357
Views
3
CrossRef citations to date
0
Altmetric
Research Article

Evaluation of angiogenic potential of heparin and thyroxine releasing wound dressings

, , , , , & show all
Pages 1164-1175 | Received 23 Apr 2021, Accepted 22 Jul 2021, Published online: 17 Nov 2021

References

  • Stadelmann, W. K.; Digenis, A. G.; Tobin, G. R. Physiology and Healing Dynamics of Chronic Cutaneous Wounds. Am. J. Surg. 1998, 176, 26S–38S. DOI: 10.1016/S0002-9610(98)00183-4.
  • Tavakoli, S.; Klar, A. S. Bioengineered Skin Substitutes: Advances and Future Trends. App. Sci. 2021, 11, 1493. DOI: 10.3390/app11041493.
  • Cho, Y.-D.; Kim, K.-H.; Lee, Y.-M.; Ku, Y.; Seol, Y.-J. Periodontal Wound Healing and Tissue Regeneration: A Narrative Review. Pharmaceuticals 2021, 14, 456. DOI: 10.3390/ph14050456.
  • Metcalfe, A. D.; Ferguson, M. W. Tissue Engineering of Replacement Skin: The Crossroads of Biomaterials, Wound Healing, Embryonic Development, Stem Cells and Regeneration. J. R. Soc. Interface 2007, 4, 413–437. DOI: 10.1098/rsif.2006.0179.
  • Gefen, A. How Medical Engineering Has Changed Our Understanding of Chronic Wounds and Future Prospects. Med. Eng. Phys. 2019, 72, 13–18. DOI: 10.1016/j.medengphy.2019.08.010.
  • Zhang, G.-Y.; Langan, E. A.; Meier, N. T.; Funk, W.; Siemers, F.; Paus, R. Thyroxine (T4) May Promote Re-Epithelialisation and Angiogenesis in Wounded Human Skin Ex Vivo. PLOS One. 2019, 14, e0212659. DOI: 10.1371/journal.pone.0212659.
  • Rema, R. B.; Rajendran, K.; Ragunathan, M. Angiogenic Efficacy of Heparin on Chick Chorioallantoic Membrane. Vasc. Cell. 2012, 4, 8–7. DOI: 10.1186/2045-824X-4-8.
  • Aleem, A. R.; Shahzadi, L.; Alvi, F.; Khan, A. F.; Chaudhry, A. A.; Ur Rehman, I.; Yar, M. Thyroxin Releasing Chitosan/Collagen Based Smart Hydrogels to Stimulate Neovascularization. Materials & Design 2017, 133, 416–425. DOI: 10.1016/j.matdes.2017.07.053.
  • Safer, J. D.; Fraser, L. M.; Ray, S.; Holick, M. F. Topical Triiodothyronine Stimulates Epidermal Proliferation, Dermal Thickening, and Hair Growth in Mice and Rats. Thyroid 2001, 11, 717–724. DOI: 10.1089/10507250152484547.
  • Safer, J. D.; Crawford, T. M.; Fraser, L. M.; Hoa, M.; Ray, S.; Chen, T. C.; Persons, K.; Holick, M. F. Thyroid Hormone Action on Skin: diverging Effects of Topical versus Intraperitoneal Administration. Thyroid 2003, 13, 159–165. DOI: 10.1089/105072503321319468.
  • Holt, P. J. In Vitro Responses of the Epidermis to Triiodothyronine. J. Invest. Dermatol. 1978, 71, 202–204. DOI: 10.1111/1523-1747.ep12547158.
  • Schmohl, K. A.; Mueller, A. M.; Dohmann, M.; Spellerberg, R.; Urnauer, S.; Schwenk, N.; Ziegler, S. I.; Bartenstein, P.; Nelson, P. J.; Spitzweg, C.; et al. Integrin αvβ3-Mediated Effects of Thyroid Hormones on Mesenchymal Stem Cells in Tumor Angiogenesis. Thyroid 2019, 29, 1843–1857. DOI: 10.1089/thy.2019.0413.
  • Luidens, M. K.; Mousa, S. A.; Davis, F. B.; Lin, H.-Y.; Davis, P. J. Thyroid Hormone and Angiogenesis. Vascul. Pharmacol. 2010, 52, 142–145. DOI: 10.1016/j.vph.2009.10.007.
  • Mousa, S. A.; Bergh, J. J.; Dier, E.; Rebbaa, A.; O’Connor, L. J.; Yalcin, M.; Aljada, A.; Dyskin, E.; Davis, F. B.; Lin, H.-Y.; et al. Tetraiodothyroacetic Acid, a Small Molecule Integrin Ligand, Blocks Angiogenesis Induced by Vascular Endothelial Growth Factor and Basic Fibroblast Growth Factor. Angiogenesis 2008, 11, 183–190. DOI: 10.1007/s10456-007-9088-7.
  • Danilucci, T. M.; Santos, P. K.; Pachane, B. C.; Pisani, G. F. D.; Lino, R. L. B.; Casali, B. C.; Altei, W. F.; Selistre-de-Araujo, H. S. Recombinant RGD-Disintegrin DisBa-01 Blocks Integrin αvβ3 and Impairs VEGF Signaling in Endothelial Cells . Cell Commun. Signal. 2019, 17, 27–15. DOI: 10.1186/s12964-019-0339-1.
  • van Beek, N.; Bodó, E.; Kromminga, A.; Gáspár, E.; Meyer, K.; Zmijewski, M. A.; Slominski, A.; Wenzel, B. E.; Paus, R. Thyroid Hormones Directly Alter Human Hair Follicle Functions: Anagen Prolongation and Stimulation of Both Hair Matrix Keratinocyte Proliferation and Hair Pigmentation. J. Clin. Endocrinol. Metab. 2008, 93, 4381–4388. DOI: 10.1210/jc.2008-0283.
  • Erdoğan, M.; Ilhan, Y. S.; Akkuş, M. A.; Caboğlu, S. A.; Ozercan, I.; Ilhan, N.; Yaman, M. Effects of L-Thyroxine and Zinc Therapy on Wound Healing in Hypothyroid Rats. Acta Chir. Belg. 1999, 99, 72–77. DOI: 10.1080/00015458.1999.12098449.
  • Post, H.; Hundt, J. E.; Zhang, G.; Depping, R.; Rose, C.; Langan, E. A.; Paus, R. Thyroxine Restores Severely Impaired Cutaneous Re-epithelialisation and Angiogenesis in a Novel Preclinical Assay for Studying Human Skin Wound Healing Under “Pathological” Conditions Ex Vivo. Arch. Dermatol. Res. 2021, 313, 181–192. DOI: 10.1007/s00403-020-02092-z.
  • Safer, J. D.; Crawford, T. M.; Holick, M. F. Topical Thyroid Hormone Accelerates Wound Healing in Mice. Endocrinology 2005, 146, 4425–4430. DOI: 10.1210/en.2005-0192.
  • Malik, M. H.; Shahzadi, L.; Batool, R.; Safi, S. Z.; Khan, A. S.; Khan, A. F.; Chaudhry, A. A.; Rehman, I. U.; Yar, M. Thyroxine-Loaded Chitosan/Carboxymethyl Cellulose/Hydroxyapatite Hydrogels Enhance Angiogenesis in In-Ovo Experiments. Int. J. Biol. Macromol. 2020, 145, 1162–1170. DOI: 10.1016/j.ijbiomac.2019.10.043.
  • Shahzadi, L.; Bashir, M.; Tehseen, S.; Zehra, M.; Mehmood, A.; Chaudhry, A. A.; Rehman, I. U.; Yar, M. Thyroxine Impregnated Chitosan-Based Dressings Stimulate Angiogenesis and Support Fast Wounds Healing in Rats: Potential Clinical Candidates. Int. J. Biol. Macromol. 2020, 160, 296–306. DOI: 10.1016/j.ijbiomac.2020.05.127.
  • Li, G.; Xiao, Q.; Zhang, L.; Zhao, Y.; Yang, Y. Nerve Growth Factor Loaded Heparin/Chitosan Scaffolds for Accelerating Peripheral Nerve Regeneration. Carbohydr. Polym. 2017, 171, 39–49. DOI: 10.1016/j.carbpol.2017.05.006.
  • Pan, C.-J.; Pang, L.-Q.; Gao, F.; Wang, Y.-N.; Liu, T.; Ye, W.; Hou, Y.-H. Anticoagulation and Endothelial Cell Behaviors of Heparin-Loaded Graphene Oxide Coating on Titanium Surface. Mater. Sci. Eng. C Mater. Biol. Appl. 2016, 63, 333–340. DOI: 10.1016/j.msec.2016.03.001.
  • Joshi, A.; Xu, Z.; Ikegami, Y.; Yoshida, K.; Sakai, Y.; Joshi, A.; Kaur, T.; Nakao, Y.; Yamashita, Y-i.; Baba, H.; et al. Exploiting Synergistic Effect of Externally Loaded bFGF and Endogenous Growth Factors for Accelerated Wound Healing Using Heparin Functionalized PCL/Gelatin co-Spun Nanofibrous Patches. Chem. Eng. J. 2021, 404, 126518. DOI: 10.1016/j.cej.2020.126518.
  • Goh, M.; Hwang, Y.; Tae, G. Epidermal Growth Factor Loaded Heparin-Based Hydrogel Sheet for Skin Wound Healing. Carbohydr. Polym. 2016, 147, 251–260. DOI: 10.1016/j.carbpol.2016.03.072.
  • Peng, J.; Zhao, H.; Tu, C.; Xu, Z.; Ye, L.; Zhao, L.; Gu, Z.; Zhao, D.; Zhang, J.; Feng, Z.; et al. In Situ Hydrogel Dressing Loaded with Heparin and Basic Fibroblast Growth Factor for Accelerating Wound Healing in Rat. Mater. Sci. Eng.: C. 2020, 116, 111169. DOI: 10.1016/j.msec.2020.111169.
  • Yergoz, F.; Hastar, N.; Cimenci, C. E.; Ozkan, A. D.; Tekinay, T.; Guler, M. O.; Tekinay, A. B. Heparin Mimetic Peptide Nanofiber Gel Promotes Regeneration of Full Thickness Burn Injury. Biomaterials. 2017, 134, 117–127. DOI: 10.1016/j.biomaterials.2017.04.040.
  • Freudenberg, U.; Zieris, A.; Chwalek, K.; Tsurkan, M. V.; Maitz, M. F.; Atallah, P.; Levental, K. R.; Eming, S. A.; Werner, C. Heparin Desulfation Modulates VEGF Release and Angiogenesis in Diabetic Wounds. J. Control Release. 2015, 220, 79–88. DOI: 10.1016/j.jconrel.2015.10.028.
  • Ulery, B. D.; Nair, L. S.; Laurencin, C. T. Biomedical Applications of Biodegradable Polymers. J. Polym. Sci. B Polym. Phys. 2011, 49, 832–864. DOI: 10.1002/polb.22259.
  • Wang, L.; et al. Fabrication of Open‐Porous PCL/PLA Tissue Engineering Scaffolds and the Relationship of Foaming Process, Morphology, and Mechanical Behavior. Polym. Adv. Technol. 2019, 30(10), 2539–2548.
  • Woodruff, M. A.; Hutmacher, D. W. The Return of a Forgotten Polymer—Polycaprolactone in the 21st Century. Prog. Polym. Sci. 2010, 35, 1217–1256. DOI: 10.1016/j.progpolymsci.2010.04.002.
  • Fortelny, I.; Ujcic, A.; Fambri, L.; Slouf, M. Phase Structure, Compatibility, and Toughness of PLA/PCL Blends: A Review. Front. Mater. 2019, 6, 206. DOI: 10.3389/fmats.2019.00206.
  • Augustine, R.; Nethi, S. K.; Kalarikkal, N.; Thomas, S.; Patra, C. R. Electrospun Polycaprolactone (PCL) Scaffolds Embedded with Europium Hydroxide Nanorods (EHNs) with Enhanced Vascularization and Cell Proliferation for Tissue Engineering Applications. J. Mater. Chem. B. 2017, 5, 4660–4672. DOI: 10.1039/c7tb00518k.
  • Ghaee, A.; Bagheri-Khoulenjani, S.; Amir Afshar, H.; Bogheiri, H. Biomimetic Nanocomposite Scaffolds Based on Surface Modified PCL-Nanofibers Containing Curcumin Embedded in Chitosan/Gelatin for Skin Regeneration. Compos. Part B: Eng. 2019, 177, 107339. DOI: 10.1016/j.compositesb.2019.107339.
  • Liu, M.; Duan, X.-P.; Li, Y.-M.; Yang, D.-P.; Long, Y.-Z. Electrospun Nanofibers for Wound Healing . Mater. Sci. Eng. C Mater. Biol. Appl. 2017, 76, 1413–1423. DOI: 10.1016/j.msec.2017.03.034.
  • Nangare, S.; Jadhav, N.; Ghagare, P.; Muthane, T. Pharmaceutical Applications of Electrospinning. Ann. Pharm. Fr. 2020, 78, 1–11. in Elsevier. DOI: 10.1016/j.pharma.2019.07.002.
  • Gao, Y.; Bach Truong, Y.; Zhu, Y.; Louis Kyratzis, I. E-Spun Antibacterial Nanofibers: Production, Activity, and in Vivo Applications. J. Appl. Polym. Sci. 2014, 131, n/a–n/a. DOI: 10.1002/app.40797.
  • Keirouz, A.; Radacsi, N.; Ren, Q.; Dommann, A.; Beldi, G.; Maniura-Weber, K.; Rossi, R. M.; Fortunato, G. Nylon-6/Chitosan Core/Shell Antimicrobial Nanofibers for the Prevention of Mesh-Associated Surgical Site Infection. J. Nanobiotechnology. 2020, 18, 51–17. DOI: 10.1186/s12951-020-00602-9.
  • Jiang, K.; Long, Y.-Z.; Chen, Z.-J.; Liu, S.-L.; Huang, Y.-Y.; Jiang, X.; Huang, Z.-Q. Airflow-Directed in Situ Electrospinning of a Medical Glue of Cyanoacrylate for Rapid Hemostasis in Liver Resection. Nanoscale. 2014, 6, 7792–7798. DOI: 10.1039/c4nr01412j.
  • Zhang, J.; Zhao, Y.-T.; Hu, P.-Y.; Liu, J.-J.; Liu, X.-F.; Hu, M.; Cui, Z.; Wang, N.; Niu, Z.; Xiang, H.-F.; et al. Laparoscopic Electrospinning for In Situ Hemostasis in Minimally Invasive Operation. Chem. Eng. J. 2020, 395, 125089. DOI: 10.1016/j.cej.2020.125089.
  • Zahedi, P.; Rezaeian, I.; Ranaei-Siadat, S.-O.; Jafari, S.-H.; Supaphol, P. A Review on Wound Dressings with an Emphasis on e-Spun Nanofibrous Polymeric Bandages. Polym. Adv. Technol. 2010, 21, 77–95. DOI: 10.1002/pat.1625.
  • Fahimirad, S.; Ajalloueian, F. Naturally-Derived Electrospun Wound Dressings for Target Delivery of Bio-Active Agents. Int. J. Pharm. 2019, 566, 307–328. DOI: 10.1016/j.ijpharm.2019.05.053.
  • Meinel, A. J.; Germershaus, O.; Luhmann, T.; Merkle, H. P.; Meinel, L. Electrospun Matrices for Localized Drug Delivery: Current Technologies and Selected Biomedical Applications. Eur. J. Pharm. Biopharm. 2012, 81, 1–13. DOI: 10.1016/j.ejpb.2012.01.016.
  • Balaji, A.; Vellayappan, M. V.; John, A. A.; Subramanian, A. P.; Jaganathan, S. K.; Supriyanto, E.; Razak, S. I. A. An Insight on e-Spun-Nanofibers-Inspired Modern Drug Delivery System in the Treatment of Deadly Cancers. RSC Adv. 2015, 5, 57984–58004. DOI: 10.1039/C5RA07595E.
  • Hu, J.; Kai, D.; Ye, H.; Tian, L.; Ding, X.; Ramakrishna, S.; Loh, X. J. Electrospinning of Poly(Glycerol Sebacate)-Based Nanofibers for Nerve Tissue Engineering . Mater. Sci. Eng. C. Mater. Biol. Appl. 2017, 70, 1089–1094. DOI: 10.1016/j.msec.2016.03.035.
  • Khil, M. S.; Cha, D. I.; Kim, H. Y.; Kim, I. S.; Bhattarai, N. E-Spun Nanofibrous Polyurethane Membrane as Wound Dressing. J Biomed Mater Res Part B: Appl. Biomater. 2003, 67, 675–679. DOI: 10.1002/jbm.b.10058.
  • Álvarez-Suárez, A. S.; Dastager, S. G.; Bogdanchikova, N.; Grande, D.; Pestryakov, A.; García-Ramos, J. C.; Pérez-González, G. L.; Juárez-Moreno, K.; Toledano-Magaña, Y.; Smolentseva, E.; Paz-González, J. A. Electrospun fibers and sorbents as a possible basis for effective composite wound dressings. Micromachines. 2020, 11, 441. DOI: 10.3390/mi11040441.
  • Du, F.; Wang, H.; Zhao, W.; Li, D.; Kong, D.; Yang, J.; Zhang, Y. Gradient Nanofibrous Chitosan/Poly ɛ-Caprolactone Scaffolds as Extracellular Microenvironments for Vascular Tissue Engineering. Biomaterials. 2012, 33, 762–770. DOI: 10.1016/j.biomaterials.2011.10.037.
  • Mattanavee, W.; Suwantong, O.; Puthong, S.; Bunaprasert, T.; Hoven, V. P.; Supaphol, P. Immobilization of Biomolecules on the Surface of Electrospun Polycaprolactone Fibrous Scaffolds for Tissue Engineering . ACS Appl. Mater. Interfaces. 2009, 1, 1076–1085. DOI: 10.1021/am900048t.
  • Zehra, M.; Mehmood, A.; Yar, M.; Shahzadi, L.; Riazuddin, S. Development of NSAID-Loaded Nano-Composite Scaffolds for Skin Tissue Engineering Applications. J. Biomed. Mater. Res. B Appl. Biomater. 2020, 108, 3064–3075. DOI: 10.1002/jbm.b.34634.
  • Nájera-Romero, G. V.; Yar, M.; Rehman, I. U. Heparinized Chitosan/Hydroxyapatite Scaffolds Stimulate Angiogenesis. Funct Compos Mater. 2020, 1, 1–15. DOI: 10.1186/s42252-020-00012-y.
  • Falanga, V. Wound Healing and Its Impairment in the Diabetic Foot. Lancet. 2005, 366, 1736–1743. DOI: 10.1016/S0140-6736(05)67700-8.
  • Gurtner, G. C.; Werner, S.; Barrandon, Y.; Longaker, M. T. Wound Repair and Regeneration. Nature. 2008, 453, 314–321. DOI: 10.1038/nature07039.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.