Evaluation of changes in morphology and function of human induced pluripotent stem cell derived cardiomyocytes (hiPSC-CMs) cultured on an aligned-nanofiber cardiac patch

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Khan, Mahmood ^a   Xu, Yanyi ^a   Hua, Serena ^a   Johnson, Jed ^b   Belevych, Andriy ^a   Janssen, Paul M L ^a   Gyorke, Sandor ^a   Guan, Jianjun ^a   Angelos, Mark G ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b Nanofiber Solutions   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; CALCIUM; CONNEXIN 43; MESSENGER RNA; MOLECULAR SCAFFOLD; NANOFIBER; POLYGLACTIN; TROPONIN T;

ARTICLE; CELL CULTURE; CELL FUNCTION; CELL STRUCTURE; EXTRACELLULAR MATRIX; GAP JUNCTION; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN INDUCED PLURIPOTENT STEM CELL DERIVED CARDIOMYOCYTE; IN VITRO STUDY; INTRACARDIAC PATCH; NONHUMAN; PATCH CLAMP TECHNIQUE; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; ACTION POTENTIAL; CARDIAC MUSCLE CELL; CONFOCAL MICROSCOPY; CYTOLOGY; INDUCED PLURIPOTENT STEM CELL; METABOLISM; TISSUE SCAFFOLD; TRANSMISSION ELECTRON MICROSCOPY;

RATTUS;

ACTION POTENTIALS; CALCIUM; CELLS, CULTURED; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MYOCYTES, CARDIAC; NANOFIBERS; TISSUE SCAFFOLDS;

EID: 84930652067     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126338     Document Type: Article

References (39)

