Journal Home > Volume 6 , Issue 1

Peripheral nerve injury is an important clinical problem that can exert hazardous effects on the health of patients. For this reason, there are more studies conducted on the regeneration of the peripheral nerves via the usage of the nerves belonging to various animals with different types of lesions, ages, and by using different methods of assessment with regular follow-up. Contrary to data obtained through experimentation and clinical observation, no ideal way of treatment was found to increase the regeneration of the peripheral nerves. Finally, the effects of melatonin in the protection of peripheral nerves against trauma, especially the protection of sciatic nerve from pathological conditions, have come into attention in a wide group of scientists as there are beneficial effects of melatonin after surgery. While numerous studies indicate the melatonin’s protective effects on the pathologies of nerves, there are also studies reporting its toxic effects on peripheral nerves. Melatonin is a widespread and crucial signaling molecule due to its features of free radical scavenging and anti-oxidation at both pharmacological and physiological conditions in vivo. In this context, although there are numerous studies elaborating the effects of melatonin in various tissues, its effects on peripheral nerves was documented in only a limited number of studies. The aim of this article was to perform a review of the knowledge in the literature on the subject of mostly beneficial or hazardous effects of melatonin on the repair of the damaged peripheral nerves.


menu
Abstract
Full text
Outline
About this article

Melatonin and sciatic nerve injury repair: a current perspective

Show Author's information Berrin Zuhal Altunkaynak1( )Burcu Delibaş2Gamze Altun2Ömür Gülsüm Deniz2
Department of Histology and Embryology, Medical Faculty, Okan University, Istanbul; Turkey
Department of Histology and Embryology, Medical Faculty, Ondokuz Mayıs University, Samsun, Turkey

Abstract

Peripheral nerve injury is an important clinical problem that can exert hazardous effects on the health of patients. For this reason, there are more studies conducted on the regeneration of the peripheral nerves via the usage of the nerves belonging to various animals with different types of lesions, ages, and by using different methods of assessment with regular follow-up. Contrary to data obtained through experimentation and clinical observation, no ideal way of treatment was found to increase the regeneration of the peripheral nerves. Finally, the effects of melatonin in the protection of peripheral nerves against trauma, especially the protection of sciatic nerve from pathological conditions, have come into attention in a wide group of scientists as there are beneficial effects of melatonin after surgery. While numerous studies indicate the melatonin’s protective effects on the pathologies of nerves, there are also studies reporting its toxic effects on peripheral nerves. Melatonin is a widespread and crucial signaling molecule due to its features of free radical scavenging and anti-oxidation at both pharmacological and physiological conditions in vivo. In this context, although there are numerous studies elaborating the effects of melatonin in various tissues, its effects on peripheral nerves was documented in only a limited number of studies. The aim of this article was to perform a review of the knowledge in the literature on the subject of mostly beneficial or hazardous effects of melatonin on the repair of the damaged peripheral nerves.

Keywords: regeneration, melatonin, peripheral nerve injury, light and electron microscopy

References(142)

