Fibrin-based Bioinks: New Tricks from an Old Dog

Anastasia Shpichka^1,2*, Daria Osipova¹, Yuri Efremov¹, Polina Bikmulina¹, Nastasia Kosheleva^3,4, Marina Lipina⁵, Evgeny A. Bezrukov⁶, Roman B. Sukhanov⁶, Anna B. Solovieva⁷, Massoud Vosough⁸, Peter Timashev^1,2,7,9

Show Less

¹ Department of Advanced Biomaterials, Institute for Regenerative Medicine, Sechenov First Moscow State Medical University, Moscow, Russia

² Department of Chemistry, Lomonosov Moscow State University, Moscow, Russia

³ Department of Molecular and Cell Pathophysiology, FSBSI Institute of General Pathology and Pathophysiology, Moscow, Russia

⁴ Department of Embryology, Lomonosov Moscow State University, Faculty of Biology, Moscow, Russia

⁵ Department of Traumatology, Orthopedics and Disaster Surgery, Sechenov First Moscow State Medical University, Moscow, Russia

⁶ Department of Urology, Sechenov First Moscow State Medical University, Moscow, Russia

⁷ Department of Polymers and Composites, NN Semenov Institute of Chemical Physics, Moscow, Russia

⁸ Department of Regenerative Medicine, Cell Science Research Centre, Royan Institute for Stem Cell Biology and Technology, ACECR, Tehran, Iran

⁹ Institute of Photon Technologies, Federal Research Center Crystallography and Photonics RAS, Moscow, Russia

IJB 2020, 6(3), 269 https://doi.org/10.18063/ijb.v6i3.269

© Invalid date 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/ )

Download PDF

Cite

XML

Abstract

For the past 10 years, the main efforts of most bioprinting research teams have focused on creating new bioink formulations, rather than inventing new printing set-up concepts. New tissue-specific bioinks with good printability, shape fidelity, and biocompatibility are based on “old” (well-known) biomaterials, particularly fibrin. While the interest in fibrin-based bioinks is constantly growing, it is essential to provide a framework of material’s properties and trends. This review aims to describe the fibrin properties and application in three-dimensional bioprinting and provide a view on further development of fibrin-based bioinks.

Keywords

Fibrin

Bioink

Tissue engineering

Regenerative medicine

Bioprinting

Biofabrication

References

1. Antoshin AA, Churbanov SN, Minaev NV, et al., 2019, LIFTbioprinting, is it Worth it? Bioprinting, 15: e00052. DOI: 10.1016/j.bprint.2019.e00052.

2. Jiang T, Munguia-Lopez JG, Flores-Torres S, et al., 2019, Extrusion Bioprinting of Soft Materials: An Emerging Technique for Biological Model Fabrication. Appl Phys Rev, 6:011310. DOI: 10.1063/1.5059393.

3. Gudapati H, Dey M, Ozbolat I, 2016, A Comprehensive Review on Droplet-based Bioprinting: Past, Present and Future. Biomaterials, 102:20–42. DOI: 10.1016/j.biomaterials.2016.06.012.

4. Unagolla JM, Jayasuriya AC, 2020, Hydrogel-based 3D Bioprinting: A Comprehensive Review on Cellladen Hydrogels, Bioink Formulations, and Future Perspectives. Appl Mater Today, 18:100479. DOI: 10.1016/j.apmt.2019.100479.

5. Kurniawan NA, Van Kempen TH, Sonneveld S, et al., 2017, Buffers Strongly Modulate Fibrin Self-Assembly into Fibrous Networks. Langmuir, 33:6342–52. DOI: 10.1021/acs.langmuir.7b00527.

6. Kurniawan NA, Grimbergen J, Koopman J, et al., 2014, Factor XIII Stiffens Fibrin Clots by Causing Fiber Compaction. J Thromb Haemost, 12:1687–96. DOI: 10.1111/jth.12705.

7. Weisel JW, Litvinov RI, 2017, Fibrin Formation, Structure and Properties. Subcell Biochem, 82:405–56.

8. Kim E, Kim OV, Machlus KR, et al., 2011, Correlation between Fibrin Network Structure and Mechanical Properties: An Experimental and Computational Analysis. Soft Matter, 7:4983–92. DOI: 10.1039/c0sm01528h.

