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Host Response and Inflammation

Failure of CD4 T Cell-Deficient Hosts To Control Chronic Nontyphoidal Salmonella Infection Leads to Exacerbated Inflammation, Chronic Anemia, and Altered Myelopoiesis

Wendy P. Loomis, Martha A. Delaney, Matthew L. Johnson, Brad T. Cookson
Manuela Raffatellu, Editor
Wendy P. Loomis
aDepartment of Laboratory Medicine, University of Washington, Seattle, Washington, USA
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Martha A. Delaney
bDepartment of Comparative Medicine, University of Washington, Seattle, Washington, USA
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Matthew L. Johnson
aDepartment of Laboratory Medicine, University of Washington, Seattle, Washington, USA
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Brad T. Cookson
aDepartment of Laboratory Medicine, University of Washington, Seattle, Washington, USA
cDepartment of Microbiology, University of Washington, Seattle, Washington, USA
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Manuela Raffatellu
University of California San Diego School of Medicine
Roles: Editor
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DOI: 10.1128/IAI.00417-20
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ABSTRACT

Immunocompromised patients are more susceptible to recurrent nontyphoidal Salmonella (NTS) bacteremia. A key manifestation of HIV infection is the loss of CD4 T cells, which are crucial for immunity to Salmonella infection. We characterized the consequences of CD4 T cell depletion in mice where virulent Salmonella establish chronic infection, similar to chronic NTS disease in humans. Salmonella-infected, CD4-depleted 129X1/SvJ mice remained chronically colonized for at least 5 weeks, displaying increased splenomegaly and more severe splenitis than infected mice with CD4 T cells. Mature erythrocytes, immature erythroid cells, and phagocytes accounted for the largest increase in splenic cellularity. Anemia, which is associated with increased mortality in Salmonella-infected humans, was exacerbated by CD4 depletion in infected mice and was accompanied by increased splenic sequestration of erythrocytes and fewer erythropoietic elements in the bone marrow, despite significantly elevated levels of circulating erythropoietin. Splenic sequestration of red blood cells, the appearance of circulating poikilocytes, and elevated proinflammatory cytokines suggest inflammation-induced damage to erythrocytes contributes to anemia and splenic retention of damaged cells in infected animals. Depleting CD4 T cells led to increased myeloid cells in peripheral blood, spleen, and bone marrow, as well as expansion of CD8 T cells, which has been observed in CD4-depleted humans. This work describes a mouse model of Salmonella infection that recapitulates several aspects of human disease and will allow us to investigate the interplay of innate and adaptive immune functions with chronic inflammation, anemia, and susceptibility to Salmonella infection.

FOOTNOTES

    • Received 6 July 2020.
    • Returned for modification 5 August 2020.
    • Accepted 5 October 2020.
    • Accepted manuscript posted online 12 October 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Failure of CD4 T Cell-Deficient Hosts To Control Chronic Nontyphoidal Salmonella Infection Leads to Exacerbated Inflammation, Chronic Anemia, and Altered Myelopoiesis
Wendy P. Loomis, Martha A. Delaney, Matthew L. Johnson, Brad T. Cookson
Infection and Immunity Dec 2020, 89 (1) e00417-20; DOI: 10.1128/IAI.00417-20

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Failure of CD4 T Cell-Deficient Hosts To Control Chronic Nontyphoidal Salmonella Infection Leads to Exacerbated Inflammation, Chronic Anemia, and Altered Myelopoiesis
Wendy P. Loomis, Martha A. Delaney, Matthew L. Johnson, Brad T. Cookson
Infection and Immunity Dec 2020, 89 (1) e00417-20; DOI: 10.1128/IAI.00417-20
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KEYWORDS

CD4 T cell
CD4 deficiency
Salmonella
anemia
Bone Marrow
cellular immune response
inflammation

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