Helicobacter pylori cell translocating kinase (CtkA/JHP0940) is pro-apoptotic in mouse macrophages and acts as auto-phosphorylating tyrosine kinase

International Journal of Medical Microbiology

Volumn 304, Issue 8, 2014, Pages 1066-1076

  Tenguria, Shivendra ^a   Ansari, Suhail A ^a   Khan, Nooruddin ^a   Ranjan, Amit ^a   Devi, Savita ^a   Tegtmeyer, Nicole ^b   Lind, Judith ^b   Backert, Steffen ^b   Ahmed, Niyaz ^a  

^a UNIVERSITY OF HYDERABAD   (India)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Apoptosis; H. pylori; Inflammation; JHP0940; Kinases; Plasticity region

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; JHP 0940; PROTEIN TYROSINE KINASE; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; BACTERIAL CELL; BACTERIAL SECRETION SYSTEM; CELL VIABILITY; CHRONIC INFLAMMATION; DRUG EXPOSURE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HELICOBACTER PYLORI; IN VITRO STUDY; INCUBATION TIME; INNATE IMMUNITY; MACROPHAGE; MOUSE; NICK END LABELING; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 84940166533     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2014.07.017     Document Type: Article

References (58)

1. Alm R.A., Ling L.S., Moir D.T., King B.L., Brown E.D., Doig P.C., Smith D.R., Noonan B., Guild B.C., deJonge B.L., Carmel G., Tummino P.J., Caruso A., Uria-Nickelsen M., Mills D.M., Ives C., Gibson R., Merberg D., Mills S.D., Jiang Q., Taylor D.E., Vovis G.F., Trust T.J. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 1999, 397:176-180.
2. Alvi A., Ansari S.A., Ehtesham N.Z., Rizwan M., Devi S., Sechi L.A., Qureshi I.A., Hasnain S.E., Ahmed N. Concurrent proinflammatory and apoptotic activity of a Helicobacter pylori protein (HP986) points to its role in chronic persistence. PLoS One 2011, 6:e22530.
3. Backert S., Tegtmeyer N., Selbach M. The versatility of Helicobacter pylori CagA effector protein functions: the master key hypothesis. Helicobacter 2010, 15:163-176.
4. Barila D., Rufini A., Condo I., Ventura N., Dorey K., Superti-Furga G., Testi R. Caspase-dependent cleavage of c-Abl contributes to apoptosis. Mol. Cell Biol. 2003, 23:2790-2799.
5. Basso D., Plebani M., Kusters J.G. Pathogenesis of Helicobacter pylori infection. Helicobacter 2010, 15(Suppl 1):14-20.
6. Boehm M., Hoy B., Rohde M., Tegtmeyer N., Bæk K.T., Oyarzabal O.A., Brøndsted L., Wessler S., Backert S. Rapid paracellular transmigration of Campylobacter jejuni across polarized epithelial cells without affecting TER: role of proteolytic-active HtrA cleaving E-cadherin but not fibronectin. Gut Pathog. 2012, 4:3.
7. Cheng Y., Zhang C., Zhao J., Wang C., Xu Y., Han Z., Jiang G., Guo X., Li R., Bu X., Wu M., Wei L. Correlation of CpG island methylator phenotype with poor prognosis in hepatocellular carcinoma. Exp. Mol. Pathol. 2010, 88:112-117.
8. Chuang Y.T., Lin Y.C., Lin K.H., Chou T.F., Kuo W.C., Yang K.T., Wu P.R., Chen R.H., Kimchi A., Lai M.Z. Tumor suppressor death-associated protein kinase is required for full IL-1beta production. Blood 2011, 117:960-970.
9. Conradi J., Tegtmeyer N., Woźna M., Wissbrock M., Michalek C., Gagell C., Cover T.L., Frank R., Sewald N., Backert S. An RGD helper sequence in CagL of Helicobacter pylori assists in interactions with integrins and injection of CagA. Front. Cell Infect. Microbiol. 2012, 2:70.
10. Covacci A., Censini S., Bugnoli M., Petracca R., Burroni D., Macchia G., Massone A., Papini E., Xiang Z., Figura N., et al. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc. Nat Acad. Sci. U.S.A. 1993, 90:5791-5795.
