Interpenetrating networks based on gelatin methacrylamide and PEG formed using concurrent thiol click chemistries for hydrogel tissue engineering scaffolds

Biomaterials

Volumn 35, Issue 6, 2014, Pages 1845-1856

  Daniele, Michael A ^a   Adams, André A ^a   Naciri, Jawad ^a   North, Stella H ^a   Ligler, Frances S ^a  

^a NAVAL RESEARCH LABORATORY   (United States)

Author keywords

Click chemistry; Extracellular matrix; Gelatin; Interpenetrating network (IPN); Poly(ethylene glycol); Thiol yne

Indexed keywords

CLICK CHEMISTRY; EXTRACELLULAR MATRICES; GELATIN; INTERPENETRATING NETWORK (IPN); THIOL-YNE;

CELL ADHESION; ENDOTHELIAL CELLS; HYDROGELS; INTERPENETRATING POLYMER NETWORKS; PHYSICAL PROPERTIES; POLYETHYLENE GLYCOLS; TISSUE;

SCAFFOLDS (BIOLOGY);

BIOMATERIAL; BIOSYNTHETIC INTERPENETRATING NETWORK; GELATIN; GELATIN METHACRYLAMIDE; MACROGOL; THIOL; TISSUE SCAFFOLD; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL CULTURE; CELL ENCAPSULATION; CELL SURFACE; CELL SUSPENSION; CLICK CHEMISTRY; CONTROLLED STUDY; CROSS LINKING; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HYDRODYNAMICS; HYDROGEL; POLYMERIZATION; PRIORITY JOURNAL; SWELLING; SYNTHESIS; TISSUE ENGINEERING;

CLICK CHEMISTRY; EXTRACELLULAR MATRIX; GELATIN; INTERPENETRATING NETWORK (IPN); POLY(ETHYLENE GLYCOL); THIOL-YNE;

ACRYLAMIDES; CLICK CHEMISTRY; EXTRACELLULAR MATRIX; GELATIN; HYDROGEL; POLYETHYLENE GLYCOLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84890242253     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.11.009     Document Type: Article

References (57)

