Sanguisorba officinalis L. derived from herbal medicine prevents intestinal inflammation by inducing autophagy in macrophages.
Animals
Autophagy
/ drug effects
Colitis
/ drug therapy
Crohn Disease
/ drug therapy
Cytokines
/ metabolism
Dextran Sulfate
/ pharmacology
Epithelial Cells
/ drug effects
Female
Herbal Medicine
/ methods
Inflammation
/ drug therapy
Inflammatory Bowel Diseases
/ drug therapy
Intestines
/ drug effects
Macrophages
/ drug effects
Mice
Mice, Inbred C57BL
Microfilament Proteins
/ metabolism
Myeloid Cells
/ drug effects
Phytotherapy
/ methods
Plant Preparations
/ pharmacology
Plants, Medicinal
/ chemistry
Sanguisorba
/ chemistry
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
19 06 2020
19 06 2020
Historique:
received:
05
12
2019
accepted:
04
05
2020
entrez:
21
6
2020
pubmed:
21
6
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Disturbed activation of autophagy is implicated in the pathogenesis of inflammatory bowel disease. Accordingly, several autophagy-related genes have been identified as Crohn's disease susceptibility genes. We screened the autophagy activators from a library including 3,922 natural extracts using a high-throughput assay system. The extracts identified as autophagy activators were administered to mice with 2% dextran sodium sulfate (DSS). Among the autophagy inducers, Sanguisorba officinalis L. (SO) suppressed DSS-induced colitis. To identify the mechanism by which SO ameliorates colitis, epithelial cell and innate myeloid cells-specific Atg7-deficient mice (Villin-cre; Atg7
Identifiants
pubmed: 32561763
doi: 10.1038/s41598-020-65306-4
pii: 10.1038/s41598-020-65306-4
pmc: PMC7305163
doi:
Substances chimiques
Cytokines
0
Microfilament Proteins
0
Plant Preparations
0
villin
0
Dextran Sulfate
9042-14-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9972Références
Murakami, Y. et al. Estimated prevalence of ulcerative colitis and Crohn’s disease in Japan in 2014: an analysis of a nationwide survey. J Gastroenterol (In press) (2019).
Maaser, C. et al. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: Initial diagnosis, monitoring of known IBD, detection of complications. J Crohns Colitis 13, 144–164 (2019).
pubmed: 30137275
doi: 10.1093/ecco-jcc/jjy113
Kawai, S. et al. Indigo naturalis ameliorates murine dextran sodium sulfate-induced colitis via aryl hydrocarbon receptor activation. J Gastroenterol 52, 904–919 (2017).
pubmed: 27900483
doi: 10.1007/s00535-016-1292-z
Naganuma, M. et al. Efficacy of indigo naturalis in a multicenter randomized controlled trial of patients with ulcerative colitis. Gastroenterology 154, 935–947 (2018).
pubmed: 29174928
doi: 10.1053/j.gastro.2017.11.024
Jang, E., Inn, K. S., Jang, Y. P., Lee, K. T. & Lee, J. H. Phytotherapeutic Activities of Sanguisorba officinalis and its Chemical Constituents: A Review. Am J Chin Med 46, 299–318 (2018).
pubmed: 29433389
doi: 10.1142/S0192415X18500155
Li, Z. F. et al. A Sample and Sensitive HPLC-MS/MS Method for Simultaneous Determination of Ziyuglycoside I and Its Metabolite Ziyuglycoside II in Rat Pharmacokinetics. Molecules 23 (2018).
Chen, X. et al. Saponins from Sanguisorba officinalis Improve Hematopoiesis by Promoting Survival through FAK and Erk1/2 Activation and Modulating Cytokine Production in Bone Marrow. Front Pharmacol 8, 130 (2017).
pubmed: 28360858
pmcid: 5353277
Zhao, Z. et al. Traditional Uses, Chemical Constituents and Biological Activities of Plants from the Genus Sanguisorba L. Am J Chin Med 45, 199–224 (2017).
pubmed: 28249548
doi: 10.1142/S0192415X17500136
Liu, M. P. et al. Sanguisorba officinalis L synergistically enhanced 5-fluorouracil cytotoxicity in colorectal cancer cells by promoting a reactive oxygen species-mediated, mitochondria-caspase-dependent apoptotic pathway. Sci Rep 6, 34245 (2016).
pubmed: 27671231
pmcid: 5037464
doi: 10.1038/srep34245
Lee, H. A. et al. Catechin ameliorates Porphyromonas gingivalis-induced inflammation via the regulation of TLR2/4 and inflammasome signaling. J Periodontol (2019).
Rios, J. L., Giner, R. M., Marin, M. & Recio, M. C. A Pharmacological Update of Ellagic Acid. Planta Med 84, 1068–1093 (2018).
pubmed: 29847844
doi: 10.1055/a-0633-9492
Dludla, P. V. et al. Inflammation and Oxidative Stress in an Obese State and the Protective Effects of Gallic Acid. Nutrients 11 (2018).
Kim, Y. H. et al. Anti-wrinkle activity of ziyuglycoside I isolated from a Sanguisorba officinalis root extract and its application as a cosmeceutical ingredient. Biosci Biotechnol Biochem 72, 303–311 (2008).
pubmed: 18256460
doi: 10.1271/bbb.70268
Kabeya, Y. et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo j 19, 5720–5728 (2000).
pubmed: 11060023
pmcid: 305793
doi: 10.1093/emboj/19.21.5720
Tanida, I. et al. Apg7p/Cvt2p: A novel protein-activating enzyme essential for autophagy. Mol Biol Cell 10, 1367–1379 (1999).
pubmed: 10233150
pmcid: 25280
doi: 10.1091/mbc.10.5.1367
Hampe, J. et al. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet 39, 207–211 (2007).
pubmed: 17200669
doi: 10.1038/ng1954
Muzes, G., Tulassay, Z. & Sipos, F. Interplay of autophagy and innate immunity in Crohn’s disease: A key immunobiologic feature. World J Gastroenterol 19, 4447–4454 (2013).
pubmed: 23901219
pmcid: 3725368
doi: 10.3748/wjg.v19.i28.4447
Harley, J. B. et al. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542, and other loci. Nat Genet 40, 204–210 (2008).
pubmed: 18204446
pmcid: 3712260
doi: 10.1038/ng.81
Gateva, V. et al. A large-scale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1, and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 41, 1228–1233 (2009).
pubmed: 19838195
pmcid: 2925843
doi: 10.1038/ng.468
Lin, N. Y. et al. Autophagy regulates TNFalpha-mediated joint destruction in experimental arthritis. Ann Rheum Dis 72, 761–768 (2013).
pubmed: 22975756
doi: 10.1136/annrheumdis-2012-201671
Ogura, Y. et al. Expression of NOD2 in Paneth cells: a possible link to Crohn’s ileitis. Gut 52, 1591–1597 (2003).
pubmed: 14570728
pmcid: 1773866
doi: 10.1136/gut.52.11.1591
Wehkamp, J. et al. NOD2 (CARD15) mutations in Crohn’s disease are associated with diminished mucosal alpha-defensin expression. Gut 53, 1658–1664 (2004).
pubmed: 15479689
pmcid: 1774270
doi: 10.1136/gut.2003.032805
Liu, T. C. et al. LRRK2 but not ATG16L1 is associated with Paneth cell defect in Japanese Crohn’s disease patients. JCI Insight 2, e91917 (2017).
pubmed: 28352666
pmcid: 5358495
doi: 10.1172/jci.insight.91917
Saitoh, T. et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456, 264–268 (2008).
pubmed: 18849965
doi: 10.1038/nature07383
pmcid: 18849965
Macias-Ceja, D. C., Cosin-Roger, J., Ortiz-Masia, D., Salvador, P. & Hernandez, C. Stimulation of autophagy prevents intestinal mucosal inflammation and ameliorates murine colitis. Br J Pharmacol 174, 2501–2511 (2017).
pubmed: 28500644
pmcid: 5513861
doi: 10.1111/bph.13860
Asano, J. et al. Intrinsic autophagy is required for the maintenance of intestinal stem cells and for irradiation-induced intestinal regeneration. Cell Rep 20, 1050–1060 (2017).
pubmed: 28768191
doi: 10.1016/j.celrep.2017.07.019
Pott, J., Kabat, A. M. & Maloy, K. J. Intestinal epithelial cell autophagy is required to protect against TNF-induced apoptosis during chronic colitis in Mice. Cell Host Microbe 23, 191–202.e194 (2018).
pubmed: 29358084
doi: 10.1016/j.chom.2017.12.017
Shakeri, A. & Cicero, A. F. G. Curcumin: A naturally occurring autophagy modulator. J Cell Physiol 234, 5643–5654 (2019).
pubmed: 30239005
doi: 10.1002/jcp.27404
Li, X. et al. Curcumin inhibits apoptosis of chondrocytes through activation ERK1/2 signaling pathways induced autophagy. Nutrients 9 (2017).
Guo, S. et al. Curcumin activates autophagy and attenuates oxidative damage in EA.hy926 cells via the Akt/mTOR pathway. Mol Med Rep 13, 2187–2193 (2016).
pubmed: 26781771
doi: 10.3892/mmr.2016.4796
Lee, Y. J., Kim, N. Y., Suh, Y. A. & Lee, C. Involvement of ROS in curcumin-induced autophagic cell death. Korean J Physiol Pharmacol 15, 1–7 (2011).
pubmed: 21461234
pmcid: 3062078
doi: 10.4196/kjpp.2011.15.1.1
Zhao, J. et al. Celastrol ameliorates experimental colitis in IL-10 deficient mice via the up-regulation of autophagy. Int Immunopharmacol 26, 221–228 (2015).
pubmed: 25858875
doi: 10.1016/j.intimp.2015.03.033
Ueno, A., Ghosh, A., Hung, D., Li, J. & Jijon, H. Th17 plasticity and its changes associated with inflammatory bowel disease. World J Gastroenterol 21, 12283–12295 (2015).
pubmed: 26604637
pmcid: 4649113
doi: 10.3748/wjg.v21.i43.12283
Soukou, S. et al. Role of IL-10 Receptor Signaling in the Function of CD4+ T-Regulatory Type 1 cells: T-Cell Therapy in Patients with Inflammatory Bowel Disease. Crit Rev Immunol 38, 415–431 (2018).
pubmed: 30806217
doi: 10.1615/CritRevImmunol.2018026850
Bain, C. C. et al. Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol 6, 498–510 (2013).
pubmed: 22990622
doi: 10.1038/mi.2012.89
Wolf, Y., Yona, S., Kim, K. W. & Jung, S. Microglia, seen from the CX3CR1 angle. Front Cell Neurosci 7, 26 (2013).
pubmed: 23507975
pmcid: 3600435
doi: 10.3389/fncel.2013.00026
Bao, Y. & Cao, X. The immune potential and immunopathology of cytokine-producing B cell subsets: a comprehensive review. J Autoimmun 55, 10–23 (2014).
pubmed: 24794622
doi: 10.1016/j.jaut.2014.04.001
Sun, M., He, C., Cong, Y. & Liu, Z. Regulatory immune cells in regulation of intestinal inflammatory response to microbiota. Mucosal Immunol 8, 969–978 (2015).
pubmed: 26080708
pmcid: 4540654
doi: 10.1038/mi.2015.49
Torchinsky, M. B. & Blander, J. M. T helper 17 cells: discovery, function, and physiological trigger. Cell Mol Life Sci 67, 1407–1421 (2010).
pubmed: 20054607
doi: 10.1007/s00018-009-0248-3
Singh, S. B., Wilson, M., Ritz, N. & Lin, H. C. Autophagy genes of host responds to disruption of gut microbial community by antibiotics. Dig Dis Sci 62, 1486–1497 (2017).
pubmed: 28466260
doi: 10.1007/s10620-017-4589-8
Nighot, P. K., Hu, C. A. & Ma, T. Y. Autophagy enhances intestinal epithelial tight junction barrier function by targeting claudin-2 protein degradation. J Biol Chem 290, 7234–7246 (2015).
pubmed: 25616664
pmcid: 4358142
doi: 10.1074/jbc.M114.597492
Lee, H. Y. et al. Autophagy deficiency in myeloid cells increases susceptibility to obesity-induced diabetes and experimental colitis. Autophagy 12, 1390–1403 (2016).
pubmed: 27337687
pmcid: 4968230
doi: 10.1080/15548627.2016.1184799
Ohashi, W., Hattori, K. & Hattori, Y. Control of macrophage dynamics as a potential therapeutic approach for clinical disorders involving chronic inflammation. J Pharmacol Exp Ther 354, 240–250 (2015).
pubmed: 26136420
doi: 10.1124/jpet.115.225540
Kamada, N. et al. Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-gamma axis. J Clin Invest 118, 2269–2280 (2008).
pubmed: 18497880
pmcid: 2391067
Wittkopf, N. et al. Lack of intestinal epithelial atg7 affects paneth cell granule formation but does not compromise immune homeostasis in the gut. Clin Dev Immunol 2012, 278059 (2012).
pubmed: 22291845
pmcid: 3265132
doi: 10.1155/2012/278059
Tsuboi, K. et al. Autophagy protects against colitis by the maintenance of normal gut microflora and secretion of mucus. J Biol Chem 290, 20511–20526 (2015).
