Chitosan-based thermoreversible hydrogel as an in Vitro tumor microenvironment for testing breast cancer therapies

Molecular Pharmaceutics

Volumn 11, Issue 7, 2014, Pages 2134-2142

  Tsao, Ching Ting ^a   Kievit, Forrest M ^b   Wang, Kui ^a   Erickson, Ariane E ^a   Ellenbogen, Richard G ^b   Zhang, Miqin ^a,b  

^a University of Washington   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

breast cancer; chitosan; hydrogel; malignancy; microenvironment

Indexed keywords

CHITOSAN; COLONY STIMULATING FACTOR 1; DOXORUBICIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GELATINASE B; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; INTERCELLULAR ADHESION MOLECULE 1; MACROGOL; MACROPHAGE INFLAMMATORY PROTEIN 2; MATRIGEL; PLATELET DERIVED GROWTH FACTOR AA; RANTES; STROMELYSIN; THROMBOCYTE FACTOR 4; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; HYDROGEL; MACROGOL DERIVATIVE; SIGNAL PEPTIDE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CELL GROWTH; CELL INTERACTION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; COST EFFECTIVENESS ANALYSIS; CYTOKINE RELEASE; DOSE RESPONSE; FEMALE; GOLD STANDARD; HYDROGEL; IMMUNITY; IN VITRO STUDY; LD 50; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE CULTURE; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; TUMOR MODEL; UPREGULATION; ADMINISTRATION AND DOSAGE; ANIMAL; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; TUMOR CELL LINE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CHITOSAN; CYTOKINES; DRUG RESISTANCE, NEOPLASM; FEMALE; HYDROGEL; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NEOVASCULARIZATION, PATHOLOGIC; POLYETHYLENE GLYCOLS; TUMOR MICROENVIRONMENT;

EID: 84903954051     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp5002119     Document Type: Article

References (70)

