Thermoresponsive platforms for tissue engineering and regenerative medicine

AIChE Journal

Volumn 57, Issue 12, 2011, Pages 3249-3258

  Tekin, Halil ^a,b,c   Sanchez, Jefferson G ^b,d   Tsinman, Tonia ^b,d   Langer, Robert ^c,d   Khademhosseini, Ali ^b,c,d,e  

^a USA   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d Massachusetts Institute of Technology Cambridge   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cell culture substrates; Thermoresponsive polymers; Tissue engineering

Indexed keywords

EID: 80355146828     PISSN: 00011541     EISSN: 15475905     Source Type: Journal    
DOI: 10.1002/aic.12801     Document Type: Article

References (73)

1. Khademhosseini A, Vacanti JP, Langer R. Progress in tissue engineering. Sci Am. 2009; 300(5): 64-71.
2. Griffith LG, Naughton G. Tissue engineering - Current challenges and expanding opportunities. Science. 2002; 295(5557): 1009-1014.
3. Nichol JW, Khademhosseini A. Modular tissue engineering: engineering biological tissues from the bottom up. Soft Matter. 2009 2009; 5(7): 1312-1319.
4. Du YA, Ghodousi M, Qi H, Haas N, Xiao WQ, Khademhosseini A. Sequential assembly of cell-laden hydrogel constructs to engineer vascular-like microchannels. Biotechnol Bioeng. 2011; 108(7): 1693-1703.
5. Ohashi K, Yokoyama T, Yamato M et al. Engineering functional two- and three-dimensional liver systems in vivo using hepatic tissue sheets. Nature Med. 2007; 13(7): 880-885.
6. Shimizu T, Yamato M, Isoi Y, Akutsu T, Setomaru T, Abe K, Kikuchi A, Umezu M, Okano T. Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circulation Res. 2002; 90(3): E40-E48.
7. Sekine H, Shimizu T, Yang J, Kobayashi E, Okano T. Pulsatile myocardial tubes fabricated with cell sheet engineering. Circulation. 2006; 114: I87-I93.
8. Franzesi GT, Ni B, Ling Y, Khademhosseini A. A controlled-release strategy for the generation of cross-linked hydrogel microstructures. J Am Chem Soc. 2006; 128(47): 15064-15065.
9. Motlagh D, Hartman TJ, Desai TA, Russell B. Microfabricated grooves recapitulate neonatal myocyte connexin43 and N-cadherin expression and localization. J Biomed Mater Res, Part A. 2003; 67A(1): 148-157.
10. Nakazawa K, Izumi Y, Fukuda J, Yasuda T. Hepatocyte spheroid culture on a polydimethylsiloxane chip having microcavities. J Biomater Sci Polym Ed. 2006; 17(8): 859-873.
11. Fukuda J, Khademhosseini A, Yeo Y, Yang X, Yeh J, Eng G, Blumling J, Wang CF, Kohane DS, Langer RX. Micromolding of photocrosslinkable chitosan hydrogel for spheroid microarray and co-cultures. Biomaterials. 2006; 27(30): 5259-5267.
12. Moeller H-C, Mian MK, Shrivastava S, Chung BG, Khademhosseini A. A microwell array system for stem cell culture. Biomaterials. 2008; 29(6): 752-763.
13. Tekin H, Tsinman T, Sanchez JG, Jones BJ, Camci-Unal G, Nichol JW, Langer R, Khademhosseini A. Responsive micromolds for sequential patterning of hydrogel microstructures. J Am Chem Soc. 2011; 133(33): 12944-12947.
14. Canavan HE, Cheng XH, Graham DJ, Ratner BD, Castner DG. Cell sheet detachment affects the extracellular matrix: A surface science study comparing thermal liftoff, enzymatic, and mechanical methods. J Biomed Mater Res, Part A. 2005; 75A(1): 1-13.
15. Yamada N, Okano T, Sakai H, Karikusa F, Sawasaki Y, Sakurai Y. Thermo-responsive polymeric surfaces; control of attachment and detachment of cultured cells. Makromol Chemie Rapid Commun. 1990; 11(11): 571-576.
16. Alarcon CDH, Pennadam S, Alexander C. Stimuli responsive polymers for biomedical applications. Chem Soc Rev. 2005; 34(3): 276-285.
17. Da Silva RMP, Mano JF, Reis RL. Smart thermoresponsive coatings and surfaces for tissue engineering: switching cell-material boundaries. Trends Biotechnol. 2007; 25(12): 577-583.