pubmed: 26149685
pmcid: 4536456
doi: 10.1074/jbc.M114.632257
Pan, X. H. et al. Mechanism and therapeutic effect of umbilical cord mesenchymal stem cells in inflammatory bowel disease. Sci Rep 9, 17646 (2019).
pubmed: 31776475
pmcid: 6881332
doi: 10.1038/s41598-019-54194-y
Nishida, Y. et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461, 654–658 (2009).
pubmed: 19794493
doi: 10.1038/nature08455
Enderlin Vaz da Silva, Z., Lehr, H. A. & Velin, D. In vitro and in vivo repair activities of undifferentiated and classically and alternatively activated macrophages. Pathobiology 81, 86–93 (2014).
pubmed: 24457836
doi: 10.1159/000357306
Liu, K. et al. Impaired macrophage autophagy increases the immune response in obese mice by promoting proinflammatory macrophage polarization. Autophagy 11, 271–284 (2015).
pubmed: 25650776
pmcid: 4502775
doi: 10.1080/15548627.2015.1009787
Kang, Y. H. et al. Impaired macrophage autophagy induces systemic insulin resistance in obesity. Oncotarget 7, 35577–35591 (2016).
pubmed: 27229537
pmcid: 5094946
doi: 10.18632/oncotarget.9590
Sanjurjo, L. et al. CD5L Promotes M2 Macrophage Polarization through Autophagy-Mediated Upregulation of ID3. Front Immunol 9, 480 (2018).
pubmed: 29593730
pmcid: 5858086
doi: 10.3389/fimmu.2018.00480
Krause, P. et al. IL-10-producing intestinal macrophages prevent excessive antibacterial innate immunity by limiting IL-23 synthesis. Nature Commun. 6, 7055 (2015).
doi: 10.1038/ncomms8055
Shouval, D. S. et al. Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity 40, 706–719 (2014).
pubmed: 24792912
pmcid: 4513358
doi: 10.1016/j.immuni.2014.03.011
Zigmond, E. et al. Macrophage-restricted interleukin-10 receptor deficiency, but not IL-10 deficiency, causes severe spontaneous colitis. Immunity 40, 720–733 (2014).
pubmed: 24792913
doi: 10.1016/j.immuni.2014.03.012
Murai, M. et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol 10, 1178–1184 (2009).
pubmed: 19783988
pmcid: 2898179
doi: 10.1038/ni.1791
Nonaka, G., Tanaka, T. & Nishioka, I. Tannins and related compounds. Part3. A new phenolic acid, sanguisorbic acid dilactone and three new ellagtannins, sanguiins H-1, H-2 and H-3, from Sanguisorba officinalis. J. Chem Society, Perkin Transactions 1: Org. Bio-Org. Chem., 1067–1073 (1982).
Tanaka, T., Nonaka, G. & Nishioka, I. Tannins and related compounds. Part 28. Revision of the structure of sanguiins H-6, H-2, and H-3, and isolation and characterization of sanguiin H-11, a noveltetrameric hydrolyzable tannin and isolation, and seven related tannins, from Sanguisorba officinalis. J chem Res, 176–177 (1985).
Konishi, K., Urada, M., Adachi, I. & Tanaka, T. Inhibitory effect of sanguiin H-11 on chemotaxis of neutrophil. Biol Pharm Bull 23, 213–218 (2000).
pubmed: 10706387
doi: 10.1248/bpb.23.213
Li, W. et al. A tannin compound from Sanguisorba officinalis blocks Wnt/beta-catenin signaling pathway and induces apoptosis of colorectal cancer cells. Chin Med 14, 22 (2019).
pubmed: 31164916
pmcid: 6544925
doi: 10.1186/s13020-019-0244-y
Kamada, N. et al. Abnormally differentiated subsets of intestinal macrophage play a key role in Th1-dominant chronic colitis through excess production of IL-12 and IL-23 in response to bacteria. J Immunol 175, 6900–6908 (2005).
pubmed: 16272349
doi: 10.4049/jimmunol.175.10.6900
Hausmann, M. et al. In vivo treatment with the herbal phenylethanoid acteoside ameliorates intestinal inflammation in dextran sulphate sodium-induced colitis. Clin Exp Immunol 148, 373–381 (2007).
pubmed: 17437425
pmcid: 1868873
doi: 10.1111/j.1365-2249.2007.03350.x
Atarashi, K. et al. ATP drives lamina propria T(H)17 cell differentiation. Nature 455, 808–812 (2008).
pubmed: 18716618
doi: 10.1038/nature07240