1.
Hasegawa T, Kuroda M. A new role of uric acid as an antioxidant in human plasma. Rinsho Byori. 1989;37(9):1020-1027.
2.
Grogan BF, Hsu JR. Volumetric muscle loss. J Am Acad Orthop Surg. 2011;19(1):35-37.
3.
Grasman JM, Zayas MJ, Page RL, Pins GD. Biomimetic scaffolds for regeneration of volumetric muscle loss in skeletal muscle injuries. Acta Biomater. 2015;25:2-15.
4.
Dagum AB. Peripheral nerve regeneration, repair, and grafting. J Hand Ther. 1998;11(2):111-117.
5.
Sunderland S. A classification of peripheral nerve injuries producing loss of function. Brain. 1951;74(4):491-516.
6.
Seddon HJ. Three types of nerve injuries. Brain. 1943;66(4):237-288.
7.
Ichihara S, Inada Y, Nakamura T. Artificial nerve tubes and their application for repair of peripheral nerve injury: an update of current concepts. Injury. 2008;39(4):29-39.
8.
Allodi I, Udina E, Navarro X. Specificity of peripheral nerve regeneration: interactions at the axon level. Prog Neurobiol. 2012;98(1):16-37.
9.
Sivak WN, White JD, Bliley JM, et al. Delivery of chondroitinase ABC and glial cell line-derived neurotrophic factor from silk fibroin conduits enhances peripheral nerve regeneration. J Tissue Eng Regen Med. 2014;11(3):733-742.
10.
Waller A. Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos Trans R Soc Lond. 1850;140:423-429.
11.
Rotshenker S, Aamar S, Barak V. Interleukin-1 activity inlesioned peripheral nerve. J Neuroimmunol. 1992;39(1-2):75-80.
12.
Reicherd F, Rotshenker S. Deficient activation of microglia during optic nerve regeneration. J Neuroimmunol. 1996;70:153-161.
13.
Brück W. The role of macrophages in Wallerian degeneration. Brain Pathol. 1997;7(2):741-752.
14.
Stoll G, Jander S. The role of the microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol. 1999;58(3):233-247.
15.
Jander S, Pohl J, Gillen C, Stoll G. Differential expression of inter-leukin-10 Mrna in Wallerian degeneration and immune mediated inflamation of the rat peripheral nervous system. J Neurosci Res. 1996;43(2):254-259.
DOI
16.
LoPachin RM, Lehning EJ. Mechanism of calcium entry during axon injury and degeneration. Toxicol Appl Pharmacol. 1997;143(2):233-244.
17.
Manev H, Favaron M, Guidotti A, Costa E. Delayed increase of Ca2þ influx elicited by glutamate: role in neuronal death. Mol Pharmacol. 1989;36(1):106-112.
18.
Yang KJ, Yan Y, Zhang LL, et al. Increasing calcium level limits Schwann cell numbers in vitro following peripheral nerve injury. J Reconstr Microsurg. 2017;33(6):435-440.
19.
Perry VH, Brown MC, Lunn ER, Tree P, Gordon S. Evidence that very slow Wallerian degeneration in C57BL/Ola mice is an intrinsic property of the peripheral nerve. Eur J Neurosci. 1990;2(9):802-808.
20.
Glass JD, Brushart TM, George EB, Griffin JW. Prolonged survival of transsected nerve fibres in C57BL/Ola mice is an intrinsic characteristic of the axon. J Neurocytol. 1993;22(5):311-321.
21.
Bolin LM, Verity AN, Silver JE, Shooter EM, Abrams JS. Interleukin-6 production by schwann cells and induction in sciatic nerve injury. J Neurochem. 1995;64(2):850-858.
22.
Bourde O, Kiefer R, Toyka KV, Hartung HP. Quantification of interleukin 6 Mrna in Wallerian degeneration by competititve reverse transcription polymerase chain reaction. J Neuroimmunol. 1996;69(1-2):135-140.
23.
Lin SF, Chien JY, Kapupara K, Huang CF, Huang SP. Oroxylin A promotes retinal ganglion cell survival in a rat optic nerve crush model. PLoS One. 2017;12(6):e0178584.
24.
Lunn ER, Perry VH, Brown MC, Rosen H, Gordon S. Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur J Neurosci. 1989;1(1):27-33.
25.
Beirowski B, Adalbert R, Wagner D, et al. The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves. BMC Neurosci. 2005;6:6.
26.
Gilley J, Coleman MP. Endogenous NMNAT2 is an essential survival factor for maintenance of healthy axons. PLoS Biol. 2010;8(1):e1000300.
27.
Osterloh JM, Yang J, Rooney TM, et al. dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science. 2012;337(6093): 481-484.
28.
Gerdts J, Summers DW, Sasaki Y, DiAntonio A, Milbrandt J. Sarm1-mediated axon degeneration requires both SAM and TIR interactions. J Neurosci. 2013;33(33):13569-13580.
29.
Lauria G, Lombardi R. Skin biopsy: a new tool for diagnosing peripheral neuropathy. BMJ. 2007;334(7604):1159-1162.
30.
Conforti L, Gilley J, Coleman MP. Wallerian degeneration: an emerging axon death pathway linking injury and disease. Nat Rev Neurosci. 2014;15(6):394-409.
31.
Perrin FE, Lacroix S, Aviles-Trigueros M, David S. Involvement of monocyte chemoattractant protein-1, macrophage inflammatory protein-1 alpha and interleukin-1beta in Wallerian degeneration. Brain. 2005;128(pt 4):854-866.
32.
Boivin A, Pineau I, Barrette B, et al. Toll-like receptor signalling is critical for Wallerian degeneration and functional recovery after peripheral nerve injury. J Neurosci. 2017;27(46):12565-12576.
33.
Chen ZL, Yu WM, Strickland S. Peripheral regeneration. Annu Rev Neurosci. 2007;30:209-233.
34.
Vargas ME, Barres BA. Why is Wallerian degeneration in the CNS so slow? Annu Rev Neurosci. 2007;30:153-179.
35.
Camara-Lemarroy CR, Guzman-de la Garza FJ, Fernandez-Garza NE. Molecular inflammatory mediators in peripheral nerve degeneration and regeneration. Neuroimmunomodulation. 2010;17(5):314-324.
36.
Bosse F. Extrinsic cellular and molecular mediators of peripheral axonal regeneration. Cell Tissue Res. 2012;349(1):5-14.
37.
Napoli I, Noon LA, Ribeiro S, et al. A central role for ERK-signalling pathway in controlling Schwan cell plasticity and peripheral nevre regeneration in vivo. Neuron. 2012;73(4):729-742.
38.
Menorca RM, Fussell TS, Elfar JC. Nerve physiology: mechanisms of injury and recovery. Hand Clin. 2013;29(3):317-330.
39.
Bastien D, Lacroix S. Cytokine pathways regulating glial and leukocyte function after spinal cord and peripheral nerve injury. Exp Neurol. 2014;258:62-77.
40.
Brosius LA, Barres BA. Contrasting the glial response to axon injury in the central and peripheral nervous systems. Dev Cell. 2014;28(1):7-17.
41.
DeFrancesco-Lisowitz A, Lindborg JA, Niemi JP, Zigmond RE. The neuroimmunology of degeneration and regeneration in the peripheral nervous system. Neuroscience. 2015;302:174-203.
42.
Mietto BS, Mostacada K, Martinez AM. Neurotrauma and inflammation: CNS and PNS responses. Mediators Inflamm. 2015;2015:251204.
43.
Reiter RJ. The pineal gland and melatonin in relation to aging: a summary of the theories and of the data. Exp Gerontol. 1995;30(3-4):199-212.
44.
Rodriguez C, Mayo JC, Sainz RM, et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res. 2004;36(1):1-9.
45.
Uyanikgil Y, Baka M, Ateş U, et al. Neuroprotective effects of melatonin upon the offspring cerebellar cortex in the rat model of BCNU-induced cortical dysplasia. Brain Res. 2007;1160:134-144.
46.
Axelrod J, Wurtman RJ. Photic and neural control of indoleamine metabolism in the rat pineal gland. Adv Pharmacol. 1968;6(pt A):157-166.
47.
Claustrat B, Brun J, Chazot G. The basic physiology and pathophysiology of melatonin. Sleep Med Rev. 2005;9(1):11-24.
48.
