A tissue-engineered chondrocyte cell sheet induces extracellular matrix modification to enhance ventricular biomechanics and attenuate myocardial stiffness in ischemic cardiomyopathy

Tissue Engineering - Part A

Volumn 21, Issue 19-20, 2015, Pages 2515-2525

  Shudo, Yasuhiro ^a,d   Cohen, Jeffrey E ^a,b   Macarthur, John W ^a,b   Goldstone, Andrew B ^a,b   Otsuru, Satoru ^c   Trubelja, Alen ^b   Patel, Jay ^a   Edwards, Bryan B ^a   Hung, George ^b   Fairman, Alexander S ^b   Brusalis, Christopher ^b   Hiesinger, William ^b   Atluri, Pavan ^b   Hiraoka, Arudo ^b   Miyagawa, Shigeru ^d   Sawa, Yoshiki ^d   Woo, Y Joseph ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c NATIONWIDE CHILDREN S HOSPITAL   (United States)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; BODY FLUIDS; CARTILAGE; CELLS; CYTOLOGY; DISEASES; ELASTICITY; HEART; HYDROGELS; RATS; STIFFNESS; STIFFNESS MATRIX;

ARTICULAR CARTILAGES; BIOMECHANICAL PROPERTIES; CELL SHEET ENGINEERING; EXTRACELLULAR MATRICES; LEFT ANTERIOR DESCENDING; MYOCARDIAL FUNCTION; NATURAL ENVIRONMENTS; TEMPERATURE-RESPONSIVE;

CELL ENGINEERING;

ADHERENT CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTICULAR CARTILAGE; BIOMECHANICS; CAPILLARY DENSITY; CARTILAGE CELL; CELL SHEET TRANSPLANTATION; CELL TRANSPLANTATION; CONTROLLED STUDY; ELASTICITY; EXTRACELLULAR MATRIX; HEART FUNCTION; HEART INFARCTION; HEART LEFT VENTRICLE MASS; HEART LEFT VENTRICLE VOLUME; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; ISCHEMIC CARDIOMYOPATHY; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RIGIDITY; TISSUE ENGINEERING; WALL STRESS; ANIMAL; CARDIOMYOPATHY; CHONDROCYTE; CYTOLOGY; IMMUNOHISTOCHEMISTRY; METABOLISM; PROCEDURES; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; BLOTTING, WESTERN; CARDIOMYOPATHIES; CHONDROCYTES; IMMUNOHISTOCHEMISTRY; MALE; RATS; RATS, WISTAR; TISSUE ENGINEERING;

EID: 84944104264     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2014.0155     Document Type: Article

References (31)

