Thiol-ene hydrogels as desmoplasia-mimetic matrices for modeling pancreatic cancer cell growth, invasion, and drug resistance

Biomaterials

Volumn 35, Issue 36, 2014, Pages 9668-9677

  Ki, Chang Seok ^a,b   Lin, Tsai Yu ^a   Korc, Murray ^c   Lin, Chien Chi ^a  

^a Indiana University Purdue University Indianapolis   (United States)

^b Seoul National University   (South Korea)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chemo resistance; Epithelial mesenchymal transition; Hydrogel; Pancreatic cancer stem cell; Pancreatic ductal adenocarcinoma

Indexed keywords

BIOMIMETICS; CELL PROLIFERATION; COLLAGEN; CYTOLOGY; DISEASES; HYDROGELS; POLYETHYLENE GLYCOLS; STEM CELLS;

BIOMIMETIC HYDROGELS; CHEMORESISTANCE; DUCTAL ADENOCARCINOMAS; ENCAPSULATED CELL; EPITHELIAL-MESENCHYMAL TRANSITION; MATRIX REMODELING; PANCREATIC CANCERS; VASCULAR ENDOTHELIAL GROWTH FACTOR;

CELL ENGINEERING;

COLLAGEN TYPE 1; EPIDERMAL GROWTH FACTOR; GEMCITABINE; MACROGOL; MATRIX METALLOPROTEINASE 14; NORBORNENE DERIVATIVE; NUCLEAR PROTEIN; NUCLEAR PROTEIN YAP; POLY(ETHYLENE GLYCOL) NORBORNENE; PROTEINASE; THIOL GROUP; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; BIOMIMETIC MATERIAL; HYDROGEL; THIOL DERIVATIVE;

ARTICLE; CANCER GROWTH; CANCER STEM CELL; CELL CULTURE; CELL ENCAPSULATION; CELL FATE; CELL FUNCTION; CELL INVASION; CELL NUCLEUS; CELL PROLIFERATION; CELL SPREADING; CELL STRUCTURE; CELL VIABILITY; COLLAGEN FIBRIL; CONTROLLED STUDY; CROSS LINKING; DRUG RESISTANCE; EPITHELIAL MESENCHYMAL TRANSITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYDROGEL; MORPHOGENESIS; PANCREAS ADENOCARCINOMA; PHOTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR INVASION; UPREGULATION; ADENOCARCINOMA; CARCINOMA, PANCREATIC DUCTAL; CHEMISTRY; CULTURE TECHNIQUE; DRUG EFFECTS; PANCREAS; PANCREATIC NEOPLASMS; PATHOLOGY; PROCEDURES; TUMOR CELL LINE;

ERINACEIDAE;

ADENOCARCINOMA; BIOMIMETIC MATERIALS; CARCINOMA, PANCREATIC DUCTAL; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; HYDROGELS; NEOPLASM INVASIVENESS; PANCREAS; PANCREATIC NEOPLASMS; SULFHYDRYL COMPOUNDS;

EID: 84911376619     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.08.014     Document Type: Article

References (45)

1. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013, 63:11-30.
2. Liu F., Gore A.J., Wilson J.L., Korc M. DUSP1 is a novel target for enhancing pancreatic cancer cell sensitivity to gemcitabine. PLoS One 2014, 9:e84982.
3. Heinemann V., Reni M., Ychou M., Richel D.J., Macarulla T., Ducreux M. Tumour-stroma interactions in pancreatic ductal adenocarcinoma: rationale and current evidence for new therapeutic strategies. Cancer Treat Rev 2014, 40:118-128.
4. McCarroll J.A., Naim S., Sharbeen G., Russia N., Lee J., Kavallaris M., et al. Role of pancreatic stellate cells in chemoresistance in pancreatic cancer. Front Physiol 2014, 5:141.
5. Huang F.T., Zhuan-Sun Y.X., Zhuang Y.Y., Wei S.L., Tang J., Chen W.B., et al. Inhibition of hedgehog signaling depresses self-renewal of pancreatic cancer stem cells and reverses chemoresistance. Int J Oncol 2012, 41:1707-1714.
6. Lee C.J., Dosch J., Simeone D.M. Pancreatic cancer stem cells. JClin Oncol 2008, 26:2806-2812.
7. Maccalli C., Volonte A., Cimminiello C., Parmiani G. Immunology of cancer stem cells in solid tumours. A review. Eur J Cancer 2014, 50:649-655.
8. Hwang W.L., Jiang J.K., Yang S.H., Huang T.S., Lan H.Y., Teng H.W., et al. MicroRNA-146a directs the symmetric division of snail-dominant colorectal cancer stem cells. Nat Cell Biol 2014, 16:268-280.
9. Fessler E., Dijkgraaf F.E., De Sousa E.M.F., Medema J.P. Cancer stem cell dynamics in tumor progression and metastasis: is the microenvironment to blame?. Cancer Lett 2013, 341:97-104.
10. Li C., Heidt D.G., Dalerba P., Burant C.F., Zhang L., Adsay V., et al. Identification of pancreatic cancer stem cells. Cancer Res 2007, 67:1030-1037.
11. Xu M., Li L., Liu Z., Jiao Z., Xu P., Kong X., et al. ABCB2 (TAP1) as the downstream target of SHH signaling enhances pancreatic ductal adenocarcinoma drug resistance. Cancer Lett 2013, 333:152-158.
12. Ng M.R., Brugge J.S. Astiff blow from the stroma: collagen crosslinking drives tumor progression. Cancer Cell 2009, 16:455-457.
13. Raza A., Ki C.S., Lin C.C. The influence of matrix properties on growth and morphogenesis of human pancreatic ductal epithelial cells in 3D. Biomaterials 2013, 34:5117-5127.
14. Ki C.S., Shih H., Lin C.C. Effect of 3D matrix compositions on the efficacy of EGFR inhibition in pancreatic ductal adenocarcinoma cells. Biomacromolecules 2013, 14:3017-3026.
15. Sempere L.F., Gunn J.R., Korc M. Anovel 3-dimensional culture system uncovers growth stimulatory actions by TGF beta in pancreatic cancer cells. Cancer Biol Ther 2011, 12:198-207.
16. Miroshnikova Y.A., Jorgens D.M., Spirio L., Auer M., Sarang-Sieminski A.L., Weaver V.M. Engineering strategies to recapitulate epithelial morphogenesis within synthetic three-dimensional extracellular matrix with tunable mechanical properties. Phys Biol 2011, 8:026013.
17. Fairbanks B.D., Schwartz M.P., Halevi A.E., Nuttelman C.R., Bowman C.N., Anseth K.S. Aversatile synthetic extracellular matrix mimic via thiol-norbornene photopolymerization. Adv Mater 2009, 21:5005-5010.
18. Raza A., Lin C.C. The influence of matrix degradation and functionality on cell survival and morphogenesis in PEG-based hydrogels. Macromol Biosci 2013, 13:1048-1058.
19. Fairbanks B.D., Schwartz M.P., Bowman C.N., Anseth K.S. Photoinitiated polymerization of PEG-diacrylate with lithium phenyl-2,4,6-trimethylbenzoylphosphinate: polymerization rate and cytocompatibility. Biomaterials 2009, 30:6702-6707.
20. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159.
21. Patterson J., Hubbell J.A. Enhanced proteolytic degradation of molecularly engineered PEG hydrogels in response to MMP-1 and MMP-2. Biomaterials 2010, 31:7836-7845.
22. Tibbitt M.W., Anseth K.S. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng 2009, 103:655-663.
23. Pandol S., Edderkaoui M., Gukovsky I., Lugea A., Gukovskaya A. Desmoplasia of pancreatic ductal adenocarcinoma. Clin Gastroenterol Hepatol 2009, 7:S44-S47.
24. Dangi-Garimella S., Krantz S.B., Barron M.R., Shields M.A., Heiferman M.J., Grippo P.J., et al. Three-dimensional collagen I promotes gemcitabine resistance in pancreatic cancer through MT1-MMP-mediated expression of HMGA2. Cancer Res 2011, 71:1019-1028.
25. Dangi-Garimella S., Strouch M.J., Grippo P.J., Bentrem D.J., Munshi H.G. Collagen regulation of let-7 in pancreatic cancer involves TGF-beta 1-mediated membrane type 1-matrix metalloproteinase expression. Oncogene 2011, 30:1002-1008.
