Tissue Engineered Skin Substitutes Created by Laser-Assisted Bioprinting Form Skin-Like Structures in the Dorsal Skin Fold Chamber in Mice

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Michael, Stefanie ^a   Sorg, Heiko ^a   Peck, Claas Tido ^a   Koch, Lothar ^b   Deiwick, Andrea ^b   Chichkov, Boris ^b   Vogt, Peter M ^a   Reimers, Kerstin ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b LASER ZENTRUM HANNOVER E V   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; UVOMORULIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOPRINTING; CELL DIFFERENTIATION; CELL JUNCTION; CELL MIGRATION; CELL PROLIFERATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; EPIDERMIS; EXTRACELLULAR MATRIX; FIBROBLAST; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; LASER ASSISTED BIOPRINTING; MOUSE; NONHUMAN; SKIN GRAFT; SKIN INJURY; SKIN TRANSPLANTATION; SKINFOLD; STRATUM CORNEUM; TISSUE ENGINEERING;

ANIMALS; BIOLOGICAL MARKERS; BIOPRINTING; BURNS; CADHERINS; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN; ELASTIN; FIBROBLASTS; KERATINOCYTES; LASERS; MICE; MICE, NUDE; NEOVASCULARIZATION, PHYSIOLOGIC; SKIN; SKIN, ARTIFICIAL; TISSUE ENGINEERING; WOUND HEALING;

EID: 84874591959     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057741     Document Type: Article

References (43)

