Stiffness of photocrosslinked RGD-alginate gels regulates adipose progenitor cell behavior

Biotechnology and Bioengineering

Volumn 108, Issue 7, 2011, Pages 1683-1692

  Chandler, Emily M ^a   Berglund, Caroline M ^a   Lee, Jason S ^a   Polacheck, William J ^a   Gleghorn, Jason P ^a   Kirby, Brian J ^a   Fischbach, Claudia ^a  

^a School of Chemical and Molecular Engineering   (United States)

Author keywords

Adipose progenitor cells; Adipose tissue engineering; Alginate; Angiogenesis; Mechanical stiffness

Indexed keywords

3D CULTURE; ADIPOGENIC; ADIPOSE TISSUE; ADIPOSE TISSUE ENGINEERING; ANGIOGENESIS; ANGIOGENIC CAPACITY; BIOMATERIAL SCAFFOLDS; EXTRACELLULAR; EXTRACELLULAR MATRICES; MATRIX; MATRIX RIGIDITY; MECHANICAL STIFFNESS; PREADIPOCYTES; PROGENITOR CELL; SOFT TISSUE; TUMOR RESECTION; VASCULARIZATION;

ALGINATE; BIOMATERIALS; CELL CULTURE; ENZYME ACTIVITY; MECHANICS; STIFFNESS; STIFFNESS MATRIX; TISSUE;

SCAFFOLDS (BIOLOGY);

ALGINIC ACID; BIOMATERIAL;

ARTICLE; CANCER SURGERY; EXTRACELLULAR CALCIUM; EXTRACELLULAR MATRIX; HYDROGEL; PROADIPOCYTE; TISSUE ENGINEERING; TISSUE REGENERATION; VASCULARIZATION;

ADIPOSE TISSUE; ALGINATES; GLUCURONIC ACID; HEXURONIC ACIDS; HYDROGEL; LIGHT; STEM CELLS; TISSUE ENGINEERING;

EID: 79956068370     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.23079     Document Type: Article

References (51)

