Two-carbon folate cycle of commensal Lactobacillus reuteri 6475 gives rise to immunomodulatory ethionine, a source for histone ethylation

FASEB Journal

Volumn 33, Issue 3, 2019, Pages 3536-3548

  Röth, Daniel ^a   Chiang, Abby J ^a   Hu, Weidong ^a   Gugiu, Gabriel B ^a   Morra, Christina N ^b   Versalovic, James ^b,c   Kalkum, Markus ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

ethenyltetrahydrofolate; lysine ethylation; microbiome; posttranslational modification; probiotic bacteria

Indexed keywords

CARBON; ETHIONINE; FOLIC ACID; HISTONE; HOMOCYSTEINE; TUMOR NECROSIS FACTOR; TYROSINE; AMINO ACID; METHIONINE; PROBIOTIC AGENT;

ARTICLE; CELL PROLIFERATION; CHROMATIN; CONTROLLED STUDY; HISTONE METHYLATION; IMMUNOMODULATION; LACTOBACILLUS REUTERI; MASS SPECTROMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN PROCESSING; CELL CULTURE; CULTURE MEDIUM; HUMAN; METABOLISM; METHYLATION; MICROFLORA; PHYSIOLOGY; THP-1 CELL LINE;

AMINO ACIDS; CARBON; CELL PROLIFERATION; CELLS, CULTURED; CULTURE MEDIA; ETHIONINE; FOLIC ACID; HISTONES; HOMOCYSTEINE; HUMANS; IMMUNOMODULATION; LACTOBACILLUS REUTERI; METHIONINE; METHYLATION; MICROBIOTA; PROBIOTICS; THP-1 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85071953736     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201801848R     Document Type: Article

References (56)