1. DeSantis, C.; Ma, J.; Bryan, L.; Jemal, A. Breast cancer statistics, 2013 Ca-Cancer J. Clin. 2013, 64, 52-62
2. Mouawad, R.; Spano, J. P.; Khayat, D. Lymphocyte Infiltration in Breast Cancer: A Key Prognostic Factor That Should Not Be Ignored J. Clin. Oncol. 2011, 29, 1935-1936
3. DeNardo, D. G.; Coussens, L. M. Inflammation and Breast Cancer. Balancing Immune Response: Crosstalk between Adaptive and Innate Immune Cells during Breast Cancer Progression Breast Cancer Res. 2007, 9, 212-221
4. Zhou, J.; Zhong, Y. Breast Cancer Immunotherapy Cell Mol. Immunol. 2004, 1, 247-255
5. Li, L.; Lu, Y. Optimizing a 3D Culture System to Study the Interaction between Epithelial Breast Cancer and Its Surrounding Fibroblasts J. Cancer 2011, 2, 458-466
6. Leung, M.; Kievit, F. M.; Florczyk, S. J.; Veiseh, O.; Wu, J.; Park, J. O.; Zhang, M. Chitosan-Alginate Scaffold Culture System for Hepatocellular Carcinoma Increases Malignancy and Drug Resistance Pharm. Res. 2010, 27, 1939-1948
7. Kim, J. B.; Stein, R.; OHare, M. J. Three-Dimensional in Vitro Tissue Culture Models of Breast Cancer-A Review Breast Cancer Res. Treat. 2004, 85, 281-291
8. Yamada, K. M.; Cukierman, E. Modeling Tissue Morphogenesis and Cancer in 3D Cell 2007, 130, 601-610
9. Kim, J. B.; OHare, M. J.; Stein, R. Models of Breast Cancer: Is Merging Human and Animal Models the Future? Breast Cancer Res. 2004, 6, 22-30
10. Kievit, F. M.; Florczyk, S. J.; Leung, M. C.; Veiseh, O.; Park, J. O.; Disis, M. L.; Zhang, M. Chitosan-Alginate 3D Scaffolds as a Mimic of the Glioma Tumor Microenvironment Biomaterials 2010, 31, 5903-5910
11. Florczyk, S. J.; Wang, K.; Jana, S.; Wood, D. L.; Sytsma, S. K.; Sham, J. G.; Kievit, F. M.; Zhang, M. Porous Chitosan-Hyaluronic Acid Scaffolds as a Mimic of Glioblastoma Microenvironment ECM Biomaterials 2013, 34, 10143-10150
12. Fischbach, C.; Chen, R.; Matsumoto, T.; Schmelzle, T.; Brugge, J. S.; Polverini, P. J.; Mooney, D. J. Engineering Tumors with 3D Scaffolds Nat. Methods 2007, 4, 855-860
13. Yang, Y.; Basu, S.; Tomasko, D. L.; Lee, L. J.; Yang, S. T. Fabrication of Well-Defined PLGA Scaffolds Using Novel Microembossing and Carbon Dioxide Bonding Biomaterials 2005, 26, 2585-2594
14. Lutolf, M. P.; Hubbell, J. A. Synthetic Biomaterials as Instructive Extracellular Microenvironments for Morphogenesis in Tissue Engineering Nat. Biotechnol. 2005, 23, 47-55
15. Tsao, C. T.; Chang, C. H.; Lin, Y. Y.; Wu, M. F.; Han, J. L.; Hsieh, K. H. Tissue Response to Chitosan/Gamma-PGA Polyelectrolyte Complex Using a Rat Model J. Bioact. Compat. Polym. 2011, 26, 191-206
16. Smalley, K. S.; Herlyn, M. Towards the Targeted Therapy of Melanoma Mini-Rev. Med. Chem. 2006, 6, 387-393
17. Bhattarai, N.; Ramay, H. R.; Gunn, J.; Matsen, F. A.; Zhang, M. PEG-Grafted Chitosan as an Injectable Thermosensitive Hydrogel for Sustained Protein Release J. Controlled Release 2005, 103, 609-624
18. Bhattarai, N.; Matsen, F. A.; Zhang, M. PEG-Grafted Chitosan as an Injectable Thermoreversible Hydrogel Macromol. Biosci. 2005, 5, 107-111
19. Chen, S. H.; Tsao, C. T.; Chang, C. H.; Lai, Y. T.; Wu, M. F.; Chuang, C. N.; Chou, H. C.; Wang, C. K.; Hsieh, K. H. Synthesis and Characterization of Reinforced Poly(ethylene glycol)/Chitosan Hydrogel as Wound Dressing Materials Macromol. Mater. Eng. 2013, 298, 429-438
