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REVIEW

Vascularization strategies for human skin tissue engineering via 3D bioprinting

Arvind Kumar Shukla1 ,  Dongjun Lee2 ,  Sik Yoon3,4 ,  Minjun Ahn5* ,  Byoung Soo Kim1,5*
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1 School of Biomedical Convergence Engineering, Pusan National University, Yangsan, Republic of Korea
2 Department of Convergence Medicine, Pusan National University College of Medicine, Yangsan, Republic of Korea
3 Department of Anatomy and Convergence Medical Sciences, Pusan National University College of Medicine, Yangsan, Republic of Korea
4 Immune Reconstitution Research Center of Medical Research Institute, Pusan National University College of Medicine, Yangsan, Republic of Korea
5 Medical Research Institute, Pusan National University, Yangsan, Republic of Korea
IJB 2024, 10(3), 1727 https://doi.org/10.36922/ijb.1727
Submitted: 31 August 2023 | Accepted: 20 November 2023 | Published: 28 January 2024
(This article belongs to the Special Issue 3D printing for tissue engineering and regenerative medicine)
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
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Abstract

The skin is composed of many cells that are organized into different layers and connected by dense and complex vascular networks. This creates a dynamic microenvironment in which cells interact within the matrix. Significant advancements have been made in this field over the past decade, and various strategies have been developed for accelerating and enhancing skin regeneration. The primary challenge for successful skin grafts is the integration of the functional vasculature, which can supply essential nutrients and oxygen to cell-laden structures and damaged native tissues. An inadequate vascular network can lead to ischemia, which can cause slow wound healing—particularly in the case of chronic skin conditions. Therefore, blood vessel formation remains one of the most significant obstacles that skin tissue engineering must overcome to create vascularized skin tissue substitutes with specific living cells. Technological advances can augment effective vascularization. The three-dimensional (3D) bioprinting platform is a promising technology that allows precise deposition of living cells and bioactive materials. The application of this technology to skin tissue engineering can provide solutions for augmenting pre-vascularization in engineered in vitro skin models and in vivo skin substitutes. This review presents the significance of skin vascularization in in vitro modeling and in vivo wound healing. Various strategies and related applications involving 3D bioprinting technology are introduced for the biofabrication of enhanced vascularized skin in vitro and in vivo, followed by a discussion of their limitations and future research directions.

Keywords
Vascularization
Angiogenesis
Human skin
Biofabrication
3D bioprinting
Regenerative medicine
Funding
This work was supported by Pusan National University Research Grant, 2021 and by National Research Foundation of Korea (NRF) grants funded by the Korean government (MSIT) (No. 2022R1A5A2027161, 2022R1C1C1004803, and RS-2023-00214149) and by the Institute of Civil-Military Technology Cooperation funded by the Defense Acquisition Program Administration and Ministry of Trade, Industry, and Energy of the Korean government (No. 22-CM-BR-12).
References
  1. Talikowska M, Fu X, Lisak G. Application of conducting polymers to wound care and skin tissue engineering: a review. Biosens Bioelectron. 2019;135:50-63. doi: 10.1016/j.bios.2019.04.001
  2. Fenner J, Clark RAF. Anatomy, physiology, histology, and immunohistochemistry of human skin. In: Skin Tissue Engineering and Regenerative Medicine. New York: Elsevier; 2016:1-17. doi: 10.1016/B978-0-12-801654-1.00001-2
  3. Pittman RN. Regulation of Tissue Oxygenation. San Rafael, CA:Morgan & Claypool Life Sciences; 2011:1-100. doi: 10.4199/c00029ed1v01y201103isp017
  4. Arroyo JA, Winn VD. Vasculogenesis and Angiogenesis in the IUGR Placenta. In: Seminars in Perinatology. New York: Elsevier; 2008:172-177. doi: 10.1053/j.semperi.2008.02.006
  5. Chouhan D, Dey N, Bhardwaj N, Mandal BB. Emerging and innovative approaches for wound healing and skin regeneration: current status and advances. Biomaterials. 2019;216:119267. doi: 10.1016/j.biomaterials.2019.119267
  6. Winter GD. Effect of air exposure and occlusion on experimental human skin wounds. Nature. 1963;200: 378-379. doi: 10.1038/200377a0
  7. Dhivya S, Padma VV, Santhini E. Wound dressings–a review. BioMedicine. 2015;5(4):22. doi: 10.7603/s40681-015-0022-9
  8. Kamoun EA, Kenawy E-RS, Chen X. A review on polymeric hydrogel membranes for wound dressing applications: PVA-based hydrogel dressings. J Adv Res. 2017;8(3): 217-233. doi: 10.1016/j.jare.2017.01.005
  9. Ahmed S, Ali A, Sheikh J. A review on chitosan centred scaffolds and their applications in tissue engineering. Int J Biol Macromol. 2018;116:849-862. doi: 10.1016/j.ijbiomac.2018.04.176
  10. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407(6801):249-257. doi: 10.1038/35025220
  11. Jain R, Au P, Tam J, Duda DG, Fukumura D. Engineering vascularized tissue. Nat Biotechnol. 2005;23(7):821. doi: 10.1038/nbt0705-821
