Three-dimensional matrix stiffness and adhesive ligands affect cancer cell response to toxins

Biotechnology and Bioengineering

Volumn 113, Issue 2, 2016, Pages 443-452

  Zustiak, Silviya Petrova ^a   Dadhwal, Smritee ^b   Medina, Carlos ^b   Steczina, Sonette ^b   Chehreghanianzabi, Yasaman ^a   Ashraf, Anisa ^a   Asuri, Prashanth ^b  

^a Saint Louis University   (United States)

^b SANTA CLARA UNIVERSITY   (United States)

Author keywords

3D cell culture; Cancer drug screening; Cell matrix adhesions; Drug toxicity; Matrix stiffness

Indexed keywords

ADHESION; CELL CULTURE; CYTOLOGY; DIAGNOSIS; DISEASES; LIGANDS; METABOLITES; SCAFFOLDS (BIOLOGY); STIFFNESS; STIFFNESS MATRIX; TOXIC MATERIALS; TOXICITY;

3-D CELL CULTURE; ALGINATE-BASED SCAFFOLDS; BIOCHEMICAL PROPERTIES; CANCER DRUG; CELL MATRIX INTERACTIONS; CELL-MATRIX ADHESION; THREE DIMENSIONAL MATRICES; THREE-DIMENSIONAL (3D) CELL CULTURE;

CELLS;

ALGINIC ACID; ARGINYLGLYCYLASPARTIC ACID; BIOMATERIAL; CYTOTOXIC AGENT; INTEGRIN; LIGAND; TOXIN; ANTINEOPLASTIC AGENT; GLUCURONIC ACID; HEXURONIC ACID;

ARTICLE; BIOCHEMICAL ANALYSIS; CANCER CELL; CANCER RESISTANCE; CELL ADHESION; CELL FATE; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; RIGIDITY; TUMOR MICROENVIRONMENT; BIOLOGICAL MODEL; CELL CULTURE TECHNIQUE; GLIOBLASTOMA; PROCEDURES; TISSUE SCAFFOLD; TUMOR CELL LINE;

ALGINATES; ANTINEOPLASTIC AGENTS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; GLIOBLASTOMA; GLUCURONIC ACID; HEXURONIC ACIDS; HUMANS; MODELS, BIOLOGICAL; TISSUE SCAFFOLDS;

EID: 84965155668     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25709     Document Type: Article

References (60)