20. Linhardt, R. J.; Toida, T. Role of Glycosaminoglycans in Cellular Communication Acc. Chem. Res. 2004, 37, 431-438
21. Chen, S. H.; Tsao, C. T.; Chang, C. H.; Lai, Y. T.; Wu, M. F.; Chuang, C. N.; Chou, H. C.; Wang, C. K.; Hsieh, K. H. Assessment of Reinforced Poly(ethylene glycol) Chitosan Hydrogels as Dressings in a Mouse Skin Wound Defect Model Mater. Sci. Eng., C 2013, 33, 2584-2594
22. Bhattarai, N.; Gunn, J.; Zhang, M. Chitosan-Based Hydrogels for Controlled, Localized Drug Delivery Adv. Drug Delivery Rev. 2010, 62, 83-99
23. K, K. Chitin and Chitosan: Functional Biopolymers from Marine Crustaceans Mar. Biotechnol. 2006, 8, 203-226
24. Lu, H.; Knutson, K. L.; Gad, E.; Disis, M. L. The Tumor Antigen Repertoire Identified in Tumor-Bearing Neu Transgenic Mice Predicts Human Tumor Antigens Cancer Res. 2006, 66, 9754-9761
25. Phan-Lai, V.; Florczyk, S. J.; Kievit, F. M.; Wang, K.; Gad, E.; Disis, M. L.; Zhang, M. Three-Dimensional Scaffolds to Evaluate Tumor Associated Fibroblast-Mediated Suppression of Breast Tumor Specific T Cells Biomacromolecules 2013, 14, 1330-1337
26. Phan-Lai, V.; Kievit, F. M.; Florczyk, S. J.; Wang, K.; Disis, M. L.; Zhang, M. CCL21 and IFNgamma Recruit and Activate Tumor Specific T Cells in 3D Scaffold Model of Breast Cancer Anti-Cancer Agents Med. Chem. 2013, 14, 204-210
27. Xu, F.; Burg, K. J. Three-Dimensional Polymeric Systems for Cancer Cell Studies Cytotechnology 2007, 54, 135-143
28. Waugh, D. J.; Wilson, C. The Interleukin-8 Pathway in Cancer Clin. Cancer Res. 2008, 14, 6735-6741
29. Lee, E.; Koskimaki, J. E.; Pandey, N. B.; Popel, A. S. Inhibition of Lymphangiogenesis and Angiogenesis in Breast Tumor Xenografts and Lymph Nodes by a Peptide Derived from Transmembrane Protein 45A Neoplasia 2013, 15, 112-124
30. Yoshiji, H.; Gomez, D. E.; Shibuya, M.; Thorgeirsson, U. P. Expression of Vascular Endothelial Growth Factor, Its Receptor, and Other Angiogenic Factors in Human Breast Cancer Cancer Res. 1996, 56, 2013-2016
31. Relf, M.; LeJeune, S.; Scott, P. A.; Fox, S.; Smith, K.; Leek, R.; Moghaddam, A.; Whitehouse, R.; Bicknell, R.; Harris, A. L. Expression of the Angiogenic Factors Vascular Endothelial Cell Growth Factor, Acidic and Basic Fibroblast Growth Factor, Tumor Growth Factor Beta-1, Platelet-Derived Endothelial Cell Growth Factor, Placenta Growth Factor, and Pleiotrophin in Human Primary Breast Cancer and Its Relation to Angiogenesis Cancer Res. 1997, 57, 963-969
32. Heinzman, J. M.; Brower, S. L.; Bush, J. E. Comparison of Angiogenesis-Related Factor Expression in Primary Tumor Cultures under Normal and Hypoxic Growth Conditions Cancer Cell Int. 2008, 8, 11-1-11-9
33. Balkwill, F.; Mantovani, A. Inflammation and Cancer: Back to Virchow? Lancet 2001, 357, 539-5345
34. Madsen, C. V.; Steffensen, K. D.; Olsen, D. A.; Waldstrom, M.; Sogaard, C. H.; Brandslund, I.; Jakobsen, A. Serum Platelet-Derived Growth Factor and Fibroblast Growth Factor in Patients with Benign and Malignant Ovarian Tumors Anticancer Res. 2012, 32, 3817-3825
35. Ongusaha, P. P.; Kwak, J. C.; Zwible, A. J.; Macip, S.; Higashiyama, S.; Taniguchi, N.; Fang, L.; Lee, S. W. HB-EGF is a Potent Inducer of Tumor Growth and Angiogenesis Cancer Res. 2004, 64, 5283-5290
