Keratin-Butyrate Scaffolds Promote Skin Wound Healing in Diabetic Rats Through Down-Regulation of IL-1β and Up-Regulation of Keratins 16 and 17

References

• Adamskaya, N., P. Dungel, R. Mittermayr, J. Hartinger, G. Feichtinger, K. Wassermann, H. Redl, and M. van Griensven. 2011. Light therapy by blue LED improves wound healing in an excision model in rats. Injury 42 (9):917–16. doi:10.1016/j.injury.2010.03.023.
   PubMed Web of Science ®Google Scholar
• Amoras, E. D. S. G., S. T. Monteiro Gomes, M. A. Freitas Queiroz, M. S. M. de Araújo, M. T. F. de Araújo, S. R. S. da Silva Conde, R. Ishak, and A. C. R. Vallinoto. 2020. Intrahepatic interleukin 10 expression modulates fibrinogenesis during chronic HCV infection. PLoS ONE 15 (10):e0241199. doi:10.1371/journal.pone.0241199.
   PubMed Web of Science ®Google Scholar
• Ashcroft, G. S., Jeong, M. J., Ashworth, J. J., Hardman, M., Jin, W., Moutsopoulos, N., Wild, T., McCartney-Francis, N., Sim, D., McGrady, G., Song, X. Y., & Wahl, S. M. 2013. TNFα is a therapeutic target for impaired cutaneous wound healing. Wound Repair and Regeneration : Official Publication of the Wound Healing Society [And] the European Tissue Repair Society 20 (1):38–49. doi:10.1111/j.1524-475X.2011.00748.x.
   Web of Science ®Google Scholar
• Baffi, T. R., G. Lordén, J. M. Wozniak, A. Feichtner, W. Yeung, A. P. Kornev, C. C. King, J. C. Del Rio, A. J. Limaye, J. Bogomolovas, et al. 2021. mTORC2 controls the activity of PKC and Akt by phosphorylating a conserved TOR interaction motif. Science Signaling 14 (678):eabe4509. doi:10.1126/scisignal.abe4509.
   PubMed Web of Science ®Google Scholar
• Bochynska-Czyz, M., P. Redkiewicz, H. Kozlowska, J. Matalinska, M. Konop, and P. Kosson. 2020. Can keratin scaffolds be used for creating three-dimensional cell cultures? Open Medicine 15 (1):249–53. doi:10.1515/med-2020-0031.
   Web of Science ®Google Scholar
• Brown, L. F., K. T. Yeo, B. Berse, T. K. Yeo, D. R. Senger, H. F. Dvorak, and L. van de Water. 1992. Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing. The Journal of Experimental Medicine 176 (5):1375–79. doi:10.1084/jem.176.5.1375.
   PubMed Web of Science ®Google Scholar
• Castro, P. R., L. F. F. Bittencourt, S. Larochelle, S. P. Andrade, C. R. Mackay, M. Slevin, V. J. Moulin, and L. S. Barcelos. 2021. GPR43 regulates sodium butyrate-induced angiogenesis and matrix remodeling. American Journal of Physiology - Heart and Circulatory Physiology 320 (3):H1066–79. doi:10.1152/ajpheart.00515.2019.
   PubMed Web of Science ®Google Scholar
• Chang, P. V., L. Hao, S. Offermanns, and R. Medzhitov. 2014. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proceedings of the National Academy of Sciences of the United States of America 111 (6):2247–52. doi:10.1073/pnas.1322269111.
   PubMed Web of Science ®Google Scholar
• Chen, G., X. Ran, B. Li, Y. Li, D. He, B. Huang, S. Fu, J. Liu, and W. Wang. 2018. Sodium butyrate inhibits inflammation and maintains epithelium barrier integrity in a TNBS-induced inflammatory bowel disease mice model. eBioMedicine 30:317–25. doi:10.1016/j.ebiom.2018.03.030.
   PubMed Web of Science ®Google Scholar
• Dyson, J. E. D., J. Daniel, and C. R. Surrey. 1992. The effect of sodium butyrate on the growth characteristics of human cervix tumour cells. British Journal of Cancer 65 (6):803–08. doi:10.1038/bjc.1992.172.
   PubMed Web of Science ®Google Scholar
• Elnozahi, N. A., E. A. Said, A. E. Bistawroos, and R. G. Aly. 2020. Effect of sodium butyrate on gastric ulcer aggravation and hepatic injury inflicted by bile duct ligation in rats. Saudi Pharmaceutical Journal 28 (6):675–82. doi:10.1016/j.jsps.2020.04.008.
   PubMed Web of Science ®Google Scholar
• Feng, W., Y. Wu, G. Chen, S. Fu, B. Li, B. Huang, D. Wang, W. Wang, and J. Liu. 2018. Sodium butyrate attenuates diarrhea in weaned piglets and promotes tight junction protein expression in colon in a GPR109A-dependent manner. Cellular Physiology and Biochemistry 47 (4):1617–29. doi:10.1159/000490981.
   PubMedGoogle Scholar
• Feroz, S., N. Muhammad, J. Ranayake, and G. Dias. 2020. Keratin - based materials for biomedical applications. Bioactive Materials 5 (3):496–509. doi:10.1016/j.bioactmat.2020.04.007.
   PubMed Web of Science ®Google Scholar
• Frank, S., G. Hübner, G. Breier, M. T. Longaker, D. G. Greenhalgh, and S. Werner. 1995. Regulation of vascular endothelial growth factor expression in cultured keratinocytes. Implications for normal and impaired wound healing. The Journal of Biological Chemistry 270 (21):12607–13. doi:10.1074/jbc.270.21.12607.
   PubMed Web of Science ®Google Scholar
• Gangnuss, S., A. J. Cowin, I. S. Daehn, N. Hatzirodos, J. A. Rothnagel, A. Varelias, and T. E. Rayner. 2004. Regulation of MAPK activation, AP-1 transcription factor expression and keratinocyte differentiation in wounded fetal skin. The Journal of Investigative Dermatology 122 (3):791–804. doi:10.1111/j.0022-202X.2004.22319.x.
   PubMed Web of Science ®Google Scholar
• Guilloteau, P., G. Savary, Y. Jaguelin-Peyrault, V. Romé, L. Le Normand, and R. Zabielski. 2010. Dietary sodium butyrate supplementation increases digestibility and pancreatic secretion in young milk-fed calves. Journal of Dairy Science 93 (12):5842–50. doi:10.3168/jds.2009-2751.
   PubMed Web of Science ®Google Scholar
• Haake, A. R., and M. Cooklis. 1997. Incomplete differentiation of fetal keratinocytes in the skin equivalent leads to the default pathway of apoptosis. Experimental Cell Research 231 (1):83–85. doi:10.1006/excr.1996.3441.
   PubMed Web of Science ®Google Scholar
• Hobbs, R. P., J. C. Lessard, and P. A. Coulombe. 2012. Keratin intermediate filament proteins - novel regulators of inflammation and immunity in skin. Journal of Cell Science 125 (22):5257–58. doi:10.1242/jcs.122929.
   PubMed Web of Science ®Google Scholar
• Huang, H., W. Cui, W. Qiu, M. Zhu, R. Zhao, D. Zeng, C. Dong, X. Wang, W. Guo, W. Xing, et al. 2015. Impaired wound healing results from the dysfunction of the Akt/MTOR pathway in diabetic rats. Journal of Dermatological Science 79 (3):241–51. doi:10.1016/j.jdermsci.2015.06.002.
   PubMed Web of Science ®Google Scholar
• Hui, Y., and K. M. Ajuwon. 2017. Butyrate modifies intestinal barrier function in IPEC-J2 cells through a selective upregulation of tight junction proteins and activation of the Akt signaling pathway. PLoS ONE 12 (6):20179586. doi:10.1371/journal.pone.0179586.
   Web of Science ®Google Scholar
• Keshava, R., and R. Gope. 2015. Sodium butyrate plus EGF and PDGF-BB aids cutaneous wound healing in diabetic mice. Advances in Biology 2015:1–10. ID 527231. doi:10.1155/2015/527231.
   Google Scholar
• Kim, H. J., and D. M. Chuang. 2014. HDAC inhibitors mitigate ischemia-induced oligodendrocyte damage: Potential roles of oligodendrogenesis, VEGF, and anti-inflammation. American Journal of Translational Research 6 (3):206–23.
   PubMed Web of Science ®Google Scholar
• Konop, M., J. Czuwara, E. Kłodzińska, A. K. Laskowska, D. Sulejczak, T. Damps, U. Zielenkiewicz, I. Brzozowska, A. Sureda, T. Kowalkowski, et al. 2020. Evaluation of keratin biomaterial containing silver nanoparticles as a potential wound dressing in full-thickness skin wound model in diabetic mice. Journal of Tissue Engineering and Regenerative Medicine 14 (2):334–46. doi:10.1002/term.2998.
   PubMed Web of Science ®Google Scholar
• Konop, M., J. Czuwara, E. Kłodzińska, A. K. Laskowska, U. Zielenkiewicz, I. Brzozowska, S. M. Nabavi, and L. Rudnicka. 2018. Development of a novel keratin dressing which accelerates full-thickness skin wound healing in diabetic mice: In vitro and in vivo studies. Journal of Biomaterials Applications 33 (4):527–40. doi:10.1177/0885328218801114.
   PubMed Web of Science ®Google Scholar
• Konop, M., A. K. Laskowska, M. Rybka, E. Kłodzińska, D. Sulejczak, R. A. Schwartz, and J. Czuwara. 2021. Keratin scaffolds containing casomorphin stimulate macrophage infiltration and accelerate full-thickness cutaneous wound healing in diabetic mice. Molecules 26 (9):2554. doi:10.3390/molecules26092554.
   PubMed Web of Science ®Google Scholar
• Konop, M., M. Rybka, and A. Drapała. 2021. Keratin biomaterials in skin wound healing, an old player in modern medicine: A mini review. Pharmaceutics 13 (12):2029. doi:10.3390/pharmaceutics13122029.
   PubMed Web of Science ®Google Scholar
• Konop, M., D. Sulejczak, J. Czuwara, P. Kosson, A. Misicka, A. W. Lipkowski, and L. Rudnicka. 2017. The role of allogenic keratin-derived dressing in wound healing in a mouse model. Wound Repair and Regeneration 25 (1):62–74. doi:10.1111/wrr.12500.
   PubMed Web of Science ®Google Scholar
• Lahiri, D., M. Nag, B. Dutta, A. Dey, T. Sarkar, S. Pati, H. A. Edinur, Z. Abdul Kari, N. H. Mohd Noor, and R. R. Ray. 2021. Bacterial cellulose: Production, characterization, and application as antimicrobial agent. International Journal of Molecular Sciences 22 (23):12984. doi:10.3390/ijms222312984.
   PubMed Web of Science ®Google Scholar
• Lee, C., B. G. Kim, J. H. Kim, J. Chun, J. P. Im, and J. S. Kim. 2017. Sodium butyrate inhibits the NF-Kappa B signaling pathway and histone deacetylation, and attenuates experimental colitis in an IL-10 independent manner. International Immunopharmacology 51:47–56. doi:10.1016/j.intimp.2017.07.023.
   PubMed Web of Science ®Google Scholar
• Leonardo, T. R., J. Shi, D. Chen, H. M. Trivedi, and L. Chen. 2020. Differential expression and function of bicellular tight junctions in skin and oral wound healing. International Journal of Molecular Sciences 21 (8):2966. doi:10.3390/ijms21082966.
   PubMed Web of Science ®Google Scholar
• Liu, H., J. Wang, T. He, S. Becker, G. Zhang, D. Li, and X. Ma. 2018. Butyrate: A double-edged sword for health? Advances in Nutrition 9 (1):21–29. doi:10.1093/advances/nmx009.
   PubMed Web of Science ®Google Scholar
• Ma, X., P. X. Fan, L. S. Li, S. Y. Qiao, G. L. Zhang, and D. F. Li. 2012. Butyrate promotes the recovering of intestinal wound healing through its positive effect on the tight junctions. Journal of Animal Science 90 (Suppl 4):266–68. doi:10.2527/jas.50965.
   PubMed Web of Science ®Google Scholar
• Mazzalupo, S., P. Wong, P. Martin, and P. A. Coulombe. 2003. Role for keratins 6 and 17 during wound closure in embryonic mouse skin. Developmental Dynamics 226 (2):356–65. doi:10.1002/dvdy.10245.
   PubMed Web of Science ®Google Scholar
• Mazzarino, L., G. Loch-Neckel, L. dos Santos Bubniak, F. Ourique, I. Otsuka, S. Halila, R. Curi Pedrosa, M. C. Santos-Silva, E. Lemos-Senna, E. Curti Muniz, et al. 2015. Nanoparticles made from xyloglucan-block-polycaprolactone copolymers: Safety assessment for drug delivery. Toxicological Sciences 147 (1):104–15. doi:10.1093/toxsci/kfv114.
   PubMed Web of Science ®Google Scholar
• Moay, Z. K., L. T. H. Nguyen, P. Hartrianti, D. P. Lunny, D. Leavesley, Y. O. Kok, S. J. Chong, A. W. C. Chua, S. I. Tee, and K. W. Ng. 2021. Keratin-alginate sponges support healing of partial-thickness burns. International Journal of Molecular Sciences 22 (16):8594. doi:10.3390/ijms22168594.
   PubMed Web of Science ®Google Scholar
• Morhardt, T. L., A. Hayashi, T. Ochi, M. Quirós, S. Kitamoto, H. Nagao-Kitamoto, P. Kuffa, K. Atarashi, K. Honda, J. Y. Kao, et al. 2019. IL-10 produced by macrophages regulates epithelial integrity in the small intestine. Scientific Reports 9 (1):1223. doi:10.1038/s41598-018-38125-x.
   PubMedGoogle Scholar
• Mowat, A. M., and W. W. Agace. 2014. Regional specialization within the intestinal immune system. Nature Reviews Immunology 14 (10):667–85. doi:10.1038/nri3738.
   PubMed Web of Science ®Google Scholar
• Ndishimye, P., F. Seghrouchni, B. Domokos, O. Soritau, A. Sadak, D. Homorodean, R. E. Aouada, and C. M. Pop. 2015. Evaluation of interleukin-10 levels in the plasma of patients with various stages of tuberculosis. Medicine and Pharmacy Reports 88 (2):164–67. doi:10.15386/cjmed-459.
   Google Scholar
• Ohira, H., Y. Fujioka, C. Katagiri, M. Yano, R. Mamoto, M. Aoyama, M. Usami, and M. Ikeda. 2012. Butyrate enhancement of inteleukin-1β production via activation of oxidative stress pathways in lipopolysaccharide-stimulated THP-1 cells. Journal of Clinical Biochemistry and Nutrition 50 (1):59–66. doi:10.3164/jcbn.11-22.
   PubMed Web of Science ®Google Scholar
• Onyszkiewicz, M., M. Gawrys-Kopczynska, P. Konopelski, M. Aleksandrowicz, A. Sawicka, E. Koźniewska, E. Samborowska, and M. Ufnal. 2019. Butyric acid, a gut bacteria metabolite, lowers arterial blood pressure via colon-vagus nerve signaling and GPR41/43 receptors. Pflügers Archiv - European Journal of Physiology 471 (11–12):1441–53. doi:10.1007/s00424-019-02322-y.
   PubMed Web of Science ®Google Scholar
• Park, J.-S., E.-J. Lee, J.-C. Lee, W.-K. Kim, and H.-S. Kim. 2007. Anti-inflammatory effects of short chain fatty acids in IFN-γ-stimulated RAW 264.7 murine macrophage cells: Involvement of NF-ΚB and ERK signaling pathways. International Immunopharmacology 7 (1):70–77. doi:10.1016/j.intimp.2006.08.015.
   PubMed Web of Science ®Google Scholar
• Park, M., H. K. Shin, B. S. Kim, M. J. Kim, I. S. Kim, B. Y. Park, and H. Y. Kim. 2015. Effect of discarded keratin-based biocomposite hydrogels on the wound healing process in vivo. Materials Science & Engineering: C, Materials for Biological Applications 55:88–94. doi:10.1016/j.msec.2015.03.033.
   PubMed Web of Science ®Google Scholar
• Pauline, W., and P. A. Coulombe. 2003. Loss of Keratin 6 (K6) proteins reveals a function for intermediate filaments during wound repair. The Journal of Cell Biology 163 (2):327–37. doi:10.1083/jcb.200305032.
   PubMed Web of Science ®Google Scholar
• Pechter, P. M., J. Gil, J. Valdes, M. Tomic-Canic, I. Pastar, O. Stojadinovic, R. S. Kirsner, and S. C. Davis. 2012. Keratin dressings speed epithelialization of deep partial-thickness wounds. Wound Repair and Regeneration 20 (2):236–42. doi:10.1111/j.1524-475X.2012.00768.x.
   PubMed Web of Science ®Google Scholar
• Peddibhotla, S. S. D., B. F. Brinkmann, D. Kummer, H. Tuncay, M. Nakayama, R. H. Adams, V. Gerke, and K. Ebnet. 2013. Tetraspanin CD9 links junctional adhesion molecule-A to αvβ3 integrin to mediate basic fibroblast growth factor–specific angiogenic signaling. Molecular Biology of the Cell 24 (7):933–44. doi:10.1091/mbc.e12-06-0481.
   PubMed Web of Science ®Google Scholar
• Plöger, S., F. Stumpff, G. B. Penner, J.-D. Schulzke, G. Gäbel, H. Martens, Z. Shen, D. Günzel, and J. R. Aschenbach. 2012. Microbial butyrate and its role for barrier function in the gastrointestinal tract. Annals of the New York Academy of Sciences 1258 (1):52–59. doi:10.1111/j.1749-6632.2012.06553.x.
   PubMedGoogle Scholar
• Qiu, Y., X. Ma, X. Yang, L. Wang, and Z. Jiang. 2017. Effect of sodium butyrate on cell proliferation and cell cycle in porcine intestinal epithelial (IPEC-J2) cells. Vitro Cellular and Developmental Biology - Animal 53 (4):304–11. doi:10.1007/s11626-016-0119-9.
   PubMed Web of Science ®Google Scholar
• Ritsu, M., Kawakami K, Kanno E, Tanno H, Ishii K, Imai Y, Maruyama R, Tachi M. 2017. Critical role of tumor necrosis factor-α in the early process of wound healing in skin. Journal of Dermatology & Dermatologic Surgery 21 (1)14–19.
   Google Scholar
• Rodero, M. P., and K. Khosrotehrani. 2010. Skin wound healing modulation by macrophages. International Journal of Clinical and Experimental Pathology 3 (7):643–53.
   PubMed Web of Science ®Google Scholar
• Ruvinsky, I., and O. Meyuhas. 2006. Ribosomal protein S6 phosphorylation: From protein synthesis to cell size. Trends in Biochemical Sciences 31 (6):342–48. doi:10.1016/j.tibs.2006.04.003.
   PubMed Web of Science ®Google Scholar
• Salmond, R. J., J. Emery, K. Okkenhaug, and R. Zamoyska. 2009. MAPK, phosphatidylinositol 3-Kinase, and mammalian target of rapamycin pathways converge at the level of ribosomal protein S6 phosphorylation to control metabolic signaling in CD8 T cells. The Journal of Immunology 183 (11):7388–97. doi:10.4049/jimmunol.0902294.
   PubMed Web of Science ®Google Scholar
• Sapan, H. B., I. Paturusi, A. A. Islam, I. Yusuf, I. Patellongi, M. N. Massi, A. D. Pusponegoro, S. K. Arief, I. Labeda, L. Rendy, et al. 2017. Interleukin-6 and interleukin-10 plasma levels and MRNA expression in polytrauma patients. Chinese Journal of Traumatology 20 (6):318–22. doi:10.1016/j.cjtee.2017.05.003.
   PubMed Web of Science ®Google Scholar
• Seyun, K., P. Wong, and P. A. Coulombe. 2006. A keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth. Nature 441 (7091):362–65. doi:10.1038/nature04659.
   PubMed Web of Science ®Google Scholar
• Shi, J., M. Barakat, D. Chen, and L. Chen. 2018. Bicellular tight junctions and wound healing. International Journal of Molecular Sciences 19 (12):3862. doi:10.3390/ijms19123862.
   PubMed Web of Science ®Google Scholar
• Spampinato, S. F., G. I. Caruso, R. De Pasquale, M. A. Sortino, and S. Merlo. 2020. The treatment of impaired wound healing in diabetes: Looking among old drugs. Pharmaceuticals 13 (4):60. doi:10.3390/ph13040060.
   Web of Science ®Google Scholar
• Tachibana, A., Y. Furuta, H. Takeshima, T. Tanabe, and K. Yamauchi. 2002. Fabrication of wool keratin sponge scaffolds for long-term cell cultivation. Journal of Biotechnology 93 (2):165–70. doi:10.1016/S0168-1656(01)00395-9.
   PubMed Web of Science ®Google Scholar
• Verma, V., P. Verma, P. Ray, and A. R. Ray. 2008. Preparation of scaffolds from human hair proteins for tissue-engineering applications. Biomedical Matererials 3 (2):025007. doi:10.1088/1748-6041/3/2/025007.
   PubMed Web of Science ®Google Scholar
• Volksdorf, T., Heilmann J, Eming SA, Schawjinski K, Zorn-Kruppa M, Ueck C, Vidal-y-Sy S, Windhorst S, Jücker M, Moll I, et al. 2017. Tight junction proteins claudin-1 and occludin are important for cutaneous wound healing. The American Journal of Pathology 187 (6):1301–12. doi:10.1016/j.ajpath.2017.02.006.
   PubMed Web of Science ®Google Scholar
• Wang, P.-Y., and P.-Y. Wang. 2012. Tu1343 butyrate enhances intestinal epithelial barrier function via up-regulation of tight junction protein claudin-1 transcription. Gastroenterology 142 (5): S-807. doi:10.1016/S0016-5085(12)63137-0.
   Google Scholar
• Wan, R., J. P. Weissman, K. Grundman, L. Lang, D. J. Grybowski, and R. D. Galiano. 2021. Diabetic wound healing: The impact of diabetes on myofibroblast activity and its potential therapeutic treatments. Wound Repair and Regeneration 29 (4):573–81. doi:10.1111/wrr.12954.
   PubMed Web of Science ®Google Scholar
• Yang, X., Z. Jing, W. Wei, Z. Chun, Q. Quan, Z. Qing, X. Jiamin, and H. Shuwen. 2021. Inhibitory effect of sodium butyrate on colorectal cancer cells and construction of the related molecular network. BMC Cancer 21 (1):1. doi:10.1186/s12885-021-07845-1.
   PubMed Web of Science ®Google Scholar
• Yang, G., D. S. Murashige, S. J. Humphrey, and D. E. James. 2015. A positive feedback loop between Akt and mTORC2 via SIN1 phosphorylation. Cell Reports 12 (6):937–43. doi:10.1016/j.celrep.2015.07.016.
   PubMed Web of Science ®Google Scholar
• Yano, T., M. Ferlito, A. Aponte, A. Kuno, T. Miura, E. Murphy, and C. Steenbergen. 2014. Pivotal role of MTORC2 and involvement of ribosomal protein S6 in cardioprotective signaling. Circulation Research 114 (8):1268–80. doi:10.1161/CIRCRESAHA.114.303562.
   PubMed Web of Science ®Google Scholar
• Zhang, X., M. Yin, and L. Juan Zhang. 2019. Keratin 6, 16 and 17-critical barrier alarmin molecules in skin wounds and psoriasis. Cells 8 (8):807. doi:10.3390/cells8080807.
   PubMed Web of Science ®Google Scholar
• Zheng, L., C. J. Kelly, K. D. Battista, R. Schaefer, J. M. Lanis, E. E. Alexeev, R. X. Wang, J. C. Onyiah, D. J. Kominsky, and S. P. Colgan. 2017. Microbial-derived butyrate promotes epithelial barrier function through IL-10 receptor–dependent repression of Claudin-2. The Journal of Immunology 199 (8):2976–84. doi:10.4049/jimmunol.1700105.
   PubMed Web of Science ®Google Scholar
• Zhong, Y., F. Seidi, C. Li, Z. Wan, Y. Jin, J. Song, and H. Xiao. 2021. Antimicrobial/Biocompatible hydrogels dual-reinforced by cellulose as ultrastretchable and rapid self-healing wound dressing. Biomacromolecules 22 (4):1654–63. doi:10.1021/acs.biomac.1c00086.
   PubMed Web of Science ®Google Scholar