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

Volumn 8, Issue 10, 2013, Pages

  Zhang, Guangzhi ^a   Ducatelle, Richard ^a   Pasmans, Frank ^a   D'Herde, Katharina ^a   Huang, Liping ^b   Smet, Annemieke ^a   Haesebrouck, Freddy ^a   Flahou, Bram ^a  

^a GHENT UNIVERSITY   (Belgium)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; GAMMA GLUTAMYLTRANSFERASE; GAMMA INTERFERON; GLUTAMINE; GLUTATHIONE; INTERLEUKIN 17; INTERLEUKIN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL METABOLISM; BACTERIUM MUTANT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELL LYSATE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; FEMALE; FLOW CYTOMETRY; GROWTH INHIBITION; HELICOBACTER; HELICOBACTER INFECTION; HELICOBACTER SUIS; HUMAN; HUMAN CELL; INTESTINE FLORA; LEUKEMIA CELL LINE; LYMPHOCYTE FUNCTION; MEMBRANE VESICLE; MICROBIAL DEGRADATION; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; WHOLE CELL; WILD TYPE;

ANIMALS; ANTIGENS, CD19; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL MEMBRANE; CELLS, CULTURED; GAMMA-GLUTAMYLTRANSFERASE; GLUTAMINE; GLUTATHIONE; HELICOBACTER HEILMANNII; INTERLEUKIN-17; INTERLEUKIN-4; LYMPHOCYTES; MICE; PROTEIN TRANSPORT;

EID: 84885784110     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077966     Document Type: Article

References (74)

1. Ernst PB, Gold BD, (2000) The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol 54: 615-640. doi:10.1146/annurev.micro.54.1.615. PubMed: 11018139.
2. Axon AT, (1999) Are all helicobacters equal? Mechanisms of gastroduodenal pathology and their clinical implications. Gut 45 (Suppl 1):: I1-4. doi:10.1136/gut.45.2008.i1. PubMed: 10457027.
3. Flahou B, Haesebrouck F, Pasmans F, D'Herde K, Driessen A, et al. (2010) Helicobacter suis causes severe gastric pathology in mouse and mongolian gerbil models of human gastric disease. PLOS ONE 5: e14083. doi:10.1371/journal.pone.0014083. PubMed: 21124878.
4. Haesebrouck F, Pasmans F, Flahou B, Chiers K, Baele M, et al. (2009) Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin Microbiol Rev 22: 202-223, Table of Contents doi:10.1128/CMR.00041-08. PubMed: 19366912.
5. Van den Bulck K, Decostere A, Baele M, Driessen A, Debongnie JC, et al. (2005) Identification of non-Helicobacter pylori spiral organisms in gastric samples from humans, dogs, and cats. J Clin Microbiol 43: 2256-2260. doi:10.1128/JCM.43.5.2256-2260.2005. PubMed: 15872252.
6. Joosten M, Flahou B, Meyns T, Smet A, Arts J, et al. (2013) Case Report: Helicobacter suis Infection in a Pig Veterinarian. Helicobacter.
7. Suzuki A, Kobayashi M, Matsuda K, Matsumoto T, Kawakubo M, et al. (2010) Induction of high endothelial venule-like vessels expressing GlcNAc6ST-1-mediated L-selectin ligand carbohydrate and mucosal addressin cell adhesion molecule 1 (MAdCAM-1) in a mouse model of "Candidatus Helicobacter heilmannii"-induced gastritis and gastric mucosa-associated lymphoid tissue (MALT) lymphoma. Helicobacter 15: 538-548. doi:10.1111/j.1523-5378.2010.00801.x. PubMed: 21073611.
8. Trebesius K, Adler K, Vieth M, Stolte M, Haas R, (2001) 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. doi:10.1128/JCM.39.4.1510-1516.2001. PubMed: 11283079.
9. O'Rourke JL, Dixon MF, Jack A, Enno A, Lee A, (2004) Gastric B-cell mucosa-associated lymphoid tissue (MALT) lymphoma in an animal model of 'Helicobacter heilmannii' infection. J Pathol 203: 896-903. doi:10.1002/path.1593. PubMed: 15258991.
