J Appl Biomed 20:87-97, 2022
Effects of 17-β-estradiol released from shape-memory terpolymer rods on sciatic nerve regeneration after injury and repair with chitosan nerve conduit in female rats
Edyta Olakowska1, Adam Waszczuk1, *, Artur Turek2, Aleksandra Borecka3, Arkadiusz Likiewicz1, Dariusz Wawro4, Janusz Kasperczyk2, 3, Halina Jdrzejowska-Szypuka1
1Medical University of Silesia, Faculty of Medical Sciences in Katowice, Department of Physiology, Katowice, Poland
2Medical University of Silesia, Faculty of Pharmaceutical Sciences in Sosnowiec, Department of Biopharmacy, Sosnowiec, Poland
3Polish Academy of Sciences, Centre of Polymer and Carbon Materials, Zabrze, Poland
4Institute of Biopolymers and Chemical Fibres, d, Poland
The aim of this study was to assess 17-β-estradiol (E2) influence on sciatic nerve regeneration after injury followed by a repair with chitosan conduit in ovariectomized female rats. The study was performed in 2 groups (n = 16) of rats: OVChit - after excision of a fragment of the sciatic nerve, a chitosan conduit was implanted; OVChitE10 group - additionally to chitosan conduit, shape-memory terpolymer rods based on poly(L-lactide-co-glycolide- co-trimethylene carbonate) releasing 17-β-estradiol for 20 weeks were implanted. The mean number of regenerating axons and mean fiber area were significantly greater in 17-β-estradiol-treated animals. In this group, the infiltrate of leukocytes was diminished. The presence of 17-β-estradiol receptors alpha and beta in motoneurons in the spinal cord were discovered. This may indicate the location where 17-β-estradiol affects the regeneration of the injured nerve. Estradiol released from the terpolymer rods for 20 weeks could enhance, to some extent, sciatic nerve regeneration after injury, and diminish the inflammatory reaction. In the future, 17-β-estradiol entrapped in terpolymer rods could be used in the repair of injured peripheral nerves, but there is a need for further studies.
Keywords: 17-β-estradiol (E2); Chitosan conduit; Inflammation; Sciatic nerve injury; Shape-memory terpolymer
Grants and funding:
This study was supported by grant PCN-1-090/K/0/O (Medical University of Silesia, Katowice, Poland).
Conflicts of interest:
The authors have no conflict of interests to declare.
Olakowska E, Waszczuk A,
Download citation
Open full article
References
Alluin O, Wittmann C, Marqueste T, Chabas J-F, Garcia S, Lavaut M-N, et al. (2009). Functional recovery after peripheral nerve injury and implantation of a collagen guide. Biomaterials 30(3): 363-373. DOI: 10.1016/j.biomaterials.2008.09.043.
Go to original source... Go to PubMed...
Arevalo M-A, Azcoitia I, Garcia-Segura LM (2014). The neuroprotective actions of oestradiol and oestrogen receptors. Nat Rev Neurosci 16(1): 17-29. DOI: 10.1038/nrn3856.
Go to original source... Go to PubMed...
Azcoitia I, Barreto GE, Garcia-Segura LM (2019). Molecular mechanisms and cellular events involved in the neuroprotective actions of estradiol. Analysis of sex differences. Front Neuroendocrinol 55, 100787. DOI: 10.1016/j.yfrne.2019.100787.
Go to original source... Go to PubMed...
Bk M, Gutkowska ON, Wagner E, Gosk J (2017). The role of chitin and chitosan in peripheral nerve reconstruction. Polim Med 47(1): 43-47. DOI: 10.17219/pim/75653.
Go to original source... Go to PubMed...
Caceres LG, Uran SL, Zorilla Zubilete MA, Romero JI, Capani F, Guelman LR (2011). An early treatment with 17-beta estradiol is neuroprotective against the long-term effects of neonatal ionizing radiation exposure. J Neurochem 118(4): 626-635. DOI: 10.1111/j.1471-4159.2011.07334.x.
Go to original source... Go to PubMed...
Chen Y, Guo W, Xu L, Li W, Cheng M, Hu Y, Xu W (2016). 17β-Estradiol Promotes Schwann Cell Proliferation and Differentiation, Accelerating Early Remyelination in a Mouse Peripheral Nerve Injury Model. Biomed Res Int 2016: 7891202. DOI: 10.1155/2016/7891202.
Go to original source... Go to PubMed...
Cox A, Varma A, Barry J, Vertegel A, Banik N (2015). Nanoparticle Estrogen in Rat Spinal Cord Injury Elicits Rapid Anti-Inflammatory Effects in Plasma, Cerebrospinal Fluid, and Tissue. J Neurotrauma 32(18): 1413-1421. DOI: 10.1089/neu.2014.3730.
Go to original source... Go to PubMed...
Dobrzyski P, Kasperczyk J, Smola A, Pastusiak M, Sobota M, Jaworska J (2013). Bioresorbable and biocompatible thermoplastic elastomer having a shape memory, particularly for biomedical applications and a process for their preparation. EP 2647656 A2.
Engler-Chiurazzi EB, Brown CM, Povroznik JM, Simpkins JW (2017). Estrogens as neuroprotectants: Estrogenic actions in the context of cognitive aging and brain injury. Prog Neurobiol 157: 188-211. DOI: 10.1016/j.pneurobio.2015.12.008.
Go to original source... Go to PubMed...
Engler-Chiurazzi EB, Singh M, Simpkins JW (2016). From the 90's to now: A brief historical perspective on more than two decades of estrogen neuroprotection. Brain Res 1633: 96-100. DOI: 10.1016/j.brainres.2015.12.044.
Go to original source... Go to PubMed...
Gbarowska K, Kasperczyk J, Dobrzynski P, Scandola M, Zini E, Li S (2011). NMR analysis of the chain microstructure of biodegradable terpolymers with shape memory properties. Eur Polym J 47(6): 1315-1327. DOI: 10.1016/j.eurpolymj.2011.02.022.
Go to original source...
Herzog R, Zendedel A, Lammerding L, Beyer C, Slowik A (2017). Impact of 17beta-estradiol and progesterone on inflammatory and apoptotic microRNA expression after ischemia in rat model. J Steroid Biochem Mol Biol 167: 126-134. DOI: 10.1016/j.jsbmb.2016.11.018.
Go to original source... Go to PubMed...
Hsu S-H, Kuo W-C, Chen Y-T, Yen C-T, Chen Y-F, Chen K-S, et al. (2013). New nerve regeneration strategy combining laminin-coated chitosan conduits and stem cell therapy. Acta Biomater 9(5): 6606-6615. DOI: 10.1016/j.actbio.2013.01.025.
Go to original source... Go to PubMed...
Huppenbauer CB, Tanzer L, DonCarlos LL, Jones KJ (2005). Gonadal steroids attenuation of developing hamster facial motoneuron loss by axotomy: equal efficacy of testosterone, dihydrotestosterone and 17-beta estradiol. J Neurosci 25(16): 4004-4013. DOI: 10.1523/JNEUROSCI.5279-04.2005.
Go to original source... Go to PubMed...
Islamov RR, Hendricks WA, Jones RJ, Lyall GJ, Spanier NS, Murashov AK (2002). 17beta-estradiol stimulates regeneration of sciatic nerve in female mice. Brain Res 943(2): 283-286. DOI: 10.1016/s0006-8993(02)02827-5.
Go to original source... Go to PubMed...
Kalbermatten DF, Pettersson J, Kingham PJ, Pierer G, Wiberg M, Terenghi G (2009). New fibrin conduit for peripheral nerve repair. J Reconstr Microsurg 25(1): 27-33. DOI: 10.1055/s-0028-1090619.
Go to original source... Go to PubMed...
Kou SG, Peters LM, Mucalo MR (2021). Chitosan: A review of sources and preparation methods. Int J Biol Macromol 169: 85-94. DOI: 10.1016/j.ijbiomac.2020.12.005.
Go to original source... Go to PubMed...
Kvesdi E, Szab-Meleg E, Abrahm IM (2021). The role of estradiol in traumatic brain injury: mechanism of treatment potential. Int J Mol Sci 22(1): 11. DOI: 10.3390/ijms22010011.
Go to original source... Go to PubMed...
Meyer C, Stenberg L, Gonzales-Perez F, Wrobel S, Ronchi G, Udina E, et al. (2016). Chitosan-film enhanced chitosan nerve guides for long- distance regeneration of peripheral nerves. Biomaterials 76: 33-51. DOI: 10.1016/j.biomaterials.2015.10.040.
Go to original source... Go to PubMed...
Minami S, Suzuki H, Okamoto Y, Fujinaga T, Shigemasa Y (1998). Chitin and chitosan activate complement via the alternative pathway. Carbohydr Polym 36(2-3): 151-155. DOI: 10.1016/S0144-8617(98)00015-0.
Go to original source...
Modrak M, Talukder MAH, Gurgenashvili K, Noble M, Elfar JC (2020). Peripheral nerve injury and myelination: Potential therapeutic strategies. J Neurosci Res 98(5): 780-795. DOI: 10.1002/jnr.24538.
Go to original source... Go to PubMed...
Murashov AK, Islamov RR, McMurray RJ, Pak ES, Weidner DA (2004). Estrogen increases retrograde labeling of motoneurons: evidence of a nongenomic mechanism. Am J Physiol Cell Physiol 287(2): C320-326. DOI: 10.1152/ajpcell.00542.2003.
Go to original source... Go to PubMed...
Nguyen HX, O'Barr TJ, Anderson AJ (2007). Polymorphonuclear leukocytes promote neurotoxicity through release of matrix metalloproteinases, reactive oxygen species, and TNF-alpha. J Neurochem 102(3): 900-912. DOI: 10.1111/j.1471-4159.2007.04643.x
Go to original source... Go to PubMed...
Nobakhti-Asfhar A, Najafpour A, Mohammadi R, Zarei L (2016) Assessment of neuroprotective effects on local administration of 17-beta-estradiol on peripheral nerve regeneration in ovariectomized female rats. Bull Emerg Trauma 4(3): 141-149.
Samantaray S, Das A, Matzelle DC, Yu SP, Wei L, Varma A, et al. (2016). Administration of low dose estrogen attenuates persistent inflammation, promotes angiogenesis and improves locomotor function following chronic spinal cord injury. J Neurochem 137(4): 604-617. DOI: 10.1111/jnc.13610.
Go to original source... Go to PubMed...
Santizo RA, Anderson S, Ye S, Koenig HM, Pelligrino DA (2000). Effects of estrogen on leukocyte adhesion after transient forebrain ischemia. Stroke 31(9): 2231-2235. DOI: 10.1161/01.str.31.9.2231.
Go to original source... Go to PubMed...
Siddiqui AN, Siddiqui N, Khan RA, Kalam A, Jabir NR, Kamal MA, et al. (2016). Neuroprotective role of steroidal sex hormones: an overview. CNS Neurosci Ther 22(5): 342-350. DOI: 10.1111/cns.12538.
Go to original source... Go to PubMed...
Smith PG, George M, Bradshaw S (2009). Estrogen promotes sympathetic nerve regeneration in rat proximal urethre. Urology 73(6): 1392-1396. DOI: 10.1016/j.urology.2008.11.052.
Go to original source... Go to PubMed...
Sribnick EA, Matzelle DD, Ray SK, Banik NL (2006). Estrogen treatment of spinal cord injury attenuates calpain activation and apoptosis. J Neurosci Res 84(5): 1064-1075. DOI: 10.1002/jnr.21016.
Go to original source... Go to PubMed...
Stenberg L, Kodama A, Lindwall-Blom C, Dahlin LB (2016). Nerve regeneration in chitosan conduits and in autologous nerve grafts in healthy and in type 2 diabetic Goto-Kakizaki rats. Eur J Neurosci 43(3): 463-473. DOI: 10.1111/ejn.13068.
Go to original source... Go to PubMed...
Turek A, Borecka A, Janeczek H, Sobota M, Kasperczyk J (2018). Formulation of delivery systems with risperidone based on biodegradable terpolymers. Int J Pharm 548(1): 159-172. DOI: 10.1016/j.ijpharm.2018.06.051.
Go to original source... Go to PubMed...
Turek A, Kasperczyk J, Jelonek K, Borecka A, Janeczek H, Libera M, et al. (2015). Thermal properties and morphology changes in degradation process of poly(L-lactide-co-glycolide) matrices with risperidone. Acta Bioeng Biomech 17(1): 11-20.
Turek A, Olakowska E, Borecka A, Janeczek H, Sobota M, Jaworska J, et al. (2016). Shape-memory terpolymer rods with 17-β-estradiol for the treatment of neurodegenerative diseases: in vitro and in vivo study. Pharm Res 33(12): 2967-2978. DOI: 10.1007/s11095-016-2019-9.
Go to original source... Go to PubMed...
Turek A, Stoklosa K, Borecka A, Paul-Samojedny M, Kaczmarczyk B, Marcinkowski A, Kasperczyk J (2020). Designing biodegradable wafers based on poly(L-lactide-co-glycolide) and poly(glycolide-co-ε-caprolactone) for the prolonged and local release of idarubicin for the therapy of glioblastoma multiforme. Pharm Res 37(5): 90. DOI: 10.1007/s11095-020-02810-2.
Go to original source... Go to PubMed...
Vegeto E, Ciana P, Maggi A (2002). Estrogen and inflammation: hormone generous action spreads to the brain. Mol Psychiatry 7(3): 236-238. DOI: 10.1038/sj.mp.4001007.
Go to original source... Go to PubMed...
Vrtanik P, Ostanek B, Mencej-Bedra S, Marc J (2014). The many faces of estrogen signaling. Biochem Med 24(3): 329-342. DOI: 10.11613/BM.2014.035.
Go to original source... Go to PubMed...
Wall PD, Devor M, Inbal R, Scadding JW, Schonfeld D, Seltzer Z, Tomkiewitz MM (1979). Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa. Pain 7(2): 103-111. DOI: 10.1016/0304-3959(79)90002-2.
Go to original source... Go to PubMed...
Wiliska J, Turek A, Borecka A, Rech J, Kasperczyk J (2019). Electron beam sterilization of implantable rods with risperidoneand with 17-β-estradiol: a structural, thermal and morphology study. Acta Bioeng Biomech 21(3): 39-47. DOI: 10.5277/ABB-01399-2019-01.
Go to original source...
Wlaszczuk A, Marcol W, Kucharska M, Wawro D, Palen P, Lewin-Kowalik J (2016). Poly (D, L-Lactide-Co-Glycolide) tubes with multifilament chitosan yarn or chitosan sponge core in nerve regeneration. J Oral Maxillofac Surg 74(11): 2327.e1-2327.e12. DOI: 10.1016/j.joms.2016.07.009.
Go to original source... Go to PubMed...
Zhao Y, Wang Y, Gong J, Yang L, Niu C, Ni X, et al. (2017). Chitosan degradation products facilitate peripheral nerve regeneration by improving macrophage-constructed microenvironments. Biomaterials 134: 64-77. DOI: 10.1016/j.biomaterials.2017.02.026.
Go to original source... Go to PubMed...
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.
Comments (0)