18. Peppas NA, Bures P, Leobandung W, Ichikawa H. Hydrogels in pharmaceutical formulations. Euro J Pharma Biopharma. 2000; 50(1): 27-46.
19. Eeckman F, Moes AJ, Amighi K. Synthesis and characterization of thermosensitive copolymers for oral controlled drug delivery. Euro Polym J. 2004; 40(4): 873-881.
20. Hirotsu S, Hirokawa Y, Tanaka T. Volume-phase transitions of ionized N-isopropylacrylamide gels. J Chem Phys. 1987; 87(2): 1392-1395.
21. Beltran S, Baker JP, Hooper HH, Blanch HW, Prausnitz JM. Swelling equilibria for weakly ionizable, temperature-sensitive hydrogels. Macromolecules. 1991; 24(2): 549-551.
22. Inoue T, Chen GH, Nakamae K, Hoffman AS. Temperature sensitivity of a hydrogel network containing different LCST oligomers grafted to the hydrogel backbone. Polym Gels Networks. 1997; 5(6): 561-575.
23. Allan SH. Applications of thermally reversible polymers and hydrogels in therapeutics and diagnostics. J Controlled Release. 1987; 6(1): 297-305.
24. Kaneko Y, Nakamura S, Sakai K, Aoyagi T, Kikuchi A, Sakurai Y, Okano T. Rapid deswelling response of poly(N-isopropylacrylamide) hydrogels by the formation of water release channels using poly(ethylene oxide) graft chains. Macromolecules. 1998; 31(18): 6099-6105.
25. Yoshida R, Uchida K, Kaneko Y, Sakai K, Kikuchi A, Sakurai Y, Okano T. Comb-type grafted hydrogels with rapid deswelling response to temperature changes. Nature. 1995; 374(6519): 240-242.
26. Kaneko Y, Nakamura S, Sakai K, Kikuchi A, Aoyagi T, Sakurai Y, Okano T. Deswelling mechanism for comb-type grafted poly(N-isopropylacrylamnide) hydrogels with rapid temperature responses. Polym Gels Networks. 1998; 6(5): 333-345.
27. Chen GH, Hoffman AS. Graft copolymers that exhibit temperature-induced phase-transitions over a wide-range of pH. Nature. 1995; 373(6509): 49-52.
28. Diez-Pena E, Quijada-Garrido I, Barrales-Rienda JM. On the water swelling behaviour of poly(N-isopropylacrylamide) P(N-iPAAm), poly(methacrylic acid) P(MAA), their random copolymers and sequential interpenetrating polymer networks (IPNs). Polymer. 2002; 43(16): 4341-4348.
29. Diez-Pena E, Quijada-Garrido I, Frutos P, Barrales-Rienda JM. Thermal properties of cross-linked poly(N-isopropylacrylamide) P(N-iPAAm), poly(methacrylic acid) P(MAA), their random copolymers P(N-iPAAm-co-MAA), and sequential interpenetrating polymer networks (IPNs). Macromolecules. 2002; 35(7): 2667-2675.
30. Bromberg L. Zein-poly(N-isopropylacrylamide) conjugates. J Phys Chem B. 23 1997; 101(4): 504-507.
31. Ju HK, Kim SY, Lee YM. pH/temperature-responsive behaviors of semi-IPN and comb-type graft hydrogels composed of alginate and poly(N-isopropylacrylamide). Polymer. 2001; 42(16): 6851-6857.
32. Dhara D, Rathna GVN, Chatterji PR. Volume phase transition in interpenetrating networks of poly(N-isopropylacrylamide) with gelatin. Langmuir. 2000; 16(6): 2424-2429.
33. Gil ES, Hudson SM. Stimuli-reponsive polymers and their bioconjugates. Progr Polym Sci. 2004; 29(12): 1173-1222.
34. Takezawa T, Mori Y, Yoshizato K. Cell-culture on a thermoresponsive polymer surface. Bio Technol. 1990; 8(9): 854-856.
35. Shimizu T, Yamato M, Kikuchi A, Okano T. Cell sheet engineering for myocardial tissue reconstruction. Biomaterials. 2003; 24(13): 2309-2316.
36. Harimoto M, Yamato M, Hirose M, Takahashi C, Isoi Y, Kikuchi A, Okano T. Novel approach for achieving double-layered cell sheets co-culture: overlaying endothelial cell sheets onto monolayer hepatocytes utilizing temperature-responsive culture dishes. J Biomed Mater Res. 2002; 62(3): 464-470.
37. Yamato M, Utsumi M, Kushida A, Konno C, Kikuchi A, Okano T. Thermo-responsive culture dishes allow the intact harvest of multilayered keratinocyte sheets without dispase by reducing temperature. Tissue Eng. 2001; 7(4): 473-480.
