Oral glutathione supplementation drastically reduces Helicobacter-induced gastric pathologies

Scientific Reports

Volumn 6, Issue , 2016, Pages

  De Bruyne, Ellen ^a   Ducatelle, Richard ^a   Foss, Dennis ^b   Sanchez, Margaret ^b   Joosten, Myrthe ^a   Zhang, Guangzhi ^a   Smet, Annemieke ^a   Pasmans, Frank ^a   Haesebrouck, Freddy ^a   Flahou, Bram ^a  

^a GHENT UNIVERSITY   (Belgium)

^b ZOETIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMMONIA; CARBOHYDRATE; CYTOKINE; GAMMA GLUTAMYLTRANSFERASE; GLUTAMINE; GLUTATHIONE; KI 67 ANTIGEN;

ANIMAL; CELL PROLIFERATION; DIETARY SUPPLEMENT; DRUG EFFECTS; EPITHELIUM CELL; FEMALE; GERBIL; GROWTH, DEVELOPMENT AND AGING; HELICOBACTER; HELICOBACTER INFECTIONS; INFLAMMATION; LYMPHOCYTE; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; ORAL DRUG ADMINISTRATION; PATHOLOGY; PHYSIOLOGY; STOMACH;

ADMINISTRATION, ORAL; AMINO ACIDS; AMMONIA; ANIMALS; CARBOHYDRATES; CELL PROLIFERATION; CYTOKINES; DIETARY SUPPLEMENTS; EPITHELIAL CELLS; FEMALE; GAMMA-GLUTAMYLTRANSFERASE; GERBILLINAE; GLUTAMINE; GLUTATHIONE; HELICOBACTER; HELICOBACTER INFECTIONS; INFLAMMATION; KI-67 ANTIGEN; LYMPHOCYTES; MICROBIAL VIABILITY; STOMACH;

EID: 84957576047     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20169     Document Type: Article

References (61)

