Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2016

Open Access 01-12-2016 | Research article

Bogijetong decoction and its active herbal components protect the peripheral nerve from damage caused by taxol or nerve crush

Authors: So Hyun Ahn, In Ae Chang, Ki-Joong Kim, Chul-Jung Kim, Uk Namgung, Chung-Sik Cho

Published in: BMC Complementary Medicine and Therapies | Issue 1/2016

Login to get access

Abstract

Background

Bogijetong decoction (BGJTD) is a herbal drug formulation used in the traditional Asian medicine to treat neuropathic insults associated with diabetes and anticancer therapy. To understand the biological basis of BGJTD on protective effects against neuropathy, we investigated physiological and biochemical responses of the sciatic nerves deranged by taxol injection or crush injury in the rats.

Methods

Dissociated Schwann cells and neurons were prepared from the sciatic nerve and dorsal root ganglia (DRG) respectively and were treated with taxol and BGJTD. The sciatic nerve in the rat was injected with taxol or given crush injury. Animals were then administered orally with BGJTD. Effects of BGJTD treatment on cultured cells and in vivo sciatic nerves and DRG tissues were examined by immunofluorescence staining and western blot analysis. Sciatic nerve regeneration was assessed by histological observation using retrograde tracing technique and by behavioral hot plate test. Eighteen different herbal components of BGJTD were divided into 4 subgroups and were used to select herbal drugs that enhanced neurite outgrowth in cultured neurons.

Results

Morphological abnormalities in the sciatic nerve axons and DRG tissue caused by taxol injection were largely improved by BGJTD treatment. BGJTD treatment enhanced neurite outgrowth in cultured DRG neurons and improved Schwann cell survival. Phospho-Erk1/2 levels were elevated by BGJTD administration in the injured- or taxol-injected sciatic nerves. Vimentin phosphorylation catalyzed by cell division cycle 2 (Cdc2) kinase was induced from Schwann cells in the sciatic nerves after taxol injection and crush injury, and phospho-vimentin levels were further upregulated by BGJTD treatment. Retrograde tracing of DiI-labeled DRG sensory neurons revealed growth-promoting activity of BGJTD on axonal regeneration. A drug group (Be) composed of 4 active herbal components which were selected by neurite growth-enhancing activity was as effective as BGJDT for the recovery of thermal sensitivity of the hind paws which had been suppressed by taxol administration.

Conclusions

These data suggest that BGJTD and its active herbal components may protects the peripheral nerve from damage caused by taxol injection and nerve crush.
Literature
2.
go back to reference Scholz J, Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci. 2007;10:1361–8.CrossRefPubMed Scholz J, Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci. 2007;10:1361–8.CrossRefPubMed
4.
go back to reference Rowinsky EK, Donehower RC. The clinical pharmacology of paclitaxel (Taxol). Semin Oncol. 1993;20(4 Suppl 3):16–25.PubMed Rowinsky EK, Donehower RC. The clinical pharmacology of paclitaxel (Taxol). Semin Oncol. 1993;20(4 Suppl 3):16–25.PubMed
5.
go back to reference Chaudhry V, Rowinsky EK, Sartorius SE, Donehower RC, Cornblath DR. Peripheral neuropathy from taxol and cisplatin combination chemotherapy: clinical and electrophysiological studies. Ann Neurol. 1994;35:304–11.CrossRefPubMed Chaudhry V, Rowinsky EK, Sartorius SE, Donehower RC, Cornblath DR. Peripheral neuropathy from taxol and cisplatin combination chemotherapy: clinical and electrophysiological studies. Ann Neurol. 1994;35:304–11.CrossRefPubMed
6.
go back to reference Cavaletti G, Bogliun G, Crespi V, Marzorati L, Zincone A, Marzola M, et al. Neurotoxicity and ototoxicity of cisplatin plus paclitaxel in comparison to cisplatin plus cyclophosphamide in patients with epithelial ovarian cancer. J Clin Oncol. 1997;15:199–206.PubMed Cavaletti G, Bogliun G, Crespi V, Marzorati L, Zincone A, Marzola M, et al. Neurotoxicity and ototoxicity of cisplatin plus paclitaxel in comparison to cisplatin plus cyclophosphamide in patients with epithelial ovarian cancer. J Clin Oncol. 1997;15:199–206.PubMed
7.
go back to reference Peters CM, Jimenez-Andrade JM, Kuskowski MA, Ghilardi JR, Mantyh PW. An evolving cellular pathology occurs in dorsal root ganglia, peripheral nerve and spinal cord following intravenous administration of paclitaxel in the rat. Brain Res. 2007;1168:46–59.CrossRefPubMedPubMedCentral Peters CM, Jimenez-Andrade JM, Kuskowski MA, Ghilardi JR, Mantyh PW. An evolving cellular pathology occurs in dorsal root ganglia, peripheral nerve and spinal cord following intravenous administration of paclitaxel in the rat. Brain Res. 2007;1168:46–59.CrossRefPubMedPubMedCentral
8.
go back to reference Cavaletti G, Tredici G, Braga M, Tazzari S. Experimental peripheral neuropathy induced in adult rats by repeated intraperitoneal administration of taxol. Exp Neurol. 1995;133:64–72.CrossRefPubMed Cavaletti G, Tredici G, Braga M, Tazzari S. Experimental peripheral neuropathy induced in adult rats by repeated intraperitoneal administration of taxol. Exp Neurol. 1995;133:64–72.CrossRefPubMed
9.
go back to reference Carozzi VA, Canta A, Oggioni N, Sala B, Chiorazzi A, Meregalli C, et al. Neurophysiological and neuropathological characterization of new murine models of chemotherapy-induced chronic peripheral neuropathies. Exp Neurol. 2010;226:301–9.CrossRefPubMed Carozzi VA, Canta A, Oggioni N, Sala B, Chiorazzi A, Meregalli C, et al. Neurophysiological and neuropathological characterization of new murine models of chemotherapy-induced chronic peripheral neuropathies. Exp Neurol. 2010;226:301–9.CrossRefPubMed
10.
go back to reference Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ, Umlauf M, et al. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science. 2011;331:928–31.CrossRefPubMedPubMedCentral Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ, Umlauf M, et al. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science. 2011;331:928–31.CrossRefPubMedPubMedCentral
11.
go back to reference Cho JH, Kim JM, Kim JH, Oh YS, Kim CJ. A case report of chemotherapy-induced neuropathic pain treated with oriental medicine. J Korean Orient Med. 2010;31:58–63. Cho JH, Kim JM, Kim JH, Oh YS, Kim CJ. A case report of chemotherapy-induced neuropathic pain treated with oriental medicine. J Korean Orient Med. 2010;31:58–63.
12.
go back to reference Kim JM, Cho CS, Kim CJ. Clinical study of 8 diabetic patients with paresthesia. Kor J Ori Internal Med. 2010;31:184–91. Kim JM, Cho CS, Kim CJ. Clinical study of 8 diabetic patients with paresthesia. Kor J Ori Internal Med. 2010;31:184–91.
13.
go back to reference Lee JB, Kim CJ, Cho CS. Effects of Bogijetong-tang on diabetic-peripheral neuropathy induced by streptozotocin in the mouse. J Korean Med. 2013;34:126–42.CrossRef Lee JB, Kim CJ, Cho CS. Effects of Bogijetong-tang on diabetic-peripheral neuropathy induced by streptozotocin in the mouse. J Korean Med. 2013;34:126–42.CrossRef
14.
go back to reference Park SW, Kim CJ, Cho CS. Effects of nerve regeneration by Bogijetong-tang on peripheral nerves damaged by taxol and crush injury. Kor J Orient Int Med. 2013;34:384–404. Park SW, Kim CJ, Cho CS. Effects of nerve regeneration by Bogijetong-tang on peripheral nerves damaged by taxol and crush injury. Kor J Orient Int Med. 2013;34:384–404.
15.
go back to reference Röyttä M, Horwitz SB, Raine CS. Taxol-induced neuropathy: short-term effects of local injection. J Neurocytol. 1984;13:685–701.CrossRefPubMed Röyttä M, Horwitz SB, Raine CS. Taxol-induced neuropathy: short-term effects of local injection. J Neurocytol. 1984;13:685–701.CrossRefPubMed
16.
go back to reference Ertürk A, Hellal F, Enes J, Bradke F. Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J Neurosci. 2007;27:9169–80.CrossRefPubMed Ertürk A, Hellal F, Enes J, Bradke F. Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J Neurosci. 2007;27:9169–80.CrossRefPubMed
17.
go back to reference Seo TB, Han IS, Yoon JH, Hong KE, Yoon SJ, Namgung U, et al. Involvement of Cdc2 in axonal regeneration enhanced by exercise training in rats. Med Sci Sports Exerc. 2006;38:1267–76.CrossRefPubMed Seo TB, Han IS, Yoon JH, Hong KE, Yoon SJ, Namgung U, et al. Involvement of Cdc2 in axonal regeneration enhanced by exercise training in rats. Med Sci Sports Exerc. 2006;38:1267–76.CrossRefPubMed
18.
go back to reference Tsujimura K, Ogawara M, Takeuchi Y, Imajoh-Ohmi S, Ha MH, Inagaki M. Visualization and function of vimentin phosphorylation by cdc2 kinase during mitosis. J Biol Chem. 1994;269:31097–106.PubMed Tsujimura K, Ogawara M, Takeuchi Y, Imajoh-Ohmi S, Ha MH, Inagaki M. Visualization and function of vimentin phosphorylation by cdc2 kinase during mitosis. J Biol Chem. 1994;269:31097–106.PubMed
19.
go back to reference Han IS, Seo TB, Kim KH, Yoon JH, Yoon SJ, Namgung U. Cdc2-mediated Schwann cell migration during peripheral nerve regeneration. J Cell Sci. 2007;120:246–55.CrossRefPubMed Han IS, Seo TB, Kim KH, Yoon JH, Yoon SJ, Namgung U. Cdc2-mediated Schwann cell migration during peripheral nerve regeneration. J Cell Sci. 2007;120:246–55.CrossRefPubMed
20.
go back to reference Chang IA, Oh MJ, Kim MH, Park SK, Kim BG, Namgung U. Vimentin phosphorylation by Cdc2 in Schwann cell controls axon growth via β1-integrin activation. FASEB J. 2012;26:2401–13.CrossRefPubMed Chang IA, Oh MJ, Kim MH, Park SK, Kim BG, Namgung U. Vimentin phosphorylation by Cdc2 in Schwann cell controls axon growth via β1-integrin activation. FASEB J. 2012;26:2401–13.CrossRefPubMed
21.
go back to reference Loprinzi CL, Reeves BN, Dakhil SR, Sloan JA, Wolf SL, Burger KN, et al. Natural history of paclitaxel-associated acute pain syndrome: prospective cohort study NCCTG N08C1. J Clin Oncol. 2011;29:1472–8.CrossRefPubMedPubMedCentral Loprinzi CL, Reeves BN, Dakhil SR, Sloan JA, Wolf SL, Burger KN, et al. Natural history of paclitaxel-associated acute pain syndrome: prospective cohort study NCCTG N08C1. J Clin Oncol. 2011;29:1472–8.CrossRefPubMedPubMedCentral
22.
24.
go back to reference Namgung U. The role of Schwann cell-axon interaction n peripheral nerve regeneration. Cells Tissues Organs. 2014;200:6–12.CrossRefPubMed Namgung U. The role of Schwann cell-axon interaction n peripheral nerve regeneration. Cells Tissues Organs. 2014;200:6–12.CrossRefPubMed
25.
go back to reference Weiss MD, Luciano CA, Quarles RH. Nerve conduction abnormalities in aging mice deficient for myelin-associated glycoprotein. Muscle Nerve. 2001;24:1380–7.CrossRefPubMed Weiss MD, Luciano CA, Quarles RH. Nerve conduction abnormalities in aging mice deficient for myelin-associated glycoprotein. Muscle Nerve. 2001;24:1380–7.CrossRefPubMed
26.
27.
go back to reference Tsuda Y, Kanje M, Dahlin LB. Axonal outgrowth is associated with increased ERK 1/2 activation but decreased caspase 3 linked cell death in Schwann cells after immediate nerve repair in rats. BMC Neurosci. 2011;12:12.CrossRefPubMedPubMedCentral Tsuda Y, Kanje M, Dahlin LB. Axonal outgrowth is associated with increased ERK 1/2 activation but decreased caspase 3 linked cell death in Schwann cells after immediate nerve repair in rats. BMC Neurosci. 2011;12:12.CrossRefPubMedPubMedCentral
28.
go back to reference Reynolds AJ, Hendry IA, Bartlett SE. Anterograde and retrograde transport of active extracellular signal-related kinase 1 (ERK1) in the ligated rat sciatic nerve. Neuroscience. 2001;105:761–71.CrossRefPubMed Reynolds AJ, Hendry IA, Bartlett SE. Anterograde and retrograde transport of active extracellular signal-related kinase 1 (ERK1) in the ligated rat sciatic nerve. Neuroscience. 2001;105:761–71.CrossRefPubMed
29.
go back to reference Segal RA, Greenberg ME. Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci. 1996;19:463–89.CrossRefPubMed Segal RA, Greenberg ME. Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci. 1996;19:463–89.CrossRefPubMed
30.
go back to reference Alessandri-Haber N, Dina OA, Joseph EK, Reichling DB, Levine JD. Interaction of transient receptor potential vanilloid 4, integrin, and SRC tyrosine kinase in mechanical hyperalgesia. J Neurosci. 2008;28:1046–57.CrossRefPubMed Alessandri-Haber N, Dina OA, Joseph EK, Reichling DB, Levine JD. Interaction of transient receptor potential vanilloid 4, integrin, and SRC tyrosine kinase in mechanical hyperalgesia. J Neurosci. 2008;28:1046–57.CrossRefPubMed
31.
33.
34.
go back to reference Seo TB, Baek K, Kwon KB, Lee SI, Lim JS, Seol IC, et al. Shengmai-san-mediated enhancement of regenerative responses of spinal cord axons after injury in rats. J Pharmacol Sci. 2009;110:483–92.CrossRefPubMed Seo TB, Baek K, Kwon KB, Lee SI, Lim JS, Seol IC, et al. Shengmai-san-mediated enhancement of regenerative responses of spinal cord axons after injury in rats. J Pharmacol Sci. 2009;110:483–92.CrossRefPubMed
35.
go back to reference Ma J, Li W, Tian R, Lei W. Ginsenoside Rg1 promotes peripheral nerve regeneration in rat model of nerve crush injury. Neurosci Lett. 2010;478:66–71.CrossRefPubMed Ma J, Li W, Tian R, Lei W. Ginsenoside Rg1 promotes peripheral nerve regeneration in rat model of nerve crush injury. Neurosci Lett. 2010;478:66–71.CrossRefPubMed
36.
go back to reference Cheung ZH, So KF, Lu Q, Yip HK, Wu W, Shan JJ, Pang PK, Chen CF. Enhanced survival and regeneration of axotomized retinal ganglion cells by a mixture of herbal extracts. J Neurotrauma. 2002;19:369–78.CrossRefPubMed Cheung ZH, So KF, Lu Q, Yip HK, Wu W, Shan JJ, Pang PK, Chen CF. Enhanced survival and regeneration of axotomized retinal ganglion cells by a mixture of herbal extracts. J Neurotrauma. 2002;19:369–78.CrossRefPubMed
37.
go back to reference Wang L, Yuan D, Zhang D, Zhang W, Liu C, Cheng H, et al. Ginsenoside Re promotes nerve regeneration by facilitating the proliferation, differentiation and migration of Schwann cells via the ERK- and JNK-dependent pathway in rat model of sciatic nerve crush injury. Cell Mol Neurobiol. 2015;35:827–40.CrossRefPubMed Wang L, Yuan D, Zhang D, Zhang W, Liu C, Cheng H, et al. Ginsenoside Re promotes nerve regeneration by facilitating the proliferation, differentiation and migration of Schwann cells via the ERK- and JNK-dependent pathway in rat model of sciatic nerve crush injury. Cell Mol Neurobiol. 2015;35:827–40.CrossRefPubMed
38.
go back to reference Tohda C, Kuboyama T, Komatsu K. Search for natural products related to regeneration of the neuronal network. Neurosignals. 2005;14:34–45.CrossRefPubMed Tohda C, Kuboyama T, Komatsu K. Search for natural products related to regeneration of the neuronal network. Neurosignals. 2005;14:34–45.CrossRefPubMed
Metadata
Title
Bogijetong decoction and its active herbal components protect the peripheral nerve from damage caused by taxol or nerve crush
Authors
So Hyun Ahn
In Ae Chang
Ki-Joong Kim
Chul-Jung Kim
Uk Namgung
Chung-Sik Cho
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2016
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-016-1391-7

Other articles of this Issue 1/2016

BMC Complementary Medicine and Therapies 1/2016 Go to the issue