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Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Research

B7-H3 participates in human salivary gland epithelial cells apoptosis through NF-κB pathway in primary Sjögren’s syndrome

Authors: Ping Li, Ying Yang, Yi Jin, Rui Zhao, Chen Dong, Wenjie Zheng, Tianyi Zhang, Jing Li, Zhifeng Gu

Published in: Journal of Translational Medicine | Issue 1/2019

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Abstract

Background

Primary Sjögren’s syndrome (pSS) is an autoimmune disorder mainly characterized by exocrine gland injury. Costimulatory molecules play an important role in immune-regulatory networks. Although B7 family costimulatory molecules were previously discovered in human salivary gland epithelial (HSGE) cells in pSS, the effects of the B7 family member B7-H3 (CD276) have not been well elucidated. Thus, this study aimed to investigate the role and mechanism of B7-H3 in HSGE cells in pSS.

Methods

The expression of B7-H3, B7-H1, PD-1 in serum, saliva and salivary gland were examined by immunohistochemistry (IHC) and enzyme-linked immunosorbent assay (ELISA). Immunofluorescence was used to test the expression and distribution of B7-H3, AQP5 and CK-8 in salivary gland tissues. Flow cytometry, Cell Counting Kit 8 (CCK-8) and western blot (WB) were performed to research the apoptotic, proliferative and inflammatory effects of B7-H3 in primary HSGE cells and HSGE cell lines.

Results

Our results showed that the expression of PD-1, B7-H1 and B7-H3 in peripheral blood, and salivary glands in pSS patients was higher than that in healthy controls, which was positive correlation with the grade of the salivary glands. The expression of B7-H3 in saliva was higher in pSS patients than that in healthy controls, which was detected with the most significant difference of them. The expression of B7-H3 in primary HSGE cells of pSS patients was significantly higher than healthy controls. B7-H3 increased activity of NF-κB pathway and promoted inflammation of HSGE cells, decreasing the expression of AQP5. Furthermore, B7-H3 overexpression inhibited proliferation and induced apoptosis in HSGE cell lines.

