Home LiteratureArticle Details
PMID: 15618192 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mucosal FOXP3-expressing CD4+ CD25high regulatory T cells in Helicobacter pylori-infected patients.

Infection and immunity ·Vol. 73 ·No. 1 ·2005-01-00 ·Pages 523-31

Lundgren A, Strömberg E, Sjöling A, Lindholm C, Enarsson K, Edebo A, Johnsson E, Suri-Payer E, Larsson P, Rudin A, Svennerholm AM, Lundin BS

Abstract

Helicobacter pylori chronically colonizes the stomach and duodenum and causes peptic ulcers or gastric adenocarcinoma in 10 to 20% of infected individuals. We hypothesize that the inability of patients to clear H. pylori infections is a consequence of active suppression of the immune response. Here we show that H. pylori-infected individuals have increased frequencies of CD4(+) CD25(high) T cells in both the stomach and duodenal mucosa compared to uninfected controls. These cells have the phenotype of regulatory T cells, as they express FOXP3, a key gene for the development and function of regulatory T cells, as well as high levels of the cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) protein. In contrast, mucosal CD4(+) CD25(low) and CD4(+) CD25(-) cells express little FOXP3 mRNA and low levels of the CTLA-4 protein. Mucosal CD4(+) CD25(high) T cells are present in individuals with asymptomatic H. pylori infections as well as in duodenal ulcer patients. The frequencies of CD4(+) CD25(high) cells are also increased in the stomachs of H. pylori-infected patients with gastric adenocarcinoma, particularly in cancer-affected tissues. These findings suggest that regulatory T cells may suppress mucosal immune responses and thereby contribute to the persistence of H. pylori infections.