1. Ananthanarayanan B, Kim Y, Kumar S. 2011. Elucidating the mechanobiology of malignant brain tumors using a brain matrix-mimetic hyaluronic acid hydrogel platform. Biomaterials 32(31):7913-7923.
2. Aoudjit F, Vuori K. 2001. Integrin signaling inhibits paclitaxel-induced apoptosis in breast cancer cells. Oncogene 20(36):4995-5004.
3. Aoudjit F, Vuori K. 2012. Integrin signaling in cancer cell survival and chemoresistance. Chemothe Res Pract Article ID 283181.
4. Chen WLK, Simmons CA. 2011. Lessons from (patho) physiological tissue stiffness and their implications for drug screening, drug delivery and regenerative medicine. Adv Drug Deliv Rev 63(4):269-276.
5. Cordes N, Blaese MA, Plasswilm L, Rodemann HP, Van Beuningen D. 2003. Fibronectin and laminin increase resistance to ionizing radiation and the cytotoxic drug Ukrain in human tumour and normal cells in vitro. Int J Radiat Biol 79(9):709-720.
6. Desgrosellier JS, Cheresh DA. 2010. Integrins in cancer: Biological implications and therapeutic opportunities. Nature Reviews Cancer 10(1):9-22.
7. Discher DE, Janmey P, Wang Y-l. 2005. Tissue cells feel and respond to the stiffness of their substrate. Science 310(5751):1139-1143.
8. Dragunow M. 2008. High-content analysis in neuroscience. Nat Rev Neurosci 9(10):779-788.
9. Feurstein D, Stemmer K, Kleinteich J, Speicher T, Dietrich DR. 2011. Microcystin congener-and concentration-dependent induction of murine neuron apoptosis and neurite degeneration. Toxicol Sci 124(2):424-431.
10. Friedman MA, Dulak LH, Stedham MA. 1995. A lifetime oncogenicity study in rats with acrylamide. Toxicol Sci 27(1):95-105.
11. Giacomotto J, Ségalat L. 2010. High-throughput screening and small animal models, where are we?. Br J Pharmacol 160(2):204-216.
12. Godugu C, Patel AR, Desai U, Andey T, Sams A, Singh M. 2013. AlgiMatrix™ based 3D cell culture system as an in-vitro tumor model for anticancer studies. PLoS ONE 8(1):e53708.
13. Golmohamadi M, Wilkinson KJ. 2013. Diffusion of ions in a calcium alginate hydrogel-structure is the primary factor controlling diffusion. Carbohydr Polymers 94(1):82-87.
14. Griffin JW, Price DL, Drachman DB. 1977. Impaired axonal regeneration in acrylamide intoxication. J Neurobiol 8(4):355-370.
15. Griffith LG, Naughton G. 2002. Tissue engineering-current challenges and expanding opportunities. Science 295(5557):1009-1014.
16. Guelcher SA, Lee B-H., Guo R, Li B. 2012. Encapsulated cells and composites thereof. US 20120183622 A1.
17. Hayman E, Pierschbacher M, Ruoslahti E. 1985. Detachment of cells from culture substrate by soluble fibronectin peptides. J Cell Biol 100(6):1948-1954.
18. Hazlehurst LA, Landowski TH, Dalton WS. 2003. Role of the tumor microenvironment in mediating de novo resistance to drugs and physiological mediators of cell death. Oncogene 22(47):7396-7402.
19. Holland EC. 2000. Glioblastoma multiforme: the terminator. Pro Natl Acad Sci USA 97(12):6242-6244.
20. Hood JD, Cheresh DA. 2002. Role of integrins in cell invasion and migration. Nat Rev Cancer 2(2):91-100.
21. Huebsch N, Arany PR, Mao AS, Shvartsman D, Ali OA, Bencherif SA, Rivera-Feliciano J, Mooney DJ. 2010. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 9(6):518-526.
22. Janouskova H, Maglott A, Leger DY, Bossert C, Noulet F, Guerin E, Guenot D, Pinel S, Chastagner P, Plenat F. 2012. Integrin α5β1 plays a critical role in resistance to temozolomide by interfering with the p53 pathway in high-grade glioma. Cancer Res 72(14):3463-3470.
23. Jeon O, Alsberg E. 2013. Photofunctionalization of alginate hydrogels to promote adhesion and proliferation of human mesenchymal stem cells. Tissue Eng Part A 19(11-12):1424-1432.
24. Ju L, Zhou C, Li W, Yan L. 2010. Integrin beta1 over-expression associates with resistance to tyrosine kinase inhibitor gefitinib in non-small cell lung cancer. J Cell Biochem 111(6):1565-1574.
25. Kümper S, Marshall CJ. 2011. ROCK-driven actomyosin contractility induces tissue stiffness and tumor growth. Cancer Cell 19(6):695-697.
26. Lan S-F, Starly B. 2011. Alginate based 3D hydrogels as an in vitro co-culture model platform for the toxicity screening of new chemical entities. Toxicol Appl Pharmacol 256(1):62-72.
27. Lang P, Yeow K, Nichols A, Scheer A. 2006. Cellular imaging in drug discovery. Nat Rev Drug Discov 5(4):343-356.
28. Lee KY, Mooney DJ. 2012. Alginate: properties and biomedical applications. Prog Polymer Sci 37(1):106-126.
29. Lee M-Y, Kumar RA, Sukumaran SM, Hogg MG, Clark DS, Dordick JS. 2008. Three-dimensional cellular microarray for high-throughput toxicology assays. Proc Nat Acad Sci USA 105(1):59-63.
30. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SF, Csiszar K, Giaccia A, Weninger W. 2009. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139(5):891-906.
31. Lilienblum W, Dekant W, Foth H, Gebel T, Hengstler JG, Kahl R, Kramer PJ, Schweinfurth H, Wollin KM. 2008. Alternative methods to safety studies in experimental animals: Role in the risk assessment of chemicals under the new European Chemicals Legislation (REACH). Arch of Toxicol 82(4):211-236.
