Enzymatic conjugation of a bioactive peptide into an injectable hyaluronic acid-tyramine hydrogel system to promote the formation of functional vasculature

Acta Biomaterialia

Volumn 10, Issue 6, 2014, Pages 2539-2550

  Wang, Li Shan ^a   Lee, Fan ^a   Lim, Jaehong ^a   Du, Chan ^a   Wan, Andrew C A ^a   Lee, Su Seong ^a   Kurisawa, Motoichi ^a  

^a INSTITUTE OF BIOENGINEERING AND NANOTECHNOLOGY   (Singapore)

Author keywords

Functionalization; Hyaluronic acid; Hydrogel; RGD; Vascularization

Indexed keywords

AMINES; CELL ADHESION; CELL CULTURE; CELL ENGINEERING; CELL PROLIFERATION; CROSSLINKING; ENDOTHELIAL CELLS; ETHYLENE GLYCOL; HYALURONIC ACID; MOLECULES; ORGANIC ACIDS; PEPTIDES; PHENOLS; POLYETHYLENE GLYCOLS; POLYOLS; TISSUE; TISSUE ENGINEERING;

BIOACTIVE PEPTIDES; FUNCTIONALIZATIONS; HORSE-RADISH PEROXIDASE; HYDROGEL SYSTEM; INJECTABLES; MULTI-FUNCTIONAL; PHENOL MOIETY; RGD; VASCULARIZATION; VASCULATURE;

HYDROGELS;

ARGINYLGLYCYLASPARTIC ACID; HORSERADISH PEROXIDASE; HYALURONIC ACID; HYDROGEN PEROXIDE; MACROGOL; PEPTIDE; PHENOL; TYRAMINE; ENZYME; HYDROGEL;

ARTICLE; BIOLOGICAL ACTIVITY; CAPILLARY; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CONJUGATION; CONTROLLED STUDY; CROSS LINKING; FLOW KINETICS; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION; ANIMAL; BLOOD VESSEL; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; MOUSE;

ARMORACIA RUSTICANA;

ANIMALS; BLOOD VESSELS; ENZYMES; HYALURONIC ACID; HYDROGELS; MICE; PEPTIDES; TYRAMINE;

EID: 84899632719     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.02.022     Document Type: Article

References (42)

