Direct hydrogel encapsulation of pluripotent stem cells enables ontomimetic differentiation and growth of engineered human heart tissues

Biomaterials

Volumn 83, Issue , 2016, Pages 383-395

  Kerscher, Petra ^a   Turnbull, Irene C ^b   Hodge, Alexander J ^a   Kim, Joonyul ^c   Seliktar, Dror ^d   Easley, Christopher J ^c   Costa, Kevin D ^b   Lipke, Elizabeth A ^a  

^a AUBURN UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c AUBURN UNIVERSITY   (United States)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Developing heart tissue; Embryonic; Engineered cardiac tissue; Hydrogel; Maturation; Microenvironment; PEG fibrinogen; Pluripotent; Stem cell

Indexed keywords

BIOMIMETICS; CELLS; CYTOLOGY; DIAGNOSIS; DISEASES; GENE EXPRESSION; HEART; HISTOLOGY; HYDROGELS; POLYETHYLENE GLYCOLS; STEM CELLS;

CARDIAC TISSUES; DEVELOPING HEARTS; EMBRYONIC; MATURATION; MICROENVIRONMENTS; PLURIPOTENT;

TISSUE;

ARGINYLGLYCYLASPARTIC ACID; BIOMATERIAL; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; MACROGOL; SILICON DIOXIDE; HYDROGEL; MACROGOL DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INNATE IMMUNITY; MOUSE; NONHUMAN; POROSITY; PRIORITY JOURNAL; SURFACE PROPERTY; UPREGULATION; CARDIAC MUSCLE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; HEART; HUMAN; HYDROGEL; IMMOBILIZED CELL; PHARMACOLOGY; PLURIPOTENT STEM CELL; PROCEDURES; TISSUE ENGINEERING; ULTRASTRUCTURE;

CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, IMMOBILIZED; GENE EXPRESSION REGULATION; HEART; HUMANS; HYDROGEL; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS; POLYETHYLENE GLYCOLS; TISSUE ENGINEERING;

EID: 84958093310     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.12.011     Document Type: Article

References (64)

