Systems modeling of the role of interleukin-21 in the maintenance of effector CD4+T cell responses during chronic Helicobacter pylori infection

mBio

Volumn 5, Issue 4, 2014, Pages 1-11

  Carbo, Adria ^c   Olivares Villagómez, Danyvid ^b   Hontecillas, Raquel ^c   Bassaganya Riera, Josep ^c   Chaturvedi, Rupesh ^b   Blanca Piazuelo, M ^b   Delgado, Alberto ^b   Kay Washington, M ^b   Wilson, Keith T ^a,b   Scott Algood, Holly M ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 21; RETINOID RELATED ORPHAN RECEPTOR GAMMA; STAT1 PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR T BET; INTERLEUKIN DERIVATIVE; STAT1 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME MECHANISM; FEMALE; GASTRITIS; GENE EXPRESSION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; IN VIVO STUDY; INTESTINE FLORA; MALE; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; RORC GENE; STOMACH CANCER; TBX21 GENE; TH1 CELL; TH17 CELL; ANIMAL; C57BL MOUSE; FLOW CYTOMETRY; GENETICS; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHOSPHORYLATION; STOMACH; THEORETICAL MODEL;

HELICOBACTER PYLORI;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; INTERLEUKINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, THEORETICAL; PHOSPHORYLATION; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; STOMACH;

EID: 85003047735     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01243-14     Document Type: Article

References (52)