9. Brown AE, Litvinov RI, Discher DE, et al., 2009, Multiscale Mechanics of Fibrin Polymer: Gel Stretching with Protein Unfolding and Loss of Water. Science, 325:741–4. DOI: 10.4016/12254.01

10. Mosesson MW, 2005, Fibrinogen and Fibrin Structure and Functions. J Thromb Haemost, 3:1894–904.

11. Fuss C, Palmaz JC, Sprague EA, 2001, Fibrinogen: Structure, Function, and Surface Interactions. J Vasc Interv Radiol, 12:677–82.

12. Kattula S, Byrnes JR, Wolberg AS, 2017, Fibrinogen and Fibrin in Hemostasis and Thrombosis. Arterioscler Thromb Vasc Biol, 37: e13–e21. DOI: 10.1161/atvbaha.117.308564.

13. Fish RJ, Neerman-Arbez M, 2012, Fibrinogen Gene Regulation. Thromb Haemost, 108:419–26. DOI: 10.1160/th12-04-0273.

14. Yang Z, Mochalkin I, Doolittle RF, 2000, A Model of Fibrin Formation Based on Crystal Structures of Fibrinogen and Fibrin Fragments Complexed with Synthetic Peptides. Proc Natl Acad Sci U S A, 97:14156–61. DOI: 10.1073/pnas.97.26.14156.

15. Chapin JC, Hajjar KA, 2015, Fibrinolysis and the Control of Blood Coagulation. Blood Rev, 29:17–24. DOI: 10.1016/j.blre.2014.09.003.

16. Cesarman-Maus G, Hajjar KA, 2005, Molecular Mechanisms of Fibrinolysis. Br J Haematol, 129:307-21. DOI: 10.1111/j.1365-2141.2005.05444.x.

17. Litvinov RI, Weisel JW, 2017, Fibrin Mechanical Properties and their Structural Origins. Matrix Biol, 60–61:110–23. DOI: 10.1016/j.matbio.2016.08.003.

18. Janmey PA, Amis EJ, Ferry JD, 1983, Rheology of Fibrin Clots. VI. Stress Relaxation, Creep, and Differential Dynamic Modulus of Fine Clots in Large Shearing Deformations. J Rheol, 27:135–53. DOI: 10.1122/1.549722.

19. Martens TP, Godier AF, Parks JJ, et al., 2009, Percutaneous Cell Delivery into the Heart Using Hydrogels Polymerizing in Situ. Cell Transplant, 18:297–304. DOI: 10.3727/096368909788534915.

20. Metry G, Adhikarla R, Schneditz D, et al., 2011, Effect of Changes in the Intravascular Volume during Hemodialysis on Blood Viscoelasticity. Indian J Nephrol, 21:95. DOI: 10.4103/0971-4065.82139.

21. Zhao H, Ma L, Zhou J, et al., 2008, Fabrication and Physical and Biological Properties of Fibrin gel Derived from Human Plasma. Biomed Mater, 3:1–10. DOI: 10.1088/1748-6041/3/1/015001.

22. Roberts WW, Lorand L, Mockros LF, 1973, Viscoelastic Properties of Fibrin Clots. Biorheology, 10:29–42. DOI: 10.3233/bir-1973-10105.

23. Weisel JW, 2004, The Mechanical Properties of Fibrin for Basic Scientists and Clinicians. Biophys Chem, 112:267–76.

24. Carr ME, Shen LL, Hermans J, 1976, A Physical Standard of Fibrinogen: Measurement of the Elastic Modulus of Dilute Fibrin Gels with a New Elastometer. Anal Biochem, 72:202–11. DOI: 10.1016/0003-2697(76)90522-4.

25. Kaibara M, 1973, Dynamic Viscoelastic Study of the Formation of Fibrin Networks in Fibrinogen-Thrombin Systems and Plasma. Biorheology, 10:61–73. DOI: 10.3233/bir-1973-10109.

26. Kim OV, Litvinov RI, Weisel JW, et al., 2014, Structural Basis for the Nonlinear Mechanics of Fibrin Networks under Compression. Biomaterials, 35:6739–49. DOI: 10.1016/j.biomaterials.2014.04.056.