38. Kushida A, Yamato M, Kikuchi A, Okano T. Two-dimensional manipulation of differentiated Madin-Darby canine kidney (MDCK) cell sheets: The noninvasive harvest from temperature-responsive culture dishes and transfer to other surfaces. J Biomed Mater Res. 2001; 54(1): 37-46.
39. Nishida K, Yamato M, Hayashida Y, Watanabe K, Maeda N, Watanabe H, Yamamoto K, Nagai S, Kikuchi A, Tano Y, Okano T. Functional bioengineered corneal epithelial sheet grafts from corneal stem cells expanded ex vivo on a temperature-responsieve cell culture surface. Transplantation. 2004; 77(3): 379-385.
40. Ista LK, Mendez S, Perez-Luna VH, Lopez GP. Synthesis of poly(N-isopropylacrylamide) on initiator-modified self-assembled monolayers. Langmuir. 2001; 17(9): 2552-2555.
41. Akiyama Y, Kikuchi A, Yamato M, Okano T. Ultrathin poly(N-isopropylacrylamide) grafted layer on polystyrene surfaces for cell adhesion/detachment control. Langmuir. 2004; 20(13): 5506-5511.
42. Yamato M, Konno C, Koike S, Isoi Y, Shimizu T, Kikuchi A, Makino K, Okano T. Nanofabrication for micropatterned cell arrays by combining electron beam-irradiated polymer grafting and localized laser ablation. J Biomed Mater Res Part A. 2003; 67A(4): 1065-1071.
43. Canavan HE, Cheng XH, Graham DJ, Ratner BD, Castner DG. Surface characterization of the extracellular matrix remaining after cell detachment from a thermoresponsive polymer. Langmuir. 2005; 21(5): 1949-1955.
44. Cheng XH, Canavan HE, Stein MJ, Hull JR, Kweskin SJ, Wagner MS, Somorjai GA, Castner DG, Ratner BD. Surface chemical and mechanical properties of plasma-polymerized N-isopropylacrylamide. Langmuir. 2005; 21(17): 7833-7841.
45. von Recum HA, Kim SW, Kikuchi A, Okuhara M, Sakurai Y, Okano T. Novel thermally reversible hydrogel as detachable cell culture substrate. J Biomed Mater Res. 1998; 40(4): 631-639.
46. Chen GP, Imanishi Y, Ito Y. Effect of protein and cell behavior on pattern-grafted thermoresponsive polymer. J Biomed Mater Res. 1998; 42(1): 38-44.
47. Ito Y, Chen GP, Guan YQ, Imanishi Y. Patterned immobilization of thermoresponsive polymer. Langmuir. 1997; 13(10): 2756-2759.
48. Tamada Y, Ikada Y. Fibroblast growth on polymer surfaces and biosynthesis of collagen. J Biomed Mater Res. 1994; 28(7): 783-789.
49. Bullett NA, Talib RA, Short RD, McArthur SL, Shard AG. Chemical and thermo-responsive characterisation of surfaces formed by plasma polymerisation of N-isopropyl acrylamide. Surf Interface Anal. 2006; 38(7): 1109-1116.
50. Matsuda N, Shimizu T, Yamato M, Okano T. Tissue engineering based on cell sheet technology. Adv Mater. 2007; 19(20): 3089-3099.
51. Yamato M, Okuhara M, Karikusa F, Kikuchi A, Sakurai Y, Okano T. Signal transduction and cytoskeletal reorganization are required for cell detachment from cell culture surfaces grafted with a temperature-responsive polymer. J Biomed Mater Res. 1999; 44(1): 44-52.
52. Okano T, Yamada N, Okuhara M, Sakai H, Sakurai Y. Mechanism of cell detachment from temperature-modulated, hydrophilic-hydrophobic polymer surfaces. Biomaterials. 1995; 16(4): 297-303.
53. Kushida A, Yamato M, Konno C, Kikuchi A, Sakurai Y, Okano T. Decrease in culture temperature releases monolayer endothelial cell sheets together with deposited fibronectin matrix from temperature-responsive culture surfaces. J Biomed Mater Res. 1999; 45(4): 355-362.
54. Yamato M, Konno C, Utsumi M, Kikuchi A, Okano T. Thermally responsive polymer-grafted surfaces facilitate patterned cell seeding and co-culture. Biomaterials. 2002; 23(2): 561-567.
55. Yamato M, Kwon OH, Hirose M, Kikuchi A, Okano T. Novel patterned cell coculture utilizing thermally responsive grafted polymer surfaces. J Biomed Mater Res. 2001; 55(1): 137-140.