32. Loessner D, Stok KS, Lutolf MP, Hutmacher DW, Clements JA, Rizzi SC. 2010. Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells. Biomaterials 31(32):8494-8506.
33. Magde D, Elson EL, Webb WW. 1974. Fluorescence correlation spectroscopy. II. An experimental realization. Biopolymers 13(1):29-61.
34. Martinez-Rico C, Pincet F, Thiery J-P, Dufour S. 2010. Integrins stimulate E-cadherin-mediated intercellular adhesion by regulating Src-kinase activation and actomyosin contractility. J Cell Sci 123(5):712-722.
35. Mazzoleni G, Di Lorenzo D, Steimberg N. 2009. Modelling tissues in 3D: the next future of pharmaco-toxicology and food research? Genes Nutr 4(1):13-22.
36. McVaya K, Uthb N. 2014. Design of brain tumor phantoms replicating the elasticity of gliomas. Miami Eng Comp Rev 2(1).
37. Mih JD, Sharif AS, Liu F, Marinkovic A, Symer MM, Tschumperlin DJ. 2011. A multiwell platform for studying stiffness-dependent cell biology. PLoS ONE 6(5):e19929.
38. Oshita F, Kameda Y, Ikehara M, Tanaka G, Yamada K, Nomura I, Noda K, Shotsu A, Fujita A, Arai H, et al. 2002. Increased expression of integrin beta1 is a poor prognostic factor in small-cell lung cancer. Anticancer Res 22(2B):1065-1070.
39. Park HR, Kim M-S, Kim SJ, Park M, Kong KH, Kim HS, Kwack SJ, Kang TS, Kim SH, Kim HS. 2010. Acrylamide induces cell death in neural progenitor cells and impairs hippocampal neurogenesis. Toxicol Lett 193(1):86-93.
40. Pettikiriarachchi JT, Parish CL, Shoichet MS, Forsythe JS, Nisbet DR. 2010. Biomaterials for brain tissue engineering. Austr J Chem 63(8):1143-1154.
41. Polacheck WJ, Zervantonakis IK, Kamm RD. 2013. Tumor cell migration in complex microenvironments. Cell Mol Life Sci 70(8):1335-1356.
42. Prestwich GD. 2007. Evaluating drug efficacy and toxicology in three dimensions: using synthetic extracellular matrices in drug discovery. Acc Chem Res 41(1):139-148.
43. Ramamoorthi K, Hara J, Ito C, Asuri P. 2014. Role of three-dimensional matrix stiffness in regulating the response of human neural cells to toxins. Cell Mol Bioeng 7(2)):278-284.
44. Rowley JA, Madlambayan G, Mooney DJ. 1999. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 20(1):45-53.
45. Russo MA, Paolillo M, Sanchez-Hernandez Y, Curti D, Ciusani E, Serra M, Colombo L, Schinelli S. 2013. A small-molecule RGD-integrin antagonist inhibits cell adhesion, cell migration and induces anoikis in glioblastoma cells. Int J Oncol 42(1):83-92.
46. Schrader J, Gordon-Walker TT, Aucott RL, van Deemter M, Quaas A, Walsh S, Benten D, Forbes SJ, Wells RG, Iredale JP. 2011. Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 53(4):1192-1205.
47. Sethi T, Rintoul RC, Moore SM, MacKinnon AC, Salter D, Choo C, Chilvers ER, Dransfield I, Donnelly SC, Strieter R, et al. 1999. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat Med 5(6):662-668.
48. Starkuviene V, Pepperkok R. 2007. The potential of high-content high-throughput microscopy in drug discovery. Br J Pharmacol 152(1):62-71.
49. Syed S, Karadaghy A, Zustiak S. 2015. Simple polyacrylamide-based multiwell stiffness assay for the study of stiffness-dependent cell responses. J Visual Exp 97:e52643
50. Tanaka H, Matsumura M, Veliky I, . 1984. Diffusion characteristics of substrates in Ca-alginate gel beads. Biotechnol Bioeng 26(1):53-58.
51. Wang C, Tong X, Yang F. 2014. Bioengineered 3D brain tumor model to elucidate the effects of matrix stiffness on glioblastoma cell behavior using PEG-based hydrogels. Mol Pharm 11(7):2115-2125.
52. Weaver VM, Lelievre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, Werb Z, Bissell MJ. 2002. β4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2(3):205-216.
53. Wong K-L, Klaassen CD. 1982. Neurotoxic effects of cadmium in young rats. Toxicol Appl Pharmacol 63(3):330-337.
54. Zanders ED. 2011. The science and business of drug discovery. Springer, New York. p 93-95.
55. Zhang L, Yu J, Pan H, Hu P, Hao Y, Cai W, Zhu H, Albert DY, Xie X, Ma D. 2007. Small molecule regulators of autophagy identified by an image-based high-throughput screen. Proc Nat Acad Sci USA 104(48):19023-19028.
56. Zirino A, Yamamoto S. 1972. A pH-dependent model for the chemical speciation of copper, zinc, cadmium, and lead in seawater. Limnol Oceanography 17(5):661-671.
57. Zustiak S, Nossal R, Sackett DL. 2013. Multiwell stiffness assay for the study of cell responsiveness to cytotoxic drugs. Biotechnol Bioeng 111(2):396-403.
58. Zustiak SP. 2015. The Role of Matrix Compliance on Cell Responses to Drugs and Toxins: Towards Predictive Drug Screening Platforms. Macromol Biosci 15(5):589-599.
59. Zustiak SP, Boukari H, Leach JB. 2010. Solute diffusion and interactions in cross-linked poly (ethylene glycol) hydrogels studied by fluorescence correlation spectroscopy. Soft Matter 6(15):3609-3618.
60. Zustiak SP, Leach JB. 2010. Hydrolytically degradable poly(ethylene glycol) hydrogel scaffolds with tunable degradation and mechanical properties. Biomacromolecules 11(5):1348-1357.