Lessons from developmental biology for regenerative medicine

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 99, Issue 3, 2013, Pages 149-159

  Turner, Neill J ^a,b   Keane, Timothy J ^a,c   Badylak, Stephen F ^a,b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c University of Pittsburgh   (United States)

Author keywords

Developmental biology; Regenerative medicine; Tissue engineering

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN 2; GLYCOSAMINOGLYCAN; GROWTH FACTOR; INFUSE; OSTEOGENIC PROTEIN 1; PROTEOGLYCAN; UNCLASSIFIED DRUG; WNT PROTEIN;

BONE GRAFT; BONE MARROW TRANSPLANTATION; CELL FUNCTION; CELL PROLIFERATION; CHONDROCYTE IMPLANTATION; DEVELOPMENTAL BIOLOGY; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; FETUS DEVELOPMENT; HEMATOPOIETIC STEM CELL; HUMAN; INNATE IMMUNITY; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MORPHOGENESIS; NEURAL STEM CELL; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL TRANSPLANTATION; TISSUE REGENERATION;

DEVELOPMENTAL BIOLOGY; REGENERATIVE MEDICINE; TISSUE ENGINEERING;

BIOCOMPATIBLE MATERIALS; DEVELOPMENTAL BIOLOGY; HUMANS; IMMUNE SYSTEM; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION; STEM CELLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84884926133     PISSN: 1542975X     EISSN: 15429768     Source Type: Journal    
DOI: 10.1002/bdrc.21040     Document Type: Review

References (189)

1. Agrawal V, Johnson SA, Reing J, et al. 2010. Epimorphic regeneration approach to tissue replacement in adult mammals. Proc Natl Acad Sci USA 107:3351-3355.
2. Agrawal V, Tottey S, Johnson SA, et al. 2011. Recruitment of progenitor cells by an extracellular matrix cryptic peptide in a mouse model of digit amputation. Tissue Eng Part A 17:2435-2443.
3. Aleckovic M, Simon C. 2008. Is teratoma formation in stem cell research a characterization tool or a window to developmental biology? Reprod Biomed Online 17:270-280.
4. Allan CH, Fleckman P, Fernandes RJ, et al. 2006. Tissue response and Msx1 expression after human fetal digit tip amputation in vitro. Wound Repair Regen 14:398-404.
5. Arnold L, Henry A, Poron F, et al. 2007. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204:1057-1069.
6. Ashcroft GS, Horan MA, Ferguson MW. 1997. Aging is associated with reduced deposition of specific extracellular matrix components, an upregulation of angiogenesis, and an altered inflammatory response in a murine incisional wound healing model. J Invest Dermatol 108:430-437.
7. Atala A, Bauer SB, Soker S, et al. 2006. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 367:1241-1246.
8. Au P, Hursh DA, Lim A, et al. 2012. FDA oversight of cell therapy clinical trials. Sci Transl Med 4:149fs131.
9. Austin L, Bower J, Kurek J, Vakakis N. 1992. Effects of leukaemia inhibitory factor and other cytokines on murine and human myoblast proliferation. J Neurol Sci 112:185-191.
10. Badylak S, Liang A, Record R, et al. 1999. Endothelial cell adherence to small intestinal submucosa: an acellular bioscaffold. Biomaterials 20:2257-2263.
11. Badylak SF. 2007. The extracellular matrix as a biologic scaffold material. Biomaterials 28:3587-3593.
12. Badylak SF, Gilbert TW. 2008. Immune response to biologic scaffold materials. Semin Immunol 20:109-116.
13. Badylak SF, Hoppo T, Nieponice A, et al. 2011a. Esophageal preservation in five male patients after endoscopic inner-layer circumferential resection in the setting of superficial cancer: a regenerative medicine approach with a biologic scaffold. Tissue Eng Part A 17:1643-1650.
14. Badylak SF, Lantz GC, Coffey A, Geddes LA. 1989. Small intestinal submucosa as a large diameter vascular graft in the dog. J Surg Res 47:74-80.