11. Covacci A., Telford J.L., Del Giudice G., Parsonnet J., Rappuoli R. Helicobacter pylori virulence and genetic geography. Science 1999, 284:1328-1333.
12. Cover T.L., Blanke S.R. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat. Rev. Microbiol. 2005, 3:320-332.
13. Cover T.L., Blaser M.J. Purification and characterization of the vacuolating toxin from Helicobacter pylori. J. Biol. Chem. 1992, 267:10570-10575.
14. Datta S., Khan A., Nandy R.K., Rehman M., Sinha S., Chattopadhyay S., Das S.C., Nair G.B. Environmental isolates of Aeromonas spp. harboring the cagA-like gene of Helicobacter pylori. Appl. Environ. Microbiol. 2003, 69:4291-4295.
15. Devi S., Ansari S.A., Vadivelu J., Megraud F., Tenguria S., Ahmed N. Helicobacter pylori antigen HP0986 (TieA) interacts with cultured gastric epithelial cells and induces IL8 secretion via NF-kappaB mediated pathway. Helicobacter 2014, 19:26-36.
16. Dinarello C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 2009, 27:519-550.
17. Donaldson L.W., Gish G., Pawson T., Kay L.E., Forman-Kay J.D. Structure of a regulatory complex involving the Abl SH3 domain, the Crk SH2 domain, and a Crk-derived phosphopeptide. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14053-14058.
18. Ferlay J., Shin H.R., Bray F., Forman D., Mathers C., Parkin D.M. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 2010, 127:2893-2917.
19. Fernandez-Gonzalez E., Backert S. DNA transfer in the gastric pathogen Helicobacter pylori. J. Gastroenterol. 2014, 49:594-604.
20. Gardy J.L., Spencer C., Wang K., Ester M., Tusnady G.E., Simon I., Hua S., deFays K., Lambert C., Nakai K., Brinkman F.S. PSORT-B: Improving protein subcellular localization prediction for Gram-negative bacteria. Nucleic Acids Res. 2003, 31:3613-3617.
21. Gong J., Traganos F., Darzynkiewicz Z. A selective procedure for DNA extraction from apoptotic cells applicable for gel electrophoresis and flow cytometry. Anal. Biochem. 1994, 218:314-319.
22. Graham D.Y. Helicobacter pylori infection in the pathogenesis of duodenal ulcer and gastric cancer: a model. Gastroenterology 1997, 113:1983-1991.
23. Graham J.E., Peek R.M., Krishna U., Cover T.L. Global analysis of Helicobacter pylori gene expression in human gastric mucosa. Gastroenterology 2002, 123:1637-1648.
24. Gu J.J., Lavau C.P., Pugacheva E., Soderblom E.J., Moseley M.A., Pendergast A.M. Abl family kinases modulate T cell-mediated inflammation and chemokine-induced migration through the adaptor HEF1 and the GTPase Rap1. Sci. Signal. 2012, 5:ra51.
25. Hitzler I., Sayi A., Kohler E., Engler D.B., Koch K.N., Hardt W.D., Muller A. Caspase-1 has both proinflammatory and regulatory properties in Helicobacter infections, which are differentially mediated by its substrates IL-1beta and IL-18. J. Immunol. 2012, 188:3594-3602.
26. Hoy B., Geppert T., Boehm M., Reisen F., Plattner P., Gadermaier G., Sewald N., Ferreira F., Briza P., Schneider G., Backert S., Wessler S. Distinct roles of secreted HtrA proteases from gram-negative pathogens in cleaving the junctional protein and tumor suppressor E-cadherin. J. Biol. Chem. 2012, 287:10115-10120.
27. Hunt R.H., Xiao S.D., Megraud F., Leon-Barua R., Bazzoli F., van der Merwe S., Vaz Coelho L.G., Fock M., Fedail S., Cohen H., Malfertheiner P., Vakil N., Hamid S., Goh K.L., Wong B.C., Krabshuis J., Le Mair A. Helicobacter pylori in developing countries World Gastroenterology Organisation Global Guideline. J. Gastrointestin Liver Dis. 2011, 20:299-304.