Skene DJ, Papagiannidou E, Hashemi E, et al. Contribution of CYP1A2 in the hepatic metabolism of melatonin: studies with isolated microsomal preparations and liver slices. J Pineal Res. 2001;31(4):333-342.
49.
Hirata F. Melatonin. No Shinkei Geka. 1974;2(3):207-212.
50.
Hardeland R, Reiter RJ, Poeggeler B, Tan DX. The significance of the metabolism of the neurohormone melatonin: antioxidative protection and formation of bioactive substances. Neurosci Biobehav Rev. 1993;17(3):347-357.
51.
Tan DX, Manchester LC, Terron MP, Flores LJ, Reiter RJ. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res. 2007;42(1): 28-42.
52.
Cassone VM. Effects of melatonin on vertebrate circadian systems. Trends Neurosci. 1990;13(11):457-464.
53.
Blask DE, Hill SM, Orstead KM, Massa JS. Inhibitory effects of the pineal hormone melatonin and underfeeding during the promotional phase of 7,12 dimethylbenzanthracene-(DMBA)-induced mammary tumorigenesis. J Neural Transm. 1986;67(1-2):125-138.
54.
Maestroni GJ, Conti A, Pierpaoli W. Role of the pineal gland in immunity: II. Melatonin enhances the antibody response via an opiatergic mechanism. Clin Exp Immunol. 1987;68(2):384-391.
55.
Tan DX, Chen LD, Poeggeler B, et al. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocr J. 1993;1:57-60.
56.
Steinhilber D, Brungs M, Werz O, et al. The nuclear receptor for melatonin repress 5-lipoxygenase gene expression in human B lymphocytes. J Biol Chem. 1995;270(13):7037-7040.
57.
Reiter RJ. Oxidative processes and antioxidative defense mechanisms in the aging brain. FASEB J. 1995;9(7):526-533.
58.
Reiter RJ. Oxidative damage in the central nervous system: protection by melatonin. Prog Neurobiol. 1998;56(3):359-384.
59.
Reiter RJ, Maestroni G. Melatonin in relation to the antioxidative defense and immune systems: possible implications for cell and organ transplantation. J Mol Med. 1999;77(1):36-39.
60.
Karbownik M, Reiter RJ. Antioxidative effects of melatonin in protection against cellular damage caused by ionizing radiation. Proc Soc Exp Biol Med. 2000;225(1):9-22.
61.
Reiter RJ, Tan DX. Melatonin: a novel protective agent against oxidative injury of the ischemic/reperfused heart. Cardiovasc Res. 2003;58(1):10-19.
62.
Allegra M, Reiter RJ, Tan DX, Gentile C, Tesoriere L, Livrea MA. The chemistry of melatonin’s interaction with reactive species. J Pineal Res. 2003;34(1):1-10.
63.
Tan DX, Manchester LC, Sanchez-Barcelo E, Mediavilla MD, Reiter RJ. Significance of high levels of endogenous melatonin in Mammalian cerebrospinal fluid and in the central nervous system. Curr Neuropharmacol. 2010;8(3):162-167.
64.
Tan DX, Manchester LC, Liu X, Rosales-Corral SA, Acuna-Castroviejo D, Reiter RJ. Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin’s primary function and evolution in eukaryotes. J Pineal Res. 2013;54(2): 127-138.
65.
Qiu T, Yin Y, Li B. PDLLA/PRGD/beta-TCP conduits build the neurotrophin-rich microenvironment suppressing the oxidative stress and promoting the sciatic nerve regeneration. J Biomed Mater Res A. 2014;102(10):3734-3743.
66.
Menovsky T, Beek JF. Laser, fibrin glue, or suture repair of peripheral nerves: a comparative functional, histological, and morphometric study in the rat sciatic nerve. J Neurosurg. 2001;95(4):694-699.
67.
Pichichero M, Beer B, Clody DE. Effects of dibutyryl cyclic AMP on restoration of function of damaged sciatic nerve in rats. Science. 1973;182(4113):724-725.
68.
Cockett SA, Kiernan JA. Acceleration of peripheral nervous regeneration in the rat by exogenous triiodothyronine. Exp Neurol. 1973;39(3):389-394.