1. Lasser K.E., Allen P.D., Woolhandler S.J., Himmelstein D.U., Wolfe S.M., Bor D.H. Timing of new black box warnings and withdrawals for prescription medications. Jama 2002, 287:2215-2220.
2. Frank C., Himmelstein D.U., Woolhandler S., Bor D.H., Wolfe S.M., Heymann O., Zallman L., Lasser K.E. Era of faster FDA drug approval has also seen increased black-box warnings and market withdrawals. Health Aff. 2014, 33:1453-1459.
3. Yang X., Pabon L., Murry C.E. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ. Res. 2014, 114:511-523.
4. Bertassoni L.E., Cardoso J.C., Manoharan V., Cristino A.L., Bhise N.S., Araujo W.A., Zorlutuna P., Vrana N.E., Ghaemmaghami A.M., Dokmeci M.R., Khademhosseini A. Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels. Biofabrication 2014, 6:024105.
5. Zwi L., Caspi O., Arbel G., Huber I., Gepstein A., Park I.H., Gepstein L. Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation 2009, 120:1513-1523.
6. Kattman S.J., Witty A.D., Gagliardi M., Dubois N.C., Niapour M., Hotta A., Ellis J., Keller G. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 2011, 8:228-240.
7. Lev S., Kehat I., Gepstein L. Differentiation pathways in human embryonic stem cell-derived cardiomyocytes. Ann. N. Y. Acad. Sci. 2005, 1047:50-65.
8. Lian X., Zhang J., Azarin S.M., Zhu K., Hazeltine L.B., Bao X., Hsiao C., Kamp T.J., Palecek S.P. Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/beta-catenin signaling under fully defined conditions. Nat. Protoc. 2013, 8:162-175.
9. Burridge P.W., Matsa E., Shukla P., Lin Z.C., Churko J.M., Ebert A.D., Lan F., Diecke S., Huber B., Mordwinkin N.M., Plews J.R., Abilez O.J., Cui B., Gold J.D., Wu J.C. Chemically defined generation of human cardiomyocytes. Nat. Methods 2014, 11:855-860.
10. Nunes S.S., Miklas J.W., Liu J., Aschar-Sobbi R., Xiao Y., Zhang B., Jiang J., Masse S., Gagliardi M., Hsieh A., Thavandiran N., Laflamme M.A., Nanthakumar K., Gross G.J., Backx P.H., Keller G., Radisic M. Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat. Methods 2013, 10:781-787.
11. Turnbull I.C., Karakikes I., Serrao G.W., Backeris P., Lee J.J., Xie C., Senyei G., Gordon R.E., Li R.A., Akar F.G., Hajjar R.J., Hulot J.S., Costa K.D. Advancing functional engineered cardiac tissues toward a preclinical model of human myocardium. FASEB J. 2014, 28:644-654.
12. Zhang D., Shadrin I.Y., Lam J., Xian H.Q., Snodgrass H.R., Bursac N. Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 2013, 34:5813-5820.
13. Schaaf S., Shibamiya A., Mewe M., Eder A., Stohr A., Hirt M.N., Rau T., Zimmermann W.H., Conradi L., Eschenhagen T., Hansen A. Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. PLoS One 2011, 6:e26397.
14. Tulloch N.L., Muskheli V., Razumova M.V., Korte F.S., Regnier M., Hauch K.D., Pabon L., Reinecke H., Murry C.E. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ. Res. 2011, 109:47-59.
15. Mihic A., Li J., Miyagi Y., Gagliardi M., Li S.H., Zu J., Weisel R.D., Keller G., Li R.K. The effect of cyclic stretch on maturation and 3D tissue formation of human embryonic stem cell-derived cardiomyocytes. Biomaterials 2014, 35:2798-2808.
16. Shapira-Schweitzer K., Seliktar D. Matrix stiffness affects spontaneous contraction of cardiomyocytes cultured within a PEGylated fibrinogen biomaterial. Acta biomater. 2007, 3:33-41.
17. Mironi-Harpaz I., Wang D.Y., Venkatraman S., Seliktar D. Photopolymerization of cell-encapsulating hydrogels: crosslinking efficiency versus cytotoxicity. Acta Biomater. 2012, 8:1838-1848.
18. Dikovsky D., Bianco-Peled H., Seliktar D. The effect of structural alterations of PEG-fibrinogen hydrogel scaffolds on 3-cellular morphology and cellular migration. Biomaterials 2006, 27:1496-1506.
19. Franco C.L., Price J., West J.L. Development and optimization of a dual-photoinitiator, emulsion-based technique for rapid generation of cell-laden hydrogel microspheres. Acta Biomater. 2011, 7:3267-3276.
20. Lian X., Hsiao C., Wilson G., Zhu K., Hazeltine L.B., Azarin S.M., Raval K.K., Zhang J., Kamp T.J., Palecek S.P. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E1848-E1857.
21. Beers J., Gulbranson D.R., George N., Siniscalchi L.I., Jones J., Thomson J.A., Chen G. Passaging and colony expansion of human pluripotent stem cells by enzyme-free dissociation in chemically defined culture conditions. Nat. Protoc. 2012, 7:2029-2040.