10. Lee A, Eckstein RP, Fevre DI, Dick E, Kellow JE, (1989) Non Campylobacter pylori spiral organisms in the gastric antrum. Aust N Z J Med 19: 156-158. doi:10.1111/j.1445-5994.1989.tb00232.x. PubMed: 2764819.
11. Solnick JV, O'Rourke J, Lee A, Paster BJ, Dewhirst FE, et al. (1993) An uncultured gastric spiral organism is a newly identified Helicobacter in humans. J Infect Dis 168: 379-385. doi:10.1093/infdis/168.2.379. PubMed: 8335974.
12. Reinherz EL, Schlossman SF, (1980) The differentiation and function of human T lymphocytes. Cell 19: 821-827. doi:10.1016/0092-8674(80)90072-0. PubMed: 6991122.
13. Beigier-Bompadre M, Moos V, Belogolova E, Allers K, Schneider T, et al. (2011) Modulation of the CD4+ T-cell response by Helicobacter pylori depends on known virulence factors and bacterial cholesterol and cholesterol alpha-glucoside content. J Infect Dis 204: 1339-1348. doi:10.1093/infdis/jir547. PubMed: 21921201.
14. Gong M, Ling SS, Lui SY, Yeoh KG, Ho B, (2010) Helicobacter pylori gamma-glutamyl transpeptidase is a pathogenic factor in the development of peptic ulcer disease. Gastroenterology 139: 564-573. doi:10.1053/j.gastro.2010.03.050. PubMed: 20347814.
15. Schmees C, Prinz C, Treptau T, Rad R, Hengst L, et al. (2007) Inhibition of T-cell proliferation by Helicobacter pylori gamma-glutamyl transpeptidase. Gastroenterology 132: 1820-1833. doi:10.1053/j.gastro.2007.02.031. PubMed: 17484877.
16. Vermoote M, Vandekerckhove TT, Flahou B, Pasmans F, Smet A, et al. (2011) Genome sequence of Helicobacter suis supports its role in gastric pathology. Vet Res 42: 51. doi:10.1186/1297-9716-42-51. PubMed: 21414191.
17. Flahou B, Haesebrouck F, Chiers K, Van Deun K, De Smet L, et al. (2011) Gastric epithelial cell death caused by Helicobacter suis and Helicobacter pylori gamma-glutamyl transpeptidase is mainly glutathione degradation-dependent. Cell Microbiol 13: 1933-1955. doi:10.1111/j.1462-5822.2011.01682.x. PubMed: 21899697.
18. Rossi M, Bolz C, Revez J, Javed S, El-Najjar N, et al. (2012) Evidence for conserved function of gamma-glutamyltranspeptidase in Helicobacter genus. PLOS ONE 7: e30543. doi:10.1371/journal.pone.0030543. PubMed: 22348013.
19. Shibayama K, Wachino J, Arakawa Y, Saidijam M, Rutherford NG, et al. (2007) Metabolism of glutamine and glutathione via gamma-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism. Mol Microbiol 64: 396-406. doi:10.1111/j.1365-2958.2007.05661.x. PubMed: 17381553.
20. Perego P, Paolicchi A, Tongiani R, Pompella A, Tonarelli P, et al. (1997) The cell-specific anti-proliferative effect of reduced glutathione is mediated by gamma-glutamyl transpeptidase-dependent extracellular pro-oxidant reactions. Int J Cancer 71: 246-250. doi:10.1002/(SICI)1097-0215(19970410)71:2. PubMed: 9139850.
21. Curthoys NP, Watford M, (1995) Regulation of glutaminase activity and glutamine metabolism. Annu Rev Nutr 15: 133-159. doi:10.1146/annurev.nu.15.070195.001025. PubMed: 8527215.
22. Rhoads JM, Argenzio RA, Chen W, Rippe RA, Westwick JK, et al. (1997) L-glutamine stimulates intestinal cell proliferation and activates mitogen-activated protein kinases. Am J Physiol 272: G943-G953. PubMed: 9176200.
23. Carr EL, Kelman A, Wu GS, Gopaul R, Senkevitch E, et al. (2010) Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation. J Immunol 185: 1037-1044. doi:10.4049/jimmunol.0903586. PubMed: 20554958.
24. Johnson IR, Ball RO, Baracos VE, Field CJ, (2006) Glutamine supplementation influences immune development in the newly weaned piglet. Dev Comp Immunol 30: 1191-1202. doi:10.1016/j.dci.2006.03.003. PubMed: 16697041.
25. Rieder G, Fischer W, Haas R, (2005) Interaction of Helicobacter pylori with host cells: function of secreted and translocated molecules. Curr Opin Microbiol 8: 67-73. doi:10.1016/j.mib.2004.12.004. PubMed: 15694859.
26. Salama NR, Hartung ML, Müller A, (2013) Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat Rev Microbiol 11: 385-399. doi:10.1038/nrmicro3016. PubMed: 23652324.
27. Olofsson A, Vallström A, Petzold K, Tegtmeyer N, Schleucher J, et al. (2010) Biochemical and functional characterization of Helicobacter pylori vesicles. Mol Microbiol 77: 1539-1555. doi:10.1111/j.1365-2958.2010.07307.x. PubMed: 20659286.
28. Parker H, Chitcholtan K, Hampton MB, Keenan JI, (2010) Uptake of Helicobacter pylori outer membrane vesicles by gastric epithelial cells. Infect Immun 78: 5054-5061. doi:10.1128/IAI.00299-10. PubMed: 20876296.
29. Beveridge TJ, (1999) Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181: 4725-4733. PubMed: 10438737.
30. Kuehn MJ, Kesty NC, (2005) Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19: 2645-2655. doi:10.1101/gad.1299905. PubMed: 16291643.
31. Ellis TN, Kuehn MJ, (2010) Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 74: 81-94. doi:10.1128/MMBR.00031-09. PubMed: 20197500.
32. Kulp A, Kuehn MJ, (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64: 163-184. doi:10.1146/annurev.micro.091208.073413. PubMed: 20825345.
33. Wang Y, Taylor DE, (1990) Chloramphenicol resistance in Campylobacter coli: nucleotide sequence, expression, and cloning vector construction. Gene 94: 23-28. doi:10.1016/0378-1119(90)90463-2. PubMed: 2227449.
34. Huang L, Lu Y, Wei Y, Guo L, Wu H, et al. (2011) Construction and biological characterisation of recombinant porcine circovirus type 2 expressing the V5 epitope tag. Virus Res 161: 115-123. doi:10.1016/j.virusres.2011.05.015. PubMed: 21641944.
35. Fischer W, Püls J, Buhrdorf R, Gebert B, Odenbreit S, et al. (2001) Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol Microbiol 42: 1337-1348. PubMed: 11886563.
36. Josenhans C, Ferrero RL, Labigne A, Suerbaum S, (1999) Cloning and allelic exchange mutagenesis of two flagellin genes of Helicobacter felis. Mol Microbiol 33: 350-362. doi:10.1046/j.1365-2958.1999.01478.x. PubMed: 10411751.
37. Flahou B, Deun KV, Pasmans F, Smet A, Volf J, et al. (2012) The local immune response of mice after Helicobacter suis infection: strain differences and distinction with Helicobacter pylori. Vet Res 43: 75. doi:10.1186/1297-9716-43-75. PubMed: 23107128.
38. Verbrugghe E, Boyen F, Van Parys A, Van Deun K, Croubels S, et al. (2011) Stress induced Salmonella Typhimurium recrudescence in pigs coincides with cortisol induced increased intracellular proliferation in macrophages. Vet Res 42: 118. doi:10.1186/1297-9716-42-118. PubMed: 22151081.
39. Eeckhaut V, Ducatelle R, Sas B, Vermeire S, Van Immerseel F, (2013) Progress towards butyrate-producing pharmabiotics: Butyricicoccus pullicaecorum capsule and efficacy in TNBS models in comparison with therapeutics. Gut. PubMed: 23766442.
40. Verbrugghe E, Vandenbroucke V, Dhaenens M, Shearer N, Goossens J, et al. (2012) T-2 toxin induced Salmonella Typhimurium intoxication results in decreased Salmonella numbers in the cecum contents of pigs, despite marked effects on Salmonella-host cell interactions. Vet Res 43: 22. doi:10.1186/1297-9716-43-22. PubMed: 22440148.
41. Akhiani AA, Pappo J, Kabok Z, Schön K, Gao W, et al. (2002) Protection against Helicobacter pylori infection following immunization is IL-12-dependent and mediated by Th1 cells. J Immunol 169: 6977-6984. PubMed: 12471132.
