Anti-inflammatory effects of ethanolic extract from Abeliophyllum distichum (Miseon Tree) leaves in mice with dextran sulfate sodium-induced ulcerative colitis

Hye-Jung Moon; Youn-Soo Cha; Kyung-Ah Kim

doi:10.29219/fnr.v69.11052

Hye-Jung Moon Department of Food Science and Human Nutrition, Jeonbuk National University
Youn-Soo Cha Department of Food Science and Human Nutrition, Jeonbuk National University, Jeonju, Republic of Korea; K-Food Research Center, Jeonju, Republic of Korea
Kyung-Ah Kim Department of Food and Nutrition, Chungnam National University, Daejeon, Republic of Korea

DOI: https://doi.org/10.29219/fnr.v69.11052

Keywords: Abeliophyllum distichum, dextran sulfate sodium, colitis, NF-kappa B

Abstract

Abeliophyllum distichum (Miseon tree), a native Korean plant, is known for the high phenolic content in its leaves. The ethanolic leaf extracts of A. distichum have shown antioxidant, anti-obesity, and anti-inflammatory properties. However, studies on its potential to improve colitis are limited. This study aimed to determine whether the ethanolic extract of A. distichum leaves (ADE) could alleviate dextran sulfate sodium (DSS)-induced colitis in mice. The mice were divided into three groups, and the experimental group was given 300 mg/kg ADE for 4 weeks. One week before the end of the experiment, 3% DSS was added to the drinking water to induce colitis. The clinical symptoms of colitis and damage to colon tissue, including the increase in Enterobacteriaceae abundance and a decrease in Bifidobacterium in the colon, were evaluated during DSS treatment. DSS overactivated the nuclear factor (NF)-κB signaling pathway, resulting in excessive production of pro-inflammatory cytokines. In contrast, ADE alleviated the DSS-induced colitis symptoms, protected against colonic tissue damage, and restored the balance of Enterobacteriaceae and Bifidobacterium levels in the colon. Moreover, ADE effectively inhibited the DSS-induced overactivation of the NF-κB signaling pathway within the colon and mitigated abnormal inflammatory responses. These findings suggest that ADE protects against colitis by modulating the growth of some intestinal strains and the NF-κB pathway in the colon, supporting its potential as a natural agent.

Downloads

Download data is not yet available.

References

1.
Gajendran M, Loganathan P, Jimenez G, Catinella AP, Ng N, Umapathy C, et al. A comprehensive review and update on ulcerative colitis. Dis Mon 2019; 65(12): 100851. doi: 10.1016/j.disamonth.2019.02.004

2.
Yu YR, Rodriguez JR. Clinical presentation of Crohn’s, ulcerative colitis, and indeterminate colitis: symptoms, extraintestinal manifestations, and disease phenotypes. Semin in Pediat Surg 2017; 26(6): 349–55. doi: 10.1053/j.sempedsurg.2017.10.003

3.
Ng SC, Shi HY, Hamidi N, Underwood FE, Tang W, Benchimol EI, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet 2017; 390(10114): 2769–78. doi: 10.1016/s0140-6736(17)32448-0

4.
Lobionda S, Sittipo P, Kwon HY, Lee YK. The role of gut microbiota in intestinal inflammation with respect to diet and extrinsic stressors. Microorganisms 2019; 7(8): 271. doi: 10.3390/microorganisms7080271

5.
Sartor RB. Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 2006; 3(7): 390–407. doi: 10.1038/ncpgasthep0528

6.
Zhou Y, Wang D, Yan W. Treatment effects of natural products on inflammatory bowel disease in vivo and their mechanisms: based on animal experiments. Nutrients 2023; 15(4): 1031. doi: 10.3390/nu15041031
7.Burisch J, Vardi H, Schwartz D, Friger M, Kiudelis G, Kupčinskas J, et al. Health-care costs of inflammatory bowel disease in a pan-European, community-based, inception cohort during 5 years of follow-up: a population-based study. Lancet Gastroenterol Hepatol 2020; 5(5): 454–64. doi: 10.1016/s2468-1253(20)30012-1

8.
Cai Z, Wang S, Li J. Treatment of inflammatory bowel disease: a comprehensive review. Front Med (Lausanne) 2021; 8: 765474. doi: 10.3389/fmed.2021.765474

