Home LiteratureArticle Details
PMID: 15226449 Published · ppublish English Journal Article

Distinct regions of the interleukin-7 receptor regulate different Bcl2 family members.

Molecular and cellular biology ·Vol. 24 ·No. 14 ·2004-07-00 ·Pages 6501-13

Jiang Q, Li WQ, Hofmeister RR, Young HA, Hodge DR, Keller JR, Khaled AR, Durum SK

Abstract

The antiapoptotic function of the interleukin-7 (IL-7) receptor is related to regulation of three members of the Bcl2 family: synthesis of Bcl2, phosphorylation of Bad, and cytosolic retention of Bax. Here we show that, in an IL-7-dependent murine T-cell line, different regions of the IL-7 receptor initiate the signal transduction pathways that regulate these proteins. Both Box1 and Y449 are required to signal Bcl2 synthesis and Bax cytosolic retention. This suggests a sequential model in which Jak1, which binds to Box1, is first activated and then phosphorylates Y449, leading to Bcl2 and Bax regulation, accounting for approximately 90% of the survival function. Phosphorylation of Bad required Box1 but not Y449, suggesting that Jak1 also initiates an additional signaling cascade that accounts for approximately 10% of the survival function. Stat5 was activated from the Y449 site but only partially accounted for the survival signal. Proliferation required both Y449 and Box1. Thymocyte development in vivo showed that deletion of Y449 eliminated 90% of alphabeta T-cell development and completely eliminated gammadelta T-cell development, whereas deleting Box 1 completely eliminated both alphabeta and gammadelta T-cell development. Thus the IL-7 receptor controls at least two distinct pathways, in addition to Stat5, that are required for cell survival.

