B7-H1 enhances proliferation ability of gastric cancer stem-like cells as a receptor

Yang,Yupeng; Wu,Ke; Zhao,Ende; Li,Wei; Shi,Liang; Xie,Gengchen; Jiang,Bin; Wang,Yaxin; Li,Ruidong; Zhang,Peng; Shuai,Xiaoming; Wang,Guobin; Tao,Kaixiong

doi:10.3892/ol.2015.2949

B7-H1 enhances proliferation ability of gastric cancer stem-like cells as a receptor

Authors:
- Yupeng Yang
- Ke Wu
- Ende Zhao
- Wei Li
- Liang Shi
- Gengchen Xie
- Bin Jiang
- Yaxin Wang
- Ruidong Li
- Peng Zhang
- Xiaoming Shuai
- Guobin Wang
- Kaixiong Tao
View Affiliations

Affiliations: Department of General Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430022, P.R. China, Department of Clinical Laboratory, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430022, P.R. China, Department of Anesthesiology and Critical Care, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430022, P.R. China
Published online on: February 10, 2015 https://doi.org/10.3892/ol.2015.2949
Pages: 1833-1838

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Cancer stem‑like cells (CSCs) are a rare tumorigenic population with the ability to self‑renew in numerous cancer types. Their existence is considered a pivotal contributor to tumor recurrence. B7‑H1 is a ligand of inhibitory inducible co‑stimulator (ICOS) that is broadly expressed on various human cancers. ICOS acts as a ligand of programmed death‑1 (PD‑1) on T cells, induces the immune escape of cancer cells and also acts as a receptor mediating anti‑apoptotic effects on cancer cells. However, the expression and function of B7‑H1 on CSCs is not yet clear. In the present study, gastric cancer samples were collected and the B7‑H1 expression in gastric cancer CSCs was detected. Ki67, a proliferation marker, was found to be expressed at a higher rate in B7‑H1+ CSCs compared with the B7‑H1‑ counterparts. SGC‑7901 cells, a gastric cancer cell line, were cultured in serum‑free medium to form sphere cells that possessed stem cell characteristics and could express B7‑H1 with the stimulation of interferon‑γ. The proliferative ability of sphere cells was enhanced following B7‑H1 activation with recombinant PD‑1 in vivo and in vitro. This effect could be eliminated by neutralizing B7‑H1. Overall, B7‑H1 can act as a stimulating receptor for CSCs, and induce CSC proliferation. Blocking B7‑H1 on CSCs may possess therapeutic potential for treating gastric cancer.

