Published in Issue 2018-05-12
How to Cite
Augustine, R. (2018). Skin bioprinting: a novel approach for creating artificial skin from synthetic and natural building blocks. Progress in Biomaterials, 7(2 (June 2018). https://doi.org/10.1007/s40204-018-0087-0
Abstract
Abstract Significant progress has been made over the past few decades in the development of in vitro-engineered substitutes that mimic human skin, either as grafts for the replacement of lost skin, or for the establishment of in vitro human skin models. Tissue engineering has been developing as a novel strategy by employing the recent advances in various fields such as polymer engineering, bioengineering, stem cell research and nanomedicine. Recently, an advancement of 3D printing technology referred as bioprinting was exploited to make cell loaded scaffolds to produce constructs which are more matching with the native tissue. Bioprinting facilitates the simultaneous and highly specific deposition of multiple types of skin cells and biomaterials, a process that is lacking in conventional skin tissue-engineering approaches. Bioprinted skin substitutes or equivalents containing dermal and epidermal components offer a promising approach in skin bioengineering. Various materials including synthetic and natural biopolymers and cells with or without signalling molecules like growth factors are being utilized to produce functional skin constructs. This technology emerging as a novel strategy to overcome the current bottle-necks in skin tissue engineering such as poor vascularization, absence of hair follicles and sweat glands in the construct.Keywords
- Bioprinting,
- Skin,
- Skin substitutes,
- Wound healing,
- Tissue engineering
References
- Aasen et al. (2008) Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes (pp. 1276-1284) https://doi.org/10.1038/nbt.1503
- Abrigo et al. (2014) Electrospun nanofibers as dressings for chronic wound care: advances, challenges, and future prospects (pp. 772-792) https://doi.org/10.1002/mabi.201300561
- An et al. (2016) A Perspective on 4D Bioprinting https://doi.org/10.18063/IJB.2016.01.003
- Antoine et al. (2014) Review of Collagen I Hydrogels for Bioengineered Tissue Microenvironments: characterization of Mechanics, Structure, and Transport (pp. 683-696) https://doi.org/10.1089/ten.teb.2014.0086
- Armentano et al. (2010) Biodegradable polymer matrix nanocomposites for tissue engineering: a review 95(11) (pp. 2126-2146) https://doi.org/10.1016/j.polymdegradstab.2010.06.007
- Ataç et al. (2013) Skin and hair on-a-chip: in vitro skin models versus ex vivo tissue maintenance with dynamic perfusion https://doi.org/10.1039/c3lc50227a
- Athenstaedt et al. (1982) Epidermis of human skin: pyroelectric and piezoelectric sensor layer (pp. 1018-1020) https://doi.org/10.1126/science.6177041
- Augustine et al. (2013) Biopolymers for health, food, and cosmetic applications (pp. 801-849) Wiley https://doi.org/10.1002/9783527652457.ch27
- Augustine et al. (2014) Investigation of angiogenesis and its mechanism using zinc oxide nanoparticle-loaded electrospun tissue engineering scaffolds (pp. 51528-51536) https://doi.org/10.1039/C4RA07361D
- Augustine et al. (2014) Advancement of wound care from grafts to bioengineered smart skin substitutes (pp. 103-113) https://doi.org/10.1007/s40204-014-0030-y
- Augustine et al. (2015) Electrospun poly(ε-caprolactone)-based skin substitutes: in vivo evaluation of wound healing and the mechanism of cell proliferation (pp. 1445-1454) https://doi.org/10.1002/jbm.b.33325
- Augustine et al. (2016) Fabrication and characterization of biosilver nanoparticles loaded calcium pectinate nano-micro dual-porous antibacterial wound dressings (pp. 223-235) https://doi.org/10.1007/s40204-016-0060-8
