Fully defined in situ cross-linkable alginate and hyaluronic acid hydrogels for myocardial tissue engineering

Biomaterials

Volumn 34, Issue 4, 2013, Pages 940-951

  Dahlmann, Julia ^a   Krause, Andreas ^b   Möller, Lena ^b   Kensah, George ^a   Möwes, Markus ^c   Diekmann, Astrid ^c   Martin, Ulrich ^a   Kirschning, Andreas ^b   Gruh, Ina ^a   Dräger, Gerald ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^c Elastomer Chemistry Deutsches Institut für Kautschuktechnologie E V DIK E V   (Germany)

Author keywords

Alginate; Cardiomyocytes; Hyaluronic acid; Hydrazones; Hydrogels; Myocardial tissue engineering

Indexed keywords

3D STRUCTURE; BIOARTIFICIAL; CARDIAC DIFFERENTIATION; CARDIAC TISSUES; CARDIOMYOCYTES; CLINICAL TRANSLATION; COLLAGEN I; CONTRACTION FORCE; CROSS-LINKABLE; DERIVATIZATIONS; HEART MUSCLES; HUMAN CELLS; HYALURONIC ACID HYDROGELS; HYALURONIC ACIDS; HYDRAZONES; HYDROGELATION; IN-VITRO; MATRIX COMPONENTS; MODULAR SYSTEM; MYOCARDIAL TISSUE; MYOCARDIAL TISSUE ENGINEERING; MYOCYTES; NEONATAL RAT; SITU CROSS-LINKING; THERAPEUTIC APPLICATION;

ALDEHYDES; ALGINATE; BIOMECHANICS; COLLAGEN; MECHANICAL PROPERTIES; ORGANIC ACIDS; TISSUE;

HYDROGELS;

ALGINIC ACID; COLLAGEN TYPE 1; HYALURONIC ACID; HYDRAZONE DERIVATIVE; POLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOARTIFICIAL LIVER; BIOCOMPATIBILITY; BIOMECHANICS; CELL VIABILITY; CONTROLLED STUDY; CROSS LINKING; FLOW KINETICS; HEART; HEART MUSCLE CELL; HUMAN; HUMAN TISSUE; HYDROGEL; IN VITRO STUDY; NONHUMAN; OXIDATION; POLYMERIZATION; PRIORITY JOURNAL; RAT; TISSUE ENGINEERING;

ALGINATES; ANIMALS; ANIMALS, NEWBORN; BIOCOMPATIBLE MATERIALS; CELLS, CULTURED; CROSS-LINKING REAGENTS; EQUIPMENT DESIGN; GLUCURONIC ACID; HEART; HEXURONIC ACIDS; HYALURONIC ACID; HYDROGELS; MATERIALS TESTING; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOCYTES, CARDIAC; RATS; RATS, SPRAGUE-DAWLEY; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

HYA; RATTUS;

EID: 84870373723     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.10.008     Document Type: Article

References (66)

