Vascularization and engraftment of a human skin substitute using circulating progenitor cell-derived endothelial cells

FASEB Journal

Volumn 20, Issue 10, 2006, Pages

  Shepherd, Benjamin R ^a   Enis, David R ^a   Wang, Feiya ^a,b   Suarez, Yajaira ^a   Pober, Jordan S ^a,c   Schechner, Jeffrey S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Endothelial progenitor cell; Leukapheresis; Tissue engineering; Umbilical cord blood

Indexed keywords

ALPHA ACTIN; PROTEIN BCL 2; RAPAMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MATURATION; CELL SPECIFICITY; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; KERATINOCYTE; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN BLOOD FLOW; SKIN GRAFT; SKIN TRANSPLANTATION; STEM CELL; UMBILICAL CORD BLOOD; ANGIOGENESIS; ANIMAL; ARTIFICIAL SKIN; CYTOLOGY; GENETIC TRANSDUCTION; GENETICS; METHODOLOGY; MOUSE MUTANT; TISSUE ENGINEERING; VASCULAR ENDOTHELIUM; XENOGRAFT;

ANIMALS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; MICE; MICE, SCID; NEOVASCULARIZATION, PHYSIOLOGIC; PROTO-ONCOGENE PROTEINS C-BCL-2; SIROLIMUS; SKIN, ARTIFICIAL; STEM CELLS; TISSUE ENGINEERING; TRANSDUCTION, GENETIC; TRANSPLANTATION, HETEROLOGOUS;

EID: 33845661462     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-5682fje     Document Type: Article

References (39)

