Integration and regression of implanted engineered human vascular networks during deep wound healing

Stem Cells Translational Medicine

Volumn 2, Issue 4, 2013, Pages 297-306

  Hanjaya Putra, Donny ^a   Shen, YU I ^a   Wilson, Abigail ^a   Fox Talbot, Karen ^b   Khetan, Sudhir ^c   Burdick, Jason A ^c   Steenbergen, Charles ^b   Gerecht, Sharon ^a  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Angiogenesis and bull; Endothelial progenitors and bull; Hyaluronan and bull; Hydrogel and bull; Microvasculature; Tissue regeneration and bull; Vascular engineering and bull; Wound healing and bull

Indexed keywords

CD31 ANTIGEN; HYALURONIC ACID;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BURN; CELL PROLIFERATION; COLONY FORMING CELL; COMPARATIVE STUDY; ENCAPSULATION; ENDOTHELIAL PROGENITOR CELL; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MOUSE; NONHUMAN; TISSUE ENGINEERING; TRANSPLANTATION; VASCULAR IMPLANT; VASCULARIZATION; WOUND HEALING;

EID: 84876261425     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2012-0111     Document Type: Article

References (45)

1. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003; 9:702-712.
2. 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;106:14990-14995.
3. 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; 108:14789-14794.
4. Caspi O, Lesman A, Basevitch Y et al. Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 2007;100:263-272.
5. Nör JE, Peters MC, Christensen JB et al. Engineering and characterization of functional human microvessels in immunodeficient mice. Lab Invest 2001;81:453-463.
6. Levenberg S, Rouwkema J, Macdonald M et al. Engineering vascularized skeletal muscle tissue. Nat Biotechnol 2005;23:879-884.
7. Wang ZZ, Au P, Chen T et al. Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat Biotechnol 2007;25:317-318.
8. Ferreira LS, Gerecht S, Shieh HF et al. Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res 2007;101: 286-294.
9. Melero-Martin JM, De Obaldia ME, Kang SY et al. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 2008;103:194-202.
10. Au P, Daheron LM, Duda DG et al. Differential in vivo potential of endothelial progenitor cells from human umbilical cord blood and adult peripheral blood to form functional long-lasting vessels. Blood 2008; 111:1302-1305.
11. Critser PJ, Kreger ST, Voytik-Harbin SL et al. Collagen matrix physical properties modulate endothelial colony forming cellderived vessels in vivo. Microvasc Res 2010; 80:23-30.
12. Kang K-T, Allen P, Bischoff J. Bioengineered human vascular networks transplanted into secondary mice reconnect with the host vasculature and re-establish perfusion. Blood 2011;118:6718-6721.
13. Au P, Tam J, Fukumura D et al. Bone marrow derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 2008;111:4551-4558.
14. Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005;23:47-55.
15. Hanjaya-Putra D, Gerecht S. Mending the failing heart with a vascularized cardiac patch. Cell Stem Cell 2009;5:575-576.
16. Phelps EA, Landázuri N, Thulé PMetal. Bioartificial matrices for therapeutic vascularization. Proc Natl Acad Sci USA 2010;107: 3323-3328.
17. Webber MJ, Tongers J, Newcomb CJ et al. Supramolecular nanostructures that mimic VEGF as a strategy for ischemic tissue repair. Proc Natl Acad Sci USA 2011;108:13438- 13443.
18. Chen Y-C, Lin R-Z, Qi H et al. Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels. Adv Funct Mater 2013;22:2027-2039.
19. Moon JJ, Saik JE, Poché RA et al. Biomimetic hydrogels with pro-angiogenic properties. Biomaterials 2010;31:3840-3847.
20. Hanjaya-Putra D, Bose V, Shen Y-I et al. Controlled activation of morphogenesis to generate a functional human microvasculature in a synthetic matrix. Blood 2011;118:804- 815.
21. Hanjaya-Putra D, Wong KT, Hirotsu K et al. Spatial control of cell-mediated degradation to regulate vasculogenesis and angiogenesis in hyaluronan hydrogels. Biomaterials 2012;33: 6123-6131.
22. Gurtner GC, Werner S, Barrandon Y et al. Wound repair and regeneration. Nature 2008; 453:314-321.
23. Tibbs MK. Wound healing following radiation therapy: A review. Radiother Oncol 1997; 42:99-106.
24. Singer AJ, Clark RAF. Cutaneous wound healing. N Engl J Med 1999;341:738-746.
25. Capla JM, Ceradini DJ, Tepper OM et al. Skin graft vascularization involves precisely regulated regression and replacement of endothelial cells through both angiogenesis and vasculogenesis. Plast Reconstr Surg 2006;117: 836-844
26. Bhora FY, Dunkin BJ, Batzri S et al. Effect of growth factors on cell proliferation and epithelialization in human skin. J Surg Res 1995; 59:236-244.
27. Martin P. Wound healing: Aiming for perfect skin regeneration. Science 1997;276:75- 81.
28. Blanpain C, Fuchs E. Epidermal homeostasis: A balancing act of stem cells in the skin. Nat Rev Mol Cell Biol 2009;10:207-217.
29. Sun G, Zhang X, Shen Y-I et al. Dextran hydrogel scaffolds enhance angiogenic responses and promote complete skin regeneration during burn wound healing. Proc Natl Acad Sci USA 2011;108:20976-20981.
30. Kung EF, Wang F, Schechner JS. In vivo perfusion of human skin substitutes with microvessels formed by adult circulating endothelial progenitor cells. Dermatol Surg 2008; 34:137-146.
31. Schechner JS, Nath AK, Zheng L et al. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci USA 2000;97: 9191-9196.
32. Shepherd BR, Enis DR, Wang F et al. Vascularization and engraftment of a human skin substitute using circulating progenitor cell-derived endothelial cells. FASEB J 2006;20:1739- 1741.
33. Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2008;28:1584-1595.
34. Yoder MC, Mead LE, Prater D et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 2007;109:1801-1809.
35. Hanjaya-Putra D, Yee J, Ceci D et al. Vascular endothelial growth factor and substrate mechanics regulate in vitro tubulogenesis of endothelial progenitor cells. J Cell Mol Med 2010;14:2436-2447.
36. Khetan S, Katz JS, Burdick JA. Sequential crosslinking to control cellular spreading in 3-dimensional hydrogels. Soft Matter 2009;5: 1601-1606.
37. Khetan S, Burdick JA. Patterning network structure to spatially control cellular remodeling and stem cell fate within 3-dimensional hydrogels. Biomaterials 2010;31:8228-8234.
38. Zhang X, Wei X, Liu L et al. Association of increasing burn severity in mice with delayed mobilization of circulating angiogenic cells. Arch Surg 2010;145:259-266.
39. Sun G, Shen Y-I, Kusuma S et al. Functional neovascularization of biodegradable dextran hydrogels with multiple angiogenic growth factors. Biomaterials 2011;32:95-106.
40. Robertson D, Savage K, Reis-Filho J et al. Multiple immunofluorescence labelling of formalin-fixed paraffin-embedded (FFPE) tissue. BMC Cell Biol 2008;9:13.
41. Sun G, Shen Y-I, Ho CC et al. Functional groups affect physical and biological properties of dextran-based hydrogels. J Biomed Mater Res A 2010;93:1080-1090.
42. Cheng G, Liao S, Kit Wong H et al. Engineered blood vessel networks connect to host vasculature via wrapping-and-tapping anastomosis. Blood 2011;118:4740-4749.
43. Vo E, Hanjaya-Putra D, Zha Y et al. Smooth-muscle-like cells derived from human embryonic stem cells support and augment cord-like structures in vitro. Stem Cell Rev 2010;6:237-247.
44. Wanjare M, Kuo F, Gerecht S. Derivation and maturation of synthetic and contractile vascular smooth muscle cells from human pluripotent stem cells. Cardiovasc Res 2013;97: 321-330.
45. Skardal A, Mack D, Kapetanovic E et al. Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. STEM CELLS TRANSLATIONAL MEDICINE 2012;1:792-802.