15. Badylak SF, Taylor D, Uygun K. 2011b. Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng 13:27-53.
16. Badylak SF, Tullius R, Kokini K, et al. 1995. The use of xenogeneic small intestinal submucosa as a biomaterial for Achilles tendon repair in a dog model. J Biomed Mater Res 29:977-985.
17. Badylak SF, Vorp DA, Spievack AR, et al. 2005. Esophageal reconstruction with ECM and muscle tissue in a dog model. J Surg Res 128:87-97.
18. Baiguera S, Jungebluth P, Burns A, et al. 2010. Tissue engineered human tracheas for in vivo implantation. Biomaterials 31:8931-8938.
19. Bang OY, Lee JS, Lee PH, Lee G. 2005. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol 57:874-882.
20. Barker N. 2008. The canonical Wnt/beta-catenin signalling pathway. Methods Mol Biol 468:5-15.
21. Beanes SR, Hu FY, Soo C, et al. 2002. Confocal microscopic analysis of scarless repair in the fetal rat: defining the transition. Plastic Reconstr Surg 109:160-170.
22. Becerra J, Santos-Ruiz L, Andrades JA, Mari-Beffa M. 2011. The stem cell niche should be a key issue for cell therapy in regenerative medicine. Stem Cell Rev 7:248-255.
23. Berthiaume F, Maguire TJ, Yarmush ML. 2011. Tissue engineering and regenerative medicine: history, progress, and challenges. Annu Rev Chem Biomol Eng 2:403-430.
24. Boden SD. 2005. The ABCs of BMPs. Orthop Nurs 24:49-52; quiz 53-44.
25. Boot-Handford RP, Tuckwell DS. 2003. Fibrillar collagen: the key to vertebrate evolution? A tale of molecular incest. Bioessays 25:142-151.
26. Boquest AC, Collas P. 2012. Obtaining freshly isolated and cultured mesenchymal stem cells from human adipose tissue. Methods Mol Biol 879:269-278.
27. Bourin P, Gadelorge M, Peyrafitte JA, et al. 2008. Mesenchymal progenitor cells: tissue origin, isolation and culture. Transfus Med Hemother 35:160-167.
28. Brittberg M, Lindahl A, Nilsson A, et al. 1994. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331:889-895.
29. Brockes JP. 1997. Amphibian limb regeneration: rebuilding a complex structure. Science 276:81-87.
30. Brockes JP, Kumar A. 2008. Comparative aspects of animal regeneration. Annu Rev Cell Dev Biol 24:525-549.
31. Brohem CA, Cardeal LB, Tiago M, et al. 2011. Artificial skin in perspective: concepts and applications. Pigment Cell Melanoma Res 24:35-50.
32. Brown BN, Londono R, Tottey S, et al. 2012. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater 8:978-987.
33. Brown BN, Valentin JE, Stewart-Akers AM, et al. 2009. Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30:1482-1491.
34. Brunt KR, Weisel RD, Li RK. 2012. Stem cells and regenerative medicine-future perspectives. Can J Physiol Pharmacol 90:327-335.
35. Call MK, Tsonis PA. 2005. Vertebrate limb regeneration. Adv Biochem Eng Biotechnol 93:67-81.
36. Calve S, Odelberg SJ, Simon HG. 2010. A transitional extracellular matrix instructs cell behavior during muscle regeneration. Dev Biol 344:259-271.
37. Carragee EJ, Hurwitz EL, Weiner BK. 2011. A critical review of recombinant human bone morphogenetic protein-2 trials in spinal surgery: emerging safety concerns and lessons learned. Spine J 11:471-491.
38. Clifford DM, Fisher SA, Brunskill SJ, et al. 2012. Stem cell treatment for acute myocardial infarction. Cochrane Database Syst Rev 2:CD006536.
39. Cohen M, Joester D, Geiger B, Addadi L. 2004. Spatial and temporal sequence of events in cell adhesion: from molecular recognition to focal adhesion assembly. Chembiochem 5:1393-1399.
40. Colwell AS, Longaker MT, Lorenz HP. 2005. Mammalian fetal organ regeneration. Adv Biochem Eng Biotechnol 93:83-100.
41. Conklin BS, Richter ER, Kreutziger KL, et al. 2002. Development and evaluation of a novel decellularized vascular xenograft. Med Eng Phys 24:173-183.
