on proliferation of pancreatic cancer cells. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(8): 940-944. doi: 10.7507/1007-9424.201911060 Copy

1.	Shojaei F, Singh M, Thompson JD, et al. Role of Bv8 in neutrophil-dependent angiogenesis in a transgenic model of cancer progression. Proc Natl Acad Sci U S A, 2008, 105(7): 2640-2645.
2.	Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
3.	Hidalgo M, Cascinu S, Kleeff J, et al. Addressing the challenges of pancreatic cancer: future directions for improving outcomes. Pancreatology, 2015, 15(1): 8-18.
4.	Wen Z, Liao Q, Zhao J, et al. High expression of interleukin-22 and its receptor predicts poor prognosis in pancreatic ductal adenocarcinoma. Ann Surg Oncol, 2014, 21(1): 125-132.
5.	Oberg HH, Wesch D, Kalyan S, et al. Regulatory interactions between neutrophils, tumor cells and T cells. Front Immunol, 2019, 10: 1690.
6.	Dou H, Yan Z, Zhang M, et al. APRIL promotes non-small cell lung cancer growth and metastasis by targeting ERK1/2 signaling. Oncotarget, 2017, 8(65): 109289-109300.
7.	Zhi X, Tao J, Xiang G, et al. APRIL induces cisplatin resistance in gastric cancer cells via activation of the NF-κB pathway. Cell Physiol Biochem, 2015, 35(2): 571-585.
8.	Bat-Erdene U, Quan E, Chan K, et al. Neutrophil TLR4 and PKR are targets of breast cancer cell glycosaminoglycans and effectors of glycosaminoglycan-induced APRIL secretion. Oncogenesis, 2018, 7(6): 45.
9.	Wen X, Jin T, Xu X. Imaging G protein-coupled receptor-mediated chemotaxis and its signaling events in neutrophil-like HL60 cells. J Vis Exp, 2016, 115: e54511.
10.	Deer EL, González-Hernández J, Coursen JD, et al. Phenotype and genotype of pancreatic cancer cell lines. Pancreas, 2010, 39(4): 425-435.
11.	Hahne M, Kataoka T, Schr?ter M, et al. APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth. J Exp Med, 1998, 188(6): 1185-1190.
12.	He B, Xu W, Santini PA, et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity, 2007, 26(6): 812-826.
13.	Litinskiy MB, Nardelli B, Hilbert DM, et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol, 2002, 3(9): 822-829.
14.	Gross JA, Johnston J, Mudri S, et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature, 2000, 404(6781): 995-999.
15.	Sakurai D, Kanno Y, Hase H, et al. TACI attenuates antibody production costimulated by BAFF-R and CD40. Eur J Immunol, 2007, 37(1): 110-118.
16.	Salazar-Camarena DC, Ortíz-Lazareno P, Marín-Rosales M, et al. BAFF-R and TACI expression on CD3⁺ T cells: Interplay among BAFF, APRIL and T helper cytokines profile in systemic lupus erythematosus. Cytokine, 2019, 114: 115-127.
17.	Takahara M, Nagato T, Nozaki Y, et al. A proliferation-inducing ligand (APRIL) induced hyper-production of IgA from tonsillar mononuclear cells in patients with IgA nephropathy. Cell Immunol, 2019, 341: 103925.
18.	Sun B, Xia Z, Cai F, et al. APRIL is involved in the proliferation and metastasis of acute lymphoblastic leukemia cells. J Pediatr Hematol Oncol, 2018, 40(8): 588-593.
19.	Kubo H, Murakami T, Matsuyama R, et al. Prognostic impact of the neutrophil-to-lymphocyte ratio in borderline resectable pancreatic ductal adenocarcinoma treated with neoadjuvant chemoradiotherapy followed by surgical resection. World J Surg, 2019, 43(12): 3153-3160.
20.	Guo J, Wu M, Guo L, et al. Pretreatment blood neutrophil/lymphocyte ratio is associated with metastasis and predicts survival in patients with pancreatic cancer. Bull Cancer, 2018, 105(2): 146-154.
21.	Sakamoto T, Saito H, Uchinaka EI, et al. The combination of neutrophil-to-lymphocyte ratio and serum carbohydrate antigen 19-9 level as a prognostic indicator in patients with recurrent pancreatic cancer. Anticancer Res, 2018, 38(9): 5497-5503.
22.	Lee BM, Chung SY, Chang JS, et al. The neutrophil-lymphocyte ratio and platelet-lymphocyte ratio are prognostic factors in patients with locally advanced pancreatic cancer treated with chemoradiotherapy. Gut Liver, 2018, 12(3): 342-352.
23.	Athens JW, Haab OP, Raab SO, et al. Leukokinetic studies. IV. The total blood, circulating and marginal granulocyte pools and the granulocyte turnover rate in normal subjects. J Clin Invest, 1961, 40: 989-995.
24.	Zou W, Chu X, Cai C, et al. AKT-mediated regulation of polarization in differentiated human neutrophil-like HL-60 cells. Inflamm Res, 2012, 61(8): 853-862.

1. Shojaei F, Singh M, Thompson JD, et al. Role of Bv8 in neutrophil-dependent angiogenesis in a transgenic model of cancer progression. Proc Natl Acad Sci U S A, 2008, 105(7): 2640-2645.
2. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
3. Hidalgo M, Cascinu S, Kleeff J, et al. Addressing the challenges of pancreatic cancer: future directions for improving outcomes. Pancreatology, 2015, 15(1): 8-18.
4. Wen Z, Liao Q, Zhao J, et al. High expression of interleukin-22 and its receptor predicts poor prognosis in pancreatic ductal adenocarcinoma. Ann Surg Oncol, 2014, 21(1): 125-132.
5. Oberg HH, Wesch D, Kalyan S, et al. Regulatory interactions between neutrophils, tumor cells and T cells. Front Immunol, 2019, 10: 1690.
6. Dou H, Yan Z, Zhang M, et al. APRIL promotes non-small cell lung cancer growth and metastasis by targeting ERK1/2 signaling. Oncotarget, 2017, 8(65): 109289-109300.
7. Zhi X, Tao J, Xiang G, et al. APRIL induces cisplatin resistance in gastric cancer cells via activation of the NF-κB pathway. Cell Physiol Biochem, 2015, 35(2): 571-585.
8. Bat-Erdene U, Quan E, Chan K, et al. Neutrophil TLR4 and PKR are targets of breast cancer cell glycosaminoglycans and effectors of glycosaminoglycan-induced APRIL secretion. Oncogenesis, 2018, 7(6): 45.
9. Wen X, Jin T, Xu X. Imaging G protein-coupled receptor-mediated chemotaxis and its signaling events in neutrophil-like HL60 cells. J Vis Exp, 2016, 115: e54511.
10. Deer EL, González-Hernández J, Coursen JD, et al. Phenotype and genotype of pancreatic cancer cell lines. Pancreas, 2010, 39(4): 425-435.
11. Hahne M, Kataoka T, Schr?ter M, et al. APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth. J Exp Med, 1998, 188(6): 1185-1190.
12. He B, Xu W, Santini PA, et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity, 2007, 26(6): 812-826.
13. Litinskiy MB, Nardelli B, Hilbert DM, et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol, 2002, 3(9): 822-829.
14. Gross JA, Johnston J, Mudri S, et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature, 2000, 404(6781): 995-999.
15. Sakurai D, Kanno Y, Hase H, et al. TACI attenuates antibody production costimulated by BAFF-R and CD40. Eur J Immunol, 2007, 37(1): 110-118.
16. Salazar-Camarena DC, Ortíz-Lazareno P, Marín-Rosales M, et al. BAFF-R and TACI expression on CD3⁺ T cells: Interplay among BAFF, APRIL and T helper cytokines profile in systemic lupus erythematosus. Cytokine, 2019, 114: 115-127.
17. Takahara M, Nagato T, Nozaki Y, et al. A proliferation-inducing ligand (APRIL) induced hyper-production of IgA from tonsillar mononuclear cells in patients with IgA nephropathy. Cell Immunol, 2019, 341: 103925.
18. Sun B, Xia Z, Cai F, et al. APRIL is involved in the proliferation and metastasis of acute lymphoblastic leukemia cells. J Pediatr Hematol Oncol, 2018, 40(8): 588-593.
19. Kubo H, Murakami T, Matsuyama R, et al. Prognostic impact of the neutrophil-to-lymphocyte ratio in borderline resectable pancreatic ductal adenocarcinoma treated with neoadjuvant chemoradiotherapy followed by surgical resection. World J Surg, 2019, 43(12): 3153-3160.
20. Guo J, Wu M, Guo L, et al. Pretreatment blood neutrophil/lymphocyte ratio is associated with metastasis and predicts survival in patients with pancreatic cancer. Bull Cancer, 2018, 105(2): 146-154.
21. Sakamoto T, Saito H, Uchinaka EI, et al. The combination of neutrophil-to-lymphocyte ratio and serum carbohydrate antigen 19-9 level as a prognostic indicator in patients with recurrent pancreatic cancer. Anticancer Res, 2018, 38(9): 5497-5503.
22. Lee BM, Chung SY, Chang JS, et al. The neutrophil-lymphocyte ratio and platelet-lymphocyte ratio are prognostic factors in patients with locally advanced pancreatic cancer treated with chemoradiotherapy. Gut Liver, 2018, 12(3): 342-352.
23. Athens JW, Haab OP, Raab SO, et al. Leukokinetic studies. IV. The total blood, circulating and marginal granulocyte pools and the granulocyte turnover rate in normal subjects. J Clin Invest, 1961, 40: 989-995.
24. Zou W, Chu X, Cai C, et al. AKT-mediated regulation of polarization in differentiated human neutrophil-like HL-60 cells. Inflamm Res, 2012, 61(8): 853-862.

Previous Article
Effect of up-regulation of miRNA-21 in vitro on bone marrow mesenchymal stem cells
Next Article
Effect of up-regulation of miRNA-21 in vitro on bone marrow mesenchymal stem cells

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Effect of tumor-associated neutrophil releasing APRIL on proliferation of pancreatic cancer cells

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content