1. Baier Leach J, Bivens KA, Patrick CW, Jr, Schmidt CE. 2003. Photocrosslinked hyaluronic acid hydrogels: Natural, biodegradable tissue engineering scaffolds. Biotechnol Bioeng 82(5): 578-589.
2. Boontheekul T, Kong HJ, Hsiong SX, Huang YC, Mahadevan L, Vandenburgh H, Mooney DJ. 2008. Quantifying the relation between bond number and myoblast proliferation. Faraday Discuss 139: 53-70. discussion 105-128, 419-420.
3. Boynton AL, Whitfield JF, Isaacs RJ, Morton HJ. 1974. Control of 3T3 cell proliferation by calcium. In Vitro 10: 12-17.
4. Chou AI, Nicoll SB. 2009. Characterization of photocrosslinked alginate hydrogels for nucleus pulposus cell encapsulation. J Biomed Mater Res A 91(1): 187-194.
5. Corr DT, Gallant-Behm CL, Shrive NG, Hart DA. 2009. Biomechanical behavior of scar tissue and uninjured skin in a porcine model. Wound Repair Regen 17(2): 250-259.
6. Cukierman E, Pankov R, Stevens DR, Yamada KM. 2001. Taking cell-matrix adhesions to the third dimension. Science 294(5547): 1708-1712.
7. Discher DE, Janmey P, Wang YL. 2005. Tissue cells feel and respond to the stiffness of their substrate. Science 310(5751): 1139-1143.
8. Engler AJ, Sen S, Sweeney HL, Discher DE. 2006. Matrix elasticity directs stem cell lineage specification. Cell 126(4): 677-689.
9. Fischbach C, Spruss T, Weiser B, Neubauer M, Becker C, Hacker M, Gopferich A, Blunk T. 2004. Generation of mature fat pads in vitro and in vivo utilizing 3-D long-term culture of 3T3-L1 preadipocytes. Exp Cell Res 300(1): 54-64.
10. Gimble JM, Katz AJ, Bunnell BA. 2007. Adipose-derived stem cells for regenerative medicine. Circ Res 100(9): 1249-1260.
11. Gimeno RE, Klaman LD. 2005. Adipose tissue as an active endocrine organ: Recent advances. Curr Opin Pharmacol 5(2): 122-128.
12. Jensen B, Farach-Carson MC, Kenaley E, Akanbi KA. 2004. High extracellular calcium attenuates adipogenesis in 3T3-L1 preadipocytes. Exp Cell Res 301(2): 280-292.
13. Jeon O, Bouhadir KH, Mansour JM, Alsberg E. 2009. Photocrosslinked alginate hydrogels with tunable biodegradation rates and mechanical properties. Biomaterials 30(14): 2724-2734.
14. Jeon O, Powell C, Ahmed SM, Alsberg E. 2010. Biodegradable, photocrosslinked alginate hydrogels with independently tailorable physical properties and cell adhesivity. Tissue Eng Part A 16(9): 2915-2925.
15. Kang JH, Gimble JM, Kaplan DL. 2009. In vitro 3D model for human vascularized adipose tissue. Tissue Eng Part A 15(8): 2227-2236.
16. Karamichos D, Brown RA, Mudera V. 2007. Collagen stiffness regulates cellular contraction and matrix remodeling gene expression. J Biomed Mater Res Part A 83A(3): 887-894.
17. Kershaw EE, Flier JS. 2004. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89(6): 2548-2556.
18. Kong HJ, Liu J, Riddle K, Matsumoto T, Leach K, Mooney DJ. 2005. Non-viral gene delivery regulated by stiffness of cell adhesion substrates. Nat Mater 4(6): 460-464.
19. Lai N, Jayaraman A, Lee K. 2009. Enhanced proliferation of human umbilical vein endothelial cells and differentiation of 3T3-L1 adipocytes in coculture. Tissue Eng Part A 15(5): 1053-1061.
20. Lee KY, Alsberg E, Hsiong S, Comisar W, Linderman J, Ziff R, Mooney D. 2004. Nanoscale adhesion ligand organization regulates osteoblast proliferation and differentiation. Nano Lett 4(8): 1501-1506.
21. Li Q, Williams CG, Sun DD, Wang J, Leong K, Elisseeff JH. 2004. Photocrosslinkable polysaccharides based on chondroitin sulfate. J Biomed Mater Res A 68(1): 28-33.
22. Lin CC, Sawicki SM, Metters AT. 2008. Free-radical-mediated protein inactivation and recovery during protein photoencapsulation. Biomacromolecules 9(1): 75-83.
23. Mammoto A, Connor KM, Mammoto T, Yung CW, Huh D, Aderman CM, Mostoslavsky G, Smith LE, Ingber DE. 2009. A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457(7233): 1103-1108.
24. Mariman EC, Wang P. 2010. Adipocyte extracellular matrix composition, dynamics and role in obesity. Cell Mol Life Sci 67(8): 1277-1292.
25. Matthews BD, Overby DR, Mannix R, Ingber DE. 2006. Cellular adaptation to mechanical stress: Role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J Cell Sci 119(Pt 3): 508-518.
26. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. 2004. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6(4): 483-495.
27. Naumov GN, Akslen LA, Folkman J. 2006. Role of angiogenesis in human tumor dormancy: Animal models of the angiogenic switch. Cell Cycle 5(16): 1779-1787.