42. Cowin AJ, Brosnan MP, Holmes TM, Ferguson MW. 1998. Endogenous inflammatory response to dermal wound healing in the fetal and adult mouse. Dev Dyn 212:385-393.
43. Crapo PM, Gilbert TW, Badylak SF. 2011. An overview of tissue and whole organ decellularization processes. Biomaterials 32:3233-3243.
44. Cristante AF, Barros-Filho TE, Tatsui N, et al. 2009. Stem cells in the treatment of chronic spinal cord injury: evaluation of somatosensitive evoked potentials in 39 patients. Spinal Cord 47:733-738.
45. Dahl SL, Koh J, Prabhakar V, Niklason LE. 2003. Decellularized native and engineered arterial scaffolds for transplantation. Cell Transplant 12:659-666.
46. Daly AB, Wallis JM, Borg ZD, et al. 2012. Initial binding and recellularization of decellularized mouse lung scaffolds with bone marrow-derived mesenchymal stromal cells. Tissue Eng Part A 18:1-16.
47. De Robertis EM. 2009. Spemann's organizer and the self-regulation of embryonic fields. Mech Dev 126:925-941.
48. DeLong SA, Moon JJ, West JL. 2005. Covalently immobilized gradients of bFGF on hydrogel scaffolds for directed cell migration. Biomaterials 26:3227-3234.
49. den Haan MC, Grauss RW, Smits AM, et al. 2012. Cardiomyogenic differentiation-independent improvement of cardiac function by human cardiomyocyte progenitor cell injection in ischaemic mouse hearts. J Cell Mol Med 16:1508-1521.
50. Denham M, Conley B, Olsson F, et al. 2005. Stem cells: an overview. Curr Prot Cell Biol Chapter 23:Unit 23.1.
51. Dreymueller D, Denecke B, Ludwig A, Jahnen-Dechent W. 2013. Embryonic stem cell-derived M2-like macrophages delay cutaneous wound healing. Wound Repair Regen 21:44-54.
52. Evans MJ, Kaufman MH. 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154-156.
53. Fata JE, Werb Z, Bissell MJ. 2004. Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res 6:1-11.
54. Fausto N. 2004. Liver regeneration and repair: hepatocytes, progenitor cells, and stem cells. Hepatology 39:1477-1487.
55. Franchini A, Bertolotti E. 2012. The thymus and tail regenerative capacity in Xenopus laevis tadpoles. Acta Histochem 114:334-341.
56. French KM, Boopathy AV, Dequach JA, et al. 2012. A naturally derived cardiac extracellular matrix enhances cardiac progenitor cell behavior in vitro. Acta Biomater 8:4357-4364.
57. Friedenstein AJ, Gorskaja JF, Kulagina NN. 1976. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4:267-274.
58. Frolov AA, Bryukhovetskiy AS. 2012. Effects of hematopoietic autologous stem cell transplantation to the chronically injured human spinal cord evaluated by motor and somatosensory evoked potentials methods. Cell Transplant 21 Suppl 1:S49-S55.
59. Gilbert TW, Gilbert S, Madden M, et al. 2008a. Morphologic assessment of extracellular matrix scaffolds for patch tracheoplasty in a canine model. Ann Thorac Surg 86:967-974; discussion 967-974.
60. Gilbert TW, Nieponice A, Spievack AR, et al. 2008b. Repair of the thoracic wall with an extracellular matrix scaffold in a canine model. J Surg Res 147:61-67.
61. Gilbert TW, Stewart-Akers AM, Simmons-Byrd A, Badylak SF. 2007. Degradation and remodeling of small intestinal submucosa in canine Achilles tendon repair. J Bone Joint Surg Am 89:621-630.
62. Grogan BF, Hsu JR, Skeletal Trauma Research C. 2011. Volumetric muscle loss. J Am Acad Orthop Surg 19 Suppl 1:S35-S37.
63. Hammerman MR. 2012. Development of a novel xenotransplantation strategy for treatment of diabetes mellitus in rat hosts and translation to non-human primates. Organogenesis 8:41-48.
