Butanol extracts of Asparagus cochinchinensis fermented with Weissella cibaria inhibit iNOS‑mediated COX‑2 induction pathway and inflammatory cytokines in LPS‑stimulated RAW264.7 macrophage cells

Lee,Hyun  Ah; Song,Bo  Ram; Kim,Hye  Ryeong; Kim,Ji  Eun; Yun,Woo  Bin; Park,Jin  Ju; Lee,Mi  Lim; Choi,Jun  Young; Lee,Hee  Seob; Hwang,Dae  Youn

doi:10.3892/etm.2017.5200

Butanol extracts of Asparagus cochinchinensis fermented with Weissella cibaria inhibit iNOS‑mediated COX‑2 induction pathway and inflammatory cytokines in LPS‑stimulated RAW264.7 macrophage cells

Authors:
- Hyun Ah Lee
- Bo Ram Song
- Hye Ryeong Kim
- Ji Eun Kim
- Woo Bin Yun
- Jin Ju Park
- Mi Lim Lee
- Jun Young Choi
- Hee Seob Lee
- Dae Youn Hwang
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Affiliations: Department of Biomaterials Science, College of Natural Resources and Life Science/Life and Industry Convergence Research Institute, Pusan National University, Miryang, Gyeongsangnam-do 627‑706, Republic of Korea, Department of Food Science and Nutrition, College of Human Ecology, Pusan National University, Busan 609‑735, Republic of Korea
Published online on: September 25, 2017 https://doi.org/10.3892/etm.2017.5200
Pages: 4986-4994
Copyright: © Lee et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Roots of Asparagus cochinchinesis have been widely used to treat fever, cough, kidney disease, breast cancer, inflammatory and brain disease, although the effects of their fermented products have not been assessed until now. To investigate the anti‑inflammatory effects on macrophages of a butanol extract from A. cochinchinensis roots fermented with Weissella cibaria (BAW), alterations in the inducible nitric oxide synthase (iNOS)‑mediated cyclooxygenase‑2 (COX‑2) induction pathway and inflammatory cytokine expression were measured in lipopolysaccharide (LPS)‑activated RAW264.7 cells following pretreatment with BAW. Briefly, W. cibaria was selected from two bacterial strains for the fermentation of A. cochinchinensis roots based on its hyaluronidase inhibition and NO suppression rates. Following fermentation with W. cibaria, the level of various key components including total phenols and protodioscin were significantly enhanced in BAW. In addition, BAW exhibited high free radical scavenging activity (IC50=31.62 µg/ml) and induced a decrease of intracellular ROS production in RAW264.7 cells following DCFH‑DA staining. Significant suppressions in the expression level of important members of the iNOS‑mediated COX‑2 induction pathway and the phosphorylation of mitogen‑activated protein kinase members were detected. The expressions of pro‑inflammatory and anti‑inflammatory cytokines were recovered in BAW pretreated RAW264.7 cells. Overall, these results suggest that BAW may suppress inflammatory responses through differential regulation of the iNOS‑mediated COX‑2 induction pathway and inflammatory cytokine expressions in LPS‑activated RAW264.7 cells.

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1	Krishnamoorthy S and Honn KV: Inflammation and disease progression. Cancer Metastasis Rev. 25:481–491. 2006. View Article : Google Scholar : PubMed/NCBI
2	Arulselvan P, Fard MT, Tan WS, Gothai S, Fakurazi S, Norhaizan ME and Kumar SS: Role of antioxidants and natural products in inflammation. Oxid Med Cell Longev. 2016:52761302016. View Article : Google Scholar : PubMed/NCBI
3	Henson PM, Larsen GL, Henson JE, Newman SL, Musson RA and Leslie CC: Resolution of pulmonary inflammation. Fed Pro. 43:2799–2806. 1984.