  12. Bouhadir KH, Mooney DJ. Promoting angiogenesis in engineered tissues. J Drug Targeting. 2001;9(6):397-406. doi: 10.3109/10611860108998775
  13. Utzinger U, Baggett B, Weiss JA, Hoying JB, Edgar LT. Large-scale time series microscopy of neovessel growth during angiogenesis. Angiogenesis. 2015;18:219-232. doi: 10.1007/s10456-015-9461-x
  14. Malda J, Rouwkema J, Martens D, et al. Oxygen gradients in tissue‐engineered PEGT/PBT cartilaginous constructs: measurement and modeling. Biotechnol Bioeng. 2004;86(1):9-18. doi: 10.1002/bit.20038
  15. Hsu Y-C, Li L, Fuchs E. Emerging interactions between skin stem cells and their niches. Nat Med. 2014;20(8):847-856. doi: 10.1038/nm.3643
  16. Nguyen AV, Soulika AM. The dynamics of the skin’s immune system. Int J Mol Sci. 2019;20(8):1811. doi: 10.3390/ijms20081811
  17. Abdo JM, Sopko NA, Milner SM. The applied anatomy of human skin: A model for regeneration. Wound Med. 2020;28:100179. doi: 10.1016/j.wndm.2020.100179
  18. Roger M, Fullard N, Costello L, et al. Bioengineering the microanatomy of human skin. J Anat. 2019;234(4):438-455. doi: 10.1111/joa.12942
  19. Pincelli C, Marconi A. Keratinocyte stem cells: friends and foes. J Cell Physiol. 2010;225(2):310-315. doi: 10.1002/jcp.22275
  20. Clayton K, Vallejo AF, Davies J, Sirvent S, Polak ME. Langerhans cells—programmed by the epidermis. Front Immunol. 2017;8:1676. doi: 10.3389/fimmu.2017.01676
  21. Haeberle H, Lumpkin EA. Merkel cells in somatosensation. Chemosens Percept. 2008;1:110-118. doi: 10.1007/s12078-008-9012-6
  22. Roig-Rosello E, Rousselle P. The human epidermal basement membrane: a shaped and cell instructive platform that aging slowly alters. Biomolecules. 2020;10(12):1607. doi: 10.3390/biom10121607
  23. Prost-Squarcioni C, Fraitag S, Heller M, Boehm N. Functional histology of dermis. Ann Dermatol Venereol. 2008:1S5-20. doi: 10.1016/s0151-9638(08)70206-0
  24. Grinnell F. Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol. 2003;13(5):264-269. doi: 10.1016/s0962-8924(03)00057-6
  25. Muiznieks LD, Keeley FW. Molecular assembly and mechanical properties of the extracellular matrix: a fibrous protein perspective. Biochim Biophys Acta. 2013;1832(7):866-875. doi: 10.1016/j.bbadis.2012.11.022
  26. Moon TC, Befus AD, Kulka M. Mast cell mediators: their differential release and the secretory pathways involved. Front Immunol. 2014;5:569. doi: 10.3389/fimmu.2014.00569
  27. Driskell RR, Jahoda CA, Chuong CM, Watt FM, Horsley V. Defining dermal adipose tissue. Exp Dermatol. 2014;23(9):629-631. doi: 10.1111/exd.12450
  28. Driskell RR, Jahoda CA, Chuong CM, Watt FM, Horsley V. Defining dermal adipose tissue. Exp. Dermatol. 2014; 23(9):629-631. doi: 10.1111/exd.12450
  29. Frueh FS, Menger MD, Lindenblatt N, Giovanoli P, Laschke MW. Current and emerging vascularization strategies in skin tissue engineering. Crit Rev Biotechnol. 2016;37(5): 613-625. doi: 10.1080/07388551.2016.1209157
  30. Hendrickx B, Vranckx JJ, Luttun A. Cell-based vascularization strategies for skin tissue engineering. Tissue Eng Part B Rev. 2011;17(1):13-24. doi: 10.1089/ten.teb.2010.0315
  31. Laschke MW, Menger MD. Prevascularization in tissue engineering: current concepts and future directions. Biotechnol Adv. 2016;34(2):112-121. doi: 10.1016/j.biotechadv.2015.12.004
  32. Laschke M, Menger M. Vascularization in tissue engineering: angiogenesis versus inosculation. Eur Surg Res. 2012;48(2):85-92. doi: 10.1159/000336876
  33. Johnson KE, Wilgus TA. Vascular endothelial growth factor and angiogenesis in the regulation of cutaneous wound repair. Adv Wound Care. 2014;3(10):647-661. doi: 10.1089/wound.2013.0517
  34. Kolte D, McClung JA, Aronow WS. Chapter 6 - Vasculogenesis and angiogenesis. In: Translational Research in Coronary Artery Disease. New York: Elsevier; 2016:49-65. doi: 10.1016/B978-0-12-802385-3.00006-1
  35. Demidova-Rice TN, Durham JT, Herman IM. Wound healing angiogenesis: innovations and challenges in acute and chronic wound healing. Adv Wound Care. 2012;1(1):17-22. doi: 10.1089/wound.2011.0308
  36. Heller M, Bauer HK, Schwab R, et al. The impact of intercellular communication for the generation of complex multicellular prevascularized tissue equivalents. J Biomed Mater Res Part A. 2020;108(3):734-748. doi: 10.1002/jbm.a.36853
  37. Liew AWL, Zhang Y. In vitro pre-vascularization strategies for tissue engineered constructs–Bioprinting and others. Int J Bioprint. 2017;3(1). doi: 10.18063/iib.2017.01.008
  38. Tomasina C, Bodet T, Mota C, Moroni L, Camarero- Espinosa S. Bioprinting vasculature: materials, cells and emergent techniques. Materials. 2019;12(17):2701. doi: 10.3390/ma12172701
  39. Yang G, Mahadik B, Choi JY, Fisher JP. Vascularization in tissue engineering: fundamentals and state-of-art. Prog Biomed Eng. 2020;2(1):012002. doi: 10.1088/2516-1091/ab5637
  40. Richardson RJ. Parallels between vertebrate cardiac and cutaneous wound healing and regeneration. Npj Regener Med. 2018;3(1):21. doi: 10.1038/s41536-018-0059-y
  41. Chandra P, Atala A. Engineering blood vessels and vascularized tissues: technology trends and potential clinical applications. Clin Sci. 2019;133(9):1115-1135. doi: 10.1042/cs20180155
