The Anti-atherosclerotic Dipeptide, Trp-His, Reduces Intestinal Inflammation through the Blockade of L-Type Ca2+ Channels

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 26, 2015, Pages 6041-6050

  Kobayashi, Yutaro ^a,b   Kovacs Nolan, Jennifer ^a   Matsui, Toshiro ^b   Mine, Yoshinori ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

dextran sodium sulfate; dipeptide; inflammatory bowel disease; intestinal epithelial cell; L type Ca2+ channels; Trp His

Indexed keywords

CELLS; DEXTRAN; PATHOLOGY; PEPTIDES; SODIUM SULFATE; SULFUR COMPOUNDS;

DI-PEPTIDES; INFLAMMATORY BOWEL DISEASE; INTESTINAL EPITHELIAL CELLS; L-TYPE CA^2+ CHANNELS; TRP-HIS;

DISEASES;

MUS;

ANTIINFLAMMATORY AGENT; CALCIUM CHANNEL L TYPE; DIPEPTIDE; INTERLEUKIN 8; TRYPTOPHYL-HISTIDINE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASES; INTESTINE; MOUSE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CALCIUM CHANNELS, L-TYPE; DIPEPTIDES; FEMALE; HUMANS; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-8; INTESTINES; MICE; MICE, INBRED BALB C; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84936806762     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b01682     Document Type: Article

References (44)

1. Macdermott, R. Alterations of the mucosal immune system in inflammatory bowel disease J. Gastroenterol. 1996, 31, 907-916 10.1007/BF02358624
2. Calder, P. C.; Albers, R.; Antoine, J. M.; Blum, S.; Bourdet-Sicard, R.; Ferns, G. A.; Folkerts, G.; Friedmann, P. S.; Frost, G. S.; Guarner, F.; Lovik, M.; Macfarlane, S.; Meyer, P. D.; M'Rabet, L.; Serafini, M.; Eden, W. V.; Loo, J. V.; Dias, W. V.; Virdy, S.; Winklhofer-Roob, B. M.; Zhao, J. Inflammatory disease processes and interactions with nutrition Br. J. Nutr. 2009, 101, S1-S45 10.1017/S0007114509377867
3. Gentschew, L.; Ferguson, L. R. Role of nutrition and microbiota in susceptibility to inflammatory bowel diseases Mol. Nutr. Food Res. 2012, 56, 524-535 10.1002/mnfr.201100630
4. Pithadia, A. B.; Jain, S. Treatment of inflammatory bowel disease (IBD) Pharmacol. Rep. 2011, 63, 629-642 10.1016/S1734-1140(11)70575-8
5. Stallmach, A.; Hagel, S.; Bruns, T. Adverse effects of biologics used for treating IBD Best Pract. Res. Clin. Gastroenterol. 2010, 24, 167-182 10.1016/j.bpg.2010.01.002
6. Lee, M.; Kovacs-Nolan, J.; Yang, C.; Archbold, T.; Fan, M. Z.; Mine, Y. Hen egg lysozyme attenuates inflammation and modulates local gene expression in a porcine model of dextran sodium sulfate (DSS)-induced colitis J. Agric. Food Chem. 2009, 57, 2233-2240 10.1021/jf803133b
7. Kobayashi, Y.; Rupa, P.; Kovacs-Nolan, J.; Turner, P. V.; Matsui, T.; Mine, Y. Oral administration of hen egg white ovotransferrin attenuates the development of colitis induced by dextran sodium sulfate in mice J. Agric. Food Chem. 2015, 63, 1532-1539 10.1021/jf505248n
8. Young, D.; Ibuki, M.; Nakamori, T.; Fan, M.; Mine, Y. Soy-derived di- and tripeptides alleviate colon and ileum inflammation in pigs with dextran sodium sulfate-induced colitis J. Nutr. 2012, 142, 363-368 10.3945/jn.111.149104
9. Kovacs-Nolan, J.; Zhang, H.; Ibuki, M.; Nakamori, T.; Yoshiura, K.; Turner, P. V.; Matsui, T.; Mine, Y. The PepT1-transportable soy tripeptide VPY reduces intestinal inflammation Biochim. Biophys. Acta, Gen. Subj. 2012, 1820, 1753-1763 10.1016/j.bbagen.2012.07.007
10. Wada, S.; Sato, K.; Ohta, R.; Wada, E.; Bou, Y.; Fujiwara, M.; Kiyono, T.; Park, E. Y.; Aoi, W.; Takagi, T.; Nito, Y.; Yoshikawa, T. Ingestion of low dose pyroglutamyl leucine improves dextran sulfate sodium-induced colitis and intestinal microbiota in mice J. Agric. Food Chem. 2013, 61, 8807-8813 10.1021/jf402515a
11. Shi, Y.; Rupa, P.; Jiang, B.; Mine, Y. Hydrolysate from eggshell membrane ameliorates intestinal inflammation in mice Int. J. Mol. Sci. 2014, 15, 22728-22742 10.3390/ijms151222728
12. Zhang, H.; Kovacs-Nolan, J.; Kodera, T.; Eto, Y.; Mine, Y. γ-Glutamyl cysteine and γ-glutamyl valine inhibit TNF-α signaling in intestinal epithelial cells and reduce inflammation in a mouse model of colitis via allosteric activation of the calcium-sensing receptor Biochim. Biophys. Acta, Mol. Basis Dis. 2015, 1852, 792-804 10.1016/j.bbadis.2014.12.023
13. Kim, C. J.; Kovacs-Nolan, J.; Yang, C.; Archbold, T.; Fan, M. Z.; Mine, Y. l -Cysteine supplementation attenuates local inflammation and restores gut homeostasis in a porcine model of colitis Biochim. Biophys. Acta, Gen. Subj. 2009, 1790, 1161-1169 10.1016/j.bbagen.2009.05.018
14. Kim, C. J.; Kovacs-Nolan, J.; Yang, C.; Archbold, T.; Fan, M. Z.; Mine, Y. l -Tryptophan exhibits therapeutic function in a porcine model of dextran sodium sulfate (DSS)-induced colitis J. Nutr. Biochem. 2010, 21, 468-475 10.1016/j.jnutbio.2009.01.019
15. Tanaka, M.; Hong, S. M.; Akiyama, S.; Hu, Q. Q.; Matsui, T. Visualized absorption of anti-atherosclerotic dipeptide, Trp-His, in Sprague-Dawley rats by LC-MS and MALDI-MS imaging analyses Mol. Nutr. Food Res. 2015, n/a 10.1002/mnfr.201500075
16. Matsui, T.; Sato, M.; Tanaka, M.; Yamada, Y.; Watanabe, S.; Fujimoto, Y.; Imaizumi, K.; Matsumoto, K. Vasodilating dipeptide Trp-His can prevent atherosclerosis in Apo E-deficient mice Br. J. Nutr. 2010, 103, 309-313 10.1017/S0007114509991814
17. Hansson, G. K. Inflammation, atherosclerosis, and coronary artery disease N. Engl. J. Med. 2005, 352, 1685-1695 10.1056/NEJMra043430
18. 2+ channels Peptides 2010, 31, 2060-2066 10.1016/j.peptides.2010.07.013
19. 2+ channels in rat vascular smooth muscle cells FEBS Open Bio 2012, 2, 83-88 10.1016/j.fob.2012.04.005
20. Bang, L.; Chapman, T.; Goa, K. Lercanidipine: a review of its efficacy in the management of hypertension Drugs 2003, 63, 2449-2472 10.2165/00003495-200363220-00013
21. Wang, X. T.; Nagaba, Y.; Cross, H. S.; Wrba, F.; Zhang, L.; Guggino, S. E. The mRNA of L-type calcium channel elevated in colon cancer: protein distribution in normal and cancerous colon Am. J. Pathol. 2000, 157, 1549-1562 10.1016/S0002-9440(10)64792-X
22. 2+ channels inhibits T cell cytokine production and T-box transcription factor T-bet in inflammatory bowel disease J. Immunol. 2009, 183, 3454-3462 10.4049/jimmunol.0802887
