Tumor‑associated macrophages recruited by periostin in intrahepatic cholangiocarcinoma stem cells

Zeng,Jiehong; Liu,Zhengkai; Sun,Shuwen; Xie,Jianhong; Cao,Li; Lv,Pin; Nie,Shengdan; Zhang,Bao; Xie,Bowen; Peng,Siyuan; Jiang,Bo

doi:10.3892/ol.2018.8372

Tumor‑associated macrophages recruited by periostin in intrahepatic cholangiocarcinoma stem cells

Authors:
- Jiehong Zeng
- Zhengkai Liu
- Shuwen Sun
- Jianhong Xie
- Li Cao
- Pin Lv
- Shengdan Nie
- Bao Zhang
- Bowen Xie
- Siyuan Peng
- Bo Jiang
View Affiliations

Affiliations: Department of Hepatobiliary Surgery, The First Affiliated Hospital of Hunan Normal University‑Hunan Provincial People's Hospital, Changsha, Hunan 410006, P.R. China, Department of Pharmacy, Yiyang Central Hospital, Yiyang, Hunan 413000, P.R. China, Department of General Surgery, Yiyang Central Hospital, Yiyang, Hunan 413000, P.R. China, Intistute of Clinical Medical Research, The First Affiliated Hospital of Hunan Normal University‑Hunan Provincial People's Hospital, Changsha, Hunan 410006, P.R. China
Published online on: March 29, 2018 https://doi.org/10.3892/ol.2018.8372
Pages: 8681-8686

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

Periostin (POSTN) secreted by intrahepatic cholangiocarcinoma stem cells (ICSCs) serves important roles in promoting tumor progression. The present study aimed to investigate POSTN‑recruited tumor‑associated macrophages (TAMs) in intrahepatic cholangiocarcinoma (ICC). A total of 50 cases were used to investigate the distribution of ICSCs and TAMs in ICC. HCCC‑9810 cells were sorted by cluster of differentiation (CD)44, the expression of POSTN of CD44+ (cancer stem cells) and CD44‑ cells (non‑cancer stem cells), and medium were evaluated by western blot analysis. HCCC‑9810 cells and THP‑1 macrophages were used to detect the effects of POSTN on recruiting TAMs in vitro. The present study revealed that CD44+ cells in ICC tissues and the HCCC‑9810 cell line were associated with high POSTN secretion levels. Furthermore, POSTN was associated with TAM density in primary ICC tissues. Additionally, POSTN increased the migration of TAMs derived from THP‑1 cells. These findings suggested that POSTN secreted by ICSCs may serve important functions in TAM recruitment, and it may be a potential curative strategy to target the tumor microenvironment in ICC.

View Figures

View References

1	Goodman ZD: Neoplasms of the liver. Mod Pathol. 20:S49–S60. 2007. View Article : Google Scholar : PubMed/NCBI
2	Nakanuma Y, Harada K, Ishikawa A, Zen Y and Sasaki M: Anatomic and molecular pathology of intrahepatic cholangiocarcinoma. J Hepatobiliary Pancreat Surg. 10:265–281. 2003. View Article : Google Scholar : PubMed/NCBI
3	Parkin DM, Bray F, Ferlay J and Pisani P: Global cancer statistics, 2002. CA Cancer J Clin. 55:74–108. 2005. View Article : Google Scholar : PubMed/NCBI
4	Okuno M, Ebata T, Yokoyama Y, Igami T, Sugawara G, Mizuno T, Yamaguchi J and Nagino M: Appraisal of inflammation-based prognostic scores in patients with unresectable perihilar cholangiocarcinoma. J Hepatobiliary Pancreat Sci. 23:636–642. 2016. View Article : Google Scholar : PubMed/NCBI
5	Shaib Y and El-Serag HB: The epidemiology of cholangiocarcinoma. Semin Liver Dis. 24:115–125. 2004. View Article : Google Scholar : PubMed/NCBI
6	Patel T: Worldwide trends in mortality from biliary tract malignancies. BMC Cancer. 2:102002. View Article : Google Scholar : PubMed/NCBI
7	Sun YF, Xu Y, Yang XR, Guo W, Zhang X, Qiu SJ, Shi RY, Hu B, Zhou J and Fan J: Circulating stem cell-like epithelial cell adhesion molecule-positive tumor cells indicate poor prognosis of hepatocellular carcinoma after curative resection. Hepatology. 57:1458–1468. 2013. View Article : Google Scholar : PubMed/NCBI
8	Chiba T, Zheng YW, Kita K, Yokosuka O, Saisho H, Onodera M, Miyoshi H, Nakano M, Zen Y, Nakanuma Y, et al: Enhanced self-renewal capability in hepatic stem/progenitor cells drives cancer initiation. Gastroenterology. 133:937–950. 2007. View Article : Google Scholar : PubMed/NCBI
9	Wu XZ and Yu XH: Bone marrow cells: The source of hepatocellular carcinoma? Med Hypotheses. 69:36–42. 2007. View Article : Google Scholar : PubMed/NCBI
10	Borovski T, De Sousa E, Melo F, Vermeulen L and Medema JP: Cancer stem cell niche: The place to be. Cancer Res. 71:634–639. 2011. View Article : Google Scholar : PubMed/NCBI
11	Schiavoni G, Gabriele L and Mattei F: The tumor microenvironment: A pitch for multiple players. Front Oncol. 3:902013. View Article : Google Scholar : PubMed/NCBI
12	Biswas SK, Allavena P and Mantovani A: Tumor-associated macrophages: Functional diversity, clinical significance, and open questions. Semin Immunopathol. 35:585–600. 2013. View Article : Google Scholar : PubMed/NCBI
13	Cook J and Hagemann T: Tumour-associated macrophages and cancer. Curr Opin Pharmacol. 13:595–601. 2013. View Article : Google Scholar : PubMed/NCBI
14	Sielska M, Przanowski P, Wylot B, Gabrusiewicz K, Maleszewska M, Kijewska M, Zawadzka M, Kucharska J, Vinnakota K, Kettenmann H, et al: Distinct roles of CSF family cytokines in macrophage infiltration and activation in glioma progression and injury response. J Pathol. 230:310–321. 2013. View Article : Google Scholar : PubMed/NCBI
15	Staudt ND, Jo M, Hu J, Bristow JM, Pizzo DP, Gaultier A, VandenBerg SR and Gonias SL: Myeloid cell receptor LRP1/CD91 regulates monocyte recruitment and angiogenesis in tumors. Cancer Res. 73:3902–3912. 2013. View Article : Google Scholar : PubMed/NCBI
16	Zhang G, Guo L, Yang C, Liu Y, He Y, Du Y, Wang W and Gao F: A novel role of breast cancer-derived hyaluronan on inducement of M2-like tumor-associated macrophages formation. Oncoimmunology. 5:e11721542016. View Article : Google Scholar : PubMed/NCBI
17	Oishi K, Sakaguchi T, Baba S, Suzuki S and Konno H: Macrophage density and macrophage colony-stimulating factor expression predict the postoperative prognosis in patients with intrahepatic cholangiocarcinoma. Surg Today. 45:715–722. 2015. View Article : Google Scholar : PubMed/NCBI
18	Mantovani A and Sica A: Macrophages, innate immunity and cancer: Balance, tolerance, and diversity. Curr Opin Immunol. 22:231–237. 2010. View Article : Google Scholar : PubMed/NCBI
19	Liu JY, Yang XJ, Geng XF, Huang CQ, Yu Y and Li Y: Prognostic significance of tumor-associated macrophages density in gastric cancer: A systemic review and meta-analysis. Minerva Med. 107:314–321. 2016.PubMed/NCBI
20	Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, Shao R, Anderson RM, Rich JN and Wang XF: Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell. 5:329–339. 2004. View Article : Google Scholar : PubMed/NCBI
21	Baril P, Gangeswaran R, Mahon PC, Caulee K, Kocher HM, Harada T, Zhu M, Kalthoff H, Crnogorac-Jurcevic T and Lemoine NR: Periostin promotes invasiveness and resistance of pancreatic cancer cells to hypoxia-induced cell death: Role of the beta4 integrin and the PI3k pathway. Oncogene. 26:2082–2094. 2007. View Article : Google Scholar : PubMed/NCBI
22	Malanchi I, Santamaria-Martínez A, Susanto E, Peng H, Lehr HA, Delaloye JF and Huelsken J: Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 481:85–89. 2011. View Article : Google Scholar : PubMed/NCBI
23	Zhou W, Ke SQ, Huang Z, Flavahan W, Fang X, Paul J, Wu L, Sloan AE, McLendon RE, Li X, et al: Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat Cell Biol. 17:170–182. 2015. View Article : Google Scholar : PubMed/NCBI
24	Michaylira CZ, Wong GS, Miller CG, Gutierrez CM, Nakagawa H, Hammond R, Klein-Szanto AJ, Lee JS, Kim SB, Herlyn M, et al: Periostin, a cell adhesion molecule, facilitates invasion in the tumor microenvironment and annotates a novel tumor-invasive signature in esophageal cancer. Cancer Res. 70:5281–5292. 2010. View Article : Google Scholar : PubMed/NCBI
25	Liu Y, Li F, Gao F, Xing L, Qin P, Liang X, Zhang J, Qiao X, Lin L, Zhao Q and Du L: Periostin promotes tumor angiogenesis in pancreatic cancer via Erk/VEGF signaling. Oncotarget. 7:40148–40159. 2016.PubMed/NCBI
26	Nathan H, Aloia TA, Vauthey JN, Abdalla EK, Zhu AX, Schulick RD, Choti MA and Pawlik TM: A proposed staging system for intrahepatic cholangiocarcinoma. Ann Surg Oncol. 16:14–22. 2009. View Article : Google Scholar : PubMed/NCBI
27	Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A and Locati M: The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25:677–686. 2004. View Article : Google Scholar : PubMed/NCBI
28	Popivanova BK, Kostadinova FI, Furuichi K, Shamekh MM, Kondo T, Wada T, Egashira K and Mukaida N: Blockade of a chemokine, CCL2, reduces chronic colitis-associated carcinogenesis in mice. Cancer Res. 69:7884–7892. 2009. View Article : Google Scholar : PubMed/NCBI
29	Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA and Pollard JW: CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 475:222–225. 2011. View Article : Google Scholar : PubMed/NCBI
30	Pyonteck SM, Gadea BB, Wang HW, Gocheva V, Hunter KE, Tang LH and Joyce JA: Deficiency of the macrophage growth factor CSF-1 disrupts pancreatic neuroendocrine tumor development. Oncogene. 31:1459–1467. 2012. View Article : Google Scholar : PubMed/NCBI
31	Germano G, Frapolli R, Belgiovine C, Anselmo A, Pesce S, Liguori M, Erba E, Uboldi S, Zucchetti M, Pasqualini F, et al: Role of macrophage targeting in the antitumor activity of trabectedin. Cancer Cell. 23:249–262. 2013. View Article : Google Scholar : PubMed/NCBI