Impact of interferon-γ on hematopoiesis

de Bruin, Alexander M.; Voermans, Carlijn; Nolte, Martijn A.

doi:10.1182/blood-2014-04-568451

Cited by 215Hematopoietic Stem Cell TransplantationCytokine Signaling Pathways and Interactionsinterferon and immune responses

Impact of interferon-γ on hematopoiesis

Open access

de Bruin, Alexander M., Voermans, Carlijn, Nolte, Martijn A.·2014·Blood

DOI 10.1182/blood-2014-04-568451

Open this paper in CoChat — free account Open PDF

Abstract

The proinflammatory cytokine interferon-γ (IFN-γ) is well known for its important role in innate and adaptive immunity against intracellular infections and for tumor control. Yet, it has become clear that IFN-γ also has a strong impact on bone marrow (BM) output during inflammation, as it affects the differentiation of most hematopoietic progenitor cells. Here, we review the impact of IFN-γ on hematopoiesis, including the function of hematopoietic stem cells (HSCs) and more downstream progenitors. We discuss which hematopoietic lineages are functionally modulated by IFN-γ and through which underlying molecular mechanism(s). We propose the novel concept that IFN-γ acts through upregulation of suppressor of cytokine signaling molecules, which impairs signaling of several cytokine receptors. IFN-γ has also gained clinical interest from different angles, and we discuss how chronic IFN-γ production can lead to the development of anemia and BM failure and how it is involved in malignant hematopoiesis. Overall, this review illustrates the wide-ranging effect of IFN-γ on the (patho-)physiological processes in the BM.

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.

Integrity signals

Registry

Crossref · 10.1182/blood-2014-04-568451

Cites

98 of 98 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.

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?

Chronic exposure to IFN-g functionally impairs HSCs in vitro and in vivo, particularly when secreted by stromal cells within the hematopoietic niche.
“Chronic exposure, however, functionally impairs HSCs in vitro and in vivo, 21 in particular when secreted by stromal cells within the hematopoietic niche.22”
From Inflammatory bone marrow microenvironment (2019) · cites this paper as [21]
IFN-g mainly affects the self-renewal and repopulating capacity of hematopoietic progenitors by moderating their response to other cytokines, mediated by STAT1 and SOCS1 and SOCS3.
“IFN-g mainly affects the self-renewal and repopulating capacity of hematopoietic progenitors by moderating their response to other cytokines.23 This effect is mainly mediated by STAT1 and suppressor of cytokine signaling 1 (SOCS1) and SOCS3 as effector molecules.21,24”
From Inflammatory bone marrow microenvironment (2019) · cites this paper as [21]

Self-check

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

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

Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide
Ren, G., Zhang, L., Zhao, X., Xu, G., Zhang, Y., Roberts, A. I., Zhao, R. C., & Shi, Y. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2007.11.014 · Cited by 2,101 · see citing works
Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase–mediated tryptophan degradation
Meisel, R., Zibert, A., Laryea, M. D., Göbel, U., Däubener, W., & Dilloo, D. (2004) · Blood · doi:10.1182/blood-2003-11-3909 · Cited by 1,638 · see citing works
IFNα activates dormant haematopoietic stem cells in vivo
Essers, M. A. G., Offner, S., Blanco-Bose, W. E., Waibler, Z., Kalinke, U., Duchosal, M. A., & Trumpp, A. (2009) · Nature · doi:10.1038/nature07815 · Cited by 1,368 · see citing works
Quiescent haematopoietic stem cells are activated by IFN-γ in response to chronic infection
Baldridge, M. T., King, K. Y., Boles, N. C., Weksberg, D. C., & Goodell, M. A. (2010) · Nature · doi:10.1038/nature09135 · Cited by 877 · see citing works
SOCS Proteins: Negative Regulators of Cytokine Signaling
Krebs, D. L., & Hilton, D. J. (2001) · Stem Cells · doi:10.1634/stemcells.19-5-378 · Cited by 826 · see citing works
Regulation of B lymphocyte and macrophage development by graded expression of PU.1
DeKoter, R. P., & Singh, H. (2000) · Science · doi:10.1126/science.288.5470.1439 · Cited by 749 · see citing works
Human MSC Suppression Correlates With Cytokine Induction of Indoleamine 2,3-Dioxygenase and Bystander M2 Macrophage Differentiation
François, M., Romieu, R., Li, M., & Galipeau, J. (2011) · Molecular Therapy · doi:10.1038/mt.2011.189 · Cited by 694 · see citing works
Plasma cells from multiple myeloma patients express B7-H1 (PD-L1) and increase expression after stimulation with IFN-γ and TLR ligands via a MyD88-, TRAF6-, and MEK-dependent pathway
Liu, J., Hamrouni, A., Wołowiec, D., Coiteux, V., Kuliczkowski, K., Hétuin, D., Saudemont, A., & Quesnel, B. (2007) · Blood · doi:10.1182/blood-2006-10-051482 · Cited by 580 · see citing works
Inflammatory modulation of HSCs: viewing the HSC as a foundation for the immune response
King, K. Y., & Goodell, M. A. (2011) · Nature reviews. Immunology · doi:10.1038/nri3062 · Cited by 565 · see citing works
SOCS1 Deficiency Causes a Lymphocyte-Dependent Perinatal Lethality
Marine, J., Topham, D. J., McKay, C., Wang, D., Parganas, E., Stravopodis, D. J., Yoshimura, A., & Ihle, J. N. (1999) · Cell · doi:10.1016/s0092-8674(00)80048-3 · Cited by 515 · see citing works
Aplastic Anemia
Schrezenmeier, H. (1999) · Cited by 502 · see citing works
ADAR1 is essential for the maintenance of hematopoiesis and suppression of interferon signaling
Hartner, J. C., Walkley, C. R., Lü, J., & Orkin, S. H. (2008) · Nature Immunology · doi:10.1038/ni.1680 · Cited by 493 · see citing works
Fas antigen expression on CD34+ human marrow cells is induced by interferon gamma and tumor necrosis factor alpha and potentiates cytokine-mediated hematopoietic suppression in vitro
Maciejewski, J. P., Selleri, C., Anderson, S. M., & Young, N. S. (1995) · Blood · doi:10.1182/blood.v85.11.3183.bloodjournal85113183 · Cited by 474 · see citing works
The suppressive influences of human tumor necrosis factors on bone marrow hematopoietic progenitor cells from normal donors and patients with leukemia: synergism of tumor necrosis factor and interferon- gamma .
Broxmeyer, H. E., Williams, D. E., Lu, L., Cooper, S. H., Anderson, S. L., Beyer, G. S., Hoffman, R., & Rubin, B. Y. (1986) · The Journal of Immunology · doi:10.4049/jimmunol.136.12.4487 · Cited by 469 · see citing works
Direct interaction of hematopoietic transcription factors PU.1 and GATA-1: functional antagonism in erythroid cells
Rekhtman, N., Radparvar, F., Evans, T., & Skoultchi, A. I. (1999) · Genes & Development · doi:10.1101/gad.13.11.1398 · Cited by 454 · see citing works
Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon–dependent exhaustion
Sato, T., Onai, N., Yoshihara, H., Arai, F., Suda, T., & Ohteki, T. (2009) · Nature Medicine · doi:10.1038/nm.1973 · Cited by 412 · see citing works
Demand-adapted regulation of early hematopoiesis in infection and inflammation
Takizawa, H., Boettcher, S., & Manz, M. G. (2012) · Blood · doi:10.1182/blood-2011-12-380113 · Cited by 404 · see citing works
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.