1. Pfeffer M., and Braunwald E. Ventricular remodeling after myocardial infaction. Experimental observations and clinical implications. Circulation 81, 1161, 1990
2. Spinale F.G. Matrix metalloproteinases: regulation and dysregulation in the failing heart. Circ Res 90, 520, 2002
3. Blom A.S., Mukherjee R., Pilla J.J., Lowry A.S., Yarbrough W.M., Mingoia J.T., Hendrick J.W., Stroud R.E., McLean J.E., Affuso J., Gorman R.C., Gorman J.H., III, Acker M.A., and Spinale F.G. Cardiac support device modifies left ventricular geometry and myocardial structure after myocardial infarction. Circulation 112, 1274, 2005
4. Philla J.J., Blom A.S., Brockman D.J., Bowen F., Yuan Q., Giammarco J., Ferrari V.A., Gorman J.H., III, Gorman R.C., and Acker M.A. Ventricular constraint using the acorn cardiac support device reduces myocardial akinetic area in an ovine model of acute infarction. Circulation 106, I207, 2002
5. Yano F., Hojo H., Ohba S., Saito T., Honnami M., Mochizuki M., Takato T., Kawaguchi H., and Chung U. Cell-sheet technology combined with a thienoindazole derivative small compound TD-198946 for cartilage regeneration. Biomaterials 34, 5581, 2013
6. Kokubo M., Sato M., Yamato M., Mitani G., Kutsuna T., Ebihara G., Okano T., and Mochida J. Characterization of chondrocyte sheets prepared using a co-culture method with temperature-responsive culture inserts. J Tissue Eng Regen Med 2013; DOI: 10.1002/term.1764
7. Sawa Y., and Miyagawa S. Cell sheet technology for heart failure. Curr Pharm Biotechnol 14, 61, 2013
8. Okano T., Yamada N., Sakai H., and Sakurai Y. A novel recovery system for cultured cells using plasma-treated polystyrene dishes grafted with poly(N-iso-propylacrylamide). J Biomed Mater Res 27, 1243, 1993
9. Miyagawa S., Roth M., Saito A., Sawa Y., and Kostin S. Tissue-engineered cardiac constructs for cardiac repair. Ann Thorac Surg 91, 320, 2011
10. Miyagawa S., Sawa Y., Sakakida S., Taketani S., Kondoh H., Memon I.A., Imanishi Y., Shimizu T., Okano T., and Matsuda H. Tissue cardiomyoplasty using bioengineered contractile cardiomyocyte sheets to repair damaged myocardium: their integration with recipient myocardium. Transplantation 80, 1586, 2005
11. Weber G.F., Bjerke M.A., and DeSimone D.W. A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev Cell 22, 104, 2012
12. Shudo Y., Cohen J.E., MacArthur J.W., Atluri P., Hsiao P.F., Yang E.C., Fairman A.S., Trubelja A., Patel J., Miyagawa S., Sawa Y., and Woo Y.J. Spatially-oriented, temporally-sequential SMC-EPC bi-level cell-sheet neovascularizes ischemic myocardium. Circulation 128(26 Suppl 1): S59, 2013
13. Atluri P., Trubelja A., Fairman A.S., Hsiao P.F., Mac-Arthur J.W., Cohen J.E., Shudo Y., Frederick J., and Woo Y.J. Normalization of post-infarct biomechanics utilizing a novel tissue engineered angiogenic construct. Circulation 128(26 Suppl 1): S95, 2013
14. MacArthur J.W., Purcell B., Shudo Y., Cohen J.E., Fairman A.S., Trubelja A., Patel J., Hsiao P.F., Yang E.C., Lloyd K., Hiesinger W., Atluri P., Burdick J., and Woo Y.J. Sustained release of engineered stromal cellderived factor 1-alpha from injectable hydrogels effectively recruits endothelial progenitor cells and preserves ventricular function following myocardial infarction. Circulation 128(26 Suppl 1): S79, 2013
15. Hiesinger W., Perez-Aguilar J.M., Atluri P., Marotta N.A., Frederick J.R., Fitzpatrick J.R., III, McCormick R.C., Muenzer J.R., Yang E.C., Levit R.D., Yuan L.J., MacArthur J.W., Saven J.G., and Woo Y.J. Computational protein design to reengineer stromal cell-derived factor-1a generates an effective and translatable angiogenic polypeptide analog. Circulation 124, S18, 2011
16. Frederick J.R., Fitzpatrick J.R., III, McCormick R.C., Harris D.A., Kim A.Y., Muenzer J.R., Marotta N., Smith M.J., Cohen J.E., Hiesinger W., Atluri P., and Woo Y.J. Stromal cell-derived factor-1 alpha activation of tissueengineered endothelial progenitor cell matrix enhances ventricular function after myocardial infarction by inducing neovasculogenesis. Circulation 122, S107, 2010
