Inhibitory effect of Zanthoxylum bungeanum seed oil on ovalbumin‑induced lung inflammation in a murine model of asthma

Wang,Jun‑Qin; Li,Xiao‑Wei; Liu,Mingyi; Wang,Sheng‑Chun; Cao,Zeng‑Fa

doi:10.3892/mmr.2016.5050

Inhibitory effect of Zanthoxylum bungeanum seed oil on ovalbumin‑induced lung inflammation in a murine model of asthma

Authors:
- Jun‑Qin Wang
- Xiao‑Wei Li
- Mingyi Liu
- Sheng‑Chun Wang
- Zeng‑Fa Cao
View Affiliations

Affiliations: Department of Pharmacy, Xijing Hospital, The Fourth Military Medical University, Xi'an, Shaanxi 710032, P.R. China, Xin Run Pharmaceutical Limited Company, Xi'an, Shaanxi 710075, P.R. China
Published online on: March 28, 2016 https://doi.org/10.3892/mmr.2016.5050
Pages: 4289-4302

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

The present study aimed to investigate the therapeutic efficacy of Zanthoxylum bungeanum seed oil (Z. seed oil) to alleviate airway inflammation in asthmatic mice. The asthmatic mice were treated with vehicle, ovalbumin (OVA), or OVA + Z. seed oil (2 g/kg) for between 24 h and 14 days. Following treatment, inflammatory cell infiltration and pulmonary tissue damage were assessed by hematoxylin and eosin staining, and immunohistochemistry. The expression levels of pro‑inflammatory cytokines, chemokines, adhesion molecules and mitogen activated protein kinase signaling proteins were measured by enzyme‑linked immunosorbent assays, reverse transcription quantitative‑polymerase chain reaction and western blot analysis. In asthmatic mice, administration of Z. seed oil attenuated lung tissue injury and airway remodeling, and inhibited the infiltration of leukocytes and eosinophils into the airway by reducing the expression levels of inflammatory cytokines and chemokines compared with OVA‑treated mice (P<0.05). Z. seed oil also reduced the levels of inflammatory chemokine and adhesion molecules via downregulation of extracellular signal‑regulated kinase and activation of c‑JUN N‑terminal kinase in the Z. seed‑treated mice compared with OVA‑treated mice (P<0.05). Thus, data from the present study indicates that Z. seed oil can suppress pulmonary inflammation and tissue injury during asthma, and suggests that it may be used to effectively treat allergen‑induced asthma.

View Figures

View References

1	Takeda M, Ito W, Tanabe M, Ueki S, Kato H, Kihara J, Tanigai T, Chiba T, Yamaguchi K, Kayaba H, et al: Allergic airway hyper-responsiveness, inflammation, and remodeling do not develop in phosphoinositide 3-kinase γ-deficient mice. J Allergy Clin Immunol. 123:805–812. 2009. View Article : Google Scholar : PubMed/NCBI
2	Akbari O, Faul JL, Hoyte EG, Berry GJ, Wahlström J, Kronenberg M, DeKruyff RH and Umetsu DT: CD4⁺ invariant T-cell-receptor⁺ natural killer T cells in bronchial asthma. N Engl J Med. 354:1117–1129. 2006. View Article : Google Scholar : PubMed/NCBI
3	Elias JA, Lee CG, Zheng T, Ma B, Homer RJ and Zhu Z: New insights into the pathogenesis of asthma. J Clin Invest. 111:291–297. 2003. View Article : Google Scholar : PubMed/NCBI
4	Expert Panel Report 3 (EPR-3): Guidelines for the diagnosis and management of asthma-summary report 2007. J Allergy Clin Immunol. 120:S94–S138. 2007. View Article : Google Scholar
5	Torén K and Hermansson BA: Incidence rate of adult-onset asthma in relation to age, sex, atopy and smoking: A Swedish population-based study of 15813 adults. Int J Tuberc Lung Dis. 3:192–197. 1999.PubMed/NCBI
6	de Marco R, Locatelli F, Cazzoletti F, Bugianio M, Carosso A and Marinoni A: Incidence of asthma and mortality in a cohort of young adults: A 7-year prospective study. Respir Res. 6:952005. View Article : Google Scholar : PubMed/NCBI
7	Karjalainen A, Kurppa K, Martikainen R, Klaukka T and Karjalainen J: Work is related to a substantial portion of adult-onset asthma incidence in the Finnish population. Am J Respir Crit Care Med. 164:565–568. 2001. View Article : Google Scholar : PubMed/NCBI
8	National Heart Blood and Lung Institute: Guidelines for the diagnosis and management of asthma. National Institutes of Health; Bethesda, USA: 2002
9	Duan W, Chan JH, Wong CH, Leung BP and Wong WS: Anti-inflammatory effects of mitogen-activated protein kinase kinase inhibitor U0126 in an asthma mouse model. J Immunol. 172:7053–7059. 2004. View Article : Google Scholar : PubMed/NCBI
10	Pelaia G, Cuda G, Vatrella A, Gallelli L, Caraglia M, Marra M, Abbruzzese A, Caputi M, Maselli R, Costanzo FS, et al: Mitogen-activated protein kinases and asthma. J Cell Physiol. 202:642–653. 2005. View Article : Google Scholar
11	Kumar A, Lnu S, Malya R, Barron D, Moore J, Corry DB and Boriek AM: Mechanical stretch activates nuclear factor-kappaB, activator protein-1, and mitogen-activated protein kinases in lung parenchyma: Implications in asthma. FASEB J. 17:1800–1811. 2003. View Article : Google Scholar : PubMed/NCBI
12	Dong C, Davis RJ and Flavell RA: MAP kinases in the immune response. Annu Rev Immunol. 20:55–72. 2002. View Article : Google Scholar : PubMed/NCBI
13	Atherton HC, Jones G and Danahay H: IL-13-induced changes in the goblet cell density of human bronchial epithelial cell cultures: MAP kinase and phosphatidylinositol 3-kinase regulation. Am J Physiol Lung Cell Mol Physiol. 285:L730–L739. 2003. View Article : Google Scholar : PubMed/NCBI
14	Yamashita M, Kimura M, Kubo M, Shimizu C, Tada T, Perlmutter RM and Nakayama T: T cell antigen receptor-mediated activation of the Ras/mitogen-activated protein kinase pathway controls interleukin 4 receptor function and type-2 helper T cell differentiation. Proc Natl Acad Sci USA. 96:1024–1029. 1999. View Article : Google Scholar : PubMed/NCBI
15	Rahman MT and Alimuzzaman M: Antinociceptive and antidiarrhoeal activity of Zanthoxylum rhetsa. Fitoterapia. 73:340–342. 2002. View Article : Google Scholar : PubMed/NCBI
16	Chang CT, Doong SL, Tsai IL and Chen IS: Coumarins and anti-HBV constituents from Zanthoxylum schionifolium. Phytochemistry. 45:1419–1422. 1997. View Article : Google Scholar
17	Bracke ME, Depypere HT, Boterberg T, Van Marck VL, Veenekens KM, Vanleuchene E, Nuytinck M, Serreyn R and Mareel MM: Influence of tangeretin on tamoxifen's therapeutic benefit in mammary cancer. J Nat Cancer Inst. 91:354–359. 1999. View Article : Google Scholar : PubMed/NCBI
18	Tanaka S, Sato T, Akimoto N, Yano M and Ito A: Prevention of UVB-induced photoinflammation and photoaging by a polymethoxy flavonoid, nobiletin, in human keratinocytes in vivo and in vitro. Biochem Pharmacol. 68:433–439. 2004. View Article : Google Scholar : PubMed/NCBI
19	Tan GT, Pezzuto JM, Kinghorn AD and Hughes SH: Evaluation of natural products as inhibitors of human immunodeficiency virus type 1 (HIV-1) reverse transcriptase. J Nat Prod. 54:143–154. 1991. View Article : Google Scholar : PubMed/NCBI
20	Xia L, You J, Li G, Sun Z and Suo Y: Compositional and antioxidant activity analysis of Zanthoxylum bungeanum seed oil obtained by supercritical CO2 fluid extraction. J Am Oil Chem Soc. 88:23–32. 2011. View Article : Google Scholar
21	Myou S, Leff AR, Myo S, et al: Blockade of inflammation and airway hyperresponsiveness in immune-sensitized mice by dominant-negative phosphoinositide 3-kinase-TAT. J Exp Med 17. 198(10): 1573–82. 2003. View Article : Google Scholar