  42. Min S, Ko IK, Yoo JJ. State-of-the-art strategies for the vascularization of three-dimensional engineered organs. Vasc Spec Int. 2019;35(2):77. doi: 10.5758/vsi.2019.35.2.77
  43. Sharma D, Ross D, Wang G, Jia W, Kirkpatrick SJ, Zhao F. Upgrading prevascularization in tissue engineering: a review of strategies for promoting highly organized microvascular network formation. Acta Biomater. 2019;95:112-130. doi: 10.1016/j.actbio.2019.03.016
  44. Takei T, Sakai S, Yoshida M. In vitro formation of vascular-like networks using hydrogels. J Biosci Bioeng. 2016;122(5):519-527. doi: 10.1016/j.jbiosc.2016.03.023
  45. Wong HK, Lam CRI, Wen F, et al. Novel method to improve vascularization of tissue engineered constructs with biodegradable fibers. Biofabrication. 2016;8(1):015004. doi: 10.1088/1758-5090/8/1/015004
  46. Datta P, Ayan B, Ozbolat IT. Bioprinting for vascular and vascularized tissue biofabrication. Acta Biomater. 2017; 51:1-20. doi: 10.1016/j.actbio.2017.01.035
  47. Herrmann M, Binder A, Menzel U, Zeiter S, Alini M, Verrier S. CD34/CD133 enriched bone marrow progenitor cells promote neovascularization of tissue engineered constructs in vivo. Stem Cell Res. 2014;13(3):465-477. doi: 10.1016/j.scr.2014.10.005
  48. Kniebs C, Kreimendahl F, Köpf M, Fischer H, Jockenhoevel S, Thiebes AL. Influence of different cell types and sources on pre-vascularisation in fibrin and agarose–collagen gels. Organogenesis. 2020;16(1):14-26. doi: 10.1080/15476278.2019.1697597
  49. Liu X, Chen W, Zhang C, et al. Co-seeding human endothelial cells with human-induced pluripotent stem cell-derived mesenchymal stem cells on calcium phosphate scaffold enhances osteogenesis and vascularization in rats. Tissue Eng Part A. 2017;23(11-12):546-555. doi: 10.1089/ten.tea.2016.0485
  50. Rouwkema J, Khademhosseini A. Vascularization and angiogenesis in tissue engineering: beyond creating static networks. Trends Biotechnol. 2016;34(9):733-745. doi: 10.1016/j.tibtech.2016.03.002
  51. Sarker M, Chen X, Schreyer D. Experimental approaches to vascularisation within tissue engineering constructs. J Biomater Sci. 2015;26(12):683-734. doi: 10.1080/09205063.2015.1059018
  52. Xiao X, Wang W, Liu D, et al. The promotion of angiogenesis induced by three-dimensional porous beta-tricalcium phosphate scaffold with different interconnection sizes via activation of PI3K/Akt pathways. Sci Rep. 2015;5(1): 9409. doi: 10.1038/srep09409
  53. Xie R, Zheng W, Guan L, Ai Y, Liang Q. Engineering of hydrogel materials with perfusable microchannels for building vascularized tissues. Small. 2020;16(15): 1902838. doi: 10.1002/smll.201902838
  54. Blatchley MR, Hall F, Wang S, Pruitt HC, Gerecht S. Hypoxia and matrix viscoelasticity sequentially regulate endothelial progenitor cluster-based vasculogenesis. Sci Adv. 2019;5(3):eaau7518. doi: 10.1126/sciadv.aau7518
  55. Auger FA, Gibot L, Lacroix D. The pivotal role of vascularization in tissue engineering. Annu Rev Biomed Eng. 2013;15:177-200. doi: 10.1146/annurev-bioeng-071812-152428
  56. Phua QH, Han HA, Soh B-S. Translational stem cell therapy: vascularized skin grafts in skin repair and regeneration. J Transl Med. 2021;19:1-11. doi: 10.1186/s12967-021-02752-2
  57. Gao C, Lu C, Qiao H, et al. Strategies for vascularized skin models in vitro. Biomater Sci. 2022;10(17):4724-4739. doi: 10.1039/d2bm00784c
  58. Baldwin J, Antille M, Bonda U, et al. In vitro pre-vascularisation of tissue-engineered constructs A co-culture perspective. Vasc Cell. 2014;6:1-16. doi: 10.1186/2045-824x-6-13
  59. Costa-Almeida R, Granja P, Soares R, Guerreiro S. Cellular strategies to promote vascularisation in tissue engineering applications. Eur Cell Mater. 2014;28:51-66. doi: 10.22203/ecm.v028a05
  60. Heller M, Frerick-Ochs E, Bauer H-K, et al. Tissue engineered pre-vascularized buccal mucosa equivalents utilizing a primary triculture of epithelial cells, endothelial cells and fibroblasts. Biomaterials. 2016;77:207-215. doi: 10.1016/j.biomaterials.2015.10.073
  61. Um Min Allah N, Berahim Z, Ahmad A, Kannan TP. Biological interaction between human gingival fibroblasts and vascular endothelial cells for angiogenesis: a co-culture perspective. Tissue Eng Regener Med. 2017;14:495-505. doi: 10.1007/s13770-017-0065-y
  62. Weinandy S, Laffar S, Unger RE, et al. Biofunctionalized microfiber-assisted formation of intrinsic three-dimensional capillary-like structures. Tissue Eng Part A. 2014;20(13- 14):1858-1869. doi: 10.1089/ten.tea.2013.0330
  63. Miyazaki H, Tsunoi Y, Akagi T, Sato S, Akashi M, Saitoh D. A novel strategy to engineer pre-vascularized 3-dimensional skin substitutes to achieve efficient, functional engraftment. Sci Rep. 2019;9(1):7797. doi: 10.1038/s41598-019-44113-6
  64. Costa-Almeida R, Gomez-Lazaro M, Ramalho C, Granja PL, Soares R, Guerreiro SG. Fibroblast-endothelial partners for vascularization strategies in tissue engineering. Tissue Eng Part A. 2015;21(5-6):1055-1065. doi: 10.1089/ten.tea.2014.0443
  65. Morin KT, Tranquillo RT. In vitro models of angiogenesis and vasculogenesis in fibrin gel. Exp Cell Res. 2013;319(16): 2409-2417. doi: 10.1016/j.yexcr.2013.06.006
