Essential oil from Korean Chamaecyparis obtusa leaf ameliorates respiratory activity in Sprague‑Dawley rats and exhibits protection from NF-κB-induced inflammation in WI38 fibroblast cells

Raha,Suchismita; Kim,Seong   Min; Lee,Ho   Jeong; Lee,Sang   Joon; Heo,Jeong   Doo; Venkatarame Gowda Saralamma,Venu; Ha,Sang  Eun; Kim,Eun   Hee; Mun,Sung   Phil; Kim,Gon   Sup

doi:10.3892/ijmm.2018.3966

Essential oil from Korean Chamaecyparis obtusa leaf ameliorates respiratory activity in Sprague‑Dawley rats and exhibits protection from NF-κB-induced inflammation in WI38 fibroblast cells

Authors:
- Suchismita Raha
- Seong Min Kim
- Ho Jeong Lee
- Sang Joon Lee
- Jeong Doo Heo
- Venu Venkatarame Gowda Saralamma
- Sang Eun Ha
- Eun Hee Kim
- Sung Phil Mun
- Gon Sup Kim
View Affiliations

Affiliations: Research Institute of Life Science, College of Veterinary Medicine, Gyeongsang National University, Jinju, Gyeongsang 52828, Republic of Korea, Gyeongnam Department of Environment Toxicology and Chemistry, Toxicology Screening Research Center, Korea Institute of Toxicology, Jinju, Gyeongsang 52828, Republic of Korea, Department of Nursing Science, International University of Korea, Jinju, Gyeongsang 52833, Republic of Korea, Department of Wood Science and Technology, Chonbuk National University, Jeonju, Jeollabuk 54896, Republic of Korea
Published online on: October 31, 2018 https://doi.org/10.3892/ijmm.2018.3966
Pages: 393-403
Copyright: © Raha 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

To date, Korean hinoki cypress (Chamaecyparis obtusa), has been widely used for household and commercial purposes. Although the medicinal efficacy of hinoki cypress essential oil has been observed, that of the essential oil‑derived terpenes, which exhibit a mechanism that acts against lung inflammation, remains to be fully elucidated. The present study investigated the anti‑inflammatory effect of hinoki cypress leaf extracted essential oil on lipopolysaccharide (LPS)‑stimulated WI38 fibroblast cells by inhibiting the nuclear factor κ‑light‑chain‑enhancer of activated B cells (NF‑κB) pathway, which exhibited lung tissue protection through the olfactory administration of essential oil in Sprague‑Dawley rats. GC/MS analysis derived 24 terpenes from the essential oil. The morphological observations revealed that, upon LPS stimulation of WI38 fibroblast cells, inflammation was induced, whereas the condition of the cells reverted to normal in the essential oil extract pre‑treated group. The results of western blot analysis revealed the inhibition of inducible nitric oxide synthase, activation of cyclooxygnase‑2, and the degradation of cytosolic p65 and inhibitor of NF‑κB‑α in the LPS‑stimulated group. Additionally, confocal imaging of nuclei revealed the translocation of phosphorylated p65, which was recovered in the cytosol in the phytoncide essential oil pre‑treated group. Histopathological observation revealed that the alveolar capacity was enhanced in the essential oil olfactory administered rat group, compared with that in the normal rat group. These findings suggest that terpenes in essential oil from the Chamaecyparis obtusa leaf have therapeutic potential against respiratory inflammation‑related disease.

View Figures

View References

1	Naura AS, Zerfaoui M, Kim H, Abd Elmageed ZY, Rodriguez PC, Hans CP, Ju J, Errami Y, Park J, Ochoa AC, et al: Requirement for inducible nitric oxide synthase in chronic allergen exposure-induced pulmonary fibrosis but not inflammation. J Immunol. 185:3076–3085. 2010. View Article : Google Scholar : PubMed/NCBI
2	Moldoveanu B, Otmishi P, Jani P, Walker J, Sarmiento X, Guardiola J, Saad M and Yu J: Inflammatory mechanisms in the lung. J Inflamm Res. 2:1–11. 2009.PubMed/NCBI
3	Stellari F, Bergamini G, Ruscitti F, Sandri A, Ravanetti F, Donofrio G, Boschi F, Villetti G, Sorio C, Assael BM, et al: In vivo monitoring of lung inflammation in CFTR-deficient mice. J Transl Med. 14:2262016. View Article : Google Scholar : PubMed/NCBI
4	Eutamene H, Theodorou V, Schmidlin F, Tondereau V, Garcia-Villar R, Salvador-Cartier C, Chovet M, Bertrand C and Bueno L: LPS-induced lung inflammation is linked to increased epithelial permeability: Role of MLCK. Eur Respir J. 25:789–796. 2005. View Article : Google Scholar : PubMed/NCBI
5	Van Linthout S, Miteva K and Tschöpe C: Crosstalk between fibroblasts and inflammatory cells. Cardiovasc Res. 102:258–269. 2014. View Article : Google Scholar : PubMed/NCBI
6	Vancheri C, Mastruzzo C, Tomaselli V, Sortino MA, D’Amico L, Bellistrí G, Pistorio MP, Salinaro ET, Palermo F, Mistretta A, et al: Normal human lung fibroblasts differently modulate interleukin-10 and interleukin-12 production by monocytes: Implications for an altered immune response in pulmonary chronic inflammation. Am J Respir Cell Mol Biol. 25:592–599. 2001. View Article : Google Scholar : PubMed/NCBI
7	Flavell SJ, Hou TZ, Lax S, Filer AD, Salmon M and Buckley CD: Fibroblasts as novel therapeutic targets in chronic inflammation. Br J Pharmacol. 153(Suppl 1): S241–S246. 2008. View Article : Google Scholar
8	Ikei H, Song C and Miyazaki Y: Physiological effect of olfactory stimulation by Hinoki cypress (Chamaecyparis obtusa) leaf oil. J Physiol Anthropol. 34:442015. View Article : Google Scholar : PubMed/NCBI
9	Lee SH, Do HS and Min KJ: Effects of essential oil from Hinoki cypressChamaecyparis obtusa, on physiology and behavior of flies. PLoS One. 10:e01434502015. View Article : Google Scholar
10	Abe T, Hisama M, Tanimoto S, Shibayama H, Mihara Y and Nomura M: Antioxidant effects and antimicrobial activites of phytoncide. Biocontrol Sci. 13:23–27. 2008. View Article : Google Scholar : PubMed/NCBI
11	Zhang S, Jung JH, Kim HS, Kim BY and Kim IH: Influences of phytoncide supplementation on growth performance, nutrient digestibility, blood profiles, diarrhea scores and fecal microflora shedding in weaning pigs. Asian-Australas J Anim Sci. 25:1309–1315. 2012. View Article : Google Scholar : PubMed/NCBI
12	Li Q: Effect of forest bathing trips on human immune function. Environ Health Prev Med. 15:9–17. 2010. View Article : Google Scholar :
13	Li Q, Kobayashi M, Wakayama Y, Inagaki H, Katsumata M, Hirata Y, Hirata K, Shimizu T, Kawada T, Park BJ, et al: Effect of phytoncide from trees on human natural killer cell function. Int J Immunopathol Pharmacol. 22:951–959. 2009. View Article : Google Scholar
14	Sobral MV, Xavier AL, Lima TC and de Sousa DP: Antitumor activity of monoterpenes found in essential oils. Scientific World Journal. 2014.e9534512014.
15	Juergens UR: Anti-inflammatory properties of the monoterpene 1.8-cineole: Current evidence for co-medication in inflammatory airway diseases. Drug Res (Stuttg). 64:638–646. 2014. View Article : Google Scholar
16	Guerreiro M, Mernak M, Santana F, Pinheiro N, Ramanholo BS, Capello T, Lolanda T, Martins M, Lago J and Prado C: Essential oils reduced lung inflammation in a model of acute lung injury. Eur Respir J. 44:39252014.
17	Games E, Guerreiro M, Santana FR, Pinheiro NM, de Oliveira EA, Lopes FD, Olivo CR, Tibério IF, Martins MA, Lago JH, et al: Structurally related monoterpenes p-Cymene, carvacrol and thymol isolated from essential oil from leaves of Lippia si Cham. (Verbenaceae) protect mice against elastase-induced emphysemades. Molecules. 21:E13902016. View Article : Google Scholar
18	Park Y, Yoo SA, Kim WU, Cho CS, Woo JM and Yoon CH: Anti-inflammatory effects of essential oils extracted from Chamaecyparis obtusa on murine models of inflammation and RAW 264.7 cells. Mol Med Rep. 13:3335–3341. 2016. View Article : Google Scholar : PubMed/NCBI
19	Kuiate JR, Bessière JM, Zollo PH and Kuate SP: Chemical composition and antidermatophytic properties of volatile fractions of hexanic extract from leaves of Cupressus lusitanica Mill. from Cameroon. J Ethnopharmacol. 103:160–165. 2006. View Article : Google Scholar
20	Su YC and Ho CL: Composition and two activities of the leaf essential oil of Litsea acuminata (Blume) Kurata from Taiwan. Rec Nat Prod. 7:27–34. 2013.
21	Wang SY, Wang YS, Tseng YH, Lin CT and Liu CP: Analysis of fragrance compositions of precious coniferous woods grown in Taiwan. Holzforschung. 60:528–532. 2006. View Article : Google Scholar
22	Xu Brittany M, Baker George L, Sarnoski Paul J and Goodrich-Schneide Renée M: A comparison of the volatile components of cold pressed Hamlin and Valencia (Citrus sinensis (L.) Osbeck) orange oils affected by Huanglongbing. J Food Qual. 2017.6793986:2017.
23	Okin D and Medzhitov R: Evolution of inflammatory diseases. Curr Biol. 22:R733–R740. 2012. View Article : Google Scholar : PubMed/NCBI
24	Tak PP, Firestein GS and NF-kappa B: A key role in inflammatory diseases. J Clin Invest. 107:7–11. 2001. View Article : Google Scholar : PubMed/NCBI
25	Jin MH, Yook J, Lee E, Lin CX, Quan Z, Son KH, Bae KH, Kim HP, Kang SS and Chang HW: Anti-inflammatory activity of Ailanthus altissima in ovalbumin-induced lung inflammation. Biol Pharm Bull. 29:884–888. 2006. View Article : Google Scholar : PubMed/NCBI
26	Lee H, Kim Y, Kim HJ, Park S, Jang YP, Jung S, Jung H and Bae H: Herbal formula, PM014, attenuates lung inflammation in a murine model of chronic obstructive pulmonary disease. Evid Based Complement Alternat Med. 2012.769830:2012.
27	Husari A, Hashem Y, Bitar H, Dbaibo G, Zaatari G and El Sabban M: Antioxidant activity of pomegranate juice reduces emphysematous changes and injury secondary to cigarette smoke in an animal model and human alveolar cells. Int J Chron Obstruct Pulmon Dis. 11:227–237. 2016. View Article : Google Scholar : PubMed/NCBI
28	Kloesch B, Dietersdorfer E, Loebsch S and Steiner G: Anti-inflammatory and pro-apoptotic effects of curcumin and resveratrol on the human lung fibroblast cell line MRC-5. Altern Integr Med. 3:1742014.
29	Swamy MK, Akhtar MS and Sinniah UR: Antimicrobial properties of plant essential oils against human pathogens and their mode of action: An updated review. Evid Based Complement Alternat Med. 2016.3012462:2016.
30	Wang H, Song L, Ju W, Wang X, Dong L, Zhang Y, Ya P, Yang C and Li F: The acute airway inflammation induced by PM2.5 exposure and the treatment of essential oils in Balb/c mice. Sci Rep. 7:442562017. View Article : Google Scholar :
31	Li Q, Nakadai A, Matsushima H, Miyazaki Y, Krensky AM, Kawada T and Morimoto K: Phytoncides (wood essential oils) induce human natural killer cell activity. Immunopharmacol Immunotoxicol. 28:319–333. 2006. View Article : Google Scholar : PubMed/NCBI
32	Ikei H, Song C and Miyazaki Y: Physiological effects of touching hinoki cypress (Chamaecyparis obtusa). J Wood Sci. 64:226–236. 2018. View Article : Google Scholar