22	Livak KJ and Schmittgen TD: Analysis of the relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar
23	Murphy PM: Chemokine receptors: Structure, function and role in microbial pathogenesis. Cytokine Growth Factor Rev. 7:47–64. 1996. View Article : Google Scholar : PubMed/NCBI
24	Foessmann UUM, Loetscher P, Dahinden CA, Langen H, Thelen M and Baggiolini M: Eotaxin-2s like eotaxin on human eosinophil and receptor. J Exp Med. 183:2349–2354. 1997.
25	Alam R, York J, Boyars M, Stafford S, Grant JA, Lee J, Forsythe P, Sim T and Ida N: Increased MCP-1, RANTES, and MIP-1alpha in bronchoalveolar lavage fluid of allergic asthmatic patients. Am J Respir Crit Care Med. 153:13981404. View Article : Google Scholar
26	Parent C and Eichacker PQ: Neutrophil and endothelial cell interactions in sepsis. The role of adhesion molecules. Infect Dis Clin North Am. 13:427–447. 1999. View Article : Google Scholar : PubMed/NCBI
27	Shanley TP, Warner RL and Ward PA: The role of cytokines and adhesion molecules in the development of inflammatory injury. Mol Med Today. 1:40–45. 1995. View Article : Google Scholar : PubMed/NCBI
28	Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC and Calderwood SK: HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med. 6:435–442. 2000. View Article : Google Scholar : PubMed/NCBI
29	Duan W and Wong WS: Targeting mitogen-activated protein kinases for asthma. Curr Drug Targets. 7:691–698. 2006. View Article : Google Scholar : PubMed/NCBI
30	Talati M, Meyrick B, Peebles RS Jr, Davies SS, Dworski R, Mernaugh R, Mitchell D, Boothby M, Roberts LJ II and Sheller JR: Oxidant stress modulates murine allergic airway responses. Free Radic Biol Med. 40:1210–1219. 2006. View Article : Google Scholar : PubMed/NCBI
31	Cohn L, Elias JA and Chupp GL: Asthma: Mechanisms of disease persistence and progression. Annu Rev Immunol. 22:789–815. 2004. View Article : Google Scholar : PubMed/NCBI
32	Cameron EJ, McSharry C, Chaudhuri R, Farrow S and Thomson NC: Long-term macrolide treatment of chronic inflammatory airway diseases: Risks, benefits and future developments. Clin Exp Allergy. 42:1302–1312. 2012. View Article : Google Scholar : PubMed/NCBI
33	Zhang Y, Lamm WJ, Albert RK, Chi EY, Henderson WR Jr and Lewis DB: Influence of the route of allergen administration and genetic background on the murine allergic pulmonary response. Am J Respir Crit Care Med. 155:661–669. 1997. View Article : Google Scholar : PubMed/NCBI
34	Wills-Karp M: Interleukin-13 in asthma pathogenesis. Immunol Rev. 202:175–190. 2004. View Article : Google Scholar : PubMed/NCBI
35	Cho JY, Miller M, Baek KJ, Han JW, Nayar J, Lee SY, McElwain K, McElwain S, Friedman S and Broide DH: Inhibition of airway remodeling in IL-5-deficient mice. J Clin Invest. 113:551–560. 2004. View Article : Google Scholar : PubMed/NCBI
36	Huber AR, Kunkel SL, Todd RF III and Weiss SJ: Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science. 254:99–102. 1991. View Article : Google Scholar : PubMed/NCBI
37	Jatakanon A, Uasuf C, Maziak W, Lim S, Chung KF and Barnes PJ: Neutrophilic inflammation in severe persistent asthma. Am J Respir Crit Care Med. 160:1532–1539. 1999. View Article : Google Scholar : PubMed/NCBI
38	Lukacs NW, Miller AL and Hogaboam CM: Chemokine receptors in asthma: Searching for the correct immune targets. J Immunol. 171:11–15. 2003. View Article : Google Scholar : PubMed/NCBI
39	ten Hove W, Houben LA, Raaijmakers JAM, Bracke M and Koenderman L: Differential regulation of TNF and GM-CSF induced activation of P38 MAPK in neutrophils and eosinophils. Molecular Immunology. 44:2492–2496. 2007. View Article : Google Scholar
40	Fujiwara N and Kobayashi K: Macrophages in inflammation. Curr Drug Targets Inflamm Allergy. 4:281–286. 2005. View Article : Google Scholar : PubMed/NCBI
41	Lee T and Sousa A: Immunoinflammatory role of the airway epithelial cell in asthma. Eur Respir Rev. 4:368–370. 1994.
42	Kampen GT, Stafford S, Adachi T, Jinquan T, Quan S, Grant JA, Skov PS, Poulsen LK and Alam R: Eotaxin induces degranulation and chemotaxis of eosinophils through the activation of ERK2 and p38 mitogen-activated protein kinases. Blood. 95:1911–1917. 2000.PubMed/NCBI
43	Carl VS, Brown-Steinke K, Nicklin MJH and Smith MFS Jr: Toll-like receptor 2 and 4 (TLR2 and TLR4) agonists differentially regulate secretory interleukin-1 receptor antagonist gene expression in macrophages. J Biol Chem. 277:17448–17456. 2002. View Article : Google Scholar : PubMed/NCBI
44	Moon EY, Kang JS, Han SH, Yang KH, Pyo S, Lee MY, Lee HK and Yu DY: Differential role of peroxiredoxin II (PrxII) on the expression of toll-like receptor 4 (TLR4) and B-cell activating factor (BAFF) in ovalbumin (OVA)-induced mouse asthma. Int Immunopharmacol. 8:935–944. 2008. View Article : Google Scholar : PubMed/NCBI
45	Arbabi S and Maier RV: Mitogen-activated protein kinases. Crit Care Med. 30(Suppl): S74–S79. 2002. View Article : Google Scholar : PubMed/NCBI