42. Eaton KA, Mefford M, Thevenot T, (2001) The role of T cell subsets and cytokines in the pathogenesis of Helicobacter pylori gastritis in mice. J Immunol 166: 7456-7461. PubMed: 11390498.
43. Aebischer T, Lucas B, Koesling J, Bumann D, Meyer TF, (2000) How CD4(+) T cells may eliminate extracellular gastric Helicobacter? J Biotechnol 83: 77-84. doi:10.1016/S0168-1656(00)00301-1. PubMed: 11000463.
44. Baele M, Decostere A, Vandamme P, Ceelen L, Hellemans A, et al. (2008) Isolation and characterization of Helicobacter suis sp. nov. from pig stomachs. Int J Syst Evol Microbiol 58: 1350-1358. doi:10.1099/ijs.0.65133-0. PubMed: 18523177.
45. Fischer W, Prassl S, Haas R, (2009) Virulence mechanisms and persistence strategies of the human gastric pathogen Helicobacter pylori. Curr Top Microbiol Immunol 337: 129-171. doi:10.1007/978-3-642-01846-6_5. PubMed: 19812982.
46. Sundrud MS, Torres VJ, Unutmaz D, Cover TL, (2004) Inhibition of primary human T cell proliferation by Helicobacter pylori vacuolating toxin (VacA) is independent of VacA effects on IL-2 secretion. Proc Natl Acad Sci U S A 101: 7727-7732. doi:10.1073/pnas.0401528101. PubMed: 15128946.
47. Hu X, Legler PM, Khavrutskii I, Scorpio A, Compton JR, et al. (2012) Probing the donor and acceptor substrate specificity of the gamma-glutamyl transpeptidase. Biochemistry 51: 1199-1212. doi:10.1021/bi200987b. PubMed: 22257032.
48. Newsholme P, (2001) Why is L-glutamine metabolism important to cells of the immune system in health, postinjury, surgery or infection? J Nutr 131: 2514S-2523S; discussion:.
49. Grimble RF, (2001) Nutritional modulation of immune function. Proc Nutr Soc 60: 389-397. doi:10.1079/PNS2001102. PubMed: 11681814.
50. Calder PC, (1994) Glutamine and the immune system. Clin Nutr 13: 2-8. doi:10.1016/0261-5614(94)90120-1. PubMed: 16843345.
51. Aledo JC, (2004) Glutamine breakdown in rapidly dividing cells: waste or investment? Bioessays 26: 778-785. doi:10.1002/bies.20063. PubMed: 15221859.
52. Yaqoob P, Calder PC, (1997) Glutamine requirement of proliferating T lymphocytes. Nutrition 13: 646-651. doi:10.1016/S0899-9007(97)83008-0. PubMed: 9263257.
53. Nakamura E, Hagen SJ, (2002) Role of glutamine and arginase in protection against ammonia-induced cell death in gastric epithelial cells. Am J Physiol Gastrointest Liver Physiol 283: G1264-G1275. PubMed: 12388179.
54. Chang WK, Yang KD, Chuang H, Jan JT, Shaio MF, (2002) Glutamine protects activated human T cells from apoptosis by up-regulating glutathione and Bcl-2 levels. Clin Immunol 104: 151-160. doi:10.1006/clim.2002.5257. PubMed: 12165276.
55. O'Riordain MG, Fearon KC, Ross JA, Rogers P, Falconer JS, et al. (1994) Glutamine-supplemented total parenteral nutrition enhances T-lymphocyte response in surgical patients undergoing colorectal resection. Ann Surg 220: 212-221. doi:10.1097/00000658-199408000-00014. PubMed: 8053744.
56. Leduc D, Gallaud J, Stingl K, de Reuse H, (2010) Coupled amino acid deamidase-transport systems essential for Helicobacter pylori colonization. Infect Immun 78: 2782-2792. doi:10.1128/IAI.00149-10. PubMed: 20368342.
57. Wu G, (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37: 1-17. doi:10.1007/s00726-009-0269-0. PubMed: 19301095.
58. Reeds PJ, Burrin DG, (2001) Glutamine and the bowel. J Nutr 131: 2504S-2523S; discussion: 11533302.
59. Windmueller HG, Spaeth AE, (1980) Respiratory fuels and nitrogen metabolism in vivo in small intestine of fed rats. Quantitative importance of glutamine, glutamate, and aspartate. J Biol Chem 255: 107-112. PubMed: 7350142.