4	Gautam R and Jachak SM: Recent developments in anti-inflammatory natural products. Med Res Rev. 29:767–820. 2009. View Article : Google Scholar : PubMed/NCBI
5	Parker KL and Schimmer BP: Genetics of the development and function of the adrenal cortex. Rev Endocr Metab Disord. 2:245–252. 2001. View Article : Google Scholar : PubMed/NCBI
6	Ravipati AS, Zhang L, Koyyalamudi SR, Jeong SC, Reddy N, Bartlett J, Smith PT, Shanmugam K, Münch G, Wu MJ, et al: Antioxidant and anti-inflammatory activities of selected Chinese medicinal plants and their relation with antioxidant content. BMC Complement Altern Med. 12:1732012. View Article : Google Scholar : PubMed/NCBI
7	Kim HY, Hwang KW and Park SY: Extracts of Actinidia arguta stems inhibited LPS-induced inflammatory responses through nuclear factor-κB pathway in Raw 264.7 cells. Nutr Res. 34:1008–1016. 2014. View Article : Google Scholar : PubMed/NCBI
8	Hou XL, Tong Q, Wang WQ, Shi CY, Xiong W, Chen J, Liu X and Fang JG: Suppression of inflammatory responses by dihydromyricetin, a flavonoid from Ampelopsis grossedentata, via inhibiting the activation of NF-κB and MAPK signaling pathways. J Nat Prod. 78:1689–1696. 2015. View Article : Google Scholar : PubMed/NCBI
9	Oh YC, Jeong YH, Kim T, Cho WK and Ma JY: Anti-inflammatory effect of Artemisiae annuae herba in lipopolysaccharide-stimulated RAW 264.7 cells. Pharmacogn Mag. 10 Suppl 3:S588–S595. 2014. View Article : Google Scholar : PubMed/NCBI
10	Lamichhane R, Kim SG, Poudel A, Sharma D, Lee KH and Jung HJ: Evaluation of in vitro and in vivo biological activities of Cheilanthes albomarginata Clarke. BMC Complement Altern Med. 14:3422014. View Article : Google Scholar : PubMed/NCBI
11	Kim DH, Kim ME and Lee JS: Inhibitory effects of extract from G. lanceolata on LPS-induced production of nitric oxide and IL-1β via down-regulation of MAPK in macrophages. Appl Biochem Biotechnol. 175:657–665. 2015. View Article : Google Scholar : PubMed/NCBI
12	Kim H, Lee E, Lim T, Jung J and Lyu Y: Inhibitory effect of Asparagus cochinchinensis on tumor necrosis factor-alpha secretion from astrocytes. Int J Immunopharmacol. 20:153–162. 1998. View Article : Google Scholar : PubMed/NCBI
13	Lee DY, Choo BK, Yoon T, Cheon MS, Lee HW, Lee YA and Kim HK: Anti-inflammatory effects of Asparagus cochinchinensis extract in acute and chronic cutaneous inflammation. J Ethnopharmacol. 121:28–34. 2009. View Article : Google Scholar : PubMed/NCBI
14	Koo HN, Jeong HJ, Choi JY, Choi SD, Choi TJ, Cheon YS, Kim KS, Kang BK, Park ST, Chang CH, et al: Inhibition of tumor necrosis factor-alpha-induced apoptosis by Asparagus cochlnchinensis in HepG2 cells. J Ethnopharmacol. 73:137–143. 2000. View Article : Google Scholar : PubMed/NCBI
15	Xiong D, Yu LX, Yan X, Guo C and Xiong Y: Effects of root and stem extracts of Asparagus cochinchinensis on biochemical indicators related to aging in the brain and liver of mice. Am J Chinese Med. 39:719–726. 2011. View Article : Google Scholar
16	Jung KH, Choi HL, Park S, Lee G, Kim M, Min JK, Min BI and Bae H: The effects of the standardized herbal formula PM014 on pulmonary inflammation and airway responsiveness in a murine model of cockroach allergen-induced asthma. J Ethnopharmacol. 155:113–122. 2014. View Article : Google Scholar : PubMed/NCBI
17	Elson LA and Morgan WTJ: A colorimetric method for the determination of glucosamine and chondrosamine. Biochem J. 27:1824–1828. 1933. View Article : Google Scholar : PubMed/NCBI
18	Kaegawa H, Matsumoto H, Endo K, Satoh T, Nonaka GI and Noshioka I: Inhibitory effects of tannins on hyaluronidase activation and on the degranulation from rat mesentery mast cells. Chem Pharm Bull. 33:5079–5082. 1985. View Article : Google Scholar : PubMed/NCBI
19	Lee KK, Kim JH, Cho JJ and Choi JD: Inhibitory effects of 150 plant extracts on elastase activity and their anti-inflammatory effects. Int J Cosmet Sci. 21:71–82. 1999. View Article : Google Scholar : PubMed/NCBI