1. Roger VL (2013) Epidemiology of heart failure. Circ Res 113:646-659. doi: 10.1161/CIRCRESAHA. 113.300268 PMID: 23989710
2. Bartunek J, BehfarA, Dolatabadi D, Vanderheyden M, OstojicM, Dens J, et al. (2013) Cardiopoietic Stem Cell Therapy in Heart Failure. Journal of the American College of Cardiology 61:2329-2338. doi: 10.1016/j.jacc.2013.02.071 PMID: 23583246
3. TerzicA, BehfarA (2014) Regenerative heart failure therapy headed for optimization. European heart journal 35:1231-1234. doi: 10.1093/eurheartj/ehu117 PMID: 24670713
4. Hou D, Youssef EA, Brinton TJ, Zhang P, Rogers P, et al. (2005) Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation 112:I150-156. PMID: 16159808
5. Hong KU, LiQH, Guo Y, Patton NS, MoktarA, BhatnagarA, et al. (2013) A highly sensitive and accurate method to quantify absolute numbers of c-kit+ cardiac stem cells following transplantation in mice. Basic Res Cardiol 108:346. doi: 10.1007/s00395-013-0346-0 PMID: 23549981
6. Agudelo-Garcia PA, De Jesus JK, Williams SP, Nowicki MO, Chiocca EA, Liyanarachchi S, et al. (2011) Glioma Cell Migration on Three-dimensional Nanofiber Scaffolds Is Regulated by Substrate Topography and Abolished by Inhibition of STAT3 Signaling. Neoplasia 13:831-U896. PMID: 21969816
7. Johnson J, Nowicki MO, Lee CH, Chiocca EA, Viapiano MS, Lawler SE, et al. (2009) Quantitative Analysis of Complex Glioma Cell Migration on Electrospun Polycaprolactone Using Time-Lapse Microscopy. Tissue Engineering Part C-Methods 15:531-540. doi: 10.1089/ten. TEC.2008.0486 PMID: 19199562
8. Nam J, Huang Y, Agarwal S, Lannutti J (2008) Materials Selection and Residual Solvent Retention in Biodegradable Electrospun Fibers. Journal Of Applied Polymer Science 107:1547-1554.
9. Citro L, Naidu S, Hassan F, Kuppusamy ML, Kuppusamy P, Angelos MG, et al. (2014) Comparison of human induced pluripotent stem-cell derived cardiomyocytes with human mesenchymal stem cells following acute myocardial infarction. PLoSOne 9:e116281. doi: 10.1371/journal.pone.0116281 PMID: 25551230
10. Huang H, Ding Y, Sun XS, Nguyen TA (2013) Peptide hydrogelation and cell encapsulation for 3D culture of MCF-7 breast cancer cells. PLoSOne 8:e59482. doi: 10.1371/journal.pone.0059482 PMID: 23527204
11. McBane JE, VulesevicB, Padavan DT, McEwan KA, KorbuttGS, Suuronen EJ (2013) Evaluation of a collagen-chitosan hydrogel for potential use as a pro-angiogenic site for islet transplantation. PLoS One 8:e77538. doi: 10.1371/journal.pone.0077538 PMID: 24204863
12. Brunello L, Slabaugh JL, Radwanski PB, Ho HT, Belevych AE, Lou Q, et al. (2013) Decreased RyR2 refractoriness determines myocardial synchronization of aberrant Ca2+ release in a genetic model of arrhythmia. Proc Natl Acad Sci USA 110:10312-10317. doi: 10.1073/pnas.1300052110 PMID: 23733959
13. Belevych AE, Terentyev D, Terentyeva R, Ho HT, Gyorke I, Bonilla IM, et al. (2012) Shortened Ca2+ signaling refractoriness underlies cellular arrhythmogenesis in a postinfarction model of sudden cardiac death. Circ Res 110:569-577. doi: 10.1161/CIRCRESAHA.111.260455 PMID: 22223353
14. Rhett JM, Jourdan J, Gourdie RG (2011) Connexin 43 connexon to gap junction transition is regulated by zonula occludens-1. Mol Biol Cell 22:1516-1528. doi: 10.1091/mbc. E10-06-0548 PMID: 21411628
15. Sacconi L, FerrantiniC, Lotti J, Coppini R, Yan P, LoewLM, et al. (2012) Action potential propagation in transverse-axial tubular system is impaired in heart failure. Proc Natl Acad Sci USA 109:5815-5819. doi: 10.1073/pnas.1120188109 PMID: 22451916
16. Johnson J, Ghosh A, Lannutti J (2007) Microstructure-property relationships in a tissue-engineering scaffold. Journal Of Applied Polymer Science 104:2919-2927.
17. Besse P, Terrasson C, ChoussatA, Broustet JP, Bricaud H (1971) Contractile properties of the normal human cardiac muscle. Archives des Maladies duCoeuretdes Vaisseaux 64:485-500. PMID: 4997256
18. Engelmayr GC Jr., Cheng M, BettingerCJ, Borenstein JT, Langer R, Freed LE. (2008) Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nature Materials 7:1003-1010. doi: 10. 1038/nmat2316 PMID: 18978786
19. Rubin E GF (Liincott Williams & Wilkins; 2004) Pathology. Clinicoathologic Foudations of Medicine.
20. Bian W, Jackman CP, Bursac N (2014) Controlling the structural and functional anisotropy of engineered cardiac tissues. Biofabrication 6:024109. doi: 10.1088/1758-5082/6/2/024109 PMID: 24717534