26. Nicolas F.J., Hill C.S. Attenuation of the TGF-beta-Smad signaling pathway in pancreatic tumor cells confers resistance to TGF-beta-induced growth arrest. Oncogene 2003, 22:3698-3711.
27. Zhao B., Wei X., Li W., Udan R.S., Yang Q., Kim J., et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007, 21:2747-2761.
28. Zeng Q., Hong W. The emerging role of the hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 2008, 13:188-192.
29. Diep C.H., Zucker K.M., Hostetter G., Watanabe A., Hu C., Munoz R.M., et al. Down-regulation of yes associated protein 1 expression reduces cell proliferation and clonogenicity of pancreatic cancer cells. PLoS One 2012, 7:e32783.
30. Lin C.C., Raza A., Shih H. PEG hydrogels formed by thiol-ene photo-click chemistry and their effect on the formation and recovery of insulin-secreting cell spheroids. Biomaterials 2011, 32:9685-9695.
31. Deharvengt S., Marmarelis M., Korc M. Concomitant targeting of EGF receptor, TGF-beta and Src points to a novel therapeutic approach in pancreatic cancer. PLoS One 2012, 7:e39684.
32. Arda K., Ciledag N., Aktas E., Aribas B.K., Kose K. Quantitative assessment of normal soft-tissue elasticity using shear-wave ultrasound elastography. AJR Am J Roentgenol 2011, 197:532-536.
33. Ottaviano A.J., Sun L., Ananthanarayanan V., Munshi H.G. Extracellular matrix-mediated membrane-type 1 matrix metalloproteinase expression in pancreatic ductal cells is regulated by transforming growth factor-beta1. Cancer Res 2006, 66:7032-7040.
34. Bramhall S.R., Neoptolemos J.P., Stamp G.W., Lemoine N.R. Imbalance of expression of matrix metalloproteinases (MMPs) and tissue inhibitors of the matrix metalloproteinases (TIMPs) in human pancreatic carcinoma. JPathol 1997, 182:347-355.
35. Pugh N., Simpson A.M., Smethurst P.A., de Groot P.G., Raynal N., Farndale R.W. Synergism between platelet collagen receptors defined using receptor-specific collagen-mimetic peptide substrata in flowing blood. Blood 2010, 115:5069-5079.
36. Caswell C.C., Barczyk M., Keene D.R., Lukomska E., Gullberg D.E., Lukomski S. Identification of the first prokaryotic collagen sequence motif that mediates binding to human collagen receptors, integrins alpha2beta1 and alpha11beta1. JBiol Chem 2008, 283:36168-36175.
37. Siljander P.R., Hamaia S., Peachey A.R., Slatter D.A., Smethurst P.A., Ouwehand W.H., et al. Integrin activation state determines selectivity for novel recognition sites in fibrillar collagens. JBiol Chem 2004, 279:47763-47772.
38. Shields M.A., Dangi-Garimella S., Krantz S.B., Bentrem D.J., Munshi H.G. Pancreatic cancer cells respond to type I collagen by inducing snail expression to promote membrane type 1 matrix metalloproteinase-dependent collagen invasion. JBiol Chem 2011, 286:10495-10504.
39. Shah A.N., Summy J.M., Zhang J., Park S.I., Parikh N.U., Gallick G.E. Development and characterization of gemcitabine-resistant pancreatic tumor cells. Ann Surg Oncol 2007, 14:3629-3637.
40. Banerjee S., Zhang Y., Ali S., Bhuiyan M., Wang Z., Chiao P.J., et al. Molecular evidence for increased antitumor activity of gemcitabine by genistein invitro and invivo using an orthotopic model of pancreatic cancer. Cancer Res 2005, 65:9064-9072.
41. Sagiv E., Kazanov D., Arber N. CD24 plays an important role in the carcinogenesis process of the pancreas. Biomed Pharmacother 2006, 60:280-284.
42. Fantozzi A., Gruber D.C., Pisarsky L., Heck C., Kunita A., Yilmaz M., et al. VEGF-mediated angiogenesis links EMT-induced cancer stemness to tumor initiation. Cancer Res 2014, 74:1566-1575.
43. Liu W., Xu J., Wang M., Wang Q., Bi Y., Han M. Tumor-derived vascular endothelial growth factor (VEGF)-a facilitates tumor metastasis through the VEGF-VEGFR1 signaling pathway. Int J Oncol 2011, 39:1213-1220.
44. Onishi H., Kai M., Odate S., Iwasaki H., Morifuji Y., Ogino T., et al. Hypoxia activates the hedgehog signaling pathway in a ligand-independent manner by upregulation of Smo transcription in pancreatic cancer. Cancer Sci 2011, 102:1144-1150.
45. Spivak-Kroizman T.R., Hostetter G., Posner R., Aziz M., Hu C., Demeure M.J., et al. Hypoxia triggers hedgehog-mediated tumor-stromal interactions in pancreatic cancer. Cancer Res 2013, 73:3235-3247.