Systemic Virus Infections Differentially Modulate Cell Cycle State and Functionality of Long-Term Hematopoietic Stem Cells In Vivo

Quiescent long-term hematopoietic stem cells (LT-HSCs) are efficiently activated by type I interferon (IFN-I). However, this effect remains poorly investigated in the context of IFN-I-inducing virus infections. Here we report that both vesicular stomatitis virus (VSV) and murine cytomegalovirus (MCM...

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Published in:	Cell reports (Cambridge) Vol. 19; no. 11; pp. 2345 - 2356
Main Authors:	Hirche, Christoph, Frenz, Theresa, Haas, Simon F., Döring, Marius, Borst, Katharina, Tegtmeyer, Pia-K., Brizic, Ilija, Jordan, Stefan, Keyser, Kirsten, Chhatbar, Chintan, Pronk, Eline, Lin, Shuiping, Messerle, Martin, Jonjic, Stipan, Falk, Christine S., Trumpp, Andreas, Essers, Marieke A.G., Kalinke, Ulrich
Format:	Journal Article
Language:	English
Published:	United States Elsevier Inc 13-06-2017 Elsevier
Subjects:	Animals bone marrow transplantation Cell Cycle Cell Proliferation hematopoietic stem cells Hematopoietic Stem Cells - cytology Hematopoietic Stem Cells - metabolism Infection - virology inflammatory cytokines Mice quiescence Signal Transduction stem cell activation stem cell function systemic inflammation transplant complications virus infections systemic inflammation transplant complications stem cell activation cell cycle stem cell function quiescence inflammatory cytokines hematopoietic stem cells bone marrow transplantation virus infections
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Abstract	Quiescent long-term hematopoietic stem cells (LT-HSCs) are efficiently activated by type I interferon (IFN-I). However, this effect remains poorly investigated in the context of IFN-I-inducing virus infections. Here we report that both vesicular stomatitis virus (VSV) and murine cytomegalovirus (MCMV) infection induce LT-HSC activation that substantially differs from the effects triggered upon injection of synthetic IFN-I-inducing agents. In both infections, inflammatory responses had to exceed local thresholds within the bone marrow to confer LT-HSC cell cycle entry, and IFN-I receptor triggering was not critical for this activation. After resolution of acute MCMV infection, LT-HSCs returned to phenotypic quiescence. However, non-acute MCMV infection induced a sustained inflammatory milieu within the bone marrow that was associated with long-lasting impairment of LT-HSC function. In conclusion, our results show that systemic virus infections fundamentally affect LT-HSCs and that also non-acute inflammatory stimuli in bone marrow donors can affect the reconstitution potential of bone marrow transplants. [Display omitted] •Acute virus infections activate LT-HSCs independently of IFN-I receptor signaling•A bone marrow-intrinsic inflammatory threshold prevents excessive LT-HSC activation•Non-acute MCMV infection alters the bone marrow milieu and LT-HSC gene expression•Despite the return to phenotypic quiescence, LT-HSCs retain functional deficits Long-term hematopoietic stem cells (LT-HSCs) are activated by recombinant type I interferon (IFN-I). Hirche et al. report here that acute systemic virus infections activate LT-HSCs independently of IFN-I receptor signaling. Non-acute infection of bone marrow donors impacts LT-HSC function, but not phenotype, potentially explaining clinical complications following bone marrow transplantations.
AbstractList	Quiescent long-term hematopoietic stem cells (LT-HSCs) are efficiently activated by type I interferon (IFN-I). However, this effect remains poorly investigated in the context of IFN-I-inducing virus infections. Here we report that both vesicular stomatitis virus (VSV) and murine cytomegalovirus (MCMV) infection induce LT-HSC activation that substantially differs from the effects triggered upon injection of synthetic IFN-I-inducing agents. In both infections, inflammatory responses had to exceed local thresholds within the bone marrow to confer LT-HSC cell cycle entry, and IFN-I receptor triggering was not critical for this activation. After resolution of acute MCMV infection, LT-HSCs returned to phenotypic quiescence. However, non-acute MCMV infection induced a sustained inflammatory milieu within the bone marrow that was associated with long-lasting impairment of LT-HSC function. In conclusion, our results show that systemic virus infections fundamentally affect LT-HSCs and that also non-acute inflammatory stimuli in bone marrow donors can affect the reconstitution potential of bone marrow transplants. Quiescent long-term hematopoietic stem cells (LT-HSCs) are efficiently activated by type I interferon (IFN-I). However, this effect remains poorly investigated in the context of IFN-I-inducing virus infections. Here we report that both vesicular stomatitis virus (VSV) and murine cytomegalovirus (MCMV) infection induce LT-HSC activation that substantially differs from the effects triggered upon injection of synthetic IFN-I-inducing agents. In both infections, inflammatory responses had to exceed local thresholds within the bone marrow to confer LT-HSC cell cycle entry, and IFN-I receptor triggering was not critical for this activation. After resolution of acute MCMV infection, LT-HSCs returned to phenotypic quiescence. However, non-acute MCMV infection induced a sustained inflammatory milieu within the bone marrow that was associated with long-lasting impairment of LT-HSC function. In conclusion, our results show that systemic virus infections fundamentally affect LT-HSCs and that also non-acute inflammatory stimuli in bone marrow donors can affect the reconstitution potential of bone marrow transplants. [Display omitted] •Acute virus infections activate LT-HSCs independently of IFN-I receptor signaling•A bone marrow-intrinsic inflammatory threshold prevents excessive LT-HSC activation•Non-acute MCMV infection alters the bone marrow milieu and LT-HSC gene expression•Despite the return to phenotypic quiescence, LT-HSCs retain functional deficits Long-term hematopoietic stem cells (LT-HSCs) are activated by recombinant type I interferon (IFN-I). Hirche et al. report here that acute systemic virus infections activate LT-HSCs independently of IFN-I receptor signaling. Non-acute infection of bone marrow donors impacts LT-HSC function, but not phenotype, potentially explaining clinical complications following bone marrow transplantations.
