Transparent Porous Polysaccharide Cryogels Provide Biochemically Defined, Biomimetic Matrices for Tunable 3D Cell Culture

Chemistry of Materials

Volumn 28, Issue 11, 2016, Pages 3762-3770

  Tam, Roger Y ^a   Fisher, Stephanie A ^a,b   Baker, Alexander E G ^a,b   Shoichet, Molly S ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; BIOMIMETICS; GELATION; PORE SIZE; SCAFFOLDS (BIOLOGY); TRANSPARENCY;

BIOMIMETIC MATRICES; BIOMIMETIC SCAFFOLDS; CELLULAR RESPONSE; EXTRACELLULAR MATRICES; IMMOBILIZED LIGANDS; MONO- AND DISACCHARIDES; OPTICAL TRANSPARENCY; POLYSACCHARIDE HYDROGELS;

CELL CULTURE;

EID: 84975069841     PISSN: 08974756     EISSN: 15205002     Source Type: Journal    
DOI: 10.1021/acs.chemmater.6b00627     Document Type: Article

References (43)

1. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix elasticity directs stem cell lineage specification Cell 2006, 126, 677-689 10.1016/j.cell.2006.06.044
2. Wake, M. C.; Patrick, C. W., Jr.; Mikos, A. G. Pore morphology effects on the fibrovascular tissue growth in porous polymer substrates Cell Transplant. 1994, 3, 339-343
3. Loh, Q. L.; Choong, C. Three-dimensional scaffolds for tissue engineering applications: role of porosity and pore size Tissue Eng., Part B 2013, 19, 485-502 10.1089/ten.teb.2012.0437
4. Annabi, N.; Nichol, J. W.; Zhong, X.; Ji, C.; Koshy, S.; Khademhosseini, A.; Dehghani, F. Controlling the porosity and microarchitecture of hydrogels for tissue engineering Tissue Eng., Part B 2010, 16, 371-383 10.1089/ten.teb.2009.0639
5. Ricciardi, R.; Auriemma, F.; De Rosa, C. Structure and Properties of Poly(vinyl alcohol) Hydrogels Obtained by Freeze/Thaw Techniques Macromol. Symp. 2005, 222, 49-63 10.1002/masy.200550405
6. Bencherif, S. A.; Sands, R. W.; Bhatta, D.; Arany, P.; Verbeke, C. S.; Edwards, D. A.; Mooney, D. J. Injectable preformed scaffolds with shape-memory properties Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 19590-19595 10.1073/pnas.1211516109
7. Inci, I.; Kirsebom, H.; Galaev, I. Y.; Mattiasson, B.; Piskin, E. Gelatin cryogels crosslinked with oxidized dextran and containing freshly formed hydroxyapatite as potential bone tissue-engineering scaffolds J. Tissue Eng. Regener. Med. 2013, 7, 584-588 10.1002/term.1464
8. Appel, A. A.; Anastasio, M. A.; Larson, J. C.; Brey, E. M. Imaging challenges in biomaterials and tissue engineering Biomaterials 2013, 34, 6615-6630 10.1016/j.biomaterials.2013.05.033
9. Patachia, S.; Florea, C.; Friedrich, C.; Thomann, Y. Tailoring of poly(vinyl alcohol) cryogels properties by salts addition eXPRESS Polym. Lett. 2009, 3, 320-331 10.3144/expresspolymlett.2009.40
10. Cha, W.-I.; Hyon, S.-H.; Ikada, Y. Transparent poly(vinyl alcohol) hydrogel with high water content and high strength Makromol. Chem. 1992, 193, 1913-1925 10.1002/macp.1992.021930812
11. Zhao, S.; Shen, Z.; Wang, J.; Li, X.; Zeng, Y.; Wang, B.; He, Y.; Du, Y. Glycerol-mediated nanostructure modification leading to improved transparency of porous polymeric scaffolds for high performance 3D cell imaging Biomacromolecules 2014, 15, 2521-2531 10.1021/bm500388m
12. Dalton, P. D.; Hostert, C.; Albrecht, K.; Moeller, M.; Groll, J. Structure and properties of urea-crosslinked star poly[(ethylene oxide)-ran-(propylene oxide)] hydrogels Macromol. Biosci. 2008, 8, 923-931 10.1002/mabi.200800080