Conclusion

B7-H3 could promote inflammation and induce apoptosis of HSGE cells by activating NF-κB pathway, which might be a promising therapeutic target for pSS.
Literature
1.
go back to reference Manoussakis MN, Moutsopoulos HM. Sjogren’s syndrome: autoimmune epithelitis. Baillieres Best Pract Res Clin Rheumatol. 2000;14(1):73–95.CrossRef Manoussakis MN, Moutsopoulos HM. Sjogren’s syndrome: autoimmune epithelitis. Baillieres Best Pract Res Clin Rheumatol. 2000;14(1):73–95.CrossRef
2.
go back to reference Cui Y, Xia L, Li L, Zhao Q, Chen S, Gu Z. Anxiety and depression in primary Sjogren’s syndrome: a cross-sectional study. BMC psychiatry. 2018;18(1):131.CrossRef Cui Y, Xia L, Li L, Zhao Q, Chen S, Gu Z. Anxiety and depression in primary Sjogren’s syndrome: a cross-sectional study. BMC psychiatry. 2018;18(1):131.CrossRef
3.
go back to reference Cui Y, Li L, Xia L, Zhao Q, Chen S, Fu T, et al. The impact of disease activity and psychological status on quality of life for Chinese patients with primary Sjogren’s syndrome. Patient Prefer Adherence. 2018;12:1513–9.CrossRef Cui Y, Li L, Xia L, Zhao Q, Chen S, Fu T, et al. The impact of disease activity and psychological status on quality of life for Chinese patients with primary Sjogren’s syndrome. Patient Prefer Adherence. 2018;12:1513–9.CrossRef
4.
go back to reference Ramos-Casals M, Tzioufas AG, Font J. Primary Sjogren’s syndrome: new clinical and therapeutic concepts. Ann Rheum Dis. 2005;64(3):347–54.CrossRef Ramos-Casals M, Tzioufas AG, Font J. Primary Sjogren’s syndrome: new clinical and therapeutic concepts. Ann Rheum Dis. 2005;64(3):347–54.CrossRef
5.
go back to reference Tzioufas AG, Voulgarelis M. Update on Sjogren’s syndrome autoimmune epithelitis: from classification to increased neoplasias. Best Pract Res Clin Rheumatol. 2007;21(6):989–1010.CrossRef Tzioufas AG, Voulgarelis M. Update on Sjogren’s syndrome autoimmune epithelitis: from classification to increased neoplasias. Best Pract Res Clin Rheumatol. 2007;21(6):989–1010.CrossRef
6.
go back to reference Ohlsson M, Szodoray P, Loro LL, Johannessen AC, Jonsson R. CD40, CD154, Bax and Bcl-2 expression in Sjogren’s syndrome salivary glands: a putative anti-apoptotic role during its effector phases. Scand J Immunol. 2002;56(6):561–71.CrossRef Ohlsson M, Szodoray P, Loro LL, Johannessen AC, Jonsson R. CD40, CD154, Bax and Bcl-2 expression in Sjogren’s syndrome salivary glands: a putative anti-apoptotic role during its effector phases. Scand J Immunol. 2002;56(6):561–71.CrossRef
7.
go back to reference Sun D, Emmert-Buck MR, Fox PC. Differential cytokine mRNA expression in human labial minor salivary glands in primary Sjogren’s syndrome. Autoimmunity. 1998;28(3):125–37.CrossRef Sun D, Emmert-Buck MR, Fox PC. Differential cytokine mRNA expression in human labial minor salivary glands in primary Sjogren’s syndrome. Autoimmunity. 1998;28(3):125–37.CrossRef
8.
go back to reference Kawanami T, Sawaki T, Sakai T, Miki M, Iwao H, Nakajima A, et al. Skewed production of IL-6 and TGFbeta by cultured salivary gland epithelial cells from patients with Sjogren’s syndrome. PLoS ONE. 2012;7(10):e45689.CrossRef Kawanami T, Sawaki T, Sakai T, Miki M, Iwao H, Nakajima A, et al. Skewed production of IL-6 and TGFbeta by cultured salivary gland epithelial cells from patients with Sjogren’s syndrome. PLoS ONE. 2012;7(10):e45689.CrossRef
9.
go back to reference Chinai JM, Janakiram M, Chen F, Chen W, Kaplan M, Zang X. New immunotherapies targeting the PD-1 pathway. Trends Pharmacol Sci. 2015;36(9):587–95.CrossRef Chinai JM, Janakiram M, Chen F, Chen W, Kaplan M, Zang X. New immunotherapies targeting the PD-1 pathway. Trends Pharmacol Sci. 2015;36(9):587–95.CrossRef
10.
go back to reference de Paoli FV, Nielsen BD, Rasmussen F, Deleuran B, Sondergaard K. Abatacept induces clinical improvement in patients with severe systemic sclerosis. Scand J Rheumatol. 2014;43(4):342–5.CrossRef de Paoli FV, Nielsen BD, Rasmussen F, Deleuran B, Sondergaard K. Abatacept induces clinical improvement in patients with severe systemic sclerosis. Scand J Rheumatol. 2014;43(4):342–5.CrossRef