27. Shpichka AI, Konarev PV, Efremov YM, et al., 2020, Digging Deeper: Structural Background of PEGylated Fibrin Gels in Cell Migration and Lumenogenesis. RSC Adv, 10:4190–200. DOI: 10.1039/c9ra08169k.

28. Jaramillo M, Singh SS, Velankar S, et al., 2015, Inducing Endoderm Differentiation by Modulating Mechanical Properties of Soft Substrates. J Tissue Eng Regen Med, 9:1–12. DOI: 10.1002/term.1602.

29. Shapira-Schweitzer K, Seliktar D, 2007, Matrix Stiffness Affects Spontaneous Contraction of Cardiomyocytes Cultured within a PEGylated Fibrinogen Biomaterial. Acta Biomater, 3:33–41. DOI: 10.1016/j.actbio.2006.09.003.

30. Jansen KA, Bacabac RG, Piechocka IK, et al., 2013, Cells Actively Stiffen Fibrin Networks by Generating Contractile Stress. Biophys J, 105:2240–51. DOI: 10.1016/j.bpj.2013.10.008.

31. Panwar A, Tan LP, 2016, Current Status of Bioinks for Microextrusion-based 3D Bioprinting. Molecules, 21:685. DOI: 10.3390/molecules21060685.

32. Zhao Y, Yao R, Ouyang L, et al., 2014, Three-Dimensional Printing of Hela Cells for Cervical Tumor Model in Vitro. Biofabrication, 6:035001. DOI: 10.1088/1758-5082/6/3/035001.

33. Xu W, Wang X, Yan Y, et al., 2007, Rapid Prototyping ThreeDimensional Cell/Gelatin/Fibrinogen Constructs for Medical Regeneration. J Bioact Compat Polym, 22:363–77.

34. Shikanov A, Xu M, Woodruff TK, et al., 2009, Interpenetrating Fibrin Alginate Matrices for in Vitro Ovarian Follicle Development. Biomaterials, 30:5476–85. DOI: 10.1016/j.biomaterials.2009.06.054.

35. Lai VK, Lake SP, Frey CR, et al., 2012, Mechanical Behavior of Collagen-Fibrin Co-Gels Reflects Transition from Series to Parallel Interactions with Increasing Collagen Content. J Biomech Eng, 134:011004. DOI: 10.1115/1.4005544.

36. England S, Rajaram A, Schreyer DJ, et al., 2017, Bioprinted Fibrin-factor XIII-Hyaluronate Hydrogel Scaffolds with Encapsulated Schwann Cells and their in vitro Characterization for use in Nerve Regeneration. Bioprinting, 5:1–9. DOI:10.1016/j.bprint.2016.12.001.

37. Han J, Kim DS, Jang H, et al., 2019, Bioprinting of Threedimensional Dentin Pulp Complex with Local Differentiation of Human Dental Pulp Stem Cells. J Tissue Eng, 10:2041731419845849. DOI: 10.1177/2041731419845849.

38. Weigandt KM, White N, Chung D, et al., 2012, Fibrin Clot Structure and Mechanics Associated with Specific Oxidation of Methionine Residues in Fibrinogen. Biophys J, 103:2399–407. DOI: 10.1016/j.bpj.2012.10.036.

39. Duong H, Wu B, Tawil B, 2009, Modulation of 3D Fibrin Matrix Stiffness by Intrinsic Fibrinogen-thrombin Compositions and by Extrinsic Cellular Activity. Tissue Eng Part A, 15:1865–76. DOI: 10.1089/ten.tea.2008.0319.

40. Shpichka A, Butnaru D, Bezrukov EA, et al., 2019, Skin Tissue Regeneration for Burn Injury. Stem Cell Res Ther, 10:1–16. DOI: 10.1186/s13287-019-1203-3.

41. Murphy KC, Whitehead J, Zhou D, et al., 2017, Engineering Fibrin Hydrogels to Promote the Wound Healing Potential of Mesenchymal Stem Cell Spheroids. Acta Biomater, 64:176– 86. DOI: 10.1016/j.actbio.2017.10.007.

42. Krasna M, Planinsek F, Knezevic M, et al., 2005, Evaluation of a Fibrin-based Skin Substitute Prepared in a Defined Keratinocyte Medium. Int J Pharm, 291:31–7. DOI: 10.1016/j.ijpharm.2004.07.040.

43. Idrus RB, Rameli MA, Low KC, et al., 2014, Full-thickness Skin wound Healing Using Autologous Keratinocytes and Dermal Fibroblasts with Fibrin: Bilayered Versus SingleLayered Substitute. Adv Ski Wound Care, 27:171–80. DOI: 10.1097/01.asw.0000445199.26874.9d.

44. Falanga V, Iwamoto S, Chartier M, et al., 2007, Autologous Bone Marrow-derived Cultured Mesenchymal Stem Cells Delivered in a Fibrin Spray Accelerate Healing in Murine and Human Cutaneous Wounds. Tissue Eng, 13:1299–312. DOI: 10.1089/ten.2006.0278.

45. Mendez JJ, Ghaedi M, Sivarapatna A, et al., 2015, Mesenchymal Stromal Cells form Vascular Tubes when Placed in Fibrin Sealant and Accelerate wound Healing in vivo. Biomaterials, 40:61–71. DOI: 10.1016/j.biomaterials.2014.11.011.

46. Losi P, Briganti E, Errico C, et al., 2013, Fibrin-based Scaffold Incorporating VEGF and bFGF-Loaded Nanoparticles Stimulates Wound Healing in Diabetic Mice. Acta Biomater, 9:7814–21. DOI: 10.1016/j.actbio.2013.04.019.

47. Mittermayr R, Branski L, Moritz M, et al., 2016, Fibrin Biomatrix-conjugated Platelet-derived Growth Factor AB Accelerates wound Healing in Severe Thermal Injury. J Tissue Eng Regen Med, 10:E275–85. DOI: 10.1002/term.1749.

48. Muhamed I, Sproul EP, Ligler FS, et al., 2019, Fibrin Nanoparticles Coupled with Keratinocyte Growth Factor Enhance the Dermal Wound-Healing Rate. ACS Appl Mater Interfaces, 11:3771–80. DOI: 10.1021/acsami.8b21056.

49. Dohan DM, Choukroun J, Diss A, et al., 2006, Platelet-rich Fibrin (PRF): A Second-generation Platelet Concentrate. Part I: Technological Concepts and Evolution. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 101:37–44. DOI: 10.1016/j.tripleo.2005.07.008.

50. Choukroun J, Diss A, Simonpieri A, et al., 2006, Plateletrich Fibrin (PRF): A Second-generation Platelet Concentrate. Part IV: Clinical Effects on Tissue Healing. Oral Surg Oral Med Oral Pathol Oral Radiol
Endodontol, 101:56–60. DOI: 10.1016/j.tripleo.2005.07.011.

51. Dohan DM, Choukroun J, Diss A, et al., 2006, Platelet-rich Fibrin (PRF): A Second-generation Platelet Concentrate. Part II: Platelet-related Biologic Features. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol, 101:45–50. DOI: 10.1016/j.tripleo.2005.07.009.

52. Dohan DM, Choukroun J, Diss A, et al., 2006, Platelet-rich Fibrin (PRF): A Second-generation Platelet Concentrate. Part III: Leucocyte Activation: A New Feature for Platelet Concentrates? Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol, 101:51–5. DOI: 10.1016/j.tripleo.2005.07.010.

53. Miron RJ, Fujioka-Kobayashi M, Bishara M, et al., 2017, Platelet-Rich Fibrin and Soft Tissue Wound Healing: A Systematic Review. Tissue Eng Part B Rev, 23:83–99. DOI: 10.1089/ten.teb.2016.0233.

54. Anitua E, Nurden P, Prado R, et al., 2019, Autologous Fibrin Scaffolds: When Platelet and Plasma-derived Biomolecules Meet Fibrin. Biomaterials, 192:440–60. DOI: 10.1016/j.biomaterials.2018.11.029.

55. Nandi S, Sproul EP, Nellenbach K, et al., 2019, Platelet-like Particles Dynamically Stiffen Fibrin Matrices and Improve Wound Healing Outcomes. Biomater Sci, 7:669–82. DOI:10.1039/c8bm01201f.

56. Schense JC, Bloch J, Aebischer P, et al., 2000, Enzymatic Incorporation of Bioactive Peptides into Fibrin Matrices Enhances Neurite Extension. Nat Biotechnol, 18:415–9. DOI:10.1038/74473.

57. Galler KM, Cavender AC, Koeklue U, et al., 2011, Bioengineering of Dental Stem Cells in a PEGylated Fibrin Gel. Regen Med, 6:191–200. DOI: 10.2217/rme.11.3.

58. Gorkun AA, Shpichka AI, Zurina IM, et al., 2018, Angiogenic Potential of Spheroids from Umbilical Cord and Adiposederived Multipotent Mesenchymal Stromal Cells within Fibrin Gel. Biomed Mater, 13(4):44108. DOI: 10.1088/1748-605x/aac22d.

59. Ehrbar M, Zeisberger SM, Raeber GP, et al., 2008, The Role of Actively Released Fibrin-Conjugated VEGF for VEGF Receptor 2 Gene Activation and the Enhancement of Angiogenesis. Biomaterials, 29:1720–9. DOI: 10.1016/j.biomaterials.2007.12.002.

60. Liang MS, Andreadis ST, 2011, Engineering Fibrin-binding TGF-β1 for Sustained Signaling and Contractile Function of MSC Based Vascular Constructs. Biomaterials, 32:8684–93. DOI: 10.1016/j.biomaterials.2011.07.079.

61. Loureiro J, Torres AL, Neto T, et al., 2019, Conjugation of the T1 Sequence from CCN1 to Fibrin Hydrogels for Therapeutic Vascularization. Mater Sci Eng C, 104:109847. DOI: 10.1016/j.msec.2019.110514.

62. Zhao N, Suzuki A, Zhang X, et al., 2019, Dual AptamerFunctionalized In Situ Injectable Fibrin Hydrogel for Promotion of Angiogenesis via Codelivery of Vascular Endothelial Growth Factor and Platelet-Derived Growth Factor-BB. ACS Appl Mater Interfaces, 11:18123–32. DOI: 10.1021/acsami.9b02462.

63. Mittermayr R, Slezak P, Haffner N, et al., 2016, Controlled Release of Fibrin Matrix-Conjugated Platelet Derived Growth Factor Improves Ischemic Tissue Regeneration by Functional Angiogenesis. Acta Biomater, 29:11–20. DOI: 10.1016/j. actbio.2015.10.028.

64. Michlits W, Mittermayr R, Schäfer R, et al., 2007, Fibrinembedded Administration of VEGF Plasmid Enhances Skin Flap Survival. Wound Repair Regen, 15:360–7. DOI: 10.1111/j.1524-475x.2007.00238.x.

65. Mooney R, Tawil B, Mahoney M, 2010, Specific Fibrinogen and Thrombin Concentrations Promote Neuronal Rather than Glial Growth when Primary Neural Cells are Seeded within Plasma-derived Fibrin Gels. Tissue Eng Part A, 16:1607–19. DOI: 10.1089/ten.tea.2009.0372.

66. Shpichka AI, Koroleva AV, Deiwick A, et al., 2017, Evaluation of the Vasculogenic Potential of Hydrogels Based on Modified Fibrin. Cell Tissue Biol, 11:81–7. DOI: 10.1134/s1990519x17010126.

67. Shpichka AI, Revkova VA, Aksenova NA, et al., 2018, Transparent PEG-fibrin Gel as a Flexible Tool for Cell Encapsulation. Sovrem Technol Med, 10:64–9. DOI: 10.17691/stm2018.10.1.08.

68. Hall H, Baechi T, Hubbell JA, 2001, Molecular Properties of Fibrin-based Matrices for Promotion of Angiogenesis In Vitro. Microvasc Res, 62:315–26. DOI: 10.1006/mvre.2001.2348.

69. Bayless KJ, Salazar R, Davis GE, 2000, RGD-dependent Vacuolation and Lumen Formation Observed During Endothelial Cell Morphogenesis in Three-dimensional Fibrin Matrices Involves the Alpha(v) Beta(3) and Alpha(5)beta(1) Integrins. Am J Pathol, 156:1673–83. DOI: 10.1016/s0002- 9440(10)65038-9.

70. Bach TL, Barsigian C, Yaen CH, et al., 1998, Endothelial Cell VE-cadherin Functions as a Receptor for the β15-42 Sequence of Fibrin. J Biol Chem, 273:30719–28. DOI:10.1074/jbc.273.46.30719.