64. Han M, Yang X, Farrington JE, Muneoka K. 2003. Digit regeneration is regulated by Msx1 and BMP4 in fetal mice. Development (Cambridge, England) 130:5123-5132.
65. Hauselmann HJ, Flura T, Marti C, Hauser N, et al. 1998. [From chondrocyte culture to joint cartilage replacement. Development of de novo cartilage in vitro]. Schweiz Med Wochenschr 128:824-832.
66. He X, Ma J, Jabbari E. 2008. Effect of grafting RGD and BMP-2 protein-derived peptides to a hydrogel substrate on osteogenic differentiation of marrow stromal cells. Langmuir 24:12508-12516.
67. Hechavarria D, Dewilde A, Braunhut S, et al. 2010. BioDome regenerative sleeve for biochemical and biophysical stimulation of tissue regeneration. Med Eng Phys 32:1065-1073.
68. Hodde JP, Ernst DM, Hiles MC. 2005. An investigation of the long-term bioactivity of endogenous growth factor in OASIS Wound Matrix. J Wound Care 14:23-25.
69. Hodde JP, Record RD, Liang HA, Badylak SF. 2001. Vascular endothelial growth factor in porcine-derived extracellular matrix. Endothelium 8:11-24.
70. Hoppo T, Badylak SF, Jobe BA. 2012. A novel esophageal-preserving approach to treat high-grade dysplasia and superficial adenocarcinoma in the presence of chronic gastroesophageal reflux disease. World J Surg 36:2390-2393.
71. Hoppo T, Komori J, Manohar R, et al. 2011. Rescue of lethal hepatic failure by hepatized lymph nodes in mice. Gastroenterology 140:656-666 e652.
72. Humphries MJ, Newham P. 1998. The structure of cell-adhesion molecules. Trends Cell Biol 8:78-83.
73. Huttenlocher A, Sandborg RR, Horwitz AF. 1995. Adhesion in cell migration. Curr Opin Cell Biol 7:697-706.
74. Hutter H, Vogel BE, Plenefisch JD, et al. 2000. Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science 287:989-994.
75. Hwang NS, Zhang C, Hwang YS, Varghese S. 2009. Mesenchymal stem cell differentiation and roles in regenerative medicine. Wiley Interdiscip Rev Syst Biol Med 1:97-106.
76. Hynes RO, Zhao Q. 2000. The evolution of cell adhesion. J Cell Biol 150:F89-F96.
77. In 't Anker PS, Scherjon SA, Kleijburg-van der Keur C, et al. 2003. Amniotic fluid as a novel source of mesenchymal stem cells for therapeutic transplantation. Blood 102:1548-1549.
78. Iozzo RV. 1994. Perlecan: a gem of a proteoglycan. Matrix Biol 14:203-208.
79. Jarvinen TA, Jarvinen TL, Kaariainen M, et al. 2005. Muscle injuries: biology and treatment. Am J Sports Med 33:745-764.
80. Kaewsuwan S, Song SY, Kim JH, Sung JH. 2012. Mimicking the functional niche of adipose-derived stem cells for regenerative medicine. Expert Opin Biol Ther 12:1575-1588.
81. Kaivosoja E, Barreto G, Levon K, et al. 2012. Chemical and physical properties of regenerative medicine materials controlling stem cell fate. Ann Med 44:635-650.
82. Keane TJ, Londono R, Turner NJ, Badylak SF. 2012. Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 33:1771-1781.
83. Kemp P. 2006. History of regenerative medicine: looking backwards to move forwards. Regen Med 1:653-669.
84. Kiecker C, Lumsden A. 2012. The role of organizers in patterning the nervous system. Annu Rev Neurosci 35:347-367.
85. Koh TJ, DiPietro LA. 2011. Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med 13:e23.
86. Komori J, Boone L, DeWard A, et al. 2012. The mouse lymph node as an ectopic transplantation site for multiple tissues. Nat Biotechnol 30:976-983.
87. Kramer JM. 1997. Extracellular matrix. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C. elegans II. 2nd ed. New York: Cold Spring Harbor.
88. Kropp BP, Rippy MK, Badylak SF, et al. 1996. Regenerative urinary bladder augmentation using small intestinal submucosa: urodynamic and histopathologic assessment in long-term canine bladder augmentations. J Urol 155:2098-2104.
