Higher matrix stiffness upregulates osteopontin expression in hepatocellular carcinoma cells mediated by integrin β1/GSK3β/β-catenin signaling pathway

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  You, Yang ^a   Zheng, Qiongdan ^a   Dong, Yinying ^a   Wang, Yaohui ^b   Zhang, Lan ^a   Xue, Tongchun ^a   Xie, Xiaoying ^a   Hu, Chao ^a   Wang, Zhiming ^a   Chen, Rongxin ^a   Wang, Yanhong ^a   Cui, Jiefeng ^a   Ren, Zhenggang ^a  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BETA1 INTEGRIN; OSTEOPONTIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; GSK3B PROTEIN, HUMAN; SPP1 PROTEIN, HUMAN;

ARTICLE; CELL GROWTH; CELL NUCLEUS; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; GENE; GENE EXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MICROARRAY ANALYSIS; MMP9 GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; UPREGULATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; LIVER TUMOR; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; TUMOR CELL LINE;

ANTIGENS, CD29; BETA CATENIN; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; HUMANS; LIVER NEOPLASMS; OSTEOPONTIN; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TISSUE ARRAY ANALYSIS; UP-REGULATION;

EID: 84942875236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134243     Document Type: Article

References (61)

1. El-Tanani MK: Role of osteopontin in cellular signaling and metastatic phenotype. Front Biosci 2008, 13:4276-4284.
2. Weber GF: The metastasis gene osteopontin: a candidate target for cancer therapy. Biochim Biophys Acta 2001, 1552:61-85.
3. Ribeiro SA, Oliveira JP: Osteopontin expression according to molecular profile of invasive breast cancer. Int J Biol Markers 2008, 23(3):154-60.
4. Visintin I, Feng Z, Longton G, Ward DC, Alvero AB, Lai Y, et al. Diagnostic markers for early detection of ovarian cancer. Clin Cancer Res 2008, 15; 14(4):1065-72.
5. Cho H, Hong SW, Oh YJ, Kim MA, Kang ES, Lee JM, et al. Clinical significance of osteopontin expression in cervical cancer. J Cancer Res Clin Oncol 2008; 134(8):909-17
6. Chen RX, Xia YH, Cui JF, Xue TC, Ye SL: Osteopontin, a single marker for predicting the prognosis of patients with tumor-node-metastasis stage I hepatocellular carcinoma after surgical resection. J Gastroenterol Hepatol 2010, 25:1435-1442.
7. Lin F, Li Y, Cao J, Fan S, Wen J, Zhu G, et al. Overexpression of osteopontin in hepatocellular carcinoma and its relationships with metastasis, invasion of tumor cells. Mol Biol Rep 2011, 38:5205-5210.
8. Denhardt DT, Mistretta D, Chambers AF, Krishna S, Porter JF, Raghuram S, et al. Transcriptional regulation of osteopontin and the metastatic phenotype: evidence for a Ras-activated enhancer in the human OPN promoter. Clin Exp Metastasis 2003, 20:77-84.
9. Chuang CY, Chang H, Lin P, Sun SJ, Chen PH, Lin YY, et al. Up-regulation of osteopontin expression by aryl hydrocarbon receptor via both ligand-dependent and ligand-independent pathways in lung cancer. Gene 2012, 492:262-269.
10. Ravindranath A, Yuen HF, Chan KK, Grills C, Fennell DA, Lappin TR, et al. Wnt-beta-catenin-Tcf-4 sig-nalling-modulated invasiveness is dependent on osteopontin expression in breast cancer. Br J Cancer 2011, 105: 542-551.
11. Parkin DM, Bray F, Ferlay J, Pisani P: Estimating the world cancer burden: Globocan 2000. Int J Cancer 2001, 94:153-156.
12. Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology, 2004, 127: S35-50.
13. Georges PC1, Hui JJ, Gombos Z, McCormick ME, Wang AY, Uemura M, et al. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am J Physiol Gastrointest Liver Physiol 2007, 293(6):G1147-54.
14. Yin M1, Talwalkar JA, Glaser KJ, Manduca A, Grimm RC, et al. Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 2007, 5(10):1207-1213e2.
15. Masuzaki R, Tateishi R, Yoshida H, Yoshida H, Sato S, Ward CJ, et al. Risk assessment of hepatocellular carcinoma in chronic hepatitis C patients by transient elastography. J Clin Gastroenterol 2008, 42 (7):839-43.
16. Brabek J, Mierke CT, Rosel D, Vesely P, Fabry B: The role of the tissue microenvironment in the regulation of cancer cell motility and invasion. Cell Commun Signal 2010, 8:22. doi: 10.1186/1478-811X-8-22PMID: 20822526