Broxmeyer, H. E., Lu, L., Platzer, E., Feit, C., Juliano, L., & Rubin, B. Y. (1983) · The Journal of Immunology · doi:10.4049/jimmunol.131.3.1300 · Cited by 354 · see citing works
CIS3/SOCS-3 Suppresses Erythropoietin (EPO) Signaling by Binding the EPO Receptor and JAK2
Sasaki, A. T., Yasukawa, H., Shouda, T., Kitamura, T., Đikić, I., & Yoshimura, A. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m003456200 · Cited by 341 · see citing works
Interferon is a mediator of hematopoietic suppression in aplastic anemia in vitro and possibly in vivo
Zoumbos, N. C., Gascon, P., Djeu, J. Y., & Young, N. S. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.1.188 · Cited by 330 · see citing works
Re-entry into quiescence protects hematopoietic stem cells from the killing effect of chronic exposure to type I interferons
Pietras, E. M., Lakshminarasimhan, R., Techner, J.-M., Fong, S., Flach, J., Binnewies, M., & Passegué, E. (2014) · Journal of Experimental Medicine · doi:10.1084/jem.20131043 · Cited by 323 · see citing works
Iron metabolism in the anemia of chronic disease
Weiss, G. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2008.08.006 · Cited by 322 · see citing works
Effects of interleukin 12 on immune responses and host protection in mice infected with intestinal nematode parasites.
Finkelman, F. D., Madden, K. B., Cheever, A. W., Katona, I. M., Morris, S. C., Gately, M. K., Hubbard, B. R., Gause, W. C., & Urban, J. F. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.179.5.1563 · Cited by 273 · see citing works
Programmed death 1 signaling on chronic myeloid leukemia–specific T cells results in T-cell exhaustion and disease progression
Mumprecht, S., Schürch, C. M., Schwaller, J., Solenthaler, M., & Ochsenbein, A. F. (2009) · Blood · doi:10.1182/blood-2008-09-179697 · Cited by 267 · see citing works
In-vivo dominant immune responses in aplastic anaemia: molecular tracking of putatively pathogenetic T-cell clones by TCR β-CDR3 sequencing
Risitano, A. M., Maciejewski, J. P., Green, S., Plasilova, M. L., Zeng, W., & Young, N. S. (2004) · The Lancet · doi:10.1016/s0140-6736(04)16724-x · Cited by 242 · see citing works
TNF- and IFN- are overexpressed in the bone marrow of Fanconi anemia patients and TNF- suppresses erythropoiesis in vitro
Dufour, C. (2003) · Blood · doi:10.1182/blood-2003-01-0114 · Cited by 241 · see citing works
Constitutive CD27/CD70 Interaction Induces Expansion of Effector-Type T Cells and Results in IFNγ-Mediated B Cell Depletion
Arens, R., Tesselaar, K., Baars, P. A., van Schijndel, G. M. W., Hendriks, J., Pals, S. T., Krimpenfort, P., Borst, J. G., van Oers, M. H. J., & van Lier, R. A. W. (2001) · Immunity · doi:10.1016/s1074-7613(01)00236-9 · Cited by 239 · see citing works
STAT3 controls myeloid progenitor growth during emergency granulopoiesis
Zhang, H., Nguyen-Jackson, H., Panopoulos, A. D., Li, H. S., Murray, P. J., & Watowich, S. S. (2010) · Blood · doi:10.1182/blood-2009-12-259630 · Cited by 232 · see citing works
Hemophagocytosis causes a consumptive anemia of inflammation
Zoller, E. E., Lykens, J. E., Terrell, C. E., Aliberti, J., Filipovich, A. H., Henson, P. M., & Jordan, M. B. (2011) · Journal of Experimental Medicine · doi:10.1084/jem.20102538 · Cited by 228 · see citing works
Aplastic anemia
Young, N. S., Scheinberg, P., & Calado, R. T. (2008) · Current Opinion in Hematology · doi:10.1097/moh.0b013e3282fa7470 · Cited by 224 · see citing works
Intracellular interferon-γ in circulating and marrow T cells detected by flow cytometry and the response to immunosuppressive therapy in patients with aplastic anemia
Sloand, E. M., Kim, S., Maciejewski, J. P., Tisdale, J. F., Follmann, D. A., & Young, N. S. (2002) · Blood · doi:10.1182/blood-2002-01-0035 · Cited by 213 · see citing works
Cytotoxic CD8+ T Cells Stimulate Hematopoietic Progenitors by Promoting Cytokine Release from Bone Marrow Mesenchymal Stromal Cells
Schürch, C. M., Riether, C., & Ochsenbein, A. F. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.01.002 · Cited by 213 · see citing works
Interferon-γ impairs proliferation of hematopoietic stem cells in mice
de Bruin, A. M., Demirel, Ö., Hooibrink, B., Brandts, C., & Nolte, M. A. (2013) · Blood · doi:10.1182/blood-2012-05-432906 · Cited by 211 · see citing works
Self-citation
Interferon-gamma constitutively expressed in the stromal microenvironment of human marrow cultures mediates potent hematopoietic inhibition
Selleri, C., Maciejewski, J., Sato, T., & Young, N. (1996) · Blood · doi:10.1182/blood.v87.10.4149.bloodjournal87104149 · Cited by 209 · see citing works
