DC-LAMP+ dendritic cells are recruited to gastric lymphoid follicles in helicobacter pylori-infected individuals

Infection and Immunity

Volumn 81, Issue 10, 2013, Pages 3684-3692

  Hansson, Malin ^a   Sundquist, Malin ^a   Hering, Susanne ^a   Lundin, B Samuel ^a   Hermansson, Michael ^b   Quiding Järbrink, Marianne ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR7; DENDRITIC CELL LYSOSOME ASSOCIATED MEMBRANE PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MESSENGER RNA; SECONDARY LYMPHOID TISSUE CHEMOKINE; TRANSCRIPTION FACTOR FOXP3;

ADULT; AGED; ANTIGEN PRESENTATION; ARTICLE; BACTERIAL LOAD; CELL INTERACTION; CELL MATURATION; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GASTRECTOMY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; LYMPH FOLLICLE; MALE; NONHUMAN; PRIMARY IMMUNE RESPONSE; PRIORITY JOURNAL; PROTEIN PURIFICATION; REGULATORY T LYMPHOCYTE; STOMACH ANTRUM; STOMACH BIOPSY; STOMACH MUCOSA;

ADULT; AGED; CASE-CONTROL STUDIES; DENDRITIC CELLS; FEMALE; GASTRITIS; GENE EXPRESSION REGULATION; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; INFLAMMATION; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 3; MALE; MIDDLE AGED; STOMACH; YOUNG ADULT;

EID: 84884365684     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00801-13     Document Type: Article

References (67)