1. Alsberg E, Anderson KW, Albeiruti A, Rowley JA, Mooney DJ. Engineering growing tissues. Proc Natl Acad Sci USA 2002;99:12025-30.
2. Bidarra SJ, Barrias CC, Fonseca KB, Barbosa MA, Soares RA, Granja PL. Injectable in situ crosslinkable RGD-modified alginate matrix for endothelial cells delivery. Biomaterials 2011;32:7897-904.
3. Oliviero O, Ventre M, Netti PA. Functional porous hydrogels to study angiogenesis under the effect of controlled release of vascular endothelial growth factor. Acta Biomater 2012;8:3294-301.
4. Park YD, Tirelli N, Hubbell JA. Photopolymerized hyaluronic acid-based hydrogels and interpenetrating networks. Biomaterials 2003;24:893-900.
5. Kraehenbuehl TP, Zammaretti P, Van der Vlies AJ, Schoenmakers RG, Lutolf MP, Jaconi ME, et al. Three-dimensional extracellular matrix-directed cardioprogenitor differentiation: systematic modulation of a synthetic cellresponsive PEG-hydrogel. Biomaterials 2008;29:2757-66.
6. Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005;23:47-55.
7. Lutolf MP, Raeber GP, Zisch AH, Tirelli N, Hubbell JA. Cell-responsive synthetic hydrogels. Adv Mater 2003;15:888-91.
8. Park KM, Lee Y, Son JY, Bae JW, Park KD. In situ SVVYGLR peptide conjugation into injectable gelatin-poly(ethylene glycol)-tyramine hydrogel via enzymemediated reaction for enhancement of endothelial cell activity and neovascularization. Bioconjugate Chem 2012;23:2042-50.
9. Shu XZ, Ghosh K, Liu YC, Palumbo FS, Luo Y, Clark RA, et al. Attachment and spreading of fibroblasts on an RGD peptide-modified injectable hyaluronan hydrogel. J Biomed Mater Res A 2004;68A:365-75.
10. Schense JC, Bloch J, Aebischer P, Hubbell JA. Enzymatic incorporation of bioactive peptides into fibrin matrices enhances neurite extension. Nat Biotechnol 2000;18:415-9.
11. Bae KH, Wang L-S, Kurisawa M. Injectable biodegradable hydrogels: progress and challenges. J Mater Chem B 2013;1:5371-88.
12. Ibrahim S, Ramamurthi A. Hyaluronic acid cues for functional endothelialization of vascular constructs. J Tissue Eng Regen Med 2008;2:22-32.
13. Yee D, Hanjaya-Putra D, Bose V, Luong E, Gerecht S. Hyaluronic acid hydrogels support cord-like structures from endothelial colony-forming cells. Tissue Eng A 2011;17:1351-61.
14. Lei YG, Gojgini S, Lam J, Segura T. The spreading, migration and proliferation of mouse mesenchymal stem cells cultured inside hyaluronic acid hydrogels. Biomaterials 2011;32:39-47.
15. Seidlits SK, Drinnan CT, Petersen RR, Shear JB, Suggs LJ, Schmidt CE. Fibronectin-hyaluronic acid composite hydrogels for three-dimensional endothelial cell culture. Acta Biomater 2011;7:2401-9.
16. Suri S, Schmidt CE. Photopatterned collagen-hyaluronic acid interpenetrating polymer network hydrogels. Acta Biomater 2009;5:2385-97.
17. Lee F, Kurisawa M. Formation and stability of interpenetrating polymer network hydrogels consisting of fibrin and hyaluronic acid for tissue engineering. Acta Biomater 2013;9:5143-52.
18. Chen YC, Lin RZ, Qi H, Yang YZ, Bae HJ, Melero-Martin JM, et al. Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels. Adv Funct Mater 2012;22:2027-39.
19. Cuchiara MP, Gould DJ, McHale MK, Dickinson ME, West JL. Integration of selfassembled microvascular networks with microfabricated PEG-based hydrogels. Adv Funct Mater 2012;22:4511-8.
20. Lutolf MP, Hubbell JA. Synthesis and physicochemical characterization of endlinked poly(ethylene glycol)-co-peptide hydrogels formed by Michael-type addition. Biomacromolecules 2003;4:713-22.
21. Lutolf MP, Lauer-Fields JL, Schmoekel HG, Metters AT, Weber FE, Fields GB, et al. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci USA 2003;100:5413-8.
22. Allen P, Melero-Martin J, Type Bischoff J. Collagen, fibrin and PuraMatrix matrices provide permissive environments for human endothelial and mesenchymal progenitor cells to form neovascular networks. J Tissue Eng Regen Med 2011;5:E74-86.