Author	Döring, Marius Lin, Shuiping Tegtmeyer, Pia-K. Hirche, Christoph Kalinke, Ulrich Borst, Katharina Messerle, Martin Falk, Christine S. Haas, Simon F. Jordan, Stefan Frenz, Theresa Keyser, Kirsten Trumpp, Andreas Brizic, Ilija Essers, Marieke A.G. Chhatbar, Chintan Pronk, Eline Jonjic, Stipan
Author_xml	– sequence: 1 givenname: Christoph surname: Hirche fullname: Hirche, Christoph organization: Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Hannover Medical School and the Helmholtz Centre for Infection Research, 30625 Hannover, Germany – sequence: 2 givenname: Theresa surname: Frenz fullname: Frenz, Theresa organization: Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Hannover Medical School and the Helmholtz Centre for Infection Research, 30625 Hannover, Germany – sequence: 3 givenname: Simon F. surname: Haas fullname: Haas, Simon F. organization: Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), 69120 Heidelberg, Germany – sequence: 4 givenname: Marius surname: Döring fullname: Döring, Marius organization: Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Hannover Medical School and the Helmholtz Centre for Infection Research, 30625 Hannover, Germany – sequence: 5 givenname: Katharina surname: Borst fullname: Borst, Katharina organization: Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Hannover Medical School and the Helmholtz Centre for Infection Research, 30625 Hannover, Germany – sequence: 6 givenname: Pia-K. surname: Tegtmeyer fullname: Tegtmeyer, Pia-K. organization: Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Hannover Medical School and the Helmholtz Centre for Infection Research, 30625 Hannover, Germany – sequence: 7 givenname: Ilija surname: Brizic fullname: Brizic, Ilija organization: Department of Histology and Embryology, Faculty of Medicine, University of Rijeka, 51000 Rijeka, Croatia – sequence: 8 givenname: Stefan surname: Jordan fullname: Jordan, Stefan organization: Icahn School of Medicine at Mount Sinai, Department of Oncological Sciences, New York, NY 10029, USA – sequence: 9 givenname: Kirsten surname: Keyser fullname: Keyser, Kirsten organization: Department of Virology, Hannover Medical School, 30625 Hannover, Germany – sequence: 10 givenname: Chintan surname: Chhatbar fullname: Chhatbar, Chintan organization: Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Hannover Medical School and the Helmholtz Centre for Infection Research, 30625 Hannover, Germany – sequence: 11 givenname: Eline surname: Pronk fullname: Pronk, Eline organization: Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), 69120 Heidelberg, Germany – sequence: 12 givenname: Shuiping surname: Lin fullname: Lin, Shuiping organization: Molecular Medicine Division, Walter and Eliza Hall Institute of Medical Research, Parkville, VIC 3052, Australia – sequence: 13 givenname: Martin surname: Messerle fullname: Messerle, Martin organization: Department of Virology, Hannover Medical School, 30625 Hannover, Germany – sequence: 14 givenname: Stipan surname: Jonjic fullname: Jonjic, Stipan organization: Department of Histology and Embryology, Faculty of Medicine, University of Rijeka, 51000 Rijeka, Croatia – sequence: 15 givenname: Christine S. surname: Falk fullname: Falk, Christine S. organization: Institute of Transplant Immunology, IFB-Tx, Hannover Medical School, 30625 Hannover, Germany – sequence: 16 givenname: Andreas surname: Trumpp fullname: Trumpp, Andreas organization: Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), 69120 Heidelberg, Germany – sequence: 17 givenname: Marieke A.G. surname: Essers fullname: Essers, Marieke A.G. organization: Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), 69120 Heidelberg, Germany – sequence: 18 givenname: Ulrich surname: Kalinke fullname: Kalinke, Ulrich email: ulrich.kalinke@twincore.de organization: Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Hannover Medical School and the Helmholtz Centre for Infection Research, 30625 Hannover, Germany
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Keywords	systemic inflammation transplant complications stem cell activation cell cycle stem cell function quiescence inflammatory cytokines hematopoietic stem cells bone marrow transplantation virus infections
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Snippet	Quiescent long-term hematopoietic stem cells (LT-HSCs) are efficiently activated by type I interferon (IFN-I). However, this effect remains poorly investigated...
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SubjectTerms	Animals bone marrow transplantation Cell Cycle Cell Proliferation hematopoietic stem cells Hematopoietic Stem Cells - cytology Hematopoietic Stem Cells - metabolism Infection - virology inflammatory cytokines Mice quiescence Signal Transduction stem cell activation stem cell function systemic inflammation transplant complications virus infections
Title	Systemic Virus Infections Differentially Modulate Cell Cycle State and Functionality of Long-Term Hematopoietic Stem Cells In Vivo
URI	https://dx.doi.org/10.1016/j.celrep.2017.05.063 https://www.ncbi.nlm.nih.gov/pubmed/28614719 https://search.proquest.com/docview/1910338213 https://doaj.org/article/2995017d8b574dad8f159ba1c82bc2c7
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