1. Algood HM, Cover TL. 2006. Helicobacter pylori persistence: an overview of interactions between H. pylori and host immune defenses. Clin. Microbiol. Rev. 19:597-613. http://dx.doi.org/10.1128/CMR.00006-06.
2. Blaser MJ, Atherton JC. 2004. Helicobacter pylori persistence: biology and disease. J. Clin. Invest. 113:321-333. http://dx.doi.org/10.1172/JCI20925.
3. Peek RM, Jr, Fiske C, Wilson KT. 2010. Role of innate immunity in Helicobacter pylori-induced gastric malignancy. Physiol. Rev. 90:831-858. http://dx.doi.org/10.1152/physrev.00039.2009.
4. Blaser MJ. 2008. Disappearing microbiota: Helicobacter pylori protection against esophageal adenocarcinoma. Cancer. Prev. Res. (Phila.) 1:308-311. http://dx.doi.org/10.1158/1940-6207.CAPR-08-0170.
5. Vieth M, Masoud B, Meining A, Stolte M. 2000. Helicobacter pylori infection: protection against Barrett’s mucosa and neoplasia? Digestion 62:225-231. http://dx.doi.org/10.1159/000007820.
6. Vaezi MF, Falk GW, Peek RM, Vicari JJ, Goldblum JR, Perez-Perez GI, Rice TW, Blaser MJ, Richter JE. 2000. CagA-positive strains of Helicobacter pylori may protect against Barrett’s esophagus. Am. J. Gastroenterol. 95: 2206-2211. http://dx.doi.org/10.1111/j.1572-0241.2000.02305.x.
7. Chow WH, Blaser MJ, Blot WJ, Gammon MD, Vaughan TL, Risch HA, Perez-Perez GI, Schoenberg JB, Stanford JL, Rotterdam H, West AB, Fraumeni JF, Jr.. 1998. An inverse relation between cagA_strains of Helicobacter pylori infection and risk of esophageal and gastric cardia adenocarcinoma. Cancer Res. 58:588-590.
8. Blaser MJ, Chen Y, Reibman J. 2008. Does Helicobacter pylori protect against asthma and allergy? Gut 57:561-567. http://dx.doi.org/10.1136/gut.2007.133462.
9. Chen Y, Blaser MJ. 2008. Helicobacter pylori colonization is inversely associated with childhood asthma. J. Infect. Dis. 198:553-560. http://dx.doi.org/10.1086/590158.
10. Lang L. 2007. Childhood acquisition of Helicobacter pylori linked to reduced asthma and allergy risk. Gastroenterology 133:6. http://dx.doi.org/10.1053/S0016-5085(07)01419-9.
11. McCune A, Lane A, Murray L, Harvey I, Nair P, Donovan J, Harvey R. 2003. Reduced risk of atopic disorders in adults with Helicobacter pylori infection. Eur. J. Gastroenterol. Hepatol. 15:637-640. http://dx.doi.org/10.1097/00042737-200306000-00010.
12. Algood HM, Gallo-Romero J, Wilson KT, Peek RM, Jr, Cover TL. 2007. Host response to Helicobacter pylori infection before initiation of the adaptive immune response. FEMS Immunol. Med. Microbiol. 51:577-586. http://dx.doi.org/10.1111/j.1348-0421.2007.tb03935.x.
13. Wilson KT, Crabtree JE. 2007. Immunology of Helicobacter pylori: insights into the failure of the immune response and perspectives on vaccine studies. Gastroenterology 133:288-308. http://dx.doi.org/10.1053/j.gastro.2007.05.008.
14. Malfertheiner P, Bazzoli F, Delchier JC, Celinski K, Giguere M, Riviere M, Megraud F, Study Pylera Group. 2011. Helicobacter pylori eradication with a capsule containing bismuth subcitrate potassium, metronidazole, and tetracycline given with omeprazole versus clarithromycin-based triple therapy: a randomised, open-label, non-inferiority, phase 3 trial. Lancet 377:905-913.
15. Carbo A, Bassaganya-Riera J, Pedragosa M, Viladomiu M, Marathe M, Eubank S, Wendelsdorf K, Bisset K, Hoops S, Deng X, Alam M, Kronsteiner B, Mei Y, Hontecillas R. 2013. Predictive computational modeling of the mucosal immune responses during Helicobacter pylori infection. PLoS One 8:e73365. http://dx.doi.org/10.1371/journal.pone.0073365.
16. Karttunen R, Karttunen T, Ekre HP, MacDonald TT. 1995. Interferon gamma and interleukin 4 secreting cells in the gastric antrum in Helicobacter pylori positive and negative gastritis. Gut 36:341-345. http://dx.doi.org/10.1136/gut.36.3.341.
17. Haeberle HA, Kubin M, Bamford KB, Garofalo R, Graham DY, El-Zaatari F, Karttunen R, Crowe SE, Reyes VE, Ernst PB. 1997. Differential stimulation of interleukin-12 (IL-12) and IL-10 by live and killed Helicobacter pylori in vitro and association of IL-12 production with gamma interferon-producing T cells in the human gastric mucosa. Infect. Immun. 65:4229-4235.
18. Bamford KB, Fan X, Crowe SE, Leary JF, Gourley WK, Luthra GK, Brooks EG, Graham DY, Reyes VE, Ernst PB. 1998. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 114:482-492. http://dx.doi.org/10.1016/S0016-5085(98)70531-1.
