CoChat
Sign Up
Cited by 163T-cell and B-cell Immunologyinterferon and immune responsesImmunotoxicology and immune responses

Impairment of T and B Cell Development by Treatment with a Type I Interferon

Open access
Lin, Qun, Dong, Chen, Cooper, Max D.·1998·The Journal of Experimental Medicine
DOI 10.1084/jem.187.1.79PMC PMC2199191
Open this paper in CoChat — free accountOpen PDF

Abstract

Type I interferons α and β, naturally produced regulators of cell growth and differentiation, have been shown to inhibit IL-7–induced growth and survival of B cell precursors in vitro. After confirming an inhibitory effect on B lymphopoiesis in an ex vivo assay, we treated newborn mice with an active IFN-α2/α1 hybrid molecule to assess its potential for regulating B and T cell development in vivo. Bone marrow and splenic cellularity was greatly reduced in the IFN-α2/α1–treated mice, and B lineage cells were reduced by >80%. The bone marrow progenitor population of CD43+B220+HSA− cells was unaffected, but development of the CD19+ pro–B cells and their B lineage progeny was severely impaired. Correspondingly, IL-7–responsive cells in the bone marrow were virtually eliminated by the interferon treatment. Thymus cellularity was also reduced by >80% in the treated mice. Phenotypic analysis of the residual thymocytes indicated that the inhibitory effect was exerted during the pro–T cell stage in differentiation. In IFN-α/β receptor−/− mice, T and B cell development were unaffected by the IFN-α2/α1 treatment. The data suggest that type I interferons can reversibly inhibit early T and B cell development by opposing the essential IL-7 response.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1084/jem.187.1.79

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Only UMIs with at least 2 or more supporting reads were retained for final genotyping assignments.

    “Only UMIs with at least 2 or more supporting reads were retained for final genotyping assignments, after the UMI collapse algorithm 42,86 .”

    From Type 1 interferon perturbates clonal competition by reshaping human blood development (2026) · cites this paper as [42]

    The Materials and Methods section describes flow cytometry of mouse cells, not UMI-based sequencing or genotyping. Searches for UMI collapse, supporting-read thresholds, and genotyping assignments found no passage addressing the claimed two-read rule; page numbers are unavailable in our copy. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 74

  1. [1]Rajewsky K Clonal selection and learning in the antibody system Nature 1996 381 751 758 8657279
  2. [2]Tonegawa S Somatic generation of antibody diversity Nature 1983 302 575 581 6300689
  3. [3]Alt FW Oltz EM Young F Gorman J Taccioli G Chen J VDJ recombination Immunol Today 1992 13 306 314 1510813
  4. [4]Karasuyama H Rolink A Melchers F Surrogate light chain in B cell development Adv Immunol 1996 63 1 41 8787628
  5. [5]Lassoued K Nunez CA Billips L Kubagawa H Monteiro RC LeBlen TW Cooper MD Expression of surrogate light chain receptors is restricted to a late stage in pre–B cell differentiation Cell 1993 73 73 86 7681728
  6. [6]Karasuyama H Rolink A Shinkai Y Young F Alt FW Melchers F The expression of Vpre-B/λ5 surrogate light chain in early bone marrow precursor B cells of normal and B cell–deficient mutant mice Cell 1994 77 133 143 8156589
  7. [7]Cooper MD Mulvaney D Coutinho A Cazenave P-A A novel cell surface molecule on early B-lineage cells Nature 1986 321 616 618 3086746
  8. [8]Osmond DG Population dynamics of bone marrow B lymphocytes Immunol Rev 1986 93 103 124 3491034
  9. [9]Hardy RR Carmack CE Shinton SA Kemp JD Hayakawa K Resolution and characterization of pro-B and pre–pro-B cell stages in normal mouse bone marrow J Exp Med 1991 173 1213 1225 1827140 PMC2118850
  10. [10]Hardy RR Kemp JD Hayakawa K Analysis of lymphoid population in scid mice; detection of a potential B lymphocyte progenitor population present at normal levels in scid mice by three color flow cytometry with B220 and S7 Curr Top Microbiol Immunol 1989 152 19 25 2478339
  11. [11]Li YS Hayakawa K Hardy RR The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver J Exp Med 1993 178 951 960 8350062 PMC2191150
  12. [12]von Boehmer H The developmental biology of T lymphocytes Annu Rev Immunol 1988 6 309 326 3289569
  13. [13]Jameson SC Hogquist KA Bevan MJ Positive selection of thymocytes Annu Rev Immunol 1995 13 93 126 7612239
  14. [14]Kisielow P von Boehmer H Development and selection of T cells: facts and puzzles Adv Immunol 1995 58 87 209 7741032
  15. [15]Godfrey DI Kennedy J Suda T Zlotnik A A developmental pathway involving four phenotypically and functionally distinct subsets of CD3−CD4−CD8−triple-negative adult mouse thymocytes defined by CD44 and CD25 expression J Immunol 1993 150 4244 4252 8387091
  16. [16]Godfrey DI Zlotnik A Control points in early T-cell development Immunol Today 1993 14 547 553 7903854
  17. [17]Levelt CN Carsetti R Eichmann K Regulation of thymocyte development through CD3. II. Expression of T cell receptor β CD3 ε and maturation to the CD4+8+stage are highly correlated in individual thymocytes J Exp Med 1993 178 1867 1875 7504052 PMC2191302
  18. [18]Dudley EC Petrie HT Shah LM Owen MJ Hayday AC T cell receptor beta chain gene rearrangement and selection during thymocyte development in adult mice Immunity 1994 1 83 93 7534200
  19. [19]Godfrey DI Kennedy J Mombaerts P Tonegawa S Zlotnik A Onset of TCR-beta gene rearrangement and role of TCR-beta expression during CD3−CD4−CD8−thymocyte differentiation J Immunol 1994 152 4783 4792 7513723
  20. [20]Namen AE Lupton S Hjerrild K Wignall J Mochizuki DY Schmierer A Mosley B March CJ Urdal D Gillis S Stimulation of B-cell progenitors by cloned murine interleukin-7 Nature 1988 333 571 573 3259677
  21. [21]Sudo T Nishikawa S Ohno N Akiyama N Tamakoshi M Yoshida H Nishikawa S-I Expression and function of the interleukin 7 receptor in murine lymphocytes Proc Natl Acad Sci USA 1993 90 9125 9129 8415665 PMC47514
  22. [22]Kincade PW B lymphopoiesis: global factors, local control Proc Natl Acad Sci USA 1994 91 2888 2889 8159674 PMC43478
  23. [23]Melchers F Haasner D Streb M Rolink A B-lymphocyte lineage-committed, IL-7 and stroma cell-reactive progenitors and precursors, and their differentiation to B cells Adv Exp Med Biol 1992 323 111 117 1283045
  24. [24]Kunisada T Ogawa M Hayashi S Era T Nishikawa S Interleukin-7 and B lymphopoiesis Chem Immunol 1992 51 205 235 1567542
  25. [25]Namen AE Williams DE Goodwin RG Interleukin-7: a new hematopoietic growth factor Prog Clin Biol Res 1990 338 65 73 2189141
  26. [26]Widmer, M.B., P.J. Morrissey, R.G. Goodwin, K.H. Grabstein, L.S. Park, J.D. Watson, P.W. Kincade, P.J. Conlon, and A.E. Namen. 1990. Lymphopoiesis and IL-7. Intl. J. Cell Cloning. 8 (Suppl. 1):168–172. 2182735
  27. [27]Wang J Lin Q Langston H Cooper MD Resident bone marrow macrophages produce type 1 interferons that can selectively inhibit interleukin-7–driven growth of B lineage cells Immunity 1995 3 475 484 7584138
  28. [28]Su D-M Wang J Lin Q Cooper MD Watanabe T Interferons α/β inhibit IL-7–induced proliferation of CD4−CD8−CD3−CD44+CD25+ thymocytes, but do not inhibit CD4−CD8−CD3−CD44−CD25−thymocytes Immunology 1997 90 543 549 9176107 PMC1456697
  29. [29]De Maeyer, E., and J. De Maeyer-Guignard. 1988. Interferons and Other Regulatory Cytokines. John Wiley and Sons, Inc. New York. 448 pp.
  30. [30]Borden EC Hogan TF Voelkel JG Comparative antiproliferative activity in vitro of natural interferons alpha and beta for diploid and transformed human cells Cancer Res 1982 42 4948 4953 7139598
  31. [31]Broxmeyer HE Lu L Platzer E Feit C Juliano L Rubin BY Comparative analysis of the influences of human gamma, alpha and beta interferons on human multipotential (CFU-GEMM), erythroid (BFU-E) and granulocyte-macrophage (CFU-GM) progenitor cells J Immunol 1983 131 1300 1305 6193183
  32. [32]Clemens MJ McNurlan MA Regulation of cell proliferation and differentiation by interferons Biochem J 1985 226 345 360 2581554 PMC1144719
  33. [33]Moore RN Larsen HS Horohov DW Rouse BT Endogenous regulation of macrophage proliferative expansion by colony-stimulating factor-induced interferon Science 1984 223 178 181 6606850
  34. [34]Resnitzky D Yarden A Zipori D Kimchi A Autocrine beta-related interferon controls c-myc suppression and growth arrest during hematopoietic cell differentiation Cell 1986 46 31 40 2941150
  35. [35]Weber H Valenzuela D Lujber G Gubler M Weissmann C Single amino acid changes that render human IFN-alpha 2 biologically active on mouse cells EMBO (Eur Mol Biol Organ) J 1987 6 591 598 3034596 PMC553438
  36. [36]Borzillo GV Endo K Tsujimoto Y Bcl-2 confers growth and survival advantage to interleukin 7–dependent early pre-B cells which become factor independent by a multistep process in culture Oncogene 1992 7 869 876 1373874
  37. [37]Dumont FJ Coker LZ Interferon-alpha/beta enhances the expression of Ly-6 antigens on T cells in vivo and in vitro Eur J Immunol 1986 16 735 740 3487457
  38. [38]Rolink A ten Boekel E Melchers F Fearon DT Krop I Andersson J A subpopulation of B220+cells in murine bone marrow does not express CD19 and contains natural killer cell progenitors J Exp Med 1996 183 187 194 8551222 PMC2192422
  39. [39]Moore TA Zlotnik A T-cell lineage commitment and cytokine responses of thymic progenitors Blood 1995 86 1850 1860 7655014
  40. [41]Ardavin C Wu L Li CL Shortman K Thymic dendritic cells and T cells develop simultaneously in the thymus from a common precursor population Nature 1993 362 761 763 8469288
  41. [42]Moore TA von Freeden-Jeffry U Murray R Zlotnik A Inhibition of γδ T cell development and early thymocyte maturation in IL-7 −/−mice J Immunol 1996 157 2366 2373 8805634
  42. [43]Wang J Walker H Lin Q Jenkins N Copeland NG Watanabe T Burrows PD Cooper MD The mouse BP-1gene: structure, chromosomal localization, and regulation of expression by type I interferons and interleukin-7 Genomics 1996 33 167 176 8660964
  43. [44]Akashi K Kondo M von Freeden-Jeffry U Murray R Weissman IL Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice Cell 1997 89 1033 1041 9215626
  44. [45]Maraskovsky E O'Reilly LA Teepe M Corcoran LM Peschon JJ Strasser A Bcl-2 can rescue T lymphocyte development in interleukin-7 receptor-deficient mice but not in mutant rag-1 −/−mice Cell 1997 89 1011 1019 9215624
  45. [46]Grabstein KH Waldschmidt TJ Finkelman FD Hess BW Alpert AR Boiani NE Namen AE Morrissey PJ Inhibition of murine B and T lymphopoiesis in vivo by an anti–interleukin 7 monoclonal antibody J Exp Med 1993 178 257 264 8315381 PMC2191094
  46. [47]Watson JD Morrissey PJ Namen AE Conlon PJ Widmer MB Effect of IL-7 on the growth of fetal thymocytes in culture J Immunol 1989 143 1215 1222 2787360
  47. [48]Suda T Zlotnik A IL-7 maintains the T cell precursor potential of CD3−CD4−CD8−thymocytes J Immunol 1991 146 3068 3073 1826704
  48. [49]Plum J De Smedt M Leclercq G Exogenous IL-7 promotes the growth of CD3−CD4−CD8−CD44+ CD25+/−precursor cells and blocks the differentiation pathway of TCR-alpha beta cells in fetal thymus organ culture J Immunol 1993 150 2706 2716 8095954
  49. [50]Candéias S Muegge K Durum SK IL-7 receptor and VDJ recombination: trophic versus mechanistic actions Immunity 1997 6 501 508 9175828
  50. [51]Bhatia SK Tygrett LT Grabstein KH Waldschmidt TJ The effect of in vivo IL-7 deprivation on T cell maturation J Exp Med 1995 181 1399 1409 7699326 PMC2191957
  51. [52]von Freeden-Jeffry U Vieira P Lucian LA McNeil T Burdach SE Murray R Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine J Exp Med 1995 181 1519 1526 7699333 PMC2191954
  52. [53]Peschon JJ Morrissey PJ Grabstein KH Ramsdell FJ Maraskovsky E Gliniak BC Park LS Ziegler SF Williams DE Ware CB Meyer JD Davison BL Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice J Exp Med 1994 180 1955 1960 7964471 PMC2191751