1. Hench L.L., Thompson I. Twenty-first century challenges for biomaterials. J R Soc Interface 2010, 7:S379-S391.
2. Shin H., Jo S., Mikos A.G. Biomimetic materials for tissue engineering. Biomaterials 2003, 24:4353-4364.
3. Liu C., Xia Z., Czernuszka J.T. Design and development of three-dimensional scaffolds for tissue engineering. Chem Eng Res Des 2007, 85:1051-1064.
4. Kim B.-S., Park I.-K., Hoshiba T., Jiang H.-L., Choi Y.-J., Akaike T., et al. Design of artificial extracellular matrices for tissue engineering. Prog Polym Sci 2011, 36:238-268.
5. 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.
6. Soonpaa M.H., Field L.J. Assessment of cardiomyocyte DNA synthesis in normal and injured adult mouse hearts. Am J Phys 1997, 272:H220-H226.
7. Bergmann O., Bhardwaj R.D., Bernard S., Zdunek S., Barnabé-Heider F., Walsh S., et al. Evidence for cardiomyocyte renewal in humans. Science 2009, 324:98-102.
8. Li Z., Guan J. Hydrogels for cardiac tissue engineering. Polymers 2011, 3:740-761.
9. Slaughter B.V., Khurshid S.S., Fisher O.Z., Khademhosseini A., Peppas N.A. Hydrogels in regenerative medicine. Adv Mater 2009, 21:3307-3329.
10. Tibbitt M.W., Anseth K.S. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng 2009, 103:655-663.
11. Kim I.L., Mauck R.L., Burdick J.A. Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid. Biomaterials 2011, 32:8771-8782.
12. Bae M.S., Yang D.H., Lee J.B., Heo D.N., Kwon Y.-D., Youn I.C., et al. Photo-cured hyaluronic acid-based hydrogels containing simvastatin as a bone tissue regeneration scaffold. Biomaterials 2011, 32:8161-8171.
13. Filion T.M., Kutikov A., Song J. Chemically modified cellulose fibrous meshes for use as tissue engineering scaffolds. Bioorg Med Chem Lett 2011, 21:5067-5070.
14. Tseng H-J, Tsou T-L, Wang H-J, Hsu S-H. Characterization of chitosan-gelatin scaffolds for dermal tissue engineering. J Tissue Eng Regen Med, in press.
15. Leor J., Aboulafia-Etzion S., Dar A., Shapiro L., Barbash I.M., Battler A., et al. Bioengineered cardiac grafts: a new approach to repair the infarcted myocardium?. Circulation 2000, 102:III56-III61.
16. Sapir Y., Kryukov O., Cohen S. Integration of multiple cell-matrix interactions into alginate scaffolds for promoting cardiac tissue regeneration. Biomaterials 2011, 32:1838-1847.
17. Black L.D., Meyers J.D., Weinbaum J.S., Shvelidze Y.A., Tranquillo R.T. Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. Tissue Eng Part A 2009, 15:3099-3108.
18. Naito H., Melnychenko I., Didié M., Schneiderbanger K., Schubert P., Rosenkranz S., et al. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 2006, 114:I72-I78.
19. Fink C., Ergün S., Kralisch D., Remmers U., Weil J., Eschenhagen T. Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. Faseb J 2000, 14:669-679.
20. Zimmermann W.-H., Eschenhagen T. Cardiac tissue engineering for replacement therapy. Heart Fail Rev 2003, 8:259-269.
21. Tulloch N.L., Muskheli V., Razumova M.V., Korte F.S., Regnier M., Hauch K.D., et al. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res 2011, 109:47-59.
22. Eschenhagen T., Eder A., Vollert I., Hansen A. Physiological aspects of cardiac tissue engineering. Am J Physiol-Heart C 2012, 303:H133-H143.
23. Dvir T., Kedem A., Ruvinov E., Levy O., Freeman I., Landa N., et al. Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc Natl Acad Sci U S A 2009, 106:14990-14995.
24. Akhyari P., Kamiya H., Haverich A., Karck M., Lichtenberg A. Myocardial tissue engineering: the extracellular matrix. Euro J Cardio Thorac 2008, 34:229-241.
25. Mano J.F., Silva G.A., Azevedo H.S., Malafaya P.B., Sousa R.A., Silva S.S., et al. Natural origin biodegradable systems in tissue engineering and regenerative medicine: present status and some moving trends. J R Soc Interface 2007, 4:999-1030.
