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Role of Campylobacter Jejuni Gamma-Glutamyl Transpeptidase On Floch et al. Gut Pathogens 2014, 6:20 http://www.gutpathogens.com/content/6/1/20 RESEARCH Open Access Role of Campylobacter jejuni gamma-glutamyl transpeptidase on epithelial cell apoptosis and lymphocyte proliferation Pauline Floch1,2, Vincent Pey1,2, Michel Castroviejo3, Jean William Dupuy4, Marc Bonneu4, Anaïs Hocès de la Guardia1,2, Vincent Pitard5, Francis Mégraud1,2 and Philippe Lehours1,2,6* Abstract Background: A gamma-glutamyl transpeptidase (GGT) is produced by up to 31% of strains of Campylobacter jejuni isolates. C. jejuni GGT is close to Helicobacter pylori GGT suggesting a conserved activity but unlike the latter, C. jejuni GGT has not been studied extensively. In line with the data available for H. pylori, our objectives were to purify C. jejuni GGT from the bacteria, and to evaluate its inhibitory and proapoptotic activities on epithelial cells and human lymphocytes. Methods: C. jejuni GGT was purified from culture supernatants by chromatography. After verification of the purity by using mass spectrometry of the purified enzyme, its action on two epithelial cell lines and human lymphocytes was investigated. Cell culture as well as flow cytometry experiments were developed for these purposes. Results: This study demonstrated that C. jejuni GGT is related to Helicobacter GGTs and inhibits the proliferation of epithelial cells with no proapoptotic activity. C. jejuni GGT also inhibits lymphocyte proliferation by causing a cell cycle arrest in the G0/G1 phase. These effects are abolished in the presence of a specific pharmacological inhibitor of GGT. Conclusion: C. jejuni GGT activity is comparable to that of other Epsilonproteobacteria GGTs and more generally to Helicobacter bilis (inhibition of epithelial cell and lymphocyte proliferation, however with no proapoptotic activity). It could therefore be considered as a pathogenicity factor and promote, via the inhibition of lymphocyte proliferation, the persistence of the bacteria in the host. These observations are consistent with a role of this enzyme in the pathophysiology of chronic infections associated with C. jejuni. Keywords: Campylobacter jejuni, GGT, Lymphocytes, Epithelial cells Background in immunoproliferative small intestinal disease (IPSID) [2] Campylobacter jejuni is the main Campylobacter species which belongs to the group of digestive mucosa associated isolated from humans. The C. jejuni reservoir consists es- lymphoid tissue (MALT) lymphomas. sentially of the digestive tract of birds, including poultry. In Helicobacter pylori, a bacterium close to C. jejuni, Transmission to humans occurs mainly indirectly via the role of gamma-glutamyl transpeptidase (GGT) has food or contaminated water [1]. In humans, Campylo- been extensively studied [3-5]. GGT is an enzyme belong- bacters induce enteritis generally with a favourable evo- ing to the family of N-terminal nucleophile hydrolases, lution after a few days but with potential complications present in prokaryotes and eukaryotes, playing a major like systemic infections or post-infectious diseases role in the degradation of glutathione. GGTs of distant (Guillain–Barré syndrome). C. jejuni may also be involved species (mammals and bacteria) often exhibit a high pro- tein sequence identity (>25%) [6,7]. H. pylori GGT has been the subject of numerous stu- * Correspondence: [email protected] 1Bacteriology Laboratory, University of Bordeaux, F-33000 Bordeaux, France dies. It is present in 100% of the strains and is constitu- 2INSERM U853, F-33000 Bordeaux, France tively expressed. It can reach the periplasmic space thanks Full list of author information is available at the end of the article © 2014 Floch et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Floch et al. Gut Pathogens 2014, 6:20 Page 2 of 10 http://www.gutpathogens.com/content/6/1/20 to its signal peptide. It is synthesized as an inactive 60 kDa Two bands at approximately 40 and 20 kDa were ob- precursor which undergoes autocatalytic cleavage result- served on the gel after the final purification, which is ing in an active heterodimer composed of two subunits of consistent with the expected molecular weights of the 20 and 40 kDa respectively. The small subunit plays a key large and small subunit of C. jejuni GGT, respectively. role in the autocatalytic and enzymatic activity of GGT; it These bands were cut and analyzed by mass spectrom- includes the active site of the enzyme [6,8]. This enzyme is etry (after extraction and protein digestion). The results not essential to the bacteria, as ggt gene deletion does not showed the presence of C. jejuni GGT with a significant inhibit bacterial growth, but it provides an advantage in number of peptides (Figure 1B): the amino-acids found gastric colonization [3]. H. pylori GGT also plays a role in in the 40 kDa band represent 73.6% of the protein se- the inhibition of T-lymphocyte proliferation by blocking quence of the large subunit of C. jejuni GGT and those the cell cycle in the G1 phase [5]. In addition, several stud- found in the 20 kDa band represent 68.8% of the protein ies have shown that H. pylori GGT has a proapoptotic ef- sequence of the small subunit. fect on human gastric epithelial cells (AGS line) [9-11]. C. jejuni GGT has been studied less. It is present in up C. jejuni GGT effects on epithelial cells to 31% of strains [12] and has 67 to 69% of amino-acid The gastric epithelial cell line AGS was cultured for 24 h identity with H. pylori GGT. The cleavage site, the essen- in media supplemented with 2.5 to 320 ng/mL of purified tial residues for enzymatic activity, substrate recognition GGT with or without acivicin to determine the optimal and catalytic activity for H. pylori GGT are conserved in concentration to evaluate GGT activity. At high concen- C. jejuni GGT. It allows C. jejuni to metabolize glutamine trations epithelial cell proliferation was strongly inhibited and glutathione as a source of amino acids and possibly to with or without GGT inactivation with acivicin suggesting persist in the intestine [13]. A Finnish study showed that an artifactual phenomenon. This artifactual effect was lost C. jejuni GGT could be a marker of severity of infection, at lower concentrations (Figure 2A). At 10 ng/mL of in particular for bloody diarrhea [14]. GGT, a significant reduction of AGS cell proliferation was In this study, we used phylogenetic and functional ap- still observed whereas acivicin restored a normal prolifera- proaches to analyze C. jejuni GGT. We showed that C. tion rate. This concentration was finally chosen as the jejuni GGT is related phylogenetically to Helicobacter lowest GGT concentration to be used. The activity of GGTs and, like H. pylori GGT, C. jejuni GGT inhibits GGT at 10 ng/mL was also verified on Caco-2 cell prolif- lymphocyte and epithelial cell proliferation. The inhi- eration (Figure 2B). Compared to AGS cells, GGT also bition observed was mediated by an apoptosis-independent had a significant effect on intestinal cell proliferation. mechanism, suggesting a conserved function among Trypan blue staining and cell counts after a 24 h incuba- GGTs in Epsilonproteobacteria. tion with C. jejuni GGT was used to verify that this inhibi- tory effect was not due to a cell death phenomenon, Results rather to a cell proliferation arrest (data not shown). Phylogenetic analysis The activity of C. jejuni GGT on apoptosis was then The phylogenetic position of C. jejuni GGT among Epsi- studied by flow cytometry on AGS cells only. Compared lonproteobacteria was analyzed (Additional file 1: Figure to the control, C. jejuni GGT induced a significant in- S1). C. jejuni GGT was closer to H. bilis, Helicobacter crease in the percentage of apoptosis (Figure 3A). canis and Helicobacter trogontum GGTs than to H. pyl- However, C. jejuni GGT preincubation with acivicin ori GGTs. C. jejuni GGTs appeared to be highly con- did not decrease the percentage of epithelial cells served, including those of H. pylori. undergoing apoptosis. In conclusion, the proapoptotic activity observed in the presence of C. jejuni GGT did C. jejuni GGT purification not seem to be dependent on the presence of GGT C. jejuni GGT was purified from a bacterial supernatant. (Figure 3B) but on contaminant proteins even when Briefly, as described in Materials and Methods, proteins they were in very small amounts in the final product. from a supernatant were first precipitated with ammo- nium sulfate. The supernatant was then dialyzed and C. jejuni GGT effects on human lymphocytes purified by two ion-exchange chromatographies. To de- Lymphocyte proliferation was measured after 4 days of termine the effectiveness of the purification, the dialys- culture in the presence of. C. jejuni GGT. A significant ate, the product obtained after the first chromatography inhibition of lymphocyte proliferation was observed. Pre- and the final product were analyzed by migration on a incubation of C. jejuni GGT with acivicin or heat inacti- SDS-PAGEgelandCoomassiebluestaining(Figure1A). vation of the enzyme, restored a level of lymphocyte Efficient purification was observed between the dialys- proliferation similar to that of the lymphocytes alone ate, the product of the first chromatography and the (Figure 4). The inhibition of lymphocyte proliferation final product. could therefore be attributed to the GGT. Floch et al. Gut Pathogens 2014, 6:20 Page 3 of 10 http://www.gutpathogens.com/content/6/1/20 No significant apoptosis was observed in the presence and H. trogontum, which suggests a conserved activity of C. jejuni GGT. The lymphocyte cell cycle was how- between these GGTs.
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