11.
go back to reference Meiners PM, Vissink A, Kroese FG, Spijkervet FK, Smitt-Kamminga NS, Abdulahad WH, et al. Abatacept treatment reduces disease activity in early primary Sjogren’s syndrome (open-label proof of concept ASAP study). Ann Rheum Dis. 2014;73(7):1393–6.CrossRef Meiners PM, Vissink A, Kroese FG, Spijkervet FK, Smitt-Kamminga NS, Abdulahad WH, et al. Abatacept treatment reduces disease activity in early primary Sjogren’s syndrome (open-label proof of concept ASAP study). Ann Rheum Dis. 2014;73(7):1393–6.CrossRef
12.
go back to reference Li J, Lee Y, Li Y, Jiang Y, Lu H, Zang W, et al. Co-inhibitory molecule B7 superfamily member 1 expressed by tumor-infiltrating myeloid cells induces dysfunction of anti-tumor CD8(+) T cells. Immunity. 2018;48(4):773–86.e5.CrossRef Li J, Lee Y, Li Y, Jiang Y, Lu H, Zang W, et al. Co-inhibitory molecule B7 superfamily member 1 expressed by tumor-infiltrating myeloid cells induces dysfunction of anti-tumor CD8(+) T cells. Immunity. 2018;48(4):773–86.e5.CrossRef
13.
go back to reference Nagamatsu T, Barrier BF, Schust DJ. The regulation of T-cell cytokine production by ICOS-B7H2 interactions at the human fetomaternal interface. Immunol Cell Biol. 2011;89(3):417–25.CrossRef Nagamatsu T, Barrier BF, Schust DJ. The regulation of T-cell cytokine production by ICOS-B7H2 interactions at the human fetomaternal interface. Immunol Cell Biol. 2011;89(3):417–25.CrossRef
14.
go back to reference Singh AK, Stock P, Akbari O. Role of PD-L1 and PD-L2 in allergic diseases and asthma. Allergy. 2011;66(2):155–62.CrossRef Singh AK, Stock P, Akbari O. Role of PD-L1 and PD-L2 in allergic diseases and asthma. Allergy. 2011;66(2):155–62.CrossRef
15.
go back to reference Chen L. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol. 2004;4(5):336–47.CrossRef Chen L. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol. 2004;4(5):336–47.CrossRef
16.
go back to reference Zamani MR, Aslani S, Salmaninejad A, Javan MR, Rezaei N. PD-1/PD-L and autoimmunity: a growing relationship. Cell Immunol. 2016;310:27–41.CrossRef Zamani MR, Aslani S, Salmaninejad A, Javan MR, Rezaei N. PD-1/PD-L and autoimmunity: a growing relationship. Cell Immunol. 2016;310:27–41.CrossRef
17.
go back to reference Kobayashi M, Kawano S, Hatachi S, Kurimoto C, Okazaki T, Iwai Y, et al. Enhanced expression of programmed death-1 (PD-1)/PD-L1 in salivary glands of patients with Sjogren’s syndrome. J Rheumatol. 2005;32(11):2156–63.PubMed Kobayashi M, Kawano S, Hatachi S, Kurimoto C, Okazaki T, Iwai Y, et al. Enhanced expression of programmed death-1 (PD-1)/PD-L1 in salivary glands of patients with Sjogren’s syndrome. J Rheumatol. 2005;32(11):2156–63.PubMed
18.
go back to reference Jiang J, Jiang J, Liu C, Zhang G, Gao L, Chen Y, et al. Enhancement of membrane B7-H3 costimulatory molecule but reduction of its soluble form in multiple sclerosis. J Clin Immunol. 2013;33(1):118–26.CrossRef Jiang J, Jiang J, Liu C, Zhang G, Gao L, Chen Y, et al. Enhancement of membrane B7-H3 costimulatory molecule but reduction of its soluble form in multiple sclerosis. J Clin Immunol. 2013;33(1):118–26.CrossRef
19.
go back to reference Sun J, Liu C, Gao L, Guo Y, Zhang Y, Wu P, et al. Correlation between B7-H3 expression and rheumatoid arthritis: a new polymorphism haplotype is associated with increased disease risk. Clin Immunol (Orlando, Fla). 2015;159(1):23–32.CrossRef Sun J, Liu C, Gao L, Guo Y, Zhang Y, Wu P, et al. Correlation between B7-H3 expression and rheumatoid arthritis: a new polymorphism haplotype is associated with increased disease risk. Clin Immunol (Orlando, Fla). 2015;159(1):23–32.CrossRef
20.