28. Hussein N.R., Argent R.H., Marx C.K., Patel S.R., Robinson K., Atherton J.C. Helicobacter pylori dupA is polymorphic, and its active form induces proinflammatory cytokine secretion by mononuclear cells. J. Infect. Dis. 2010, 202:261-269.
29. Kersulyte D., Velapatino B., Mukhopadhyay A.K., Cahuayme L., Bussalleu A., Combe J., Gilman R.H., Berg D.E. Cluster of type IV secretion genes in Helicobacter pylori's plasticity zone. J. Bacteriol. 2003, 185:3764-3772.
30. Khan N., Rahim S.S., Boddupalli C.S., Ghousunnissa S., Padma S., Pathak N., Thiagarajan D., Hasnain S.E., Mukhopadhyay S. Hydrogen peroxide inhibits IL-12 p40 induction in macrophages by inhibiting c-rel translocation to the nucleus through activation of calmodulin protein. Blood 2006, 107:1513-1520.
31. Kim do J., Park K.S., Kim J.H., Yang S.H., Yoon J.Y., Han B.G., Kim H.S., Lee S.J., Jang J.Y., Kim K.H., Kim M.J., Song J.S., Kim H.J., Park C.M., Lee S.K., Lee B.I., Suh S.W. Helicobacter pylori proinflammatory protein up-regulates NF-kappaB as a cell-translocating Ser/Thr kinase. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:21418-21423.
32. Kim D.J., Park J.H., Franchi L., Backert S., Núñez G. The Cag pathogenicity island and interaction between TLR2/NOD2 and NLRP3 regulate IL-1β production in Helicobacter pylori infected dendritic cells. Eur. J. Immunol. 2013, 43:2650-2658.
33. Kumar A., Lewin A., Rani P.S., Qureshi I.A., Devi S., Majid M., Kamal E., Marek S., Hasnain S.E., Ahmed N. Dormancy Associated Translation Inhibitor (DATIN/Rv0079) of Mycobacterium tuberculosis interacts with TLR2 and induces proinflammatory cytokine expression. Cytokine 2013, 64:258-264.
34. Lind J., Backert S., Pfleiderer K., Berg D.E., Yamaoka Y., Sticht H., Tegtmeyer N. Systematic analysis of phosphotyrosine antibodies recognizing single phosphorylated EPIYA-Motifs in CagA of western-type Helicobacter pylori strains. PLoS One 2014, 9:e96488.
35. Malaty H.M., Graham D.Y. Importance of childhood socioeconomic status on the current prevalence of Helicobacter pylori infection. Gut 1994, 35:742-745.
36. Marshall B.J., Warren J.R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984, 1:1311-1315.
37. Martinon F., Mayor A., Tschopp J. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 2009, 27:229-265.
38. McGovern K.J., Blanchard T.G., Gutierrez J.A., Czinn S.J., Krakowka S., Youngman P. Gamma-glutamyltransferase is a Helicobacter pylori virulence factor but is not essential for colonization. Infect. Immun. 2001, 69:4168-4173.
39. Mueller D., Tegtmeyer N., Brandt S., Yamaoka Y., De Poire E., Sgouras D., Wessler S., Torres J., Smolka A., Backert S. c-Src and c-Abl kinases control hierarchic phosphorylation and function of the CagA effector protein in Western and East Asian Helicobacter pylori strains. J. Clin. Invest. 2012, 122:1553-1566.
40. Occhialini A., Marais A., Alm R., Garcia F., Sierra R., Megraud F. Distribution of open reading frames of plasticity region of strain J99 in Helicobacter pylori strains isolated from gastric carcinoma and gastritis patients in Costa Rica. Infect. Immun. 2000, 68:6240-6249.
41. Odenbreit S., Swoboda K., Barwig I., Ruhl S., Boren T., Koletzko S., Haas R. Outer membrane protein expression profile in Helicobacter pylori clinical isolates. Infect. Immun. 2009, 77:3782-3790.
42. Pachathundikandi S.K., Tegtmeyer N., Backert S. Signal transduction of Helicobacter pylori during interaction with host cell protein receptors of epithelial and immune cells. Gut Microbes 2013, 4(6):454-474.
