Periostin expression in intra-tumoral stromal cells is prognostic and predictive for colorectal carcinoma via creating a cancersupportive niche

Oncotarget

Volumn 7, Issue 1, 2016, Pages 798-813

  Xu, Xiaowen ^a   Chang, Wenjun ^a   Yuan, Jie ^a   Han, Xue ^b   Tan, Xiaojie ^a   Ding, Yibo ^a   Luo, Yanxin ^c   Cai, Hui ^a   Liu, Yan ^a   Gao, Xianhua ^a   Liu, Qizhi ^a   Yu, Yongwei ^a   Du, Yan ^a   Wang, Hao ^a   Ma, Liye ^a   Wang, Jianping ^c   Chen, Kun ^d   Ding, Yanqing ^e   Fu, Chuangang ^a   Cao, Guangwen ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b Center for Disease Control and Prevention of Yangpu District   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d ZHEJIANG UNIVERSITY   (China)

^e SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Colorectal carcinoma; Drug resistance; Fibroblast; Periostin; Prognosis

Indexed keywords

BETA CATENIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR RUNX2; WNT PROTEIN; ANTINEOPLASTIC AGENT; CELL ADHESION MOLECULE; FLUOROURACIL; POSTN PROTEIN, HUMAN; TUMOR MARKER;

ADULT; ARTICLE; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CANCER STAGING; CANCER TISSUE; CELL ANCHORAGE; CELL PROLIFERATION; CHINA; COLORECTAL CARCINOMA; CONTROLLED STUDY; DOSE RESPONSE; DRUG RESISTANCE; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; METASTASIS; MIDDLE AGED; POSTOPERATIVE PERIOD; PREDICTION; PROTEIN EXPRESSION; PROTEIN TARGETING; SCORING SYSTEM; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR GROWTH; TUMOR INVASION; AGED; CELL LINE; CLINICAL TRIAL; COLORECTAL NEOPLASMS; DISEASE FREE SURVIVAL; GENE EXPRESSION REGULATION; GENETICS; HT-29 CELL LINE; METABOLISM; MULTICENTER STUDY; OUTCOME ASSESSMENT; PREDICTIVE VALUE; PROCEDURES; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STATISTICS AND NUMERICAL DATA; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; WESTERN BLOTTING;

AGED; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; BLOTTING, WESTERN; CELL ADHESION MOLECULES; CELL LINE; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DISEASE-FREE SURVIVAL; FEMALE; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HT29 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; OUTCOME ASSESSMENT (HEALTH CARE); PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STROMAL CELLS; TUMOR MICROENVIRONMENT;

EID: 84985877690     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/ONCOTARGET.5985     Document Type: Article

References (40)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010; 127:2893-2917
2. Schmoll HJ, Van Cutsem E, Stein A, Valentini V, Glimelius B, Haustermans K, Nordlinger B, van de Velde CJ, Balmana J, Regula J, Nagtegaal ID, Beets-Tan RG, Arnold D, et al. ESMO Consensus Guidelines for management of patients with colon and rectal cancer. a personalized approach to clinical decision making. Ann Oncol. 2012; 23:2479-2516
3. Iinuma H, Watanabe T, Mimori K, Adachi M, Hayashi N, Tamura J, Matsuda K, Fukushima R, Okinaga K, Sasako M, Mori M. Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes' stage B and C colorectal cancer. J Clin Oncol. 2011; 29:1547-1555
4. Mao C, Wu XY, Yang ZY, Threapleton DE, Yuan JQ, Yu YY, Tang JL. Concordant analysis of KRAS, BRAF, PIK3CA mutations, and PTEN expression between primary colorectal cancer and matched metastases. Sci Rep. 2015; 5:8065
5. Kwon CH, Park HJ, Choi JH, Lee JR, Kim HK, Jo HJ, Kim HS, Oh N, Song GA, Park DY. Snail and serpinA1 promote tumor progression and predict prognosis in colorectal cancer. Oncotarget. 2015; 6:20312-20326
6. Yothers G, O'Connell MJ, Lee M, Lopatin M, Clark-Langone KM, Millward C, Paik S, Sharif S, Shak S, Wolmark N. Validation of the 12-gene colon cancer recurrence score in NSABP C-07 as a predictor of recurrence in patients with stage II and III colon cancer treated with fluorouracil and leucovorin (FU/LV) and FU/LV plus oxaliplatin. J Clin Oncol. 2013; 31:4512-4519
7. Han Y, Cai H, Ma L, Ding Y, Tan X, Liu Y, Su T, Yu Y, Chang W, Zhang H, Fu C, Cao G. Nuclear orphan receptor NR4A2 confers chemoresistance and predicts unfavorable prognosis of colorectal carcinoma patients who received postoperative chemotherapy. Eur J Cancer. 2013; 49:3420-3430
8. Chang W, Gao X, Han Y, Du Y, Liu Q, Wang L, Tan X, Zhang Q, Liu Y, Zhu Y, Yu Y, Fan X, Zhang H, et al. Gene expression profiling-derived immunohistochemistry signature with high prognostic value in colorectal carcinoma. Gut. 2014; 63:1457-1467
9. Conway SJ, Izuhara K, Kudo Y, Litvin J, Markwald R, Ouyang G, Arron JR, Holweg CT, Kudo A. The role of periostin in tissue remodeling across health and disease. Cell Mol Life Sci. 2014; 71:1279-1288
10. Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, Shao R, Anderson RM, Rich JN, Wang XF. Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell. 2004; 5:329-339
11. Wu G, Wang X, Zhang X. Clinical implications of periostin in the liver metastasis of colorectal cancer. Cancer Biother Radiopharm. 2013; 28:298-302
12. Kikuchi Y, Kashima TG, Nishiyama T, Shimazu K, Morishita Y, Shimazaki M, Kii I, Horie H, Nagai H, Kudo A, Fukayama M. Periostin is expressed in pericryptal fibroblasts and cancer-associated fibroblasts in the colon. J Histochem Cytochem. 2008; 56:753-764
13. Erkan M, KleeffJ, Gorbachevski A, Reiser C, Mitkus T, Esposito I, Giese T, Büchler MW, Giese NA, Friess H. Periostin creates a tumor-supportive microenvironment in the pancreas by sustaining fibrogenic stellate cell activity. Gastroenterology. 2007; 132:1447-1464
14. Ryner L, Guan Y, Firestein R, Xiao Y, Choi Y, Rabe C, Lu S, Fuentes E, Huw-Yuh L, Lackner MR, Fu L, Amler LC, Bais C, et al. Up-regulation of periostin and reactive stroma is associated with primary chemoresistance and predicts clinical outcomes in epithelial ovarian cancer. Clin Cancer Res. 2015; 21:2941-2951
15. Tian Y, Choi CH, Li QK, Rahmatpanah FB, Chen X, Kim SR, Veltri R, Chia D, Zhang Z, Mercola D, Zhang H. Overexpression of periostin in stroma positively associated with aggressive prostate cancer. PLoS One. 2015; 10:e0121502
16. Underwood TJ, Hayden AL, Derouet M, Garcia E, Noble F, White MJ, Thirdborough S, Mead A, Clemons N, Mellone M, Uzoho C, Primrose JN, Blaydes JP, et al. Cancer-associated fibroblasts predict poor outcome and promote periostin-dependent invasion in oesophageal adenocarcinoma. J Pathol. 2015; 235:466-477
17. Kikuchi Y, Kunita A, Iwata C, Komura D, Nishiyama T, Shimazu K, Takeshita K, Shibahara J, Kii I, Morishita Y, Yashiro M, Hirakawa K, Miyazono K, et al. The niche component periostin is produced by cancer-associated fibroblasts, supporting growth of gastric cancer through ERK activation. Am J Pathol. 2014; 184:859-870
18. Ishiba T, Nagahara M, Nakagawa T, Sato T, Ishikawa T, Uetake H, Sugihara K, Miki Y, Nakanishi A. Periostin suppression induces decorin secretion leading to reduced breast cancer cell motility and invasion. Sci Rep. 2014; 4:7069
19. Utispan K, Thuwajit P, Abiko Y, Charngkaew K, Paupairoj A, Chau-in S, Thuwajit C. Gene expression profiling of cholangiocarcinoma-derived fibroblast reveals alterations related to tumor progression and indicates periostin as a poor prognostic marker. Mol Cancer. 2010; 9:13
20. Ben QW, Zhao Z, Ge SF, Zhou J, Yuan F, Yuan YZ. Circulating levels of periostin may help identify patients with more aggressive colorectal cancer. Int J Oncol. 2009; 34:821-828
21. Baril P, Gangeswaran R, Mahon PC, Caulee K, Kocher HM, Harada T, Zhu M, KalthoffH, Crnogorac-Jurcevic T, 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. 2007; 26:2082-2094
22. Gillan L, Matei D, Fishman DA, Gerbin CS, Karlan BY, Chang DD. Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility. Cancer Res. 2002; 62:5358-5364
23. Lee YJ, Kim IS, Park SA, Kim Y, Lee JE, Noh DY, Kim KT, Ryu SH, Suh PG. Periostin-binding DNA aptamer inhibits breast cancer growth and metastasis. Mol Ther. 2013; 21:1004-1013
24. Hu Q, Tong S, Zhao X, Ding W, Gou Y, Xu K, Sun C, Xia G. Periostin mediates TGF-β-induced epithelial mesenchymal transition in prostate cancer cells. Cell Physiol Biochem. 2015; 36:799-809
25. Masuoka M, Shiraishi H, Ohta S, Suzuki S, Arima K, Aoki S, Toda S, Inagaki N, Kurihara Y, Hayashida S, Takeuchi S, Koike K, Ono J, et al. Periostin promotes chronic allergic inflammation in response to Th2 cytokines. J Clin Invest. 2012; 122:2590-2600
26. Siriwardena BS, Kudo Y, Ogawa I, Kitagawa M, Kitajima S, Hatano H, Tilakaratne WM, Miyauchi M, Takata T. Periostin is frequently overexpressed and enhances invasion and angiogenesis in oral cancer. Br J Cancer. 2006; 95:1396-1403
27. Kudo Y, Ogawa I, Kitajima S, Kitagawa M, Kawai H, Gaffney PM, Miyauchi M, Takata T. Periostin promotes invasion and anchorage-independent growth in the metastatic process of head and neck cancer. Cancer Res. 2006; 66:6928-6935
28. Aguilera ó, González-Sancho JM, Zazo S, Rincón R, Fernández AF, Tapia O, Canals F, Morte B, Calvanese V, Orgaz JL, Niell N, Aguilar S, Freije JM, et al. Nuclear DICKKOPF-1 as a biomarker of chemoresistance and poor clinical outcome in colorectal cancer. Oncotarget. 2015; 6:5903-5917
29. Allen JE, El-Deiry WS. Calcein-effluxing human colon cancer cells are enriched for self-renewal capacity and depend on β-catenin. Oncotarget. 2013; 4:184-191
30. Wang X, Liu J, Wang Z, Huang Y, Liu W, Zhu X, Cai Y, Fang X, Lin S, Yuan L, Ouyang G. Periostin contributes to the acquisition of multipotent stem cell-like properties in human mammary epithelial cells and breast cancer cells. PLoS One. 2013; 8:e72962
31. Ayadi M, Bouygues A, Ouaret D, Ferrand N, Chouaib S, Thiery JP, Muchardt C, Sabbah M, Larsen AK. Chronic chemotherapeutic stress promotes evolution of stemness and WNT/beta-catenin signaling in colorectal cancer cells: implications for clinical use of WNT-signaling inhibitors. Oncotarget. 2015; 6:18518-18533
32. Zheng Z, He X, Xie C, Hua S, Li J, Wang T, Yao M, Vignarajan S, Teng Y, Hejazi L, Liu B, Dong Q. Targeting cytosolic phospholipase A2 a in colorectal cancer cells inhibits constitutively activated protein kinase B (AKT) and cell proliferation. Oncotarget. 2014; 5:12304-12316
33. Nagaraju GP, Alese OB, Landry J, Diaz R, El-Rayes BF. HSP90 inhibition downregulates thymidylate synthase and sensitizes colorectal cancer cell lines to the effect of 5FU-based chemotherapy. Oncotarget. 2014; 5:9980-9991
34. Cui C, Feng H, Shi X, Wang Y, Feng Z, Liu J, Han Z, Fu J, Fu Z, Tong H. Artesunate down-regulates immunosuppression from colorectal cancer Colon26 and RKO cells in vitro by decreasing transforming growth factor β1 and interleukin-10. Int Immunopharmacol. 2015; 27:110-121
35. Bakhtyar N, Wong N, Kapoor A, Cutz JC, Hill B, Ghert M, Tang D. Clear cell renal cell carcinoma induces fibroblastmediated production of stromal periostin. Eur J Cancer. 2013; 49:3537-3546
36. Zhou W, Ke SQ, Huang Z, Flavahan W, Fang X, Paul J, Wu L, Sloan AE, McLendon RE, Li X, Rich JN, Bao S. Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat Cell Biol. 2015; 17:170-182
37. Li X, Tan X, Yu Y, Chen H, Chang W, Hou J, Xu D, Ma L, Cao G. D9S168 microsatellite alteration predicts a poor prognosis in patients with clear cell renal cell carcinoma and correlates with the down-regulation of protein tyrosine phosphatase receptor delta. Cancer. 2011; 117:4201-4211
38. Tan X, Wang Y, Han Y, Chang W, Su T, Hou J, Xu D, Yu Y, Ma W, Thompson TC, Cao G. Genetic variation in the GSTM3 promoter confer risk and prognosis of renal cell carcinoma by reducing gene expression. Br J Cancer. 2013; 109:3105-3115
39. Tan X, He S, Han Y, Yu Y, Xiao J, Xu D, Wang G, Du Y, Chang W, Yin J, Su T, Hou J, Cao G. Establishment and characterization of clear cell renal cell carcinoma cell lines with different metastatic potential from Chinese patients. Cancer Cell Int. 2013; 13:20
40. Han Y, Cai H, Ma L, Ding Y, Tan X, Chang W, Guan W, Liu Y, Shen Q, Yu Y, Zhang H, Cao G. Expression of orphan nuclear receptor NR4A2 in gastric cancer cells confers chemoresistance and predicts an unfavorable postoperative survival of gastric cancer patients with chemotherapy. Cancer. 2013; 119:3436-3445