22. Nie Y., Walsh P., Clarke D.L., Rowley J.A., Fellner T. Scalable passaging of adherent human pluripotent stem cells. PloS one 2014, 9:e88012.
23. Lowes B.D., Minobe W., Abraham W.T., Rizeq M.N., Bohlmeyer T.J., Quaife R.A., Roden R.L., Dutcher D.L., Robertson A.D., Voelkel N.F., Badesch D.B., Groves B.M., Gilbert E.M., Bristow M.R. Changes in gene expression in the intact human heart. Downregulation of alpha-myosin heavy chain in hypertrophied, failing ventricular myocardium. J. Clin. Investig. 1997, 100:2315-2324.
24. Itzhaki I., Rapoport S., Huber I., Mizrahi I., Zwi-Dantsis L., Arbel G., Schiller J., Gepstein L. Calcium handling in human induced pluripotent stem cell derived cardiomyocytes. PloS one 2011, 6:e18037.
25. Lou Q., Fedorov V.V., Glukhov A.V., Moazami N., Fast V.G., Efimov I.R. Transmural heterogeneity and remodeling of ventricular excitation-contraction coupling in human heart failure. Circulation 2011, 123:1881-1890.
26. Planat-Benard V., Menard C., Andre M., Puceat M., Perez A., Garcia-Verdugo J.M., Penicaud L., Casteilla L. Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ. Res. 2004, 94:223-229.
27. Matsuura K., Nagai T., Nishigaki N., Oyama T., Nishi J., Wada H., Sano M., Toko H., Akazawa H., Sato T., Nakaya H., Kasanuki H., Komuro I. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J. Biol. Chem. 2004, 279:11384-11391.
28. Zimmermann W.H., Schneiderbanger K., Schubert P., Didie M., Munzel F., Heubach J.F., Kostin S., Neuhuber W.L., Eschenhagen T. Tissue engineering of a differentiated cardiac muscle construct. Circ. Res. 2002, 90:223-230.
29. Fink C., Ergun S., Kralisch D., Remmers U., Weil J., Eschenhagen T. Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2000, 14:669-679.
30. Tiburcy M., Didie M., Boy O., Christalla P., Doker S., Naito H., Karikkineth B.C., El-Armouche A., Grimm M., Nose M., Eschenhagen T., Zieseniss A., Katschinksi D.M., Hamdani N., Linke W.A., Yin X., Mayr M., Zimmermann W.H. Terminal differentiation, advanced organotypic maturation, and modeling of hypertrophic growth in engineered heart tissue. Circ. Res. 2011, 109:1105-1114.
31. Radisic M., Park H., Shing H., Consi T., Schoen F.J., Langer R., Freed L.E., Vunjak-Novakovic G. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:18129-18134.
32. Hirt M.N., Boeddinghaus J., Mitchell A., Schaaf S., Bornchen C., Muller C., Schulz H., Hubner N., Stenzig J., Stoehr A., Neuber C., Eder A., Luther P.K., Hansen A., Eschenhagen T. Functional improvement and maturation of rat and human engineered heart tissue by chronic electrical stimulation. J. Mol. Cell. Cardiol. 2014, 74:151-161.
33. Bird S.D., Doevendans P.A., van Rooijen M.A., Brutel de la Riviere A., Hassink R.J., Passier R., Mummery C.L. The human adult cardiomyocyte phenotype. Cardiovasc. Res. 2003, 58:423-434.
34. Gerdes A.M., Kellerman S.E., Moore J.A., Muffly K.E., Clark L.C., Reaves P.Y., Malec K.B., McKeown P.P., Schocken D.D. Structural remodeling of cardiac myocytes in patients with ischemic cardiomyopathy. Circulation 1992, 86:426-430.
35. Ziman A.P., Ward C.W., Rodney G.G., Lederer W.J., Bloch R.J. Quantitative measurement of Ca(2)(+) in the sarcoplasmic reticulum lumen of mammalian skeletal muscle. Biophys. J. 2010, 99:2705-2714.
36. Knollmann B.C. Induced pluripotent stem cell-derived cardiomyocytes: boutique science or valuable arrhythmia model?. Circ. Res. 2013, 112:969-976. discussion 976.
37. Robertson C., Tran D.D., George S.C. Concise review: maturation phases of human pluripotent stem cell-derived cardiomyocytes. Stem Cells 2013, 31:829-837.
38. Priori S.G., Napolitano C., Di Pasquale E., Condorelli G. Induced pluripotent stem cell-derived cardiomyocytes in studies of inherited arrhythmias. J. Clin. Investig. 2013, 123:84-91.
39. Lundy S.D., Zhu W.Z., Regnier M., Laflamme M.A. Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev. 2013, 22:1991-2002.
40. Murphy S.V., Atala A. 3D bioprinting of tissues and organs. Nat. Biotechnol. 2014, 32:773-785.
41. Stanton M.M., Samitier J., Sanchez S. Bioprinting of 3D hydrogels. Lab. Chip 2015, 15:3111-3115.
42. Workman V.L., Dunnett S.B., Kille P., Palmer D.D. Microfluidic chip-based synthesis of alginate microspheres for encapsulation of immortalized human cells. Biomicrofluidics 2007, 1:14105.
43. Chung B.G., Lee K.H., Khademhosseini A., Lee S.H. Microfluidic fabrication of microengineered hydrogels and their application in tissue engineering. Lab. Chip 2012, 12:45-59.
