Tissue-engineered vessel derived from human fibroblasts with an electrospun scaffold.


Journal

Journal of tissue engineering and regenerative medicine
ISSN: 1932-7005
Titre abrégé: J Tissue Eng Regen Med
Pays: England
ID NLM: 101308490

Informations de publication

Date de publication:
11 2020
Historique:
received: 18 03 2020
revised: 20 07 2020
accepted: 24 08 2020
pubmed: 6 9 2020
medline: 15 10 2021
entrez: 5 9 2020
Statut: ppublish

Résumé

Advanced cardiovascular disease often requires surgical revascularization for small diameter arterial bypass procedures, and there is a need for alternative grafts in those patients lacking autologous vein. A decellularized biological vessel with the characteristics of a small artery and the ability to remodel in vivo could replace currently available bypass grafts. In this study, a biodegradable electrospun scaffold was specifically designed to be placed in a biomimetic perfusion system to generate a tissue-engineered vessel from human dermal fibroblasts. The polyglycolic acid electrospun scaffold was co-electrosprayed with a sacrificial porogen microparticle, polyethylene oxide, to increase porosity and pore size. After a 10-week culture period in the biomimetic system, the tissue-engineered vessel derived from human fibroblasts was further processed with decellularization to form an allogeneic tissue-engineered vessel. The tissue-engineered vessel had a similar morphology by histological staining for collagen and elastin before and after decellularization. The mechanical properties (burst pressure, ultimate tensile strength, and elastic modulus) remained stable after decellularization and were on the same magnitude as a human saphenous vein. The decellularization processing demonstrated no loss of collagen, near complete removal of DNA, and no presence of intracellular proteins. The decellularized tissue-engineered vessel supported the growth of endothelial cells on the surface, and fibroblasts were able to migrate into the midportion of the matrix. Therefore, an electrospun scaffold provides a versatile biomaterial to create a decellularized tissue-engineered vessel derived from human dermal fibroblasts with morphological and mechanical properties for use as a small diameter vascular graft.

Identifiants

pubmed: 32889733
doi: 10.1002/term.3130
doi:

Substances chimiques

Biocompatible Materials 0
Polyglycolic Acid 26009-03-0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1652-1660

Informations de copyright

© 2020 John Wiley & Sons, Ltd.

Références

Brown, B. N., Freund, J. M., Han, L., Rubin, J. P., Reing, J. E., Jeffries, E. M., … Badylak, S. F. (2011). Comparison of three methods for the derivation of a biologic scaffold composed of adipose tissue extracellular matrix. Tissue Engineering. Part C, Methods, 17, 411-421. https://doi.org/10.1089/ten.tec.2010.0342
Dahl, S. L., Koh, J., Prabhakar, V., & Niklason, L. E. (2003). Decellularized native and engineered arterial scaffolds for transplantation. Cell Transplantation, 12, 659-666. https://doi.org/10.3727/000000003108747136
Dahl, S. L., Kypson, A. P., Lawson, J. H., Blum, J. L., Strader, J. T., Li, Y., … Niklason, L. E. (2011). Readily available tissue-engineered vascular grafts. Science Translational Medicine, 3, 68ra9.
Ercolani, E., Del Gaudio, C., & Bianco, A. (2015). Vascular tissue engineering of small-diameter blood vessels: Reviewing the electrospinning approach. Journal of Tissue Engineering and Regenerative Medicine, 9, 861-888. https://doi.org/10.1002/term.1697
Farber, A., Major, K., Wagner, W. H., Cohen, J. L., Cossman, D. V., Lauterbach, S. R., & Levin, P. M. (2003). Cryopreserved saphenous vein allografts in infrainguinal revascularization: Analysis of 240 grafts. Journal of Vascular Surgery, 38, 15-21. https://doi.org/10.1016/S0741-5214(03)00330-6
Faulk, D. M., Carruthers, C. A., Warner, H. J., Kramer, C. R., Reing, J. E., Zhang, L., … Badylak, S. F. (2014). The effect of detergents on the basement membrane complex of a biologic scaffold material. Acta Biomaterialia, 10, 183-193. https://doi.org/10.1016/j.actbio.2013.09.006
Gilbert, T. W., Sellaro, T. L., & Badylak, S. F. (2006). Decellularization of tissues and organs. Biomaterials, 27, 3675-3683.
Heron, M. (2018). Deaths: Leading causes for 2016. National Vital Statistics Reports, 67, 1-77.
Hinderer, S., Shena, N., Ringuette, L. J., Hansmann, J., Reinhardt, D. P., Brucker, S. Y., … Schenke-Layland, K. (2015). In vitro elastogenesis: Instructing human vascular smooth muscle cells to generate an elastic fiber-containing extracellular matrix scaffold. Biomedical Materials, 10, 034102. https://doi.org/10.1088/1748-6041/10/3/034102
Hodge, J., & Quint, C. (2019). The improvement of cell infiltration in an electrospun scaffold with multiple synthetic biodegradable polymers using sacrificial PEO microparticles. Journal of Biomedical Materials Research. Part A, 107, 1954-1964. https://doi.org/10.1002/jbm.a.36706
Huang, A. H., Balestrini, J. L., Udelsman, B. V., Zhou, K. C., Zhao, L., Ferruzzi, J., … Niklason, L. E. (2016). Biaxial stretch improves elastic fiber maturation, collagen arrangement, and mechanical properties in engineered arteries. Tissue Engineering. Part C, Methods, 22, 524-533. https://doi.org/10.1089/ten.tec.2015.0309
Ingavle, G. C., & Leach, J. K. (2014). Advancements in electrospinning of polymeric nanofibrous scaffolds for tissue engineering. Tissue Engineering. Part B, Reviews, 20, 277-293. https://doi.org/10.1089/ten.teb.2013.0276
Isenberg, B. C., & Tranquillo, R. T. (2003). Long-term cyclic distention enhances the mechanical properties of collagen-based media-equivalents. Annals of Biomedical Engineering, 31, 937-949. https://doi.org/10.1114/1.1590662
Ju, Y. M., Ahn, H., Arenas-Herrera, J., Kim, C., Abolbashari, M., Atala, A., … Lee, S. J. (2017). Electrospun vascular scaffold for cellularized small diameter blood vessels: A preclinical large animal study. Acta Biomaterialia, 59, 58-67. https://doi.org/10.1016/j.actbio.2017.06.027
Kiviniemi, T. O., Pietila, A., Gunn, J. M., Aittokallio, J. M., Mahonen, M. S., Salomaa, V. V., & Niiranen, T. J. (2016). Trends in rates, patient selection and prognosis of coronary revascularisations in Finland between 1994 and 2013: The CVDR. EuroIntervention, 12, 1117-1125. https://doi.org/10.4244/EIJV12I9A183
Konig, G., Mcallister, T. N., Dusserre, N., Garrido, S. A., Iyican, C., Marini, A., … L'heureux, N. (2009). Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery. Biomaterials, 30, 1542-1550. https://doi.org/10.1016/j.biomaterials.2008.11.011
Lawson, J. H., Glickman, M. H., Ilzecki, M., Jakimowicz, T., Jaroszynski, A., Peden, E. K., … Niklason, L. E. (2016). Bioengineered human acellular vessels for dialysis access in patients with end-stage renal disease: Two phase 2 single-arm trials. Lancet, 387, 2026-2034. https://doi.org/10.1016/S0140-6736(16)00557-2
L'heureux, N., Paquet, S., Labbe, R., Germain, L., & Auger, F. A. (1998). A completely biological tissue-engineered human blood vessel. The FASEB Journal, 12, 47-56. https://doi.org/10.1096/fasebj.12.1.47
Martini, R. (2018). Trends of the treatment of critical limb ischemia during the last two decades. Clinical Hemorheology and Microcirculation, 69, 447-456. https://doi.org/10.3233/CH-170352
Mcallister, T. N., Maruszewski, M., Garrido, S. A., Wystrychowski, W., Dusserre, N., Marini, A., … L'heureux, N. (2009). Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: A multicentre cohort study. Lancet, 373, 1440-1446. https://doi.org/10.1016/S0140-6736(09)60248-8
Mrowczynski, W., Mugnai, D., De Valence, S., Tille, J. C., Khabiri, E., Cikirikcioglu, M., … Walpoth, B. H. (2014). Porcine carotid artery replacement with biodegradable electrospun poly-E-caprolactone vascular prosthesis. Journal of Vascular Surgery, 59, 210-219. https://doi.org/10.1016/j.jvs.2013.03.004
Niklason, L. E., Gao, J., Abbott, W. M., Hirschi, K. K., Houser, S., Marini, R., & Langer, R. (1999). Functional arteries grown in vitro. Science, 284, 489-493. https://doi.org/10.1126/science.284.5413.489
Quint, C., Arief, M., Muto, A., Dardik, A., & Niklason, L. E. (2012). Allogeneic human tissue-engineered blood vessel. Journal of Vascular Surgery, 55, 790-798. https://doi.org/10.1016/j.jvs.2011.07.098
Quint, C., Kondo, Y., Manson, R. J., Lawson, J. H., Dardik, A., & Niklason, L. E. (2011). Decellularized tissue-engineered blood vessel as an arterial conduit. Proceedings of the National Academy of Sciences of the United States of America, 108, 9214-9219. https://doi.org/10.1073/pnas.1019506108
Solan, A., Dahl, S. L., & Niklason, L. E. (2009). Effects of mechanical stretch on collagen and cross-linking in engineered blood vessels. Cell Transplantation, 18, 915-921. https://doi.org/10.3727/096368909X471161
Syedain, Z. H., Meier, L. A., Bjork, J. W., Lee, A., & Tranquillo, R. T. (2011). Implantable arterial grafts from human fibroblasts and fibrin using a multi-graft pulsed flow-stretch bioreactor with noninvasive strength monitoring. Biomaterials, 32, 714-722. https://doi.org/10.1016/j.biomaterials.2010.09.019
Syedain, Z. H., Meier, L. A., Lahti, M. T., Johnson, S. L., & Tranquillo, R. T. (2014). Implantation of completely biological engineered grafts following decellularization into the sheep femoral artery. Tissue Engineering. Part A, 20, 1726-1734. https://doi.org/10.1089/ten.tea.2013.0550
Veith, F. J., Gupta, S. K., Ascer, E., White-Flores, S., Samson, R. H., Scher, L. A., … Bergan, J. J. (1986). Six-year prospective multicenter randomized comparison of autologous saphenous vein and expanded polytetrafluoroethylene grafts in infrainguinal arterial reconstructions. Journal of Vascular Surgery, 3, 104-114. https://doi.org/10.1016/0741-5214(86)90073-X
Veith, F. J., Moss, C. M., Sprayregen, S., & Montefusco, C. (1979). Preoperative saphenous venography in arterial reconstructive surgery of the lower extremity. Surgery, 85, 253-256.
Wang, K., Xu, M., Zhu, M., Su, H., Wang, H., Kong, D., & Wang, L. (2013). Creation of macropores in electrospun silk fibroin scaffolds using sacrificial PEO-microparticles to enhance cellular infiltration. Journal of Biomedical Materials Research. Part A, 101, 3474-3481. https://doi.org/10.1002/jbm.a.34656
Weinberg, C. B., & Bell, E. (1986). A blood vessel model constructed from collagen and cultured vascular cells. Science, 231, 397-400. https://doi.org/10.1126/science.2934816
White, L. J., Taylor, A. J., Faulk, D. M., Keane, T. J., Saldin, L. T., Reing, J. E., … Badylak, S. F. (2017). The impact of detergents on the tissue decellularization process: A ToF-SIMS study. Acta Biomaterialia, 50, 207-219. https://doi.org/10.1016/j.actbio.2016.12.033

Auteurs

Clay Quint (C)

Department of Surgery, South Texas Veterans Health System, San Antonio, TX, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH