Encapsulated human hepatocellular carcinoma cells by alginate gel beads as an in vitro metastasis model

Experimental Cell Research

Volumn 319, Issue 14, 2013, Pages 2135-2144

  Xu, Xiao xi ^a,b   Liu, Chang ^a,b   Liu, Yang ^a   Li, Nan ^a,b   Guo, Xin ^a   Wang, Shu jun ^a,c   Sun, Guang wei ^a   Wang, Wei ^a   Ma, Xiao jun ^a  

^a DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c DALIAN UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Alginate bead; Invasion; Matrix metalloproteinase; Metastasis model; Tumor microenvironment

Indexed keywords

ALGINIC ACID;

ARTICLE; CARCINOMA CELL; CELL ADHESION; CELL INVASION; CELL PROLIFERATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL CARCINOMA; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TUMOR SPHEROID; ZYMOGRAPHY;

EID: 84880750808     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.05.013     Document Type: Article

References (52)

1. Blum H.E. Hepatocellular carcinoma: therapy and prevention. World J. Gastroenterol. 2005, 11:7391-7400.
2. Kam Y., Rejniak K.A., Anderson A.R.A. Cellular modeling of cancer invasion: Integration of in silico and in vitro approaches. J. Cell Physiol. 2012, 227:431-438.
3. Curran S., Murray G.I. Matrix metalloproteinases in tumour invasion and metastasis. J. Pathol. 1999, 189:300-308.
4. Johnson J. Cell adhesion molecules of the immunoglobulin supergene family and their role in malignant transformation and progression to metastatic disease. Cancer Metastasis Rev. 1991, 10:11-22.
5. Chen X., Lingala S., Khoobyari S., Nolta J., Zern M.A., Wu J. Epithelial mesenchymal transition and hedgehog signaling activation are associated with chemoresistance and invasion of hepatoma subpopulations. J. Hepatol. 2011, 55:838-845.
6. Yamada K.M., Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell 2007, 130:601-610.
7. Mastro A.M., Vogler E.A.A. Three-dimensional osteogenic tissue model for the study of metastatic tumor cell interactions with bone. Cancer Res. 2009, 69:4097-4100.
8. Kievit F.M., Florczyk S.J., Leung M.C., Veiseh O., Park J.O., Disis M.L., et al. Chitosan-alginate 3D scaffolds as a mimic of the glioma tumor microenvironment. Biomaterials 2010, 31:5903-5910.
9. Pampaloni F., Reynaud E.G., Stelzer E.H.K. The third dimension bridges the gap between cell culture and live tissue. Nat. Rev. Mol. Cell Biol. 2007, 8:839-845.
10. Kim J.B. Three-dimensional tissue culture models in cancer biology. Semin. Cancer Biol. 2005, 15:365-377.
11. Kunz-Schughart L.A., Kreutz M., Knuechel R. Multicellular spheroids: a three-dimensional in vitro culture system to study tumour biology. Int. J. Exp. Pathol. 1998, 79:1-23.
12. Wu L., Carlo D., Lee L. Microfluidic self-assembly of tumor spheroids for anticancer drug discovery. Biomed. Microdevices 2008, 10:197-202.
13. Zhang X., Wang W., Yu W., Xie Y., Zhang X., Zhang Y., et al. Development of an in vitro multicellular tumor spheroid model using microencapsulation and its application in anticancer drug screening and testing. Biotechnol. Prog. 2005, 21:1289-1296.
14. Liang Y., Jeong J., DeVolder R.J., Cha C., Wang F., Tong Y.W., et al. A cell-instructive hydrogel to regulate malignancy of 3D tumor spheroids with matrix rigidity. Biomaterials 2011, 32:9308-9315.
15. Goosen M.F.A., O'Shea G.M., Gharapetian H.M., Chou S., Sun A.M. Optimization of microencapsulation parameters: semipermeable microcapsules as a bioartificial pancreas. Biotechnol. Bioeng. 1985, 27:146-150.
16. Coward S.M., Legallais C., David B., Thomas M., Foo Y., Mavri-Damelin D., et al. Alginate-encapsulated HepG2 cells in a fluidized bed bioreactor maintain function in human liver failure plasma. Artif. Organs 2009, 33:1117-1126.
17. Rokstad A.M., Gustafsson B.I., Espevik T., Bakke I., Pfragner R., Svejda B., et al. Microencapsulation of small intestinal neuroendocrine neoplasm cells for tumor model studies. Cancer Sci. 2012, 103:1230-1237.
18. Akeda K., Nishimura A., Satonaka H., Shintani K., Kusuzaki K., Matsumine A., et al. Three-dimensional alginate spheroid culture system of murine osteosarcoma. Oncol. Rep. 2009, 22:997-1003.
19. Khalil M., Shariat-Panahi A., Tootle R., Ryder T., McCloskey P., Roberts E., et al. Human hepatocyte cell lines proliferating as cohesive spheroid colonies in alginate markedly upregulate both synthetic and detoxificatory liver function. J. Hepatol. 2001, 34:68-77.
20. Coward S.M., Selden C., Mantalaris A., Hodgson H.J.F. Proliferation rates of HepG2 cells encapsulated in alginate are increased in a microgravity environment compared with static cultures. Artif. Organs 2005, 29:152-158.
21. Selden C., Khalil M., Hodgson H. Three dimensional culture upregulates extracellular matrix protein expression in human liver cell lines-a step towards mimicking the liver in vivo?. Int. J. Artif. Organs 2000, 23:774-781.
22. Wang Q., Li S.Y., Xie Y.B., Yu W.T., Xiong Y., Ma X.J., et al. Cytoskeletal reorganization and repolarization of hepatocarcinoma cells in APA microcapsule to mimic native tumor characteristics. Hepatol. Res. 2006, 35:96-103.