17. Engler AJ, Griffin MA, Sen S, Bönnemann CG, Sweeney HL, Discher DE: et al. Myotubes differentiate optimally on substrates with tissue-like stiffness. J Cell Biol 2004, 166: 877-887.
18. Lo CM, Wang HB, Dembo M, Wang YL: Cell movement is guided by the rigidity of the substrate. Biophys J 2000, 79(1):144-52.
19. Yeung T, Georges PC, Flanagan LA, Marg B, Ortiz M, Funaki M, et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 2005, 60: 24-34.
20. Schrader J, Gordon-Walker TT, Aucott RL, van Deemter M, Quaas A, Walsh S, et.al. Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 2011, 53: 1192-1205.
21. Yoshioka K, Hashimoto S, Kawabe N: Measurement of liver stiffness as a non-invasive method for diagnosis of diagnosis of non-alcoholic fatty liver disease. Hepatol Res 2014 Jul 7 doi: 101111/hepr12388:T-aheadofprint
22. Dong Y, Xie X, Wang Z, Hu C, Zheng Q, Wang Y, et al. Increasing matrix stiffness upregulates vascular endothelial growth factor expression in hepatocellular carcinoma cells mediated by integrin beta1. Biochem Biophys Res Commun 2014, 444:427-432.
23. Wong CC, Tse AP, Huang YP, Zhu YT, Chiu DK, et al. Lysyl oxidase-like 2 is critical to tumor microenvironment and metastatic niche formation in hepatocellular carcinoma. Hepatology 2014, 5: 60(5):1645-58.
24. Cassereau L, Miroshnikova YA, Ou G, Lakins J, Weaver VM, Lai RK, et al. Cell tension, matrix mechanics, and cancer development. Cancer Cell, 2005. 8(3): p. 175-6. PMID: 16169461
25. Zhao G1, Cui J, Qin Q, Zhang J, Liu L, Deng S, et al. Mechanical stiffness of liver tissues in relation to integrin β1 expression may influence the development of hepatic cirrhosis and hepatocellular carcinoma. Journal of Surgical Oncology 2010, 102:482-489. doi: 10.1002/jso.21613 PMID: 20872952
26. Kumar C.CSignaling by integrin receptors. Oncogene, 1998. 17(11 Reviews): p. 1365-73. PMID: 9779984
27. Burkhalter RJ, Symowicz J, Hudson LG, Gottardi CJ, Stack MS: Integrin regulation of beta-catenin signaling in ovarian carcinoma. J Biol Chem, 2011. 286(26): p. 23467-75. doi:10.1074/jbc.M110.199539 PMID: 21518759
28. Mitra A, Menezes ME, Pannell LK, Mulekar MS, Honkanen RE: DNAJB6 chaperones PP2A mediated dephosphorylation of GSK3beta to downregulate beta-catenin transcription target, osteopontin. Oncogene 2012, 31:4472-4483.
29. Ravindranath A, Yuen HF, Chan KK, Grills C, Fennell DA, Lappin TR, et al. Wnt-beta-catenin-Tcf-4 signalling-modulated invasiveness is dependent on osteopontin expression in breast cancer. Br J Cancer, 2011. 105(4): p. 542-51. doi: 10.1038/bjc.2011.269 PMID: 21772333
30. Kang S, Bennett CN, Gerin I, Rapp LA, Hankenson KD, Macdougald OA: Wnt Signaling Stimulates Osteoblastogenesis of Mesenchymal Precursors by Suppressing CCAAT/Enhancer-binding Protein and Peroxisome Proliferator-activated Receptor. Journal of Biological Chemistry 2007, 282:14515-14524.
31. Bennett CN, Ross SE, Longo KA, Bajnok L, Hemati N, ohnson KW, et al. Regulation of Wnt signaling during adipogenesis. J Biol Chem 2002, 277:30998-31004.
32. Basson M.D: An intracellular signal pathway that regulates cancer cell adhesion in response to extra-cellular forces. Cancer Res, 2008. 68(1): p. 2-4. doi: 10.1158/0008-5472.CAN-07-2992 PMID: 18172287
33. Ooi LP, Crawford DH, Gotley DC, Clouston AD, Strong RW, Gobe GC, et al. Evidence that "myofibro-blast-like" cells are the cellular source of capsular. J Hepatol 1997, 26(4):798-807.
34. Silva R, D'Amico G, Hodivala-Dilke KM, Reynolds LE: Integrins: the keys to unlocking angiogenesis. Arterioscler Thromb Vasc Biol 2008, 28(10):1703-13.
35. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor. Cell 2005; 121(3):335-48.
36. Maegdefrau U, Amann T, Winklmeier A, Braig S, Schubert T, Naeem R, et al. Bone morphogenetic protein 4 is induced in hepato-cellular carcinoma by hypoxia. J Pathol 2009, 218:520-529.
37. Bergamini C, Sgarra C, Trerotoli P, Lupo L, Azzariti A, Antonaci S, et al. Laminin-5 stimulates hepato-cellular carcinoma growth through a different function. Hepatology 2007, 46(6):1801-9.
38. Faouzi S, Le Bail B, Neaud V, Boussarie L, Saric J, Bioulac-Sage P, et al. Myofibroblasts are responsible for collagen synthesis in the stroma of human. J Hepatol 1999, 30(2):275-84.
