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.
-estradiol (E2)
17-β
Chitosan conduit
Inflammation
Sciatic nerve injury
Shape-memory terpolymer
Journal
Journal of applied biomedicine
ISSN: 1214-0287
Titre abrégé: J Appl Biomed
Pays: Poland
ID NLM: 101221755
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
received:
23
07
2021
accepted:
07
07
2022
entrez:
11
10
2022
pubmed:
12
10
2022
medline:
13
10
2022
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 36218129
doi: 10.32725/jab.2022.010
doi:
Substances chimiques
Receptors, Estradiol
0
Estradiol
4TI98Z838E
Chitosan
9012-76-4
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
87-97Subventions
Organisme : Medical University of Silesia
ID : PCN-1-090/K/0/O
Déclaration de conflit d'intérêts
The authors report no conflicts of interest in this work.
Références
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.
pubmed: 18929405
doi: 10.1016/j.biomaterials.2008.09.043
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.
pubmed: 25423896
doi: 10.1038/nrn3856
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.
pubmed: 31513774
doi: 10.1016/j.yfrne.2019.100787
Bąk 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.
pubmed: 29160628
doi: 10.17219/pim/75653
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.
pubmed: 21631508
doi: 10.1111/j.1471-4159.2011.07334.x
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.
pubmed: 27872858
doi: 10.1155/2016/7891202
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.
pubmed: 25845398
doi: 10.1089/neu.2014.3730
Dobrzyński 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.
pubmed: 26891883
doi: 10.1016/j.pneurobio.2015.12.008
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.
pubmed: 26740397
doi: 10.1016/j.brainres.2015.12.044
Gębarowska 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.
doi: 10.1016/j.eurpolymj.2011.02.022
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.
pubmed: 27884727
doi: 10.1016/j.jsbmb.2016.11.018
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.
pubmed: 23376237
doi: 10.1016/j.actbio.2013.01.025
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.
pubmed: 15843602
doi: 10.1523/JNEUROSCI.5279-04.2005
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.
pubmed: 12101051
doi: 10.1016/s0006-8993(02)02827-5
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.
pubmed: 18925549
doi: 10.1055/s-0028-1090619
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.
pubmed: 33279563
doi: 10.1016/j.ijbiomac.2020.12.005
Kövesdi E, Szabó-Meleg E, Abrahám 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.
pubmed: 33374952
doi: 10.3390/ijms22010011
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.
pubmed: 26517563
doi: 10.1016/j.biomaterials.2015.10.040
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.
doi: 10.1016/S0144-8617(98)00015-0
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.
pubmed: 31608497
doi: 10.1002/jnr.24538
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.
pubmed: 15044155
doi: 10.1152/ajpcell.00542.2003
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
pubmed: 17561941
doi: 10.1111/j.1471-4159.2007.04643.x
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.
pubmed: 26998684
doi: 10.1111/jnc.13610
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.
pubmed: 10978057
doi: 10.1161/01.str.31.9.2231
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.
pubmed: 27012165
doi: 10.1111/cns.12538
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.
pubmed: 19362354
doi: 10.1016/j.urology.2008.11.052
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.
pubmed: 16902996
doi: 10.1002/jnr.21016
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.
pubmed: 26355640
doi: 10.1111/ejn.13068
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.
pubmed: 29953927
doi: 10.1016/j.ijpharm.2018.06.051
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.
pubmed: 27628625
doi: 10.1007/s11095-016-2019-9
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.
pubmed: 32382838
doi: 10.1007/s11095-020-02810-2
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.
pubmed: 11920150
doi: 10.1038/sj.mp.4001007
Vrtačnik P, Ostanek B, Mencej-Bedrač S, Marc J (2014). The many faces of estrogen signaling. Biochem Med 24(3): 329-342. DOI: 10.11613/BM.2014.035.
pubmed: 25351351
doi: 10.11613/BM.2014.035
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.
pubmed: 574931
doi: 10.1016/0304-3959(79)90002-2
Wilińska 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.
doi: 10.5277/ABB-01399-2019-01
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.
pubmed: 27542542
doi: 10.1016/j.joms.2016.07.009
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.
pubmed: 28456077
doi: 10.1016/j.biomaterials.2017.02.026