1. Fischbach W, Chan AO, Wong BC. 2005. Helicobacter pylori and gastric malignancy. Helicobacter 10(Suppl 1):34-39.
2. Huang JQ, Sridhar S, Hunt RH. 2002. Role of Helicobacter pylori infection and non-steroidal anti-inflammatory drugs in peptic-ulcer disease: a meta-analysis. Lancet 359:14-22.
3. Makola D, Peura DA, Crowe SE. 2007. Helicobacter pylori infection and related gastrointestinal diseases. J. Clin. Gastroenterol. 41:548-558.
4. Figueiredo C, Machado JC, Yamaoka Y. 2005. Pathogenesis of Helicobacter pylori infection. Helicobacter 10(Suppl 1):14-20.
5. Del Giudice G, Michetti P. 2004. Inflammation, immunity and vaccines for Helicobacter pylori. Helicobacter 9(Suppl 1):23-28.
6. Genta RM, Hamner HW, Graham DY. 1993. Gastric lymphoid follicles in Helicobacter pylori infection: frequency, distribution, and response to triple therapy. Hum. Pathol. 24:577-583.
7. Houghton J, Wang TC. 2005. Helicobacter pylori and gastric cancer: a new paradigm for inflammation-associated epithelial cancers. Gastroenterology 128:1567-1578.
8. 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 infection have a T helper cell 1 phenotype. Gastroenterology 114:482-492.
9. Luzza F, Parrello T, Monteleone G, Sebkova L, Romano M, Zarrilli R, Imeneo M, Pallone F. 2000. Up-regulation of IL-17 is associated with bioactive IL-8 expression in Helicobacter pylori-infected human gastric mucosa. J. Immunol. 165:5332-5337.
10. Garhart CA, Redline RW, Nedrud JG, Czinn SJ. 2002. Clearance of Helicobacter pylori infection and resolution of postimmunization gastritis in a kinetic study of prophylactically immunized mice. Infect. Immun. 70:3529-3538.
11. Sayi A, Kohler E, Hitzler I, Arnold I, Schwendener R, Rehrauer H, Muller A. 2009. The CD4+ T cell-mediated IFN-gamma response to Helicobacter infection is essential for clearance and determines gastric cancer risk. J. Immunol. 182:7085-7101.
12. Lundgren A, Suri-Payer E, Enarsson K, Svennerholm AM, Lundin BS. 2003. Helicobacter pylori-specific CD4+ CD25high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals. Infect. Immun. 71:1755-1762.
13. Enarsson K, Lundgren A, Kindlund B, Hermansson M, Roncador G, Banham AH, Lundin BS, Quiding-Jarbrink M. 2006. Function and recruitment of mucosal regulatory T cells in human chronic Helicobacter pylori infection and gastric adenocarcinoma. Clin. Immunol. 121:358-368.
14. Lundgren A, Stromberg E, Sjoling A, Lindholm C, Enarsson K, Edebo A, Johnsson E, Suri-Payer E, Larsson P, Rudin A, Svennerholm AM, Lundin BS. 2005. Mucosal FOXP3-expressing CD4+ CD25high regulatory T cells in Helicobacter pylori-infected patients. Infect. Immun. 73:523-531.
15. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767-811.
16. Schuurhuis DH, Fu N, Ossendorp F, Melief CJ. 2006. Ins and outs of dendritic cells. Int. Arch. Allergy Immunol. 140:53-72.
17. Bar-On L, Jung S. 2010. Defining dendritic cells by conditional and constitutive cell ablation. Immunol. Rev. 234:76-89.
18. Kranzer K, Eckhardt A, Aigner M, Knoll G, Deml L, Speth C, Lehn N, Rehli M, Schneider-Brachert W. 2004. Induction of maturation and cytokine release of human dendritic cells by Helicobacter pylori. Infect. Immun. 72:4416-4423.
19. Hafsi N, Voland P, Schwendy S, Rad R, Reindl W, Gerhard M, Prinz C. 2004. Human dendritic cells respond to Helicobacter pylori, promoting NK cell and Th1-effector responses in vitro. J. Immunol. 173:1249-1257.
20. Guiney DG, Hasegawa P, Cole SP. 2003. Helicobacter pylori preferentially induces interleukin 12 (IL-12) rather than IL-6 or IL-10 in human dendritic cells. Infect. Immun. 71:4163-4166.
21. Hansson M, Lundgren A, Elgbratt K, Quiding-Jarbrink M, Svennerholm AM, Johansson EL. 2006. Dendritic cells express CCR7 and migrate in response to CCL19 (MIP-3beta) after exposure to Helicobacter pylori. Microbes Infect. 8:841-850.
22. Khamri W, Walker MM, Clark P, Atherton JC, Thursz MR, Bamford KB, Lechler RI, Lombardi G. 2010. Helicobacter pylori stimulates dendritic cells to induce interleukin-17 expression from CD4+ T lymphocytes. Infect. Immun. 78:845-853.
23. Andres S, Schmidt HM, Mitchell H, Rhen M, Maeurer M, Engstrand L. 2011. Helicobacter pylori defines local immune response through interaction with dendritic cells. FEMS Immunol. Med. Microbiol. 61:168-178.
24. Fehlings M, Drobbe L, Moos V, Renner Viveros P, Hagen J, Beigier-Bompadre M, Pang E, Belogolova E, Churin Y, Schneider T, Meyer TF, Aebischer T, Ignatius R. 2012. Comparative analysis of the interaction of Helicobacter pylori with human dendritic cells, macrophages, and monocytes. Infect. Immun. 80:2724-2734.