26. Hoyle C.E., Lowe A.B., Bowman C.N. Thiol-click chemistry: a multifaceted toolbox for small molecule and polymer synthesis. Chem Soc Rev 2010, 39:1355-1387.
27. Fu S., Ni P., Wang B., Chu B., Zheng L., Luo F., et al. Injectable and thermo-sensitive PEG-PCL-PEG copolymer/collagen/n-HA hydrogel composite for guided bone regeneration. Biomaterials 2012, 33:4801-4809.
28. van Dijk M., Rijkers D.T.S., Liskamp R.M.J., van Nostrum C.F., Hennink W.E. Synthesis and applications of biomedical and pharmaceutical polymers via click chemistry methodologies. Bioconjug Chem 2009, 20:2001-2016.
29. Möller L., Krause A., Dahlmann J., Gruh I., Kirschning A., Dräger G. Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering. Int J Artif Organs 2011, 34:93-102.
30. 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.
31. 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.
32. Bouhadir K.H., Hausman D.S., Mooney D.J. Synthesis of cross-linked poly(aldehyde guluronate) hydrogels. Polymer 1999, 40:3575-3584.
33. Gurski L.A., Jha A.K., Zhang C., Jia X., Farach-Carson M.C. Hyaluronic acid-based hydrogels as 3D matrices for in vitro evaluation of chemotherapeutic drugs using poorly adherent prostate cancer cells. Biomaterials 2009, 30:6076-6085.
34. Varghese O.P., Sun W., Hilborn J., Ossipov D.A. In situ cross-linkable high molecular weight hyaluronan-bisphosphonate conjugate for localized delivery and cell-specific targeting: a hydrogel linked prodrug approach. J Am Chem Soc 2009, 131:8781-8783.
35. Ossipov D.A., Yang X., Varghese O., Kootala S., Hilborn J. Modular approach to functional hyaluronic acid hydrogels using orthogonal chemical reactions. Chem Commun 2010, 46:8368-8370.
36. Gomez C.G., Rinaudo M., Villar M.A. Oxidation of sodium alginate and characterization of the oxidized derivatives. Carbohydr Polym 2007, 67:296-304.
37. Bouhadir K.H., Lee K.Y., Alsberg E., Damm K.L., Anderson K.W., Mooney D.J. Degradation of partially oxidized alginate and its potential application for tissue engineering. Biotechnol Prog 2001, 17:945-950.
38. Lee K.Y., Bouhadir K.H., Mooney D.J. Evaluation of chain stiffness of partially oxidized polyguluronate. Biomacromolecules 2002, 3:1129-1134.
39. Wollert K.C., Taga T., Saito M., Narazaki M., Kishimoto T., Glembotski C.C., et al. Cardiotrophin-1 activates a distinct form of cardiac muscle cell hypertrophy. Assembly of sarcomeric units in series VIA gp130/leukemia inhibitory factor receptor-dependent pathways. J Biol Chem 1996, 271:9535-9545.
40. Hattori F., Chen H., Yamashita H., Tohyama S., Satoh Y.-S., Yuasa S., et al. Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat Methods 2010, 7:61-66.
41. Kensah G., Gruh I., Viering J., Schumann H., Dahlmann J., Meyer H., et al. A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation. Tissue Eng Pt C-Meth 2011, 17:463-473.
42. DeForest C.A., Anseth K.S. Cytocompatible click-based hydrogels with dynamically tunable properties through orthogonal photoconjugation and photocleavage reactions. Nat Chem 2011, 3:925-931.
43. Hudson S.P., Langer R., Fink G.R., Kohane D.S. Injectable in situ cross-linking hydrogels for local antifungal therapy. Biomaterials 2010, 31:1444-1452.
44. Ossipov D.A., Piskounova S., Hilborn J. Poly(vinyl alcohol) cross-linkers for in vivo injectable hydrogels. Macromolecules 2008, 41:3971-3982.
45. Kurzer F., Douraghi-Zandeh K. Advances in the chemistry of carbodiimides. Chem Rev 1967, 67:107-152.
46. König W., Gieger R. Eine neue Methode zur Synthese von Peptiden: Aktivierung der Carboxylgruppe mit Dicyclohexylcarbodiirnid unter Zusatz von 1-Hydrox y-benzotriazolen. Chem Ber 1970, 103:788-798.