- Augustine et al. (2016) Clogging-Free Electrospinning of Polycaprolactone Using Acetic Acid/Acetone Mixture (pp. 518-529) https://doi.org/10.1080/03602559.2015.1036451
- Augustine et al. (2016) Effect of zinc oxide nanoparticles on the in vitro degradation of electrospun polycaprolactone membranes in simulated body fluid (pp. 28-37) https://doi.org/10.1080/00914037.2015.1055628
- Augustine et al. (2017) Electrospun poly(vinylidene fluoride-trifluoroethylene)/zinc oxide nanocomposite tissue engineering scaffolds with enhanced cell adhesion and blood vessel formation (pp. 1-19) https://doi.org/10.1007/s12274-017-1549-8
- Augustine et al. (2017) Microbial barrier property and blood compatibility studies of electrospun Poly-ƹ-caprolactone/zinc oxide nanocomposite scaffolds (pp. 226-226) https://doi.org/10.17516/1997-1389-0025
- Augustine et al. (2017) Electrospun polycaprolactone (PCL) scaffolds embedded with europium hydroxide nanorods (EHNs) with enhanced vascularization and cell proliferation for tissue engineering applications (pp. 4660-4672) https://doi.org/10.1039/C7TB00518K
- Bertassoni et al. (2014) Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels https://doi.org/10.1088/1758-5082/6/2/024105
- Bonab et al. (2006) Aging of mesenchymal stem cell in vitro https://doi.org/10.1186/1471-2121-7-14
- Braziulis et al. (2012) Modified plastic compression of collagen hydrogels provides an ideal matrix for clinically applicable skin substitutes (pp. 464-474) https://doi.org/10.1089/ten.tec.2011.0561
- Brohem et al. (2011) Artificial skin in perspective: concepts and applications (pp. 35-50) https://doi.org/10.1111/j.1755-148X.2010.00786.x
- Caporali et al. (2017) Contribution of pericyte paracrine regulation of the endothelium to angiogenesis (pp. 56-64) https://doi.org/10.1016/j.pharmthera.2016.10.001
- Carrow et al. (2015) Polymers for bioprinting (pp. 229-248) Texas A&M University https://doi.org/10.1016/B978-0-12-800972-7.00013-X
- Chen et al. (2012) Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels (pp. 2027-2039) https://doi.org/10.1002/adfm.201101662
- Choi et al. (2015) 4D printing technology: a review (pp. 159-167) https://doi.org/10.1089/3dp.2015.0039
- Cifra et al. (2011) Electromagnetic cellular interactions (pp. 223-246) https://doi.org/10.1016/j.pbiomolbio.2010.07.003
- Cinar et al. (2009) Effects of a specially pulsed electric field on an animal model of wound healing (pp. 735-740) https://doi.org/10.1007/s10103-008-0631-6
- Colosi et al. (2017) Microfluidic Bioprinting of Heterogeneous 3D Tissue Constructs (pp. 369-380) Humana Press https://doi.org/10.1007/978-1-4939-7021-6_26
- Coyer et al. (2015) Reducing pressure injuries in critically ill patients by using a patient skin integrity care bundle (inspire) (pp. 199-209) https://doi.org/10.4037/ajcc2015930
- Cubo et al. (2016) 3D bioprinting of functional human skin: production and in vivo analysis https://doi.org/10.1088/1758-5090/9/1/015006
- Cui et al. (2016) Hierarchical Fabrication of Engineered Vascularized Bone Biphasic Constructs via Dual 3D Bioprinting: integrating Regional Bioactive Factors into Architectural Design (pp. 2174-2181) https://doi.org/10.1002/adhm.201600505
- Dababneh and Ozbolat (2014) Bioprinting technology: a current state-of-the-art review https://doi.org/10.1115/1.4028512
- Dai et al. (2017) Novel low temperature (< 37 & #xB0;C) chitosan hydrogel fabrication under the synergistic effect of graphene oxide (pp. 671-676) https://doi.org/10.1039/C6NJ03509D