MeSH Terms
Animals Carrier Proteins/genetics,metabolism Cell Division Cell Line Cell Survival DNA-Binding Proteins/metabolism Enzyme Activation Hematopoietic Stem Cells/cytology,physiology Humans Janus Kinase 1 Mice Milk Proteins Phosphorylation Protein Structure, Tertiary Protein-Tyrosine Kinases/metabolism Proto-Oncogene Proteins/metabolism Proto-Oncogene Proteins c-bcl-2/genetics,metabolism Receptors, Interleukin-4/genetics,metabolism Receptors, Interleukin-7/genetics,metabolism Recombinant Fusion Proteins/genetics,metabolism Retroviridae/genetics,metabolism STAT5 Transcription Factor Signal Transduction/physiology T-Lymphocytes/cytology,immunology,physiology Trans-Activators/metabolism bcl-2-Associated X Protein bcl-Associated Death Protein
Chemicals
BAD protein, human BAX protein, human Bad protein, mouse Bax protein, mouse Carrier Proteins DNA-Binding Proteins Milk Proteins Proto-Oncogene Proteins Proto-Oncogene Proteins c-bcl-2 Receptors, Interleukin-4 Receptors, Interleukin-7 Recombinant Fusion Proteins STAT5 Transcription Factor Trans-Activators bcl-2-Associated X Protein bcl-Associated Death Protein Protein-Tyrosine Kinases JAK1 protein, human Jak1 protein, mouse Janus Kinase 1
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Jiang Qiong
Laboratory of Molecular Immunoregulation, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Frederick, Maryland 21702-1201, USA.
Li Wen Qing
Hofmeister Robert R
Young Howard A
Hodge David R
Keller Jonathan R
Khaled Annette R
Durum Scott K
References (40)
40 references, click to expand
  1. Defective IL7R expression in T(-)B(+)NK(+) severe combined immunodeficiency.
    Nat Genet. 1998 Dec;20(4):394-7 PMID: 9843216
  2. Activation of phosphatidylinositol-3 kinase by ligation of the interleukin-7 receptor is dependent on protein tyrosine kinase activity.
    Blood. 1994 Sep 1;84(5):1579-86 PMID: 7520779
  3. Interleukin-7 induces the association of phosphatidylinositol 3-kinase with the alpha chain of the interleukin-7 receptor.
    Eur J Immunol. 1994 Sep;24(9):2168-74 PMID: 7522165
  4. p90(RSK) blocks bad-mediated cell death via a protein kinase C-dependent pathway.
    J Biol Chem. 1999 Dec 3;274(49):34859-67 PMID: 10574959
  5. Withdrawal of IL-7 induces Bax translocation from cytosol to mitochondria through a rise in intracellular pH.
    Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14476-81 PMID: 10588730
  6. Interleukin (IL)-7 induces rapid activation of Pyk2, which is bound to Janus kinase 1 and IL-7Ralpha.
    J Biol Chem. 2000 Mar 10;275(10):7060-5 PMID: 10702271
  7. A partial deficiency of interleukin-7R alpha is sufficient to abrogate T-cell development and cause severe combined immunodeficiency.
    Blood. 2000 Oct 15;96(8):2803-7 PMID: 11023514
  8. Control of T cell development in vivo by subdomains within the IL-7 receptor alpha-chain cytoplasmic tail.
    J Immunol. 2001 Jan 1;166(1):262-9 PMID: 11123301
  9. Interleukin-7 mediates the homeostasis of naïve and memory CD8 T cells in vivo.
    Nat Immunol. 2000 Nov;1(5):426-32 PMID: 11062503
  10. Bax deficiency partially corrects interleukin-7 receptor alpha deficiency.
    Immunity. 2002 Nov;17(5):561-73 PMID: 12433363
  11. Characterization of an interleukin-7-dependent thymic cell line derived from a p53(-/-) mouse.
    J Immunol Methods. 2003 Mar 1;274(1-2):177-84 PMID: 12609543
  12. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells.
    Nucleic Acids Res. 1991 May 11;19(9):2499 PMID: 2041787
  13. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice.
    J Exp Med. 1994 Nov 1;180(5):1955-60 PMID: 7964471
  14. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain.
    Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):377-81 PMID: 7831294
  15. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain.
    Immunity. 1995 Mar;2(3):223-38 PMID: 7697543
  16. The effect of in vivo IL-7 deprivation on T cell maturation.
    J Exp Med. 1995 Apr 1;181(4):1399-409 PMID: 7699326
  17. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine.
    J Exp Med. 1995 Apr 1;181(4):1519-26 PMID: 7699333
  18. Mutations of Jak-3 gene in patients with autosomal severe combined immune deficiency (SCID).
    Nature. 1995 Sep 7;377(6544):65-8 PMID: 7659163
  19. Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3.
    Science. 1995 Nov 3;270(5237):794-7 PMID: 7481767
  20. Mutation of Jak3 in a patient with SCID: essential role of Jak3 in lymphoid development.
    Science. 1995 Nov 3;270(5237):797-800 PMID: 7481768
  21. Defective lymphoid development in mice lacking Jak3.
    Science. 1995 Nov 3;270(5237):800-2 PMID: 7481769
  22. Interleukin-7 activates p56lck and p59fyn, two tyrosine kinases associated with the p90 interleukin-7 receptor in primary human T cells.
    Eur J Immunol. 1995 Oct;25(10):2956-60 PMID: 7589097
  23. Interleukin-7 can induce the activation of Jak 1, Jak 3 and STAT 5 proteins in murine T cells.
    Eur J Immunol. 1995 Nov;25(11):3041-6 PMID: 7489741
  24. Developmental defects of lymphoid cells in Jak3 kinase-deficient mice.
    Immunity. 1995 Dec;3(6):771-82 PMID: 8777722
  25. The interleukin-7 receptor alpha chain transmits distinct signals for proliferation and differentiation during B lymphopoiesis.
    EMBO J. 1996 Apr 15;15(8):1924-32 PMID: 8617239
  26. Interleukin 7 receptor-deficient mice lack gammadelta T cells.
    Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7172-7 PMID: 8692964
  27. Interleukin-7 signaling in human B cell precursor acute lymphoblastic leukemia cells and murine BAF3 cells involves activation of STAT1 and STAT5 mediated via the interleukin-7 receptor alpha chain.
    Leukemia. 1996 Aug;10(8):1317-25 PMID: 8709637
  28. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus.
    Hum Gene Ther. 1996 Aug 1;7(12):1405-13 PMID: 8844199
  29. Bcl-2 can rescue T lymphocyte development in interleukin-7 receptor-deficient mice but not in mutant rag-1-/- mice.
    Cell. 1997 Jun 27;89(7):1011-9 PMID: 9215624
  30. Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice.
    Cell. 1997 Jun 27;89(7):1033-41 PMID: 9215626
  31. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery.
    Cell. 1997 Oct 17;91(2):231-41 PMID: 9346240
  32. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses.
    Cell. 1998 May 29;93(5):841-50 PMID: 9630227
  33. Identification and characterization of a constitutively active STAT5 mutant that promotes cell proliferation.
    Mol Cell Biol. 1998 Jul;18(7):3871-9 PMID: 9632771
  34. Expression vectors and delivery systems.
    Curr Opin Biotechnol. 1998 Oct;9(5):447-50 PMID: 9821270
  35. Critical cytoplasmic region of the interleukin 6 signal transducer gp130 is conserved in the cytokine receptor family.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11349-53 PMID: 1662392
  36. Interleukin 7 receptor functions by recruiting the tyrosine kinase p59fyn through a segment of its cytoplasmic tail.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):12083-7 PMID: 1465444
  37. Inhibition of murine B and T lymphopoiesis in vivo by an anti-interleukin 7 monoclonal antibody.
    J Exp Med. 1993 Jul 1;178(1):257-64 PMID: 8315381
  38. Interleukin-2 receptor gamma chain: a functional component of the interleukin-7 receptor.
    Science. 1993 Dec 17;262(5141):1877-80 PMID: 8266077
  39. Activation of src family kinases in human pre-B cells by IL-7.
    J Immunol. 1994 Jul 1;153(1):97-109 PMID: 7515933
  40. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A.
    Mol Cell. 1999 Apr;3(4):413-22 PMID: 10230394
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2004-07-00
Pages
6501-13
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC434255
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