Effect of butylphthalide intervention on experimental autoimmune myositis in guinea pigs

Chen,Juan; Wang,Jingyang; Zhang,Jiyan; Pu,Chuanqiang

doi:10.3892/etm.2017.5416

Effect of butylphthalide intervention on experimental autoimmune myositis in guinea pigs

Authors:
- Juan Chen
- Jingyang Wang
- Jiyan Zhang
- Chuanqiang Pu
View Affiliations

Affiliations: Department of Neurology, Chinese PLA Medical School, Beijing 100853, P.R. China, Department of Immunology, Academy of Military Medical Sciences, Beijing 100850, P.R. China
Published online on: November 1, 2017 https://doi.org/10.3892/etm.2017.5416
Pages: 152-158
Copyright: © Chen et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Idiopathic inflammatory myopathies are a group of rare muscular diseases that are characterized by acute, subacute or chronic proximal and symmetric muscle weakness, muscle fiber necrosis and infiltration of inflammatory cells, particularly activated CD8+ cytotoxic T cells and phagocytes. 3‑n‑butylphthalide (NBP) protects mitochondria and reduces the inflammatory response in multiple disease models. In myositis, it has remained elusive whether NBP can protect muscle cells from muscle fiber injury. Experimental autoimmune myositis (EAM) was induced in a total of 40 guinea pigs by myosin immunization. After 4 weeks, low‑ or high‑dose NBP solution was intraperitoneally injected. Saline solution was used as a negative control. After 10 days, the clinical manifestations were assessed by determining rodent grasping power, histopathological changes, Ca2+‑adenosinetriphosphatase (ATPase) activity by an ATPase kit, and mRNA expression of interferon (IFN)‑γ, retinoic acid receptor‑related orphan nuclear receptor (ROR)γt and forkhead box (Fox) p3 in muscle tissue by reverse‑transcription quantitative polymerase chain reaction analysis. It was demonstrated that NBP improved the myodynamia of guinea pigs with EAM and reduced the pathological inflammatory cell infiltration in a dose‑dependent manner. NBP improved the Ca2+‑ATPase activity of the muscle mitochondrial membrane and muscle plasma membrane in animals with EAM. It also reduced the mRNA expression of IFN‑γ and RORγt, and significantly increased the mRNA expression of Foxp3 in muscle tissue. These results provided a basis for the consideration of NBP as a novel agent for the treatment of myositis and other muscular diseases associated with autoimmunity and inflammation.

View Figures

View References

1	Vincze M and Danko K: Idiopathic inflammatory myopathies. Best Pract Res Clin Rheumatol. 26:25–45. 2012. View Article : Google Scholar : PubMed/NCBI
2	Dimachkie MM and Barohn RJ: Idiopathic inflammatory myopathies. Semin Neurol. 32:227–236. 2012. View Article : Google Scholar : PubMed/NCBI
3	Cox S, Limaye V, Hill C, Blumbergs P and Roberts-Thomson P: Idiopathic inflammatory myopathies: Diagnostic criteria, classification and epidemiological features. Int J Rheum Dis. 13:117–124. 2010. View Article : Google Scholar : PubMed/NCBI
4	Szodoray P, Alex P, Knowlton N, Centola M, Dozmorov I, Csipo I, Nagy AT, Constantin T, Ponyi A, Nakken B and Danko K: Idiopathic inflammatory myopathies, signified by distinctive peripheral cytokines, chemokines and the TNF family members B-cell activating factor and a proliferation inducing ligand. Rheumatology (Oxford). 49:1867–1877. 2010. View Article : Google Scholar : PubMed/NCBI
5	Gazeley DJ and Cronin ME: Diagnosis and treatment of the idiopathic inflammatory myopathies. Ther Adv Musculoskelet Dis. 3:315–324. 2011. View Article : Google Scholar : PubMed/NCBI
6	Carstens PO and Schmidt J: Diagnosis, pathogenesis and treatment of myositis: Recent advances. Clin Exp Immunol. 175:349–358. 2014. View Article : Google Scholar : PubMed/NCBI
7	Bodoki L, Vincze M, Griger Z and Dankó K: Intravenous immunoglobulin treatment in idiopathic inflammatory myopathy. Orv Hetil. 154:723–728. 2013.(In Hungarian). View Article : Google Scholar : PubMed/NCBI
8	Mathur T, Manadan AM, Thiagarajan S, Hota B and Block JA: Corticosteroid monotherapy is usually insufficient treatment for idiopathic inflammatory myopathy. Am J Ther. 22:350–354. 2015. View Article : Google Scholar : PubMed/NCBI
9	Wilson CW III: Relative recovery and identification of carbonyl compounds from celery essential oil. J Food Sci. 35:766–768. 1970. View Article : Google Scholar
10	Zhang T, Yan W, Li Q, Fu J, Liu K, Jia W, Sun X and Liu X: 3-n-Butylphthalide (NBP) attenuated neuronal autophagy and amyloid-β expression in diabetic mice subjected to brain ischemia. Nerol Res. 33:396–404. 2011. View Article : Google Scholar
11	Feng X, Peng Y, Liu M and Cui L: DL-3-n-butylphthalide extends survival by attenuating glial activation in a mouse model of amyotrophic lateral sclerosis. Neuropharmacology. 62:1004–1010. 2012. View Article : Google Scholar : PubMed/NCBI
12	Xu HL and Feng YP: Inhibitory effects of chiral 3-n-butylphthalide on inflammation following focal ischemic brain injury in rats. Acta Pharmacol Sin. 21:433–438. 2000.PubMed/NCBI
13	Wang HM, Zhang T, Huang JK and Sun XJ: 3-N-butylphthalide (NBP) attenuates the amyloid-β-induced inflammatory responses in cultured astrocytes via the nuclear factor-κB signaling pathway. Cell Physiol Biochem. 32:235–242. 2013. View Article : Google Scholar : PubMed/NCBI
14	Allenbach Y, Solly S, Grégoire S, Dubourg O, Salomon B, Butler-Browne G, Musset L, Herson S, Klatzmann D and Benveniste O: Role of regulatory T cells in a new mouse model of experimental autoimmune myositis. Am J Pathol. 174:989–998. 2009. View Article : Google Scholar : PubMed/NCBI
15	Wang YG, Li Y, Wang CY, Ai JW, Dong XY, Huang HY, Feng ZY, Pan YM, Lin Y, Wang BX and Yao LL: L-3-n-Butylphthalide protects rats' cardiomyocytes from ischaemia/reperfusion-induced apoptosis by affecting the mitochondrial apoptosis pathway. Acta Physiol (Oxf). 210:524–533. 2014. View Article : Google Scholar : PubMed/NCBI
16	Xin DL, Harris MY, Wade CK, Amin M, Barr AE and Barbe MF: Aging enhances serum cytokine response but not task-induced grip strength declines in a rat model of work-relatedmusculoskeletal disorders. BMC Musculoskelet Disord. 12:632011. View Article : Google Scholar : PubMed/NCBI
17	Mitzelfelt JD, Dupree JP, Seo DO, Carter CS and Morgan D: Effects of chronic fentanyl administration on physical performance of aged rats. Exp Gerontol. 46:65–72. 2011. View Article : Google Scholar : PubMed/NCBI
18	Kietrys DM, Barr AE and Barbe MF: Exposure to repetitive tasks induces motor changes related to skill acquisition and inflammation in rats. J Mot Behav. 43:465–476. 2011. View Article : Google Scholar : PubMed/NCBI
19	Michael G, Kane KA and Coker SJ: Adrenaline reveals the torsadogenic effect of combined blockade of potassium channels in anaesthetized guinea pigs. Br J Pharmacol. 154:1414–1426. 2008. View Article : Google Scholar : PubMed/NCBI
20	Mengistu M, Abebe Y, Mekonnen Y and Tolessa T: In vivo and in vitro hypotensive effect of aqueous extract of Moringa stenopetala. Afr Health Sci. 12:545–551. 2012.PubMed/NCBI
21	Johnson DM, Geys R, Lissens J and Guns PJ: Drug-induced effects on cardiovascular function in pentobarbital anesthetized guinea-pigs: Invasive LVP measurements versus the QA interval. J Pharmacol Toxicological Methods. 66:152–159. 2012. View Article : Google Scholar
22	Guns PJ, Johnson DM, Weltens E and Lissens J: Negative electro-mechanical windows are required for drug-induced Torsades de Pointes in the anesthetized guinea pig. J Pharmacol Toxicol Methods. 66:125–134. 2012. View Article : Google Scholar : PubMed/NCBI
23	Mooney L, Marks L, Philp KL, Skinner M, Coker SJ and Currie S: Optimising conditions for studying the acute effects of drugs on indices of cardiac contractility and on haemodynamics in anaesthetized guinea pigs. J Pharmacol Toxicol Methods. 66:43–51. 2012. View Article : Google Scholar : PubMed/NCBI
24	Kågström J, Laumola EL, Poijes N, Johansson M and Ericson AC: Assessment of the effects of changes in body temperature on cardiac electrophysiology in anaesthetised guinea pigs. J Pharmacol Toxicol Methods. 65:1–7. 2012. View Article : Google Scholar : PubMed/NCBI
25	Michael G, Kane KA and Coker SJ: Adrenaline reveals the torsadogenic effect of combined blockade of potassium channels in anaesthetized guinea pigs. Br J Pharmacol. 154:1414–1426. 2008. View Article : Google Scholar : PubMed/NCBI
26	Lopes FDTQS, Alvarenga GS, Quiles R, Dorna MB, Vieira JE, Dolhnikoff M and Martins MA: Pulmonary responses to tracheal or esophageal acidification in guinea pigs with airway inflammation. J Appl Physiol. 93:842–847. 2002. View Article : Google Scholar : PubMed/NCBI
27	Kojima T, Tanuma N, Aikawa Y, Shin T, Sasaki A and Matsumoto Y: Myosin-induced autoimmune polymyositis in the rat. J Neurol Sci. 151:141–148. 1997. View Article : Google Scholar : PubMed/NCBI
28	Ito T, Kumamoto T, Horinouchi H, Yukishige K, Sugihara R, Fujimoto S and Tsuda T: Adhesion molecule expression in experimental myositis. Muscle Nerve. 25:409–418. 2002. View Article : Google Scholar : PubMed/NCBI
29	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-tie quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
30	Currie S: Experimental myositis: The in-vivo and in-vitro activity of lymph-node cells. J Pathol. 105:169–185. 1971. View Article : Google Scholar : PubMed/NCBI
31	Dawkins RL: Experimental myositis associated with hypersensitivity to muscle. J Pathol Bacteriol. 90:619–625. 1965. View Article : Google Scholar : PubMed/NCBI
