Scarring, stem cells, scaffolds and skin repair

Journal of Tissue Engineering and Regenerative Medicine

Volumn 9, Issue 6, 2015, Pages 649-668

  Markeson, Daniel ^a,b,c,d   Pleat, Jonathon M ^b,e   Sharpe, Justin R ^f   Harris, Adrian L ^g   Seifalian, Alexander M ^d   Watt, Suzanne M ^a,c  

^a NHS BLOOD AND TRANSPLANT   (United Kingdom)

^b STOKE MANDEVILLE HOSPITAL   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d LONDON CENTRE FOR NANOTECHNOLOGY   (United Kingdom)

^e FRENCHAY HOSPITAL   (United Kingdom)

^f QUEEN VICTORIA HOSPITAL   (United Kingdom)

^g UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Burns; ECFCs; Revascularization; Scaffolds; Skin repair; Stem cells

Indexed keywords

MORPHOLOGY; REPAIR; SCAFFOLDS (BIOLOGY); TISSUE; TISSUE REGENERATION;

'CURRENT; BURN; CELL SCAFFOLD; ECFC; ENGINEERED-SUBSTRATE; FUNCTIONAL DEMANDS; IN-VIVO; REVASCULARIZATION; SKIN REPAIR; STEM-CELL;

STEM CELLS;

BIOMATERIAL;

ANGIOGENESIS; AUTOLOGOUS STEM CELL TRANSPLANTATION; BURN; BURN CONTRACTURE; CELL RENEWAL; DERMIS; EPIDERMIS; EPIDERMIS CELL; FULL THICKNESS SKIN GRAFT; HUMAN; HUMAN CELL; IN VIVO STUDY; MORPHOLOGY; PHENOTYPE; PRIORITY JOURNAL; REVASCULARIZATION; REVIEW; SCAR FORMATION; SKIN CELL; SKIN DEFECT; SKIN SCAR; SKIN TRANSPLANTATION; STEM CELL; STEM CELL NICHE; TISSUE ENGINEERING; TISSUE SCAFFOLD; WOUND HEALING; ANIMAL; CHEMISTRY; CYTOLOGY; PATHOLOGY; SCAR; SKIN;

ANIMALS; CICATRIX; HUMANS; SKIN; STEM CELL NICHE; STEM CELLS; TISSUE SCAFFOLDS; WOUND HEALING;

EID: 84931005735     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.1841     Document Type: Review

References (124)