- Das et al. (2015) Bioprintable, cell-laden silk fibroin-gelatin hydrogel supporting multilineage differentiation of stem cells for fabrication of three-dimensional tissue constructs (pp. 233-246) https://doi.org/10.1016/j.actbio.2014.09.023
- Debels et al. (2015) Dermal matrices and bioengineered skin substitutes: a critical review of current options https://doi.org/10.1097/GOX.0000000000000219
- Duarte Campos et al. (2016) Bioprinting organotypic hydrogels with improved mesenchymal stem cell remodeling and mineralization properties for bone tissue engineering (pp. 1336-1345) https://doi.org/10.1002/adhm.201501033
- Engler et al. (2006) Matrix elasticity directs stem cell lineage specification (pp. 677-689) https://doi.org/10.1016/j.cell.2006.06.044
- Foda et al. (2011) Models of human thermoregulation and the prediction of local and overall thermal sensations (pp. 2023-2032) https://doi.org/10.1016/j.buildenv.2011.04.010
- Gao et al. (2014) Bioactive nanoparticles stimulate bone tissue formation in bioprinted three-dimensional scaffold and human mesenchymal stem cells (pp. 1304-1311) https://doi.org/10.1002/biot.201400305
- Gao et al. (2016) 4D Bioprinting for Biomedical Applications (pp. 746-756) https://doi.org/10.1016/j.tibtech.2016.03.004
- Groeber et al. (2011) Skin tissue engineering—In vivo and in vitro applications (pp. 352-366) https://doi.org/10.1016/j.addr.2011.01.005
- Gudapati et al. (2014) Alginate gelation-induced cell death during laser-assisted cell printing https://doi.org/10.1088/1758-5082/6/3/035022
- Hassanzadeh et al. (2016) Ultrastrong and flexible hybrid hydrogels based on solution self-assembly of chitin nanofibers in gelatin methacryloyl (GelMA) (pp. 2539-2543) https://doi.org/10.1039/C6TB00021E
- Heijmen et al. (1997) Cross-linking of dermal sheep collagen with tannic acid (pp. 749-754) https://doi.org/10.1016/S0142-9612(96)00202-5
- Hendrickx et al. (2011) Cell-Based Vascularization Strategies for Skin Tissue Engineering (pp. 13-24) https://doi.org/10.1089/ten.teb.2010.0315
- Hinsenkamp et al. (1997) Effects of low frequency pulsed electrical current on keratinocytes in vitro (pp. 250-254) https://doi.org/10.1002/(SICI)1521-186X(1997)18:3<250::AID-BEM8>3.0.CO;2-1
- Hockaday et al. (2012) Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogel scaffolds https://doi.org/10.1088/1758-5082/4/3/035005
- Hölzl et al. (2016) Bioink properties before, during and after 3D bioprinting https://doi.org/10.1088/1758-5090/8/3/032002
- Horiuchi et al. (2010) A wound protector shields incision sites from bacterial invasion (pp. 501-503) https://doi.org/10.1089/sur.2009.072
- Hospodiuk et al. (2017) The bioink: a comprehensive review on bioprintable materials (pp. 217-239) https://doi.org/10.1016/j.biotechadv.2016.12.006
- Hou et al. (2017) Interplay between materials and microfluidics https://doi.org/10.1038/natrevmats.2017.16
- Huang et al. (2016) 3D bioprinted extracellular matrix mimics facilitate directed differentiation of epithelial progenitors for sweat gland regeneration (pp. 170-177) https://doi.org/10.1016/j.actbio.2015.12.039
- Hutmacher et al. (2004) Hutmacher, DW; Sittinger, M; Risbud, MV. Scaffold-based tissue engineering: rationale for computer-aided design and solid free-form fabrication systems (pp. 2003-2003) https://doi.org/10.1016/j.tibtech.2004.05.005
- Jank et al. (2017) Creation of a bioengineered skin flap scaffold with a perfusable vascular pedicle (pp. 696-707) https://doi.org/10.1089/ten.tea.2016.0487
- Jia et al. (2014) Engineering alginate as bioink for bioprinting (pp. 4323-4331) https://doi.org/10.1016/j.actbio.2014.06.034
- Jia et al. (2016) Direct 3D bioprinting of perfusable vascular constructs using a blend bioink (pp. 58-68) https://doi.org/10.1016/j.biomaterials.2016.07.038