23. 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 in tumour-like microcapsules. J. Mech. Behav. Biomed. Mater. 2012, 9:113-121.
24. Drury J.L., Mooney D.J. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 2003, 24:4337-4351.
25. Li Y., Tang Z.Y., Ye S.L., Liu Y.K., Chen J., Xue Q., et al. Establishment of cell clones with different metastatic potential from the metastatic hepatocellular carcinoma cell line MHCC97. World J. Gastroenterol. 2001, 7:630-636.
26. Li Y., Tang Z.Y., Ye S.L., Liu B.B., Liu Y.K., Chen J., et al. Establishment of a hepatocellular carcinoma cell line with unique metastatic characteristics through in vivo selection and screening for metastasis-related genes through cDNA microarray. J. Cancer Res. Clin. Oncol. 2003, 129:43-51.
27. Bugarski B., Li Q., Goosen M.F.A., Poncelet D., Neufeld R.J., Vunjak G. Electrostatic droplet generation: mechanism of polymer droplet formation. AIChE J. 1994, 40:1026-1031.
28. Loessner D., Stok K.S., Lutolf M.P., Hutmacher D.W., Clements J.A., Rizzi S.C. Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells. Biomaterials 2010, 31:8494-8506.
29. Lengyel E., Gum R., Juarez J., Clayman G., Seiki M., Sato H., et al. Induction of Mr 92,000 type IV collagenase expression in a squamous cell carcinoma cell line by fibroblasts. Cancer Res. 1995, 55:963-967.
30. Albini A., Iwamoto Y., Kleinman H.K., Martin G.R., Aaronson S.A., Kozlowski J.M., et al. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res. 1987, 47:3239-3245.
31. Welch D. Technical considerations for studying cancer metastasis in vivo. Clin. Exp. Metastasis 1997, 15:272-306.
32. Tian B., Li Y., Ji X.-N., Chen J., Xue Q., Ye S.-L., et al. Basement membrane proteins play an active role in the invasive process of human hepatocellular carcinoma cells with high metastasis potential. J. Cancer Res. Clin. Oncol. 2005, 131:80-86.
33. Qin L.-X., Tang Z.-Y. Recent progress in predictive biomarkers for metastatic recurrence of human hepatocellular carcinoma: a review of the literature. J. Cancer Res. Clin. Oncol. 2004, 130:497-513.
34. Yang C., Zeisberg M., Lively J.C., Nyberg P., Afdhal N., Kalluri R. Integrin alpha1beta1 and alpha2beta1 are the key regulators of hepatocarcinoma cell invasion across the fibrotic matrix microenvironment. Cancer Res. 2003, 63:8312-8317.
35. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2:161-174.
36. Yamaguchi H., Wyckoff J., Condeelis J. Cell migration in tumors. Curr. Opin. Cell Biol. 2005, 17:559-564.
37. Fischbach C., Chen R., Matsumoto T., Schmelzle T., Brugge J.S., Polverini P.J., et al. Engineering tumors with 3D scaffolds. Nat. Methods 2007, 4:855-860.
38. Heppner G.H. Tumor heterogeneity. Cancer Res. 1984, 44:2259-2265.
39. Deryugina E.I., Quigley J.P. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006, 25:9-34.
40. Stetler-Stevenson W. Progelatinase A activation during tumor cell invasion. Invasion Metastasis 1994, 14:259.
41. Chae K.J., Rha S.Y., Oh B.K., Koo J.S., Kim Y.J., Choi J., et al. Expression of matrix metalloproteinase-2 and -9 and tissue inhibitor of metalloproteinase-1 and -2 in intraductal and nonintraductal growth type of cholangiocarcinoma. Am. J. Gastroenterol. 2004, 99:68-75.
42. Murnane M.J., Cai J., Shuja S., McAneny D., Klepeis V., Willett J.B. Active MMP-2 effectively identifies the presence of colorectal cancer. Int. J. Cancer 2009, 125:2893-2902.
43. Talukdar S., Mandal M., Hutmacher D.W., Russell P.J., Soekmadji C., Kundu S.C. Engineered silk fibroin protein 3D matrices for in vitro tumor model. Biomaterials 2011, 32:2149-2159.
44. Wang N., Zhu M., Tsao S.-W., Man K., Zhang Z., Feng Y. Up-regulation of TIMP-1 by genipin inhibits MMP-2 activities and suppresses the metastatic potential of human hepatocellular carcinoma. PLoS One 2012, 7:e46318.
45. Thiery J.P., Acloque H., Huang R.Y.J., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
46. Lin R.Z., Chou L.F., Chien C.C.M., Chang H.Y. Dynamic analysis of hepatoma spheroid formation: roles of E-cadherin and beta 1-integrin. Cell Tissue Res. 2006, 324:411-422.
47. Christiansen J.J., Rajasekaran A.K. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res. 2006, 66:8319-8326.
48. Pinkas J., Leder P. MEK1 signaling mediates transformation and metastasis of EpH4 mammary epithelial cells independent of an epithelial to mesenchymal transition. Cancer Res. 2002, 62:4781-4790.
49. Sun A., O'Shea G., Goosen M. Injectable microencapsulated islet cells as a bioartificial pancreas. Appl. Biochem. Biotechnol. 1984, 10:87-99.
50. Huang X., Hang R., Wang X., Lin N., Zhang X., Tang B. Matrix stiffness in three-dimensional systems effects on the behavior of C3A cells. Artif. Organs 2013, 37:166-174.
51. Schrader J., Gordon-Walker T.T., Aucott R.L., 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.
52. Wells R.G. The role of matrix stiffness in regulating cell behavior. Hepatology 2008, 47:1394-1400.