9.
Alsoud D, Verstockt B, Fiocchi C, Vermeire S. Breaking the therapeutic ceiling in drug development in ulcerative colitis. Lancet Gastroenterol Hepatol 2021; 6(7): 589–95. doi: 10.1016/s2468-1253(21)00065-0
10.Fumery M, Singh S, Dulai PS, Gower-Rousseau C, Peyrin-Biroulet L, Sandborn WJ. Natural history of adult ulcerative colitis in population-based cohorts: a systematic review. Clin Gastroenterol Hepatol 2018; 16(3): 343–56.e3. doi: 10.1016/j.cgh.2017.06.016

11.
Volk N, Siegel CA. Defining failure of medical therapy for inflammatory bowel disease. Inflamm Bowel Dis 2019; 25(1): 74–7. doi: 10.1093/ibd/izy238

12.
Bergemalm D, Andersson E, Hultdin J, Eriksson C, Rush ST, Kalla R, et al. Systemic inflammation in preclinical ulcerative colitis. Gastroenterology 2021; 161(5): 1526–39.e9. doi: 10.1053/j.gastro.2021.07.026

13.
Kim G, Jang M, Hwang I, Cho J, Kim S. Radish sprout alleviates DSS-induced colitis via regulation of NF-κB signaling pathway and modifying gut microbiota. Biomed Pharmacother 2021; 144: 112365. doi: 10.1016/j.biopha.2021.112365

14.
Terra X, Valls J, Vitrac X, Mérrillon JM, Arola L, Ardèvol A, et al. Grape-seed procyanidins act as antiinflammatory agents in endotoxin-stimulated RAW 264.7 macrophages by inhibiting NFκB signaling pathway. J Agric Food Chem 2007; 55(11): 4357–65. doi: 10.1021/jf0633185

15.
Kang U, Chang C-S, Kim YS. Genetic structure and conservation considerations of rare endemic Abeliophyllum distichum Nakai (Oleaceae) in Korea. J Plant Res 2000; 113(2): 127–38. doi: 10.1007/PL00013923

16.
Lee NN, Kim J-A, Kim Y-W, Choi YE, Moon HK. Effect of explant’s position and culture method on shoot proliferation and micro-cuttings for a rare and endangered species, Abeliophyllum distichum Nakai. J Plant Biotechnol 2015; 42(3): 228–34. doi: 10.5010/JPB.2015.42.3.228
17.Park GH, Park JH, Eo HJ, Song HM, Woo SH, Kim MK, et al. The induction of activating transcription factor 3 (ATF3) contributes to anti-cancer activity of Abeliophyllum distichum Nakai in human colorectal cancer cells. BMC Complement Altern Med 2014; 14: 487. doi: 10.1186/1472-6882-14-487

18.
Yoo TK, Kim JS, Hyun TK. Polyphenolic composition and anti-melanoma activity of white forsythia (Abeliophyllum distichum Nakai) organ extracts. Plants (Basel) 2020; 9(6): 757. doi: 10.3390/plants9060757

19.
Lee HD, Kim JH, Pang QQ, Jung PM, Cho EJ, Lee S. Antioxidant activity and acteoside analysis of Abeliophyllum distichum. Antioxidants (Basel) 2020; 9(11): 1148. doi: 10.3390/antiox9111148

20.
Kim HW, Yu AR, Kang M, Sung NY, Lee BS, Park SY, et al. Verbascoside-rich Abeliophyllum distichum Nakai leaf extracts prevent LPS-induced preterm birth through inhibiting the expression of proinflammatory cytokines from macrophages and the cell death of trophoblasts induced by TNF-α. Molecules 2020; 25(19): 4579. doi: 10.3390/molecules25194579

21.
Choi YJ, Fan M, Tang Y, Moon S, Lee SH, Lee B, et al. Ameliorative effect of Abeliophyllum distichum Nakai on benign prostatic hyperplasia in vitro and in vivo. Nutr Res Pract 2022; 16(4): 419–34. doi: 10.4162/nrp.2022.16.4.419

22.
Eom J, Thomas SS, Sung NY, Kim DS, Cha YS, Kim KA. Abeliophyllum distichum ameliorates high-fat diet-induced obesity in C57BL/6J mice by upregulating the AMPK pathway. Nutrients 2020; 12(11): 3320. doi: 10.3390/nu12113320

23.
Thomas SS, Eom J, Sung NY, Kim DS, Cha YS, Kim KA. Inhibitory effect of ethanolic extract of Abeliophyllum distichum leaf on 3T3-L1 adipocyte differentiation. Nutr Res Pract 2021; 15(5): 555–67. doi: 10.4162/nrp.2021.15.5.555