1. Haesebrouck, F. et al. Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin. Microbiol. Rev. 22, 202-223 (2009).
2. Stolte, M. et al. Helicobacter and gastric MALT lymphoma. Gut 50, suppl. iii19-iii23 (2002).
3. Haesebrouck, F. et al. Non-Helicobacter pylori Helicobacter species in the human gastric mucosa: a proposal to introduce the terms H. heilmannii sensu lato and sensu stricto. Helicobacter 16, 339-340 (2011).
4. Trebesius, K., Adler, K., Vieth, M., Stolte, M. & Haas, R. Specific detection and prevalence of Helicobacter heilmannii-like organisms in the human gastric mucosa by fluorescent in situ hybridization and partial 16S ribosomal DNA sequencing. J. Clin. Microbiol. 39, 1510-1516 (2001).
5. De Groote, D. et al. Detection of non-Helicobacter pylori species in "Helicobacter heilmanni"-infected humans. Helicobacter 10, 398-406 (2005).
6. Van den Bulck, K. et al. Identification of non-Helicobacter pylori spiral organisms in gastric samples from humans, dogs, and cats. J. Clin. Microbiol. 43, 2256-2260 (2005).
7. Nakamura, M. et al. "Candidatus Helicobacter heilmannii" from a cynomolgus monkey induces gastric mucosa-associated lymphoid tissue lymphomas in C57BL/6 mice. Infect. Immun. 75, 1214-1222 (2007).
8. Flahou, B. et al. Helicobacter suis causes severe gastric pathology in mouse and mongolian gerbil models of human gastric disease. PLoS One 5, e14083 (2010).
9. Nakamura, M. et al. Microcirculatory alteration in low-grade gastric mucosa-associated lymphoma by Helicobacter heilmannii infection: Its relation to vascular endothelial growth factor and cyclooxygenase-2. J. Gastroenterol. Hepatol. 23, S157-S160 (2008).
10. De Bruyne, E. et al. An experimental Helicobacter suis infection causes gastritis and reduced daily weight gain in pigs. Vet. Microbiol. 160, 449-454 (2012).
11. Joosten, M. et al. Case report: Helicobacter suis infection in a pig veterinarian. Helicobacter 18, 392-396 (2013).
12. De Cooman, L. M. et al. Survival of Helicobacter suis bacteria in retail pig meat. Int. J. Food Microbiol. 1, 164-167 (2013).
13. Morgner, A. et al. Helicobacter heilmannii-associated primary low-grade MALT lymphoma: complete remission after curing the infection. Gastroenterol 118, 821-828 (2000).
14. Kokkola, A. et al. The effect of Helicobacter pylori eradication on the natural course of atrophic gastritis with dysplasia. Aliment. Pharmacol. Ther. 16, 515-520 (2002).
15. Flahou, B. et al. Gastric epithelial cell death caused by Helicobacter suis and Helicobacter pylori gamma-glutamyl transpeptidase is mainly glutathione degradation-dependent. Cell. Microbiol. 13, 1933-1955 (2011).
16. Zhang, G. et al. Effects of Helicobacter suis γ- glutamyl transpeptidase on lymphocytes: modulation by glutamine and glutathione supplementation and outer membrane vesicles as a putative delivery route of the enzyme. PLoS One 10, e77966 (2013).
17. Rimbara, E., Mori, S., Kim, H. & Shibayama, K. Role of γ-glutamyltranspeptidase in the pathogenesis of Helicobacter pylori infection. Microbiol. Immunol. 57, 665-673 (2013).
18. Wüstner, S. et al. Helicobacter pylori γ-glutamyltranspeptidase impairs T-lymphocyte function by compromising metabolic adaption through inhibition of cMyc and IRF 4 expression. Cell. Microbiol. 17, 51-61 (2015).
19. Chevalier, C., Thiberge, J. M., Ferrero, R. L. & Labigne, A. Essential role of Helicobacter pylori γ-glutamyltranspeptidase for the colonization of the gastric mucosa of mice. Mol. Microbiol. 31, 1359-1372 (1999).
20. Shibayama, K. et al. Metabolism of glutamine and glutathione via γ-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism. Mol. Microbiol. 64, 396-406 (2007).
21. Vermoote, M. et al. Genome sequence of Helicobacter suis supports its role in gastric pathology. Vet. Res. 42, 51 (2011).
22. Rossi, M. et al. Evidence of conserved function of γ-glutamyltranspeptidase in Helicobacter Genus. PloS One 7, e30543 (2012).
23. Aledo, C. J. Glutamine breakdown in rapidly dividing cells: waste or investment? Bioessays 26, 778-785 (2004).
24. DeBerardinis, R. J. & Cheng, T. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 29, 313-324 (2010).
25. Hsu, C. B., Huang, H. J., Wang, C. H., Yen, W. H. T. & Yu, B. The effect of glutamine supplement on small intestinal morphology and xylose absorptive ability of weaned piglets. Afr. J. Biotechnol. 9, 7003-7008 (2010).
26. Shibayama, K. et al. Apoptotic signaling pathway activated by Helicobacter pylori infection and increase of apoptosis-inducing activity under serum-starved conditions. Infect. Immun. 69, 3181-3189 (2001).
27. Zhang, H. & Forman, H. J. Redox regulation of gamma-glutamyl transpeptidase. Am. J. Resp. Cell. Mol. 41, 510-515 (2009).
28. Drozdz, R. et al. Gamma-glutamyltransferase dependent generation of reactive oxygen species from a glutathione/transferrin system. Free Radical Bio. Med. 25, 786-792 (1998).
29. Leduc, D., Gallaud, J., Stingl, K. & De Reuse, H. Coupled amino acid deamidase-transport systems essential for Helicobacter pylori colonization. Infect. Immun. 78, 2782-792 (2010).
30. Schilling, C. H. et al. Genome-scale metabolic model of Helicobacter pylori 26695. J. Bacteriol. 184, 4582-4593 (2002).