36. Borgstrom, P.; Discipio, R.; Maione, T. E. Recombinant Platelet Factor 4, an Angiogenic Marker for Human Breast Carcinoma Anticancer Res. 1998, 18, 4035-4041
37. Cervi, D.; Yip, T. T.; Bhattacharya, N.; Podust, V. N.; Peterson, J.; Abou-Slaybi, A.; Naumov, G. N.; Bender, E.; Almog, N.; Italiano, J. E., Jr.; Folkman, J.; Klement, G. L. Platelet-Associated PF-4 as a Biomarker of Early Tumor Growth Blood 2008, 111, 1201-1207
38. Thorgeirsson, U. P.; Yoshiji, H.; Sinha, C. C.; Gomez, D. E. Breast Cancer; Tumor Neovasculature and the Effect of Tissue Inhibitor of Metalloproteinases-1 (TIMP-1) on Angiogenesis In Vivo 1996, 10, 137-144
39. Bendrik, C.; Dabrosin, C. MMP-3 and MMP-9 Gene Transfer Decrease Growth and Angiogenesis in Breast Cancer Xenografts in Vivo Cancer Res. 2009, 69, 4164
40. Bendrik, C.; Robertson, J.; Gauldie, J.; Dabrosin, C. Gene Transfer of Matrix Metalloproteinase-9 Induces Tumor Regression of Breast Cancer in Vivo Cancer Res. 2008, 68, 3405-3412
41. Nicolini, A.; Carpi, A.; Rossi, G. Cytokines in Breast Cancer Cytokine Growth Factor Rev. 2006, 17, 325-337
42. Rollins, B. J. Inflammatory Chemokines in Cancer Growth and Progression Eur. J. Cancer. 2006, 42, 760-767
43. Tanaka, T.; Bai, Z.; Srinoulprasert, Y.; Yang, B. G.; Hayasaka, H.; Miyasaka, M. Chemokines in Tumor Progression and Metastasis Cancer Sci. 2005, 96, 317-322
44. Yu, M.; Zhou, X.; Niu, L.; Lin, G.; Huang, J.; Zhou, W.; Gan, H.; Wang, J.; Jiang, X.; Yin, B.; Li, Z. Targeting Transmembrane TNF-alpha Suppresses Breast Cancer Growth Cancer Res. 2013, 73, 4061-4074
45. Mancino, A. T.; Klimberg, V. S.; Yamamoto, M.; Manolagas, S. C.; Abe, E. Breast Cancer Increases Osteoclastogenesis by Secreting M-CSF and Upregulating RANKL in Stromal Cells J. Surg. Res. 2001, 100, 18-24
46. Bernardini, G.; Spinetti, G.; Ribatti, D.; Camarda, G.; Morbidelli, L.; Ziche, M.; Santoni, A.; Capogrossi, M. C.; Napolitano, M. I-309 Binds to and Activates Endothelial Cell Functions and Acts as an Angiogenic Molecule in Vivo Blood 2000, 96, 4039-4045
47. Soria, G.; Ben-Baruch, A. The Inflammatory Chemokines CCL2 and CCL5 in Breast Cancer Cancer Lett. 2008, 267, 271-285
48. Rosette, C.; Roth, R. B.; Oeth, P.; Braun, A.; Kammerer, S.; Ekblom, J.; Denissenko, M. F. Role of ICAM1 in Invasion of Human Breast Cancer Cells Carcinogenesis 2005, 26, 943-950
49. Feliciano, P. CXCL1 and CXCL2 Link Metastasis and Chemoresistance Nat. Genet. 2012, 44, 840
50. Bronger, H.; Kraeft, S.; Schwarz-Boeger, U.; Cerny, C.; Stockel, A.; Avril, S.; Kiechle, M.; Schmitt, M. Modulation of CXCR3 Ligand Secretion by Prostaglandin E2 and Cyclooxygenase Inhibitors in Human Breast Cancer Breast Cancer Res. 2012, 14, R30-1-R30-14
51. Sagvolden, G.; Giaever, I.; Pettersen, E. O.; Feder, J. Cell Adhesion Force Microscopy Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 471-416
52. Dowling, D. P.; Miller, I. S.; Ardhaoui, M.; Gallagher, W. M. Effect of Surface Wettability and Topography on the Adhesion of Osteosarcoma Cells on Plasma-Modified Polystyrene J. Biomater. Appl. 2011, 26, 327-347
53. Horbett, T. A.; Waldburger, J. J.; Ratner, B. D.; Hoffman, A. S. Cell Adhesion to a Series of Hydrophilic-Hydrophobic Copolymers Studied with a Spinning Disc Apparatus J. Biomed. Mater. Res. 1988, 22, 383-404
54. Tredan, O.; Galmarini, C. M.; Patel, K.; Tannock, I. F. Drug Resistance and the Solid Tumor Microenvironment J. Natl. Cancer Inst. 2007, 99, 1441-1454