  66. Wan X, Bovornchutichai P, Cui Z, O’Neill E, Ye H. Morphological analysis of human umbilical vein endothelial cells co-cultured with ovarian cancer cells in 3D: an oncogenic angiogenesis assay. PLoS One. 2017;12(7):e0180296. doi: 10.1371/journal.pone.0180296
  67. Ren L, Ma D, Liu B, et al. Preparation of three-dimensional vascularized MSC cell sheet constructs for tissue regeneration. BioMed Res Int. 2014;2014. doi: 10.1155/2014/301279
  68. Liu X, Michael S, Bharti K, Ferrer M, Song MJ. A biofabricated vascularized skin model of atopic dermatitis for preclinical studies. Biofabrication. 2020;12(3):035002. doi: 10.1088/1758-5090/ab76a1
  69. Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32(8):773-785. doi: 10.1038/nbt.2958
  70. Ng WL, Wang S, Yeong WY, Naing MW. Skin bioprinting: impending reality or fantasy? Trends Biotechnol. 2016;34(9):689-699. doi: 10.1016/j.tibtech.2016.04.006
  71. Guillotin B, Guillemot F. Cell patterning technologies for organotypic tissue fabrication. Trends Biotechnol. 2011;29(4):183-190. doi: 10.1016/j.tibtech.2010.12.008
  72. Lee W, Debasitis JC, Lee VK, et al. Multi-layered culture of human skin fibroblasts and keratinocytes through three-dimensional freeform fabrication. Biomaterials. 2009;30(8):1587-1595. doi: 10.1016/j.biomaterials.2008.12.009
  73. Binder KW, Zhao W, Aboushwareb T, Dice D, Atala A, Yoo JJ. In situ bioprinting of the skin for burns. J Am Coll Surg. 2010;211(3):S76. doi: 10.1016/j.jamcollsurg.2010.06.198
  74. Koch L, Deiwick A, Schlie S, et al. Skin tissue generation by laser cell printing. Biotechnol Bioeng. 2012;109(7): 1855-1863. doi: 10.1002/bit.24455
  75. Richards D, Jia J, Yost M, Markwald R, Mei Y. 3D bioprinting for vascularized tissue fabrication. Ann Biomed Eng. 2017;45:132-147. doi: 10.1007/s10439-016-1653-z
  76. Yu J, Park SA, Kim WD, et al. Current advances in 3D bioprinting technology and its applications for tissue engineering. Polymers. 2020;12(12):2958. doi: 10.3390/polym12122958
  77. Klebe RJ. Cytoscribing: a method for micropositioning cells and the construction of two-and three-dimensional synthetic tissues. Exp Cell Res. 1988;179(2):362-373. doi: 10.1016/0014-4827(88)90275-3
  78. Zikulnig J, Kosel J. Fabrication technologies for flexible printed sensors. In: Encyclopedia of Sensors and Biosensors. New York: Elsevier; 2023:33–50. doi: 10.1016/b978-0-12-822548-6.00010-8
  79. Cui X, Boland T. Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials. 2009;30(31):6221-6227. doi: 10.1016/j.biomaterials.2009.07.056
  80. Malda J, Visser J, Melchels FP, et al. 25th anniversary article: engineering hydrogels for biofabrication. Adv Mater. 2013;25(36):5011-5028. doi: 10.1002/adma.201302042
  81. Cui X, Boland T, DD’Lima D, Lotz MK. Thermal inkjet printing in tissue engineering and regenerative medicine. Recent Pat Drug Delivery Formulation. 2012;6(2):149-155. doi: 10.2174/187221112800672949
  82. Cui X, Dean D, Ruggeri ZM, Boland T. Cell damage evaluation of thermal inkjet printed Chinese hamster ovary cells. Biotechnol Bioeng. 2010;106(6):963-969. doi: 10.1002/bit.22762
  83. Ning L, Chen X. A brief review of extrusion‐based tissue scaffold bio‐printing. Biotechnol J. 2017;12(8):1600671. doi: 10.1002/biot.201600671
  84. Kim BS, Lee J-S, Gao G, Cho D-W. Direct 3D cell-printing of human skin with functional transwell system. Biofabrication. 2017;9(2):025034. doi: 10.1088/1758-5090/aa71c8
  85. Ramasamy S, Davoodi P, Vijayavenkataraman S, et al. Optimized construction of a full thickness human skin equivalent using 3D bioprinting and a PCL/collagen dermal scaffold. Bioprinting. 2021;21:e00123. doi: 10.1016/j.bprint.2020.e00123
  86. Park JH, Ahn M, Park SH, et al. 3D bioprinting of a trachea-mimetic cellular construct of a clinically relevant size. Biomaterials. 2021;279:121246. doi: 10.1016/j.biomaterials.2021.121246
  87. Choi Y-J, Jun Y-J, Kim DY, et al. A 3D cell printed muscle construct with tissue-derived bioink for the treatment of volumetric muscle loss. Biomaterials. 2019;206:160-169. doi: 10.1016/j.biomaterials.2019.03.036
  88. Kang H-W, Lee SJ, Ko IK, Kengla C, Yoo JJ, Atala A. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol. 2016;34(3): 312-319. doi: 10.1038/nbt.3413
  89. Ma Y, Wang Y, Chen D, et al. 3D bioprinting of a gradient stiffened gelatin–alginate hydrogel with adipose-derived stem cells for full-thickness skin regeneration. J Mater Chem B. 2023;11(13):2989-3000. doi: 10.1039/d2tb02200a
  90. Pati F, Jang J, Ha D-H, et al. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun. 2014;5(1):3935. doi: 10.1038/ncomms4935
  91. Ahn M, Cho WW, Lee H, et al. Engineering of uniform epidermal layers via sacrificial gelatin bioink‐assisted 3D extrusion bioprinting of skin. Adv Healthc Mater. 2023:2301015. doi: 10.1002/adhm.202301015
  92. Odde DJ, Renn MJ. Laser-guided direct writing for applications in biotechnology. Trends Biotechnol. 1999;17(10):385-389. doi: 10.1016/s0167-7799(99)01355-4
  93. Derakhshanfar S, Mbeleck R, Xu K, Zhang X, Zhong W, Xing M. 3D bioprinting for biomedical devices and tissue engineering: a review of recent trends and advances. Bioact Mater. 2018;3(2):144-156. doi: 10.1016/j.bioactmat.2017.11.008
  94. Li H, Tan C, Li L. Review of 3D printable hydrogels and constructs. Mater Des. 2018;159:20-38. doi: 101016/jmatdes201808023