23. Maxwell, J. R.; Brown, W. A.; Smith, C. L.; Byrne, F. R.; Viney, J. L. Methods of inducing inflammatory bowel disease in mice Curr. Protoc. Pharmacol. 2009, 47, 5.58.1-5.58.37 10.1002/0471141755.ph0558s47
24. δ δCt method Methods 2001, 25, 402-408 10.1006/meth.2001.1262
25. Katayama, S.; Xu, X.; Fan, M. Z.; Mine, Y. Antioxidative stress activity of oiligophosphopeptides derived from hen egg yolk phosvitin in Caco-2 cells J. Agric. Food Chem. 2006, 54, 773-778 10.1021/jf052280d
26. Okayasu, I.; Hatakeyama, S.; Yamada, M.; Ohkusa, T.; Inagaki, Y.; Nakaya, R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice Gastroenterology 1990, 98, 694-702
27. Eckmann, L.; Jung, H. C.; Schurer-Maly, C.; Panja, A.; Morzycka-wroblewska, E.; Kagnoff, M. Differential cytokine expression by human intestinal epithelial cell lines: regulated expression of interleukin 8 Gastroenterology 1993, 105, 1689-1697
28. Russo, M. P.; Bennett, B. L.; Manning, A. M.; Brenner, D. A.; Jobin, C. Differential requirement for NF-κB-inducing kinase in the induction of NF-κB by IL-1β, TNF-α, and Fas Am. J. Physiol.-Cell Physiol. 2002, 283, C347-C357 10.1152/ajpcell.00166.2001
29. Reimund, J. M.; Wittersheim, C.; Dumont, S.; Muller, C. D.; Baumann, R.; Poindron, P.; Duclos, B. mucosal inflammatory cytokine production by intestinal biopsies in patients with ulcerative colitis and Crohn's disease J. Clin. Immunol. 1996, 16, 144-150 10.1007/BF01540912
30. Wang, F.; Schwarz, B. T.; Graham, W. V.; Wang, Y.; Su, L.; Clayburgh, D. R.; Abraham, C.; Turner, J. R. IFN-γ-induced TNFR2 expression is required for TNF-dependent intestinal epithelial barrier dysfunction Gastroenterology 2006, 131, 1153-1163 10.1053/j.gastro.2006.08.022
31. Khan, W. I.; Motomura, Y.; Wang, H.; El-Sharkawy, R. T.; Verdu, E. F.; Verma-Gandhu, M.; Rollins, B. J.; Collins, S. M. 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, G803-G811 10.1152/ajpgi.00069.2006
32. Rousset, M. The human colon carcinoma cell lines HT-29 and Caco-2: two in vitro models for the study of intestinal differentiation Biochimie 1986, 68, 1035-1040 10.1016/S0300-9084(86)80177-8
33. Jung, H. C.; Eckmann, L.; Yang, S. K.; Panja, A.; Fierer, J.; Morzycka-Wroblewska, E.; Kagnoff, M. F. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion J. Clin. Invest. 1995, 95, 55-65 10.1172/JCI117676
34. Cho, E. J.; Shin, J. S.; Chung, K. S.; Lee, Y. S.; Cho, Y. W.; Baek, N. I.; Chung, H. G.; Lee, K. T. Arvelexin inhibits colonic inflammation by suppression of NF-κB activation in dextran sulfate sodium-induced mice and TNF-α-induced colonic epithelial cells J. Agric. Food Chem. 2012, 60, 7398-7407 10.1021/jf3009553
35. Zawadzki, A.; Liu, Q.; Wang, Y.; Melander, A.; Jeppsson, B.; Thorlacius, H. Verapamil inhibits L-type calcium channel mediated apoptosis in human colon cancer cells Dis. Colon Rectum 2008, 51, 1696-1702 10.1007/s10350-008-9372-7
36. Yu, Y.; De Waele, C.; Chadee, K. Calcium-dependent interleukin-8 gene expression in T84 human colonic epithelial cells Inflammation Res. 2001, 50, 220-226 10.1007/s000110050747
37. Zahradnikova, A.; Minarovic, I.; Zahradnik, I. Competitive and cooperative effects of Bay K 8644 on the L-type calcium channel current inhibition by calcium channel antagonists J. Pharmacol. Exp. Ther. 2007, 322, 638-645 10.1124/jpet.107.122176
38. Jijon, H. B.; Panenka, W. J.; Madsen, K. L.; Parsons, H. G. MAP kinases contribute to IL-8 secretion by intestinal epithelial cells via a posttranscriptional mechanism Am. J. Physiol. Cell Physiol. 2002, 283, C31-C41 10.1152/ajpcell.00113.2001
39. Rodríguez-Ramiro, I.; Ramos, S.; López-Oliva, E.; Agis-Torres, A.; Bravo, L.; Goya, L.; Martín, M. A. Cocoa polyphenols prevent inflammation in the colon of azoxymethane-treated rats and in TNF-α-stimulated Caco-2 cells Br. J. Nutr. 2013, 110, 206-215 10.1017/S0007114512004862
40. Jobin, C.; Haskill, S.; Mayer, L.; Panja, A.; Sartor, R. Evidence for altered regulation of IκBα degradation in human colonic epithelial cells J. Immunol. 1997, 158, 226-234
41. Sethu, S.; Melendez, A. J. New developments on the TNFα-mediated signalling pathways Biosci. Rep. 2011, 31, 63-76 10.1042/BSR20100040
42. Théâtre, E.; Bours, V.; Oury, C. A P2X ion channel-triggered NF-κB pathway enhances TNF-α-induced IL-8 expression in airway epithelial cells Am. J. Respir. Cell Mol. Biol. 2009, 41, 705-713 10.1165/rcmb.2008-0452OC
43. v1.2 calcium channel: identification of the phosphorylation sites J. Biol. Chem. 2006, 281, 25560-25567 10.1074/jbc.M508661200
44. Kumrungsee, T.; Saiki, T.; Akiyama, S.; Nakashima, K.; Tanaka, M.; Kobayashi, Y.; Matsui, T. Inhibition of calcium-calmodulin complex formation by vasorelaxant basic dipeptides demonstrated by in vitro and in silico analyses Biochim. Biophys. Acta, Gen. Subj. 2014, 1840, 3073-3078 10.1016/j.bbagen.2014.07.020