TNFα signaling restores steady-state hematopoiesis in a TNFαKO mouse model of anemia of inflammation

A Amaliris Guerra (1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA) V Vania lo Presti D Ding-Wen Chen (1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA) A Ana Catarina Martins (3iNOVA4Health, Nova Medical School, Faculdade de Ciências Médicas, Universidade Nova de Lisboa, Lisbon, Portugal) A Ariel Rivera (1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA) N Nolan Hamilton (1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA) P Pankja Sharma (1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA) Y Yelena Z. Ginzburg (Division of Hematology and Medical Oncology, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai) C Carlo Castruccio Castracani (4The Children's Hospital of Philadelphia, Philadelphia, United States) C Carla Casu (1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA) R Ritama Gupta (1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA) R Raffaella Gozzelino (3iNOVA4Health, Nova Medical School, Faculdade de Ciências Médicas, Universidade Nova de Lisboa, Lisbon, Portugal) E Edward M. Behrens (5Division of Rheumatology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA) L Laura F. Bennett (6Center for Molecular Immunology and Infectious Disease, The Pennsylvania State University, University Park, PA) R Robert F. Paulson (6Center for Molecular Immunology and Infectious Disease, The Pennsylvania State University, University Park, PA) P Peter Kurre (1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA) S Stefano Rivella (4The Children's Hospital of Philadelphia, Philadelphia, United States)

Abstract

Abstract Anemia of inflammation (AI) is the second most common form of anemia and is prevalent in patients with chronic inflammatory states, such as infection, autoimmunity, and cancer. Interleukin 6 (IL-6) is well-known to induce the iron-sequestering hormone hepcidin, which results in iron-restricted anemia. The contributions of other proinflammatory cytokines, such as tumor necrosis factor-α (TNFα) and interferon gamma (IFNγ), are less understood in the pathophysiology of AI. This study investigated the role of TNFα in a mouse model of AI by administering heat-killed Brucella abortus (HKBA) to germ line TNFα knockout (KO) mice. We hypothesized that TNFα possessed an important role in restoring steady-state erythropoiesis after inflammatory insult. TNFαKO injected with HKBA displayed a chronic anemia, with elevated proinflammatory IL12p40 and IFNγ cytokines that did not resolve. However, IFNγKO and TNFαKO/FNγKO double knockout mice showed reduced inflammation and anemia following HKBA administration. Because IFNγKO displayed normal serum TNFα and IL12p40 levels, we hypothesized that the persistent anemia was IFNγ induced and TNFα was necessary for AI cessation. However, treatment with recombinant TNFα (rTNFα) accelerated death, while reducing IFNγ using an anti-IFNγ antibody (Ab) only briefly improved anemia. Only the combination of both the Ab and rTNFα together reversed the hyperinflammatory phenotype, restored erythropoiesis, and prevented death of TNFαKO + HKBA mice. Our data provide compelling evidence for an anti-inflammatory role of TNFα that is necessary for the restoration of erythropoiesis and mitigation of proinflammatory IFNγ action in a mouse model of AI.

Article Details

Journal Blood
Volume / Issue Vol. 146, Issue 8
Published August 21, 2025
Pages 984-997
ISSN 0006-4971
Publisher Elsevier BV

Journal Info

Blood

Elsevier BV

ISSN: 0006-4971 Health Sciences

Authors (17)

A

Amaliris Guerra

1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA

V

Vania lo Presti

D

Ding-Wen Chen

1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA

A

Ana Catarina Martins

3iNOVA4Health, Nova Medical School, Faculdade de Ciências Médicas, Universidade Nova de Lisboa, Lisbon, Portugal

A

Ariel Rivera

1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA

N

Nolan Hamilton

1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA

P

Pankja Sharma

1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA

Y

Yelena Z. Ginzburg

Division of Hematology and Medical Oncology, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai

C

Carlo Castruccio Castracani

4The Children's Hospital of Philadelphia, Philadelphia, United States

C

Carla Casu

1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA

R

Ritama Gupta

1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA

R

Raffaella Gozzelino

3iNOVA4Health, Nova Medical School, Faculdade de Ciências Médicas, Universidade Nova de Lisboa, Lisbon, Portugal

E

Edward M. Behrens

5Division of Rheumatology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA

L

Laura F. Bennett

6Center for Molecular Immunology and Infectious Disease, The Pennsylvania State University, University Park, PA

R

Robert F. Paulson

6Center for Molecular Immunology and Infectious Disease, The Pennsylvania State University, University Park, PA

P

Peter Kurre

1Division of Hematology, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA

S

Stefano Rivella

4The Children's Hospital of Philadelphia, Philadelphia, United States