1. Geckil H., Xu F., Zhang X.H., Moon S., Demirci U. Engineering hydrogels as extracellular matrix mimics. Nanomedicine-UK 2010, 5:469-484.
2. Hu X., Cebe P., Weiss A.S., Omenetto F., Kaplan D.L. Protein-based composite materials. Mater Today 2012, 15:208-215.
3. Kim T.G., Shin H., Lim D.W. Biomimetic scaffolds for tissue engineering. Adv Funct Mater 2012, 22:2446-2468.
4. Fairbanks B.D., Schwartz M.P., Halevi A.E., Nuttelman C.R., Bowman C.N., Anseth K.S. Aversatile synthetic extracellular matrix mimic via thiol-norbornene photopolymerization. Adv Mater 2009, 21:5005-5010.
5. Hansen K.C., Kiemele L., Maller O., O'Brien J., Shankar A., Fornetti J., et al. An in-solution ultrasonication-assisted digestion method for improved extracellular matrix proteome coverage. Mol Cell Proteomics 2009, 8:1648-1657.
6. Oommen O.P., Wang S., Kisiel M., Sloff M., Hilborn J., Varghese O.P. Smart design of stable extracellular matrix mimetic hydrogel: synthesis, characterization, and invitro and invivo evaluation for tissue engineering. Adv Funct Mater 2013, 23:1273-1280.
7. Xu K.D., Fu Y., Chung W.J., Zheng X.X., Cui Y.J., Hsu I.C., et al. Thiol-ene-based biological/synthetic hybrid biomatrix for 3-D living cell culture. Acta Biomater 2012, 8:2504-2516.
8. Fu Y., Xu K.D., Zheng X.X., Giacomin A.J., Mix A.W., Kao W.Y.J. 3D cell entrapment in crosslinked thiolated gelatin-poly(ethylene glycol) diacrylate hydrogels. Biomaterials 2012, 33:48-58.
9. Burmania J.A., Stevens K.R., Kao W.Y.J. Cell interaction with protein-loaded interpenetrating networks containing modified gelatin and poly(ethylene glycol) diacrylate. Biomaterials 2003, 24:3921-3930.
10. Yang T., Malkoch M., Hult A. Sequential interpenetrating poly(ethylene glycol) hydrogels prepared by UV-initiated thiol-ene coupling chemistry. JPolym Sci Part A-Polymer Chem 2013, 51:363-371.
11. DeForest C.A., Polizzotti B.D., Anseth K.S. Sequential click reactions for synthesizing and patterning three-dimensional cell microenvironments. Nat Mater 2009, 8:659-664.
12. Hutson C.B., Nichol J.W., Aubin H., Bae H., Yamanlar S., Al-Haque S., et al. Synthesis and characterization of tunable poly(ethylene glycol): gelatin methacrylate composite hydrogels. Tissue Eng Pt A 2011, 17:1713-1723.
13. Tunca U. Triple click reaction strategy for macromolecular diversity. Macromol Rapid Commun 2013, 34:38-46.
14. Iha R.K., Wooley K.L., Nystrom A.M., Burke D.J., Kade M.J., Hawker C.J. Applications of orthogonal "click" chemistries in the synthesis of functional soft materials. Chem Rev 2009, 109:5620-5686.
15. Nimmo C.M., Shoichet M.S. Regenerative biomaterials that "click": simple, aqueous-based protocols for hydrogel synthesis, surface immobilization, and 3D patterning. Bioconjugate Chem 2011, 22:2199-2209.
16. Malkoch M., Vestberg R., Gupta N., Mespouille L., Dubois P., Mason A.F., et al. Synthesis of well-defined hydrogel networks using click chemistry. Chem Commun 2006, 2774-2776.
17. Anderson S.B., Lin C.C., Kuntzler D.V., Anseth K.S. The performance of human mesenchymal stem cells encapsulated in cell-degradable polymer-peptide hydrogels. Biomaterials 2011, 32:3564-3574.
18. Lin C.C., Raza A., Shih H. PEG hydrogels formed by thiol-ene photo-click chemistry and their effect on the formation and recovery of insulin-secreting cell spheroids. Biomaterials 2011, 32:9685-9695.
19. Toepke M.W., Impellitteri N.A., Theisen J.M., Murphy W.L. Characterization of thiol-ene crosslinked PEG hydrogels. Macromol Mater Eng 2012, 298:699-703.
20. Massi A., Nanni D. Thiol-yne coupling: revisiting old concepts as a breakthrough for up-to-date applications. Org Biomol Chem 2012, 10:3791-3807.
21. Van den Bulcke A.I., Bogdanov B., De Rooze N., Schacht E.H., Cornelissen M., Berghmans H. Structural and rheological properties of methacrylamide modified gelatin hydrogels. Biomacromolecules 2000, 1:31-38.
22. Habeeb A.F.S. Determination of free amino groups in proteins by trinitrobenzenesulfonic acid. Anal Biochem 1966, 14:328-335.
23. Brinkman W.T., Nagapudi K., Thomas B.S., Chaikof E.L. Photo-cross-linking of type I collagen gels in the presence of smooth muscle cells: mechanical properties, cell viability, and function. Biomacromolecules 2003, 4:890-895.
24. Dakin H.D. Amino-acids of gelatin. JBiol Chem 1920, 44:499-529.
25. Eastoe J.E. Amino acid composition of mammalian collagen and gelatin. Biochem J 1955, 61:589-600.
26. van Dijk M., van Nostrum C.F., Hennink W.E., Rijkers D.T.S., Liskamp R.M.J. Synthesis and characterization of enzymatically biodegradable PEG and peptide-based hydrogels prepared by click chemistry. Biomacromolecules 2010, 11:1608-1614.
27. Shin H., Olsen B.D., Khademhosseini A. The mechanical properties and cytotoxicity of cell-laden double-network hydrogels based on photocrosslinkable gelatin and gellan gum biomacromolecules. Biomaterials 2012, 33:3143-3152.
28. Chen Y.C., Lin R.Z., Qi H., Yang Y.Z., Bae H.J., Melero-Martin J.M., et al. Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels. Adv Funct Mater 2012, 22:2027-2039.
29. Shields A.R., Spillmann C.M., Naciri J., Howell P.B., Thangawng A.L., Ligler F.S. Hydrodynamically directed multiscale assembly of shaped polymer fibers. Soft Matter 2012, 8:6656-6660.