View Figures

View References

1	Yuasa Y: Control of gut differentiation and intestinal-type gastric carcinogenesis. Nat Rev Cancer. 3:592–600. 2003. View Article : Google Scholar : PubMed/NCBI
2	Dean M, Fojo T and Bates S: Tumour stem cells and drug resistance. Nat Rev Cancer. 5:275–284. 2005. View Article : Google Scholar : PubMed/NCBI
3	Dalerba P, Cho RW and Clarke MF: Cancer stem cells: models and concepts. Annu Rev Med. 58:267–284. 2007. View Article : Google Scholar
4	Nishikawa S, Konno M, Hamabe A, et al: Aldehyde dehydrogenase high gastric cancer stem cells are resistant to chemotherapy. Int J Oncol. 42:1437–1442. 2013.PubMed/NCBI
5	Takaishi S, Okumura T, Tu S, et al: Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells. 27:1006–1020. 2009. View Article : Google Scholar : PubMed/NCBI
6	Yang L, Levi E, Zhu S, Du J and Majumdar AP: Cancer stem cells biomarkers in gastric carcinogenesis. J Gastrointest Cancer. 44:428–435. 2013. View Article : Google Scholar : PubMed/NCBI
7	Liu WD, Zhang T, Wang CL, et al: Sphere-forming tumor cells possess stem-like properties in human fibrosarcoma primary tumors and cell lines. Oncol Lett. 4:1315–1320. 2012.PubMed/NCBI
8	Salerno M, Avnet S, Bonuccelli G, et al: Sphere-forming cell subsets with cancer stem cell properties in human musculoskeletal sarcomas. Int J Oncol. 43:95–102. 2013.PubMed/NCBI
9	Tian T, Zhang Y, Wang S, Zhou J and Xu S: Sox2 enhances the tumorigenicity and chemoresistance of cancer stem-like cells derived from gastric cancer. J Biomed Res. 26:336–345. 2012. View Article : Google Scholar
10	Jiang J, Zhang Y, Chuai S, et al: Trastuzumab (herceptin) targets gastric cancer stem cells characterized by CD90 phenotype. Oncogene. 31:671–682. 2012. View Article : Google Scholar
11	Yang L, Ping YF, Yu X, et al: Gastric cancer stem-like cells possess higher capability of invasion and metastasis in association with a mesenchymal transition phenotype. Cancer Lett. 310:46–52. 2011.PubMed/NCBI
12	Chen L: Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol. 4:336–347. 2004. View Article : Google Scholar : PubMed/NCBI
13	Dong H, Strome SE, Salomao DR, et al: Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 8:793–800. 2002. View Article : Google Scholar : PubMed/NCBI
14	Chen XL, Cao XD, Kang AJ, et al: In situ expression and significance of B7 costimulatory molecules within tissues of human gastric carcinoma. World J Gastroenterol. 9:1370–1373. 2003.PubMed/NCBI
15	Lu B, Chen L, Liu L, et al: T-cell-mediated tumor immune surveillance and expression of B7 co-inhibitory molecules in cancers of the upper gastrointestinal tract. Immunol Res. 50:269–275. 2011. View Article : Google Scholar : PubMed/NCBI
16	Wu C, Zhu Y, Jiang J, et al: Immunohistochemical localization of programmed death-1 ligand-1 (PD-L1) in gastric carcinoma and its clinical significance. Acta Histochem. 108:19–24. 2006. View Article : Google Scholar : PubMed/NCBI
17	Shi F, Shi M, Zeng Z, et al: PD-1 and PD-L1 upregulation promotes CD8(+) T-cell apoptosis and postoperative recurrence in hepatocellular carcinoma patients. Int J Cancer. 128:887–896. 2011. View Article : Google Scholar
18	Wang L, Qian J, Lu Y, et al: Immune evasion of mantle cell lymphoma: expression of B7-H1 leads to inhibited T-cell response to and killing of tumor cells. Haematologica. 98:1458–1466. 2013. View Article : Google Scholar : PubMed/NCBI
19	Sznol M and Chen L: Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer-response. Clin Cancer Res. 19:55422013. View Article : Google Scholar
20	Azuma T, Yao S, Zhu G, et al: B7-H1 is a ubiquitous antiapoptotic receptor on cancer cells. Blood. 111:3635–3643. 2008. View Article : Google Scholar : PubMed/NCBI
21	Curiel TJ, Wei S, Dong H, et al: Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat Med. 9:562–567. 2003. View Article : Google Scholar : PubMed/NCBI
22	Eppihimer MJ, Gunn J, Freeman GJ, et al: Expression and regulation of the PD-L1 immunoinhibitory molecule on microvascular endothelial cells. Microcirculation. 9:133–145. 2002. View Article : Google Scholar : PubMed/NCBI
23	Yamazaki T, Akiba H, Iwai H, et al: Expression of programmed death 1 ligands by murine T cells and APC. J Immunol. 169:5538–5545. 2002. View Article : Google Scholar : PubMed/NCBI
24	Zhang P, Su DM, Liang M and Fu J: Chemopreventive agents induce programmed death-1-ligand 1 (PD-L1) surface expression in breast cancer cells and promote PD-L1-mediated T cell apoptosis. Mol Immunol. 45:1470–1476. 2008. View Article : Google Scholar
25	Tao K, Wu C, Wu K, et al: Quantitative analysis of promoter methylation of the EDNRB gene in gastric cancer. Med Oncol. 29:107–112. 2012. View Article : Google Scholar
26	Leng Z, Tao K, Xia Q, et al: Kruppel-like factor 4 acts as an oncogene in colon cancer stem cell-enriched spheroid cells. PloS One. 8:e560822013. View Article : Google Scholar
27	Kim YS, Park GB, Lee HK, et al: Cross-linking of B7-H1 on EBV-transformed B cells induces apoptosis through reactive oxygen species production, JNK signaling activation, and fasL expression. J Immunol. 181:6158–6169. 2008. View Article : Google Scholar : PubMed/NCBI
28	Radziewicz H, Ibegbu CC, Fernandez ML, et al: Liver-infiltrating lymphocytes in chronic human hepatitis C virus infection display an exhausted phenotype with high levels of PD-1 and low levels of CD127 expression. J Virol. 81:2545–2553. 2007. View Article : Google Scholar :
29	Freeman GJ, Long AJ, Iwai Y, et al: Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med. 192:1027–1034. 2000. View Article : Google Scholar : PubMed/NCBI
30	Tsushima F, Yao S, Shin T, et al: Interaction between B7-H1 and PD-1 determines initiation and reversal of T-cell anergy. Blood. 110:180–185. 2007. View Article : Google Scholar : PubMed/NCBI
31	Blank C, Kuball J, Voelkl S, et al: Blockade of PD-L1 (B7-H1) augments human tumor-specific T cell responses in vitro. Int J Cancer. 119:317–327. 2006. View Article : Google Scholar : PubMed/NCBI
32	Wong RM, Scotland RR, Lau RL, et al: Programmed death-1 blockade enhances expansion and functional capacity of human melanoma antigen-specific CTLs. Int Immunol. 19:1223–1234. 2007. View Article : Google Scholar : PubMed/NCBI
33	Butte MJ, Keir ME, Phamduy TB, Sharpe AH and Freeman GJ: Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity. 27:111–122. 2007. View Article : Google Scholar : PubMed/NCBI