55. Discher, D. E.; Janmey, P.; Wang, Y. L. Tissue Cells Feel and Respond to the Stiffness of Their Substrate Science 2005, 310, 1139-1143
56. Zaman, M. H.; Trapani, L. M.; Sieminski, A. L.; Mackellar, D.; Gong, H.; Kamm, R. D.; Wells, A.; Lauffenburger, D. A.; Matsudaira, P. Migration of Tumor Cells in 3D Matrices Is Governed by Matrix Stiffness along with Cell-Matrix Adhesion and Proteolysis Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 10889-10894
57. Lu, P.; Weaver, V. M.; Werb, Z. The Extracellular Matrix: A Dynamic Niche in Cancer Progression J. Cell Biol. 2012, 196, 395-406
58. Levental, K. R.; Yu, H.; Kass, L.; Lakins, J. N.; Egeblad, M.; Erler, J. T.; Fong, S. F.; Csiszar, K.; Giaccia, A.; Weninger, W.; Yamauchi, M.; Gasser, D. L.; Weaver, V. M. Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling Cell 2009, 139, 891-906
59. Devi, C. U.; Bharat Chandran, R. S.; Vasu, R. M.; Sood, A. K. Measurement of Visco-Elastic Properties of Breast-Tissue Mimicking Materials Using Diffusing Wave Spectroscopy J. Biomed. Opt. 2007, 12, 034035
60. Sinkus, R.; Tanter, M.; Xydeas, T.; Catheline, S.; Bercoff, J.; Fink, M. Viscoelastic Shear Properties of in Vivo Breast Lesions Measured by MR Elastography Magn. Reson. Imaging 2005, 23, 159-165
61. Lii, J.; Hsu, W. J.; Parsa, H.; Das, A.; Rouse, R.; Sia, S. K. Real-Time Microfluidic System for Studying Mammalian Cells in 3D Microenvironments Anal. Chem. 2008, 80, 3640-3647
62. Wurtz, S. O.; Schrohl, A. S.; Sorensen, N. M.; Lademann, U.; Christensen, I. J.; Mouridsen, H.; Brunner, N. Tissue Inhibitor of Metalloproteinases-1 in Breast Cancer Endocr. Relat. Cancer 2005, 12, 215-227
63. Davies, G. F.; Berg, A.; Postnikoff, S. D.; Wilson, H. L.; Arnason, T. G.; Kusalik, A.; Harkness, T. A. TFPI1 Mediates Resistance to Doxorubicin in Breast Cancer Cells by Inducing a Hypoxic-Like Response PLoS One 2014, 9, e84611-1-e84611-16
64. Cohen, S.; Cohen, M. C. Mechanisms of Tumor Immunity. An Overview Am. J. Pathol. 1978, 93, 449-458
65. Drake, C. G.; Jaffee, E.; Pardoll, D. M. Mechanisms of Immune Evasion by Tumors Adv. Immunol. 2006, 90, 51-81
66. Rahir, G.; Moser, M. Tumor Microenvironment and Lymphocyte Infiltration Cancer Immunol. Immunother. 2012, 61, 751-759
67. Gajewski, T. F.; Schreiber, H.; Fu, Y. X. Innate and Adaptive Immune Cells in the Tumor Microenvironment Nat. Immunol. 2013, 14, 1014-1122
68. Hanks, B. A.; Holtzhausen, A.; Evans, K. S.; Jamieson, R.; Gimpel, P.; Campbell, O. M.; Hector-Greene, M.; Sun, L.; Tewari, A.; George, A.; Starr, M.; Nixon, A.; Augustine, C.; Beasley, G.; Tyler, D. S.; Osada, T.; Morse, M. A.; Ling, L.; Lyerly, H. K.; Blobe, G. C. Type III TGF-beta Receptor Downregulation Generates an Immunotolerant Tumor Microenvironment J. Clin. Invest. 2013, 123, 3925-3940
69. Walser, T. C.; Ma, X.; Kundu, N.; Dorsey, R.; Goloubeva, O.; Fulton, A. M. Immune-Mediated Modulation of Breast Cancer Growth and Metastasis by the Chemokine MIG (CXCL9) in a Murine Model J. Immunother. 2007, 30, 490-498
70. Florczyk, S. J.; Liu, G.; Kievit, F. M.; Lewis, A. M.; Wu, J. D.; Zhang, M. 3D Porous Chitosan-Alginate Scaffolds: A New Matrix for Studying Prostate Cancer Cell-Lymphocyte Interactions in Vitro Adv. Healthcare Mater. 2012, 1, 590-599