30. Boyd D.A., Shields A.R., Naciri J., Ligler F.S. Hydrodynamic shaping, polymerization and subsequent modification of thiol click fibers. Acs Appl Mater Inter 2013, 5:114-119.
31. Daniele M.A., North S.H., Naciri J., Howell P.B., Foulger S.H., Ligler F.S., et al. Rapid and continuous hydrodynamically controlled fabrication of biohybrid microfibers. Adv Funct Mater 2013, 23:698-704.
32. Brandl F., Sommer F., Goepferich A. Rational design of hydrogels for tissue engineering: impact of physical factors on cell behavior. Biomaterials 2007, 28:134-146.
33. Williams C.G., Malik A.N., Kim T.K., Manson P.N., Elisseeff J.H. Variable cytocompatibility of six cell lines with photoinitiators used for polymerizing hydrogels and cell encapsulation. Biomaterials 2005, 26:1211-1218.
34. Bryant S.J., Nuttelman C.R., Anseth K.S. Cytocompatibility of UV and visible light photoinitiating systems on cultured NIH/3T3 fibroblasts invitro. JBiomat Sci-Polym E 2000, 11:439-457.
35. Xiao W.Q., He J.K., Nichol J.W., Wang L.Y., Hutson C.B., Wang B., et al. Synthesis and characterization of photocrosslinkable gelatin and silk fibroin interpenetrating polymer network hydrogels. Acta Biomater 2011, 7:2384-2393.
36. Benton J.A., DeForest C.A., Vivekanandan V., Anseth K.S. Photocrosslinking of gelatin macromers to synthesize porous hydrogels that promote valvular interstitial cell function. Tissue Eng Pt A 2009, 15:3221-3230.
37. Nichol J.W., Koshy S.T., Bae H., Hwang C.M., Yamanlar S., Khademhosseini A. Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 2010, 31:5536-5544.
38. Peppas N.A., Hilt J.Z., Khademhosseini A., Langer R. Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv Mater 2006, 18:1345-1360.
39. Benmouna F., Bouabdellah-Dembahri Z., Benmouna M. Polymerization-induced phase separation: phase behavior developments and hydrodynamic interaction. JMacromol Sci B 2013, 52:998-1008.
40. Cuatrecasas P. Isolation of the insulin receptor of liver and fat-cell membranes. Proc Natl Acad Sci U S A 1972, 69:318-322.
41. Haire R.N., Tisel W.A., White J.G., Rosenberg A. On the precipitation of proteins by polymers: the hemoglobin-polyethylene glycol system. Biopolymers 1984, 23:2761-2779.
42. Morita T., Horikiri Y., Suzuki T., Yoshino H. Preparation of gelatin microparticles by co-lyophilization with poly(ethylene glycol): characterization and application to entrapment into biodegradable microspheres. Int J Pharm 2001, 219:127-137.
43. Hanjaya-Putra D., Wong K.T., Hirotsu K., Khetan S., Burdick J.A., Gerecht S. Spatial control of cell-mediated degradation to regulate vasculogenesis and angiogenesis in hyaluronan hydrogels. Biomaterials 2012, 33:6123-6131.
44. Khetan S., Burdick J.A. Patterning network structure to spatially control cellular remodeling and stem cell fate within 3-dimensional hydrogels. Biomaterials 2010, 31:8228-8234.
45. Ye S., Cramer N.B., Smith I.R., Voigt K.R., Bowman C.N. Reaction kinetics and reduced shrinkage stress of thiol-yne-methacrylate and thiol-yne-acrylate ternary systems. Macromolecules 2011, 44:9084-9090.
46. Flory P.J., Rehner J. Statistical mechanics of cross-linked polymer networks II: swelling. JChem Phys 1943, 11:521-526.
47. Flory P.J., Rehner J. Statistical mechanics of cross-linked polymer networks I: rubberlike elasticity. JChem Phys 1943, 11:512-520.
48. Obukhov S.P., Rubinstein M., Colby R.H. Network modulus and superelasticity. Macromolecules 1994, 27:3191-3198.
49. Huebsch N., Arany P.R., Mao A.S., Shvartsman D., Ali O.A., Bencherif S.A., et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 2010, 9:518-526.
50. Gilbert P.M., Havenstrite K.L., Magnusson K.E.G., Sacco A., Leonardi N.A., Kraft P., et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 2010, 329:1078-1081.
51. Bott K., Upton Z., Schrobback K., Ehrbar M., Hubbell J.A., Lutolf M.P., et al. The effect of matrix characteristics on fibroblast proliferation in 3D gels. Biomaterials 2010, 31:8454-8464.
52. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
53. Ramon-Azcon J., Ahadian S., Obregon R., Camci-Unal G., Ostrovidov S., Hosseini V., et al. Gelatin methacrylate as a promising hydrogel for 3D microscale organization and proliferation of dielectrophoretically patterned cells. Lab Chip 2012, 12:2959-2969.
54. Nikkhah M., Eshak N., Zorlutuna P., Annabi N., Castello M., Kim K., et al. Directed endothelial cell morphogenesis in micropatterned gelatin methacrylate hydrogels. Biomaterials 2012, 33:9009-9018.
55. Hu M., Kurisawa M., Deng R., Teo C.M., Schumacher A., Thong Y.X., et al. Cell immobilization in gelatin-hydroxyphenylpropionic acid hydrogel fibers. Biomaterials 2009, 30:3523-3531.
56. Hu M., Deng R.S., Schumacher K.M., Kurisawa M., Ye H.Y., Purnamawati K., et al. Hydrodynamic spinning of hydrogel fibers. Biomaterials 2010, 31:863-869.
57. Thangawng A.L., Howell P.B., Richards J.J., Erickson J.S., Ligler F.S. Asimple sheath-flow microfluidic device for micro/nanomanufacturing: fabrication of hydrodynamically shaped polymer fibers. Lab Chip 2009, 9:3126-3130.