39. Guirouilh J, Castroviejo M, Balabaud C, Desmouliere A, Rosenbaum J. Hepatocarcinoma cells stimulate hepatocyte growth factor secretion in human liver. Int J Oncol 2000, 17(4):777-81.
40. Liang Y, Jeong J, DeVolder RJ, Cha C, Wang F, Tong YW, et al. A cell-instructive hydrogel to regulate malignancy of 3D tumor spheroids with matrix rigidity. Biomaterials 2011, 32(35):9308-15.
41. Leal-Egaña A, Fritsch A, Heidebrecht F, Díaz-Cuenca A, Nowicki M, Bader A, et al. Tuning liver stiffness against tumours: an in vitro study using entrapped cells. J Mech Behav Biomed Mater 2012, 9:113-21
42. Fiorino S, Bacchi-Reggiani L, Pontoriero L, Gallo C, Chili E, Masetti M, et al. Tensegrity model hypothesis: may this paradigm be useful to explain hepatic and persistent hepatitis B or hepatitis C virus infection? JOP 2014, 15(2):151-64.
43. Liu C, Liu Y, Xie H, Zhao S, Xu X, Fan L, et al. Role of three-dimensional matrix stiffness in regulating the chemoresistance of hepatocellular carcinoma cells. Biotechnol Appl Biochem 2014 Oct 2 doi: 10.1002/bab.1302 [Epub ahead of print]
44. Schrader J, Gordon-Walker TT, Aucott RL, van Deemter M, Quaas A, Walsh S, et al. Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy. Hepatology 2011; 53(4):1192-205.
45. Huang X, Hang R, Wang X, Lin N, Zhang X, Tang B. Matrix stiffness in three-dimensional systems effects on the behavior of C3A. Artif Organs 2013, 37(2):166-74.
46. Zhao G, Cui J, Qin Q, Zhang J, Liu L, Deng S, et al. Mechanical stiffness of liver tissues in relation to integrin beta1 expression. J Surg Oncol 2010, 102(5):482-9.
47. Kim SH, Chung YH, Yang SH, Kim JA, Jang MK, Kim SE, et al. Prognostic value of serum osteopontin in hepatocellular carcinoma patients. Korean J Hepatol 2009, 15(3):320-30.
48. Sun J, Xu HM, Zhou HJ, Dong QZ, Zhao Y, Fu LY, et al. The prognostic significance of preoperative plasma levels of osteopontin in patients with TNM stage-I of hepatocellular carcinoma. J Cancer Res Clin Oncol 2010, 136(1):1-7.
49. Weber GF, Lett GS, Haubein NC.Osteopontin is a marker for cancer aggressiveness and patient survival. Br J Cancer 2010, 103(6):861-9.
50. Ye QH, Qin LX, Forgues M, He P, Kim JW, et al. Predicting hepatitis B virus-positive metastatic hepatocellular carcinomas using. Nat Med 2003, 9(4):416-23.
51. Zhang H, Ye QH, Ren N, Zhao L, Wang YF, Peng AC, et al. The prognostic significance of preoperative plasma levels of osteopontin in patients with hepatocellular carcinoma. J Cancer Res Clin Oncol 2006, 132:709-717.
52. Pan HW, Ou YH, Peng SY, Liu SH, Lai PL, Lee PH, et al. Overexpression of osteopontin is associated with intrahepatic metastasis, early. Cancer 2003, 98(1):119-27.
53. Zhao J, Dong L, Lu B, Wu G, Xu D, Chen J, et al. Down-regulation of osteopontin suppresses growth and metastasis of hepatocellular. Gastroenterology 2008, 135(3):956-68.
54. Ramachandran S, Kwon KY, Shin SJ, Kwon SH, Cha SD, Lee HG, et al. Regulatory role of osteopontin in malignant transformation of endometrial cancer. Mol Biol Rep 2013, 40(5):3623-9.
55. Tuck AB, Chambers AF, Allan AL. Osteopontin overexpression in breast cancer: knowledge gained and possible implications for clinical management. J Cell Biochem 2007, 102(4):859-68.
56. El-Tanani M, Platt-Higgins A, Rudland PS, Campbell FC. Ets gene PEA3 cooperates with beta-catenin-Lef-1 and c-Jun in regulation of osteopontin transcription. J Biol Chem 2004, 279(20):20794-806.
57. Chen HT, Tsou HK, Chang CH, Tang CH. Hepatocyte growth factor increases osteopontin expression in human osteoblasts. PLoS One 2012; 7(6):e38378.
58. Doble BW, Patel S, Wood GA, Kockeritz LK, Woodgett JR. Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev Cell 2007, 12(6):957-71.
59. Wang Hua, Sun Wen, Ma Junqing, Pan Yongchu, Wang Lin, Zhang Weibing. Polycystin-1 Mediates Mechanical Strain-Induced Osteoblastic Mechanoresponses via Potentiation of Intracellular Calcium and Akt/β-Catenin Pathway. PLoS One. 2014; 9(3): e91730.
60. Cadigan KM, Waterman ML. TCF/LEFs and Wnt signaling in the nucleus. Cold Spring Harb Perspect Biol 2012, 4(11)
61. Li TW1, Ting JH, Yokoyama NN, Bernstein A, van de Wetering M, Waterman ML. Wnt activation and alternative promoter repression of LEF1 in colon cancer. Mol Cell Biol 2006, 26(14):5284-99.