17. Yamato M., Utsumi M., Kushida A., Konno C., Kikuchi A., and Okano T. Thermo-responsive culture dishes allow the intact harvest of multilayered keratinocyte sheets without dispase by reducing temperature. Tissue Eng 7, 473, 2001
18. Shudo Y., Miyagawa S., Ohkura H., Fukushima S., Saito A., Kawaguchi N., Matsuura N., Shimizu T., Okano T., Matsuyama A., and Sawa Y. Addition of mesenchymal stem cells enhances the therapeutic effects of skeletal myoblast cell-sheet transplantation in a rat ischemic cardiomyopathy model. Tissue Eng Part A 20, 728, 2014
19. Shudo Y., Miyagawa S., Fukushima S., Saito A., Shimizu T., Okano T., and Sawa Y. Novel regenerative therapy using cell-sheet covered with omentum flap delivers a huge number of cells in a porcine myocardial infarction model. J Thorac Cardiovasc Surg 142, 1188, 2011
20. Mourouzis I., Giagourta I., Galanopoulos G., Mantzouratou P., Kostakou E., Kokkinos A.D., Tentolouris N., and Pantos C. Thyroid hormone improves the mechanical performance of the post-infarcted diabetic myocardium: a response associated with up-regulation of Akt/mTOR and AMPK activation. Metabolism 62, 1387, 2013
21. MacArthur J.W., Jr., Trubelja A., Shudo Y., Hsiao P., Fairman A., Yang E., Hiesinger W., Sarver J.J., Atluri P., and Woo Y.J. Mathematically engineered stromal cellderived factor-1a stem cell cytokine analog enhances mechanical properties of infarcted myocardium. J Thorac Cardiovasc Surg 145, 278, 2013
22. Ducharme A., Frantz S., Aikawa M., Rabkin E., Lindsey M., Rohde L.E., Schoen F.J., Kelly R.A., Werb Z., Libby P., and Lee R.T. Targeted delotion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J Clin Invest 106, 55, 2000
23. Grossman W. Cardiac hypertrophy: useful adaptation or pathologic process. Am J Med 69, 576, 1980
24. Shudo Y., Taniguchi K., Takeda K., Sakaguchi T., Funatsu T., Kondoh H., and Sawa Y. Serial multidetector computed tomography assessment of left ventricular reverse remodeling, mass, and regional wall stress after restrictive mitral annuloplasty in dilated cardiomyopathy. J Thorac Cardiovasc Surg 143(4 Suppl): S43, 2012
25. Li A.H., Liu P.P., Villarreal F.J., and Garcia R.A. Dynamic changes in myocardial matrix and relevance to disease: translational perspectives. Circ Res 114, 916, 2014
26. Uchinaka A., Kawaguchi N., Hamada Y., Miyagawa S., Saito A., ori S., Sawa Y., and Matsuura N. Transplantation of elastin-secreting myoblast sheets improves cardiac function in infarcted rat heart. Mol Cell Biochem 368, 203, 2012
27. Nakamura T., Lozano P.R., Ikeda Y., Iwanaga Y., Hinek A., Minamisawa S., Cheng C.F., Kobuke K., Dalton N., Takeda Y., Tashiro K., Ross J., Jr., Honjo T., and Chien K.R. Fibulin-5/DANCE is essential for elastogenesis in vivo. Nature 415, 171, 2002
28. Zhang C., Li Y., Cornelia R., Swisher S., and Kim H. Regulation of VEGF expression by HIF-1a in the femoral head cartilage following ischemia osteonecrosis. SciRep2, 650, 2012
29. Shudo Y., Miyagawa S., Nakatani S., Fukushima S., Sakaguchi T., Saito, ., Asanuma T., awaguchi, ., atsuura, ., Shimizu T., kano T., and Sawa Y. Myocardial layer-specific effect of myoblast cell-sheet implantation evaluated by tissue strain imaging. Circ J 77, 1063, 2013
30. Makris E.A., Hu J.C., and Athanasiou K.A. Hypoxiainduced collagen crosslinking as a mechanism for enhancing mechanical proper. Osteoarthritis Cartilage 21, 634, 2013
31. Trubelja A., MacArthur J.W., Sarver J.J., Cohen J.E., Hung G., Shudo Y., Fairman A.S., Patel J., Edwards B.B., Damrauer S.M., Hiesinger W., Atluri P., and Woo Y.J. Bioengineered stromal cell-derived factor-1a analogue delivered as an angiogenic therapy significantly restores viscoelastic material properties of infarcted cardiac muscle. J Biomech Eng 136, 2014; DOI: 10.1115/1.4027731