25. Bimczok D, Clements RH, Waites KB, Novak L, EckhoffDE, Mannon PJ, Smith PD, Smythies LE. 2010. Human primary gastric dendritic cells induce a Th1 response to H. pylori. Mucosal Immunol. 3:260-269.
26. Rad R, Ballhorn W, Voland P, Eisenacher K, Mages J, Rad L, Ferstl R, Lang R, Wagner H, Schmid RM, Bauer S, Prinz C, Kirschning CJ, Krug A. 2009. Extracellular and intracellular pattern recognition receptors cooperate in the recognition of Helicobacter pylori. Gastroenterology 136: 2247-2257.
27. Rad R, Brenner L, Krug A, Voland P, Mages J, Lang R, Schwendy S, Reindl W, Dossumbekova A, Ballhorn W, Wagner H, Schmid RM, Bauer S, Prinz C. 2007. Toll-like receptor-dependent activation of antigen-presenting cells affects adaptive immunity to Helicobacter pylori. Gastroenterology 133:150-163.e3.
28. Bergman MP, Engering A, Smits HH, van Vliet SJ, van Bodegraven AA, Wirth HP, Kapsenberg ML, Vandenbroucke-Grauls CM, van Kooyk Y, Appelmelk BJ. 2004. Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J. Exp. Med. 200:979-990.
29. Gringhuis SI, den Dunnen J, Litjens M, van der Vlist M, Geijtenbeek TB. 2009. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat. Immunol. 10:1081-1088.
30. Reis e Sousa C. 2006. Dendritic cells in a mature age. Nat. Rev. Immunol. 6:476-483.
31. Mitchell P, Germain C, Fiori PL, Kahmri W, Forster GR, Ghosh S, Lechler RI, Bamford KB, Lombardi G. 2007. Chronic exposure to Helicobacter pylori impairs dendritic cell function. Infect. Immun. 75:810-819.
32. Oertli M, Sundquist M, Hitzler I, Engler DB, Arnold IC, Reuter S, Maxeiner J, Hansson M, Taube C, Quiding-Jarbrink M, Muller A. 2012. DC-derived IL-18 drives Treg differentiation, murine Helicobacter pylorispecific immune tolerance, and asthma protection. J. Clin. Invest. 122: 1082-1096.
33. Quiding-Jarbrink M, Raghavan S, Sundquist M. 2010. Enhanced M1 macrophage polarization in human Helicobacter pylori-associated atrophic gastritis and in vaccinated mice. PLoS One 5:e15018. doi:10.1371/journal.pone.0015018.
34. Hitzler I, Oertli M, Becher B, Agger EM, Muller A. 2011. Dendritic cells prevent rather than promote immunity conferred by a Helicobacter vaccine using a mycobacterial adjuvant. Gastroenterology 141:186-196.
35. Kao JY, Zhang M, Miller MJ, Mills JC, Wang B, Liu M, Eaton KA, Zou W, Berndt BE, Cole TS, Takeuchi T, Owyang SY, Luther J. 2010. Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice. Gastroenterology 138:1046-1054.
36. Bimczok D, Grams JM, Stahl RD, Waites KB, Smythies LE, Smith PD. 2011. Stromal regulation of human gastric dendritic cells restricts the Th1 response to Helicobacter pylori. Gastroenterology 141:929-938.
37. Luther J, Owyang SY, Takeuchi T, Cole TS, Zhang M, Liu M, Erb-Downward J, Rubenstein JH, Chen CC, Pierzchala AV, Paul JA, Kao JY. 2011. Helicobacter pylori DNA decreases pro-inflammatory cytokine production by dendritic cells and attenuates dextran sodium sulphateinduced colitis. Gut 60:1479-1486.
38. Arnold IC, Dehzad N, Reuter S, Martin H, Becher B, Taube C, Muller A. 2011. Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells. J. Clin. Invest. 121: 3088-3093.
39. Higgins PD, Johnson LA, Luther J, Zhang M, Sauder KL, Blanco LP, Kao JY. 2011. Prior Helicobacter pylori infection ameliorates Salmonella typhimurium-induced colitis: mucosal crosstalk between stomach and distal intestine. Inflamm. Bowel Dis. 17:1398-1408.
40. Ninomiya T, Matsui H, Akbar SM, Murakami H, Onji M. 2000. Localization and characterization of antigen-presenting dendritic cells in the gastric mucosa of murine and human autoimmune gastritis. Eur. J. Clin. Invest. 30:350-358.
41. Karthaus N, Torensma R, Tel J. 2012. Deciphering the message broadcast by tumor-infiltrating dendritic cells. Am. J. Pathol. 181:733-742.
42. de Saint-Vis B, Vincent J, Vandenabeele S, Vanbervliet B, Pin JJ, Ait-Yahia S, Patel S, Mattei MG, Banchereau J, Zurawski S, Davoust J, Caux C, Lebecque S. 1998. A novel lysosome-associated membrane glycoprotein, DC-LAMP, induced upon DC maturation, is transiently expressed in MHC class II compartment. Immunity 9:325-336.
43. Hamlet A, Thoreson AC, Nilsson O, Svennerholm AM, Olbe L. 1999. Duodenal Helicobacter pylori infection differs in cagA genotype between asymptomatic subjects and patients with duodenal ulcers. Gastroenterology 116:259-268.
44. Dixon MF, Genta RM, Yardley JH, Correa P. 1997. Histological classification of gastritis and Helicobacter pylori infection: an agreement at last? The International Workshop on the Histopathology of Gastritis. Helicobacter 2(Suppl 1):S17-S24.