go back to reference Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, et al. Classification criteria for Sjogren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis. 2002;61(6):554–8.CrossRef Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, et al. Classification criteria for Sjogren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis. 2002;61(6):554–8.CrossRef
21.
go back to reference Chen X, Aqrawi LA, Utheim TP, Tashbayev B, Utheim OA, Reppe S, et al. Elevated cytokine levels in tears and saliva of patients with primary Sjogren’s syndrome correlate with clinical ocular and oral manifestations. Scientific Rep. 2019;9(1):7319.CrossRef Chen X, Aqrawi LA, Utheim TP, Tashbayev B, Utheim OA, Reppe S, et al. Elevated cytokine levels in tears and saliva of patients with primary Sjogren’s syndrome correlate with clinical ocular and oral manifestations. Scientific Rep. 2019;9(1):7319.CrossRef
22.
go back to reference Nakamura H, Kawakami A, Ida H, Koji T, Eguchi K. EGF activates PI3 K-Akt and NF-kappaB via distinct pathways in salivary epithelial cells in Sjogren’s syndrome. Rheumatol Int. 2007;28(2):127–36.CrossRef Nakamura H, Kawakami A, Ida H, Koji T, Eguchi K. EGF activates PI3 K-Akt and NF-kappaB via distinct pathways in salivary epithelial cells in Sjogren’s syndrome. Rheumatol Int. 2007;28(2):127–36.CrossRef
23.
go back to reference Yoshimura S, Nakamura H, Horai Y, Nakajima H, Shiraishi H, Hayashi T, et al. Abnormal distribution of AQP5 in labial salivary glands is associated with poor saliva secretion in patients with Sjogren’s syndrome including neuromyelitis optica complicated patients. Mod Rheumatol. 2016;26(3):384–90.CrossRef Yoshimura S, Nakamura H, Horai Y, Nakajima H, Shiraishi H, Hayashi T, et al. Abnormal distribution of AQP5 in labial salivary glands is associated with poor saliva secretion in patients with Sjogren’s syndrome including neuromyelitis optica complicated patients. Mod Rheumatol. 2016;26(3):384–90.CrossRef
24.
go back to reference Xie C, Liu D, Chen Q, Yang C, Wang B, Wu H. Soluble B7-H3 promotes the invasion and metastasis of pancreatic carcinoma cells through the TLR4/NF-kappaB pathway. Scientific Rep. 2016;6:27528.CrossRef Xie C, Liu D, Chen Q, Yang C, Wang B, Wu H. Soluble B7-H3 promotes the invasion and metastasis of pancreatic carcinoma cells through the TLR4/NF-kappaB pathway. Scientific Rep. 2016;6:27528.CrossRef
25.
go back to reference Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369(2):122–33.CrossRef Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369(2):122–33.CrossRef
26.
go back to reference Sznol M, Chen L. Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer. Clin Cancer Res. 2013;19(5):1021–34.CrossRef Sznol M, Chen L. Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer. Clin Cancer Res. 2013;19(5):1021–34.CrossRef
27.
go back to reference Chapoval AI, Ni J, Lau JS, Wilcox RA, Flies DB, Liu D, et al. B7-H3: a costimulatory molecule for T cell activation and IFN-gamma production. Nat Immunol. 2001;2(3):269–74.CrossRef Chapoval AI, Ni J, Lau JS, Wilcox RA, Flies DB, Liu D, et al. B7-H3: a costimulatory molecule for T cell activation and IFN-gamma production. Nat Immunol. 2001;2(3):269–74.CrossRef
28.
go back to reference Prasad DV, Nguyen T, Li Z, Yang Y, Duong J, Wang Y, et al. Murine B7-H3 is a negative regulator of T cells. J Immunol (Baltimore, Md: 1950). 2004;173(4):2500–6.CrossRef Prasad DV, Nguyen T, Li Z, Yang Y, Duong J, Wang Y, et al. Murine B7-H3 is a negative regulator of T cells. J Immunol (Baltimore, Md: 1950). 2004;173(4):2500–6.CrossRef
29.
go back to reference Wang J, Chong KK, Nakamura Y, Nguyen L, Huang SK, Kuo C, et al. B7-H3 associated with tumor progression and epigenetic regulatory activity in cutaneous melanoma. J Invest Dermatol. 2013;133(8):2050–8.CrossRef Wang J, Chong KK, Nakamura Y, Nguyen L, Huang SK, Kuo C, et al. B7-H3 associated with tumor progression and epigenetic regulatory activity in cutaneous melanoma. J Invest Dermatol. 2013;133(8):2050–8.CrossRef
30.