69.
Roisen FJ, Murphy RA, Pichichero ME, Braden WG. Cyclic adenosine monophosphate stimulation of axonal elongation. Science. 1972;175(4017):73-74.
70.
Behram Kandemir Y, Sarikcioglu L. Melatonin and its therapeutic actions on peripheral nerve regeneration. Folia Morphol (Warsz). 2015;74(3):283-289.
71.
KayaY, Savas K, Sarikcioglu L, Yaras N, Angelov DN. Melatonin leads to axonal regeneration, reduction in oxidative stress, and improved functional recovery following sciatic nerve injury. Curr Neurovasc Res. 2015;12(1):53-62.
72.
Keskin I, Kaplan S, Kalkan S, Sutcu M, Ulkay MB, Esener OB. Evaluation of neuroprotection by melatonin against adverse effects of prenatal exposure to a nonsteroidal anti-inflammatory drug during peripheral nerve development. Int J Dev Neurosci. 2015;41:1-7.
73.
Yanilmaz M, Akduman D, Sagun OF, et al. The effects of aminoguanidine, methylprednisolone, and melatonin on nerve recovery in peripheral facial nerve neurorrhaphy. J Craniofac Surg. 2015;26(3):667-672.
74.
Matsuyama T, Mackay M, Midha R. Peripheral nerve repair and grafting techniques: a review. Neurol Med Chir (Tokyo). 2000;40(4):187-199.
75.
Mekaj AY, Morina AA, Bytyqi CI, Mekaj YH, Duci SB. Application of topical pharmacological agents at the site of peripheral nerve injury and methods used for evaluating the success of the regenerative process. J Orthop Surg Res. 2014;9:94.
76.
Onger ME, Kaplan S, Deniz OG, et al. Possible promoting effects of melatonin, leptin and alcar on regeneration of the sciatic nerve. J Chem Neuroanat. 2017;81:34-41.
77.
Onger ME, Kaplan S, Geuna S. Possible effects of some agents on the injured nerve in obese rats: a stereological and electron microscopic study. J Craniomaxillofac Surg. 2017;45(8):1258-1267.
78.
Altun A, Ugur-Altun B. Melatonin: therapeutic and clinical utilization. Int J Clin Pract. 2007;61(5):835-845.
79.
Reiter RJ, Tan DX, Leon J, Kilic U, Kilic E. When melatonin gets on your nerves: its beneficial actions in experimental models of stroke. Exp Biol Med (Maywood). 2005;230(2):104-117.
80.
Sahna E, Acet A, Ozer MK, Olmez E. Myocardial ischemia-reperfusion in rats: reduction of infarct size by either supplemental physiological or pharmacological doses of melatonin. J Pineal Res. 2002;33(4):234-238.
81.
Turgut M, Uysal A, Pehlivan M, Oktem G, Yurtseven ME. Assessment of effects of pinealectomy and exogenous melatonin administration on rat sciatic nerve suture repair: an electrophysiological, electron microscopic, and immunohistochemical study. Acta Neurochir (Wien). 2005;147(1):67-77.
82.
Davison SP, McCaffrey TV, Porter MN, Manders E. Improved nerve regeneration with neutralization of transforming growth factor-beta1. Laryngoscope. 1999;109(4):631-635.
83.
Kaplan S, Piskin A, Ayyildiz M, et al. The effect of melatonin and platelet gel on sciatic nerve repair: an electrophysiological and stereological study. Microsurgery. 2011;31(4):306-313.
84.
Drobnik J, Dabrowski R. Melatonin suppresses the pinealectomy-induced elevation of collagen content in a wound. Cytobios. 1996;85(340):51-58.
85.
Shokouhi G, Tubbs RS, Shoja MM, et al. Neuroprotective effects of high-dose vs low-dose melatonin after blunt sciatic nerve injury. Childs Nerv Syst. 2008;24(1):111-117.
86.
Stavisky RC, Britt JM, Zuzek A, Truong E, Bittner GD. Melatonin enhances the in vitro and in vivo repair of severed rat sciatic axons. Neurosci Lett. 2005;376(2):98-101.
87.
Khalil Z, Khodr B. A role for free radicals and nitric oxide in delayed recovery in aged rats with chronic constriction nerve injury. Free Radic Biol Med. 2001;31(4):430-439.
88.
Naik AK, Tandan SK, Dudhgaonkar SP, et al. Role of oxidative stress in pathophysiology of peripheral neuropathy and modulation by N-acetyl-L-cysteine in rats. Eur J Pain. 2006;10(7):573-579.
89.
Kong X, Li X, Cai Z, et al. Melatonin regulates the viability and differentiation of rat midbrain neural stem cells. Cell Mol Neurobiol. 2008;28(4):569-579.
90.
Odaci E, Kaplan S. Chapter 16: melatonin and nerve regeneration. Int Rev Neurobiol. 2009;87:317-335.
91.
Huerto-Delgadillo L, Anton-Tay F, Benitez-King G. Effects of melatonin on microtubule assembly depend on hormone concentration: role of melatonin as a calmodulin antagonist. J Pineal Res. 1994;17(2):55-62.
92.
Atik B, Erkutlu I, Tercan M, Buyukhatipoglu H, Bekerecioglu M, Pence S. The effects of exogenous melatonin on peripheral nerve regeneration and collagen formation in rats. J Surg Res. 2011;166(2):330-336.
93.
Turgut M, Kaplan S. Effects of melatonin on peripheral nerve regeneration. Recent Pat Endocr Metab Immune Drug Discov. 2011;5(2):100-108.
94.
Chang HM, Huang YL, Lan CT, Wu UI, Hu ME, Youn SC. Melatonin preserves superoxide dismutase activity in hypoglossal motoneurons of adult rats following peripheral nerve injury. J Pineal Res. 2008;44(2):172-180.
95.
El-Abhar HS, Shaalan M, Barakat M, El-Denshary ES. Effect of melatonin and nifedipine on some antioxidant enzymes and different energy fuels in the blood and brain of global ischemic rats. J Pineal Res. 2002;33(2):87-94.
96.
Sayan H, Ozacmak VH, Ozen OA, et al. Beneficial effects of melatonin on reperfusion injury in rat sciatic nerve. J Pineal Res. 2004;37(3):143-148.
97.
Okatani Y, Wakatsuki A, Kaneda C. Melatonin increases activities of glutathione peroxidase and superoxide dismutase in fetal rat brain. J Pineal Res. 2000;28(2):89-96.
98.
Reiter RJ, Acuna-Castroviejo D, Tan DX, Burkhardt S. Free radicalmediated molecular damage. Mechanisms for the protective actions of melatonin in the central nervous system. Ann N Y Acad Sci. 2001;939:200-215.
99.
Reiter RJ, Tan DX, Galano A. Melatonin: exceeding expectations. Physiology (Bethesda). 2014;29(5):325-333.
100.
Chang HM, Ling EA, Lue JH, Wen CY, Shieh JY. Melatonin attenuates neuronal NADPH-d/NOS expression in the hypoglossal nucleus of adult rats following peripheral nerve injury. Brain Res. 2000;873(2):243-251.
101.
Reiter R, Tang L, Garcia JJ, Munoz-Hoyos A. Pharmacological actions of melatonin in oxygen radical pathophysiology. Life Sci. 1997;60(25):2255-2271.
102.
Galindo Moreno P, Avila Ortiz G, Wang HL, Padial Molina M, Ortega Oller I, O’Valle F. The role of melatonin in periodontal and periimplant bone homeostasis and regeneration. J Oral Sci Rehabil. 2016;2(2): 8-15.
103.
Mauriz JL, Collado PS, Veneroso C, Reiter RJ, Gonzalez-Gallego J. A review of the molecular aspects of melatonin’s anti-inflammatory actions: recent insights and new perspectives. J Pineal Res. 2013;54(1):1-14.
104.
Manchester LC, Coto-Montes A, Boga JA, et al. Melatonin: an ancient molecule that makes oxygen metabolically tolerable. J Pineal Res. 2015;59(4):403-419.
105.
Reiter RJ, Mayo JC, Tan DX, Sainz RM, Alatorre-Jimenez M, Qin L. Melatonin as an antioxidant: under promises but over delivers. J Pineal Res. 2016;61(3):253-278.
106.
Bekyarova G, Tzaneva M. Melatonin ameliorates burn-induced liver injury by modulation of Nrf2 and Nf-kB signalling pathways. SOJ Immunol. 2015;3(2):1-8.
107.
Ianăş O, Olinescu R, Bădescu I. Melatonin involvement in oxidative processes. Endocrinologie. 1991;29(3-4):147-153.
108.
Reiter RJ. Interactions of the pineal hormone melatonin with oxygen-centered freeradicals: a brief review. Braz J Med Biol Res. 1993;26(11):1141-1155.
109.
Lundborg G. A 25-year perspective of peripheral nerve surgery: evolving neuroscientific concepts and clinical significance. J Hand Surg Am. 2000;25(3):391-414.
110.
Terenghi G. Peripheral nerve regeneration and neurotrophic factors. J Anat. 1999;194(pt 1):1-14.
111.
Webber CA, Christie KJ, Cheng C, et al. Schwann cells direct peripheral nerve regeneration through the Netrin-1 receptors, DCC and Unc5H2. Glia. 2011;59(10):1503-1517.
112.
Carey DJ, Bunge RP. Factors influencing the release of proteins by cultured Schwann cells. J Cell Biol. 1981;91(3 pt 1):666-672.
113.
Fansa H, Dodic T, Wolf G, Schneider W, Keilhoff G. Tissue engineering of peripheral nerves: epineurial grafts with application of cultured Schwann cells. Microsurgery. 2003;23(1):72-77.
114.
Turgut M, Oktem G, Uysal A, Yurtseven ME. Immunohistochemical profile of transforming growth factor-beta1 and basic fibroblast growth factor in sciatic nerve anastomosis following pinealectomy and exogenous melatonin administration in rats. J Clin Neurosci. 2006;13(7):753-758.
115.
Chang HM, Liu CH, Hsu WM, et al. Proliferative effects of melatonin on Schwann cells: implication for nerve regeneration following peripheral nerve injury. J Pineal Res. 2014;56(3):322-332.
116.
Ogata T, Yamamoto S, Nakamura K, Tanaka S. Signalling axis in schwann cell proliferation and differentiation. Mol Neurobiol. 2006;33(1):51-62.
117.
Noon LA, Lloyd AC. Treating leprosy: an Erb-al remedy? Trends Pharmacol Sci. 2007;28(3):103-105.
118.
Harrisingh MC, Perez-Nadales E, Parkinson DB, Malcolm DS, Mudge AW, Lloyd AC. The Ras/Raf/ERK signalling pathway drives Schwann cell dedifferentiation. EMBO J. 2004;23(15):3061-3071.
119.
Syed N, Reddy K, Yang DP, et al. Soluble neuregulin-1 has bifunctional, concentration-dependent effects on Schwann cell myelination. J Neurosci. 2010;30(17):6122-6131.
120.
Seo TB, Oh MJ, You BG, et al. ERK1/2-mediated Schwann cell proliferation in the regenerating sciatic nerve by treadmill training. J Neurotrauma. 2009;26(10):1733-1744.
121.
Corfas G, Velardez MO, Ko CP, Ratner N, Peles E. Mechanisms and roles of axon-Schwann cell interactions. J Neurosci. 2004;24(42):9250-9260.
122.
Hall ED, Braughler JM. Effects of intravenous methylprednisolone on spinal cord lipid peroxidation and (Na+ + K+)-ATPase activity. Dose-response analysis during 1st hour after contusion injury in the cat. J Neurosurg. 1982;57(2):247-253.
123.
Genovese T, Mazzon E, Muia C, Bramanti P, De Sarro A, Cuzzocrea S. Attenuation in the evolution of experimental spinal cord trauma by treatment with melatonin. J Pineal Res. 2005;38(3):198-208.
124.
Kaya Y, Sarikcioglu L, Aslan M, et al. Comparison of the beneficial effect of melatonin on recovery after cut and crush sciatic nerve injury: a combined study using functional, electrophysiological, biochemical, and electron microscopic analyses. Childs Nerv Syst. 2013;29(3):389-401.
125.
KayaY, Sarikcioglu L, Yildirim FB, Aslan M, Demir N. Does circadian rhythm disruption induced by light-at-night has beneficial effect of melatonin on sciatic nerve injury? J Chem Neuroanat. 2013;53:18-24.
126.
Iguchi H, Kato KI, Ibayashi H. Melatonin serum levels and metabolic clearance rate in patients with liver cirrhosis. J Clin Endocrinol Metab. 1982;54(5):1025-1027.
127.
Sack RL, Lewy AJ, Hughes RJ. Use of melatonin for sleep and circadian rhythm disorders. Ann Med. 1998;30(1):115-121.
128.
Rogerio F, de Souza Queiroz L, Teixeira SA, Oliveira AL, de Nucci G, Langone F. Neuroprotective action of melatonin on neonatal rat motoneurons after sciatic nerve transection. Brain Res. 2002;926(1-2):33-41.
129.
Cunnane SC, Manku MS, Horrobin DF. The pineal and regulation of fibrosis: pinealectomy as a model of primary biliary cirrhosis: roles of melatonin and prostaglandins in fibrosis and regulation of T lymphocytes. Med Hypotheses. 1979;5(4):403-414.
130.
Esposito E, Cuzzocrea S. Antiinflammatory activity of melatonin in central nervous system. Curr Neuropharmacol. 2010;8(3):228-242.
131.
Turgut M, Uyanikgil Y, Baka M, et al. Pinealectomy exaggerates and melatonin treatment suppresses neuroma formation of transected sciatic nerve in rats: gross morphological, histological and stereological analysis. J Pineal Res. 2005;38(4):284-291.
132.
Gul S, Celik SE, Kalayci M, Tasyurekli M, Cokar N, Bilge T. Dose-dependent neuroprotective effects of melatonin on experimental spinal cord injury in rats. Surg Neurol. 2005;64(4):355-361.
133.
Ulugol A, Dokmeci D, Guray G, Sapolyo N, Ozyigit F, Tamer M. Antihyperalgesic, but not antiallodynic, effect of melatonin in nerve-injured neuropathic mice: possible involvements of the L-arginine-NO pathway and opioid system. Life Sci. 2006;78(14):1592-1597.
134.
Golombek DA, Escolar E, Burin LJ, De Brito Sanchez MG, Cardinali DP. Time-dependent melatonin analgesia in mice: inhibition by opiate or benzodiazepine antagonism. Eur J Pharmacol. 1991;194(1): 25-30.
135.
Mantovani M, Pertile R, Calixto JB, Santos AR, Rodrigues AL. Melatonin exerts an antidepressant-like effect in the tail suspension test in mice: evidence for involvement of N-methyl-D-aspartate receptors and the L-arginine-nitric oxide pathway. Neurosci Lett. 2003;343(1): 1-4.
136.
Turgut M, Kaplan S, Unal BZ, et al. Stereological analysis of sciatic nerve in chickens following neonatal pinealectomy: an experimental study. J Brachial Plex Peripher Nerve Inj. 2010;5:10.
137.
Daglioglu E, Serdar Dike M, Kilinc K, et al. Neuroprotective effect of melatonin on experimental peripheral nerve injury: an electron microscopic and biochemical study. Cent Eur Neurosurg. 2009;70(3):109-114.
138.
Zencirci SG, Bilgin MD, Yaraneri H. Electrophysiological and theoretical analysis of melatonin in peripheral nerve crush injury. J Neurosci Methods. 2010;191(2):277-282.
139.
Salehi M, Naseri-Nosar M, Ebrahimi-Barough S, et al. Polyurethane/gelatin nanofibrils neural guidance conduit containing platelet-rich plasma and melatonin for transplantation of Schwann cells. Cell Mol Neurobiol. 2017:1-11.
140.
Reiter RJ, Tan DX, Osuna C, Gitto E. Actions of melatonin in the reduction of oxidative stress. J Biomed Sci. 2000;7(6):444-458.
141.
Lehman NL, Johnson LN. Toxic optic neuropathy after concomitant use of melatonin, zoloft, and a high-protein diet. J Neuroophthalmol. 1999;19(4):232-234.
142.
Piezzi RS, Cavicchia JC. Effects of cold and melatonin on the microtubules of the toad sciatic nerve. Anat Rec. 1981;200(1):115-120.
Publication history
Copyright
Rights and permissions

Publication history

Published: 26 June 2018
Issue date: December 2018

Copyright

© The author(s) 2018.

Rights and permissions

This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms. php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License (http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms (https://www.dovepress.com/terms.php).

Return