Identification of eosinophil lineage–committed progenitors in the murine bone marrow
Iwasaki, H., Mizuno, S.-I., Mayfield, R., Shigematsu, H., Arinobu, Y., Seed, B., Gurish, M. F., Takatsu, K., & Akashi, K. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050548 · Cited by 205 · see citing works
Chronic IFN-γ production in mice induces anemia by reducing erythrocyte life span and inhibiting erythropoiesis through an IRF-1/PU.1 axis
Libregts, S. F., Gutiérrez, L., de Bruin, A. M., Wensveen, F. M., Papadopoulos, P., van Ijcken, W., Özgür, Z., Philipsen, S., & Nolte, M. A. (2011) · Blood · doi:10.1182/blood-2010-10-315218 · Cited by 204 · see citing works
Self-citation
Studies of interferon as a regulator of hematopoietic cell proliferation.
Raefsky, E. L., Platanias, L. C., Zoumbos, N. C., & Young, N. S. (1985) · The Journal of Immunology · doi:10.4049/jimmunol.135.4.2507 · Cited by 186 · see citing works
Interferon is the suppressor of hematopoiesis generated by stimulated lymphocytes in vitro.
Zoumbos, N. C., Djeu, J. Y., & Young, N. S. (1984) · The Journal of Immunology · doi:10.4049/jimmunol.133.2.769 · Cited by 179 · see citing works
Virus-induced Transient Bone Marrow Aplasia: Major Role of Interferon-α/β during Acute Infection with the Noncytopathic Lymphocytic Choriomeningitis Virus
Binder, D., Fehr, J., Hengartner, H., & Zinkernagel, R. M. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.185.3.517 · Cited by 178 · see citing works
In acute myeloid leukemia, B7-H1 (PD-L1) protection of blasts from cytotoxic T cells is induced by TLR ligands and interferon-gamma and can be reversed using MEK inhibitors
Berthon, C., Driss, V., Liu, J., Kuranda, K., Leleu, X. P., Jouy, N., Hétuin, D., & Quesnel, B. (2010) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-010-0909-y · Cited by 167 · see citing works
T-bet, a Th1 transcription factor, is up-regulated in T cells from patients with aplastic anemia
Solomou, E. E., Keyvanfar, K., & Young, N. S. (2006) · Blood · doi:10.1182/blood-2005-10-4201 · Cited by 148 · see citing works
IFNγ induces monopoiesis and inhibits neutrophil development during inflammation
de Bruin, A. M., Libregts, S. F., Valkhof, M., Boon, L., Touw, I. P., & Nolte, M. A. (2012) · Blood · doi:10.1182/blood-2011-07-367706 · Cited by 146 · see citing works
Self-citation
Induction of an IL7-R+c-Kithi myelolymphoid progenitor critically dependent on IFN-γ signaling during acute malaria
Belyaev, N. N., Brown, D. E., Diaz, A. I. G., Rae, A. J., Jarra, W., Thompson, J., Langhorne, J., & Potocnik, A. J. (2010) · Nature Immunology · doi:10.1038/ni.1869 · Cited by 135 · see citing works
The p47 GTPase Lrg-47 (Irgm1) Links Host Defense and Hematopoietic Stem Cell Proliferation
Feng, C. G., Weksberg, D. C., Taylor, G. A., Sher, A., & Goodell, M. A. (2008) · Cell stem cell · doi:10.1016/j.stem.2007.10.007 · Cited by 124 · see citing works
Infection-Induced Myelopoiesis during Intracellular Bacterial Infection Is Critically Dependent upon IFN-γ Signaling
MacNamara, K. C., Oduro, K. A., Martin, O., Jones, D. D., McLaughlin, M., Choi, K., Borjesson, D. L., & Winslow, G. M. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001893 · Cited by 122 · see citing works
Inflammation and Lymphocyte Activation during Mycobacterial Infection in the Interferon-γ-Deficient Mouse
Pearl, J. E., Saunders, B. M., Ehlers, S., et al. (2001) · Cellular Immunology · doi:10.1006/cimm.2001.1819 · Cited by 118 · see citing works
Indoleamine 2,3-dioxygenase 1 (IDO1) activity in leukemia blasts correlates with poor outcome in childhood acute myeloid leukemia
Folgiero, V., Goffredo, B. M., Filippini, P., Masetti, R., Bonanno, G., Caruso, R., Bertaina, V., Mastronuzzi, A., Gaspari, S., Zecca, M., et al. (2013) · Oncotarget · doi:10.18632/oncotarget.1504 · Cited by 110 · see citing works
Interferon‐γ exerts its negative regulatory effect primarily on the earliest stages of murine erythroid progenitor cell development
Wang, C. Q., Udupa, K. B., & Lipschitz, D. A. (1995) · Journal of Cellular Physiology · doi:10.1002/jcp.1041620116 · Cited by 107 · see citing works
STAT1 promotes megakaryopoiesis downstream of GATA-1 in mice
Huang, Z., Richmond, T. D., Muntean, A. G., Barber, D. L., Weiss, M. J., & Crispino, J. D. (2007) · Journal of Clinical Investigation · doi:10.1172/jci33010 · Cited by 106 · see citing works
Association between immune activation, changes of iron metabolism and anaemia in patients with HIV infection
Fuchs, D., Zangerle, R., Artner‐Dworzak, E., Weiß, G., Fritsch, P. O., Tilz, G. P., Dierich, M. P., & Wächter, H. (1993) · European Journal Of Haematology · doi:10.1111/j.1600-0609.1993.tb00147.x · Cited by 105 · see citing works
Gamma interferon (IFN gamma) and IFNalpha/beta suppress murine myeloid colony formation (CFU-C)N: magnitude of suppression is dependent upon level of colony-stimulating factor (CSF).
Klimpel, G. R., Fleischmann, W. R., & Klimpel, K. D. (1982) · The Journal of Immunology · doi:10.4049/jimmunol.129.1.76 · Cited by 103 · see citing works
A mouse model of lymphocyte infusion-induced bone marrow failure
Bloom, M. L., Wolk, A. G., Simon-Stoos, K. L., et al. (2004) · Experimental Hematology · doi:10.1016/j.exphem.2004.08.006 · Cited by 103 · see citing works
IFN-γ Negatively Modulates Self-Renewal of Repopulating Human Hemopoietic Stem Cells
Yang, L., Dybedal, I., Bryder, D., Nilsson, L., Sitnicka, E., Sasaki, Y., & Jacobsen, S. E. W. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.2.752 · Cited by 99 · see citing works
Transient Activation of Hematopoietic Stem and Progenitor Cells by IFNγ during Acute Bacterial Infection
MacNamara, K. C., Jones, M., Martin, O., & Winslow, G. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028669 · Cited by 87 · see citing works
Bone Marrow and Thymus Expression of Interferon-γ Results in Severe B-Cell Lineage Reduction, T-Cell Lineage Alterations, and Hematopoietic Progenitor Deficiencies
Young, H. A., Klinman, D. M., Reynolds, D. A., et al. (1997) · Blood · doi:10.1182/blood.v89.2.583 · Cited by 85 · see citing works
Specific depletion of the B-cell population induced by aberrant expression of human interferon regulatory factor 1 gene in transgenic mice.
Yamada, G., Ogawa, M., Akagi, K., Miyamoto, H., Nakano, N., Itoh, S., Miyazaki, J., Nishikawa, S.-I., Yamamura, K., & Taniguchi, T. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.2.532 · Cited by 83 · see citing works
Interferon‐γ 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
Grawunder, U., Melchers, F., & Rolink, A. G. (1993) · European Journal of Immunology · doi:10.1002/eji.1830230237 · Cited by 82 · see citing works
Cytotoxic T cells induce proliferation of chronic myeloid leukemia stem cells by secreting interferon-γ
Schürch, C. M., Riether, C., Amrein, M. A., & Ochsenbein, A. F. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20121229 · Cited by 81 · see citing works
Hematopoietic Remodeling in Interferon-γ–Deficient Mice Infected With Mycobacteria
Murray, P. J., Young, R. A., & Daley, G. Q. (1998) · Blood · doi:10.1182/blood.v91.8.2914.2914_2914_2924 · Cited by 79 · see citing works
Opposing roles of interferon-gamma on CD4+ T cell-mediated graft-versus-host disease: Effects of conditioning
Welniak, L. A., Blazar, B. R., Anver, M. R., et al. (2000) · Transplantation and Cellular Therapy · doi:10.1016/s1083-8791(00)70025-5 · Cited by 79 · see citing works
Fas/APO-1 (CD95)–Mediated Apoptosis Is Activated by Interferon-γ and Interferon- in Interleukin-6 (IL-6)–Dependent and IL-6–Independent Multiple Myeloma Cell Lines
Spets, H., Georgii‐Hemming, P., Siljason, J., Nilsson, K., & Jernberg‐Wiklund, H. (1998) · Blood · doi:10.1182/blood.v92.8.2914 · Cited by 76 · see citing works
Brief Report: Interferon-γ Induces Expansion of Lin−Sca-1+C-Kit+ Cells
Zhao, X., Ren, G., Li, L., Ai, P. Z., Zheng, H. B., Tischfield, J. A., Shi, Y., & Shao, C. (2009) · Stem Cells · doi:10.1002/stem.252 · Cited by 75 · see citing works
Interferon gamma selectively inhibits very primitive CD342+CD38- and not more mature CD34+CD38+ human hematopoietic progenitor cells.
Snoeck, H., Bockstaele, D. R. V., Nys, G., Lenjou, M., Lardon, F., Haenen, L., Rodrigus, I. R., Peetermans, M. E., & Berneman, Z. N. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.180.3.1177 · Cited by 66 · see citing works
Vaccinia Virus Infection Modulates the Hematopoietic Cell Compartments in the Bone Marrow
Singh, P., Yao, Y., Weliver, A., Broxmeyer, H. E., Hong, S., & Chang, C. (2008) · Stem Cells · doi:10.1634/stemcells.2007-0461 · Cited by 66 · see citing works
Homozygosis for (12) CA repeats in the first intron of the human IFN‐γ gene is significantly associated with the risk of aplastic anaemia in Caucasian population
Dufour, C., Capasso, M., Svahn, J., Marrone, A., Haupt, R., Bacigalupo, A. P., Giordani, L., Longoni, D. V., Pillon, M., Pistorio, A., et al. (2004) · British Journal of Haematology · doi:10.1111/j.1365-2141.2004.05102.x · Cited by 65 · see citing works