20	Singleton VL and Rossi JA: Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic. 16:144–158. 1965.
21	Hassan SM, Al Aqil AA and Attimarad M: Determination of crude saponin and total flavonoids content in guar meal. Adv Med Plant Res. 1:24–28. 2013.
22	Oh H, Ko EK, Kim DH, Jan KK, Park SE, Lee HS and Kim YC: Secoiridoid glucosides with free radical scavenging activity from the leaves of Syringa dilatata. Phytother Res. 17:417–419. 2003. View Article : Google Scholar : PubMed/NCBI
23	Jie S, Xueji Z, Mark B and Harry F: Measurement of nitric oxide production in biological systems by using griess reaction assay. Sensors. 3:276–284. 2003. View Article : Google Scholar
24	Kim JE, Park SH, Kwak MH, Go J, Koh EK, Song SH, Sung JE, Lee HS, Hong JT and Hwang DY: Characterization of changes in global genes expression in the distal colon of loperamide-induced constipation SD rats in response to the laxative effects of Liriope platyphylla. PLoS One. 10:e01296642015. View Article : Google Scholar : PubMed/NCBI
25	Ishimura N, Bronk SF and Gores GJ: Inducible nitric oxide synthase upregulates cyclooxygenase-2 in mouse cholangiocytes promoting cell growth. Am J Physiol Gastrointest Liver Physiol. 287:G88–G95. 2004. View Article : Google Scholar : PubMed/NCBI
26	Rahman M: Medical application of fermentation technology. Adv Mat Res. 810:127–157. 2013.
27	Oh YC, Cho WK, Jeong YH, Im GY, Yang MC and Ma JY: Fermentation improves anti-inflammatory effect of sipjeondaebotang on LPS-stimulated RAW 264.7 cells. Am J Chin Med. 40:813–831. 2012. View Article : Google Scholar : PubMed/NCBI
28	Bose S, Jeon S, Eom T, Song MY and Kim H: Evaluation of the in vitro and in vivo protective effects of unfermented and fermented Rhizoma coptidis formulations against lipopolysaccharide insult. Food Chem. 135:452–459. 2012. View Article : Google Scholar : PubMed/NCBI
29	Giriwono PE, Shirakawa H, Hokazono H, Goto T and Komai M: Fermented barley extract supplementation maintained antioxidative defense suppressing lipopolysaccharide-induced inflammatory liver injury in rats. Biosci Biotechnol Biochem. 75:1971–1976. 2011. View Article : Google Scholar : PubMed/NCBI
30	Xiao PG: Modern Chinese Materia Medica. Chemical Industry Press; Beijing: pp. 1502002
31	Liu YZ, Qu FY and Zhang PX: EfBFct of chloroform extract of Tiandong on the brain antioxidation of D-galactose-induced senile mice. Heilongjiang Med Pharm. 24:7–8. 2001.
32	Ni JM, Zhao R and Wang R: Comparison on amino acid content in prepared and unprepared Asparagus cochinchinensis. Chin Tradit Herb Drugs. 23:182–183. 1992.
33	Tenji K and Junzo S: Studies on the constituents of Asparagi Radix. I. On the structures of furostanol oligosides of Asparagus cochinchinensis (Lour.) Merr. Chem Pharm Bull. 27:3086–3094. 1979. View Article : Google Scholar
34	Liang ZZ, Aquino R, De Simone F, Dini A, Schettino O and Pizza C: Oligofurostanosides from Asparagus cochinchinensis. Planta Med. 54:344–346. 1988. View Article : Google Scholar : PubMed/NCBI
35	Yang YC, Huang SY and Shi JG: Two new furostanol glycosides from Asparagus cochinchinensis. Chin Chem Lett. 13:1185–1188. 2002.