89. Kurek JB, Nouri S, Kannourakis G, et al. 1996. Leukemia inhibitory factor and interleukin-6 are produced by diseased and regenerating skeletal muscle. Muscle Nerve 19:1291-1301.
90. Langer R, Vacanti JP. 1993. Tissue engineering. Science 260:920-926.
91. Larson BJ, Longaker MT, Lorenz HP. 2010. Scarless fetal wound healing: a basic science review. Plastic Reconstr Surg 126:1172-1180.
92. Lataillade JJ, Doucet C, Bey E, et al. 2007. New approach to radiation burn treatment by dosimetry-guided surgery combined with autologous mesenchymal stem cell therapy. Regen Med 2:785-794.
93. Lee AC, Yu VM, Lowe JB 3rd, et al. 2003. Controlled release of nerve growth factor enhances sciatic nerve regeneration. Exp Neurol 184:295-303.
94. Lee OK, Kuo TK, Chen WM, et al. 2004. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 103:1669-1675.
95. Leibovich SJ, Ross R. 1975. The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am J Pathol 78:71-100.
96. Lemaire P, Kodjabachian L. 1996. The vertebrate organizer: structure and molecules. Trends Genetics 12:525-531.
97. Lepilina A, Coon AN, Kikuchi K, et al. 2006. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127:607-619.
98. Lewis CJ. 2013. Stem cell application in acute burn care and reconstruction. J Wound Care 22:7-8, 10, 12-16.
99. Lin P, Chan WC, Badylak SF, Bhatia SN. 2004. Assessing porcine liver-derived biomatrix for hepatic tissue engineering. Tissue Eng 10:1046-1053.
100. Liu C, Dib-Hajj SD, Waxman SG. 2001. Fibroblast growth factor homologous factor 1B binds to the C terminus of the tetrodotoxin-resistant sodium channel rNav1.9a (NaN). J Biol Chem 276:18925-18933.
101. Longaker MT, Whitby DJ, Adzick NS, et al. 1990. Studies in fetal wound healing, VI. Second and early third trimester fetal wounds demonstrate rapid collagen deposition without scar formation. J Pediatr Surg 25:63-68; discussion 68-69.
102. Lorenz HP, Adzick NS. 1993. Scarless skin wound repair in the fetus. West J Med 159:350-355.
103. Macchiarini P, Jungebluth P, Go T, et al. 2008. Clinical transplantation of a tissue-engineered airway. Lancet 372:2023-2030.
104. Mansbridge J. 1998. Skin substitutes to enhance wound healing. Expert Opin Investig Drugs 7:803-809.
105. Mantovani A, Sica A, Locati M. 2005. Macrophage polarization comes of age. Immunity 23:344-346.
106. Mantovani A, Sica A, Sozzani S, et al. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677-686.
107. Martin GR. 1981. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 78:7634-7638.
108. Martin I, Wendt D, Heberer M. 2004. The role of bioreactors in tissue engineering. Trends Biotechnol 22:80-86.
109. Martin PG, Martinez AR, Lara VG, Naveros BC. Regulatory considerations in production of a cell therapy medicinal product in Europe to clinical research. Clin Exp Med (in press).
110. Martinez FO, Gordon S, Locati M, Mantovani A. 2006. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 177:7303-7311.
111. Martinez FO, Sica A, Mantovani A, Locati M. 2008. Macrophage activation and polarization. Front Biosci 13:453-461.
112. Mase VJ Jr, Hsu JR, Wolf SE, et al. 2010. Clinical application of an acellular biologic scaffold for surgical repair of a large, traumatic quadriceps femoris muscle defect. Orthopedics 33:511.
113. Midha R, Munro CA, Dalton PD, et al. 2003. Growth factor enhancement of peripheral nerve regeneration through a novel synthetic hydrogel tube. J Neurosurg 99:555-565.
114. Mills CD, Kincaid K, Alt JM, et al. 2000. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164:6166-6173.
115. Mirza R, DiPietro LA, Koh TJ. 2009. Selective and specific macrophage ablation is detrimental to wound healing in mice. Am J Pathol 175:2454-2462.