1. Phillips, T. J., Manzoor, J., Rojas, A., Isaacs, C., Carson, P., Sabolinski, M., Young, J., Falanga, V. (2002) The longevity of a bilayered skin substitute after application to venous ulcers. Arch. Dermatol. 138, 1079-1081
2. Boyce, S. T., Goretsky, M. J., Greenhalgh, D. G., Kagan, R. J., Rieman, M. T., Warden, G. D. (1995) Comparative assessment of cultured skin substitutes and native skin autograft for treatment of full-thickness burns. Ann. Surg. 222, 743-752
3. Curran, M. P., Plosker, G. L. (2002) Bilayered bioengineered skin substitute (Apligraf): a review of its use in the treatment of venous leg ulcers and diabetic foot ulcers. BioDrugs 16, 439-455
4. Lambert, P. B. (1971) Vascularization of skin grafts. Nature 232, 279-280
5. Krejci, N. C., Cuono, C. B., Langdon, R. C., McGuire, J. (1991) In vitro reconstitution of skin: fibroblasts facilitate keratinocyte growth and differentiation on acellular reticular dermis. J. Invest Dermatol. 97, 843-848
6. Demarchez, M., Hartmann, D. J., Regnier, M., Asselineau, D. (1992) The role of fibroblasts in dermal vascularization and remodeling of reconstructed human skin after transplantation onto the nude mouse. Transplantation 54, 317-326
7. Medalie, D. A., Eming, S. A., Tompkins, R. G., Yarmush, M. L., Krueger, G. G., Morgan, J. R. (1996) Evaluation of human skin reconstituted from composite grafts of cultured keratinocytes and human acellular dermis transplanted to athymic mice. J. Invest. Dermatol. 107, 121-127
8. Sivan-Loukianova, E., Awad, O. A., Stepanovic, V., Bickenbach, J., Schatteman, G. C. (2003) CD34+ blood cells accelerate vascularization and healing of diabetic mouse skin wounds. J. Vasc. Res. 40, 368-377
9. Young, D. M., Greulich, K. M., Weier, H. G. (1996) Species-specific in situ hybridization with fluorochrome-labeled DNA probes to study vascularization of human skin grafts on athymic mice. J. Burn Care Rehabil. 17, 305-310
10. Supp, D. M., Supp, A. P., Bell, S. M., Boyce, S. T. (2000) Enhanced vascularization of cultured skin substitutes genetically modified to overexpress vascular endothelial growth factor. J. Invest Dermatol. 114, 5-13
11. Black, A. F., Berthod, F., L'heureux, N., Germain, L., Auger, F. A. (1998) In vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. FASEB J. 12, 1331-1340
12. Kearney, J. N. (2001) Clinical evaluation of skin substitutes. Burns 27, 545-551
13. Supp, D. M., Wilson-Landy, K., Boyce, S. T. (2002) Human dermal microvascular endothelial cells form vascular analogs in cultured skin substitutes after grafting to athymic mice. FASEB J. 16, 797-804
14. Drosou, A., Kirsner, R. S., Kato, T., Mittal, N., Al Niami, A., Miller, B., Tzakis, A. G. (2005) Use of a bioengineered skin equivalent for the management of difficult skin defects after pediatric multivisceral transplantation. J. Am. Acad. Dermatol. 52, 854-858
15. Marston, W. A. (2004) Dermagraft, a bioengineered human dermal equivalent for the treatment of chronic nonhealing diabetic foot ulcer. Expert. Rev. Med. Devices. 1, 21-31
16. Greenberg, S., Margulis, A., Garlick, J. A. (2005) In vivo transplantation of engineered human skin. Methods Mol. Biol. 289, 425-430
17. Tremblay, P. L., Hudon, V., Berthod, F., Germain, L., Auger, F. A. (2005) Inosculation of tissue-engineered capillaries with the host's vasculature in a reconstructed skin transplanted on mice. Am. J. Transplant. 5, 1002-1010
18. Schechner, J. S., Crane, S. K., Wang, F., Szeglin, A. M., Tellides, G., Lorber, M. I., Bothwell, A. L., Pober, J. S. (2003) Engraftment of a vascularized human skin equivalent. FASEB J. 17, 2250-2256
19. Schechner, J. S., Nath, A. K., Zheng, L., Kluger, M. S., Hughes, C. C., Sierra-Honigmann, M. R., Lorber, M. I., Tellides, G., Kashgarian, M., Bothwell, A. L., Pober, J. S. (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
20. Enis, D. R., Shepherd, B. R., Wang, Y., Qasim, A., Shanahan, C. M., Weissberg, P. L., Kashgarian, M., Pober, J. S., Schechner, J. S. (2005) Induction, differentiation, and remodeling of blood vessels after transplantation of Bcl-2-transduced endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 102, 425-430
21. Pober, J. S., Collins, T., Gimbrone, M. A., Jr., Cotran, R. S., Gitlin, J. D., Fiers, W., Clayberger, C., Krensky, A. M., Burakoff, S. J., Reiss, C. S. (1983) Lymphocytes recognize human vascular endothelial and dermal fibroblast Ia antigens induced by recombinant immune interferon. Nature 305, 726-729
22. Morhenn, V. B., Nickoloff, B. J. (1987) Interleukin-2 stimulates resting human T lymphocytes' response to allogeneic, gamma interferon-treated keratinocytes. J. Invest. Dermatol. 89, 464-468
23. Zheng, L., Dengler, T. J., Kluger, M. S., Madge, L. A., Schechner, J. S., Maher, S. E., Pober, J. S., Bothwell, A. L. (2000) Cytoprotection of human umbilical vein endothelial cells against apoptosis and CTL-mediated lysis provided by caspaseresistant Bcl-2 without alterations in growth or activation responses. J. Immunol. 164, 4665-4671
24. Zheng, L., Gibson, T. F., Schechner, J. S., Pober, J. S., Bothwell, A. L. (2004) Bcl-2 transduction protects human endothelial cell synthetic microvessel grafts from allogeneic T cells in vivo. J. Immunol. 173, 3020-3026
25. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der, Z. R., Li, T., Witzenbichler, B., Schatteman, G., Isner, J. M. (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275, 964-967
26. Asahara, T., Masuda, H., Takahashi, T., Kalka, C., Pastore, C., Silver, M., Kearne, M., Magner, M., Isner, J. M. (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 85, 221-228
27. Crosby, J. R., Kaminski, W. E., Schatteman, G., Martin, P. J., Raines, E. W., Seifert, R. A., Bowen-Pope, D. F. (2000) Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ. Res. 87, 728-730
28. Kocher, A. A., Schuster, M. D., Szabolcs, M. J., Takuma, S., Burkhoff, D., Wang, J., Homma, S., Edwards, N. M., Itescu, S. (2001) Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat. Med. 7, 430-436
29. Gehling, U. M., Ergun, S., Schumacher, U., Wagener, C., Pantel, K., Otte, M., Schuch, G., Schafhausen, P., Mende, T., Kilic, N., et al. (2000) In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95, 3106-3112
30. Peichev, M., Naiyer, A. J., Pereira, D., Zhu, Z., Lane, W. J., Williams, M., Oz, M. C., Hicklin, D. J., Witte, L., Moore, M. A., Rafii, S. (2000) Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 95, 952-958
31. Hristov, M., Erl, W., Weber, P. C. (2003) Endothelial progenitor cells: isolation and characterization. Trends Cardiovasc. Med. 13, 201-206
32. Harraz, M., Jiao, C., Hanlon, H. D., Hartley, R. S., Schatteman, G. C. (2001) Stem Cells 19, 304-312
33. Rehman, J., Li, J., Orschell, C. M., March, K. L. (2003) Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107, 1164-1169
34. Lin, Y., Weisdorf, D. J., Solovey, A., Hebbel, R. P. (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J. Clin. Invest. 105, 71-77
35. Gimbrone, M. A., Jr., Cotran, R. S., Folkman, J. (1974) Human vascular endothelial cells in culture. Growth and DNA synthesis. J. Cell Biol. 60, 673-684
36. Thomson, A. W., Woo, J. (1989) Immunosuppressive properties of FK-506 and rapamycin. Lancet 2, 443-444
37. Kuypers, D. R. (2005) Benefit-risk assessment of sirolimus in renal transplantation. Drug Saf. 28, 153-181
38. Guilbeau, J. M. (2002) Delayed wound healing with sirolimus after liver transplant. Ann. Pharmacother. 36, 1391-1395
39. Wu, X., Rabkin-Aikawa, E., Guleserian, K. J., Perry, T. E., Masuda, Y., Sutherland, F. W., Schoen, F. J., Mayer, J. E., Jr., Bischoff, J. (2004) Tissue-engineered microvessels on threedimensional biodegradable scaffolds using human endothelial progenitor cells. Am. J. Physiol. Heart Circ. Physiol. 287, H480-H487