Natural compound methyl protodioscin protects against intestinal inflammation through modulation of intestinal immune responses

Pharmacology Research and Perspectives

Volumn 3, Issue 2, 2015, Pages

  Zhang, Rongli ^b   Gilbert, Shila ^a   Yao, Xinsheng ^c   Vallance, Jefferson ^a   Steinbrecher, Kris ^a   Moriggl, Richard ^e   Zhang, Dongsheng ^a   Eluri, Madhu ^a   Chen, Haifeng ^d   Cao, Huiqing ^b   Shroyer, Noah ^a   Denson, Lee ^a   Han, Xiaonan ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b PEKING UNIVERSITY   (China)

^c JINAN UNIVERSITY   (China)

^d XIAMEN UNIVERSITY   (China)

^e UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Colitis; Inflammatory bowel diseases (IBD); Intestinal barrier function; Intestinal stem cells; Methyl protodioscin (MPD); Traditional chinese herbal (TCH)

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHYL PROTODIOSCIN; PLANT EXTRACT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL TRANSLOCATION; CELL INFILTRATION; CHINESE MEDICINE; COLITIS; CONTROLLED STUDY; ENTERITIS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOFLUORESCENCE TEST; INFLAMMATORY BOWEL DISEASE; LAMINA PROPRIA; MESENTERY LYMPH NODE; MICROSCOPY; MODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SCORING SYSTEM; WESTERN BLOTTING;

EID: 84990067243     PISSN: None     EISSN: 20521707     Source Type: Journal    
DOI: 10.1002/prp2.118     Document Type: Article

References (65)

