Inflammation induces stress erythropoiesis through heme-dependent activation of SPI-C

Laura F. Bennett; Chang Liao; Michael D. Quickel; Beng San Yeoh; Matam Vijay-Kumar; Pamela Hankey-Giblin; K. Sandeep Prabhu; Robert F. Paulson

doi:10.1126/scisignal.aap7336

Research ArticleInflammation

Inflammation induces stress erythropoiesis through heme-dependent activation of SPI-C

View ORCID ProfileLaura F. Bennett ¹,²,
View ORCID ProfileChang Liao²,³,⁴,*,
Michael D. Quickel ²,³,⁵,
View ORCID ProfileBeng San Yeoh⁶,†,
Matam Vijay-Kumar ⁴,⁶,⁷,†,
View ORCID ProfilePamela Hankey-Giblin¹,²,³,⁴,
K. Sandeep Prabhu²,³,⁴,⁶, and
View ORCID ProfileRobert F. Paulson ¹,²,⁴,⁶,‡

¹Intercollege Graduate Program in Genetics, Penn State University, University Park, PA 16802, USA.
²Department of Veterinary and Biomedical Sciences, Penn State University, University Park, PA 16802, USA.
³Graduate Program in Pathobiology, Penn State University, University Park, PA 16802, USA.
⁴Center for Molecular Immunology and Infectious Disease, Penn State University, University Park, PA 16802, USA.
⁵Clinical and Translational Science Institute, Penn State College of Medicine, Hershey, PA 17033, USA.
⁶Graduate Program in Molecular, Cellular and Integrative Biosciences, Penn State University, University Park, PA 16802, USA.
⁷Department of Nutritional Sciences, Penn State University, University Park, PA 16802, USA.

↵‡Corresponding author. Email: rfp5{at}psu.edu

↵* Present address: Department of Medicine, University California, San Francisco, San Francisco, CA 94143, USA.
↵† Present address: Department of Physiology and Pharmacology, University of Toledo College of Medicine and Life Sciences, Toledo, OH 43614, USA.

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Science Signaling 10 Sep 2019:
Vol. 12, Issue 598, eaap7336
DOI: 10.1126/scisignal.aap7336

Laura F. Bennett

1Intercollege Graduate Program in Genetics, Penn State University, University Park, PA 16802, USA.

2Department of Veterinary and Biomedical Sciences, Penn State University, University Park, PA 16802, USA.

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ORCID record for Laura F. Bennett

Chang Liao

2Department of Veterinary and Biomedical Sciences, Penn State University, University Park, PA 16802, USA.

3Graduate Program in Pathobiology, Penn State University, University Park, PA 16802, USA.

4Center for Molecular Immunology and Infectious Disease, Penn State University, University Park, PA 16802, USA.

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Michael D. Quickel

2Department of Veterinary and Biomedical Sciences, Penn State University, University Park, PA 16802, USA.

3Graduate Program in Pathobiology, Penn State University, University Park, PA 16802, USA.

5Clinical and Translational Science Institute, Penn State College of Medicine, Hershey, PA 17033, USA.

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Beng San Yeoh

6Graduate Program in Molecular, Cellular and Integrative Biosciences, Penn State University, University Park, PA 16802, USA.

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Matam Vijay-Kumar

4Center for Molecular Immunology and Infectious Disease, Penn State University, University Park, PA 16802, USA.

6Graduate Program in Molecular, Cellular and Integrative Biosciences, Penn State University, University Park, PA 16802, USA.

7Department of Nutritional Sciences, Penn State University, University Park, PA 16802, USA.

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Pamela Hankey-Giblin

1Intercollege Graduate Program in Genetics, Penn State University, University Park, PA 16802, USA.

2Department of Veterinary and Biomedical Sciences, Penn State University, University Park, PA 16802, USA.

3Graduate Program in Pathobiology, Penn State University, University Park, PA 16802, USA.

4Center for Molecular Immunology and Infectious Disease, Penn State University, University Park, PA 16802, USA.

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K. Sandeep Prabhu

2Department of Veterinary and Biomedical Sciences, Penn State University, University Park, PA 16802, USA.

3Graduate Program in Pathobiology, Penn State University, University Park, PA 16802, USA.

4Center for Molecular Immunology and Infectious Disease, Penn State University, University Park, PA 16802, USA.

6Graduate Program in Molecular, Cellular and Integrative Biosciences, Penn State University, University Park, PA 16802, USA.

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Robert F. Paulson

1Intercollege Graduate Program in Genetics, Penn State University, University Park, PA 16802, USA.

2Department of Veterinary and Biomedical Sciences, Penn State University, University Park, PA 16802, USA.

4Center for Molecular Immunology and Infectious Disease, Penn State University, University Park, PA 16802, USA.

6Graduate Program in Molecular, Cellular and Integrative Biosciences, Penn State University, University Park, PA 16802, USA.

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ORCID record for Robert F. Paulson
For correspondence: rfp5@psu.edu

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Stress erythropoiesis during inflammation

Whereas steady-state erythropoiesis occurs in the bone marrow, stress erythropoiesis occurs in the spleen and liver. Hypoxia and acute anemia induce stress erythropoiesis to restore adequate numbers of red blood cells. Bennett et al. found that sterile inflammation mediated by Toll-like receptors (TLRs) induced stress erythropoiesis in mice by stimulating erythrocyte phagocytosis by splenic macrophages. This resulted in production of the transcription factor SPI-C, which cooperated with TLR signaling to induce the production of cytokines that increased the number of stress erythroid progenitors in the spleen. This work reveals a mechanism that compensates for the inhibition of steady-state erythropoiesis by proinflammatory cytokines.

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Inflammation induces stress erythropoiesis through heme-dependent activation of SPI-C

Stress erythropoiesis during inflammation

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