  95. Donderwinkel I, Van Hest JC, Cameron NR. Bio-inks for 3D bioprinting: recent advances and future prospects. Polym Chem. 2017;8(31):4451-4471. doi: 10.1039/C7PY00826K
  96. Catros S, Guillotin B, Bačáková M, Fricain J-C, Guillemot F. Effect of laser energy, substrate film thickness and bioink viscosity on viability of endothelial cells printed by laser-assisted bioprinting. Appl Surf Sci. 2011;257(12): 5142-5147. doi: 10.1016/j.apsusc.2010.11.049
  97. Magalhães LSS, Santos FEP, Elias CdMV, et al. Printing 3D hydrogel structures employing low-cost stereolithography technology. J Funct Biomater. 2020;11(1):12. doi: 10.3390/jfb11010012
  98. Choi KY, Ajiteru O, Hong H, et al. A digital light processing 3D-printed artificial skin model and full-thickness wound models using silk fibroin bioink. Acta Biomater. 2023;164:159-174. doi: 10.1016/j.actbio.2023.04.034
  99. Zhang G, Zhang Z, Cao G, et al. Engineered dermis loaded with confining forces promotes full-thickness wound healing by enhancing vascularisation and epithelialisation. Acta Biomater. 2023;170:464-478. doi: 10.1016/j.actbio.2023.08.049
  100. Xu T, Binder KW, Albanna MZ, et al. Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication. 2012;5(1):015001. doi: 10.1088/1758-5082/5/1/015001
  101. Gudapati H, Dey M, Ozbolat I. A comprehensive review on droplet-based bioprinting: past, present and future. Biomaterials. 2016;102:20-42. doi: 10.1016/j.biomaterials.2016.06.012
  102. LaBarge W, Morales A, Pretorius D, Kahn-Krell AM, Kannappan R, Zhang J. Scaffold-free bioprinter utilizing layer-by-layer printing of cellular spheroids. Micromachines. 2019;10(9):570. doi: 10.3390/mi10090570
  103. Hakimi N, Cheng R, Leng L, et al. Handheld skin printer: in situ formation of planar biomaterials and tissues. Lab Chip. 2018;18(10):1440-1451. doi: 10.1039/c7lc01236e
  104. Vijayavenkataraman S, Lu W, Fuh J. 3D bioprinting of skin: a state-of-the-art review on modelling, materials, and processes. Biofabrication. 2016;8(3):032001. doi: 10.1088/1758-5090/8/3/032001
  105. Matai I, Kaur G, Seyedsalehi A, McClinton A, Laurencin CT. Progress in 3D bioprinting technology for tissue/organ regenerative engineering. Biomaterials. 2020;226:119536. doi: 10.1016/j.biomaterials.2019.119536
  106. Ning L, Gil CJ, Hwang B, et al. Biomechanical factors in three-dimensional tissue bioprinting. Appl Phys Rev. 2020;7(4):041319. doi: 10.1016/j.biomaterials.2019.119536
  107. Zorlutuna P, Vrana NE, Khademhosseini A. The expanding world of tissue engineering: the building blocks and new applications of tissue engineered constructs. IEEE Rev Biomed Eng. 2012;6:47-62. doi: 10.1109/rbme.2012.2233468
  108. Wang Y, Kankala RK, Ou C, Chen A, Yang Z. Advances in hydrogel-based vascularized tissues for tissue repair and drug screening. Bioact Mater. 2022;9:198-220. doi: 10.1016/j.bioactmat.2021.07.005
  109. Bedell ML, Navara AM, Du Y, Zhang S, Mikos AG. Polymeric systems for bioprinting. Chem Rev. 2020;120(19): 10744-10792. doi: 10.1021/acs.chemrev.9b00834
  110. Nyström A, Bruckner‐Tuderman L. Matrix molecules and skin biology. In: Seminars in Cell & Developmental Biology. New York: Elsevier; 2019;89:136-146. doi: 10.1016/j.semcdb.2018.07.025
  111. Wells A, Nuschke A, Yates CC. Skin tissue repair: matrix microenvironmental influences. Matrix Biol. 2016; 49:25-36. doi: 10.1016/j.matbio.2015.08.001
  112. Dzobo K, Motaung KSCM, Adesida A. Recent trends in decellularized extracellular matrix bioinks for 3D printing: an updated review. Int J Mol Sci. 2019;20(18):4628. doi: 10.3390/ijms20184628
  113. Kim BS, Das S, Jang J, Cho D-W. Decellularized extracellular matrix-based bioinks for engineering tissue-and organ-specific microenvironments. Chem Rev. 2020;120(19): 10608-10661. doi: 10.1021/acs.chemrev.9b00808
  114. Choudhury D, Tun HW, Wang T, Naing MW. Organ-derived decellularized extracellular matrix: a game changer for bioink manufacturing? Trends Biotechnol. 2018;36(8):787-805. doi: 10.1016/j.tibtech.2018.03.003
  115. Kim BS, Kim H, Gao G, Jang J, Cho D-W. Decellularized extracellular matrix: a step towards the next generation source for bioink manufacturing. Biofabrication. 2017;9(3):034104. doi: 10.1088/1758-5090/aa7e98
  116. Kim BS, Kwon YW, Kong J-S, et al. 3D cell printing of in vitro stabilized skin model and in vivo pre-vascularized skin patch using tissue-specific extracellular matrix bioink: A step towards advanced skin tissue engineering. Biomaterials. 2018;168:38-53. doi: 10.1016/j.biomaterials.2018.03.040
  117. Jorgensen AM, Chou Z, Gillispie G, et al. Decellularized skin extracellular matrix (dsECM) improves the physical and biological properties of fibrinogen hydrogel for skin bioprinting applications. Nanomaterials. 2020;10(8):1484. doi: 10.3390/nano10081484
  118. Zhang Q, Johnson JA, Dunne LW, et al. Decellularized skin/ adipose tissue flap matrix for engineering vascularized composite soft tissue flaps. Acta Biomater. 2016;35:166-184. doi: 10.1016/j.actbio.2016.02.017
  119. Parmaksiz M, Elçin AE, Elçin YM. Decellularized bSIS-ECM as a regenerative biomaterial for skin wound repair. Skin Stem Cell Methods Protoc. 2019:175-185. doi: 10.1007/7651_2018_147