28. Niemisto A, Dunmire V, Yli-Harja O, Zhang W, Shmulevich I. 2005. Robust quantification of in vitro angiogenesis through image analysis. IEEE Trans Med Imaging 24(4): 549-553.
29. Ntambi JM, Young-Cheul K. 2000. Adipocyte differentiation and gene expression. J Nutr 130(12): 3122S-3126S.
30. Ono K, Saito Y, Yura H, Ishikawa K, Kurita A, Akaike T, Ishihara M. 2000. Photocrosslinkable chitosan as a biological adhesive. J Biomed Mater Res 49(2): 289-295.
31. Parker AM, Katz AJ. 2006. Adipose-derived stem cells for the regeneration of damaged tissues. Expert Opin Biol Ther 6(6): 567-578.
32. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3): 241-254.
33. Patrick CW, Jr. 2000. Adipose tissue engineering: The future of breast and soft tissue reconstruction following tumor resection. Semin Surg Oncol 19(3): 302-311.
34. Pirone DM, Liu WF, Ruiz SA, Gao L, Raghavan S, Lemmon CA, Romer LH, Chen CS. 2006. An inhibitory role for FAK in regulating proliferation: A link between limited adhesion and RhoA-ROCK signaling. J Cell Biol 174(2): 277-288.
35. Rouillard AD, Tsui Y, Polacheck WJ, Lee JY, Bonassar LJ, Kirby BJ. 2010. Control of the electromechanical properties of alginate hydrogels via ionic and covalent cross-linking and microparticle doping. Biomacromolecules 11(8): 2184-2189.
36. Rouillard AD, Berglund CM, Lee JY, Polacheck WJ, Tsui Y, Bonassar LJ, Kirby BJ. 2011. Methods for photocrosslinking alginate hydrogel scaffolds with high cell viability. Tissue Eng Part C Methods 17(2): 173-179.
37. Rowley JA, Madlambayan G, Mooney DJ. 1999. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 20(1): 45-53.
38. Rubina K, Kalinina N, Efimenko A, Lopatina T, Melikhova V, Tsokolaeva Z, Sysoeva V, Tkachuk V, Parfyonova Y. 2009. Adipose stromal cells stimulate angiogenesis via promoting progenitor cell differentiation, secretion of angiogenic factors, and enhancing vessel maturation. Tissue Eng Part A 15(8): 2039-2050.
39. Samani A, Bishop J, Luginbuhl C, Plewes DB. 2003. Measuring the elastic modulus of ex vivo small tissue samples. Phys Med Biol 48(14): 2183-2198.
40. Sawhney AS, Pathak CP, Hubbell JA. 1993. Bioerodible hydrogels based on photopolymerized poly(ethylene glycol)-co-poly(alpha-hydroxy acid) diacrylate macromers. Macromolecules 26(4): 581-587.
41. Seib FP, Prewitz M, Werner C, Bornhauser M. 2009. Matrix elasticity regulates the secretory profile of human bone marrow-derived multipotent mesenchymal stromal cells (MSCs). Biochem Biophys Res Commun 389(4): 663-667.
42. Smeds KA, Pfister-Serres A, Miki D, Dastgheib K, Inoue M, Hatchell DL, Grinstaff MW. 2001. Photocrosslinkable polysaccharides for in situ hydrogel formation. J Biomed Mater Res 54(1): 115-121.
43. Stacey DH, Hanson SE, Lahvis G, Gutowski KA, Masters KS. 2009. In vitro adipogenic differentiation of preadipocytes varies with differentiation stimulus, culture dimensionality, and scaffold composition. Tissue Eng Part A 15(11): 3389-3399.
44. Subramanian A, Lin HY. 2005. Crosslinked chitosan: Its physical properties and the effects of matrix stiffness on chondrocyte cell morphology and proliferation. J Biomed Mater Res A 75(3): 742-753.
45. Taraboletti G, Roberts D, Liotta LA, Giavazzi R. 1990. Platelet thrombospondin modulates endothelial cell adhesion, motility, and growth: A potential angiogenesis regulatory factor. J Cell Biol 111(2): 765-772.
46. Ulrich TA, de Juan Pardo EM, Kumar S. 2009. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res 69(10): 4167-4174.
47. Underhill GH, Chen AA, Albrecht DR, Bhatia SN. 2007. Assessment of hepatocellular function within PEG hydrogels. Biomaterials 28(2): 256-270.
48. Wang N, Butler JP, Ingber DE. 1993. Mechanotransduction across the cell surface and through the cytoskeleton. Science 260(5111): 1124-1127.
49. Winer JP, Janmey PA, McCormick ME, Funaki M. 2009. Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng Part A 15(1): 147-154.
50. Yoshida S, Ono M, Shono T, Izumi H, Ishibashi T, Suzuki H, Kuwano M. 1997. Involvement of interleukin-8, vascular endothelial growth factor, and basic fibroblast growth factor in tumor necrosis factor alpha-dependent angiogenesis. Mol Cell Biol 17(7): 4015-4023.
51. Zaman MH, Trapani LM, Sieminski AL, Mackellar D, Gong H, Kamm RD, Wells A, Lauffenburger DA, Matsudaira P. 2006. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci USA 103(29): 10889-10894.