19. Lindholm C, Quiding-Järbrink M, Lönroth H, Hamlet A, Svennerholm AM. 1998. Local cytokine response in Helicobacter pylori-infected subjects. Infect. Immun. 66:5964-5971.
20. Sommer F, Faller G, Konturek P, Kirchner T, Hahn EG, Zeus J, Röllinghoff M, Lohoff M. 1998. Antrum-and corpus mucosa-infiltrating CD4(+) lymphocytes in Helicobacter pylori gastritis display a Th1 phenotype. Infect. Immun. 66:5543-5546.
21. Luzza F, Parrello T, Sebkova L, Pensabene L, Imeneo M, Mancuso M, La Vecchia AM, Monteleone G, Strisciuglio P, Pallone F. 2001. Expression of proinflammatory and Th1 but not Th2 cytokines is enhanced in gastric mucosa of Helicobacter pylori infected children. Dig. Liver Dis. 33:14-20. http://dx.doi.org/10.1016/S1590-8658(01)80130-4.
22. Itoh T, Yoshida M, Chiba T, Kita T, Wakatsuki Y. 2003. A coordinated cytotoxic effect of IFN-gamma and cross-reactive antibodies in the pathogenesis of Helicobacter pylori gastritis. Helicobacter 8:268-278. http://dx.doi.org/10.1046/j.1523-5378.2003.00154.x.
23. Mizuno T, Ando T, Nobata K, Tsuzuki T, Maeda O, Watanabe O, Minami M, Ina K, Kusugami K, Peek RM, Goto H. 2005. Interleukin-17 levels in Helicobacter pylori-infected gastric mucosa and pathologic sequelae of colonization. World J. Gastroenterol. 11:6305-6311.
24. Caruso R, Fina D, Paoluzi OA, Del Vecchio Blanco G, Stolfi C, Rizzo A, Caprioli F, Sarra M, Andrei F, Fantini MC, MacDonald TT, Pallone F, Monteleone G. 2008. IL-23-mediated regulation of IL-17 production in Helicobacter pylori-infected gastric mucosa. Eur. J. Immunol. 38:470-478. http://dx.doi.org/10.1002/eji.200737635.
25. Sugimoto M, Ohno T, Graham DY, Yamaoka Y. 2009. Gastric mucosal interleukin-17 and-18 mRNA expression in Helicobacter pylori-induced Mongolian gerbils. Cancer Sci. 100:2152-2159. http://dx.doi.org/10.1111/j.1349-7006.2009.01291.x.
26. Horvath DJ, Jr, Washington MK, Cope VA, Algood HM. 2012. IL-23 contributes to control of chronic Helicobacter pylori infection and the development of T helper responses in a mouse model. Front. Immunol. 3:56.
27. Monteleone G, Pallone F, Macdonald TT. 2009. Interleukin-21 (IL-21)-mediated pathways in T cell-mediated disease. Cytokine Growth Factor Rev. 20:185-191. http://dx.doi.org/10.1016/j.cytogfr.2009.02.002.
28. Algood HM, Allen SS, Washington MK, Peek RM, Jr, Miller GG, Cover TL. 2009. Regulation of gastric B cell recruitment is dependent on IL-17 receptor A signaling in a model of chronic bacterial infection. J. Immunol. 183:5837-5846. http://dx.doi.org/10.4049/jimmunol.0901206.
29. Caruso R, Fina D, Peluso I, Fantini MC, Tosti C, Del Vecchio Blanco G, Paoluzi OA, Caprioli F, Andrei F, Stolfi C, Romano M, Ricci V, MacDonald TT, Pallone F, Monteleone G. 2007. IL-21 is highly produced in Helicobacter pylori-infected gastric mucosa and promotes gelatinases synthesis. J. Immunol. 178:5957-5965. http://dx.doi.org/10.4049/jimmunol.178.9.5957.
30. Philipson CW, Bassaganya-Riera J, Viladomiu M, Pedragosa M, Guerrant RL, Roche JK, Hontecillas R. 2013. The role of peroxisome proliferator-activated receptor gamma in immune responses to enteroaggregative Escherichia coli infection. PLoS One 8:e57812. http://dx.doi.org/10.1371/journal.pone.0057812.
31. Viladomiu M, Hontecillas R, Pedragosa M, Carbo A, Hoops S, Michalak P, Michalak K, Guerrant RL, Roche JK, Warren CA, Bassaganya-Riera J. 2012. Modeling the role of peroxisome proliferator-activated receptor gamma and microRNA-146 in mucosal immune responses to Clostridium difficile. PLoS One 7:e47525. http://dx.doi.org/10.1371/journal.pone.0047525.
32. Carbo A, Hontecillas R, Kronsteiner B, Viladomiu M, Pedragosa M, Lu P, Philipson CW, Hoops S, Marathe M, Eubank S, Bisset K, Wendelsdorf K, Jarrah A, Mei Y, Bassaganya-Riera J. 2013. Systems modeling of molecular mechanisms controlling cytokine-driven CD4+T cell differentiation and phenotype plasticity. PLoS Comput. Biol. 9:e1003027. http://dx.doi.org/10.1371/journal.pcbi.1003027.
33. Huber M, Brüstle A, Reinhard K, Guralnik A, Walter G, Mahiny A, von Löw E, Lohoff M. 2008. IRF4 is essential for IL-21-mediated induction, amplification, and stabilization of the Th17 phenotype. Proc. Natl. Acad. Sci. U. S. A. 105:20846-20851. http://dx.doi.org/10.1073/pnas.0809077106.
34. Zhu J, Paul WE. 2010. Peripheral CD4+T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol. Rev. 238: 247-262. http://dx.doi.org/10.1111/j.1600-065X.2010.00951.x.