1. Adamakis I, Tyritzis SI, Stravodimos KG et al. 2011; A novel approach for the surgical management of Peyronie's disease using an acellular, human dermis tissue graft: preliminary results. World J Urol 29: 399-403.
2. Ahn CS, Maitz PKM. 2012; The true cost of burn. Burns 38: 967-974.
3. Alekseeva T, Hadjipanayi E, Abou Neel E et al. 2012; Engineering stable topography in dense bio-mimetic 3D collagen scaffolds. Euro Cell Mater 23: 28-40.
4. Ananta M, Brown RA, Mudera V. 2012; A rapid fabricated living dermal equivalent for skin tissue engineering: an in vivo evaluation in an acute wound model. Tissue Eng Part A 18: 353-61.
5. Arneja JS, Gosain AK. 2005; Giant congenital melanocytic nevi of the trunk and an algorithm for treatment. J Craniofac Surg 16(5): 886-893.
6. Athanassopoulos A, Tsaknakis G, Newey SE et al. 2012; Microvessel networks in pre-formed in artificial clinical grade dermal substitutes in vitro using cells from haematopoietic tissues. Burns 38: 691-701.
7. Auger FA, Lacroix D, Germain L. 2009; Skin substitutes and wound healing. Skin Pharm Physiol 22: 94-102.
8. Beckstrøm KJ, Brinchmann JE. 2012; Human adipose tissue as a source of cells with angiogenic potential. Cell Transplant 21: 235-250.
9. Behrens DT, Villone D, Koch M et al. 2012; The epidermal basement membrane is a composite of separate laminin- or collagen IV-containing networks connected by aggregated perlecan, but not by nidogens. J Biol Chem 287: 18700-18709.
10. Biedermann T, Pontiggia L, Böttcher-Haberzeth S et al. 2010; Human eccrine sweat gland cells can reconstitute a stratified epidermis. J Invest Dermatol 133: 316-324.
11. Bikle DD. 2011; Vitamin D metabolism and function in the skin. Molec Cell Endocrin 347: 80-89.
12. Blanpain C, Lowry WE, Geoghegan A et al. 2004; Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118: 635-648.
13. Bompais H, Chagraoui J, Canron X et al. 2004; Human endothelial cells derived from circulating progenitors display specific functional properties compared with mature vessel wall endothelial cells. Blood 103: 2577-2584.
14. Böttcher-Haberzeth S, Biedermann T, Schiestl C et al. 2012; Matriderm Ò 1mm versus Integra Ò Single Layer 1.3mm for one-step closure of full thickness skin defects: a comparative experimental study in rats. Pediatr Surg Int 28: 171-7.
15. Brown BC, Moss TP, McGrouther DA et al. 2010; Skin scar preconceptions must be challenged: importance of self-perception in skin scarring. JPRAS 63: 1022-1029.
16. Brown JJ, Bayat A. 2009; Genetic susceptibility to raised dermal scarring. Br J Dermatol 161: 8-18.
17. Carletti E, Motta A, Migliaresi C. 2011; Scaffolds for tissue engineering and 3D cell culture. Methods Mol Biol 695: 17-39.
18. Case J, Mead LE, Bessler WK et al. 2007; Human CD34+AC133+VEGFR-2+ cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp Hematol 35: 1109-1118.
19. Cervelli V, Lucarini L, Cerretani C et al. 2010; The use of MatriDerm® and skin grafting in post-traumatic wounds. Int Wound J 7: 400-405.
20. Chan YC, Roy S, Khanna S et al. 2012; Downregulation of endothelial microRNA-200b supports cutaneous wound angiogenesis by desilencing GATA binding protein 2 and vascular endothelial growth factor receptor 2. Arterioscl Thromb Vasc Biol 32: 1372-1382.
21. Chaucer G. 1385; Troilus & Criseyde. Available at: http://ebooks.gutenberg.us/DjVu_Collection/DJEDS/CHAUCER/TROILUS/Download.pdf, Accessed 3 February 2013.
22. Chen X, Aledia AS, Ghajar CM et al. 2009; Prevascularization of a fibrin-based tissue construct accelerates the formation of functional anastomosis with host vasculature. Tissue Eng Part A 15: 1363-1371.
23. Cheng G, Liao S, Kit Wong H et al. 2011; Engineered blood vessel networks connect to host vasculature via wrapping-and-tapping anastomosis. Blood 118: 4740-4749.
24. Coldwell KE, Lee SJ, Kean J et al. 2011; Effects of obstetric factors and storage temperatures on the yield of endothelial colony forming cells from umbilical cord blood. Angiogenesis 14: 381-392.