  120. Abaci A, Guvendiren M. Designing decellularized extracellular matrix‐based bioinks for 3D bioprinting. Adv Healthc Mater. 2020;9(24):2000734. doi: 10.1002/adhm.202000734
  121. Velasco D, Quílez C, Garcia M, del Cañizo JF, Jorcano JL. 3D human skin bioprinting: a view from the bio side. J 3D Print Med. 2018:141-162. doi: 10.2217/3dp-2018-0008
  122. Hayden P, Ayehunie S, Jackson G, et al. In vitro skin equivalent models for toxicity testing. In: Alternative Toxicological Methods. Boca Raton, FL: CRC Press; 2003:229-247. doi: 10.1201/9780203008799.ch20
  123. Schmook FP, Meingassner JG, Billich A. Comparison of human skin or epidermis models with human and animal skin in in-vitro percutaneous absorption. Int J Pharm. 2001;215(1-2):51-56. doi: 10.1016/s0378-5173(00)00665-7
  124. Almeida A, Sarmento B, Rodrigues F. Insights on in vitro models for safety and toxicity assessment of cosmetic ingredients. Int J Pharm. 2017;519(1-2):178-185. doi: 10.1016/j.ijpharm.2017.01.024
  125. Liebsch M, Grune B, Seiler A, et al. Alternatives to animal testing: current status and future perspectives. Arch Toxicol. 2011;85:841-858. doi: 10.1007/s00204-011-0718-x
  126. Yanez M, Rincon J, Dones A, De Maria C, Gonzales R, Boland T. In vivo assessment of printed microvasculature in a bilayer skin graft to treat full-thickness wounds. Tissue Eng Part A. 2015;21(1-2):224-233. doi: 10.1089/ten.tea.2013.0561
  127. Kim BS, Gao G, Kim JY, Cho DW. 3D cell printing of perfusable vascularized human skin equivalent composed of epidermis, dermis, and hypodermis for better structural recapitulation of native skin. Adv Healthc Mater. 2019;8(7):1801019. doi: 10.1002/adhm.201801019
  128. Abaci HE, Coffman A, Doucet Y, et al. Tissue engineering of human hair follicles using a biomimetic developmental approach. Nat Commun. 2018;9(1):5301. doi: 10.1038/s41467-018-07579-y
  129. Pontiggia L, Van Hengel IA, Klar A, et al. Bioprinting and plastic compression of large pigmented and vascularized human dermo-epidermal skin substitutes by means of a new robotic platform. J Tissue Eng. 2022;13:20417314221088513. doi: 10.1177/20417314221088513
  130. Naomi R, Ridzuan PM, Bahari H. Current insights into collagen type I. Polymers. 2021;13(16):2642. doi: 10.3390/polym13162642
  131. Zhang X, Li J, Ye P, Gao G, Hubbell K, Cui X. Coculture of mesenchymal stem cells and endothelial cells enhances host tissue integration and epidermis maturation through AKT activation in gelatin methacryloyl hydrogel-based skin model. Acta Biomater. 2017;59: 317-326. doi: 10.1016/j.actbio.2017.07.001
  132. Baltazar T, Merola J, Catarino C, et al. Three dimensional bioprinting of a vascularized and perfusable skin graft using human keratinocytes, fibroblasts, pericytes, and endothelial cells. Tissue Eng Part A. 2020;26(5-6):227-238. doi: 10.1089/ten.tea.2019.0201
  133. Kolesky DB, Homan KA, Skylar-Scott MA, Lewis JA. Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci. 2016;113(12):3179-3184. doi: 10.1073/pnas.1521342113
  134. Ng WL, Qi JTZ, Yeong WY, Naing MW. Proof-of-concept: 3D bioprinting of pigmented human skin constructs. Biofabrication. 2018;10(2):025005. doi: 10.1088/1758-5090/aa9e1e
  135. Ma J, Qin C, Wu J, et al. 3D printing of strontium silicate microcylinder‐containing multicellular biomaterial inks for vascularized skin regeneration. Adv Healthc Mater. 2021;10(16):2100523. doi: 10.1002/adhm.202100523
  136. Heinemann S, Coradin T, Desimone MF. Bio-inspired silica–collagen materials: applications and perspectives in the medical field. Biomater Sci. 2013;1(7):688-702. doi: 10.1039/c3bm00014a
  137. Desimone MF, Hélary C, Mosser G, Giraud-Guille M-M, Livage J, Coradin T. Fibroblast encapsulation in hybrid silica–collagen hydrogels. J Mater Chem. 2010;20(4): 666-668. doi: 10.1039/B921572G
  138. Desimone MF, Hélary C, Rietveld IB, et al. Silica–collagen bionanocomposites as three-dimensional scaffolds for fibroblast immobilization. Acta Biomater. 2010;6(10): 3998-4004. doi: 10.1016/j.actbio.2010.05.014
  139. Pouroutzidou GK, Liverani L, Theocharidou A, et al. Synthesis and characterization of mesoporous mg-and sr-doped nanoparticles for moxifloxacin drug delivery in promising tissue engineering applications. Int J Mol Sci. 2021;22(2):577. doi: 10.3390/ijms22020577
  140. Mao L, Xia L, Chang J, et al. The synergistic effects of Sr and Si bioactive ions on osteogenesis, osteoclastogenesis and angiogenesis for osteoporotic bone regeneration. Acta Biomater. 2017;61:217-232. doi: 10.1016/j.actbio.2017.08.015
  141. Dikici S, Claeyssens F, MacNeil S. Bioengineering vascular networks to study angiogenesis and vascularization of physiologically relevant tissue models in vitro. ACS Biomater Sci Eng. 2020;6(6):3513-3528. doi: 10.1021/acsbiomaterials.0c00191
  142. Abaci HE, Guo Z, Coffman A, et al. Human skin constructs with spatially controlled vasculature using primary and iPSC‐derived endothelial cells. Adv Healthc Mater. 2016;5(14):1800-1807. doi: 10.1002/adhm.201500936
  143. Schneider J, Biedermann T, Widmer D, et al. Matriderm® versus Integra®: a comparative experimental study. Burns. 2009;35(1):51-57. doi: 10.1016/j.burns.2008.07.018