MeSH Terms
Adenocarcinoma/immunology Adult Antigens, CD Antigens, Differentiation/analysis CD4 Antigens/analysis CD4-Positive T-Lymphocytes/physiology CTLA-4 Antigen DNA-Binding Proteins/genetics Duodenal Ulcer/immunology Female Forkhead Transcription Factors Gastric Mucosa/immunology Helicobacter Infections/immunology Helicobacter pylori Humans Immunologic Memory Male Middle Aged Receptors, Interleukin-2/analysis Stomach Neoplasms/immunology T-Lymphocytes, Regulatory/physiology
Chemicals
Antigens, CD Antigens, Differentiation CD4 Antigens CTLA-4 Antigen CTLA4 protein, human DNA-Binding Proteins FOXP3 protein, human Forkhead Transcription Factors Receptors, Interleukin-2
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Lundgren Anna
Dept. of Medical Microbiology and Immunology, Göteborg University, Box 435, 405 30 Göteborg, Sweden. anna.lundgren@microbio.gu.se
Strömberg Erika
Sjöling Asa
Lindholm Catharina
Enarsson Karin
Edebo Anders
Johnsson Erik
Suri-Payer Elisabeth
Larsson Pia
Rudin Anna
Svennerholm Ann-Mari
Lundin B Samuel
References (37)
37 references, click to expand
  1. Control of regulatory T cell development by the transcription factor Foxp3.
    Science. 2003 Feb 14;299(5609):1057-61 PMID: 12522256
  2. CD25+CD4+ regulatory T cells suppress CD4+ T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice.
    Eur J Immunol. 2002 May;32(5):1282-91 PMID: 11981815
  3. CD4 T cell activation by myelin oligodendrocyte glycoprotein is suppressed by adult but not cord blood CD25+ T cells.
    Eur J Immunol. 2003 Mar;33(3):579-87 PMID: 12616478
  4. Characterization of human CD25+ CD4+ T cells in thymus, cord and adult blood.
    Immunology. 2002 Jun;106(2):190-9 PMID: 12047748
  5. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma.
    J Immunol. 2002 Sep 1;169(5):2756-61 PMID: 12193750
  6. Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases.
    Trends Immunol. 2002 Sep;23(9):450-5 PMID: 12200067
  7. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity.
    Nature. 2002 Dec 5;420(6915):502-7 PMID: 12466842
  8. Helicobacter pylori-specific CD4+ CD25high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals.
    Infect Immun. 2003 Apr;71(4):1755-62 PMID: 12654789
  9. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells.
    Nat Immunol. 2003 Apr;4(4):330-6 PMID: 12612578
  10. An essential role for Scurfin in CD4+CD25+ T regulatory cells.
    Nat Immunol. 2003 Apr;4(4):337-42 PMID: 12612581
  11. Increased frequency of activated T-cells in the Helicobacter pylori-infected antrum and duodenum.
    FEMS Immunol Med Microbiol. 2003 May 25;36(3):159-68 PMID: 12738386
  12. Absence of CD4+CD25+ regulatory T cells is associated with a loss of regulation leading to increased pathology in Helicobacter pylori-infected mice.
    Clin Exp Immunol. 2003 Jun;132(3):393-400 PMID: 12780684
  13. Immune dysregulation, polyendocrinopathy, enteropathy, and X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FOXP3, a critical regulator of T-cell homeostasis.
    Curr Opin Rheumatol. 2003 Jul;15(4):430-5 PMID: 12819471
  14. Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells.
    J Clin Invest. 2003 Nov;112(9):1437-43 PMID: 14597769
  15. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3.
    J Exp Med. 2003 Dec 15;198(12):1875-86 PMID: 14676299
  16. Escape of malaria parasites from host immunity requires CD4+ CD25+ regulatory T cells.
    Nat Med. 2004 Jan;10(1):29-30 PMID: 14702631
  17. Human CD4+ CD25+ regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens.
    J Virol. 2004 Mar;78(5):2454-9 PMID: 14963140
  18. Induction of FOXP3-expressing regulatory CD4pos T cells by human mature autologous dendritic cells.
    Eur J Immunol. 2004 Mar;34(3):762-72 PMID: 14991606
  19. Cutting edge: TGF-beta induces a regulatory phenotype in CD4+CD25- T cells through Foxp3 induction and down-regulation of Smad7.
    J Immunol. 2004 May 1;172(9):5149-53 PMID: 15100250
  20. The Sydney System: histological division.
    J Gastroenterol Hepatol. 1991 May-Jun;6(3):209-22 PMID: 1912431
  21. Specific antibodies in sera and gastric aspirates of symptomatic and asymptomatic Helicobacter pylori-infected subjects.
    Clin Diagn Lab Immunol. 1998 May;5(3):288-93 PMID: 9605978
  22. Local cytokine response in Helicobacter pylori-infected subjects.
    Infect Immun. 1998 Dec;66(12):5964-71 PMID: 9826379
  23. Duodenal Helicobacter pylori infection differs in cagA genotype between asymptomatic subjects and patients with duodenal ulcers.
    Gastroenterology. 1999 Feb;116(2):259-68 PMID: 9922305
  24. Helicobacter pylori and gastric cancer.
    Am J Med. 1999 Feb;106(2):222-6 PMID: 10230753
  25. Decreased epithelial cytokine responses in the duodenal mucosa of Helicobacter pylori-infected duodenal ulcer patients.
    Clin Diagn Lab Immunol. 2003 Jan;10(1):116-24 PMID: 12522049
  26. Differential representations of memory T cell subsets are characteristic of polarized immunity in leprosy and atopic diseases.
    Int Immunol. 1999 Nov;11(11):1801-10 PMID: 10545484
  27. Differential effect of cholera toxin on CD45RA+ and CD45RO+ T cells: specific inhibition of cytokine production but not proliferation of human naive T cells.
    Clin Exp Immunol. 2000 Aug;121(2):283-8 PMID: 10931143
  28. The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer.
    Annu Rev Microbiol. 2000;54:615-40 PMID: 11018139
  29. The design of vaccines against Helicobacter pylori and their development.
    Annu Rev Immunol. 2001;19:523-63 PMID: 11244046
  30. Human anergic/suppressive CD4(+)CD25(+) T cells: a highly differentiated and apoptosis-prone population.
    Eur J Immunol. 2001 Apr;31(4):1122-31 PMID: 11298337
  31. Human CD4(+)CD25(+) thymocytes and peripheral T cells have immune suppressive activity in vitro.
    Eur J Immunol. 2001 Apr;31(4):1247-54 PMID: 11298351
  32. Human cd25(+)cd4(+) t regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function.
    J Exp Med. 2001 Jun 4;193(11):1295-302 PMID: 11390436
  33. CD4+CD25high regulatory cells in human peripheral blood.
    J Immunol. 2001 Aug 1;167(3):1245-53 PMID: 11466340
  34. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance.
    Immunol Rev. 2001 Aug;182:18-32 PMID: 11722621
  35. Control of intestinal inflammation by regulatory T cells.
    Immunol Rev. 2001 Aug;182:190-200 PMID: 11722634
  36. Cutting edge: Regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation.
    J Immunol. 2002 May 1;168(9):4272-6 PMID: 11970966
  37. Isolation and functional characterization of regulatory CD25brightCD4+ T cells from the target organ of patients with rheumatoid arthritis.
    Eur J Immunol. 2003 Jan;33(1):215-23 PMID: 12594850
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2005-01-00
Pages
523-31
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC538965
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com