- Kamel et al. (2013) Tissue engineering of skin (pp. 533-555) https://doi.org/10.1016/j.jamcollsurg.2013.03.027
- Kang et al. (2016) A 3D bioprinting system to produce human-scale tissue constructs with structural integrity (pp. 312-319) https://doi.org/10.1038/nbt.3413
- Kang et al. (2017) Optimizing photo-encapsulation viability of heart valve cell types in 3D printable composite hydrogels (pp. 360-377) https://doi.org/10.1007/s10439-016-1619-1
- Kanitakis (2002) Anatomy, histology and immunohistochemistry of normal human skin (pp. 390-399)
- Koch et al. (2012) Skin tissue generation by laser cell printing (pp. 1855-1863) https://doi.org/10.1002/bit.24455
- Koch et al. (2015) Bioprinting for Skin (pp. 281-306) Academic Press https://doi.org/10.1016/B978-0-12-800547-7.00013-8
- Lee et al. (2010) Bio-printing of collagen and VEGF-releasing fibrin gel scaffolds for neural stem cell culture (pp. 645-652) https://doi.org/10.1016/j.expneurol.2010.02.014
- Lei and Wang (2016) Biodegradable polymers and stem cells for bioprinting https://doi.org/10.3390/molecules21050539
- Li et al. (2016) Recent advances in bioprinting techniques: approaches, applications and future prospects https://doi.org/10.1186/s12967-016-1028-0
- Liu et al. (2013) Reprogramming of mesenchymal stem cells derived from iPSCs seeded on biofunctionalized calcium phosphate scaffold for bone engineering (pp. 7862-7872) https://doi.org/10.1016/j.biomaterials.2013.07.029
- Liu et al. (2016) Full-thickness wound healing using 3D bioprinted gelatin-alginate scaffolds in mice: a histopathological study (pp. 11197-11205)
- MacNeil (2007) Progress and opportunities for tissue-engineered skin (pp. 874-880) https://doi.org/10.1038/nature05664
- Mandrycky et al. (2016) 3D bioprinting for engineering complex tissues (pp. 422-434) https://doi.org/10.1016/j.biotechadv.2015.12.011
- Markstedt et al. (2015) 3D bioprinting human chondrocytes with nanocellulose-alginate bioink for cartilage tissue engineering applications (pp. 1489-1496) https://doi.org/10.1021/acs.biomac.5b00188
- McBeth et al. (2017) 3D bioprinting of GelMA scaffolds triggers mineral deposition by primary human osteoblasts https://doi.org/10.1088/1758-5090/aa53bd
- Metcalfe and Ferguson (2007) Tissue engineering of replacement skin: the crossroads of biomaterials, wound healing, embryonic development, stem cells and regeneration (pp. 413-437) https://doi.org/10.1098/rsif.2006.0179
- Metcalfe and Ferguson (2007) Tissue engineering of replacement skin : the crossroads of biomaterials, wound healing, embryonic development, stem cells and regeneration (pp. 413-437) https://doi.org/10.1098/rsif.2006.0179
- Michael et al. (2013) Tissue engineered skin substitutes created by laser-assisted bioprinting form skin-like structures in the dorsal skin fold chamber in mice https://doi.org/10.1371/journal.pone.0057741
- Bishop and Mostafa (2017) 3-D bioprinting technologies in tissue engineering and regenerative medicine: Current and future trends (pp. 185-195) https://doi.org/10.1016/j.gendis.2017.10.002
- Moreno et al. (2010) Crosslinking of poly(vinyl alcohol) using functionalized gold nanoparticles (pp. 2099-2104) https://doi.org/10.1016/j.eurpolymj.2010.09.010
- Müller et al. (2013) Printing Thermoresponsive reverse molds for the creation of patterned two-component hydrogels for 3d cell culture https://doi.org/10.3791/50632
- Müller et al. (2015) Nanostructured Pluronic hydrogels as bioinks for 3D bioprinting https://doi.org/10.1088/1758-5090/7/3/035006
- Murphy and Atala (2014) 3D bioprinting of tissues and organs (pp. 773-785) https://doi.org/10.1038/nbt.2958
- Murphy and Atala (2014) 3D bioprinting of tissues and organs (pp. 773-785) https://doi.org/10.1038/nbt.2958
