From biological induction to engineering assembly—— the current status and perspective on vascularization of engineered heart tissue_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

CAI Jun ,  KANG Kai , JIANG Shulin

Department of Cardiovascular Surgery, 2nd Affiliated Hospital of Harbin Medical University, Key Laboratory of Myocardial Ischemia Mechanism and Treatment, Ministry of Education, Harbin, 150086, P.R.China;

Corresponding author：

KANG Kai, Email: kangkai1975@sina.com

Keywords：

Engineered heart tissue; vascularization; biology; engineering

DOI：

10.7507/1007-4848.201604031

Video：

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The engineered heart tissues (EHTs) is regarded as a hope for myocardial repair and regeneration. But a series of " bottleneck” problems, such as vascularization, hinder their clinical translation. This review focuses on the strategies to vascularization of EHTs and encourages the emergence of novel EHTs that can meet clinic requirement properly.

Citation： CAI Jun, KANG Kai, JIANG Shulin. From biological induction to engineering assembly—— the current status and perspective on vascularization of engineered heart tissue. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2017, 24(9): 730-734. doi: 10.7507/1007-4848.201604031 Copy

1.	Walles T, Herden T, Haverich A, et al. Influence of scaffold thickness and scaffold composition on bioartificial graft survival. Biomaterials, 2003, 24(7): 1233-1239.
2.	White MP, Rufaihah AJ, Liu L, et al. Limited gene expression variation in human embryonic stem cell and induced pluripotent stem cell-derived endothelial cells. Stem cells, 2013, 31(1): 92-103.
3.	Zisch AH, Lutolf MP, Hubbell JA. Biopolymeric delivery matrices for angiogenic growth factors. Cardiovasc Pathol, 2003, 12(6): 295-310.
4.	Korpisalo P, Ylä-Herttuala S. Stimulation of functional vessel growth by gene therapy. Integr Biol (Camb), 2010, 2(2-3): 102-112.
5.	Coulombe KL, Bajpai VK, Andreadis ST. Heart regeneration with engineered myocardial tissue. Annu Rev Biomed Eng, 2014, 16: 1-28.
6.	Stratman AN, Malotte KM, Mahan RD, et al. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood, 2009, 114(24): 5091-5101.
7.	Hudon V, Berthod F, Black AF, et al. A tissue-engineered endothelialized dermis to study the modulation of angiogenic and angiostatic molecules on capillary-like tube formation in vitro. Br J Dermatol, 2003, 148(6): 1094-1104.
8.	Tsigkou O, Pomerantseva I, Spencer JA, et al. Engineered vascularized bone grafts. Proc Natl Acad Sci USA, 2010, 107(8): 3311-3316.
9.	Sun X, Altalhi W, Nunes SS. Vascularization strategies of engineered tissues and their application in cardiac regeneration. Adv Drug Deliv Rev, 2016, 96: 183-194.
10.	Steffens GC, Yao C, Prevel P, et al. Modulation of angiogenic potential of collagen matrices by covalent incorporation of heparin and loading with vascular endothelial growth factor. Tissue Eng, 2004, 10(9-10): 1502-1509.
11.	Lee KY, Peters MC, Anderson KW, et al. Controlled growth factor release from synthetic extracellular matrices. Nature, 2000, 408(6815): 998-1000.
12.	Kang K, Sun L, Xiao Y, et al. Aged human cells rejuvenated by cytokine enhancement of biomaterials for surgical ventricular restoration. J Am Coll Cardiol, 2012, 60(21): 2237-2249.
13.	Melly LF, Marsano A, Frobert A, et al. Controlled angiogenesis in the heart by cell-based expression of specific vascular endothelial growth factor levels. Hum Gene Ther Methods, 2012, 23(5): 346-356.
14.	Marsano A, Maidhof R, Luo J, et al. The effect of controlled expression of VEGF by transduced myoblasts in a cardiac patch on vascularization in a mouse model of myocardial infarction. Biomaterials, 2013, 34(2): 393-401.
15.	Meloni M, Marchetti M, Garner K, et al. Local inhibition of microRNA-24 improves reparative angiogenesis and left ventricle remodeling and function in mice with myocardial infarction. Mol Ther, 2013, 21(7): 1390-1402.
16.	Zangi L, Lui KO, von Gise A, et al. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat Biotechnol, 2013, 31(10): 898-907.
17.	Tengood JE, Ridenour R, Brodsky R, et al. Sequential delivery of basic fibroblast growth factor and platelet-derived growth factor for angiogenesis. Nat Biotechnol, 2011, 17(9-10): 1181-1189.
18.	Davis ME, Motion JP, Narmoneva DA, et al. Injectable self-assembling peptide nanofibers create intramyocardial microenvironments for endothelial cells. Circulation, 2005, 111(4): 442-450.
19.	Zhang J, Ding L, Zhao Y, et al. Collagen-targeting vascular endothelial growth factor improves cardiac performance after myocardial infarction. Circulation, 2009, 119(13): 1776-1784.
20.	Gao J, Liu J, Gao Y, et al. A myocardial patch made of collagen membranes loaded with collagen-binding human vascular endothelial growth factor accelerates healing of the injured rabbit heart. Tissue Eng Part A, 2011, 17(21-22): 2739-2747.
21.	Wu J, Zeng F, Huang XP, et al. Infarct stabilization and cardiac repair with a VEGF-conjugated, injectable hydrogel. Biomaterials, 2011, 32(2): 579-586.
22.	Miyagi Y, Zeng F, Huang XP, et al. Surgical ventricular restoration with a cell- and cytokine-seeded biodegradable scaffold. Biomaterials, 2010, 31(30): 7684-7694.
23.	Hirt MN, Hansen A, Eschenhagen T. Cardiac tissue engineering: state of the art. Circ Res, 2014, 114(2): 354-367.
24.	Dvir T, Kedem A, Ruvinov E, et al. Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc Natl Acad Sci USA, 2009, 106(35): 14990-14995.
25.	Zhang C, Hou J, Zheng S, et al. Vascularized atrial tissue patch cardiomyoplasty with omentopexy improves cardiac performance after myocardial infarction. Ann Thorac Surg, 2011, 92(4): 1435-1442.
26.	Huang W, Zhang D, Millard RW, et al. Gene manipulated peritoneal cell patch repairs infarcted myocardium. J Mol Cell Cardiol, 2010, 48(4): 702-712.
27.	Morritt AN, Bortolotto SK, Dilley RJ, et al. Cardiac tissue engineering in an in vivo vascularized chamber. Circulation, 2007, 115(3): 353-360.
28.	Sekine H, Shimizu T, Sakaguchi K, et al. In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels. Nat Commun, 2013, 4: 1399.
29.	Chiu LL, Montgomery M, Liang Y,et al. Perfusable branching microvessel bed for vascularization of engineered tissues. Proc Natl Acad Sci USA, 2012, 109(50): E3414-3423.
30.	Shimizu T, Yamato M, Isoi Y, et al. Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res, 2002, 90(3): e40.
31.	Sekine H, Shimizu T, Hobo K, et al. Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation, 2008, 118(14 Suppl): S145-152.
32.	Shimizu T, Sekine H, Yang J, et al. Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. FASEB J, 2006, 20(6): 708-710.
33.	Radisic M, Malda J, Epping E, et al. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol Bioeng, 2006, 93(2): 332-343.
34.	McGuigan AP, Sefton MV. Vascularized organoid engineered by modular assembly enables blood perfusion. Proc Natl Acad Sci USA, 2006, 103(31): 11461-11466.
35.	Leung BM, Sefton MV. A modular tissue engineering construct containing smooth muscle cells and endothelial cells. Ann Biomed Eng, 2007, 35(12): 2039-2049.
36.	Chamberlain MD, Gupta R, Sefton MV. Chimeric vessel tissue engineering driven by endothelialized modules in immunosuppressed Sprague-Dawley rats. Tissue Eng Part A, 2011, 17(1-2): 151-160.
37.	Chamberlain MD, Gupta R, Sefton MV. Bone marrow-derived mesenchymal stromal cells enhance chimeric vessel development driven by endothelial cell-coated microtissues. Tissue Eng Part A, 2012, 18(3-4): 285-294.
38.	Koffler J, Kaufman-Francis K, Shandalov Y, et al. Improved vascular organization enhances functional integration of engineered skeletal muscle grafts. Proc Natl Acad Sci USA, 2011, 108(36): 14789-14794.
39.	Baranski JD, Chaturvedi RR, Stevens KR, et al. Geometric control of vascular networks to enhance engineered tissue integration and function. Proc Natl Acad Sci USA, 2013, 110(19): 7586-7591.
40.	Kaihara S, Borenstein J, Koka R, et al. Silicon micromachining to tissue engineer branched vascular channels for liver fabrication. Tissue Eng, 2000, 6(2): 105-117.
41.	Fidkowski C, Kaazempur-Mofrad MR, Borenstein J, et al. Endothelialized microvasculature based on a biodegradable elastomer. Tissue Eng, 2005, 11(1-2): 302-309.
42.	Golden AP, Tien J. Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip, 2007, 7(6): 720-725.
43.	Miller JS, Stevens KR, Yang MT, et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater, 2012, 11(9): 768-774.

1. Walles T, Herden T, Haverich A, et al. Influence of scaffold thickness and scaffold composition on bioartificial graft survival. Biomaterials, 2003, 24(7): 1233-1239.
2. White MP, Rufaihah AJ, Liu L, et al. Limited gene expression variation in human embryonic stem cell and induced pluripotent stem cell-derived endothelial cells. Stem cells, 2013, 31(1): 92-103.
3. Zisch AH, Lutolf MP, Hubbell JA. Biopolymeric delivery matrices for angiogenic growth factors. Cardiovasc Pathol, 2003, 12(6): 295-310.
4. Korpisalo P, Ylä-Herttuala S. Stimulation of functional vessel growth by gene therapy. Integr Biol (Camb), 2010, 2(2-3): 102-112.
5. Coulombe KL, Bajpai VK, Andreadis ST. Heart regeneration with engineered myocardial tissue. Annu Rev Biomed Eng, 2014, 16: 1-28.
6. Stratman AN, Malotte KM, Mahan RD, et al. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood, 2009, 114(24): 5091-5101.
7. Hudon V, Berthod F, Black AF, et al. A tissue-engineered endothelialized dermis to study the modulation of angiogenic and angiostatic molecules on capillary-like tube formation in vitro. Br J Dermatol, 2003, 148(6): 1094-1104.
8. Tsigkou O, Pomerantseva I, Spencer JA, et al. Engineered vascularized bone grafts. Proc Natl Acad Sci USA, 2010, 107(8): 3311-3316.
9. Sun X, Altalhi W, Nunes SS. Vascularization strategies of engineered tissues and their application in cardiac regeneration. Adv Drug Deliv Rev, 2016, 96: 183-194.
10. Steffens GC, Yao C, Prevel P, et al. Modulation of angiogenic potential of collagen matrices by covalent incorporation of heparin and loading with vascular endothelial growth factor. Tissue Eng, 2004, 10(9-10): 1502-1509.
11. Lee KY, Peters MC, Anderson KW, et al. Controlled growth factor release from synthetic extracellular matrices. Nature, 2000, 408(6815): 998-1000.
12. Kang K, Sun L, Xiao Y, et al. Aged human cells rejuvenated by cytokine enhancement of biomaterials for surgical ventricular restoration. J Am Coll Cardiol, 2012, 60(21): 2237-2249.
13. Melly LF, Marsano A, Frobert A, et al. Controlled angiogenesis in the heart by cell-based expression of specific vascular endothelial growth factor levels. Hum Gene Ther Methods, 2012, 23(5): 346-356.
14. Marsano A, Maidhof R, Luo J, et al. The effect of controlled expression of VEGF by transduced myoblasts in a cardiac patch on vascularization in a mouse model of myocardial infarction. Biomaterials, 2013, 34(2): 393-401.
15. Meloni M, Marchetti M, Garner K, et al. Local inhibition of microRNA-24 improves reparative angiogenesis and left ventricle remodeling and function in mice with myocardial infarction. Mol Ther, 2013, 21(7): 1390-1402.
16. Zangi L, Lui KO, von Gise A, et al. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat Biotechnol, 2013, 31(10): 898-907.
17. Tengood JE, Ridenour R, Brodsky R, et al. Sequential delivery of basic fibroblast growth factor and platelet-derived growth factor for angiogenesis. Nat Biotechnol, 2011, 17(9-10): 1181-1189.
18. Davis ME, Motion JP, Narmoneva DA, et al. Injectable self-assembling peptide nanofibers create intramyocardial microenvironments for endothelial cells. Circulation, 2005, 111(4): 442-450.
19. Zhang J, Ding L, Zhao Y, et al. Collagen-targeting vascular endothelial growth factor improves cardiac performance after myocardial infarction. Circulation, 2009, 119(13): 1776-1784.
20. Gao J, Liu J, Gao Y, et al. A myocardial patch made of collagen membranes loaded with collagen-binding human vascular endothelial growth factor accelerates healing of the injured rabbit heart. Tissue Eng Part A, 2011, 17(21-22): 2739-2747.
21. Wu J, Zeng F, Huang XP, et al. Infarct stabilization and cardiac repair with a VEGF-conjugated, injectable hydrogel. Biomaterials, 2011, 32(2): 579-586.
22. Miyagi Y, Zeng F, Huang XP, et al. Surgical ventricular restoration with a cell- and cytokine-seeded biodegradable scaffold. Biomaterials, 2010, 31(30): 7684-7694.
23. Hirt MN, Hansen A, Eschenhagen T. Cardiac tissue engineering: state of the art. Circ Res, 2014, 114(2): 354-367.
24. Dvir T, Kedem A, Ruvinov E, et al. Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc Natl Acad Sci USA, 2009, 106(35): 14990-14995.
25. Zhang C, Hou J, Zheng S, et al. Vascularized atrial tissue patch cardiomyoplasty with omentopexy improves cardiac performance after myocardial infarction. Ann Thorac Surg, 2011, 92(4): 1435-1442.
26. Huang W, Zhang D, Millard RW, et al. Gene manipulated peritoneal cell patch repairs infarcted myocardium. J Mol Cell Cardiol, 2010, 48(4): 702-712.
27. Morritt AN, Bortolotto SK, Dilley RJ, et al. Cardiac tissue engineering in an in vivo vascularized chamber. Circulation, 2007, 115(3): 353-360.
28. Sekine H, Shimizu T, Sakaguchi K, et al. In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels. Nat Commun, 2013, 4: 1399.
29. Chiu LL, Montgomery M, Liang Y,et al. Perfusable branching microvessel bed for vascularization of engineered tissues. Proc Natl Acad Sci USA, 2012, 109(50): E3414-3423.
30. Shimizu T, Yamato M, Isoi Y, et al. Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res, 2002, 90(3): e40.
31. Sekine H, Shimizu T, Hobo K, et al. Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation, 2008, 118(14 Suppl): S145-152.
32. Shimizu T, Sekine H, Yang J, et al. Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. FASEB J, 2006, 20(6): 708-710.
33. Radisic M, Malda J, Epping E, et al. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol Bioeng, 2006, 93(2): 332-343.
34. McGuigan AP, Sefton MV. Vascularized organoid engineered by modular assembly enables blood perfusion. Proc Natl Acad Sci USA, 2006, 103(31): 11461-11466.
35. Leung BM, Sefton MV. A modular tissue engineering construct containing smooth muscle cells and endothelial cells. Ann Biomed Eng, 2007, 35(12): 2039-2049.
36. Chamberlain MD, Gupta R, Sefton MV. Chimeric vessel tissue engineering driven by endothelialized modules in immunosuppressed Sprague-Dawley rats. Tissue Eng Part A, 2011, 17(1-2): 151-160.
37. Chamberlain MD, Gupta R, Sefton MV. Bone marrow-derived mesenchymal stromal cells enhance chimeric vessel development driven by endothelial cell-coated microtissues. Tissue Eng Part A, 2012, 18(3-4): 285-294.
38. Koffler J, Kaufman-Francis K, Shandalov Y, et al. Improved vascular organization enhances functional integration of engineered skeletal muscle grafts. Proc Natl Acad Sci USA, 2011, 108(36): 14789-14794.
39. Baranski JD, Chaturvedi RR, Stevens KR, et al. Geometric control of vascular networks to enhance engineered tissue integration and function. Proc Natl Acad Sci USA, 2013, 110(19): 7586-7591.
40. Kaihara S, Borenstein J, Koka R, et al. Silicon micromachining to tissue engineer branched vascular channels for liver fabrication. Tissue Eng, 2000, 6(2): 105-117.
41. Fidkowski C, Kaazempur-Mofrad MR, Borenstein J, et al. Endothelialized microvasculature based on a biodegradable elastomer. Tissue Eng, 2005, 11(1-2): 302-309.
42. Golden AP, Tien J. Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip, 2007, 7(6): 720-725.
43. Miller JS, Stevens KR, Yang MT, et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater, 2012, 11(9): 768-774.

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