1. Food and Agriculture Organization of the United Nations WHO. (2006) Probiotics in Food: Health and Nutritional Properties and Guidelines for Evaluation, Food and Agriculture Organization of the United Nations WHO, Rome, Italy
2. Saarela, M., Lähteenmäki, L., Crittenden, R., Salminen, S., and Mattila-Sandholm, T. (2002) Gut bacteria and health foods-the European perspective. Int.f. Food Microbiol. 78, 99–117
3. Walter, J., Chagnaud, P., Tannock, G. W., Loach, D. M., Dal Bello, F., Jenkinson, H. F., Hammes, W. P., and Hertel, C. (2005) A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl. Environ. Microbiol. 71, 979–986
4. Reuter, G. (2001) The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession. Curr Issues Intest. Microbiol. 2, 43–53
5. Zella, G. G., Hait, E. J., Clavan, T., Gevers, D., Ward, D. V., Kitts, G. L., and Korzenik, J. R. (2011) Distinct microbiome in pouchitis compared to healthy pouches in ulcerative colitis and familial adenomatous polyposis. Inflamm. Bowel Dis. 17, 1092–1100
6. Vigsnaes, L. K., Brynskov, J., Steenholdt, G., Wilcks, A., and Licht, T. R. (2012) Gram-negative bacteria account for main differences between faecal microbiota from patients with ulcerative colitis and healthy controls. Benef. Microbes 3, 287–297
7. Scarpato, E., Russo, M., and Staiano, A. (2018) Probiotics in pediatric gastroenterology: emerging indications: inflammatory bowel diseases. f. Clin. Gastroenterol. 52(Suppl 1, Proceedings from the 9th Probiotics, Prebiotics and New Foods, Nutraceuticals and Botanicals for Nutrition & Human and Microbiota Health Meeting, held in Rome, Italy from September 10 to 12, 2017), S7–S9
8. Ganji-Arjenaki, M., and Rafieian-Kopaei, M. (2018) Probiotics are a good choice in remission of inflammatory bowel diseases: a meta analysis and systematic review. J. Cell. Physiol. 233, 2091–2103
9. Gupta, P., Andrew, H., Kirschner, B. S., and Guandalini, S. (2000) Is lactobacillus GG helpful in children with Crohn's disease? Results of a preliminary, open-label study. J. Pediatr. Gastroenterol. Nutr. 31, 453–457
10. Bibiloni, R., Fedorak, R. N., Tannock, G. W., Madsen, K. L., Gionchetti, P., Campieri, M., De Simone, G., and Sartor, R. B. (2005) VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am. J. Gastroenterol. 100, 1539–1546
11. Lichtenstein, L., Avni-Biron, I., and Ben-Bassat, O. (2016) Probiotics and prebiotics in Crohn's disease therapies. Best Pract. Res. Clin. Gastroenterol. 30, 81–88
12. Sebastián Domingo, J. J. (2017) Review of the role of probiotics in gastrointestinal diseases in adults [in English, Spanish]. Gastroenterol. Hepatol. 40, 417–429
13. Cummings, J. H., and Macfarlane, G. T. (1997) Role of intestinal bacteria in nutrient metabolism. JPEN f. Parenter. Enteral Nutr. 21, 357–365
14. Dahl, W. J., Agro, N. C., Eliasson, Å. M., Mialki, K. L., Olivera, J. D., Rusch, G. T., and Young, G. N. (2017) Health benefits of fiber fermentation. J. Am. Coll. Nutr. 36, 127–136
15. Topping, D. L., and Clifton, P. M. (2001) Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 81, 1031–1064
16. Hollister, E. B., Gao, G., and Versalovic, J. (2014) Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology 146, 1449–1458
17. Thomas, C. M., Hong, T., van Pijkeren, J. P., Hemarajata, P., Trinh, D. V., Hu, W., Britton, R. A., Kalkum, M., and Versalovic, J. (2012) Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERKsignaling. PLoS One 7, e31951
18. Fuller, M. F., and Reeds, P. J. (1998) Nitrogen cycling in the gut. Annu. Rev. Nutr. 18, 385–411
19. Gao, G., Major, A., Rendon, D., Lugo, M., Jackson, V., Shi, Z., Mori-Akiyama, Y., and Versalovic, J. (2015) Histamine H2 receptor-mediated suppression of intestinal inflammation by probiotic Lactobacillus reuteri. MBio 6, e01358-15
20. Ganesh, B. P., Hall, A., Ayyaswamy, S., Nelson, J. W., Fultz, R., Major, A., Haag, A., Esparza, M., Lugo, M., Venable, S., Whary, M., Fox, J. G., and Versalovic, J. (2018) Diacylglycerol kinase synthesized by commensal Lactobacillus reuteri diminishes protein kinase C phosphorylation and histamine-mediated signaling in the mammalian intestinal epithelium. Mucosal. Immunol. 11, 380–393
21. O'Mahony, L., Akdis, M., and Akdis, C. A. (2011) Regulation of the immune response and inflammation by histamine and histamine receptors. J. Allergy Clin. Immunol. 128, 1153–1162
22. Santos, F., Wegkamp, A., de Vos, W. M., Smid, E. J., and Hugenholtz, J. (2008) High-level folate production in fermented foods by the B12 producer Lactobacillus reuteri JCM1112. Appl. Environ. Microbiol. 74, 3291–3294
23. Rossi, M., Amaretti, A., and Raimondi, S. (2011) Folate production by probiotic bacteria. Nutrients 3, 118–134
24. Brosnan, M. E., MacMillan, L., Stevens, J. R., and Brosnan, J. T. (2015) Division of labour: how does folate metabolism partition between one-carbon metabolism and amino acid oxidation? Biochem. J. 472, 135–146
25. Thomas, C. M., Saulnier, D. M. A., Spinler, J. K., Hemarajata, P., Gao, C., Jones, S. E., Grimm, A., Balderas, M. A., Burstein, M. D., Morra, C., Roeth, D., Kalkum, M., and Versalovic, J. (2016) FolC2-mediated folate metabolism contributes to suppression of inflammation by probiotic Lactobacillus reuteri. Microbiology Open 5, 802–818
26. De Man, J. C., Rogosa, M., and Sharpe, M. E. (2008) A medium for the cultivation of lactobacilli. J. Appl. Bacteriol. 23, 130–135
27. Jones, S. E., and Versalovic, J. (2009) Probiotic Lactobacillus reuten biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol. 9, 35
28. Johnson, B. A., and Blevins, R. A. (1994) NMR View: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603–614
29. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277–293
30. Wlostowski, M., Czarnocka, S., and Maciejewski, P. (2010) Efficient S-alkylation of cysteine in the presence of 1,1,3,3-tetramethylguanidine. Tetrahedron Lett. 51, 5977–5979
31. Moore, G. E., Gerner, R. E., and Franklin, H. A. (1967) Culture of normal human leukocytes. JAMA 199, 519–524
32. Locasale, J. W. (2013) Serine, glycine and one-carbon units: cancer metabolism in full circle. Nat. Rev. Cancer 13, 572–583
33. Bodenhausen, G., and Ruben, D. J. (1980) Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Lett. 69, 185–189
34. Bystrov, V. F. (1976) Spin—spin coupling and the conformational states of peptide systems. Prog. Nucl. Magn. Reson. Spectrosc. 10, 41–82
35. Kay, L. E., Ikura, M., Tschudin, R., and Bax, A. (2011) Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins. 1990. J. Magn. Reson. 213, 423–441
36. Aschkenasy, A. (1975) Immunosuppressive effect of ethionine in rats. Resistance of this effect to methionine, tryptophan, ATP, adenosine and uridine [in French]. Ann. Nutr. Aliment. 29, 137–150
37. Zabos, P., Kyner, D. A., Seide-Kehoe, R., Acs, G., and Christman, J. K. (1978) Effect of L-ethionine on macromolecular synthesis in mitogen-stimulated lymphocytes. Biochim. Biophys. Acta 520, 139–152
38. Alix, J.-H. (1982) Molecular aspects of the in vivo and in vitro effects of ethionine, an analog of methionine. Microbiol. Rev. 46, 281–295
39. LaBaume, L. B., and Guynn, R. W. (1985) Investigation into the substrate capacity of the acetaldehyde-tetrahydrofolate condensation product. Prog. Clin. Biol. Res. 183, 189–200
40. Guynn, R. W., Labaume, L. B., and Henkin, J. (1982) Equilibrium constants under physiological conditions for the condensation of acetaldehyde with tetrahydrofolic acid. Arch. Biochem. Biophys. 217, 181–190
41. LaBaume, L. B., and Guynn, R. W. (1985) Investigation into the substrate capacity of the acetaldehyde-tetrahydrofolate condensation product. Prog. Clin. Biol. Res. 183, 189–200
42. De Paiva, E. P., Costa, M. M. A., and de Azevedo, C. A. (2015) Folate-analytical properties, bioavailability and stability in foods. Scientia Chromatographica 7, 199–222
43. Bailey, L. B., and Gregory III, J. F. (1999) Folate metabolism and requirements. J. Nutr. 129, 779–782
44. Fisher, J. F., and Mallette, M. F. (1961) The natural occurrence of ethionine in bactdria. J. Gen. Physiol. 45, 1–13
45. Loerch, J. D., and Mallette, M. F. (1963) Ethionine biosynthesis in Escherichia coli. Arch. Biochem. Biophys. 103, 272–275
46. Villanueva, V. R., Barbier, M., Gros, C., and Lederer, E. (1966) On the “ethionine” produced by Escherichia coli B [in French]. Biochim. Biophys. Acta. 130, 329–335
47. Radix, P. M., Walters, C. S., and Adkins J. A. (1983) The influence of ethionine-supplemented soy protein diet on cell-mediated and humoral immunity. J. Nutr. 113, 159–164
48. Den Besten, G., van Eunen, K., Groen, A. K., Venema, K., Reijngoud, D.-J., and Bakker, B. M. (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54, 2325–2340
49. Hayashi, H., Takahashi, R., Nishi, T., Sakamoto, M., and Benno, Y. (2005) Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. J. Med. Microbiol. 54, 1093–1101
50. Van der Wielen, N., Moughan, P. J., and Mensink, M. (2017) Amino acid absorption in the large intestine of humans and porcine models. J. Nutr. 147, 1493–1498
51. Maw, G. A. (1966) Incorporation and distribution of ethionine-sulfur in the protein of ethionine-sensitive and ethionine-resistant yeasts. Arch. Biochem. Biophys. 115, 291–301
52. Rabinovitz, M., Olson, M. E., and Greenberg, D. M. (1957) Characteristics of the inhibition by ethionine of the incorporation of methionine into proteins of the Ehrlich ascites carcinoma in vitro. J. Biol. Chem. 227, 217–224
53. Brown, J. L. (1973) The modification of the amino terminal region of Escherichia coli proteins after initiation with methionine analogues. Biochim. Biophys. Acta 294, 527–529
54. Cox, R., and Goorha, S. (1984) Synthesis of S-adenosylethionine by the gamma isozyme of methionine adenosyltransferase from Friend erythroleukemic cells. Cancer Res. 44, 4938–4941
55. Aswad, D. W., and Koshland, D. E., Jr. (1975) Evidence for an S-adenosylmethionine requirement in the chemotactic behavior of Salmonella typhimurium. J. Mol. Biol. 97, 207–223
56. Holloway, C. T., Greene, R. C., and Su, C. H. (1970) Regulation of S-adenosylmethionine synthetase in Escherichia coli. J. Bacteriol. 104, 734–747