56. Tsuda Y, Kikuchi A, Yamato M, Nakao A, Sakurai Y, Umezu M, Okano T. The use of patterned dual thermoresponsive surfaces for the collective recovery as co-cultured cell sheets. Biomaterials. 2005; 26(14): 1885-1893.
57. Tsuda Y, Kikuchi A, Yamato M, Sakurai Y, Umezu M, Okano T. Control of cell adhesion and detachment using temperature and thermoresponsive copolymer grafted culture surfaces. J Biomed Mater Res Part A. 2004; 69A(1): 70-78.
58. Nishida K, Yamato M, Hayashida Y, Watanabe K, Yamamoto K, Adachi E, Nagai S, Kikuchi A, Maeda N, Watanabe H, Okano T, Tano Y. Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. NE J Med. 2004; 351(12): 1187-1196.
59. Sasagawa T, Shimizu T, Sekiya S, Haraguchi Y, Yamato M, Sawa Y, Okano T. Design of prevascularized three-dimensional cell-dense tissues using a cell sheet stacking manipulation technology. Biomaterials. 2010; 31(7): 1646-1654.
60. Shimizu T, Yamato M, Akutsu T, Shibata T, Isoi Y, Kikuchi A, Umezu M, Okano T. Electrically communicating three-dimensional cardiac tissue mimic fabricated by layered cultured cardiomyocyte sheets. J Biomed Mater Res. 2002; 60(1): 110-117.
61. Sekiya S, Shimizu T, Yamato M, Kikuchi A, Okano T. Bioengineered cardiac cell sheet grafts have intrinsic angiogenic potential. Biochem Biophys Res Commun. 2006; 341(2): 573-582.
62. Tanaka Y, Morishima K, Shimizu T, Kikuchi A, Yamato M, Okano T, Kitamori T. An actuated pump on-chip powered by cultured cardiomyocytes. Lab on a Chip. 2006; 6(3): 362-368.
63. Tanaka Y, Sato K, Shimizu T, Yamato M, Okano T, Kitamori T. A micro-spherical heart pump powered by cultured cardiomyocytes. Lab on a Chip. 2007; 7(2): 207-212.
64. Yokoyama T, Ohashi K, Kuge H, Kanehiro H, Iwata H, Yamato M, Nakajima Y. In vivo engineering of metabolically active hepatic tissues in a neovascularized subcutaneous cavity. Am J. Transplant. 2006; 6(1): 50-59.
65. Lee HM, Cusick RA, Utsunomiya H, Ma PX, Langer R, Vacanti JP. Effect of implantation site on hepatocytes heterotopically transplanted on biodegradable polymer scaffolds. Tissue Eng. 2003; 9(6): 1227-1232.
66. Tsuda Y, Kikuchi A, Yamato M, Chen GP, Okano T. Heterotypic cell interactions on a dually patterned surface. Biochem Biophys Res Commun. 2006; 348(3): 937-944.
67. Isenberg BC, Tsuda Y, Williams C, Shimizu T, Yamato M, Okano T, Wong JY. A thermoresponsive, microtextured substrate for cell sheet engineering with defined structural organization. Biomaterials. 2008; 29(17): 2565-2572.
68. Tsuda Y, Yamato M, Kikuchi A, Watanabe M, Chen G, Takahashi Y, Okano T. Thermoresponsive microtextured culture surfaces facilitate fabrication of capillary networks. Adv Mater. 2007; 19(21): 3633-3636.
69. Tekin H, Ozaydin-Ince G, Tsinman T, Gleason KK, Langer R, Khademhosseini A, Demirel MC. Responsive microgrooves for the formation of harvestable tissue constructs. Langmuir. 2011; 27(9): 5671-5679.
70. Co CC, Wang YC, Ho CC. Biocompatible micropatterning of two different cell types. J Am Chem Soc. 2005; 127(6): 1598-1599.
71. Khademhosseini A, Yeh J, Jon S, Eng G, Suh KY, Burdick JA, Langer R. Molded polyethylene glycol microstructures for capturing cells within microfluidic channels. Lab on a Chip. 2004; 4(5): 425-430.
72. Tekin H, Anaya M, Brigham MD, Nauman C, Langer R, Khademhosseini A. Stimuli-responsive microwells for formation and retrieval of cell aggregates. Lab on a Chip. 2010; 10(18): 2411-2418.
73. Sasaki J-I, Asoh T-A, Matsumoto T, Egusa H, Sohmura T, Alsberg E, Akashi M, Yatani H. Fabrication of three-dimensional cell constructs using temperature-responsive hydrogel. Tissue Eng Part A. 2010; 16(8): 2497-2504.