31. Pitson, S. M., Mendz, G. L., Srinivasan, S. & Hazell, S. L. The tricarboxylic acid cycle of Helicobacter pylori. Eur. J. Biochem. 1, 258-267 (1999).
32. Krishnan, N. & Becker, D. F. Oxygen reactivity of PutA from Helicobacter species and proline-linked oxidative species. J. Bacteriol. 188, 1227-1235 (2006).
33. Nagata, K. et al. L-serine, D- and L-proline and alanine as respiratory substrates of Helicobacter pylori: correlation between in vitro and in vivo amino acid levels. Microbiology 149, 2023-2030 (2003).
34. Hughes, N. J., Clayton, C. L., Chalk, P. A. & Kelly, D. J. Helicobacter pylori porCDAB and oorDABC genes encode distinct pyruvate:flavodoxin and 2-oxoglutarate: acceptor oxidoreductases which mediate electron transport to NADP. J. Bacteriol. 180, 1119-1128 (1998).
35. Scott, T., Kondadi, P. K., Hänninen, M. & Rossi, M. Comparative Genomics of Helicobacter pylori and the human-derived Helicobacter bizzozeronii CIII-1 nature of non-pylori gastric Helicobacter infections in humans. BMC Genomics 12, 534 (2011).
36. Lam, H. M., Coschigano, K. T., Oliveira, I. C., MeloOliveira, R. & Coruzzi, G. M. The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 569-593 (1996).
37. Roth, E., Spittler, A. & Oehler, R. Glutamine: Effects on the immune system, protein metabolism and intestinal function. Wien. Klein. Wochensch. 108, 669-676 (1996).
38. Wu, G. et al. Important roles for L-glutamine in swine nutrition and production. J. Anim. Sci. 89, 2017-2030 (2011).
39. Vicarcio, M. et al. Dietary glutamine affects mucosal functions in rats with mild DSS-induced colitis. J. Nutrition. 137, 1931-1937 (2007).
40. Nakamura, E. et al. Prophylactic effect of glutamine and marzulene against Helicobacter pylori-related gastric diseases in Mongolian gerbils. Jpn. Pharmacol. Ther. 35, 479-488 (2007).
41. Hagen, S. et al. Inflammation and foveolar hyperplasia are reduced by supplemental dietary glutamine during Helicobacter pylori infection in mice. J. Nutr. 22, 912-918 (2009).
42. Amagase, A. et al. New frontiers in gut nutrient sensor research: prophylactic effect of glutamine against Helicobacter pylori-induced gastric diseases in Mongolian gerbils. J. Pharmacol. Sci. 112, 25-32 (2010).
43. Nakamura, E. & Hagen, S. Role of glutamine and arginase in protection against ammonia-induced cell death in gastric epithelial cells. Am. J. Physiol-Gastr. L. 283, G1264-G1275 (2002).
44. Evans, M. E., Jones, D. P. & Ziegler, T. R. Glutamine prevents cytokine-induced apoptosis in human colonic epithelial cells. J. Nutr. 133, 3065-3073 (2003).
45. Wagner, S. et al. Regulation of gastric epithelial cell growth by Helicobacter pylori: Evidence for a major role of apoptosis. Gastroenterol. 113, 1836-1847 (1997).
46. Shirin, H. & Moss, S. F. Helicobacter pylori induced apoptosis. Gut 45, 592-594 (1998).
47. Gong, M., Ling, S. S. M., Lui, S. Y., Yeoh, K. G. & Ho, B. Helicobacter pylori γ-glutamyl transpeptidase is a pathogenic factor in the development of peptic ulcer disease. Gastroenterol. 139, 564-573 (2010).
48. Ricci, V., Giannouli, M., Romano, M. & Zarrilli, R. Helicobacter pylori gamma-glutamyl transpeptidase and its pathogenic role. World J. Gastroenterol. 20, 630-638 (2014).
49. Schmees, C. et al. Inhibition of T-cell proliferation by Helicobacter pylori γ-glutamyl transpeptidase. Gastroenterol. 132, 1820-1833 (2007).
50. Meister, A. & Anderson, M. E. Glutathione. Ann. Rev. Biochem. 52, 711-760 (1983).
51. Martensson, J., Jain, A. & Meister, A. Glutathione is required for intestinal function. Proc. Natl. Acad. Sci. 87, 1715-1719 (1990).
52. Circu, M. L. & Aw, T. Y. Glutathione and apoptosis. Free Radical Res. 42, 689-706 (2008).
53. Liu, C. et al. The effect of dietary glutathione and coenzyme Q10 on the prevention and treatment of inflammatory bowel disease in mice. Int. J. Vitam. Nutr. Res. 74, 74-85 (2004).
54. Liang, J. et al. Purification of Helicobacter suis strains from biphasic cultures by single colony isolation: influence on strain characteristics. Helicobacter 20, 206-216 (2015).
55. Baele, M. et al. Isolation and characterization of Helicobacter suis sp. nov. from pig stomachs. Int. J. Syst. Evol. Microbiol. 58, 1350-1358 (2008).
56. Joosten, M. et al. Diversity in bacterium-host interactions within the species Helicobacter heilmannii sensu stricto. Vet. Res. 44, 65 (2013).
57. Vermoote, M. et al. Antimicrobial susceptibility pattern of Helicobacter suis strains. Vet. Microbiol. 153, 339-342 (2011).
58. Flahou, B. et al. The local immune response of mice after Helicobacter suis infection: strain differences and distinction with Helicobacter pylori. Vet. Res. 43, 75 (2012).
59. Sugimoto, M., Ohno, T., Graham, D. Y. & Yamaoka, Y. Gastric mucosal interleukin-17 and -18 mRNA expression in Helicobacter pylori-induced Mongolian gerbils. Cancer Sci. 100, 2152-2159 (2009).
60. Crabtree, J. E. et al. Gastric mucosal cytokine and epithelial cell responses to Helicobacter pylori infection in Mongolian gerbils. J. Pathol. 202, 197-207 (2004).
61. Chirgwin, S. R. et al. Infection outcome and cytokine gene expression in Brugia pahangi-infected gerbils (Meriones unguiculatus) sensitized with Brucella abortus. Infect. Immun. 70, 5938-5945 (2002).