33	Kang S, Lee JS, Lee HC, Petriello MC, Kim BY, Do JT, Lim DS, Lee HG and Han SG: Phytoncide extracted from pinecone decreases LPS-induced inflammatory responses in bovine mammary epithelial cells. J Microbiol Biotechnol. 26:579–587. 2016. View Article : Google Scholar
34	Shih MF, Chen LY, Tsai PJ and Cherng JY: In vitro and in vivo therapeutics of β-thujaplicin on LPS-induced inflammation in macrophages and septic shock in mice. Int J Immunopathol Pharmacol. 25:39–48. 2012. View Article : Google Scholar : PubMed/NCBI
35	Lin JJ, Lin JH, Hsu SC, Weng SW, Huang YP, Tang NY, Lin JG and Chung JG: Alpha-phellandrene promotes immune responses in normal mice through enhancing macrophage phagocytosis and natural killer cell activities. In Vivo. 27:809–814. 2013.PubMed/NCBI
36	Lanas A, Haggerty P and Hirschowitz BI: In vitro studies of anti-inflammatory agents and prostaglandin e2 effects on stimulated normal human fibroblast cultures. Inflammopharmacology. 2:377–387. 1994. View Article : Google Scholar
37	Seo HR, Choi MJ, Choi JM, Ko JC, Ko JY and Cho EJ: Malvidin protects WI-38 human fibroblast cells against stress-induced premature senescence. J Cancer Prev. 21:32–40. 2016. View Article : Google Scholar : PubMed/NCBI
38	Thangavel J, Samanta S, Rajasingh S, Barani B, Xuan YT, Dawn B and Rajasingh J: Epigenetic modifiers reduce inflammation and modulate macrophage phenotype during endotoxemia-induced acute lung injury. J Cell Sci. 128:3094–3105. 2015. View Article : Google Scholar : PubMed/NCBI
39	Schuliga M: NF-kappaB signaling in chronic inflammatory airway disease. Biomolecules. 5:1266–1283. 2015. View Article : Google Scholar : PubMed/NCBI
40	Barnes PJ: Transcription factors in airway diseases. Lab Invest. 86:867–872. 2006. View Article : Google Scholar : PubMed/NCBI
41	Lee IT and Yang CM: Inflammatory signalings involved in airway and pulmonary diseases. Mediators Inflamm. 2013.791231:2013.
42	Xie F, Yang L, Han L and Yue B: MicroRNA-194 regulates lipopolysaccharide-induced cell viability by inactivation of nuclear factor-κ B pathway. Cell Physiol Biochem. 43:2470–2478. 2017. View Article : Google Scholar
43	de Cassia da Silveira E Sa R, Andrade LN, Dos Reis Barreto, de Oliveira R and de Sousa DP: A review on anti-inflammatory activity of phenylpropanoids found in essential oils. Molecules. 19:1459–1480. 2014. View Article : Google Scholar
44	Kim KN, Ko YJ, Yang HM, Ham YM, Roh SW, Jeon YJ, Ahn G, Kang MC, Yoon WJ, Kim D, et al: Anti-inflammatory effect of essential oil and its constituents from fingered citron (Citrus medica L. var. sarcodactylis) through blocking JNK, ERK and NF-κB signaling pathways in LPS-activated RAW 264.7 cells. Food Chem Toxicol. 57:126–131. 2013. View Article : Google Scholar : PubMed/NCBI
45	Chiang YM, Lo CP, Chen YP, Wang SY, Yang NS, Kuo YH and Shyur LF: Ethyl caffeate suppresses NF-kappaB activation and its downstream inflammatory mediators, iNOS, COX-2, and PGE2 in vitro or in mouse skin. Br J Pharmacol. 146:352–363. 2005. View Article : Google Scholar : PubMed/NCBI
46	Wei J, Zhang X, Bi Y, Miao R, Zhang Z and Su H: Anti-inflammatory effects of cumin essential oil by blocking JNK, ERK, and NF-κB signaling pathways in LPS-stimulated RAW 264.7 cells. Evid Based Complement Alternat Med. 2015.474509:2015.
47	Raha S, Lee HJ, Yumnam S, Hong GE, Venkatarame Gowda Saralamma V, Ha YL, Kim JO, Kim YS, Heo JD, Lee SJ, et al: Vitamin D2 suppresses amyloid-β 25–35 induced microglial activation in BV2 cells by blocking the NF-κB inflammatory signaling pathway. Life Sci. 161:37–44. 2016. View Article : Google Scholar : PubMed/NCBI