  53. [54]Cao X Shores EW Hu-Li J Anver MR Kelsall BL Russell SM Drago J Noguchi M Grinberg A Bloom ET Defective lymphoid development in mice lacking expression of the common cytokine receptor γ chain Immunity 1997 2 223 238 7697543
  54. [55]DiSanto JP Muller W Guy-Grand D Fischer A Rajewsky K Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain Proc Natl Acad Sci USA 1995 92 377 381 7831294 PMC42743
  55. [56]Nosaka T van Deursen JM Tripp RA Thierfelder WE Witthuhn BA McMickle AP Doherty PC Grosveld GC Ihle JN Defective lymphoid development in mice lacking Jak3 Science 1995 270 800 802 7481769
  56. [57]Park SY Saijo K Takahashi T Osawa M Arase H Hirayama N Miyake K Nakauchi H Shirasawa T Saito T Developmental defects of lymphoid cells in Jak3 kinase-deficient mice Immunity 1995 3 771 782 8777722
  57. [58]Thomis DC Gurniak CB Tivol E Sharpe AH Berg LJ Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3 defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3 Science 1995 270 794 797 7481767
  58. [59]Witthuhn BA Silvennoinen O Miura O Lai KS Cwik C Liu ET Ihle JN Involvement of the Jak-3 Janus kinase in signalling by interleukins 2 and 4 in lymphoid and myeloid cells Nature 1994 370 153 157 8022486
  59. [60]Johnston JA Kawamura M Kirken RA Chen YQ Blake TB Shibuya K Ortaldo JR McVicar DW O'Shea JJ Phosphorylation and activation of the Jak-3 Janus kinase in response to interleukin-2 Nature 1994 370 151 153 8022485
  60. [61]Kondo M Takeshita T Higuchi M Nakamura M Sudo T Nishikawa S Sugamura K Functional participation of the IL-2 receptor gamma chain in IL-7 receptor complexes Science 1994 263 1453 1454 8128231
  61. [62]Ihle JN Cytokine receptor signalling Nature 1995 377 591 594 7566171
  62. [63]Sharfe N Dadi HK Roifman CM JAK3 protein tyrosine kinase mediates interleukin-7–induced activation of phosphatidylinositol-3′ kinase Blood 1995 86 2077 2085 7662955
  63. [64]Harada H Fujita T Miyamoto M Kimura Y Maruyama M Furia A Miyata T Taniguchi T Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes Cell 1989 58 729 739 2475256
  64. [65]Fujita T Reis LF Watanabe N Kimura Y Taniguchi T Vilcek J Induction of the transcription factor IRF-1 and interferon-beta mRNAs by cytokines and activators of second-messenger pathways Proc Natl Acad Sci USA 1989 86 9936 9940 2557635 PMC298617
  65. [66]Miyamoto M Fujita T Kimura Y Maruyama M Harada H Sudo Y Miyata T Taniguchi T Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-beta gene regulatory elements Cell 1988 54 903 913 3409321
  66. [67]Yamada G Ogawa M Akagi K Miyamoto H Nakano N Itoh S Miyazaki J-I Nishikawa S-I Yamamura K-I Taniguchi T Specific depletion of the B-cell population induced by aberrant expression of human interferon regulatory factor 1 gene in transgenic mice Proc Natl Acad Sci USA 1991 88 532 536 1988951 PMC50845
  67. [68]Diaz MO Ziemin S Le Beau MM Pitha P Smith SD Chilcote RR Rowley JD Homozygous deletion of the alpha- and beta 1-interferon genes in human leukemia and derived cell lines Proc Natl Acad Sci USA 1988 85 5259 5263 3134658 PMC281729
  68. [69]Miyakoshi J Dobler KD Allalunis-Turner J McKean JDS Petruk K Allen PBR Aronyk KN Weir B Huyser-Wierenga D Fulton D Absence of IFNA and IFNBgenes from human malignant glioma cell lines and lack of correlation with cellular sensitivity to interferons Cancer Res 1990 50 278 283 2295067
  69. [70]Muller U Steinhoff U Reis LF Hemmi S Pavlovic J Zinkernagel RM Aguet M Functional role of type I and type II interferons in antiviral defense Science 1994 264 1918 1921 8009221
  70. [71]Grawunder U Melchers F Rolink A Interferon-gamma arrests proliferation and causes apoptosis in stromal cell/interleukin-7–dependent normal murine pre-B cell lines and clones in vitro, but does not induce differentiation to surface immunoglobulin-positive B cells Eur J Immunol 1993 23 544 551 8436185
  71. [72]Hwang SY Hertzog PJ Holland KA Sumarsono SH Tymms MJ Hamilton JA Whitty G Bertoncello I Kola I A null mutation in the gene encoding a type I interferon receptor component eliminates antiproliferative and antiviral responses to interferons alpha and beta and alters macrophage responses Proc Natl Acad Sci USA 1995 92 11284 11288 7479980 PMC40616
  72. [73]Lee G Namen AE Gillis S Ellingsworth LR Kincade PW Normal B cell precursors responsive to recombinant murine IL-7 and inhibition of IL-7 activity by transforming growth factor-beta J Immunol 1989 142 3875 3883 2785567
  73. [74]Plum J De Smedt M Leclercq G Vandekerckhove B Influence of TGF-beta on murine thymocyte development in fetal thymus organ culture J Immunol 1995 154 5789 5798 7538530
  74. [75]Binder D Fehr J Hengartner H Zinkernagel RM Virus-induced transient bone marrow aplasia: major role of interferon-α/β during acute infection with the noncytopathic lymphocytic choriomeningitis virus J Exp Med 1997 185 517 530 9053452 PMC2196026