Expression and modulation of cellular receptors for interferon‐γ, tumour necrosis factor, and Fas on human bone marrow CD34+ cells
Sato, T., Selleri, C., Anderson, S. M., Young, N. S., & Maciejewski, J. P. (1997) · British Journal of Haematology · doi:10.1046/j.1365-2141.1997.562704.x · Cited by 64 · see citing works
Eosinophil differentiation in the bone marrow is inhibited by T cell–derived IFN-γ
de Bruin, A. M., Buitenhuis, M., van der Sluijs, K. F., van Gisbergen, K. P. J. M., Boon, L., & Nolte, M. A. (2010) · Blood · doi:10.1182/blood-2009-12-261339 · Cited by 57 · see citing works
Self-citation
Effects of cyclosporine on hematopoietic and immune functions in patients with hypoplastic myelodysplasia
Selleri, C., Maciejewski, J. P., Catalano, L., Ricci, P., Andretta, C., Luciano, L., & Rotoli, B. (2002) · Cancer · doi:10.1002/cncr.10915 · Cited by 54 · see citing works
Viral Infections Predisposing to Bacterial Infections
Mills, E. L. (1984) · Annual Review of Medicine · doi:10.1146/annurev.me.35.020184.002345 · Cited by 53 · see citing works
CD8 T Cells Require Gamma Interferon To Clear Borna Disease Virus from the Brain and Prevent Immune System-Mediated Neuronal Damage
Hausmann, J., Pagenstecher, A., Baur, K., et al. (2005) · Journal of Virology · doi:10.1128/jvi.79.21.13509-13518.2005 · Cited by 47 · see citing works
Differentiation-inducing effect of recombinant human tumor necrosis factor alpha and gamma-interferon in vitro on blast cells from patients with acute myeloid leukemia and myeloid blast crisis of chronic myeloid leukemia.
Geissler, K. H., Tricot, G. J. K., Leemhuis, T., et al. (1989) · PubMed · Cited by 47 · see citing works
Effect of lack of Interleukin‐4, Interleukin‐12, Interleukin‐18, or the Interferon‐γ receptor on virus replication, cytokine response, and lung pathology during respiratory syncytial virus infection in mice
Boelen, A., Kwakkel, J., Barends, M., et al. (2002) · Journal of Medical Virology · doi:10.1002/jmv.2180 · Cited by 46 · see citing works
Effect of recombinant gamma interferon on chronic myelogenous leukemia bone marrow progenitors.
McGlave, P. B., Mamus, S. W., Vilen, B. J., et al. (1987) · PubMed · Cited by 44 · see citing works
MyD88 Signaling in CD4 T Cells Promotes IFN-γ Production and Hematopoietic Progenitor Cell Expansion in Response to Intracellular Bacterial Infection
Zhang, Y., Jones, M., McCabe, A. F., Winslow, G. M., Avram, D., & MacNamara, K. C. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1203024 · Cited by 43 · see citing works
In vitro interferon‐gamma production by cultured T‐cells in severe aplastic anaemia: correlation with granulomonopoietic inhibition in patients who respond to anti‐thymocyte globulin
Laver, J., Castro-Malaspina, H., Kernan, N. A., Levick, J., Evans, R. L., O'Reilly, R. J., & Malcolm, A. (1988) · British Journal of Haematology · doi:10.1111/j.1365-2141.1988.tb02413.x · Cited by 38 · see citing works
Gamma Interferon Suppresses Erythropoiesis via Interleukin-15
Kanevsky, I., Szaba, F. M., Kummer, L. W., Wilhelm, L. B., Parent, M. A., Johnson, L. L., & Smiley, S. T. (2007) · Infection and Immunity · doi:10.1128/iai.01836-06 · Cited by 37 · see citing works
Posttranscriptional regulation of c-Myc expression in adult murine HSCs during homeostasis and interferon-α-induced stress response
Ehninger, A., Boch, T., Uckelmann, H. J., et al. (2014) · Blood · doi:10.1182/blood-2013-10-531038 · Cited by 36 · see citing works
Anticytokine Therapy, Especially Anti-Interferon-γ, as a Pathogenetic Treatment in TH-1 Autoimmune Diseases
Skurkovich, S. V., & Skurkovich, B. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1361.113 · Cited by 35 · see citing works
IFN-gamma abrogates IL-7-dependent proliferation in pre-B cells, coinciding with onset of apoptosis.
Garvy, B. A., & Riley, R. L. (1994) · PubMed · Cited by 35 · see citing works
Mesenchymal stem cells are mobilized from the bone marrow during inflammation
Koning, J. J., Kooij, G., de Vries, H. E., Nolte, M. A., & Mebius, R. E. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00049 · Cited by 34 · see citing works
Self-citation
Effects of interferon gamma on native human acute myelogenous leukaemia cells
Ersvær, E., Skavland, J., Ulvestad, E., et al. (2006) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-006-0159-1 · Cited by 32 · see citing works
Induction of Ly-6A/E expression by murine lymphocytes after in vivo immunization is strictly dependent upon the action of IFN-α/β and /or IFN-γ
Snapper, C. M., Yamaguchi, H., Urban, J. F., et al. (1991) · International Immunology · doi:10.1093/intimm/3.9.845 · Cited by 31 · see citing works
SOCS1 cooperates with FLT3-ITD in the development of myeloproliferative disease by promoting the escape from external cytokine control
Reddy, P. N. G., Sargin, B., Choudhary, C., Stein, S., Grez, M., Müller‐Tidow, C., Berdel, W. E., Serve, H. L., & Brandts, C. (2012) · Blood · doi:10.1182/blood-2010-08-301416 · Cited by 30 · see citing works
gamma-Interferon in multiple myeloma: inhibition of interleukin-6 (IL-6)-dependent myeloma cell growth and downregulation of IL-6-receptor expression in vitro.
Portier, M., Zhang, X.-G., Caron, E., Lu, Z.-Y., Bataille, R., & Klein, B. (1993) · Blood · doi:10.1182/blood.v81.11.3076.3076 · Cited by 30 · see citing works
Interferon-gamma enhances growth factor-dependent proliferation of clonogenic cells in acute myeloblastic leukemia
MUROHASHI, I., & Hoang, T. (1991) · Blood · doi:10.1182/blood.v78.4.1085.bloodjournal7841085 · Cited by 29 · see citing works
Nov/CCN3 regulates long-term repopulating activity of murine hematopoietic stem cells via integrin αvβ3
Ishihara, J., Umemoto, T., Yamato, M., Shiratsuchi, Y., Takaki, S., Petrich, B. G., Nakauchi, H., Eto, K., Kitamura, T., & Okano, T. (2014) · International Journal of Hematology · doi:10.1007/s12185-014-1534-x · Cited by 28 · see citing works
Interferon‐γ and interleukin‐4 reciprocally regulate the production of monocytes/macrophages and neutrophils through a direct effect on committed monopotential bone marrow progenitor cells
Snoeck, H., Lardon, F., Lenjou, M., Nys, G., Bockstaele, D. R. V., & Peetermans, M. E. (1993) · European Journal of Immunology · doi:10.1002/eji.1830230514 · Cited by 26 · see citing works
Interferon regulatory factor‐2 induces megakaryopoiesis in mouse bone marrow hematopoietic cells
Masumi, A., Hamaguchi, I., Kuramitsu, M., Mizukami, T., Takizawa, K., Momose, H., Naito, S., & Yamaguchi, K. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.10.006 · Cited by 25 · see citing works
Expression of interferon-γ by stromal cells inhibits murine long-term repopulating hematopoietic stem cell activity
Yu, J.-M., Emmons, R. V. B., Hanazono, Y., et al. (1999) · Experimental Hematology · doi:10.1016/s0301-472x(99)00009-0 · Cited by 24 · see citing works
Regulation of hematopoiesis by T lymphocytes and natural killer cells
Trinchieri, G., Murphy, M., PERUSSIA, B., & Griffin, J. D. (1987) · Critical Reviews in Oncology/Hematology · doi:10.1016/s1040-8428(87)80009-4 · Cited by 24 · see citing works
Modulation of IL-7 Thresholds by SOCS Proteins in Developing B Lineage Cells
Corfe, S. A., Rottapel, R. K., & Paige, C. J. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1100424 · Cited by 23 · see citing works
Interleukin‐12 inhibits eosinophil differentiation from bone marrow stem cells in an interferon‐γ‐dependent manner in a mouse model of asthma
Rais, M. A., Wild, J. S., Choudhury, B. K., et al. (2002) · Clinical & Experimental Allergy · doi:10.1046/j.0954-7894.2002.01350.x · Cited by 22 · see citing works
In vivo study of toxoplasmic parasitemia using interferon-γ-deficient mice: Absolute cell number of leukocytes, parasite load and cell susceptibility
Norose, K., Naoi, K., Fang, H., et al. (2008) · Parasitology International · doi:10.1016/j.parint.2008.05.007 · Cited by 21 · see citing works
Allogeneic Th1 Cells Home to Host Bone Marrow and Spleen and Mediate IFNγ-Dependent Aplasia
Chewning, J. H., Zhang, W., Randolph, D. A., et al. (2013) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2013.03.007 · Cited by 15 · see citing works
Induction of indoleamine-2,3 dioxygenase in bone marrow stromal cells inhibits myeloma cell growth
Pfeifer, S., Schreder, M., Bolomsky, A., Graffi, S., Fuchs, D., Sahota, S. S., Ludwig, H., & Zojer, N. (2012) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-012-1259-2 · Cited by 14 · see citing works
Effect of recombinant interferons on colony formation of blast progenitors in acute myeloblastic leukemia.
Takanashi, M., Motoji, T., Oshimi, K., et al. (1987) · PubMed · Cited by 13 · see citing works
Interferon-γ and Human Megakaryopoiesis
Tsuji, K., Muraoka, K., & NAKAHATA, T. (1998) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428199809057590 · Cited by 9 · see citing works
IMMUNE DISREGULATION OF HEMATOPOIESIS
Mangan, K. F. (1987) · Annual Review of Medicine · doi:10.1146/annurev.me.38.020187.000425 · Cited by 5 · see citing works

Flagged first, then by citations

Sorted by citations

Comprehensive Integration of Single-Cell Data
Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W. M., Hao, Y., Stoeckius, M., Smibert, P., & Satija, R. (2019) · Cell · doi:10.1016/j.cell.2019.05.031 · Cited by 15,453 · see citing works
Inflammation: a key regulator of hematopoietic stem cell fate in health and disease
Pietras, E. M. (2017) · Blood · doi:10.1182/blood-2017-06-780882 · Cited by 417 · see citing works
High fat diet exacerbates dextran sulfate sodium induced colitis through disturbing mucosal dendritic cell homeostasis
Cheng, L., Jin, H., Qiang, Y., Wu, S., Yan, C., Han, M., Xiao, T., Yan, N., An, H., Zhou, X., et al. (2016) · International Immunopharmacology · doi:10.1016/j.intimp.2016.08.018 · Cited by 98 · see citing works
IFN-γ-mediated hematopoietic cell destruction in murine models of immune-mediated bone marrow failure
Chen, J., Feng, X., Desierto, M. J., Keyvanfar, K., & Young, N. S. (2015) · Blood · doi:10.1182/blood-2015-06-652453 · Cited by 97 · see citing works
Inflammatory bone marrow microenvironment
Leimkühler, N. B., & Schneider, R. K. (2019) · Hematology · doi:10.1182/hematology.2019000045 · Cited by 82 · see citing works
Inflammatory signals directly instruct PU.1 in HSCs via TNF
Etzrodt, M., Ahmed, N., Hoppe, P. S., Loeffler, D., Skylaki, S., Hilsenbeck, O., Kokkaliaris, K. D., Kaltenbach, H.-M., Stelling, J., Nerlov, C., et al. (2019) · Blood · doi:10.1182/blood-2018-02-832998 · Cited by 67 · see citing works
Inflammation and the Alteration of B-Cell Physiology in Aging
Hagen, M., & Derudder, E. (2020) · Gerontology · doi:10.1159/000501963 · Cited by 58 · see citing works
Peripheral and systemic antigens elicit an expandable pool of resident memory CD8 <sup>+</sup> T cells in the bone marrow
Pascutti, M. F., Geerman, S., Collins, N., Brasser, G., Nota, B., Stark, R., Behr, F., Oja, A., Slot, E., Panagioti, E., et al. (2019) · European Journal of Immunology · doi:10.1002/eji.201848003 · Cited by 37 · see citing works
Self-citation
Interferon γ (IFNγ) Signaling via Mechanistic Target of Rapamycin Complex 2 (mTORC2) and Regulatory Effects in the Generation of Type II Interferon Biological Responses
Kroczynska, B., Rafidi, R. L., Majchrzak-Kita, B., Kosciuczuk, E. M., Blyth, G. T., Jemielity, J., Warminska, Z., Saleiro, D., Mehrotra, S., Arslan, A. D., et al. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.664995 · Cited by 29 · see citing works
Cell signaling and the aging of B cells
Labi, V., & Derudder, E. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.110985 · Cited by 9 · see citing works

Authors: de Bruin, A. M., Voermans, C., & Nolte, M. A.
Affiliations: Department of Pathology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; and
Amsterdam UMC Location University of Amsterdam (NL)
ORCID: Voermans, Carlijn
Nolte, Martijn A.
Venue: Blood
Publisher: American Society of Hematology
Published: 2014-10-16
Volume: 124
Issue: 16
Pages: 2479-2486
ISSN: 0006-4971 (ISSN-L)
1528-0020
DOI: 10.1182/blood-2014-04-568451
OpenAlex: W2050676604
Cited by: 215
References: 98
Citations by year: 2026: 20 · 2025: 19 · 2024: 13 · 2023: 15 · 2022: 18 · 2021: 24 · 2020: 15 · 2019: 19 · 2018: 21 · 2017: 18 · 2016: 16 · 2015: 13 · 2014: 4
FWCI: 2.60
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Blood (publishedVersion)
PubMed (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Pure Amsterdam UMC (submittedVersion)
Funders: Landsteiner Foundation for Blood Transfusion Research
National Cancer Institute
Topics: Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Health Sciences › Medicine › Oncology › Cytokine Signaling Pathways and Interactions
Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
Keywords: interferon-gamma, hematopoiesis, bone marrow, hematopoietic stem cells, hematopoietic progenitor cells, suppressor of cytokine signaling, cytokine receptor signaling, inflammation, anemia of chronic disease, bone marrow failure, malignant hematopoiesis, hematopoietic differentiation
MeSH terms: Animals, Bone Marrow, Hematopoiesis, Hematopoietic Stem Cells, Humans, Interferon-gamma, Transcription Factors, Signal Transduction, Cytokines, Gene Expression Regulation, Developmental

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

Impact of interferon-γ on hematopoiesis

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks