Home LiteratureArticle Details
PMID: 17330821 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy.

European journal of immunology ·Vol. 37 ·No. 4 ·2007-04-00 ·Pages 935-45

Kropf P, Baud D, Marshall SE, Munder M, Mosley A, Fuentes JM, Bangham CR, Taylor GP, Herath S, Choi BS, Soler G, Teoh T, Modolell M, Müller I

Abstract

Complex regulation of T cell functions during pregnancy is required to ensure materno-fetal tolerance. Here we reveal a novel pathway for the temporary suppression of maternal T cell responses in uncomplicated human pregnancies. Our results show that arginase activity is significantly increased in the peripheral blood of pregnant women and remarkably high arginase activities are expressed in term placentae. High enzymatic activity results in high turnover of its substrate L-arginine and concomitant reduction of this amino acid in the microenvironment. Amino acid deprivation is emerging as a regulatory pathway of lymphocyte responses and we assessed the consequences of this enhanced arginase activity on T cell responses. Arginase-mediated L-arginine depletion induces down-regulation of CD3 zeta, the main signalling chain of the TCR, and functional T cell hyporesponsiveness. Importantly, this arginase-mediated T cell suppression was reversible, as inhibition of arginase activity or addition of exogenous L-arginine restored CD3 zeta chain expression and T cell proliferation. Thus, L-arginine metabolism constitutes a novel physiological mechanism contributing to the temporary suppression of the maternal immune response during human pregnancy.

MeSH Terms
Adult Arginase/biosynthesis,physiology Arginine/metabolism Cells, Cultured Enzyme Activation/immunology Female Humans Immune Tolerance Placenta/enzymology Pregnancy Pregnancy Proteins/biosynthesis,physiology T-Lymphocytes/enzymology,immunology,metabolism
Chemicals
Pregnancy Proteins Arginine Arginase
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Kropf Pascale
Department of Immunology, Faculty of Medicine, Imperial College London, London, UK.
Baud David
Marshall Sara E
Munder Markus
Mosley Angelina
Fuentes José M
Bangham Charles R M
Taylor Graham P
Herath Shanti
Choi Beak-San
Soler Germán
Teoh Tg
Modolell Manuel
Müller Ingrid
References (51)
51 references, click to expand
  1. A critical role for the programmed death ligand 1 in fetomaternal tolerance.
    J Exp Med. 2005 Jul 18;202(2):231-7 PMID: 16027236
  2. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism.
    FASEB J. 1991 Aug;5(11):2516-22 PMID: 1907934
  3. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo.
    FASEB J. 2005 Jun;19(8):1000-2 PMID: 15811879
  4. L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes.
    J Immunol. 2003 Aug 1;171(3):1232-9 PMID: 12874210
  5. Myeloperoxidase accumulates at the neutrophil surface and enhances cell metabolism and oxidant release during pregnancy.
    Eur J Immunol. 2006 Jun;36(6):1619-28 PMID: 16688678
  6. Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus.
    J Immunol. 1997 May 1;158(9):4122-8 PMID: 9126971
  7. Cutting edge: soluble HLA-G1 triggers CD95/CD95 ligand-mediated apoptosis in activated CD8+ cells by interacting with CD8.
    J Immunol. 2000 Jun 15;164(12):6100-4 PMID: 10843658
  8. Prevention of allogeneic fetal rejection by tryptophan catabolism.
    Science. 1998 Aug 21;281(5380):1191-3 PMID: 9712583
  9. Comparative properties of arginases.
    Comp Biochem Physiol B Biochem Mol Biol. 1996 May;114(1):107-32 PMID: 8759304
  10. Phenotypic characterization of human decidual macrophages.
    Clin Exp Immunol. 2003 Mar;131(3):498-505 PMID: 12605704
  11. HLA-G and immune tolerance in pregnancy.
    FASEB J. 2005 May;19(7):681-93 PMID: 15857883
  12. Policing pregnancy: Tregs help keep the peace.
    Trends Immunol. 2004 Nov;25(11):563-5 PMID: 15489182
  13. Clean Western blots of membrane proteins after yeast heterologous expression following a shortened version of the method of Perini et al.
    Anal Biochem. 2000 Oct 15;285(2):276-8 PMID: 11017716
  14. TRAIL (Apo-2L) and TRAIL receptors in human placentas: implications for immune privilege.
    J Immunol. 1999 May 15;162(10):6053-9 PMID: 10229846
  15. Arginase I is constitutively expressed in human granulocytes and participates in fungicidal activity.
    Blood. 2005 Mar 15;105(6):2549-56 PMID: 15546957
  16. Pregnancy-specific down-regulation of NF-kappa B expression in T cells in humans is essential for the maintenance of the cytokine profile required for pregnancy success.
    J Immunol. 2004 Apr 1;172(7):4583-91 PMID: 15034076
  17. Arginine availability, arginase, and the immune response.
    Curr Opin Clin Nutr Metab Care. 2003 Mar;6(2):223-8 PMID: 12589193
  18. Down-regulation of zeta-chain expression in T cells: a biomarker of prognosis in cancer?
    Cancer Immunol Immunother. 2004 Oct;53(10):865-78 PMID: 15118842
  19. Latest advances in understanding preeclampsia.
    Science. 2005 Jun 10;308(5728):1592-4 PMID: 15947178
  20. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion.
    Cancer Res. 2005 Apr 15;65(8):3044-8 PMID: 15833831
  21. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines.
    Eur J Immunol. 1995 Apr;25(4):1101-4 PMID: 7537672
  22. Arginases in parasitic diseases.
    Trends Parasitol. 2003 Jan;19(1):9-12 PMID: 12488215
  23. Trophoblast contact deactivates human neutrophils.
    J Immunol. 2006 Mar 1;176(5):3205-14 PMID: 16493081
  24. CD4(+)CD25high regulatory T cells in human pregnancy.
    J Reprod Immunol. 2005 Apr;65(2):111-20 PMID: 15811516
  25. The role of arginase in the immune response.
    Immunol Today. 1985 Apr;6(4):136-40 PMID: 25289501
  26. Arginine deficiency in preterm infants: biochemical mechanisms and nutritional implications.
    J Nutr Biochem. 2004 Aug;15(8):442-51 PMID: 15302078
  27. Immune interactions at the maternal-fetal interface.
    J Reprod Immunol. 2005 Dec;68(1-2):1-13 PMID: 16236361
  28. Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation?
    Immunol Today. 1999 Oct;20(10):469-73 PMID: 10500295
  29. Tolerance, DCs and tryptophan: much ado about IDO.
    Trends Immunol. 2003 May;24(5):242-8 PMID: 12738417
  30. Antifertility effects of (+)-S-2-amino-6-iodoacetamidohexanoic acid (2-AIHA) in female rats.
    Contraception. 1996 Apr;53(4):247-51 PMID: 8706444
  31. Arginases I and II: do their functions overlap?
    Mol Genet Metab. 2004 Apr;81 Suppl 1:S38-44 PMID: 15050972
  32. Regulation of T cell receptor CD3zeta chain expression by L-arginine.
    J Biol Chem. 2002 Jun 14;277(24):21123-9 PMID: 11950832
  33. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of t-cell function in advanced cancer patients.
    Cancer Res. 2001 Jun 15;61(12):4756-60 PMID: 11406548
  34. Helicobacter pylori arginase inhibits T cell proliferation and reduces the expression of the TCR zeta-chain (CD3zeta).
    J Immunol. 2004 Jul 1;173(1):586-93 PMID: 15210820
  35. Generation of reactive oxygen species by neutrophils and endothelial cell injury in normal and preeclamptic pregnancies.
    Hypertension. 2005 Oct;46(4):696-700 PMID: 16172429
  36. Thiol-mediated redox regulation of intestinal lamina propria T lymphocytes.
    J Exp Med. 2000 Sep 18;192(6):907-12 PMID: 10993921
  37. T cell awareness of paternal alloantigens during pregnancy.
    Science. 1995 Oct 27;270(5236):630-3 PMID: 7570020
  38. Arginase from human full-term placenta.
    Biochem J. 1976 Dec 1;159(3):579-83 PMID: 1008818
  39. The GCN2 eIF2alpha kinase is required for adaptation to amino acid deprivation in mice.
    Mol Cell Biol. 2002 Oct;22(19):6681-8 PMID: 12215525
  40. TCR zeta-chain downregulation: curtailing an excessive inflammatory immune response.
    Nat Rev Immunol. 2004 Sep;4(9):675-87 PMID: 15343367
  41. Regulation of immune responses by L-arginine metabolism.
    Nat Rev Immunol. 2005 Aug;5(8):641-54 PMID: 16056256
  42. Translational control of inducible nitric oxide synthase expression by arginine can explain the arginine paradox.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4843-8 PMID: 12655043
  43. Decreased expression of CD3zeta and nuclear transcription factor kappa B in patients with pulmonary tuberculosis: potential mechanisms and reversibility with treatment.
    J Infect Dis. 2006 Nov 15;194(10):1385-93 PMID: 17054067
  44. Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific.
    J Reprod Immunol. 2004 Apr;61(2):67-77 PMID: 15063630
  45. Tolerance, suppression and the fetal allograft.
    J Mol Med (Berl). 2005 Feb;83(2):88-96 PMID: 15605274
  46. Uterine arginase inhibition affect the rat embryonic development.
    Contraception. 1986 Jun;33(6):597-604 PMID: 3095024
  47. Immunological identity of the two different molecular mass constitutive subunits of liver arginase.
    Biol Chem Hoppe Seyler. 1994 Aug;375(8):537-41 PMID: 7811393
  48. Boosting antitumor responses of T lymphocytes infiltrating human prostate cancers.
    J Exp Med. 2005 Apr 18;201(8):1257-68 PMID: 15824085
  49. Ornithine deficiency in the arginase double knockout mouse.
    Mol Genet Metab. 2006 Sep-Oct;89(1-2):87-96 PMID: 16753325
  50. Suppression of T-cell functions by human granulocyte arginase.
    Blood. 2006 Sep 1;108(5):1627-34 PMID: 16709924
  51. Pregnancy alters glucose-6-phosphate dehydrogenase trafficking, cell metabolism, and oxidant release of maternal neutrophils.
    J Clin Invest. 2002 Dec;110(12):1801-11 PMID: 12488430
Article Info
Journal
European journal of immunology
Abbr.
Eur J Immunol
ISSN
0014-2980
Published
2007-04-00
Pages
935-45
Language
English
Region
Germany
NLM ID
1273201
PMCID
PMC2699382
Subset
IM
Grants
Wellcome Trust · United Kingdom
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