1. Aguilera C, Nakagawa K, Sancho R, Chakraborty A, Hendrich B, Behrens A (2011). c-Jun N-terminal phosphorylation antagonises recruitment of the Mbd3/NuRD repressor complex. Nature 469: 231-235.
2. Al-Sadi R, Ye D, Dokladny K, Ma TY (2008). Mechanism of IL-1beta-induced increase in intestinal epithelial tight junction permeability. J Immunol 180: 5653-5661.
3. Andres PG, Friedman LS (1999). Epidemiology and the natural course of inflammatory bowel disease. Gastroenterol Clin North Am 28:255-281, vii.
4. Biteau B, Hochmuth CE, Jasper H (2011). Maintaining tissue homeostasis: dynamic control of somatic stem cell activity. Cell Stem Cell 9: 402-411.
5. Blair SA, Kane SV, Clayburgh DR, Turner JR (2006). Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease. Lab Invest 86: 191-201.
6. Boivin MA, Roy PK, Bradley A, Kennedy JC, Rihani T, Ma TY (2009). Mechanism of interferon-gamma-induced increase in T84 intestinal epithelial tight junction. J Interferon Cytokine Res 29: 45-54.
7. Bouma G, Strober W (2003). The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol 3: 521-533.
8. Cao X, Yao Z, Chen H, Dai Y, Sun P, Ye W, et al. (2008). Development and validation of a liquid chromatography/tandem mass spectrometry assay for the quantification of methyl protodioscin in rat plasma: application to a pharmacokinetic study. Biomed Chromatogr 22: 408-413.
9. Cao X, Yao Z, Shao M, Chen H, Ye W, Yao X (2010). Pharmacokinetics of methyl protodioscin in rats. Pharmazie 65: 359-362.
10. Cheng MS, Wang QL, Tian Q, Song HY, Liu YX, Li Q, et al. (2003). Total synthesis of methyl protodioscin: a potent agent with antitumor activity. J Org Chem 68: 3658-3662.
11. Chong KT, Xiang L, Wang X, Jun EL, Xi LF, Schweinfurth JM (2006). High level expression of human epithelial beta-defensins (hBD-1, 2 and 3) in papillomavirus induced lesions. Virol J 3: 75.
12. Cooper HS, Murthy SN, Shah RS, Sedergran DJ (1993). Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Labor Invest 69: 238-249.
13. Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B (2007). Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 8: 1086-1094.
14. Fichtner-Feigl S, Fuss IJ, Preiss JC, Strober W, Kitani A (2005). Treatment of murine Th1- and Th2-mediated inflammatory bowel disease with NF-kappa B decoy oligonucleotides. J Clin Investig 115: 3057-3071.
15. Fiocchi C (1998). Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 115: 182-205.
16. Flynn AN, Buret AG (2008). Tight junctional disruption and apoptosis in an in vitro model of Citrobacter rodentium infection. Microb Pathog 45: 98-104.
17. Gilbert S, Zhang R, Denson L, Moriggl R, Steinbrecher K, Shroyer N, et al. (2012). Enterocyte STAT5 promotes mucosal wound healing via suppression of myosin light chain kinase-mediated loss of barrier function and inflammation. EMBO Mol Med 4: 109-124.
18. Grossman AB, Baldassano RN (2008). Specific considerations in the treatment of pediatric inflammatory bowel disease. Expert Rev Gastroenterol Hepatol 2: 105-124.
19. Han X, Uchiyama T, Sappington PL, Yaguchi A, Yang R, Fink MP, et al. (2003). NAD+ ameliorates inflammation-induced epithelial barrier dysfunction in cultured enterocytes and mouse ileal mucosa. J Pharmacol Exp Ther 307: 443-449.
20. Han X, Fink MP, Yang R, Delude RL (2004). Increased iNOS activity is essential for intestinal epithelial tight junction dysfunction in endotoxemic mice. Shock 21: 261-270.
21. Han X, Sosnowska D, Bonkowski EL, Denson LA (2005). Growth hormone inhibits signal transducer and activator of transcription 3 activation and reduces disease activity in murine colitis. Gastroenterology 129: 185-203.
22. Han X, Ren X, Jurickova I, Groschwitz K, Pasternak BA, Xu H, et al. (2009). Regulation of intestinal barrier function by signal transducer and activator of transcription 5b. Gut 58: 49-58.
23. Han X, Gilbert S, Groschwitz K, Hogan S, Jurickova I, Trapnell B, et al. (2010). Loss of GM-CSF signalling in non-haematopoietic cells increases NSAID ileal injury. Gut 59: 1066-1078.
24. Hanauer SB (2007). Risks and benefits of combining immunosuppressives and biological agents in inflammatory bowel disease: is the synergy worth the risk? Gut 56: 1181-1183.
25. He X, Qiao A, Wang X, Liu B, Jiang M, Su L, et al. (2006). Structural identification of methyl protodioscin metabolites in rats' urine and their antiproliferative activities against human tumor cell lines. Steroids 71: 828-833.
26. Hilsden RJ, Scott CM, Verhoef MJ (1998). Complementary medicine use by patients with inflammatory bowel disease. Am J Gastroenterol 93: 697-701.
27. Hogan SP, Seidu L, Blanchard C, Groschwitz K, Mishra A, Karow ML, et al. (2006). Resistin-like molecule beta regulates innate colonic function: barrier integrity and inflammation susceptibility. J Allergy Clin Immunol 118: 257-268.
28. Hooper LV, Littman DR, Macpherson AJ (2012). Interactions between the microbiota and the immune system. Science 336: 1268-1273.
29. Hu K, Yao X (2003). The cytotoxicity of methyl protodioscin against human cancer cell lines in vitro. Cancer Invest 21: 389-393.
30. Hu K, Dong A, Yao X, Kobayashi H, Iwasaki S (1997). Antineoplastic agents. II. Four furostanol glycosides from rhizomes of Dioscorea collettii var. hypoglauca. Planta Med 63: 161-165.
31. Komesaroff PA, Black CV, Cable V, Sudhir K (2001). Effects of wild yam extract on menopausal symptoms, lipids and sex hormones in healthy menopausal women. Climacteric 4: 144-150.
