Young Developmental Age Cardiac Extracellular Matrix Promotes the Expansion of Neonatal Cardiomyocytes in Vitro

Overview

Journal Acta Biomater

Publisher Elsevier

Specialty Biomedical Engineering

Date 2013 Sep 10

PMID 24012606

Citations 99

Authors

C Williams

K P Quinn

I Georgakoudi

L D Black 3rd

Affiliations

Soon will be listed here.

Abstract

A major limitation to cardiac tissue engineering and regenerative medicine strategies is the lack of proliferation of postnatal cardiomyocytes. The extracellular matrix (ECM) is altered during heart development, and studies suggest that it plays an important role in regulating myocyte proliferation. Here, the effects of fetal, neonatal and adult cardiac ECM on the expansion of neonatal rat ventricular cells in vitro are studied. At 24h, overall cell attachment was lowest on fetal ECM; however, ~80% of the cells were cardiomyocytes, while many non-myocytes attached to older ECM and poly-l-lysine controls. After 5 days, the cardiomyocyte population remained highest on fetal ECM, with a 4-fold increase in number. Significantly more cardiomyocytes stained positively for the mitotic marker phospho-histone H3 on fetal ECM compared with other substrates at 5 days, suggesting that proliferation may be a major mechanism of cardiomyocyte expansion on young ECM. Further study of the beneficial properties of early developmental aged cardiac ECM could advance the design of novel biomaterials aimed at promoting cardiac regeneration.

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References

Porter K, Turner N . Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol Ther. 2009; 123(2):255-78. DOI: 10.1016/j.pharmthera.2009.05.002. View

Bishop J, Greenbaum R, Gibson D, Yacoub M, Laurent G . Enhanced deposition of predominantly type I collagen in myocardial disease. J Mol Cell Cardiol. 1990; 22(10):1157-65. DOI: 10.1016/0022-2828(90)90079-h. View

Jesty S, Steffey M, Lee F, Breitbach M, Hesse M, Reining S . c-kit+ precursors support postinfarction myogenesis in the neonatal, but not adult, heart. Proc Natl Acad Sci U S A. 2012; 109(33):13380-5. PMC: 3421216. DOI: 10.1073/pnas.1208114109. View

deAlmeida A, Sedmera D . Fibroblast Growth Factor-2 regulates proliferation of cardiac myocytes in normal and hypoplastic left ventricles in the developing chick. Cardiol Young. 2009; 19(2):159-69. DOI: 10.1017/S1047951109003552. View

Porrello E, Mahmoud A, Simpson E, Hill J, Richardson J, Olson E . Transient regenerative potential of the neonatal mouse heart. Science. 2011; 331(6020):1078-80. PMC: 3099478. DOI: 10.1126/science.1200708. View

Miyagawa S, Roth M, Saito A, Sawa Y, Kostin S . Tissue-engineered cardiac constructs for cardiac repair. Ann Thorac Surg. 2010; 91(1):320-9. DOI: 10.1016/j.athoracsur.2010.09.080. View

Norris R, Kern C, Wessels A, Moralez E, Markwald R, Mjaatvedt C . Identification and detection of the periostin gene in cardiac development. Anat Rec A Discov Mol Cell Evol Biol. 2004; 281(2):1227-33. DOI: 10.1002/ar.a.20135. View

Ngoka L . Sample prep for proteomics of breast cancer: proteomics and gene ontology reveal dramatic differences in protein solubilization preferences of radioimmunoprecipitation assay and urea lysis buffers. Proteome Sci. 2008; 6:30. PMC: 2600628. DOI: 10.1186/1477-5956-6-30. View

Hibino N, McGillicuddy E, Matsumura G, Ichihara Y, Naito Y, Breuer C . Late-term results of tissue-engineered vascular grafts in humans. J Thorac Cardiovasc Surg. 2010; 139(2):431-6, 436.e1-2. DOI: 10.1016/j.jtcvs.2009.09.057. View

10.

Naito H, Melnychenko I, Didie M, Schneiderbanger K, Schubert P, Rosenkranz S . Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation. 2006; 114(1 Suppl):I72-8. DOI: 10.1161/CIRCULATIONAHA.105.001560. View

11.

Sazonova O, Lee K, Isenberg B, Rich C, Nugent M, Wong J . Cell-cell interactions mediate the response of vascular smooth muscle cells to substrate stiffness. Biophys J. 2011; 101(3):622-30. PMC: 3145282. DOI: 10.1016/j.bpj.2011.06.051. View

12.

Tobita K, Garrison J, Liu L, Tinney J, Keller B . Three-dimensional myofiber architecture of the embryonic left ventricle during normal development and altered mechanical loads. Anat Rec A Discov Mol Cell Evol Biol. 2005; 283(1):193-201. DOI: 10.1002/ar.a.20133. View

13.

Lorts A, Schwanekamp J, Elrod J, Sargent M, Molkentin J . Genetic manipulation of periostin expression in the heart does not affect myocyte content, cell cycle activity, or cardiac repair. Circ Res. 2008; 104(1):e1-7. PMC: 2644415. DOI: 10.1161/CIRCRESAHA.108.188649. View

14.

Ieda M, Tsuchihashi T, Ivey K, Ross R, Hong T, Shaw R . Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev Cell. 2009; 16(2):233-44. PMC: 2664087. DOI: 10.1016/j.devcel.2008.12.007. View

15.

Roell W, Lewalter T, Sasse P, Tallini Y, Choi B, Breitbach M . Engraftment of connexin 43-expressing cells prevents post-infarct arrhythmia. Nature. 2007; 450(7171):819-24. DOI: 10.1038/nature06321. View

16.

Quinn K, Bellas E, Fourligas N, Lee K, Kaplan D, Georgakoudi I . Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios. Biomaterials. 2012; 33(21):5341-8. PMC: 3387752. DOI: 10.1016/j.biomaterials.2012.04.024. View

17.

Stumper O . Hypoplastic left heart syndrome. Heart. 2010; 96(3):231-6. DOI: 10.1136/hrt.2008.159889. View

18.

Urbanek K, Quaini F, Tasca G, Torella D, Castaldo C, Nadal-Ginard B . Intense myocyte formation from cardiac stem cells in human cardiac hypertrophy. Proc Natl Acad Sci U S A. 2003; 100(18):10440-5. PMC: 193580. DOI: 10.1073/pnas.1832855100. View

19.

Zimmermann W, Cesnjevar R . Cardiac tissue engineering: implications for pediatric heart surgery. Pediatr Cardiol. 2009; 30(5):716-23. PMC: 2691807. DOI: 10.1007/s00246-009-9405-6. View

20.

Wang B, Borazjani A, Tahai M, de Jongh Curry A, Simionescu D, Guan J . Fabrication of cardiac patch with decellularized porcine myocardial scaffold and bone marrow mononuclear cells. J Biomed Mater Res A. 2010; 94(4):1100-10. PMC: 2933781. DOI: 10.1002/jbm.a.32781. View