44. Shapira-Schweitzer K., Habib M., Gepstein L., Seliktar D. A photopolymerizable hydrogel for 3-culture of human embryonic stem cell-derived cardiomyocytes and rat neonatal cardiac cells. J. Mol. Cell. Cardiol. 2009, 46:213-224.
45. Bearzi C., Gargioli C., Baci D., Fortunato O., Shapira-Schweitzer K., Kossover O., Latronico M.V., Seliktar D., Condorelli G., Rizzi R. PlGF-MMP9-engineered iPS cells supported on a PEG-fibrinogen hydrogel scaffold possess an enhanced capacity to repair damaged myocardium. Cell Death Dis. 2014, 5:e1053.
46. Lei Y., Schaffer D.V. A fully defined and scalable 3D culture system for human pluripotent stem cell expansion and differentiation. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E5039-E5048.
47. Amit M., Laevsky I., Miropolsky Y., Shariki K., Peri M., Itskovitz-Eldor J. Dynamic suspension culture for scalable expansion of undifferentiated human pluripotent stem cells. Nat. Protoc. 2011, 6:572-579.
48. Zweigerdt R., Olmer R., Singh H., Haverich A., Martin U. Scalable expansion of human pluripotent stem cells in suspension culture. Nat. Protoc. 2011, 6:689-700.
49. Weng Z., Kong C.W., Ren L., Karakikes I., Geng L., He J., Chow M.Z., Mok C.F., Keung W., Chow H., Leung A.Y., Hajjar R.J., Li R.A., Chan C.W. A simple, cost-effective but highly efficient system for deriving ventricular cardiomyocytes from human pluripotent stem cells. Stem Cells Dev. 2014, 23:1704-1716.
50. Arduini D. Fetal Cardiac Function 1995, 43-49.
51. Li F., Wang X., Capasso J.M., Gerdes A.M. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J. Mol. Cell. Cardiol. 1996, 28:1737-1746.
52. Laflamme M.A., Murry C.E. Heart regeneration. Nature 2011, 473:326-335.
53. Mollova M., Bersell K., Walsh S., Savla J., Das L.T., Park S.Y., Silberstein L.E., Dos Remedios C.G., Graham D., Colan S., Kuhn B. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:1446-1451.
54. Bensley J.G., Stacy V.K., De Matteo R., Harding R., Black M.J. Cardiac remodelling as a result of pre-term birth: implications for future cardiovascular disease. Eur. Heart J. 2010, 31:2058-2066.
55. Mann B.K., West J.L. Cell adhesion peptides alter smooth muscle cell adhesion, proliferation, migration, and matrix protein synthesis on modified surfaces and in polymer scaffolds. J. Biomed. Mater. Res. 2002, 60:86-93.
56. Liang P., Lan F., Lee A.S., Gong T., Sanchez-Freire V., Wang Y., Diecke S., Sallam K., Knowles J.W., Wang P.J., Nguyen P.K., Bers D.M., Robbins R.C., Wu J.C. Drug screening using a library of human induced pluripotent stem cell-derived cardiomyocytes reveals disease-specific patterns of cardiotoxicity. Circulation 2013, 127:1677-1691.
57. Doyle M.J., Lohr J.L., Chapman C.S., Koyano-Nakagawa N., Garry M.G., Garry D.J. Human induced pluripotent stem cell-derived cardiomyocytes as a model for heart development and congenital heart disease. Stem Cell Rev. 2015, 11:710-727.
58. Yazawa M., Hsueh B., Jia X., Pasca A.M., Bernstein J.A., Hallmayer J., Dolmetsch R.E. Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome. Nature 2011, 471:230-234.
59. Chong J.J., Yang X., Don C.W., Minami E., Liu Y.W., Weyers J.J., Mahoney W.M., Van Biber B., Cook S.M., Palpant N.J., Gantz J.A., Fugate J.A., Muskheli V., Gough G.M., Vogel K.W., Astley C.A., Hotchkiss C.E., Baldessari A., Pabon L., Reinecke H., Gill E.A., Nelson V., Kiem H.P., Laflamme M.A., Murry C.E. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 2014, 510:273-277.
60. Dunn D.A., Hodge A.J., Lipke E.A. Biomimetic materials design for cardiac tissue regeneration. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2014, 6:15-39.
61. Lieu D.K., Liu J., Siu C.W., McNerney G.P., Tse H.F., Abu-Khalil A., Huser T., Li R.A. Absence of transverse tubules contributes to non-uniform Ca(2+) wavefronts in mouse and human embryonic stem cell-derived cardiomyocytes. Stem Cells Dev. 2009, 18:1493-1500.
62. Wei S., Guo A., Chen B., Kutschke W., Xie Y.P., Zimmerman K., Weiss R.M., Anderson M.E., Cheng H., Song L.S. T-tubule remodeling during transition from hypertrophy to heart failure. Circ. Res. 2010, 107:520-531.
63. Baharvand H., Azarnia M., Parivar K., Ashtiani S.K. The effect of extracellular matrix on embryonic stem cell-derived cardiomyocytes. J. Mol. Cell. Cardiol. 2005, 38:495-503.
64. Stevens K.R., Pabon L., Muskheli V., Murry C.E. Scaffold-free human cardiac tissue patch created from embryonic stem cells. Tissue Eng. Part A 2009, 15:1211-1222.