24.
Wasilewska E, Zlotkowska D, Wroblewska B. Yogurt starter cultures of Streptococcus thermophilus and Lactobacillus bulgaricus ameliorate symptoms and modulate the immune response in a mouse model of dextran sulfate sodium-induced colitis. J Dairy Sci 2019; 102(1): 37–53. doi: 10.3168/jds.2018-14520

25.
Kataoka K, Ogasa S, Kuwahara T, Bando Y, Hagiwara M, Arimochi H, et al. Inhibitory effects of fermented brown rice on induction of acute colitis by dextran sulfate sodium in rats. Dig Dis Sci 2008; 53(6): 1601–8. doi: 10.1007/s10620-007-0063-3

26.
Wullaert A. Role of NF-κB activation in intestinal immune homeostasis. Int J Med Microbiol 2010; 300(1): 49–56. doi: 10.1016/j.ijmm.2009.08.007

27.
Segal JP, LeBlanc JF, Hart AL. Ulcerative colitis: an update. Clin Med (Lond) 2021; 21(2): 135–9. doi: 10.7861/clinmed.2021-0080

28.
Eichele DD, Kharbanda KK. Dextran sodium sulfate colitis murine model: an indispensable tool for advancing our understanding of inflammatory bowel diseases pathogenesis. World J Gastroenterol 2017; 23(33): 6016–29. doi: 10.3748/wjg.v23.i33.6016

29.
Liu Y, Huang W, Zhu Y, Zhao T, Xiao F, Wang Y, Lu B. Acteoside, the main bioactive compound in Osmanthus fragrans flowers, palliates experimental colitis in mice by regulating the gut microbiota. J Agric Food Chem 2022; 70(4): 1148–62. doi: 10.1021/acs.jafc.1c07583

30.
Vukelić I, Detel D, Pučar LB, Potočnjak I, Buljević S, Domitrović R. Chlorogenic acid ameliorates experimental colitis in mice by suppressing signaling pathways involved in inflammatory response and apoptosis. Food Chem Toxicol 2018; 121: 140–50. doi: 10.1016/j.fct.2018.08.061

31.
Duranti S, Gaiani F, Mancabelli L, Milani C, Grandi A, Bolchi A, et al. Elucidating the gut microbiome of ulcerative colitis: bifidobacteria as novel microbial biomarkers. FEMS Microbiol Ecol 2016; 92(12): fiw191. doi: 10.1093/femsec/fiw191

32.
Khorsand B, Asadzadeh Aghdaei H, Nazemalhosseini-Mojarad E, Nadalian B, Nadalian B, Houri H. Overrepresentation of Enterobacteriaceae and Escherichia coli is the major gut microbiome signature in Crohn’s disease and ulcerative colitis; a comprehensive metagenomic analysis of IBDMDB datasets. Front Cell Infect Microbiol 2022; 12: 1015890. doi: 10.3389/fcimb.2022.1015890

33.
Larrosa M, Yañéz-Gascón MJ, Selma MV, González-Sarrías A, Toti S, Cerón JJ, et al. Effect of a low dose of dietary resveratrol on colon microbiota, inflammation and tissue damage in a DSS-induced colitis rat model. J Agric Food Chem 2009; 57(6): 2211–20. doi: 10.1021/jf803638d

34.
Atreya I, Atreya R, Neurath MF. NF-kappaB in inflammatory bowel disease. J Intern Med 2008; 263(6): 591–6. doi: 10.1111/j.1365-2796.2008.01953.x

35.
Khan WI, Motomura Y, Wang H, El-Sharkawy RT, Verdu EF, Verma-Gandhu M, et al. Critical role of MCP-1 in the pathogenesis of experimental colitis in the context of immune and enterochromaffin cells. Am J Physiol Gastrointest Liver Physiol 2006; 291(5): G803–11. doi: 10.1152/ajpgi.00069.2006
36.Bibi S, de Sousa Moraes LF, Lebow N, Zhu MJ. Dietary green pea protects against DSS-induced colitis in mice challenged with high-fat diet. Nutrients 2017; 9(5): 509. doi: 10.3390/nu9050509

37.
Yao D, Dong M, Dai C, Wu S. Inflammation and inflammatory cytokine contribute to the initiation and development of ulcerative colitis and its associated cancer. Inflamm Bowel Dis 2019; 25(10): 1595–602. doi: 10.1093/ibd/izz149

38.
Fallahi F, Borran S, Ashrafizadeh M, Zarrabi A, Pourhanifeh MH, Khaksary Mahabady M, et al. Curcumin and inflammatory bowel diseases: from in vitro studies to clinical trials. Mol Immunol 2021; 130: 20–30. doi: 10.1016/j.molimm.2020.11.016