116. Morgan TH. 1901. Regeneration and liability to injury. Science 14:235-248.
117. Muguruma Y, Reyes M, Nakamura Y, et al. 2003. In vivo and in vitro differentiation of myocytes from human bone marrow-derived multipotent progenitor cells. Exp Hematol 31:1323-1330.
118. Nelson CM, Bissell MJ. 2006. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 22:287-309.
119. Nichols JE, Niles J, Riddle M, et al. 2013. Production and assessment of decellularized pig and human lung scaffolds. Tissue Eng Part A 19:2045-2062.
120. Nieponice A, Gilbert TW, Badylak SF. 2006. Reinforcement of esophageal anastomoses with an extracellular matrix scaffold in a canine model. Ann Thorac Surg 82:2050-2058.
121. Nieponice A, McGrath K, Qureshi I, et al 2009. An extracellular matrix scaffold for esophageal stricture prevention after circumferential EMR. Gastrointest Endosc 69:289-296.
122. Oberpenning F, Meng J, Yoo JJ, Atala A. 1999. De novo reconstitution of a functional mammalian urinary bladder by tissue engineering. Nat Biotechnol 17:149-155.
123. Odelberg SJ, Kollhoff A, Keating MT. 2000. Dedifferentiation of mammalian myotubes induced by msx1. Cell 103:1099-1109.
124. Okumura M, Matthews RJ, Robb B, et al. 1996. Comparison of CD45 extracellular domain sequences from divergent vertebrate species suggests the conservation of three fibronectin type III domains. J Immunol 157:1569-1575.
125. Orlando G, Wood KJ, De Coppi P, et al. 2012. Regenerative medicine as applied to general surgery. Ann Surg 255:867-880.
126. Orlic D, Kajstura J, Chimenti S, et al. 2001. Bone marrow cells regenerate infarcted myocardium. Nature 410:701-705.
127. Ott HC, Matthiesen TS, Goh SK, et al. 2008. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 14:213-221.
128. Ovchinnikov DA. 2008. Macrophages in the embryo and beyond: much more than just giant phagocytes. Genesis 46:447-462.
129. Payne TR, Oshima H, Sakai T, et al. 2005. Regeneration of dystrophin-expressing myocytes in the mdx heart by skeletal muscle stem cells. Gene Ther 12:1264-1274.
130. Petersen TH, Calle EA, Colehour MB, Niklason LE. 2012. Matrix composition and mechanics of decellularized lung scaffolds. Cells Tissues Organs 195:222-231.
131. Petersen TH, Calle EA, Zhao L, et al. 2010. Tissue-engineered lungs for in vivo implantation. Science 329:538-541.
132. Pham C, Greenwood J, Cleland H, et al. 2007. Bioengineered skin substitutes for the management of burns: a systematic review. Burns 33:946-957.
133. Polesskaya A, Seale P, Rudnicki MA. 2003. Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell 113:841-852.
134. Porcheray F, Viaud S, Rimaniol AC, et al. 2005. Macrophage activation switching: an asset for the resolution of inflammation. Clin Exp Immunol 142:481-489.
135. Poss KD, Wilson LG, Keating MT. 2002. Heart regeneration in zebrafish. Science 298:2188-2190.
136. Redd MJ, Cooper L, Wood W, et al. 2004. Wound healing and inflammation: embryos reveal the way to perfect repair. Philos Trans R Soc Lond Ser B Biol Sci 359:777-784.
137. Reguart N, He B, Taron M, et al. 2005. The role of Wnt signaling in cancer and stem cells. Future Oncol 1:787-797.
138. Reing JE, Brown BN, Daly KA, et al. 2010. The effects of processing methods upon mechanical and biologic properties of porcine dermal extracellular matrix scaffolds. Biomaterials 31:8626-8633.
139. Remlinger NT, Czajka CA, Juhas ME, et al. 2010. Hydrated xenogeneic decellularized tracheal matrix as a scaffold for tracheal reconstruction. Biomaterials 31:3520-3526.