- Murphy et al. (2013) Evaluation of hydrogels for bio-printing applications (pp. 272-284) https://doi.org/10.1002/jbm.a.34326
- Nandagopal et al. (2016) Gentamicin loaded electrospun poly(ε-Caprolactone)/TiO2/nanocomposite membranes with antibacterial property against methicillin resistant staphylococcus aureus (pp. 1785-1796) https://doi.org/10.1080/03602559.2016.1171877
- Narayanan et al. (2016) 3D-Bioprinting of polylactic acid (PLA) nanofiber-alginate hydrogel bioink containing human adipose-derived stem cells (pp. 1732-1742) https://doi.org/10.1021/acsbiomaterials.6b00196
- Ng et al. (2016) Skin bioprinting: impending reality or fantasy? (pp. 689-699) https://doi.org/10.1016/j.tibtech.2016.04.006
- Ng et al. (2016) Polyelectrolyte gelatin-chitosan hydrogel optimized for 3D bioprinting in skin tissue engineering https://doi.org/10.18063/IJB.2016.01.009
- Nunery (2001) Risk of prion transmission with the use of xenografts and allografts in surgery (pp. 389-394) https://doi.org/10.1097/00002341-200111000-00001
- O’Connell et al. (2016) Development of the Biopen: a handheld device for surgical printing of adipose stem cells at a chondral wound site https://doi.org/10.1088/1758-5090/8/1/015019
- Ozbolat (2016) Elsevier
- Ozbolat and Hospodiuk (2016) Current advances and future perspectives in extrusion-based bioprinting (pp. 321-343) https://doi.org/10.1016/j.biomaterials.2015.10.076
- Ozbolat and Yu (2013) Bioprinting toward organ fabrication: challenges and future trends (pp. 691-699) https://doi.org/10.1109/TBME.2013.2243912
- Park et al. (2016) Three-dimensional electrospun silk-fibroin nanofiber for skin tissue engineering https://doi.org/10.1016/j.ijbiomac.2016.07.047
- Pelaez et al. (2009) Cyclic compression maintains viability and induces chondrogenesis of human mesenchymal stem cells in fibrin gel scaffolds (pp. 93-102) https://doi.org/10.1089/scd.2008.0030
- Pescosolido et al. (2011) Hyaluronic acid and dextran-based semi-IPN hydrogels as biomaterials for bioprinting (pp. 1831-1838) https://doi.org/10.1021/bm200178w
- Plouffe et al. (2009) Controlled capture and release of cardiac fibroblasts using peptide-functionalized alginate gels in microfluidic channels https://doi.org/10.1039/b823523f
- Powell et al. (2008) Influence of electrospun collagen on wound contraction of engineered skin substitutes (pp. 834-843) https://doi.org/10.1016/j.biomaterials.2007.10.036
- Recek et al. (2016) Cell adhesion on polycaprolactone modified by plasma treatment https://doi.org/10.1155/2016/7354396
- Rezwan et al. (2006) Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering (pp. 3413-3431) https://doi.org/10.1016/j.biomaterials.2006.01.039
- Rho et al. (2006) Electrospinning of collagen nanofibers: effects on the behavior of normal human keratinocytes and early-stage wound healing (pp. 1452-1461) https://doi.org/10.1016/j.biomaterials.2005.08.004
- Richards et al. (2017) 3D bioprinting for vascularized tissue fabrication (pp. 132-147) https://doi.org/10.1007/s10439-016-1653-z
- Schuurman et al. (2011) Bioprinting of hybrid tissue constructs with tailorable mechanical properties https://doi.org/10.1088/1758-5082/3/2/021001
- Sears et al. (2016) A review of three-dimensional printing in tissue engineering (pp. 298-310) https://doi.org/10.1089/ten.teb.2015.0464
- Sekine et al. (2013) In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels https://doi.org/10.1038/ncomms2406
- Shafiee et al. (2011) Nasal septum-derived multipotent progenitors: a potent source for stem cell-based regenerative medicine (pp. 2077-2091) https://doi.org/10.1089/scd.2010.0420
