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Host Response and Inflammation

Modification of the Pulmonary MyD88 Inflammatory Response Underlies the Role of the Yersinia pestis Pigmentation Locus in Primary Pneumonic Plague

Rachel M. Olson, Miqdad O. Dhariwala, William J. Mitchell, Jerod A. Skyberg, Deborah M. Anderson
Craig R. Roy, Editor
Rachel M. Olson
aDepartment of Veterinary Pathobiology, University of Missouri College of Veterinary Medicine, Columbia, Missouri, USA
bLaboratory for Infectious Disease Research, University of Missouri College of Veterinary Medicine, Columbia, Missouri, USA
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Miqdad O. Dhariwala
aDepartment of Veterinary Pathobiology, University of Missouri College of Veterinary Medicine, Columbia, Missouri, USA
bLaboratory for Infectious Disease Research, University of Missouri College of Veterinary Medicine, Columbia, Missouri, USA
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William J. Mitchell
aDepartment of Veterinary Pathobiology, University of Missouri College of Veterinary Medicine, Columbia, Missouri, USA
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Jerod A. Skyberg
aDepartment of Veterinary Pathobiology, University of Missouri College of Veterinary Medicine, Columbia, Missouri, USA
bLaboratory for Infectious Disease Research, University of Missouri College of Veterinary Medicine, Columbia, Missouri, USA
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Deborah M. Anderson
aDepartment of Veterinary Pathobiology, University of Missouri College of Veterinary Medicine, Columbia, Missouri, USA
bLaboratory for Infectious Disease Research, University of Missouri College of Veterinary Medicine, Columbia, Missouri, USA
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Craig R. Roy
Yale University School of Medicine
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DOI: 10.1128/IAI.00595-20
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ABSTRACT

Pneumonic plague, caused by Yersinia pestis, is a rapidly progressing bronchopneumonia involving focal bacterial growth, neutrophilic congestion, and alveolar necrosis. Within a short time after inhalation of Y. pestis, inflammatory cytokines are expressed via the Toll/interleukin-1 (IL-1) adaptor myeloid differentiation primary response 88 (MyD88), which facilitates the primary lung infection. We previously showed that Y. pestis lacking the 102-kb chromosomal pigmentation locus (pgm) is unable to cause inflammatory damage in the lungs, whereas the wild-type (WT) strain induces the toxic MyD88 pulmonary inflammatory response. In this work, we investigated the involvement of the pgm in skewing the inflammatory response during pneumonic plague. We show that the early MyD88-dependent and -independent cytokine responses to pgm− Y. pestis infection of the lungs are similar yet distinct from those that occur during pgm+ infection. Furthermore, we found that MyD88 was necessary to prevent growth of the iron-starved pgm− Y. pestis despite the presence of iron chelators lactoferrin and transferrin. However, while this induced neutrophil recruitment, there was no hyperinflammatory response, and pulmonary disease was mild without MyD88. In contrast, growth in blood and tissues progressed rapidly in the absence of MyD88, due to an almost total loss of serum interferon gamma (IFN-γ). We further show that the expression of MyD88 by myeloid cells is important to control bacteremia but not the primary lung infection. The combined data indicate distinct roles for myeloid and nonmyeloid MyD88 and suggest that expression of the pgm is necessary to skew the inflammatory response in the lungs to cause pneumonic plague.

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Modification of the Pulmonary MyD88 Inflammatory Response Underlies the Role of the Yersinia pestis Pigmentation Locus in Primary Pneumonic Plague
Rachel M. Olson, Miqdad O. Dhariwala, William J. Mitchell, Jerod A. Skyberg, Deborah M. Anderson
Infection and Immunity Feb 2021, 89 (3) e00595-20; DOI: 10.1128/IAI.00595-20

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Modification of the Pulmonary MyD88 Inflammatory Response Underlies the Role of the Yersinia pestis Pigmentation Locus in Primary Pneumonic Plague
Rachel M. Olson, Miqdad O. Dhariwala, William J. Mitchell, Jerod A. Skyberg, Deborah M. Anderson
Infection and Immunity Feb 2021, 89 (3) e00595-20; DOI: 10.1128/IAI.00595-20
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KEYWORDS

MyD88
Yersinia pestis
immunopathology
inflammation
interferon gamma
pigmentation locus
plague
pneumonic plague
septicemic plague

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