140. Robin NH, Nadeau JH. 2001. Disorganization in mice and humans. Am J Med Genetics 101:334-338.
141. Robinson KA, Li J, Mathison M, et al. 2005. Extracellular matrix scaffold for cardiac repair. Circulation 112(9 Suppl):I135-I143.
142. Rodero MP, Khosrotehrani K. 2010. Skin wound healing modulation by macrophages. Int J Clin Exp Pathol 3:643-653.
143. Sarugaser R, Lickorish D, Baksh D, et al. 2005. Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 23:220-229.
144. Schaffner F. 1991. Structural and functional aspects of regeneration of human liver. Dig Dis Sci 36:1282-1286.
145. Schmoekel HG, Weber FE, Schense JC, et al. 2005. Bone repair with a form of BMP-2 engineered for incorporation into fibrin cell ingrowth matrices. Biotechnol Bioeng 89:253-262.
146. Schwartz M. 2010. "Tissue-repairing" blood-derived macrophages are essential for healing of the injured spinal cord: from skin-activated macrophages to infiltrating blood-derived cells? Brain Behav Immun 24:1054-1057.
147. Scott JE. 1995. Extracellular matrix, supramolecular organisation and shape. J Anat 187 (Pt 2):259-269.
148. Seif-Naraghi SB, Singelyn JM, Salvatore MA, et al. 2013. Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction. Sci Transl Med 5:173ra125.
149. Shah M, Foreman DM, Ferguson MW. 1995. Neutralisation of TGF-beta 1 and TGF-beta 2 or exogenous addition of TGF-beta 3 to cutaneous rat wounds reduces scarring. J Cell Sci 108(Pt 3):985-1002.
150. Shamblott MJ, Axelman J, Wang S, et al. 1998. Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci USA 95:13726-13731.
151. Shi M, Ishikawa M, Kamei N, et al. 2009. Acceleration of skeletal muscle regeneration in a rat skeletal muscle injury model by local injection of human peripheral blood-derived CD133-positive cells. Stem Cells 27:949-960.
152. Sicari BM, Agrawal V, Siu BF, et al. 2012. A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng Part A 18:1941-1948.
153. Silva EA, Kim ES, Kong HJ, Mooney DJ. 2008. Material-based deployment enhances efficacy of endothelial progenitor cells. Proc Natl Acad Sci USA 105:14347-14352.
154. Slack JM, Lin G, Chen Y. 2008. The Xenopus tadpole: a new model for regeneration research. Cell Mol Life Sci 65:54-63.
155. Song F, Li B, Stocum DL. 2010. Amphibians as research models for regenerative medicine. Organogenesis 6:141-150.
156. Song JJ, Kim SS, Liu Z, et al. 2011. Enhanced in vivo function of bioartificial lungs in rats. Ann Thorac Surg 92:998-1005; discussion 1005-1006.
157. Soto-Gutierrez A, Zhang L, Medberry C, et al. 2011. A whole-organ regenerative medicine approach for liver replacement. Tissue Eng Part C Methods 17:677-686.
158. Stoick-Cooper CL, Moon RT, Weidinger G. 2007. Advances in signaling in vertebrate regeneration as a prelude to regenerative medicine. Genes Dev 21:1292-1315.
159. Strauer BE, Brehm M, Zeus T, et al. 2002. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 106:1913-1918.
160. Strey CW, Markiewski M, Mastellos D, et al. 2003. The proinflammatory mediators C3a and C5a are essential for liver regeneration. J Exp Med 198:913-923.
161. Suckow MA, Voytik-Harbin SL, Terril LA, Badylak SF. 1999. Enhanced bone regeneration using porcine small intestinal submucosa. J Invest Surg 12:277-287.
162. Szpaderska AM, DiPietro LA. 2005. Inflammation in surgical wound healing: friend or foe? Surgery 137:571-573.
163. Takahashi K, Okita K, Nakagawa M, Yamanaka S. 2007. Induction of pluripotent stem cells from fibroblast cultures. Nat Prot 2:3081-3089.
164. Takeishi T, Hirano K, Kobayashi T, et al. 1999. The role of Kupffer cells in liver regeneration. Archiv Histol Cytol 62:413-422.