13. Reichelt, S.; Becher, J.; Weisser, J.; Prager, A.; Decker, U.; Möller, S.; Berg, A.; Schnabelrauch, M. Biocompatible polysaccharide-based cryogels Mater. Sci. Eng., C 2014, 35, 164-170 10.1016/j.msec.2013.10.034
14. Plieva, F. M.; Galaev, I. Y.; Mattiasson, B. Macroporous polysaccharide cryogels. In Macroporous Polymers; Mattiasson, B.; Kumar, A.; Galaev, I. Y., Eds.; CRC Press: New York, 2010; pp 140-153.
15. Toole, B. P. Hyaluronan: from extracellular glue to pericellular cue Nat. Rev. Cancer 2004, 4, 528-539 10.1038/nrc1391
16. Owen, S. C.; Fisher, S. A.; Tam, R. Y.; Nimmo, C. M.; Shoichet, M. S. Hyaluronic Acid Click Hydrogels Emulate the Extracellular Matrix Langmuir 2013, 29, 7393-7400 10.1021/la305000w
17. Nasatto, P. L.; Pignon, F.; Silveira, J. L. M.; Duarte, M. E. R.; Noseda, M. D.; Rinaudo, M. Methylcellulose, a Cellulose Derivative with Original Physical Properties and Extended Applications Polymers 2015, 7, 777-803 10.3390/polym7050777
18. Ke, M. T.; Fujimoto, S.; Imai, T. SeeDB: a simple and morphology-preserving optical clearing agent for neuronal circuit reconstruction Nat. Neurosci. 2013, 16, 1154-1161 10.1038/nn.3447
19. Tsai, P. S.; Kaufhold, J. P.; Blinder, P.; Friedman, B.; Drew, P. J.; Karten, H. J.; Lyden, P. D.; Kleinfeld, D. Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels J. Neurosci. 2009, 29, 14553-14570 10.1523/JNEUROSCI.3287-09.2009
20. Wei, G.; Ma, P. X. Partially nanofibrous architecture of 3D tissue engineering scaffolds Biomaterials 2009, 30, 6426-6434 10.1016/j.biomaterials.2009.08.012
21. Li, H.; Wijekoon, A.; Leipzig, N. D. 3D differentiation of neural stem cells in macroporous photopolymerizable hydrogel scaffolds PLoS One 2012, 7, e48824 10.1371/journal.pone.0048824
22. Tam, R. Y.; Ferreira, S. S.; Czechura, P.; Chaytor, J. L.; Ben, R. N. Hydration Index-A Better Parameter for Explaining Small Molecule Hydration in Inhibition of Ice Recrystallization J. Am. Chem. Soc. 2008, 130, 17494-17501 10.1021/ja806284x
23. Chaytor, J. L.; Tokarew, J. M.; Wu, L. K.; Leclere, M.; Tam, R. Y.; Capicciotti, C. J.; Guolla, L.; von Moos, E.; Findlay, C. S.; Allan, D. S.; Ben, R. N. Inhibiting ice recrystallization and optimization of cell viability after cryopreservation Glycobiology 2012, 22, 123-133 10.1093/glycob/cwr115
24. Newman, Y. M.; Ring, S. G.; Colaco, C. The role of trehalose and other carbohydrates in biopreservation Biotechnol. Genet. Eng. Rev. 1993, 11, 263-294 10.1080/02648725.1993.10647903
25. Petzold, G.; Aguilera, J. M. Ice Morphology: Fundamentals and Technological Applications in Foods Food Biophysics 2009, 4, 378-396 10.1007/s11483-009-9136-5
26. Wylie, R. G.; Ahsan, S.; Aizawa, Y.; Maxwell, K. L.; Morshead, C. M.; Shoichet, M. S. Spatially controlled simultaneous patterning of multiple growth factors in three-dimensional hydrogels Nat. Mater. 2011, 10, 799-806 10.1038/nmat3101
27. Vanier, G., Microwave-Assisted Peptide Synthesis (CEM). In Peptide Synthesis and Applications; Jensen, K. J.; Shelton, P. T.; Pedersen, S. L., Eds.; Humana Press: New York, 2013; pp 235-249.
28. Galema, S.; Hoiland, H. Stereochemical aspects of hydration of carbohydrates in aqueous solutions. 3. Density and ultrasound measurements J. Phys. Chem. 1991, 95, 5321-5326 10.1021/j100166a073
29. Bucior, I.; Burger, M. M. Carbohydrate-carbohydrate interaction as a major force initiating cell-cell recognition Glycoconjugate J. 2004, 21, 111-123 10.1023/B:GLYC.0000044843.72595.7d