35. Deenick EK, Tangye SG. 2007. Autoimmunity: IL-21: a new player in Th17-cell differentiation. Immunol. Cell Biol. 85:503-505. http://dx.doi.org/10.1038/sj.icb.7100114.
36. Cope A, Le Friec G, Cardone J, Kemper C. 2011. The Th1 life cycle: molecular control of IFN-gamma to IL-10 switching. Trends Immunol. 32:278-286. http://dx.doi.org/10.1016/j.it.2011.03.010.
37. Anderson CF, Oukka M, Kuchroo VJ, Sacks D. 2007. CD4(+)CD25(-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204:285-297. http://dx.doi.org/10.1084/jem.20061886.
38. Jankovic D, Kullberg MC, Feng CG, Goldszmid RS, Collazo CM, Wilson M, Wynn TA, Kamanaka M, Flavell RA, Sher A. 2007. Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204:273-283. http://dx.doi.org/10.1084/jem.20062175.
39. McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, McClanahan T, Cua DJ. 2007. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8:1390-1397. http://dx.doi.org/10.1038/ni1539.
40. Akhiani AA, Pappo J, Kabok Z, Schön K, Gao W, Franzén LE, Lycke N. 2002. Protection against Helicobacter pylori infection following immunization is IL-12-dependent and mediated by Th1 cells. J. Immunol. 169: 6977-6984. http://dx.doi.org/10.4049/jimmunol.169.12.6977.
41. 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. http://dx.doi.org/10.4049/jimmunol.166.12.7456.
42. Eaton KA, Benson LH, Haeger J, Gray BM. 2006. Role of transcription factor T-bet expression by CD4+cells in gastritis due to Helicobacter pylori in mice. Infect. Immun. 74:4673-4684. http://dx.doi.org/10.1128/IAI.01887-05.
43. Monteleone G, Monteleone I, Fina D, Vavassori P, Del Vecchio Blanco G, Caruso R, Tersigni R, Alessandroni L, Biancone L, Naccari GC, MacDonald TT, Pallone F. 2005. Interleukin-21 enhances T-helper cell type I signaling and interferon-gamma production in Crohn’s disease. Gastroenterology 128:687-694. http://dx.doi.org/10.1053/j.gastro.2004.12.042.
44. Fina D, Sarra M, Fantini MC, Rizzo A, Caruso R, Caprioli F, Stolfi C, Cardolini I, Dottori M, Boirivant M, Pallone F, Macdonald TT, Monteleone G. 2008. Regulation of gut inflammation and Th17 cell response by interleukin-21. Gastroenterology 134:1038-1048. http://dx.doi.org/10.1053/j.gastro.2008.01.041.
45. Herber D, Brown TP, Liang S, Young DA, Collins M, Dunussi-Joannopoulos K. 2007. IL-21 has a pathogenic role in a lupus-prone mouse model and its blockade with IL-21R.Fc reduces disease progression. J. Immunol. 178:3822-3830. http://dx.doi.org/10.4049/jimmunol.178.6.3822.
46. Young DA, Hegen M, Ma HL, Whitters MJ, Albert LM, Lowe L, Senices M, Wu PW, Sibley B, Leathurby Y, Brown TP, Nickerson-Nutter C, Keith JC, Jr, Collins M. 2007. Blockade of the interleukin-21/interleukin-21 receptor pathway ameliorates disease in animal models of rheumatoid arthritis. Arthritis Rheum. 56:1152-1163. http://dx.doi.org/10.1002/art.22452.
47. Terrier B, Costedoat-Chalumeau N, Garrido M, Geri G, Rosenzwajg M, Musset L, Klatzmann D, Saadoun D, Cacoub P. 2012. Interleukin 21 correlates with T cell and B cell subset alterations in systemic lupus erythematosus. J. Rheumatol. 39:1819-1828. http://dx.doi.org/10.3899/jrheum.120468.
48. Horvath DJ, Jr, Radin JN, Cho SH, Washington MK, Algood HM. 2013. The interleukin-17 receptor B subunit is essential for the Th2 response to Helicobacter pylori, but not for control of bacterial burden. PLoS One 8:e60363. http://dx.doi.org/10.1371/journal.pone.0060363.
49. Elias JM, Greene C. 1979. Modified Steiner method for the demonstration of Spirochetes in tissue. Am. J. Clin. Pathol. 71:109-111.
50. Boivin GP, Washington K, Yang K, Ward JM, Pretlow TP, Russell R, Besselsen DG, Godfrey VL, Doetschman T, Dove WF, Pitot HC, Halberg RB, Itzkowitz SH, Groden J, Coffey RJ. 2003. Pathology of mouse models of intestinal cancer: consensus report and recommendations. Gastroenterology 124:762-777. http://dx.doi.org/10.1016/S0016-5085(03)83849-0.
51. Franco AT, Israel DA, Washington MK, Krishna U, Fox JG, Rogers AB, Neish AS, Collier-Hyams L, Perez-Perez GI, Hatakeyama M, Whitehead R, Gaus K, O’Brien DP, Romero-Gallo J, Peek RM, Jr.. 2005. Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc. Natl. Acad. Sci. U. S. A. 102:10646-10651. http://dx.doi.org/10.1073/pnas.0504927102.
52. Romero-Gallo J, Harris EJ, Krishna U, Washington MK, Perez-Perez GI, Peek RM, Jr. 2008. Effect of Helicobacter pylori eradication on gastric carcinogenesis. Lab. Invest. 88:328-336. http://dx.doi.org/10.1038/labinvest.3700719.