  144. Choi SW, Zhang Y, MacEwan MR, Xia Y. Neovascularization in biodegradable inverse opal scaffolds with uniform and precisely controlled pore sizes. Adv Healthc Mater. 2013;2(1):145-154. doi: 10.1002/adhm.201200106
  145. van Zuijlen PP, Vloemans JF, van Trier AJ, et al. Dermal substitution in acute burns and reconstructive surgery: a subjective and objective long-term follow-up. Plast Reconstr Surg. 2001;108(7):1938-1946. doi: 10.1097/00006534-200112000-00014
  146. Ring A, Langer S, Schaffran A, et al. Enhanced neovascularization of dermis substitutes via low-pressure plasma-mediated surface activation. Burns. 2010;36(8):1222-1227. doi: 10.1016/j.burns.2010.03.002
  147. Shaterian A, Borboa A, Sawada R, et al. Real-time analysis of the kinetics of angiogenesis and vascular permeability in an animal model of wound healing. Burns. 2009;35(6):811-817. doi: 10.1016/j.burns.2008.12.012
  148. Supp DM, Boyce ST. Engineered skin substitutes: practices and potentials. Clin Dermatol. 2005;23(4):403-412. doi: 10.1016/j.clindermatol.2004.07.023
  149. Cam C, Zhu S, Truong NF, Scumpia PO, Segura T. Systematic evaluation of natural scaffolds in cutaneous wound healing. J Mater Chem B. 2015;3(40):7986-7992. doi: 10.1039/c5tb00807g
  150. Griffin M, Naderi N, Kalaskar D, Seifalian A, Butler P. Argon plasma surface modification promotes the therapeutic angiogenesis and tissue formation of tissue-engineered scaffolds in vivo by adipose-derived stem cells. Stem Cell Res Ther. 2019;10:1-14. doi: 10.1186/s13287-019-1195-z
  151. Liu Q, Huang Y, Lan Y, et al. Acceleration of skin regeneration in full‐thickness burns by incorporation of bFGF‐loaded alginate microspheres into a CMCS–PVA hydrogel. J Tissue Eng Regener Med. 2017;11(5):1562-1573. doi: 10.1002/term.2057
  152. Guo R, Xu S, Ma L, Huang A, Gao C. Enhanced angiogenesis of gene-activated dermal equivalent for treatment of full thickness incisional wounds in a porcine model. Biomaterials. 2010;31(28):7308-7320. doi: 10.1016/j.biomaterials.2010.06.013
  153. Guo R, Xu S, Ma L, Huang A, Gao C. The healing of full-thickness burns treated by using plasmid DNA encoding VEGF-165 activated collagen–chitosan dermal equivalents. Biomaterials. 2011;32(4):1019-1031. doi: 10.1016/j.biomaterials.2010.08.087
  154. Yang Y, Xia T, Chen F, et al. Electrospun fibers with plasmid bFGF polyplex loadings promote skin wound healing in diabetic rats. Mol Pharm. 2012;9(1):48-58. doi: 10.1021/mp200246b
  155. Reckhenrich AK, Hopfner U, Krötz F, et al. Bioactivation of dermal scaffolds with a non-viral copolymer-protected gene vector. Biomaterials. 2011;32(7):1996-2003. doi: 10.1016/j.biomaterials.2010.11.022
  156. Scherer SS, Pietramaggiori G, Matthews J, et al. Poly-N-acetyl glucosamine nanofibers: a new bioactive material to enhance diabetic wound healing by cell migration and angiogenesis. Ann Surg. 2009;250(2):322-330. doi: 10.1097/sla.0b013e3181ae9d45
  157. Zhao S, Li L, Wang H, et al. Wound dressings composed of copper-doped borate bioactive glass microfibers stimulate angiogenesis and heal full-thickness skin defects in a rodent model. Biomaterials. 2015;53:379-391. doi: 10.1016/j.biomaterials.2015.02.112
  158. Wang X, You C, Hu X, et al. The roles of knitted mesh-reinforced collagen–chitosan hybrid scaffold in the one-step repair of full-thickness skin defects in rats. Acta Biomater. 2013;9(8):7822-7832. doi: 10.1016/j.actbio.2013.04.017
  159. 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. 2011;108(52):20976-20981. doi: 10.1073/pnas.1115973108
  160. Hohlfeld J, de Buys Roessingh A, Hirt-Burri N, et al. Tissue engineered fetal skin constructs for paediatric burns. Lancet. 2005;366(9488):840-842. doi: 10.1016/s0140-6736(05)67107-3
  161. Tonello C, Zavan B, Cortivo R, Brun P, Panfilo S, Abatangelo G. In vitro reconstruction of human dermal equivalent enriched with endothelial cells. Biomaterials. 2003;24(7):1205-1211. doi: 10.1016/s0142-9612(02)00450-7
  162. Hudon V, Berthod F, Black A, Damour O, Germain L, Auger F. A tissue‐engineered endothelialized dermis to study the modulation of angiogenic and angiostatic molecules on capillary‐like tube formation in vitro. Br J Dermatol. 2003;148(6):1094-1104. doi: 10.1046/j.1365-2133.2003.05298.x
  163. Black AF, Berthod F, L’Heureux N, Germain L, Auger FA. In vitro reconstruction of a human capillary‐like network in a tissue‐engineered skin equivalent. FASEB J. 1998;12(13):1331-1340. doi: 10.1046/j.1365-2133.2003.05298.x
  164. Tremblay P-L, Hudon V, Berthod F, Germain L, Auger FA. Inosculation of tissue-engineered capillaries with the host’s vasculature in a reconstructed skin transplanted on mice. Am J Transplant. 2005;5(5):1002-1010. doi: 10.1111/j.1600-6143.2005.00790.x
  165. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275(5302):964-966. doi: 10.1126/science.275.5302.964
  166. Sander AL, Jakob H, Henrich D, et al. Systemic transplantation of progenitor cells accelerates wound epithelialization and neovascularization in the hairless mouse ear wound model. J Surg Res. 2011;165(1):165-170. doi: 10.1016/j.jss.2009.07.003
  167. Ingram DA, Mead LE, Tanaka H, et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104(9):2752-2760. doi: 10.1182/blood-2004-04-1396
  168. Kaushal S, Amiel GE, Guleserian KJ, et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med. 2001;7(9):1035-1040. doi: 10.1038/nm0901-1035