45. Bergquist C, Mattsson-Rydberg A, Lonroth H, Svennerholm A. 2000. Development of a new method for the determination of immune responses in the human stomach. J. Immunol. Methods 234:51-59.
46. Hansson M, Lundgren A, Elgbratt K, Quiding-Jarbrink M, Svennerholm AM, Johansson EL. 2006. Dendritic cells express CCR7 and migrate in response to CCL19 (MIP-3beta) after exposure to Helicobacter pylori. Microbes Infect. 8:841-850.
47. Kandulski A, Wex T, Kuester D, Peitz U, Gebert I, Roessner A, Malfertheiner P. 2008. Naturally occurring regulatory T cells (CD4+, CD25high, FOXP3+) in the antrum and cardia are associated with higher H. pylori colonization and increased gene expression of TGF-beta1. Helicobacter 13:295-303.
48. Colonna M, Trinchieri G, Liu YJ. 2004. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5:1219-1226.
49. Hadeiba H, Sato T, Habtezion A, Oderup C, Pan J, Butcher EC. 2008. CCR9 expression defines tolerogenic plasmacytoid dendritic cells able to suppress acute graft-versus-host disease. Nat. Immunol. 9:1253-1260.
50. Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S, Buck DW, Schmitz J. 2000. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J. Immunol. 165:6037-6046.
51. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl JP, Ricciardi-Castagnoli P. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2:361-367.
52. Necchi V, Manca R, Ricci V, Solcia E. 2009. Evidence for transepithelial dendritic cells in human H. pylori active gastritis. Helicobacter 14:208-222.
53. Nishi T, Okazaki K, Kawasaki K, Fukui T, Tamaki H, Matsuura M, Asada M, Watanabe T, Uchida K, Watanabe N, Nakase H, Ohana M, Hiai H, Chiba T. 2003. Involvement of myeloid dendritic cells in the development of gastric secondary lymphoid follicles in Helicobacter pyloriinfected neonatally thymectomized BALB/c mice. Infect. Immun. 71: 2153-2162.
54. Kao JY, Rathinavelu S, Eaton KA, Bai L, Zavros Y, Takami M, Pierzchala A, Merchant JL. 2006. Helicobacter pylori-secreted factors inhibit dendritic cell IL-12 secretion: a mechanism of ineffective host defense. Am. J. Physiol. Gastrointest. Liver Physiol. 291:G73-G81.
55. Sakaguchi S, Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T. 2009. Regulatory T cells: how do they suppress immune responses? Int. Immunol. 21:1105-1111.
56. Raghavan S, Fredriksson M, Svennerholm AM, Holmgren J, Suri-Payer E. 2003. Absence of CD4+CD25+ regulatory T cells is associated with a loss of regulation leading to increased pathology in Helicobacter pyloriinfected mice. Clin. Exp. Immunol. 132:393-400.
57. Rad R, Brenner L, Bauer S, Schwendy S, Layland L, da Costa CP, Reindl W, Dossumbekova A, Friedrich M, Saur D, Wagner H, Schmid RM, Prinz C. 2006. CD25+/Foxp3+ T cells regulate gastric inflammation and Helicobacter pylori colonization in vivo. Gastroenterology 131:525-537.
58. Chen Y, Blaser MJ. 2008. Helicobacter pylori colonization is inversely associated with childhood asthma. J. Infect. Dis. 198:553-560.
59. Luther J, Dave M, Higgins PD, Kao JY. 2010. Association between Helicobacter pylori infection and inflammatory bowel disease: a metaanalysis and systematic review of the literature. Inflamm. Bowel Dis. 16: 1077-1084.
60. Agace WW, Persson EK. 2012. How vitamin A metabolizing dendritic cells are generated in the gut mucosa. Trends Immunol. 33:42-48.
61. Mattsson A, Lonroth H, Quiding-Jarbrink M, Svennerholm AM. 1998. Induction of B cell responses in the stomach of Helicobacter pylori-infected subjects after oral cholera vaccination. J. Clin. Invest. 102:51-56.
62. Drayton DL, Liao S, Mounzer RH, Ruddle NH. 2006. Lymphoid organ development: from ontogeny to neogenesis. Nat. Immunol. 7:344-353.
63. Katou F, Ohtani H, Nakayama T, Nagura H, Yoshie O, Motegi K. 2003. Differential expression of CCL19 by DC-Lamp+mature dendritic cells in human lymph node versus chronically inflamed skin. J. Pathol. 199:98-106.
64. Bardi G, Lipp M, Baggiolini M, Loetscher P. 2001. The T cell chemokine receptor CCR7 is internalized on stimulation with ELC, but not with SLC. Eur. J. Immunol. 31:3291-3297.
65. Otero C, Groettrup M, Legler DF. 2006. Opposite fate of endocytosed CCR7 and its ligands: recycling versus degradation. J. Immunol. 177: 2314-2323.
66. Byers MA, Calloway PA, Shannon L, Cunningham HD, Smith S, Li F, Fassold BC, Vines CM. 2008. Arrestin 3 mediates endocytosis of CCR7 following ligation of CCL19 but not CCL21. J. Immunol. 181:4723-4732.
67. Ohl L, Mohaupt M, Czeloth N, Hintzen G, Kiafard Z, Zwirner J, Blankenstein T, Henning G, Forster R. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21:279-288.