- Shevchenko et al. (2010) A review of tissue-engineered skin bioconstructs available for skin reconstruction (pp. 229-258) https://doi.org/10.1098/rsif.2009.0403
- Skardal et al. (2010) Photocrosslinkable hyaluronan-gelatin hydrogels for two-step bioprinting (pp. 2675-2685) https://doi.org/10.1089/ten.tea.2009.0798
- Skardal et al. (2012) Bioprinted Amniotic Fluid-Derived Stem Cells Accelerate Healing of Large Skin Wounds (pp. 792-802) https://doi.org/10.5966/sctm.2012-0088
- Smith et al. (2016) Human iPSC-derived cardiomyocytes and tissue engineering strategies for disease modeling and drug screening (pp. 77-94) https://doi.org/10.1016/j.biotechadv.2016.12.002
- Stanton et al. (2015) Bioprinting of 3D hydrogels (pp. 3111-3115) https://doi.org/10.1039/C5LC90069G
- Sun and Tan (2013) Alginate-based biomaterials for regenerative medicine applications (pp. 1285-1309) https://doi.org/10.3390/ma6041285
- Tabriz et al. (2015) Three-dimensional bioprinting of complex cell laden alginate hydrogel structures https://doi.org/10.1088/1758-5090/7/4/045012
- Tautzenberger et al. (2010) Effect of functionalised fluorescence-labelled nanoparticles on mesenchymal stem cell differentiation (pp. 2064-2071) https://doi.org/10.1016/j.biomaterials.2009.11.099
- Tran and Wen (2014) Rapid prototyping technologies for tissue regeneration (pp. 97-155) Woodhead publishing https://doi.org/10.1533/9780857097217.97
- Verseijden et al. (2010) Prevascular structures promote vascularization in engineered human adipose tissue constructs upon implantation (pp. 1007-1020) https://doi.org/10.3727/096368910X492571
- Walker and Smith (1996) The role of percutaneous penetration enhancers (pp. 295-301) https://doi.org/10.1016/0169-409X(95)00078-L
- Wang et al. (2015) A simple and high-resolution stereolithography-based 3D bioprinting system using visible light crosslinkable bioinks https://doi.org/10.1088/1758-5090/7/4/045009
- Wufuer et al. (2016) Skin-on-a-chip model simulating inflammation, edema and drug-based treatment https://doi.org/10.1038/srep37471
- Xiong et al. (2017) A gelatin-sulfonated silk composite Scaffold based on 3D printing technology enhances skin regeneration by stimulating epidermal growth and dermal neovascularization https://doi.org/10.1038/s41598-017-04149-y
- Xu et al. (2013) Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology (pp. 130-139) https://doi.org/10.1016/j.biomaterials.2012.09.035
- Xu et al. (2014) Study of droplet formation process during drop-on-demand inkjetting of living cell-laden bioink (pp. 9130-9138) https://doi.org/10.1021/la501430x
- Yang et al. (2017) Perspective: fabrication of integrated organ-on-a-chip via bioprinting https://doi.org/10.1063/1.4982945
- Yeo and Kim (2014) Cell-printed hierarchical scaffolds consisting of micro-sized polycaprolactone (PCL) and electrospun PCL nanofibers/cell-laden alginate struts for tissue regeneration (pp. 314-324) https://doi.org/10.1039/C3TB21163K
- Zein et al. (2002) Fused deposition modeling of novel scaffold architectures for tissue engineering applications (pp. 1169-1185) https://doi.org/10.1016/S0142-9612(01)00232-0
- Zhang et al. (2017) Printing-induced cell injury evaluation during laser printing of 3T3 mouse fibroblasts https://doi.org/10.1088/1758-5090/aa6ed9
- Zhao et al. (2016) Photocrosslinkable gelatin hydrogel for epidermal tissue engineering (pp. 108-118) https://doi.org/10.1002/adhm.201500005
- Zhu et al. (2017) Gold nanocomposite bioink for printing 3d cardiac constructs https://doi.org/10.1002/adfm.201605352
- Zöller et al. (2014) Clinical application of a tissue-cultured skin autograft: an alternative for the treatment of non-healing or slowly healing wounds? (pp. 190-198) https://doi.org/10.1159/000362927
10.1007/s40204-018-0087-0