  169. Hendrickx B, Verdonck K, Van den Berge S, et al. Integration of blood outgrowth endothelial cells in dermal fibroblast sheets promotes full thickness wound healing. Stem Cell. 2010;28(7):1165-1177. doi: 10.1002/stem.445
  170. Tiruvannamalai Annamalai R, Rioja AY, Putnam AJ, Stegemann JP. Vascular network formation by human microvascular endothelial cells in modular fibrin microtissues. ACS Biomater Sci Eng. 2016;2(11):1914-1925. doi: 10.1021/acsbiomaterials.6b00274
  171. Kinnaird T, Stabile E, Burnett M, et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res. 2004;94(5):678-685. doi: 10.1161/01.res.0000118601.37875.ac
  172. Yoshikawa T, Mitsuno H, Nonaka I, et al. Wound therapy by marrow mesenchymal cell transplantation. Plast Reconstr Surg. 2008;121(3):860-877. doi: 10.1097/01.prs.0000299922.96006.24
  173. Moioli EK, Clark PA, Chen M, et al. Synergistic actions of hematopoietic and mesenchymal stem/progenitor cells in vascularizing bioengineered tissues. PLoS One. 2008;3(12):e3922. doi: 10.1371/journal.pone.0003922
  174. Liu P, Deng Z, Han S, et al. Tissue‐engineered skin containing mesenchymal stem cells improves burn wounds. Artif Organs. 2008;32(12):925-931. doi: 10.1111/j.1525-1594.2008.00654.x
  175. Altman AM, Yan Y, Matthias N, et al. IFATS collection: human adipose-derived stem cells seeded on a silk fibroin-chitosan scaffold enhance wound repair in a murine soft tissue injury model. Stem Cell. 2009;27(1):250-258. doi: 10.1634/stemcells.2008-0178
  176. Gang E, Jeong J, Han S, Yan Q, Jeon C, Kim H. In vitro endothelial potential of human UC blood-derived mesenchymal stem cells. Cytotherapy. 2006;8(3): 215-227. doi: 10.1080/14653240600735933
  177. Koponen JK, Kekarainen T, Heinonen SE, et al. Umbilical cord blood–derived progenitor cells enhance muscle regeneration in mouse hindlimb ischemia model. Mol Ther. 2007;15(12):2172-2177. doi: 10.1038/sj.mt.6300302
  178. Wang Z, Zheng L, Lian C, Qi Y, Li W, Wang S. Human umbilical cord-derived mesenchymal stem cells relieve hind limb ischemia by promoting angiogenesis in mice. Stem Cell Dev. 2019;28(20):1384-1397. doi: 10.1089/scd.2019.0115
  179. Chen X, Yue Z, Winberg PC, Lou Y-R, Beirne S, Wallace GG. 3D bioprinting dermal-like structures using species-specific ulvan. Biomater Sci. 2021;9(7):2424-2438. doi: 10.1039/d0bm01784a
  180. Liu P, Shen H, Zhi Y, et al. 3D bioprinting and in vitro study of bilayered membranous construct with human cells-laden alginate/gelatin composite hydrogels. Colloid Surf B. 2019;181:1026-1034. doi: 10.1016/j.colsurfb.2019.06.069
  181. Lee V, Singh G, Trasatti JP, et al. Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng Part C. 2014;20(6):473-484. doi: 10.1089/ten.tec.2013.0335
  182. Shi Y, Xing T, Zhang H, et al. Tyrosinase-doped bioink for 3D bioprinting of living skin constructs. Biomed Mater. 2018;13(3):035008. doi: 10.1088/1748-605x/aaa5b6
  183. Huang S, Yao B, Xie J, Fu X. 3D bioprinted extracellular matrix mimics facilitate directed differentiation of epithelial progenitors for sweat gland regeneration. Acta Biomater. 2016;32:170-177. doi: 10.1016/j.actbio.2015.12.039
  184. Wang S, Xiong Y, Chen J, et al. Three dimensional printing bilayer membrane scaffold promotes wound healing. Front Bioeng Biotechnol. 2019;7:348. doi: 10.3389/fbioe.2019.00348
  185. Zidarič T, Milojević M, Gradišnik L, Stana Kleinschek K, Maver U, Maver T. Polysaccharide-based bioink formulation for 3D bioprinting of an in vitro model of the human dermis. Nanomaterials. 2020;10(4):733. doi: 10.3390/nano10040733
  186. Intini C, Elviri L, Cabral J, et al. 3D-printed chitosan-based scaffolds: an in vitro study of human skin cell growth and an in-vivo wound healing evaluation in experimental diabetes in rats. Carbohydr Polym. 2018;199: 593-602. doi: 10.1016/j.carbpol.2018.07.057
  187. Ng WL, Yeong WY, Naing MW. Development of polyelectrolyte chitosan-gelatin hydrogels for skin bioprinting. Procedia Cirp. 2016;49:105-112. doi: 10.1016/j.procir.2015.09.002
  188. Cubo N, Garcia M, Del Canizo JF, Velasco D, Jorcano JL. 3D bioprinting of functional human skin: production and in vivo analysis. Biofabrication. 2016;9(1):015006. doi: 10.1088/1758-5090/9/1/015006
  189. Hafezi F, Shorter S, Tabriz AG, et al. Bioprinting and preliminary testing of highly reproducible novel bioink for potential skin regeneration. Pharmaceutics. 2020;12(6):550. doi: 10.3390/pharmaceutics12060550
  190. Kwak H, Shin S, Lee H, Hyun J. Formation of a keratin layer with silk fibroin-polyethylene glycol composite hydrogel fabricated by digital light processing 3D printing. J Ind Eng Chem. 2019;72:232-240. doi: 10.1016/j.jiec.2018.12.023
  191. Azadmanesh F, Pourmadadi M, Zavar Reza J, Yazdian F, Omidi M, Haghirosadat BF. Synthesis of a novel nanocomposite containing chitosan as a three‐dimensional printed wound dressing technique: Emphasis on gene expression. Biotechnol Prog. 2021;37(4):e3132. doi: 10.1002/btpr.3132
Conflict of interest
The authors declare no conflicts of interest.
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International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
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