Epothilone B loaded in acellular nerve allograft enhanced sciatic nerve regeneration in rats.
EpoB
allograft
decellularization
regeneration
sciatic nerve
Journal
Fundamental & clinical pharmacology
ISSN: 1472-8206
Titre abrégé: Fundam Clin Pharmacol
Pays: England
ID NLM: 8710411
Informations de publication
Date de publication:
19 Oct 2023
19 Oct 2023
Historique:
revised:
19
08
2023
received:
17
04
2023
accepted:
06
10
2023
medline:
20
10
2023
pubmed:
20
10
2023
entrez:
19
10
2023
Statut:
aheadofprint
Résumé
Epothilone B (EpoB) is a microtubule-stabilizing agent with neuroprotective properties. This study examines the regenerative properties of ANA supplemented with EpoB on a sciatic nerve deficit in male Wistar rats. For this purpose, the 10 mm nerve gap was filled with acellular nerve allografts (ANAs) containing EpoB at 0.1, 1, and 10 nM concentrations. The sensorimotor recovery was evaluated up to 16 weeks after the operation. Real-time PCR, histomorphometry analysis, and electrophysiological evaluation were also used to evaluate the process of nerve regeneration. ANA/EpoB (0.1 nM) significantly improved sensorimotor recovery in rats compared to ANA, ANA/EpoB (1 nM), and ANA/EpoB (10 nM) groups. This led to reduced muscle atrophy, improved sciatic functional index, and thermal paw withdrawal reflex latency, indicating nerve regeneration and target organ reinnervation. The electrophysiological and histomorphometry findings also confirmed the ANA/EpoB regenerative properties (0.1 nM). EpoB only enhanced ANA regenerative properties at 0.1 nM, with no therapeutic effects at higher concentrations. Totally, we concluded that ANA loaded with 0.1 nM EpoB can effectively reconstruct the transected sciatic nerve in rats, likely by enhancing axonal sprouting and extension.
Sections du résumé
BACKGROUND
BACKGROUND
Epothilone B (EpoB) is a microtubule-stabilizing agent with neuroprotective properties.
OBJECTIVES
OBJECTIVE
This study examines the regenerative properties of ANA supplemented with EpoB on a sciatic nerve deficit in male Wistar rats.
METHODS
METHODS
For this purpose, the 10 mm nerve gap was filled with acellular nerve allografts (ANAs) containing EpoB at 0.1, 1, and 10 nM concentrations. The sensorimotor recovery was evaluated up to 16 weeks after the operation. Real-time PCR, histomorphometry analysis, and electrophysiological evaluation were also used to evaluate the process of nerve regeneration.
RESULTS
RESULTS
ANA/EpoB (0.1 nM) significantly improved sensorimotor recovery in rats compared to ANA, ANA/EpoB (1 nM), and ANA/EpoB (10 nM) groups. This led to reduced muscle atrophy, improved sciatic functional index, and thermal paw withdrawal reflex latency, indicating nerve regeneration and target organ reinnervation. The electrophysiological and histomorphometry findings also confirmed the ANA/EpoB regenerative properties (0.1 nM). EpoB only enhanced ANA regenerative properties at 0.1 nM, with no therapeutic effects at higher concentrations.
CONCLUSION
CONCLUSIONS
Totally, we concluded that ANA loaded with 0.1 nM EpoB can effectively reconstruct the transected sciatic nerve in rats, likely by enhancing axonal sprouting and extension.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : University of Mohaghegh Ardabili, Iran
Organisme : Tishk International University, Erbil, Kurdistan Region, Iraq
ID : 923
Informations de copyright
© 2023 Société Française de Pharmacologie et de Thérapeutique. Published by John Wiley & Sons Ltd.
Références
Lackington WA, Ryan AJ, O'Brien FJ. Advances in nerve guidance conduit-based therapeutics for peripheral nerve repair. ACS Biomater Sci Eng. 2017;3(7):1221-1235. doi:10.1021/acsbiomaterials.6b00500
Scheib J, Höke A. Advances in peripheral nerve regeneration. Nat Rev Neurol. 2013;9(12):668-676. doi:10.1038/nrneurol.2013.227
Siemionow M, Bozkurt M, Zor F. Regeneration and repair of peripheral nerves with different biomaterials: review. Microsurgery. 2010;30(7):574-588. doi:10.1002/micr.20799
Neubauer D, Graham JB, Muir D. Nerve grafts with various sensory and motor fiber compositions are equally effective for the repair of a mixed nerve defect. Exp Neurol. 2010;223(1):203-206. doi:10.1016/j.expneurol.2009.08.013
Mackinnon SE, Hudson AR. Clinical application of peripheral nerve transplantation. Plast Reconstr Surg. 1992;90(4):695-699. doi:10.1097/00006534-199210000-00024
Yu X, Bellamkonda RV. Tissue-engineered scaffolds are effective alternatives to autografts for bridging peripheral nerve gaps. Tissue Eng. 2003;9(3):421-430. doi:10.1089/107632703322066606
Struzyna LA, Harris JP, Katiyar KS, Chen HI, Cullen DK. Restoring nervous system structure and function using tissue engineered living scaffolds. Neural Regen Res. 2015;10(5):679-685. doi:10.4103/1673-5374.156943
Mohammad-Bagher G, Arash A, Morteza B-R, Naser M-S, Ali M. Synergistic effects of acetyl-l-carnitine and adipose-derived stromal cells on improving regenerative capacity of acellular nerve allograft in sciatic nerve defect. J Pharmacol Exp Ther. 2019;368(3):490-502. doi:10.1124/jpet.118.254540
Moore AM, Macewan M, Santosa KB, et al. Acellular nerve allografts in peripheral nerve regeneration: a comparative study. Muscle Nerve. 2011;44(2):221-234. doi:10.1002/mus.22033
Gulati AK, Cole G. Immunogenicity and regenerative potential of acellular nerve allografts to repair peripheral nerve in rats and rabbits. Acta Neurochir. 1994;126(2-4):158-164. doi:10.1007/BF01476427
Zheng C, Zhu Q, Liu X, et al. Improved peripheral nerve regeneration using acellular nerve allografts loaded with platelet-rich plasma. Tissue Eng Part A. 2014;20(23-24):3228-3240. doi:10.1089/ten.tea.2013.0729
Yu H, Peng J, Guo Q, et al. Improvement of peripheral nerve regeneration in acellular nerve grafts with local release of nerve growth factor. Microsurgery. 2009;29(4):330-336. doi:10.1002/micr.20635
Liu J, Li L, Zou Y, et al. Role of microtubule dynamics in Wallerian degeneration and nerve regeneration after peripheral nerve injury. Neural Regen Res. 2022;17(3):673-681. doi:10.4103/1673-5374.320997
Ruschel J, Bradke F. Systemic administration of epothilone D improves functional recovery of walking after rat spinal cord contusion injury. Exp Neurol. 2018;306:243-249. doi:10.1016/j.expneurol.2017.12.001
Petrášek J, Schwarzerová K. Actin and microtubule cytoskeleton interactions. Curr Opin Plant Biol. 2009;12(6):728-734. doi:10.1016/j.pbi.2009.09.010
Tanaka E, Ho T, Kirschner MW. The role of microtubule dynamics in growth cone motility and axonal growth. J Cell Biol. 1995;128(1):139-155. doi:10.1083/jcb.128.1.139
Gomez TM, Letourneau PC. Actin dynamics in growth cone motility and navigation. J Neurochem. 2014;129(2):221-234. doi:10.1111/jnc.12506
Bradke F, Fawcett JW, Spira ME. Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat Rev Neurosci. 2012;13(3):183-193. doi:10.1038/nrn3176
Kalil K, Szebenyi G, Dent EW. Common mechanisms underlying growth cone guidance and axon branching. J Neurobiol. 2000;44(2):145-158. doi:10.1002/1097-4695(200008)44:2%3C145::AID-NEU5%3E3.0.CO;2-X
Dent EW, Gertler FB. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron. 2003;40(2):209-227. doi:10.1016/S0896-6273(03)00633-0
Lowery LA, Vactor DV. The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol. 2009;10(5):332-343. doi:10.1038/nrm2679
Mahmoodi N, Ai J, Hassannejad Z, et al. Improving motor neuron-like cell differentiation of hEnSCs by the combination of epothilone B loaded PCL microspheres in optimized 3D collagen hydrogel. Sci Rep. 2021;11(1):21722. doi:10.1038/s41598-021-01071-2
Ruschel J, Hellal F, Flynn KC, et al. Systemic administration of epothilone B promotes axon regeneration after spinal cord injury. Science. 2015;348(6232):347-352. doi:10.1126/science.aaa2958
Yang Y, Zhang X, Ge H, et al. Epothilone B benefits nigrostriatal pathway recovery by promoting microtubule stabilization after intracerebral hemorrhage. J Am Heart Assoc. 2018;7(2):e007626. doi:10.1161/JAHA.117.007626
Kugler C, Thielscher C, Tambe BA, et al. Epothilones improve axonal growth and motor outcomes after stroke in the adult mammalian CNS. Cell Rep Med. 2020;1(9):100159. doi:10.1016/j.xcrm.2020.100159
Yu Z, Yang L, Yang Y, et al. Epothilone B benefits nigral dopaminergic neurons by attenuating microglia activation in the 6-hydroxydopamine lesion mouse model of Parkinson's disease. Front Cell Neurosci. 2018;12:324. doi:10.3389/fncel.2018.00324
Cartelli D, Casagrande F, Busceti CL, et al. Microtubule alterations occur early in experimental parkinsonism and the microtubule stabilizer epothilone D is neuroprotective. Sci Rep. 2013;3(1):1837. doi:10.1038/srep01837
Zhou J, Li S, Gao J, et al. Epothilone B facilitates peripheral nerve regeneration by promoting autophagy and migration in Schwann cells. Front Cell Neurosci. 2020;14:143. doi:10.3389/fncel.2020.00143
Chiorazzi A, Nicolini G, Canta A, et al. Experimental epothilone B neurotoxicity: results of in vitro and in vivo studies. Neurobiol Dis. 2009;35(2):270-277. doi:10.1016/j.nbd.2009.05.006
Jang E-H, Sim A, Im S-K, Hur E-M. Effects of microtubule stabilization by epothilone B depend on the type and age of neurons. Neural Plast. 2016;2016:5056418. doi:10.1155/2016/5056418
Ciccozzi M, Menga R, Ricci G, et al. Critical review of sham surgery clinical trials: confounding factors analysis. Ann Med Surg. 2016;12:21-26. doi:10.1016/j.amsu.2016.10.007
Wasman Smail S, Ziyad Abdulqadir S, Omar Khudhur Z, et al. IL-33 promotes sciatic nerve regeneration in mice by modulating macrophage polarization. Int Immunopharmacol. 2023;123:110711. doi:10.1016/j.intimp.2023.110711
Hu Y, Wu Y, Gou Z, et al. 3D-engineering of cellularized conduits for peripheral nerve regeneration. Sci Rep. 2016;6(1):32184. doi:10.1038/srep32184
Kim J-H, Choi Y-J, Park H-I, Ahn K-M. The effect of FK506 (tacrolimus) loaded with collagen membrane and fibrin glue on promotion of nerve regeneration in a rat sciatic nerve traction injury model. Maxillofacial Plastic Reconstr Surg. 2022;44(1):14. doi:10.1186/s40902-022-00339-5
Hudson TW, Liu SY, Schmidt CE. Engineering an improved acellular nerve graft via optimized chemical processing. Tissue Eng. 2004;10(9-10):1346-1358. doi:10.1089/ten.2004.10.1346
Raimondo S, Fornaro M, Di Scipio F, Ronchi G, Giacobini-Robecchi MG, Geuna S. Methods and protocols in peripheral nerve regeneration experimental research: part II-morphological techniques. Int Rev Neurobiol. 2009;87:81-103. doi:10.1016/S0074-7742(09)87005-0
Kerrison P, Steinke M. DAPI staining protocol. 2010.
Bernal J, Baldwin M, Gleason T, Kuhlman S, Moore G, Talcott M. Guidelines for rodent survival surgery. J Invest Surg. 2009;22(6):445-451. doi:10.3109/08941930903396412
Sarikcioglu L, Demirel B, Utuk A. Walking track analysis: an assessment method for functional recovery after sciatic nerve injury in the rat. Folia Morphol. 2009;68(1):1-7.
Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 1988;32(1):77-88. doi:10.1016/0304-3959(88)90026-7
Schulz A, Walther C, Morrison H, Bauer R. In vivo electrophysiological measurements on mouse sciatic nerves. J Vis Exp. 2014;(86):e51181. doi:10.3791/51181-v
Scipio FD, Raimondo S, Tos P, Geuna S. A simple protocol for paraffin-embedded myelin sheath staining with osmium tetroxide for light microscope observation. Microsc Res Tech. 2008;71(7):497-502. doi:10.1002/jemt.20577
Varejão AS, Melo-Pinto P, Meek MF, Filipe VM, Bulas-Cruz J. Methods for the experimental functional assessment of rat sciatic nerve regeneration. Neurol Res. 2004;26(2):186-194. doi:10.1179/016164104225013833
Marrocco F, Delli Carpini M, Garofalo S, et al. Short-chain fatty acids promote the effect of environmental signals on the gut microbiome and metabolome in mice. Commun Biol. 2022;5(1):517. doi:10.1038/s42003-022-03468-9
Piovesana R, Faroni A, Taggi M, et al. Muscarinic receptors modulate Nerve Growth Factor production in rat Schwann-like adipose-derived stem cells and in Schwann cells. Sci Rep. 2020;10(1):7159. doi:10.1038/s41598-020-63645-w
Geissler J, Stevanovic M. Management of large peripheral nerve defects with autografting. Injury. 2019;50:S64-S67. doi:10.1016/j.injury.2019.10.051
Gu X, Ding F, Williams DF. Neural tissue engineering options for peripheral nerve regeneration. Biomaterials. 2014;35(24):6143-6156. doi:10.1016/j.biomaterials.2014.04.064
Fu R-H, Wang Y-C, Liu S-P, et al. Decellularization and recellularization technologies in tissue engineering. Cell Transplant. 2014;23(4-5):621-630. doi:10.3727/096368914X678382
Lin MY, Manzano G, Gupta R. Nerve allografts and conduits in peripheral nerve repair. Hand Clin. 2013;29(3):331-348. doi:10.1016/j.hcl.2013.04.003
Önger ME, Delibaş B, Türkmen AP, Erener E, Altunkaynak BZ, Kaplan S. The role of growth factors in nerve regeneration. Drug Discov Ther. 2016;10(6):285-291. doi:10.5582/ddt.2016.01058
Li R, Li D-H, Zhang H-Y, Wang J, Li X-K, Xiao J. Growth factors-based therapeutic strategies and their underlying signaling mechanisms for peripheral nerve regeneration. Acta Pharmacol Sin. 2020;41(10):1289-1300. doi:10.1038/s41401-019-0338-1
Tomita K, Kubo T, Matsuda K, et al. The neurotrophin receptor p75NTR in Schwann cells is implicated in remyelination and motor recovery after peripheral nerve injury. Glia. 2007;55(11):1199-1208. doi:10.1002/glia.20533
Assinck P, Sparling JS, Dworski S, et al. Transplantation of skin precursor-derived Schwann cells yields better locomotor outcomes and reduces bladder pathology in rats with chronic spinal cord injury. Stem Cell Rep. 2020;15(1):140-155. doi:10.1016/j.stemcr.2020.05.017
Zhang C, Zhang P, Wang Y, Yu K, Kou Y, Jiang B. Early spatiotemporal progress of myelinated nerve fiber regenerating through biological chitin conduit after injury. Artif Cells Blood Subst Biotechnol. 2010;38(2):103-108. doi:10.3109/10731191003634836
Min Q, Parkinson DB, Dun XP. Migrating Schwann cells direct axon regeneration within the peripheral nerve bridge. Glia. 2021;69(2):235-254. doi:10.1002/glia.23892
Saheb-al-Zamani M, Yan Y, Farber SJ, et al. Limited regeneration in long acellular nerve allografts is associated with increased Schwann cell senescence. Exp Neurol. 2013;247:165-177. doi:10.1016/j.expneurol.2013.04.011
Namgung U. The role of Schwann cell-axon interaction in peripheral nerve regeneration. Cell Tissue Org. 2015;200(1):6-12. doi:10.1159/000370324
Lefcort F, Venstrom K, McDonald JA, Reichardt LF. Regulation of expression of fibronectin and its receptor, alpha 5 beta 1, during development and regeneration of peripheral nerve. Development. 1992;116(3):767-782. doi:10.1242/dev.116.3.767
Gao X, Wang Y, Chen J, Peng J. The role of peripheral nerve ECM components in the tissue engineering nerve construction. Rev Neurosci. 2013;24(4):443-453. doi:10.1515/revneuro-2013-0022
McGregor CE, English AW. The role of BDNF in peripheral nerve regeneration: activity-dependent treatments and Val66Met. Front Cell Neurosci. 2019;12:522. doi:10.3389/fncel.2018.00522