32	Kalden JR, Williamson WG and Irvine WJ: Experimental myasthenia gravis, myositis and myocarditis in guinea-pigs immunized with subcellular fractions of calf thymus or calf skeletal muscle in Freund's complete adjuvant. Clin Exp Immunol. 13:79–88. 1973.PubMed/NCBI
33	Wen-Jing L, Chuan-Qiang P, Hong-Hua L, Xiang-Hui L and Jie-Xiao L: A new modified animal model of myosin-induced experimental autoimmune myositis enhanced by defibrase. Arch Med Sci. 11:1272–1278. 2015. View Article : Google Scholar : PubMed/NCBI
34	Nemoto H, Bhopale MK, Constantinescu CS, Schotland D and Rostami A: Skeletal muscle myosin is the autoantigen for experimental autoimmune myositis. Exp Mol Pathol. 74:238–243. 2003. View Article : Google Scholar : PubMed/NCBI
35	Nakano J, Yoshimura T, Okita M, Motomura M, Kamei S, Matsuo H and Eguchi K: Laminin-induced autoimmune myositis in rats. J Neuropathol Exp Neurol. 64:790–796. 2005. View Article : Google Scholar : PubMed/NCBI
36	Matsubara S and Takamori M: Experimental allergic myositis: Strain 13 guinea pig immunised with rabbit myosin B fraction. Acta Neuropathol. 74:158–162. 1987. View Article : Google Scholar : PubMed/NCBI
37	Zhao Q, Zhang C, Wang X, Chen L, Ji H and Zhang Y: (S)-ZJM-289, a nitric oxide-releasing derivative of 3-n-butylphthalide, protects against ischemic neuronal injury by attenuating mitochondrial dysfunction and associated cell death. Neurochem Int. 60:134–144. 2012. View Article : Google Scholar : PubMed/NCBI
38	Xu J, Wang Y, Li N, Xu L, Yang H and Yang Z: L-3-n-butylphthalide improves cognitive deficits in rats with chronic cerebral ischemia. Neuropharmacology. 62:2424–2429. 2012. View Article : Google Scholar : PubMed/NCBI
39	Ma S, Xu S, Liu B, Li J, Feng N, Wang L and Wang X: Long-term treatment of l-3-n-butylphthalide attenuated neurodegenerative changes in aged rats. Naunyn Schmiedebergs Arch Pharmacol. 379:565–574. 2009. View Article : Google Scholar : PubMed/NCBI
40	Cartwright EJ, Oceandy D, Austin C and Neyses L: Ca2⁺ signalling in cardiovascular disease: The role of the plasma membrane calcium pumps. Sci China Life Sci. 54:691–698. 2011. View Article : Google Scholar : PubMed/NCBI
41	Despa S and Bers DM: Na+ transport in the normal and failing heart-remember the balance. J Mol Cell Cardiol. 61:2–10. 2013. View Article : Google Scholar : PubMed/NCBI
42	Tajiri K, Shimojo N, Sakai S, Machino-Ohtsuka T, Imanaka-Yoshida K, Hiroe M, Tsujimura Y, Kimura T, Sato A, Yasutomi Y and Aonuma K: Pitavastatin regulates helper T-cell differentiation and ameliorates autoimmune myocarditis in mice. Cardiovasc Drugs Ther. 27:413–424. 2013. View Article : Google Scholar : PubMed/NCBI
43	Pot C, Apetoh L and Kuchroo VK: Type 1 regulatory T cells (Tr1) in autoimmunity. Semin Immunol. 23:202–208. 2011. View Article : Google Scholar : PubMed/NCBI
44	Carvalho MI, Pires I, Prada J, Gregório H, Lobo L and Queiroga FL: Intratumoral FoxP3 expression is associated with angiogenesis and prognosis in malignant canine mammary tumors. Vet Immunol Immunopathol. 178:1–9. 2016. View Article : Google Scholar : PubMed/NCBI
45	Pasztoi M, Bonifacius A, Pezoldt J, Kulkarni D, Niemz J, Yang J, Teich R, Hajek J, Pisano F, Rohde M, et al: Yersinia pseudo-tuberculosis supports Th17 differentiation and limits de novo regulatory T cell induction by directly interfering with T cell receptor signaling. Cell Mol Life Sci. 74:2839–2850. 2017. View Article : Google Scholar : PubMed/NCBI
46	Du R, Zhao H, Yan F and Li H: IL-17+Foxp3+ T cells: An intermediate differentiation stage between Th17 cells and regulatory T cells. J Leukoc Biol. 96:39–48. 2014. View Article : Google Scholar : PubMed/NCBI