36	Cong PZ and Keman S: Handbook of analytical chemistry-mass volume. Chemical Industry Publishing House; Beijing: pp. 296–298. 2000
37	Gong YH: 13C NMR chemical shifts of natural organic compounds. Yunnan Science and Technology Publishing House; Kunming: pp. 2521986
38	Yang MH: Steroidal sapogenins of dioscorea. Chin Tradit Herb Drugs. 12:43–44. 1981.
39	Xu CL, Chen HS and Tan XQ: Studies on the active constituents of Asparagi radix. Nat Prod Res Dev. 17:128–130. 2005.
40	Shen Y, Chen HS and Wang Q: Studies on chemical constituents of Asparagus cochinchinensis. J Second Med Univ. 28:1241–1244. 2007.
41	Shen Y, Xu CL, Xuan WD, Li HL, Liu RH, Xu XK and Chen HS: A new furostanol saponin from Asparagus cochinchinensis. Arch Pharm Res. 34:1587–1591. 2011. View Article : Google Scholar : PubMed/NCBI
42	Li XN, Chu C, Cheng DP, Tong SQ and Yan JZ: Norlignans from Asparagus cochinchinensis. Nat Prod Commun. 7:1357–1358. 2012.PubMed/NCBI
43	Zhu GL, Hao Q, Li RT and Li HZ: Steroidal saponins from the roots of Asparagus cochinchinensis. Chin J Nat Med. 12:213–217. 2014.PubMed/NCBI
44	Oh YC, Cho WK, Oh JH, Im GY, Jeong YH, Yang MC and Ma JY: Fermentation by Lactobacillus enhances anti-inflammatory effect of Oyaksungisan on LPS-stimulated RAW 264.7 mouse macrophage cells. BMC Complement Altern Med. 12:172012. View Article : Google Scholar : PubMed/NCBI
45	Bose S, Song MY, Nam JK, Lee MJ and Kim H: In vitro and in vivo protective effects of fermented preparations of dietary herbs against lipopolysaccharide insult. Food Chem. 134:758–765. 2012. View Article : Google Scholar : PubMed/NCBI
46	Jung HJ, Choi H, Lim HW, Shin D, Kim H, Kwon B, Lee JE, Park EH and Lim CJ: Enhancement of anti-inflammatory and antinociceptive actions of red ginseng extract by fermentation. J Pharm Pharmacol. 64:756–762. 2012. View Article : Google Scholar : PubMed/NCBI
47	Lee WH, Wu HM, Lee CG, Sung DI, Song HJ, Matsui T, Kim HB and Kim SG: Specific oligopeptides in fermented soybean extract inhibit NF-κB-dependent iNOS and cytokine induction by toll-like receptor ligands. J Med Food. 17:1239–1246. 2014. View Article : Google Scholar : PubMed/NCBI
48	Endo K, Yoon BI, Pairojkul C, Demetris AJ and Sirica AE: ERBB-2 overexpression and cyclooxygenase-2 up-regulation in human cholangiocarcinoma and risk conditions. Hepatology. 36:439–450. 2002. View Article : Google Scholar : PubMed/NCBI
49	Jaiswal M, LaRusso NF, Burgart LJ and Gores GJ: Inflammatory cytokines induce DNA damage and inhibit DNA repair in cholangiocarcinoma cells by a nitric oxide-dependent mechanism. Cancer Res. 60:184–190. 2000.PubMed/NCBI
50	Hemish J, Nakaya N, Mittal V and Enikolopov G: Nitric oxide activates diverse signaling pathways to regulate gene expression. J Biol Chem. 278:42321–42329. 2003. View Article : Google Scholar : PubMed/NCBI
51	Berghe W Vanden, Plaisance S, Boone E, Debosscher K, Schmitz ML, Fiers W and Haegeman G: p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways are required for nuclear factor-kappaB p65 transactivation mediated by tumor necrosis factor. J Biol Chem. 273:3285–3290. 1998. View Article : Google Scholar : PubMed/NCBI