1. Vogt PM, Kolokythas P, Niederbichler A, Knobloch K, Reimers K, et al. (2007) Innovative wound therapy and skin substitutes for burns. Der Chirurg; Zeitschrift Fur Alle Gebiete Der Operativen Medizen 78: 335-342.
2. Supp DM, Boyce ST, (2005) Engineered skin substitutes: Practices and potentials. Clinics in Dermatology 23: 403-412.
3. Singer AJ, Clark RA, (1999) Cutaneous wound healing. The New England Journal of Medicine 341: 738-746.
4. Jakab K, Norotte C, Marga F, Murphy K, Vunjak-Novakovic G, et al. (2010) Tissue engineering by self-assembly and bio-printing of living cells. Biofabrication 2: 022001.
5. Black AF, Berthod F, L'heureux N, Germain L, Auger FA, (1998) In vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. The FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 12: 1331-1340.
6. Couet F, Mantovani D, (2012) Perspectives on the advanced control of bioreactors for functional vascular tissue engineering in vitro. Expert Review of Medical Devices 9: 233-239.
7. Barron JA, Wu P, Ladouceur HD, Ringeisen BR, (2004) Biological laser printing: A novel technique for creating heterogeneous 3-dimensional cell patterns. Biomedical Microdevices 6: 139-147.
8. Catros S, Fricain JC, Guillotin B, Pippenger B, Bareille R, et al. (2011) Laser-assisted bioprinting for creating on-demand patterns of human osteoprogenitor cells and nano-hydroxyapatite. Biofabrication 3: 025001.
9. Othon CM, Wu X, Anders JJ, Ringeisen BR, (2008) Single-cell printing to form three-dimensional lines of olfactory ensheathing cells. Biomedical Materials (Bristol, England) 3: 034101.
10. Guillotin B, Souquet A, Catros S, Duocastella M, Pippenger B, et al. (2010) Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials 31: 7250-7256.
11. Gruene M, Pflaum M, Deiwick A, Koch L, Schlie S, et al. (2011) Adipogenic differentiation of laser-printed 3D tissue grafts consisting of human adipose-derived stem cells. Biofabrication 3: 015005.
12. Gruene M, Deiwick A, Koch L, Schlie S, Unger C,et al. (2010) Laser printing of stem cells for biofabrication of scaffold-free autologous grafts. Tissue Engineering.Part C, Methods.
13. Hopp B, Smausz T, Kresz N, Barna N, Bor Z, et al. (2005) Survival and proliferative ability of various living cell types after laser-induced forward transfer. Tissue Engineering 11: 1817-1823.
14. Ringeisen BR, Kim H, Young HD, Spargo BJ, Auyeung RCY,et al. (2001) Cell-by-cell construction of living tissue. 698.
15. Ringeisen BR, Kim H, Barron JA, Krizman DB, Chrisey DB, et al. (2004) Laser printing of pluripotent embryonal carcinoma cells. Tissue Engineering 10: 483-491.
16. Koch L, Kuhn S, Sorg H, Gruene M, Schlie S, et al. (2010) Laser printing of skin cells and human stem cells. Tissue Engineering.Part C, Methods 16: 847-854.
17. Koch L, Deiwick A, Schlie S, Michael S, Gruene M, et al. (2012) Skin tissue generation by laser cell printing. Biotechnology and Bioengineering 109: 1855-1863.
18. Unger C, Gruene M, Koch L, Koch J, Chichkov BN, (2011) Time-resolved imaging of hydrogel printing via laser-induced forward transfer. Applied Physics A: Materials Science & Processing 103: 271-277.
19. Gruene M, Unger C, Koch L, Deiwick A, Chichkov B, (2011) Dispensing pico to nanolitre of a natural hydrogel by laser-assisted bioprinting. Biomedical Engineering Online 10: 19.
20. Michael S, Sorg H, Peck CT, Reimers K, Vogt PM (2012) The mouse dorsal skin fold chamber as a means for the analysis of tissue engineered skin. Burns: Journal of the International Society for Burn Injuries.
21. Xu T, Zhao W, Zhu JM, Albanna MZ, Yoo JJ, et al. (2013) Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology. Biomaterials 34: 130-139.
22. Cui X, Breitenkamp K, Finn MG, Lotz M, D'Lima DD, (2012) Direct human cartilage repair using three-dimensional bioprinting technology. Tissue Engineering.Part A 18: 1304-1312.
23. Ballaun C, Weninger W, Uthman A, Weich H, Tschachler E, (1995) Human keratinocytes express the three major splice forms of vascular endothelial growth factor. The Journal of Investigative Dermatology 104: 7-10.
24. Hacker C, Valchanova R, Adams S, Munz B, (2010) ZFP36L1 is regulated by growth factors and cytokines in keratinocytes and influences their VEGF production. Growth Factors (Chur, Switzerland) 28: 178-190.
25. Goren I, Muller E, (2009) Schiefelbein D, Gutwein P, Seitz O, et al (2009) Akt1 controls insulin-driven VEGF biosynthesis from keratinocytes: Implications for normal and diabetes-impaired skin repair in mice. The Journal of Investigative Dermatology 129: 752-764.
26. Rochon MH, Fradette J, Fortin V, Tomasetig F, Roberge CJ, et al. (2010) Normal human epithelial cells regulate the size and morphology of tissue-engineered capillaries. Tissue Engineering.Part A 16: 1457-1468.
27. Black AF, Hudon V, Damour O, Germain L, Auger FA, (1999) A novel approach for studying angiogenesis: A human skin equivalent with a capillary-like network. Cell Biology and Toxicology 15: 81-90.
28. Schechner JS, Crane SK, Wang F, Szeglin AM, Tellides G, et al. (2003) Engraftment of a vascularized human skin equivalent. The FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 17: 2250-2256.
29. Wilson WC Jr, Boland T, (2003) Cell and organ printing 1: Protein and cell printers. The Anatomical Record.Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 272: 491-496.
30. Boland T, Mironov V, Gutowska A, Roth EA, Markwald RR, (2003) Cell and organ printing 2: Fusion of cell aggregates in three-dimensional gels. The Anatomical Record.Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 272: 497-502.
31. Arai K, Iwanaga S, Toda H, Genci C, Nishiyama Y, et al. (2011) Three-dimensional inkjet biofabrication based on designed images. Biofabrication 3: 034113.
32. Zheng Q, Lu J, Chen H, Huang L, Cai J, et al. (2011) Application of inkjet printing technique for biological material delivery and antimicrobial assays. Analytical Biochemistry 410: 171-176.
33. Owczarczak AB, Shuford SO, Wood ST, Deitch S, Dean D (2012) Creating transient cell membrane pores using a standard inkjet printer. Journal of Visualized Experiments: JoVE (61). pii: 3681. doi:10.3791/3681.
34. Born C, Zhang Z, Al-Rubeai M, Thomas CR, (1992) Estimation of disruption of animal cells by laminar shear stress. Biotechnology and Bioengineering 40: 1004-1010.
35. Klingenberg JM, McFarland KL, Friedman AJ, Boyce ST, Aronow BJ, et al. (2010) Engineered human skin substitutes undergo large-scale genomic reprogramming and normal skin-like maturation after transplantation to athymic mice. The Journal of Investigative Dermatology 130: 587-601.
36. Xie JL, Li TZ, Qi SH, Huang B, Chen XG, et al. (2007) A study of using tissue-engineered skin reconstructed by candidate epidermal stem cells to cover the nude mice with full-thickness skin defect. Journal of Plastic, Reconstructive & Aesthetic Surgery: JPRAS 60: 983-990.
37. Egana JT, Fierro FA, Kruger S, Bornhauser M, Huss R, et al. (2009) Use of human mesenchymal cells to improve vascularization in a mouse model for scaffold-based dermal regeneration. Tissue Engineering.Part A 15: 1191-1200.
38. Kalyanaraman B, Boyce ST, (2009) Wound healing on athymic mice with engineered skin substitutes fabricated with keratinocytes harvested from an automated bioreactor. The Journal of Surgical Research 152: 296-302.
39. Boyce ST, Medrano EE, Abdel-Malek Z, Supp AP, Dodick JM, et al. (1993) Pigmentation and inhibition of wound contraction by cultured skin substitutes with adult melanocytes after transplantation to athymic mice. The Journal of Investigative Dermatology 100: 360-365.
40. Rasmussen CA, Gibson AL, Schlosser SJ, Schurr MJ, Allen-Hoffmann BL, (2010) Chimeric composite skin substitutes for delivery of autologous keratinocytes to promote tissue regeneration. Annals of Surgery 251: 368-376.
41. Galiano RD, Michaels J, Dobryansky M, Levine JP, Gurtner GC, (2004) Quantitative and reproducible murine model of excisional wound healing. Wound Repair and Regeneration: Official Publication of the Wound Healing Society [and] the European Tissue Repair Society 12: 485-492.
42. Kirfel G, Herzog V, (2004) Migration of epidermal keratinocytes: Mechanisms, regulation, and biological significance. Protoplasma 223: 67-78.
43. Laschke MW, Harder Y, Amon M, Martin I, Farhadi J, et al. (2006) Angiogenesis in tissue engineering: Breathing life into constructed tissue substitutes. Tissue Engineering 12: 2093-2104.