60. Wilde SW, Kilberg MS, (1991) Glutamine transport by basolateral plasma-membrane vesicles prepared from rabbit intestine. Biochem J 277(Pt 3): 687-691 PubMed: 1908221.
61. Hagen SJ, Ohtani M, Zhou JR, Taylor NS, Rickman BH, et al. (2009) Inflammation and foveolar hyperplasia are reduced by supplemental dietary glutamine during Helicobacter pylori infection in mice. J Nutr 139: 912-918. doi:10.3945/jn.108.097790. PubMed: 19261732.
62. Kaparakis M, Turnbull L, Carneiro L, Firth S, Coleman HA, et al. (2010) Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol 12: 372-385. doi:10.1111/j.1462-5822.2009.01404.x. PubMed: 19888989.
63. Nakanishi T, Sugawara M, Huang W, Martindale RG, Leibach FH, et al. (2001) Structure, function, and tissue expression pattern of human SN2, a subtype of the amino acid transport system N. Biochem Biophys Res Commun 281: 1343-1348. doi:10.1006/bbrc.2001.4504. PubMed: 11243884.
64. Hatanaka T, Huang W, Wang H, Sugawara M, Prasad PD, et al. (2000) Primary structure, functional characteristics and tissue expression pattern of human ATA2, a subtype of amino acid transport system A. Biochim Biophys Acta 1467: 1-6. doi:10.1016/S0005-2736(00)00252-2. PubMed: 10930503.
65. Kirchhoff P, Dave MH, Remy C, Kosiek O, Busque SM, et al. (2006) An amino acid transporter involved in gastric acid secretion. Pflugers Arch 451: 738-748. doi:10.1007/s00424-005-1507-2. PubMed: 16308696.
66. Bode BP, (2001) Recent molecular advances in mammalian glutamine transport. J Nutr 131: 2475S-2486S; discussion: 11533296.
67. Oertli M, Noben M, Engler DB, Semper RP, Reuter S, et al. (2013) Helicobacter pylori gamma-glutamyl transpeptidase and vacuolating cytotoxin promote gastric persistence and immune tolerance. Proc Natl Acad Sci U S A 110: 3047-3052. doi:10.1073/pnas.1211248110. PubMed: 23382221.
68. Blachier F, Boutry C, Bos C, Tomé D, (2009) Metabolism and functions of L-glutamate in the epithelial cells of the small and large intestines. Am J Clin Nutr 90: 814S-821S. doi:10.3945/ajcn.2009.27462S. PubMed: 19571215.
69. Newsholme P, Procopio J, Lima MM, Pithon-Curi TC, Curi R, (2003) Glutamine and glutamate--their central role in cell metabolism and function. Cell Biochem Funct 21: 1-9. doi:10.1002/cbf.1003. PubMed: 12579515.
70. Newsholme P, Curi R, Pithon Curi TC, Murphy CJ, Garcia C, et al. (1999) Glutamine metabolism by lymphocytes, macrophages, and neutrophils: its importance in health and disease. J Nutr Biochem 10: 316-324. doi:10.1016/S0955-2863(99)00022-4. PubMed: 15539305.
71. Wu G, Fang YZ, Yang S, Lupton JR, Turner ND, (2004) Glutathione metabolism and its implications for health. J Nutr 134: 489-492. PubMed: 14988435.
72. Paolicchi A, Dominici S, Pieri L, Maellaro E, Pompella A, (2002) Glutathione catabolism as a signaling mechanism. Biochem Pharmacol 64: 1027-1035. doi:10.1016/S0006-2952(02)01173-5. PubMed: 12213602.
73. Maellaro E, Dominici S, Del Bello B, Valentini MA, Pieri L, et al. (2000) Membrane gamma-glutamyl transpeptidase activity of melanoma cells: effects on cellular H(2)O(2) production, cell surface protein thiol oxidation and NF-kappa B activation status. J Cell Sci 113(Pt 15): 2671-2678 PubMed: 10893182.
74. Zhou L, Chong MM, Littman DR, (2009) Plasticity of CD4+ T cell lineage differentiation. Immunity 30: 646-655. doi:10.1016/j.immuni.2009.05.001. PubMed: 19464987.