Cited by

Sorted by citations

Authors
Lin, Q., Dong, C., & Cooper, M. D.
Affiliations
Howard Hughes Medical Institute (US)
Corresponding author
Dong, Chen
ORCID
Venue
The Journal of Experimental Medicine
Publisher
Rockefeller University Press
Published
1998-01-05
Volume
187
Issue
1
Pages
79-87
ISSN
  • 0022-1007 (ISSN-L)
  • 1540-9538
DOI
10.1084/jem.187.1.79
PMC
PMC2199191
OpenAlex
W2145418572
Cited by
163
References
1
Citations by year
2026: 1 · 2025: 2 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 6 · 2020: 1 · 2019: 5 · 2018: 1 · 2017: 3 · 2016: 5 · 2015: 6 · 2014: 2 · 2013: 5 · 2012: 5
FWCI
2.28
Type
journal article
Language
en
Open access
Locations
  • The Journal of Experimental Medicine (publishedVersion)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • Yale University
  • National Institutes of Health (5u01ai034568-04)
  • National Institute of Allergy and Infectious Diseases (AI39816, AI34568, R01AI039816, R37AI039816)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
  • Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
Keywords
type I interferon, interferon-alpha, B cell development, T cell development, IL-7, pro-B cells, pro-T cells, lymphocyte development, IFN-alpha/beta receptor, bone marrow, thymus, neonatal mice, CD19+ cells
MeSH terms
Animals, Animals, Newborn, B-Lymphocytes, Cell Differentiation, Cell Division, Hematopoiesis, Mice, Inbred BALB C, T-Lymphocytes, Interleukin-7, Interferon-alpha, Receptors, Interferon, Mice, Knockout, Mice, In Vitro Techniques

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review