32. Langmead L, Rampton DS (2006). Review article: complementary and alternative therapies for inflammatory bowel disease. Aliment Pharmacol Ther 23: 341-349.
33. Liu MJ, Yue PY, Wang Z, Wong RN (2005). Methyl protodioscin induces G2/M arrest and apoptosis in K562 cells with the hyperpolarization of mitochondria. Cancer Lett 224: 229-241.
34. Liu J, Walker NM, Cook MT, Ootani A, Clarke LL (2012). Functional Cftr in crypt epithelium of organotypic enteroid cultures from murine small intestine. Am J Physiol Cell Physiol 302: C1492-C1503.
35. Maloy KJ, Powrie F (2011). Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474: 298-306.
36. Mann EA, Harmel-Laws E, Cohen MB, Steinbrecher KA (2013). Guanylate cyclase C limits systemic dissemination of a murine enteric pathogen. BMC Gastroenterol 13: 135.
37. Medzhitov R (2007). Recognition of microorganisms and activation of the immune response. Nature 449: 819-826.
38. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S (2005). Citrobacter rodentium of mice and man. Cell Microbiol 7: 1697-1706.
39. Munitz A, Cole ET, Beichler A, Groschwitz K, Ahrens R, Steinbrecher K, et al. (2010). Paired immunoglobulin-like receptor B (PIR-B) negatively regulates macrophage activation in experimental colitis. Gastroenterology 139: 530-541.
40. Neurath MF, Fuss I, Schurmann G, Pettersson S, Arnold K, Muller-Lobeck H, et al. (1998). Cytokine gene transcription by NF-kappa B family members in patients with inflammatory bowel disease. Ann N Y Acad Sci 859: 149-159.
41. Ning Z, Li Y, Zhang R (2010). [Effects of methyl protodioscin on [Ca2+]i and ATPase activity in cardiomyocytes and analysis of mechanisms]. China journal of Chinese materia medica 35: 80-83.
42. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R (1990). A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98: 694-702.
43. Pereira B, Sousa S, Barros R, Carreto L, Oliveira P, Oliveira C, et al. (2013). CDX2 regulation by the RNA-binding protein MEX3A: impact on intestinal differentiation and stemness. Nucleic Acids Res 41: 3986-3999.
44. Peterson LW, Artis D (2014). Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14: 141-153.
45. Peyrin-Biroulet L, Beisner J, Wang G, Nuding S, Oommen ST, Kelly D, et al. (2010). Peroxisome proliferator-activated receptor gamma activation is required for maintenance of innate antimicrobial immunity in the colon. Proc Natl Acad Sci USA 107: 8772-8777.
46. Pollok RC, Farthing MJ, Bajaj-Elliott M, Sanderson IR, McDonald V (2001). Interferon gamma induces enterocyte resistance against infection by the intracellular pathogen Cryptosporidium parvum. Gastroenterology 120: 99-107.
47. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, Amir E, et al. (2010). Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11: 76-83.
48. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, et al. (2009). Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265.
49. Sato T, Stange DE, Ferrante M, Vries RG, vanEs JH, vanden Brink S, et al. (2011). Long-term Expansion of Epithelial Organoids From Human Colon, Adenoma, Adenocarcinoma, and Barrett's Epithelium. Gastroenterology 141: 1762-1772.
50. Schmidt C, Peng B, Li Z, Sclabas GM, Fujioka S, Niu J, et al. (2003). Mechanisms of proinflammatory cytokine-induced biphasic NF-kappaB activation. Mol Cell 12: 1287-1300.
51. Schreiber S, Nikolaus S, Hampe J (1998). Activation of nuclear factor kappa B inflammatory bowel disease. Gut 42: 477-484.
52. Scott ML, Fujita T, Liou HC, Nolan GP, Baltimore D (1993). The p65 subunit of NF-kappa B regulates I kappa B by two distinct mechanisms. Genes Dev 7: 1266-1276.
53. Spence JR, Mayhew CN, Rankin SA, Kuhar MF, Vallance JE, Tolle K, et al. (2011). Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470: 105-109.
54. Strober W, Fuss I, Mannon P (2007). The fundamental basis of inflammatory bowel disease. J Clin Investig 117: 514-521.
55. Su L, Shen L, Clayburgh DR, Nalle SC, Sullivan EA, Meddings JB, et al. (2009). Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology 136: 551-563.
56. Tak PP, Firestein GS (2001). NF-kappaB: a key role in inflammatory diseases. J Clin Investig 107: 7-11.
57. Turner JR (2009). Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9: 799-809.
58. Ulbricht C, Basch E, Ulbricht C, Sollars D, Hammerness P, Hashmi S (2003). Wild yam (Dioscoreaceae). J Herb Pharmacother 3: 77-91.
59. Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O, et al. (2011). The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334: 255-258.
60. Villarino AV, Artis D, Bezbradica JS, Miller O, Saris CJ, Joyce S, et al. (2008). IL-27R deficiency delays the onset of colitis and protects from helminth-induced pathology in a model of chronic IBD. Int Immunol 20: 739-752.
61. Wang F, Graham WV, Wang Y, Witkowski ED, Schwarz BT, Turner JR (2005). Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am J Pathol 166: 409-419.
62. Xavier RJ, Podolsky DK (2007). Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.
63. Yin J, Tezuka Y, Kouda K, Le Tran Q, Miyahara T, Chen Y, et al. (2004). In vivo antiosteoporotic activity of a fraction of Dioscorea spongiosa and its constituent, 22-O-methylprotodioscin. Planta Med 70: 220-226.
64. Yin X, Farin HF, van Es JH, Clevers H, Langer R, Karp JM (2014). Niche-independent high-purity cultures of Lgr5+ intestinal stem cells and their progeny. Nat Methods 11: 106-112.
65. Zandi E, Rothwarf DM, Delhase M, Hayakawa M, Karin M (1997). The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell 91: 243-252.