47. Bouhadir K.H., Alsberg E., Mooney D.J. Hydrogels for combination delivery of antineoplastic agents. Biomaterials 2001, 22:2625-2633.
48. Bulpitt P., Aeschlimann D. New strategy for chemical modification of hyaluronic acid: preparation of functionalized derivatives and their use in the formation of novel biocompatible hydrogels. J Biomed Mater Res 1999, 47:152-169.
49. Ossipov D.A., Piskounova S., Varghese O.P., Hilborn J. Functionalization of hyaluronic acid with chemoselective groups via a disulfide-based protection strategy for in situ formation of mechanically stable hydrogels. Biomacromolecules 2010, 11:2247-2254.
50. Boontheekul T., Kong H.-J., Mooney D.J. Controlling alginate gel degradation utilizing partial oxidation. Biomaterials 2005, 26:2455-2465.
51. Tan H., Chu C.R., Payne K.A., Marra K.G. Injectable in situ forming biodegradable chitosan-hyaluronic acid based hydrogels for cartilage tissue engineering. Biomaterials 2009, 30:2499-2506.
52. Kim J., Kim I.S., Cho T.H., Lee K.B., Hwang S.J., Tae G., et al. Bone regeneration using hyaluronic acid-based hydrogel with bonemorphogenic protein-2 and human mesenchymal stem cells. Biomaterials 2007, 28:1830-1837.
53. Kong J.H., Wong E., Mooney D.J. Independent control of rigidity and toughness of polymeric hydrogels. Macromolecules 2003, 36:4582-4588.
54. Crescenzi V., Cornelio L., Di Meo C., Nardecchia S., Lamanna R. Novel hydrogels via click chemistry: synthesis and potential biomedical applications. Biomacromolecules 2007, 8:1844-1850.
55. Hansen A., Eder A., Bönstrup M., Flato M., Mewe M., Schaaf S., et al. Development of a drug screening platform based on engineered heart tissue. Circ Res 2010, 107:35-44.
56. Schaaf S., Shibamiya A., Mewe M., Eder A., Stöhr A., Hirt M.N., et al. Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. PLoS One 2011, 6:e26397.
57. Liau B., Christoforou N., Leong K.W., Bursac N. Pluripotent stem cell-derived cardiac tissue patch with advanced structure and function. Biomaterials 2011, 32:9180-9187.
58. Huang Y.C., Khait L., Birla R.K. Contractile three-dimensional bioengineered heart muscle for myocardial regeneration. J Biomed Mater Res A 2007, 80:719-731.
59. Shachar M., Tsur-Gang O., Dvir T., Leor J., Cohen S. The effect of immobilized RGD peptide in alginate scaffolds on cardiac tissue engineering. Acta Biomater 2011, 7:152-162.
60. Chopra A., Lin V., McCollough A., Atzet S., Prestwich G.D., Wechsler A.S., et al. Reprogramming cardiomyocyte mechanosensing by crosstalk between integrins and hyaluronic acid receptors. J Biomech 2011, 45:824-831.
61. Zimmermann W.-H., Melnychenko I., Eschenhagen T. Engineered heart tissue for regeneration of diseased hearts. Biomaterials 2004, 25:1639-1647.
62. Gentleman E., Nauman E.A., Livesay G.A., Dee K.C. Collagen composite biomaterials resist contraction while allowing development of adipocytic soft tissue in vitro. Tissue Eng 2006, 12:1639-1649.
63. Bhana B., Iyer R.K., Chen W.L.K., Zhao R., Sider K.L., Likhitpanichkul M., et al. Influence of substrate stiffness on the phenotype of heart cells. Biotechnol Bioeng 2010, 105:1148-1160.
64. Slevin M., Krupinski J., Gaffney J., Matou S., West D., Delisser H., et al. Hyaluronan-mediated angiogenesis in vascular disease: uncovering RHAMM and CD44 receptor signaling pathways. Matrix Biol 2007, 26:58-68.
65. Camenisch T.D., Spicer A.P., Brehm-Gibson T., Biesterfeldt J., Augustine M.L., Calabro A., et al. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest 2000, 106:349-360.
66. Wong Y.Y., Handoko M.L., Mouchaers K.T.B., de Man F.S., Vonk-Noordegraaf A., van der Laarse W.J. Reduced mechanical efficiency of rat papillary muscle related to degree of hypertrophy of cardiomyocytes. Am J Physiol-Heart C 2010, 298:H1190-H1197.