165. Taub R. 2004. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol 5:836-847.
166. Thomas ED, Lochte HL Jr, Lu WC, Ferrebee JW. 1957. Intravenous infusion of bone marrow in patients receiving radiation and chemotherapy. N Engl J Med 257:491-496.
167. Thompson MD, Monga SP. 2007. WNT/beta-catenin signaling in liver health and disease. Hepatology 45:1298-1305.
168. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
169. Tidball JG. 2005. Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288:R345-R353.
170. Tottey S, Corselli M, Jeffries EM, et al. 2011. Extracellular matrix degradation products and low-oxygen conditions enhance the regenerative potential of perivascular stem cells. Tissue Eng Part A 17:37-44.
171. Turner NJ, Yates AJ Jr, Weber DJ, et al. 2010. Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Eng Part A 16:3309-3317.
172. Uygun BE, Soto-Gutierrez A, Yagi H, et al. 2010. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med 16:814-820.
173. Valentin JE, Stewart-Akers AM, Gilbert TW, Badylak SF. 2009. Macrophage participation in the degradation and remodeling of extracellular matrix scaffolds. Tissue Eng Part A 15:1687-1694.
174. Valentin JE, Turner NJ, Gilbert TW, Badylak SF. 2010. Functional skeletal muscle formation with a biologic scaffold. Biomaterials 31:7475-7484.
175. Vincent SD, Buckingham ME. 2010. How to make a heart: the origin and regulation of cardiac progenitor cells. Curr Top Dev Biol 90:1-41.
176. Vunjak-Novakovic G. 2003. The fundamentals of tissue engineering: scaffolds and bioreactors. Novartis Found Symp 249:34-46; discussion 46-51, 170-174, 239-141.
177. Wagers AJ. 2012. The stem cell niche in regenerative medicine. Cell Stem Cell 10:362-369.
178. Wagner DE, Bonvillain RW, Jensen T, et al. 2013. Can stem cells be used to generate new lungs? Ex vivo lung bioengineering with decellularized whole lung scaffolds. Respirology 18:895-911.
179. Wainwright JM, Hashizume R, Fujimoto KL, et al. 2012. Right ventricular outflow tract repair with a cardiac biologic scaffold. Cells Tissues Organs 195:159-170.
180. Warren GL, Hulderman T, Jensen N, et al. 2002. Physiological role of tumor necrosis factor alpha in traumatic muscle injury. FASEB J 16:1630-1632.
181. Whitby DJ, Ferguson MW. 1991. The extracellular matrix of lip wounds in fetal, neonatal and adult mice. Development 112:651-668.
182. Widera D, Hauser S, Kaltschmidt C, Kaltschmidt B. 2012. Origin and regenerative potential of vertebrate mechanoreceptor-associated stem cells. Anat Res Int 2012:837626.
183. Wood JD, Simmons-Byrd A, Spievack AR, Badylak SF. 2005. Use of a particulate extracellular matrix bioscaffold for treatment of acquired urinary incontinence in dogs. J Am Vet Med Assoc 226:1095-1097.
184. Wood JJ, Malek MA, Frassica FJ, et al. 2006. Autologous cultured chondrocytes: adverse events reported to the United States Food and Drug Administration. J Bone Joint Surg Am Vol 88:503-507.
185. Xu CS, Jiang Y, Zhang LX, et al. 2012. The role of Kupffer cells in rat liver regeneration revealed by cell-specific microarray analysis. J Cell Biochem 113:229-237.
186. Yang B, Zhang Y, Zhou L, et al. 2010. Development of a porcine bladder acellular matrix with well-preserved extracellular bioactive factors for tissue engineering. Tissue Eng Part C Methods 16:1201-1211.
187. Yokoyama H. 2008. Initiation of limb regeneration: the critical steps for regenerative capacity. Dev Growth Differ 50:13-22.
188. Zhang WY, de Almeida PE, Wu JC. 2008. Teratoma formation: a tool for monitoring pluripotency in stem cell research. StemBook [Internet]. Cambridge (MA).
189. Zhang YM, Hartzell C, Narlow M, Dudley SC Jr. 2002. Stem cell-derived cardiomyocytes demonstrate arrhythmic potential. Circulation 106:1294-1299.