go back to reference Arigami T, Narita N, Mizuno R, Nguyen L, Ye X, Chung A, et al. B7-h3 ligand expression by primary breast cancer and associated with regional nodal metastasis. Ann Surg. 2010;252(6):1044–51.CrossRef Arigami T, Narita N, Mizuno R, Nguyen L, Ye X, Chung A, et al. B7-h3 ligand expression by primary breast cancer and associated with regional nodal metastasis. Ann Surg. 2010;252(6):1044–51.CrossRef
31.
go back to reference Fauci JM, Straughn JM Jr, Ferrone S, Buchsbaum DJ. A review of B7-H3 and B7-H4 immune molecules and their role in ovarian cancer. Gynecol Oncol. 2012;127(2):420–5.CrossRef Fauci JM, Straughn JM Jr, Ferrone S, Buchsbaum DJ. A review of B7-H3 and B7-H4 immune molecules and their role in ovarian cancer. Gynecol Oncol. 2012;127(2):420–5.CrossRef
32.
go back to reference Loos M, Hedderich DM, Ottenhausen M, Giese NA, Laschinger M, Esposito I, et al. Expression of the costimulatory molecule B7-H3 is associated with prolonged survival in human pancreatic cancer. BMC Cancer. 2009;9:463.CrossRef Loos M, Hedderich DM, Ottenhausen M, Giese NA, Laschinger M, Esposito I, et al. Expression of the costimulatory molecule B7-H3 is associated with prolonged survival in human pancreatic cancer. BMC Cancer. 2009;9:463.CrossRef
33.
go back to reference Zhou Z, Luther N, Ibrahim GM, Hawkins C, Vibhakar R, Handler MH, et al. B7-H3, a potential therapeutic target, is expressed in diffuse intrinsic pontine glioma. J Neurooncol. 2013;111(3):257–64.CrossRef Zhou Z, Luther N, Ibrahim GM, Hawkins C, Vibhakar R, Handler MH, et al. B7-H3, a potential therapeutic target, is expressed in diffuse intrinsic pontine glioma. J Neurooncol. 2013;111(3):257–64.CrossRef
34.
go back to reference Lemke D, Pfenning PN, Sahm F, Klein AC, Kempf T, Warnken U, et al. Costimulatory protein 4IgB7H3 drives the malignant phenotype of glioblastoma by mediating immune escape and invasiveness. Clin Cancer Res. 2012;18(1):105–17.CrossRef Lemke D, Pfenning PN, Sahm F, Klein AC, Kempf T, Warnken U, et al. Costimulatory protein 4IgB7H3 drives the malignant phenotype of glioblastoma by mediating immune escape and invasiveness. Clin Cancer Res. 2012;18(1):105–17.CrossRef
35.
go back to reference Janakiram M, Shah UA, Liu W, Zhao A, Schoenberg MP, Zang X. The third group of the B7-CD28 immune checkpoint family: HHLA2, TMIGD2, B7x, and B7-H3. Immunol Rev. 2017;276(1):26–39.CrossRef Janakiram M, Shah UA, Liu W, Zhao A, Schoenberg MP, Zang X. The third group of the B7-CD28 immune checkpoint family: HHLA2, TMIGD2, B7x, and B7-H3. Immunol Rev. 2017;276(1):26–39.CrossRef
36.
go back to reference Suh WK, Gajewska BU, Okada H, Gronski MA, Bertram EM, Dawicki W, et al. The B7 family member B7-H3 preferentially down-regulates T helper type 1-mediated immune responses. Nat Immunol. 2003;4(9):899–906.CrossRef Suh WK, Gajewska BU, Okada H, Gronski MA, Bertram EM, Dawicki W, et al. The B7 family member B7-H3 preferentially down-regulates T helper type 1-mediated immune responses. Nat Immunol. 2003;4(9):899–906.CrossRef
37.
go back to reference Leitner J, Klauser C, Pickl WF, Stockl J, Majdic O, Bardet AF, et al. B7-H3 is a potent inhibitor of human T-cell activation: no evidence for B7-H3 and TREML2 interaction. Eur J Immunol. 2009;39(7):1754–64.CrossRef Leitner J, Klauser C, Pickl WF, Stockl J, Majdic O, Bardet AF, et al. B7-H3 is a potent inhibitor of human T-cell activation: no evidence for B7-H3 and TREML2 interaction. Eur J Immunol. 2009;39(7):1754–64.CrossRef
38.
go back to reference Hashiguchi M, Kobori H, Ritprajak P, Kamimura Y, Kozono H, Azuma M. Triggering receptor expressed on myeloid cell-like transcript 2 (TLT-2) is a counter-receptor for B7-H3 and enhances T cell responses. Proc Natl Acad Sci USA. 2008;105(30):10495–500.CrossRef Hashiguchi M, Kobori H, Ritprajak P, Kamimura Y, Kozono H, Azuma M. Triggering receptor expressed on myeloid cell-like transcript 2 (TLT-2) is a counter-receptor for B7-H3 and enhances T cell responses. Proc Natl Acad Sci USA. 2008;105(30):10495–500.CrossRef