21. Shin HJ, LeeCH, Cho IH, Kim YJ, LeeYJ, Kim IA, et al. (2006) Electrospun PLGA nanofiberscaffolds for articular cartilage reconstruction: mechanical stability, degradation and cellular responses under mechanical stimulation in vitro. Journal of Biomaterials Science-Polymer Edition 17:103-119. PMID: 16411602
22. ZongXH, Li S, Chen E, GarlickB, Kim KS, Fang D, et al. (2004) Prevention of postsurgery-induced abdominal adhesions by electrospun bioabsorbable nanofibrous poly (lactide-co-glycolide)-based membranes. Annals of Surgery 240:910-915. PMID: 15492575
23. Courtney T, Sacks MS, Stankus J, Guan J, Wagner WR (2006) Design and analysis of tissue engineering scaffolds that mimic soft tissue mechanical anisotropy. Biomaterials 27:3631-3638. PMID: 16545867
24. Kai D, Prabhakaran MP, Jin G, RamakrishnaS (2011) Guided orientation of cardiomyocytes on electrospun aligned nanofibers for cardiac tissue engineering. Journal of Biomedical Materials Research Part B-Applied Biomaterials 98 B: 379-386. doi: 10.1002/jbm.b.31862 PMID: 21681953
25. Murugan R, Ramakrishna S (2007) Design strategies of tissue engineering scaffolds with controlled fiber orientation. Tissue Engineering 13:1845-1866. PMID: 17518727
26. Pok S, Myers JD, Madihally SV, Jacot JG (2013) A multilayered scaffold of a chitosan and gelatin hydrogel supported by a PCL core for cardiac tissue engineering. Acta Biomater 9:5630-5642. doi: 10. 1016/j.actbio.2012.10.032 PMID: 23128158
27. FinkC, Ergun S, Kralisch D, Remmers U, Weil J, EschenhagenT. (2000) Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J 14:669-679. PMID: 10744624
28. Parker KK, Ingber DE (2007) Extracellular matrix, mechanotransduction and structural hierarchies in heart tissue engineering. Philos Trans RSoc Lond B Biol Sci 362:1267-1279. PMID: 17588874
29. Parrag IC, Zandstra PW, Woodhouse KA (2012) Fiber alignment and coculture with fibroblasts improves the differentiated phenotype of murine embryonic stem cell-derived cardiomyocytes for cardiac tissue engineering. Biotechnol Bioeng 109:813-822. doi: 10.1002/bit.23353 PMID: 22006660
30. Wang PY, Yu J, Lin JH, Tsai WB (2011) Modulation of alignment, elongation and contraction of cardiomyocytes through a combination of nanotopography and rigidity of substrates. Acta Biomater 7:3285-3293. doi: 10.1016/j.actbio.2011.05.021 PMID: 21664306
31. Asiri AM, Marwani HM, Khan SB, WebsterTJ (2014) Greater cardiomyocyte density on aligned compared with random carbon nanofibers in polymer composites. Int J Nanomedicine 9:5533-5539. doi: 10.2147/IJN. S71587 PMID: 25489241
32. KharazihaM, Shin SR, Nikkhah M, TopkayaSN, Masoumi N, Annabi N, et al. (2014) Tough and flexible CNT-polymeric hybrid scaffolds for engineering cardiac constructs. Biomaterials 35:7346-7354. doi: 10.1016/j.biomaterials.2014.05.014 PMID: 24927679
33. Zhang D, Shadrin IY, Lam J, Xian H-Q, Snodgrass HR, Bursac N, et al. (2013) Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 34:5813-5820. doi: 10.1016/j.biomaterials.2013.04.026 PMID: 23642535
34. Shin M, Ishii O, SuedaT, Vacanti JP (2004) Contractile cardiac grafts using a novel nanofibrous mesh. Biomaterials 25:3717-3723. PMID: 15020147
35. Nolan DJ, Ginsberg M, Israely E, Palikuqi B, PoulosMG, James D, et al. (2013) Molecular Signatures of Tissue-Specific Microvascular Endothelial Cell Heterogeneity in Organ Maintenance and Regeneration. Developmental Cell 26:204-219. doi: 10.1016/j.devcel.2013.06.017 PMID: 23871589
36. Beltrami AP, Cesselli D, Beltrami CA (2011) Multiple Sources for Cardiac Stem Cells and Their Cardiogenic Potential; Cohen IS, Gaudette GR, editors. 149-171 p.
37. Forte G, PietronaveS, Nardone G, Zamperone A, Magnani E, Pagliari S, et al. (2011) Human Cardiac Progenitor Cell Grafts as Unrestricted Source of Supernumerary Cardiac Cells in Healthy Murine Hearts. Stem Cells 29:2051-2061. doi: 10.1002/stem.763 PMID: 22009661
38. Qian L, Shim W, Gu Y, Shirhan M, Lim KP, Tan LP, et al. (2012) Hemodynamic Contribution of Stem Cell Scaffolding in Acute Injured Myocardium. Tissue Engineering Part A 18:1652-1663. doi: 10.1089/ten. TEA.2011.0591 PMID: 22607369
39. Hashizume R, Fujimoto KL, Hong Y, Guan J, TomaC, Tobita K, et al. (2013) Biodegradable elastic patch plasty ameliorates left ventricular adverse remodeling after ischemia-reperfusion injury: a preclinical study of a porous polyurethane material in a porcine model. JThoracCardiovascSurg 146:391-399 e391. doi: 10.1016/j.jtcvs.2012.11.013 PMID: 23219497