43. Raina D., Pandey P., Ahmad R., Bharti A., Ren J., Kharbanda S., Weichselbaum R., Kufe D. c-Abl tyrosine kinase regulates caspase-9 autocleavage in the apoptotic response to DNA damage. J. Biol. Chem. 2005, 280:11147-11151.
44. Replogle M.L., Glaser S.L., Hiatt R.A., Parsonnet J. Biologic sex as a risk factor for Helicobacter pylori infection in healthy young adults. Am. J. Epidemiol. 1995, 142:856-863.
45. Rizwan M., Alvi A., Ahmed N. Novel protein antigen (JHP940) from the genomic plasticity region of Helicobacter pylori induces tumor necrosis factor alpha and interleukin-8 secretion by human macrophages. J. Bacteriol. 2008, 190:1146-1151.
46. Santos A., Queiroz D.M., Menard A., Marais A., Rocha G.A., Oliveira C.A., Nogueira A.M., Uzeda M., Megraud F. New pathogenicity marker found in the plasticity region of the Helicobacter pylori genome. J. Clin. Microbiol. 2003, 41:1651-1655.
47. Satin B., Del Giudice G., Della Bianca V., Dusi S., Laudanna C., Tonello F., Kelleher D., Rappuoli R., Montecucco C., Rossi F. The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a protective antigen and a major virulence factor. J. Exp. Med. 2000, 191:1467-1476.
48. Schmidt H.M., Andres S., Kaakoush N.O., Engstrand L., Eriksson L., Goh K.L., Fock K.M., Hilmi I., Dhamodaran S., Forman D., Mitchell H. The prevalence of the duodenal ulcer promoting gene (dupA) in Helicobacter pylori isolates varies by ethnic group and is not universally associated with disease development: a case-control study. Gut Pathog. 2009, 1:5.
49. Shiota S., Matsunari O., Watada M., Hanada K., Yamaoka Y. Systematic review and meta-analysis: the relationship between the Helicobacter pylori dupA gene and clinical outcomes. Gut Pathog. 2010, 2:13.
50. Snelling W.J., Moran A.P., Ryan K.A., Scully P., McGourty K., Cooney J.C., Annuk H., O'Toole P.W. HorB (HP0127) is a gastric epithelial cell adhesin. Helicobacter 2007, 12:200-209.
51. Tegtmeyer N., Wittelsberger R., Hartig R., Wessler S., Martinez-Quiles N., Backert S. Serine phosphorylation of cortactin controls focal adhesion kinase activity and cell scattering induced by Helicobacter pylori. Cell Host Microbe 2011, 9:520-531.
52. Tegtmeyer N., Rivas Traverso F., Rohde M., Oyarzabal O.A., Lehn N., Schneider-Brachert W., Ferrero R.L., Fox J.G., Berg D.E., Backert S. Electron microscopic, genetic and protein expression analyses of Helicobacter acinonychis strains from a Bengal tiger. PLoS One 2013, 8:e71220.
53. Uemura N., Okamoto S., Yamamoto S., Matsumura N., Yamaguchi S., Yamakido M., Taniyama K., Sasaki N., Schlemper R.J. Helicobacter pylori infection and the development of gastric cancer. N. Engl. J. Med. 2001, 345:784-789.
54. van de Veerdonk F.L., Netea M.G., Dinarello C.A., Joosten L.A. Inflammasome activation and IL-1beta and IL-18 processing during infection. Trends Immunol. 2011, 32:110-116.
55. von Moltke J., Ayres J.S., Kofoed E.M., Chavarria-Smith J., Vance R.E. Recognition of bacteria by inflammasomes. Annu. Rev. Immunol. 2013, 31:73-106.
56. Xu Q., Morgan R.D., Roberts R.J., Xu S.Y., van Doorn L.J., Donahue J.P., Miller G.G., Blaser M.J. Functional analysis of iceA1, a CATG-recognizing restriction endonuclease gene in Helicobacter pylori. Nucleic Acids Res. 2002, 30:3839-3847.
57. Yakoob J., Abbas Z., Naz S., Islam M., Abid S., Jafri W. Associations between the plasticity region genes of Helicobacter pylori and gastroduodenal diseases in a high-prevalence area. Gut Liver 2010, 4:345-350.
58. Yamaoka Y. Roles of the plasticity regions of Helicobacter pylori in gastroduodenal pathogenesis. J. Med. Microbiol. 2008, 57:545-553.