71. Carrion B, Kong YP, Kaigler D, et al., 2013, Bone Marrowderived Mesenchymal Stem Cells Enhance Angiogenesis via their α6β1 Integrin Receptor. Exp Cell Res, 319:2964–76.DOI: 10.1016/j.yexcr.2013.09.007.

72. Juliar BA, Keating MT, Kong YP, et al., 2018, Sprouting Angiogenesis Induces Significant Mechanical Heterogeneities and ECM Stiffening Across Length Scales in Fibrin Hydrogels. Biomaterials, 162:99–108. DOI: 10.1016/j.biomaterials.2018.02.012.

73. Funahashi Y, Shawber CJ, Sharma A, et al., 2011, Notch Modulates VEGF Action in Endothelial Cells by Inducing Matrix Metalloprotease Activity. Vasc Cell, 3:2. DOI: 10.1186/2045-824x-3-2.

74. Thi MU, Trocmé C, Montmasson MP, et al., 2012, Investigating Metalloproteinases MMP-2 and MMP-9 Mechanosensitivity to Feedback Loops Involved in the Regulation of in vitro Angiogenesis by Endogenous Mechanical Stresses. Acta Biotheor, 60:21–40. DOI: 10.1007/s10441-012-9147-3.

75. Lafleur MA, Handsley MM, Knäuper V, et al., 2002, EC tubulogenisis in fibrin requires MT-MMPs. J Cell Sci, 115:3427–38.

76. Kachgal S, Carrion B, Janson IA, et al., 2012, Bone Marrow Stromal Cells Stimulate an Angiogenic Program that Requires Endothelial MT1-MMP. J Cell Physiol, 227:3546–55. DOI:10.1002/jcp.24056.

77. Ghajar CM, Kachgal S, Kniazeva E, et al., 2010, Mesenchymal Cells Stimulate Capillary Morphogenesis via Distinct Proteolytic Mechanisms. Exp Cell Res, 316:813–25. DOI: 10.1016/j.yexcr.2010.01.013.

78. Urech L, Bittermann AG, Hubbell JA, et al., 2005, Mechanical Properties, Proteolytic Degradability and Biological Modifications Affect Angiogenic Process Extension Into Native and Modified Fibrin Matrices In Vitro. Biomaterials, 26:1369–79. DOI: 10.1016/j.biomaterials.2004.04.045.

79. Koroleva A, Deiwick A, Nguyen A, et al., 2016, Hydrogelbased Microfluidics for Vascular Tissue Engineering. BioNanoMaterials, 17:19–32. DOI: 10.1515/bnm-2015-0026.

80. Morin KT, Smith AO, Davis GE, et al., 2013, Aligned Human Microvessels Formed in 3D Fibrin Gel by Constraint of Gel Contraction. Microvasc Res, 90:12–22. DOI: 10.1016/j.mvr.2013.07.010.

81. Bootle-Wilbraham CA, Tazzyman S, Thompson WD, et al., 2001, Fibrin Fragment E Stimulates the
Proliferation, Migration and Differentiation of Human Microvascular Endothelial Cells In Vitro. Angiogenesis, 4:269–75. DOI: 10.1023/a:1016076121918.

82. Thompson WD, Smith EB, Stirk CM, et al., 1992, Angiogenic Activity of Fibrin Degradation Products is Located in Fibrin Fragment E. J Pathol, 168:47–53. DOI: 10.1002/path.1711680109.

83. Jozkowicz A, Fügl A, Nanobashvili J, et al., 2003, Delivery of High dose VEGF Plasmid Using Fibrin Carrier does Not Influence its Angiogenic Potency. Int J Artif Organs, 26(2):161–9. DOI: 10.1177/039139880302600211.

84. Noori A, Ashrafi SJ, Vaez-Ghaemi R, et al., 2017, A Review of Fibrin and Fibrin Composites for Bone Tissue Engineering. Int J Nanomed, 12:4937–61. DOI: 10.2147/ijn.s124671.

85. Blache U, Ehrbar M, 2018, Inspired by Nature: Hydrogels as Versatile Tools for Vascular Engineering. Adv Wound Care, 7:232–46. DOI: 10.1089/wound.2017.0760.

86. Li Y, Meng H, Liu Y, et al., 2015, Fibrin Gel as an Injectable Biodegradable Scaffold and Cell Carrier for Tissue Engineering. Sci World J, 2015:685690. DOI: 10.1155/2015/685690.