25. Critser PJ, Kreger ST, Voytik-Harbin SL et al. 2010; Collagen matrix physical properties modulate endothelial colony forming cell-derived vessels in vivo. Microvasc Res 80: 23-30.
26. Critser PJ, Voytik-Harbin SL, Yoder MC. 2011; Isolating and defining cells to engineer human blood vessels. Cell Prolif 44(Suppl 1): 15-21.
27. Cubison TCS, Pape SA, Parkhouse N. 2006; Evidence for the link between healing time and the development of hypertrophic scars (HTS) in paediatric burns due to scald injury. Burns 32: 992-999.
28. Culliford A IV, Hazan A. 2007; Dermatology for plastic surgeons. In Grabb and Smith's Plastic Surgery, 5th edn. Lippincott Williams & Wilkins: Philadelphia, USA; 105.
29. Danner S, Kremer M, Petschnik AE et al. 2012; The use of human sweat gland-derived stem cells for enhancing vascularisation during dermal regeneration. J Invest Dermatol 132: 1707-1716.
30. des Rieux A, Ucakar B, Mupendwa BPK et al. 2011; 3D systems delivering VEGF to promote angiogenesis for tissue engineering. J Control Release 150: 272-278.
31. Ema H, Suda T. 2012; Two anatomically distinct niches regulate stem cell activity. Blood 120: 2174-2181.
32. Engelhardt S, Hoch E, Borchers K et al. 2011; Fabrication of 2D protein microstructures and 3D polymer-protein hybrid microstructures by two-photon polymerization. Biofabrication 3: 025003.
33. Fuchs E. 2007; Scratching the surface of skin development. Nature 445: 834-842.
34. Fuchs E, Chen T. 2013; A matter of life and death: self-renewal in stem cells. EMBO Rep 14(1): 39-48.
35. Gerlach JC, Johnen C, Ottoman C et al. 2011; Method for autologous single skin cell isolation for regenerative cell spray transplantation with non-cultured cells. Int J Artif Organs 34: 271-279.
36. Gosain AK, Santoro TD, Larson DL et al. 2001; Giant congenital nevi: a 20-year experience and an algorithm for their management. Plast Reconstr Surg 108: 622-636.
37. Gravante G, Delogu D, Giordan N et al. 2007; The use of Hyalomatrix PA in the treatment of deep partial-thickness burns. J Burn Care Res 28: 269-274.
38. Gravante G, Sorge R, Merone A et al. 2010; Hyalomatrix PA in burn care practice: results from a national retrospective survey, 2005-2006. Ann Plast Surg 64: 69-79.
39. Gulati R, Jevremovic D, Peterson TE et al. 2003; Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circ Res 93: 1023-1025.
40. Hadjipanayi E, Cheema U, Mudera V et al. 2011; First implantable device for hypoxia-mediated angiogenic induction. J Control Release 153: 217-224.
41. Harding KG, Morris HL, Patel GK. 2002; Science, medicine and the future: healing chronic wounds. BMJ 324: 160-163.
42. Hansbrough JF, Cooper ML, Cohen R, et al. 1992; Evaluation of a biodegradable matrix containing cultured human fibroblasts as a dermal replacement beneath meshed skin grafts on athymic mice. Surgery 111: 438-446.
43. Hegen A, Blois A, Tiron CE et al. 2011; Efficient in vivo vascularisation of tissue-engineering scaffolds. J Tissue Eng Regen Med 5: e52-e62.
44. Heitland A, Piatkowski A, Noah EM et al. 2004; Update on the use of collagen/glycosaminoglycate skin substitute-six years of experiences with artificial skin in 15 German burn centers. Burns 30: 471-475.
45. Helary C, Bataille I, Abed A et al. 2010; Concentrated collagen hydrogels as dermal substitutes. Biomaterials 31(3): 481-490.
46. Hendrickx B, Verdonck K, Van den Berge S et al. 2010; Integration of blood outgrowth endothelial cells in dermal fibroblast sheets promotes full thickness wound healing. Stem Cells 28: 1165-1177.
47. Hendrickx B, Vranckx JJ, Luttun A. 2011; Cell-based vascularization strategies for skin tissue engineering. Tissue Eng Part B 17: 13-24.
48. Hettiaratchy S, Dziewulski P. 2005; Introduction. In ABC of Burns, Hettiaratchy S, Papini R, Dziewulski P (eds). Wiley-Blackwell: Malden, MA, USA; 1-3.
49. Hill JM, Zalos G, Halcox JPJ et al. 2003; Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. NEJM 348: 593-600.
50. Hofmann NA, Reinisch A, Strunk D. 2009; Isolation and large scale expansion of adult human endothelial colony forming progenitor cells. J Vis Exp 28: 1-2.
51. Hogg P, Rooney P, Ingham E et al. 2012; Development of a decellularised dermis. Cell Tissue Banking 14: 465-474.
52. Hur J, Yoon CH, Kim HS et al. 2004; Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler 24(2): 288-293.
53. Ingram DA, Mead LE, Tanaka H et al. 2004; Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104: 2752-2760.
54. Ingram DA, Mead LE, Moore DB et al. 2005; Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 105: 2783-2786.
55. Janssens AS, Heide R, Den Hollander JC et al. 2005; Mast cell distribution in normal adult skin. J Clin Pathol 58: 285-289.
56. Karvonen SL, Vaajalahti P, Marenk M et al. 1992; Birthmarks in 4346 Finnish newborns. Acta Derm Venereol 72: 55-57.
57. Koenen W, Felcht M, Vockenroth K et al. 2011; One-stage reconstruction of deep facial defects with a single layer dermal regeneration template. J Eur Acad Dermatol Venereol 25: 788-793.
58. Koike N, Fukumura D, Gralla O et al. 2004; Tissue engineering: creation of long-lasting blood vessels. Nature 428: 138-139.
59. Kopp J, Magnus Noah E, Rübben A et al. 2003; Radical resection of giant congenital melanocytic nevus and reconstruction with meek-graft covered integra dermal template. Dermatol Surg 29: 653-657.
60. Krueger J, Liu D, Scholz K et al. 2011; Flt1 acts as a negative regulator of tip cell formation and branching morphogenesis in the zebrafish embryo. Devel Camb Eng 138: 2111-2120.
61. Lin RZ, Dreyzin A, Aamodt K et al. 2011; Functional endothelial progenitor cells from cryopreserved umbilical cord blood. Cell Transplant 20: 515-522.
62. Lin RZ, Moreno-Luna R, Muñoz-Hernandez R et al. 2013; Human white adipose tissue vasculature contains endothelial colony-forming cells with robust in vivo vasculogenic potential. Angiogenesis 16(4): 735-744.
63. Lin Y, Weisdorf DJ, Solovey A et al. 2000; Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105: 71-77.
64. Lu CP, Polak L, Rocha AS et al. 2012; Identification of stem cell populations in sweat glands and ducts reveals roles in homeostasis and wound repair. Cell 150: 136-150.
65. Macleod TM, Williams G, Sanders R et al. 2005; Histological evaluation of Permacol as a subcutaneous implant over a 20-week period in the rat model. Br J Plast Surg 58: 518-532.
66. MacNeil S. 2007; Progress and opportunities for tissue-engineered skin. Nature 445: 874-880.
67. Marston WA, Hanft J, Norwood P et al. 2003; The efficacy and safety of Dermagraft in improving the healing of chronic diabetic foot ulcers: results of a prospective randomized trial. Diabetes Care 26: 1701-1705.
68. Mascré G, Dekoninck S, Drogat B et al. 2012; Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 489: 257-262.
69. Mead LE, Prater D, Yoder MC et al. 2008; Isolation and characterization of endothelial progenitor cells from human blood. Curr Protoc Stem Cell Biol Chapter 2: Unit 2C.
70. Melchels FPW, Barradas AMC, Van Blitterswijk CA et al. 2010; Effects of the architecture of tissue engineering scaffolds on cell seeding and culturing. Acta Biomat 7: 3432-3445.
71. Melero-Martin JM, Khan ZA, Picard A et al. 2007; In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood 109: 4761-4768.
72. Melero-Martin JM, De Obaldia ME, Kang S-Y et al. 2008; Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 103: 194-202.
73. Montaño I, Schiestl C, Schneider J et al. 2010; Formation of human capillaries in vitro: the engineering of prevascularized matrices. Tissue Eng Part A 16: 269-282.
74. Moustafa M, Bullock AJ, Creagh FM et al. 2007; Randomized, controlled, single-blind study on use of autologous keratinocytes on a transfer dressing to treat nonhealing diabetic ulcers. Regen Med 2: 887-902.
75. Mukai N, Akahori T, Komaki M et al. 2008; A comparison of the tube forming potentials of early and late endothelial progenitor cells. Exp Cell Res 314: 430-440.
76. Munster AM 1996; Cultured skin for massive burns. A prospective controlled trial. Ann Surg 224(3): 372-377.
77. Orlando G, Wood K, De Coppi P et al. 2012; Regenerative medicine as applied to general surgery. Ann Surg 255: 867-880.
78. Pan W, Pham VN, Stratman AN et al. 2012; CDP-diacylglycerol synthetase-controlled phosphoinositide availability limits VEGFA signaling and vascular morphogenesis. Blood 120: 489-498.
79. Pankov R. 2002; Fibronectin at a glance. J Cell Sci 115: 3861-3863.
80. Paquet-Fifield S, Schlüter H, Li A, et al. 2009; A role for pericytes as microenvironmental regulators of human skin tissue regeneration. J Clin Invest 119: 2795-806.
81. Pham C, Greenwood J, Cleland H et al. 2007; Bioengineered skin substitutes for the management of burns: a systematic review. Burns 33: 946-957.
82. Plikus MV, Gay DL, Treffeisen E et al. 2012; Epithelial stem cells and implications for wound repair. Semin Cell Dev Biol 23: 946-953.
83. Rao RR, Peterson AW, Ceccarelli J et al. 2012; Matrix composition regulates three-dimensional network formation by endothelial cells and mesenchymal stem cells in collagen/fibrin materials. Angiogenesis 15: 253-264.
84. Reinisch A, Strunk D. 2009; Isolation and animal serum free expansion of human umbilical cord derived mesenchymal stromal cells (MSCs) and endothelial colony forming progenitor cells (ECFCs). J Vis Exp 32: 3-6.
85. Rittié L, Sachs DL, Orringer JS et al. 2013; Eccrine sweat glands are major contributors to reepithelialization of human wounds. Am J Pathol 182: 163-171.
86. Roubelakis MG, Tsaknakis G, Pappa KI et al. 2013; Spindle shaped human mesenchymal stem/stromal cells from amniotic fluid promote neovascularization. PLoS One 8: 1-15.
87. Rnjak J, Wise SG, Mithieux SM et al. 2011; Severe burn injuries and the role of elastin in the design of dermal substitutes. Tissue Eng Part B Rev 17: 81-91.
88. Rössner E, Smith MD, Petschke B et al. 2011; Epiflex® a new decellularised human skin tissue transplant: manufacture and properties. Cell Tissue Bank 12: 209-217.
89. Roy S, Sen CK. 2011; miRNA in wound inflammation and angiogenesis. Microcirculation 19: 224-232.
90. Ryssel H, Gazyakan E, Germann G et al. 2008; The use of MatriDerm in early excision and simultaneous autologous skin grafting in burns - a pilot study. Burns 34: 93-97.
91. Ryssel H, Radu CA, Germann G et al. 2010; Single-stage Matriderm® and skin grafting as an alternative reconstruction in high-voltage injuries. Int Wound J 7: 385-392.
92. Sakaguchi K, Shimizu T, Horaguchi S et al. 2013; In vitro engineering of vascularized tissue surrogates. Sci Rep 3: 1-7.
93. Sanz L, Santos-Valle P, Alonso-Camino V et al. 2008; Long-term in vivo imaging of human angiogenesis: critical role of bone marrow-derived mesenchymal stem cells for the generation of durable blood vessels. Microvasc Res 75: 308-314.
94. Schechner JS, Nath AK, Zheng L et al. 2000; In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci U S A 97: 9191-9196.
95. Sekine H, Shimizu T, Sakaguchi K et al. 2013; In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels. Nature Comm 4: 1-10.
96. Shelley WC, Leapley AC, Huang L et al. 2012; Changes in the frequency and in vivo vessel-forming ability of rhesus monkey circulating endothelial colony-forming cells across the lifespan (birth to aged). Ped Res 71: 156-161.
97. Shevchenko RV, James SL, James SE. 2010; A review of tissue-engineered skin bioconstructs available for skin reconstruction. J Roy Soc Interface 7: 229-258.
98. Stahl A, Wu X, Wenger A et al. 2005; Endothelial progenitor cell sprouting in spheroid cultures is resistant to inhibition by osteoblasts: a model for bone replacement grafts. FEBS lett 579: 5338-5342.
99. Stratman AN, Davis GE. 2012; Endothelial cell-pericyte interactions stimulate basement membrane matrix assembly: influence on vascular tube remodeling, maturation, and stabilization. Microsc Microanal 18: 68-80.
100. Stratman AN, Davis MJ, Davis GE. 2011; VEGF and FGF prime vascular tube morphogenesis and sprouting directed by hematopoietic stem cell cytokines. Blood 117: 3709-3719.