23. Hao XJ, Silva EA, Mansson-Broberg A, Grinnemo KH, Siddiqui AJ, Dellgren G, et al. Angiogenic effects of sequential release of VEGF-A(165) and PDGF-BB with alginate hydrogels after myocardial infarction. Cardiovasc Res 2007;75:178-85.
24. Lee WY, Wei HJ, Wang JJ, Lin KJ, Lin WW, Chen DY, et al. Vascularization and restoration of heart function in rat myocardial infarction using transplantation of human cbMSC/HUVEC core-shell bodies. Biomaterials 2012;33:2127-36.
25. Leslie-Barbick JE, Saik JE, Gould DJ, Dickinson ME, West JL. The promotion of microvasculature formation in poly(ethylene glycol) diacrylate hydrogels by an immobilized VEGF-mimetic peptide. Biomaterials 2011;32:5782-9.
26. Moon JJ, West JL. Vascularization of engineered tissues: approaches to promote angiogenesis in biomaterials. Curr Top Med Chem 2008;8:300-10.
27. Phelps EA, Landazuri N, Thule PM, Taylor WR, Garcia AJ. Bioartificial matrices for therapeutic vascularization. Proc Natl Acad Sci USA 2010;107:3323-8.
28. Sukmana I, Vermette P. The effects of co-culture with fibroblasts and angiogenic growth factors on microvascular maturation and multi-cellular lumen formation in HUVEC-oriented polymer fibre constructs. Biomaterials 2010;31:5091-9.
29. Takayama T, Taguchi T, Koyama H, Sakari M, Kamimura W, Takato T, et al. The growth of a vascular network inside a collagen-citric acid derivative hydrogel in rats. Biomaterials 2009;30:3580-7.
30. Zorlutuna P, Annabi N, Camci-Unal G, Nikkhah M, Cha JM, Nichol JW, et al. Microfabricated biomaterials for engineering 3D tissues. Adv Mater 2012;24:1782-804.
31. Kurisawa M, Chung JE, Yang YY, Gao SJ, Uyama H. Injectable biodegradable hydrogels composed of hyaluronic acid-tyramine conjugates for drug delivery and tissue engineering. Chem Commun 2005:4312-4.
32. Lee F, Chung JE, Kurisawa M. An injectable enzymatically crosslinked hyaluronic acid-tyramine hydrogel system with independent tuning of mechanical strength and gelation rate. Soft Matter 2008;4:880-7.
33. Pek YS, Kurisawa M, Gao S, Chung JE, Ying JY. The development of a nanocrystalline apatite reinforced crosslinked hyaluronic acid-tyramine composite as an injectable bone cement. Biomaterials 2009;30:822-8.
34. Wang HB, Liu ZQ, Li DX, Guo X, Kasper FK, Duan CM, et al. Injectable biodegradable hydrogels for embryonic stem cell transplantation: improved cardiac remodelling and function of myocardial infarction. J Cell Mol Med 2012;16:1310-20.
35. Xu KM, Lee F, Gao SJ, Chung JE, Yano H, Kurisawa M. Injectable hyaluronic acid-tyramine hydrogels incorporating interferon-alpha 2a for liver cancer therapy. J Controlled Release 2013;166:203-10.
36. Jin R, Hiemstra C, Zhong ZY, Feijen J. Enzyme-mediated fast in situ formation of hydrogels from dextran-tyramine conjugates. Biomaterials 2007;28:2791-800.
37. Lee F, Chung JE, Kurisawa M. An injectable hyaluronic acid-tyramine hydrogel system for protein delivery. J Controlled Release 2009;134:186-93.
38. Kurisawa M, Lee F, Wang LS, Chung JE. Injectable enzymatically crosslinked hydrogel system with independent tuning of mechanical strength and gelation rate for drug delivery and tissue engineering. J Mater Chem 2010;20:5371-5.
39. Wang LS, Boulaire J, Chan PP, Chung JE, Kurisawa M. The role of stiffness of gelatin-hydroxyphenylpropionic acid hydrogels formed by enzyme-mediated crosslinking on the differentiation of human mesenchymal stem cell. Biomaterials 2010;33:8608-16.
40. Khademhosseini A, Suh KY, Yang JM, Eng G, Yeh J, Levenberg S, et al. Layer-bylayer deposition of hyaluronic acid and poly-L-lysine for patterned cell cocultures. Biomaterials 2004;25:3583-92.
41. Eckermann CW, Lehle K, Schmid SA, Wheatley DN, Kunz-Schughart LA. Characterization and modulation of fibroblast/endothelial cell co-cultures for the in vitro preformation of three-dimensional tubular networks. Cell Biol Int 2011;35:1097-110.
42. Ghajar CM, Chen X, Harris JW, Suresh V, Hughes CCW, Jeon NL, et al. The effect of matrix density on the regulation of 3-D capillary morphogenesis. Biophys J 2008;94:1930-41.