Galectin-1 from cancer-associated fibroblasts induces epithelial-mesenchymal transition through β1 integrin-mediated upregulation of Gli1 in gastric cancer

Journal of Experimental and Clinical Cancer Research

Volumn 35, Issue 1, 2016, Pages 1-13

  Chong, Yang ^a   Tang, Dong ^a   Xiong, Qingquan ^a   Jiang, Xuetong ^a   Xu, Chuanqi ^a   Huang, Yuqin ^a   Wang, Jie ^a   Zhou, Huaicheng ^a   Shi, Youquan ^a   Wu, Xiaoqing ^a   Wang, Daorong ^a  

^a NORTHERN JIANGSU PEOPLE S HOSPITAL   (China)

Author keywords

Cancer associated fibroblasts; Epithelial mesenchymal transition; Galectin 1; Gastric cancer; Glioma associated oncogene 1; Hedgehog; 1 integrin

Indexed keywords

BETA1 INTEGRIN; GALECTIN 1; TRANSCRIPTION FACTOR GLI1; GLI1 PROTEIN, HUMAN; LGALS1 PROTEIN, HUMAN;

ADULT; ARTICLE; CANCER ASSOCIATED FIBROBLAST; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; METASTASIS; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STOMACH CANCER; STOMACH CARCINOGENESIS; TUMOR INVASION; UPREGULATION; CANCER STAGING; CELL MOTION; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PROGNOSIS; STOMACH TUMOR; SURVIVAL ANALYSIS; TUMOR CELL LINE;

CANCER-ASSOCIATED FIBROBLASTS; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GALECTIN 1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRIN BETA1; MALE; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROGNOSIS; STOMACH NEOPLASMS; SURVIVAL ANALYSIS; UP-REGULATION; ZINC FINGER PROTEIN GLI1;

EID: 84994417094     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/s13046-016-0449-1     Document Type: Article

References (35)