101. Sun G, Zhang X, Shen Y-I et al. 2011; Dextran hydrogel scaffolds enhance angiogenic responses and promote complete skin regeneration during burn wound healing. Proc Natl Acad Sci U S A 108: 20976-20981.
102. Szöke K, Beckstrøm KJ, Brinchmann JE. 2012; Human adipose tissue as a source of cells with angiogenic potential. Cell Transplant 21: 235-250.
103. + hematopoietic precursors. Arterioscler Thrombosis Vasc Biol 27: 1572-1579.
104. Tonello C, Vindigni V, Zavan B et al. 2005; In vitro reconstruction of an endothelialized skin substitute provided with a microcapillary network using biopolymer scaffolds. FASEB J 19: 1546-1548.
105. Travia G, Palmisano PA, Cervelli V et al. 2003; The use of fibroblast and keratinocyte cultures in burns treatment. Ann Burns Fire Disast XVI. Available at: http://www.medbc.com/annals/review/vol_16/num_1/text/vol16n1p19.asp, Accessed 5 October 2013.
106. Tremblay P-L, Hudon V, Berthod F et al. 2005; Inosculation of tissue-engineered capillaries with the host's vasculature in a reconstructed skin transplanted on mice. Am J Transplant 5: 1002-1010.
107. Tumbar T, Guasch G, Greco V et al. 2004; Defining the epithelial stem cell niche in skin. Science 20: 359-363.
108. Tura O, Skinner EM, Robin Barclay G et al. 2013; Late outgrowth endothelial cells resemble mature endothelial cells and are not derived from bone marrow. Stem Cells 31: 338-348.
109. Van Keymeulen A, Blanpain C. 2012; Tracing epithelial stem cells during development, homeostasis, and repair. J Cell Biol 197: 575-584.
110. Velazquez E, Murphy GF. 2009; Histopathology of the Skin, 10th edn. Lippincott Williams and Wilkins: Philadelphia, USA; 38-50.
111. Wainwright DJ, Bury SB. 2011; Acellular dermal matrix in the management of the burn patient. Aesthet Surg J 31(7 Suppl): 13S-23S.
112. Watt FM, Jensen KB. 2009; Epidermal stem cell diversity and quiescence. EMBO Mol Med 1: 260-267.
113. Watt SM, Athanassopoulos A, Harris AL et al. 2010; Human endothelial stem/progenitor cells, angiogenic factors and vascular repair. J R Soc Interface 7: S731-S751.
114. Watt SM, Gullo F, Van der Garde M et al. 2013; The angiogenic properties of mesenchymal stem/stromal cells and their therapeutic potential. Br Med Bull (in press).
115. Waymack P, Duff RG, Sabolinski M. 2000; The effect of a tissue engineered bilayered living skin analog, over meshed split-thickness autografts on the healing of excised burn wounds. Burns 26: 609-619.
116. Wells C. 2012. Skin and Wound Care Manual Online. Available at: http://westernhealth.nl.ca/uploads/PDFs/woundcaremanualfordianneclementsfinal.pdf, Accessed 5 October 2013.
117. Wood JA, Colletti E, Mead LE et al. 2012; Distinct contribution of human cord blood-derived endothelial colony forming cells to liver and gut in a fetal sheep model. Hepatol 56(3): 1086-1096.
118. Wu X, Rabkin-Aikawa E, Guleserian KJ et al. 2004; Tissue-engineered microvessels on three-dimensional biodegradable scaffolds using human endothelial progenitor cells. Am J Physiol Heart Circ Physiol 287: H480-H487.
119. Yee D, Hanjaya-Putra D, Bose V et al. 2011; Hyaluronic acid hydrogels support cord-like structures from endothelial colony-forming cells. Tissue Eng Part A 17: 1351-1361.
120. Yildirimer L, Thanh NTK, Seifalian AM. 2012; Skin regeneration scaffolds: a multimodal bottom-up approach. Trends Biotechnol 30: 638-648.
121. Yoder MC. 2012; Human endothelial progenitor cells. Cold Spring Harb Perspec Med 2(7): 1-15.
122. Yoder MC. 2013; Endothelial progenitor cell: a blood cell by many other names may serve similar functions. J Mol Med 91: 285-295.
123. Yoder MC, Mead LE, Prater D et al. 2007; Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109: 1801-1809.
124. Zhang Y, Fisher N, Newey SE et al. 2009; The impact of proliferative potential of umbilical cord-derived endothelial progenitor cells and hypoxia on vascular tubule formation in vitro. Stem Cells Dev 18: 359-375.