39.
go back to reference Sun J, Lai H, Shen D, Wu P, Yang J, Sun Z, et al. Reduced sB7-H3 Expression in the Peripheral Blood of Systemic Lupus Erythematosus Patients. J Immunol Res. 2017;2017:5728512.PubMedPubMedCentral Sun J, Lai H, Shen D, Wu P, Yang J, Sun Z, et al. Reduced sB7-H3 Expression in the Peripheral Blood of Systemic Lupus Erythematosus Patients. J Immunol Res. 2017;2017:5728512.PubMedPubMedCentral
40.
go back to reference Castagnola M, Scarano E, Passali GC, Messana I, Cabras T, Iavarone F, et al. Salivary biomarkers and proteomics: future diagnostic and clinical utilities. Acta otorhinolaryngologica Italica: organo ufficiale della Societa italiana di otorinolaringologia e chirurgia cervico-facciale. 2017;37(2):94–101. Castagnola M, Scarano E, Passali GC, Messana I, Cabras T, Iavarone F, et al. Salivary biomarkers and proteomics: future diagnostic and clinical utilities. Acta otorhinolaryngologica Italica: organo ufficiale della Societa italiana di otorinolaringologia e chirurgia cervico-facciale. 2017;37(2):94–101.
41.
go back to reference Direito I, Madeira A, Brito MA, Soveral G. Aquaporin-5: from structure to function and dysfunction in cancer. Cell Mol Life Sci CMLS. 2016;73(8):1623–40.CrossRef Direito I, Madeira A, Brito MA, Soveral G. Aquaporin-5: from structure to function and dysfunction in cancer. Cell Mol Life Sci CMLS. 2016;73(8):1623–40.CrossRef
42.
go back to reference Fang C, Li S, Xu R, Guo H, Jiang R, Ding S, et al. Soluble B7-H3 (sB7-H3) is over-expressed in the serum of type 1 diabetes patients. Diabetes Res Clin Pract. 2018;143:332–6.CrossRef Fang C, Li S, Xu R, Guo H, Jiang R, Ding S, et al. Soluble B7-H3 (sB7-H3) is over-expressed in the serum of type 1 diabetes patients. Diabetes Res Clin Pract. 2018;143:332–6.CrossRef
43.
go back to reference Hoesel B, Schmid JA. The complexity of NF-kappaB signaling in inflammation and cancer. Mol Cancer. 2013;12:86.CrossRef Hoesel B, Schmid JA. The complexity of NF-kappaB signaling in inflammation and cancer. Mol Cancer. 2013;12:86.CrossRef
44.
go back to reference Wang Y, Shnyra A, Africa C, Warholic C, McArthur C. Activation of the extrinsic apoptotic pathway by TNF-alpha in human salivary gland (HSG) cells in vitro, suggests a role for the TNF receptor (TNF-R) and intercellular adhesion molecule-1 (ICAM-1) in Sjogren’s syndrome-associated autoimmune sialadenitis. Arch Oral Biol. 2009;54(11):986–96.CrossRef Wang Y, Shnyra A, Africa C, Warholic C, McArthur C. Activation of the extrinsic apoptotic pathway by TNF-alpha in human salivary gland (HSG) cells in vitro, suggests a role for the TNF receptor (TNF-R) and intercellular adhesion molecule-1 (ICAM-1) in Sjogren’s syndrome-associated autoimmune sialadenitis. Arch Oral Biol. 2009;54(11):986–96.CrossRef
45.
go back to reference Fox RI, Kang HI, Ando D, Abrams J, Pisa E. Cytokine mRNA expression in salivary gland biopsies of Sjogren’s syndrome. J Immunol (Baltimore, Md: 1950). 1994;152(11):5532–9. Fox RI, Kang HI, Ando D, Abrams J, Pisa E. Cytokine mRNA expression in salivary gland biopsies of Sjogren’s syndrome. J Immunol (Baltimore, Md: 1950). 1994;152(11):5532–9.
46.
go back to reference Xu H, Li J, Zhao Y, Liu D. TNFalpha-induced downregulation of microRNA-186 contributes to apoptosis in rat primary cardiomyocytes. Immunobiology. 2017;222(5):778–84.CrossRef Xu H, Li J, Zhao Y, Liu D. TNFalpha-induced downregulation of microRNA-186 contributes to apoptosis in rat primary cardiomyocytes. Immunobiology. 2017;222(5):778–84.CrossRef
Metadata
Title
B7-H3 participates in human salivary gland epithelial cells apoptosis through NF-κB pathway in primary Sjögren’s syndrome
Authors
Ping Li
Ying Yang
Yi Jin
Rui Zhao
Chen Dong
Wenjie Zheng
Tianyi Zhang
Jing Li
Zhifeng Gu
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-019-2017-x

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