30. Bucior, I.; Scheuring, S.; Engel, A.; Burger, M. M. Carbohydrate-carbohydrate interaction provides adhesion force and specificity for cellular recognition J. Cell Biol. 2004, 165, 529-537 10.1083/jcb.200309005
31. Wylie, R. G.; Shoichet, M. S. Three-Dimensional Spatial Patterning of Proteins in Hydrogels Biomacromolecules 2011, 12, 3789-3796 10.1021/bm201037j
32. Furuta, T.; Wang, S. S.; Dantzker, J. L.; Dore, T. M.; Bybee, W. J.; Callaway, E. M.; Denk, W.; Tsien, R. Y. Brominated 7-hydroxycoumarin-4-ylmethyls: photolabile protecting groups with biologically useful cross-sections for two photon photolysis Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 1193-1200 10.1073/pnas.96.4.1193
33. Galperin, A.; Oldinski, R. A.; Florczyk, S. J.; Bryers, J. D.; Zhang, M.; Ratner, B. D. Integrated bi-layered scaffold for osteochondral tissue engineering Adv. Healthcare Mater. 2013, 2, 872-883 10.1002/adhm.201200345
34. Whang, K.; Healy, K. E.; Elenz, D. R.; Nam, E. K.; Tsai, D. C.; Thomas, C. H.; Nuber, G. W.; Glorieux, F. H.; Travers, R.; Sprague, S. M. Engineering bone regeneration with bioabsorbable scaffolds with novel microarchitecture Tissue Eng. 1999, 5, 35-51 10.1089/ten.1999.5.35
35. Teng, W.; Long, T. J.; Zhang, Q.; Yao, K.; Shen, T. T.; Ratner, B. D. A tough, precision-porous hydrogel scaffold: ophthalmologic applications Biomaterials 2014, 35, 8916-8926 10.1016/j.biomaterials.2014.07.013
36. Fisher, S. A.; Anandakumaran, P. N.; Owen, S. C.; Shoichet, M. S. Tuning the Microenvironment: Click-Crosslinked Hyaluronic Acid-Based Hydrogels Provide a Platform for Studying Breast Cancer Cell Invasion Adv. Funct. Mater. 2015, 25, 7163-7172 10.1002/adfm.201502778
37. Lutolf, M. P.; Lauer-Fields, J. L.; Schmoekel, H. G.; Metters, A. T.; Weber, F. E.; Fields, G. B.; Hubbell, J. A. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 5413-5418 10.1073/pnas.0737381100
38. Raeber, G. P.; Lutolf, M. P.; Hubbell, J. A. Molecularly engineered PEG hydrogels: a novel model system for proteolytically mediated cell migration Biophys. J. 2005, 89, 1374-1388 10.1529/biophysj.104.050682
39. Mao, C.-F.; Chen, J.-C. Interchain association of locust bean gum in sucrose solutions: An interpretation based on thixotropic behavior Food Hydrocolloids 2006, 20, 730-739 10.1016/j.foodhyd.2005.07.002
40. Izutsu, K.; Yoshioka, S.; Kojima, S.; Randolph, T. W.; Carpenter, J. F. Effects of sugars and polymers on crystallization of poly(ethylene glycol) in frozen solutions: phase separation between incompatible polymers Pharm. Res. 1996, 13, 1393-1400 10.1023/A:1016086319851
41. Hirschhaeuser, F.; Menne, H.; Dittfeld, C.; West, J.; Mueller-Klieser, W.; Kunz-Schughart, L. A. Multicellular tumor spheroids: an underestimated tool is catching up again J. Biotechnol. 2010, 148, 3-15 10.1016/j.jbiotec.2010.01.012
42. Hongisto, V.; Jernstrom, S.; Fey, V.; Mpindi, J. P.; Kleivi Sahlberg, K.; Kallioniemi, O.; Perala, M. High-throughput 3D screening reveals differences in drug sensitivities between culture models of JIMT1 breast cancer cells PLoS One 2013, 8, e77232 10.1371/journal.pone.0077232
43. Lagadec, C.; Vlashi, E.; Della Donna, L.; Meng, Y.; Dekmezian, C.; Kim, K.; Pajonk, F. Survival and self-renewing capacity of breast cancer initiating cells during fractionated radiation treatment Breast Cancer Res. 2010, 12, R13 10.1186/bcr2479