1. Hynes RO. Metastatic potential: generic predisposition of the primary tumor or rare, metastatic variants-or both? Cell. 2003;113:821-3.
2. Jia Y, Cao B, Yang Y, Linghu E, Zhan Q, Lu Y, Yu Y, Herman JG, Guo M. Silencing NKD2 by promoter region hypermethylation promotes gastric cancer invasion and metastasis by up-regulating SOX18 in human gastric cancer. Oncotarget. 2015;6:33470-85.
3. Cho HJ, Park SM, Kim IK, Nam IK, Baek KE, Im MJ, Yoo JM, Park SH, Ryu KJ, Han HT, et al. RhoGDI2 promotes epithelial-mesenchymal transition via induction of Snail in gastric cancer cells. Oncotarget. 2014;5:1554-64.
4. Yan Y, Wang LF, Wang RF. Role of cancer-associated fibroblasts in invasion and metastasis of gastric cancer. World J Gastroenterol. 2015;21:9717-26.
5. Zhi K, Shen X, Zhang H, Bi J. Cancer-associated fibroblasts are positively correlated with metastatic potential of human gastric cancers. J Exp Clin Cancer Res. 2010;29:66.
6. Tang D, Gao J, Wang S, Ye N, Chong Y, Huang Y, Wang J, Li B, Yin W, Wang D. Cancer-associated fibroblasts promote angiogenesis in gastric cancer through galectin-1 expression. Tumour Biol. 2016;37:1889-99.
7. Yamamichi F, Shigemura K, Behnsawy HM, Meligy FY, Huang WC, Li X, Yamanaka K, Hanioka K, Miyake H, Tanaka K, et al. Sonic hedgehog and androgen signaling in tumor and stromal compartments drives epithelial-mesenchymal transition in prostate cancer. Scand J Urol. 2014;48:523-32.
8. Savagner P. The epithelial-mesenchymal transition (EMT) phenomenon. Ann Oncol. 2010;21 Suppl 7:vii89-92.
9. Van Ry PM, Wuebbles RD, Key M, Burkin DJ. Galectin-1 Protein Therapy Prevents Pathology and Improves Muscle Function in the mdx Mouse Model of Duchenne Muscular Dystrophy. Mol Ther. 2015;23:1285-97.
10. Chen J, Tang D, Wang S, Li QG, Zhang JR, Li P, Lu Q, Niu G, Gao J, Ye NY, Wang DR. High expressions of galectin-1 and VEGF are associated with poor prognosis in gastric cancer patients. Tumour Biol. 2014;35:2513-9.
11. Bacigalupo ML, Manzi M, Espelt MV, Gentilini LD, Compagno D, Laderach DJ, Wolfenstein-Todel C, Rabinovich GA, Troncoso MF. Galectin-1 triggers epithelial-mesenchymal transition in human hepatocellular carcinoma cells. J Cell Physiol. 2015;230:1298-309.
12. Liu X, Yun F, Shi L, Li ZH, Luo NR, Jia YF. Roles of Signaling Pathways in the Epithelial-Mesenchymal Transition in Cancer. Asian Pac J Cancer Prev. 2015;16:6201-6.
13. Ohta H, Aoyagi K, Fukaya M, Danjoh I, Ohta A, Isohata N, Saeki N, Taniguchi H, Sakamoto H, Shimoda T, et al. Cross talk between hedgehog and epithelial-mesenchymal transition pathways in gastric pit cells and in diffuse-type gastric cancers. Br J Cancer. 2009;100:389-98.
14. Katoh Y, Katoh M. Integrative genomic analyses on GLI1: positive regulation of GLI1 by Hedgehog-GLI, TGFbeta-Smads, and RTK-PI3K-AKT signals, and negative regulation of GLI1 by Notch-CSL-HES/HEY, and GPCR-Gs-PKA signals. Int J Oncol. 2009;35:187-92.
15. Gao Q, Yuan Y, Gan HZ, Peng Q. Resveratrol inhibits the hedgehog signaling pathway and epithelial-mesenchymal transition and suppresses gastric cancer invasion and metastasis. Oncol Lett. 2015;9:2381-7.
16. Pasca di Magliano M, Hebrok M. Hedgehog signalling in cancer formation and maintenance. Nat Rev Cancer. 2003;3:903-11.
17. Yang L, Xie G, Fan Q, Xie J. Activation of the hedgehog-signaling pathway in human cancer and the clinical implications. Oncogene. 2010;29:469-81.
18. Yoo YA, Kang MH, Lee HJ, Kim BH, Park JK, Kim HK, Kim JS, Oh SC. Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer. Cancer Res. 2011;71:7061-70.
19. Yoo YA, Kang MH, Kim JS, Oh SC. Sonic hedgehog signaling promotes motility and invasiveness of gastric cancer cells through TGF-beta-mediated activation of the ALK5-Smad 3 pathway. Carcinogenesis. 2008;29:480-90.
20. Sakaguchi M, Imaizumi Y, Shingo T, Tada H, Hayama K, Yamada O, Morishita T, Kadoya T, Uchiyama N, Shimazaki T, et al. Regulation of adult neural progenitor cells by Galectin-1/beta1 Integrin interaction. J Neurochem. 2010;113:1516-24.
21. Moiseeva EP, Williams B, Goodall AH, Samani NJ. Galectin-1 interacts with beta-1 subunit of integrin. Biochem Biophys Res Commun. 2003;310:1010-6.
22. He XJ, Tao HQ, Hu ZM, Ma YY, Xu J, Wang HJ, Xia YJ, Li L, Fei BY, Li YQ, Chen JZ. Expression of galectin-1 in carcinoma-associated fibroblasts promotes gastric cancer cell invasion through upregulation of integrin beta1. Cancer Sci. 2014;105:1402-10.
23. Giannoni E, Bianchini F, Masieri L, Serni S, Torre E, Calorini L, Chiarugi P. Reciprocal activation of prostate cancer cells and cancer-associated fibroblasts stimulates epithelial-mesenchymal transition and cancer stemness. Cancer Res. 2010;70:6945-56.
24. Hanna A, Shevde LA. Hedgehog signaling: modulation of cancer properies and tumor mircroenvironment. Mol Cancer. 2016;15:24.
25. Sanchez-Ruderisch H, Detjen KM, Welzel M, Andre S, Fischer C, Gabius HJ, Rosewicz S. Galectin-1 sensitizes carcinoma cells to anoikis via the fibronectin receptor alpha5beta1-integrin. Cell Death Differ. 2011;18:806-16.
26. Fischer C, Sanchez-Ruderisch H, Welzel M, Wiedenmann B, Sakai T, Andre S, Gabius HJ, Khachigian L, Detjen KM, Rosewicz S. Galectin-1 interacts with the {alpha}5{beta}1 fibronectin receptor to restrict carcinoma cell growth via induction of p21 and p27. J Biol Chem. 2005;280:37266-77.
27. Barrientos G, Freitag N, Tirado-Gonzalez I, Unverdorben L, Jeschke U, Thijssen VL, Blois SM. Involvement of galectin-1 in reproduction: past, present and future. Hum Reprod Update. 2014;20:175-93.
28. Duan W, Ma J, Ma Q, Xu Q, Lei J, Han L, Li X, Wang Z, Wu Z, Lv S, et al. The Activation of beta1-integrin by Type I Collagen Coupling with the Hedgehog Pathway Promotes the Epithelial-Mesenchymal Transition in Pancreatic Cancer. Curr Cancer Drug Targets. 2014;14:446-57.
29. Ishimoto T, Sawayama H, Sugihara H, Baba H. Interaction between gastric cancer stem cells and the tumor microenvironment. J Gastroenterol. 2014;49:1111-20.
30. Briscoe J, Therond PP: The mechanisms of Hedgehog signalling and its roles in development and disease. Nat Rev Mol Cell Biol 2013, 14:416-429.
31. Amakye D, Jagani Z, Dorsch M: Unraveling the therapeutic potential of the Hedgehog pathway in cancer. Nat Med 2013, 19:1410-1422.
32. Wang ZS, Shen Y, Li X, Zhou CZ, Wen YG, Jin YB, Li JK: Significance and prognostic value of Gli-1 and Snail/E-cadherin expression in progressive gastric cancer. Tumour Biol 2014, 35:1357-1363.
33. Martinez-Bosch N, Fernandez-Barrena MG, Moreno M, Ortiz-Zapater E, Munne-Collado J, Iglesias M, Andre S, Gabius HJ, Hwang RF, Poirier F, et al: Galectin-1 drives pancreatic carcinogenesis through stroma remodeling and Hedgehog signaling activation. Cancer Res 2014, 74:3512-3524.
34. Wang ZS, Shen Y, Li X, Zhou CZ, Wen YG, Jin YB, Li JK. Significance and prognostic value of Gli-1 and Snail/E-cadherin expression in progressive gastric cancer. Tumour Biol. 2014;35:1357-63.
35. Goel HL, Underwood JM, Nickerson JA, Hsieh CC, Languino LR. Beta1 integrins mediate cell proliferation in three-dimensional cultures by regulating expression of the sonic hedgehog effector protein, GLI1. J Cell Physiol. 2010;224:210-7.