87. Cubo N, Garcia M, Del Cañizo JF, et al., 2017, 3D Bioprinting of Functional Human Skin: Production and In Vivo Analysis. Biofabrication, 9:15006. DOI: 10.1088/1758-5090/9/1/015006.

88. Albanna M, Binder KW, Murphy SV, et al., 2019, In Situ Bioprinting of Autologous Skin Cells Accelerates Wound Healing of Extensive Excisional Full-Thickness Wounds. Sci Rep, 9:1–15. DOI: 10.1038/s41598-018-38366-w.

89. Kumar SA, Alonzo M, Allen SC, et al., 2019, A Visible LightCross-Linkable, Fibrin-Gelatin-Based Bioprinted Construct with Human Cardiomyocytes and Fibroblasts. ACS Biomater Sci Eng, 5:4551–63. DOI: 10.1021/acsbiomaterials.9b00505.

90. Wang Z, Lee SJ, Cheng H, et al., 2018, 3D Bioprinted Functional and Contractile Cardiac Tissue Constructs. Acta Biomater, 70:48–56. DOI: 10.1016/j.actbio.2018.02.007.

91. Oztan YC, Nawafleh N, Zhou Y, et al., 2020, Recent Advances on Utilization of Bioprinting for Tumor Modeling. Bioprinting, 18:e00079. DOI: 10.1016/j.bprint.2020.e00079.

92. Lee C, Abelseth E, de la Vega L, et al., 2019, Bioprinting a Novel Glioblastoma Tumor Model Using a Fibrin-based Bioink for Drug Screening. Mater Today Chem, 12:78–84. DOI: 10.1016/j.mtchem.2018.12.005.

93. Piard C, Jeyaram A, Liu Y, et al., 2019, 3D Printed HUVECs/MSCs Cocultures Impact Cellular Interactions and Angiogenesis Depending on Cell-cell Distance. Biomaterials, 222:119423. DOI: 10.1016/j.biomaterials.2019.119423.

94. Zhang K, Fu Q, Yoo J, et al., 2017, 3D Bioprinting of Urethra with PCL/PLCL Blend and Dual Autologous Cells in Fibrin Hydrogel: An In Vitro Evaluation of Biomimetic Mechanical Property and Cell Growth Environment. Acta Biomater, 50:154–64. DOI: 10.1016/j.actbio.2016.12.008.

95. Freeman S, Ramos R, Chando PA, et al., 2019, A Bioink Blend for Rotary 3D Bioprinting Tissue Engineered Smalldiameter Vascular Constructs. Acta Biomater, 95:152–64. DOI: 10.1016/j.actbio.2019.06.052.

96. Koch L, Deiwick A, Franke A, et al., 2018, Laser Bioprinting of Human Induced Pluripotent Stem Cells the Effect of Printing and Biomaterials on Cell Survival, Pluripotency, and Differentiation. Biofabrication, 10:35005. DOI: 10.1088/1758-5090/aab981.

97. Gruene M, Pflaum M, Hess C, et al., 2011, Laser Printing of Three-dimensional Multicellular Arrays for Studies of Cellcell and Cell-environment Interactions. Tissue Eng Part C Methods, 17:973–82. DOI: 10.1089/ten.tec.2011.0185.

98. O’Donnell N, Okkelman IA, Timashev P, et al., 2018, Cellulose-based Scaffolds for Fluorescence Lifetime Imaging-assisted Tissue Engineering. Acta Biomater, 80:85–96. DOI: 10.1016/j.actbio.2018.09.034.

99. McQuilten ZK, Bailey M, Cameron PA, et al., 2017, Fibrinogen Concentration and Use of Fibrinogen Supplementation with Cryoprecipitate in Patients with Critical Bleeding Receiving Massive Transfusion: A Bi-national Cohort Study. Br J Haematol, 179:131–41. DOI: 10.1111/bjh.14804.

100. Ahlfeld T, Cubo-Mateo N, Cometta S, et al., 2020, A Novel Plasma-based Bioink Stimulates Cell Proliferation and Differentiation in Bioprinted, Mineralized Constructs. ACS Appl Mater Interfaces, 12:12557-72. DOI: 10.1021/acsami.0c00710.

Previous article in this issue

Next article in this issue

International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing