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

2.

Weiss

G

,

Ganz

T

,

Goodnough

LT

.

Anemia of inflammation

.

Blood

.

2019

;

133

(

1

):

40

-

50

.

3.

Crooks

CJ

,

West

J

,

Morling

JR

, et al.

Anaemia of acute inflammation: a higher acute systemic inflammatory response is associated with a larger decrease in blood haemoglobin levels in patients with COVID-19 infection

.

Clin Med

.

2023

;

23

(

3

):

201

-

205

.

4.

Kalliolias

GD

,

Ivashkiv

LB

.

TNF biology, pathogenic mechanisms and emerging therapeutic strategies

.

Nat Rev Rheumatol

.

2016

;

12

(

1

):

49

-

62

.

5.

Papadaki

HA

,

Kritikos

HD

,

Valatas

V

,

Boumpas

DT

,

Eliopoulos

GD

.

Anemia of chronic disease in rheumatoid arthritis is associated with increased apoptosis of bone marrow erythroid cells: improvement following anti-tumor necrosis factor-alpha antibody therapy

.

Blood

.

2002

;

100

(

2

):

474

-

482

.

6.

Holbrook

J

,

Lara-Reyna

S

,

Jarosz-Griffiths

H

,

McDermott

MF

.

Tumour necrosis factor signalling in health and disease

.

F1000Res

.

2019

;

8

.

7.

Roodman

GD

,

Johnson

RA

,

Clibon

U

.

Tumor necrosis factor alpha and the anemia of chronic disease: effects of chronic exposure to TNF on erythropoiesis in vivo

.

Adv Exp Med Biol

.

1989

;

271

:

185

-

196

.

8.

Alvarez-Hernández

X

,

Licéaga

J

,

McKay

IC

,

Brock

JH

.

Induction of hypoferremia and modulation of macrophage iron metabolism by tumor necrosis factor

.

Lab Invest

.

1989

;

61

(

3

):

319

-

322

.

9.

Hodge-Dufour

J

,

Marino

MW

,

Horton

MR

, et al.

Inhibition of interferon gamma induced interleukin 12 production: a potential mechanism for the anti-inflammatory activities of tumor necrosis factor

.

Proc Natl Acad Sci U S A

.

1998

;

95

(

23

):

13806

-

13811

.

10.

De Benedetti

F

,

Prencipe

G

,

Bracaglia

C

,

Marasco

E

,

Grom

AA

.

Targeting interferon-γ in hyperinflammation: opportunities and challenges

.

Nat Rev Rheumatol

.

2021

;

17

(

11

):

678

-

691

.

11.

Kak

G

,

Raza

M

,

Tiwari

BK

.

Interferon-gamma (IFN-γ): exploring its implications in infectious diseases

.

Biomol Concepts

.

2018

;

9

(

1

):

64

-

79

.

12.

Lee

SK

,

Silva

DG

,

Martin

JL

, et al.

Interferon-γ excess leads to pathogenic accumulation of follicular helper T cells and germinal centers

.

Immunity

.

2012

;

37

(

5

):

880

-

892

.

13.

Vadhan-Raj

S

,

Al-Katib

A

,

Bhalla

R

, et al.

Phase I trial of recombinant interferon gamma in cancer patients

.

J Clin Oncol

.

1986

;

4

(

2

):

137

-

146

.

14.

de Bruin

AM

,

Voermans

C

,

Nolte

MA

.

Impact of interferon-g on hematopoiesis

.

Blood

.

2014

;

124

(

16

):

2479

-

2486

.

15.

Raefsky

EL

,

Platanias

LC

,

Zoumbos

NC

,

Young

NS

.

Studies of interferon as a regulator of hematopoietic cell proliferation

.

J Immunol

.

1985

;

135

(

4

):

2507

-

2512

.

16.

Mullarky

IK

,

Szaba

FM

,

Kummer

LW

, et al.

Gamma interferon suppresses erythropoiesis via interleukin-15

.

Infect Immun

.

2007

;

75

(

5

):

2630

-

2633

.

17.

Libregts

SF

,

Gutiérrez

L

,

de Bruin

AM

, et al.

Chronic IFN-γ production in mice induces anemia by reducing erythrocyte life span and inhibiting erythropoiesis through an IRF-1/PU.1 axis

.

Blood

.

2011

;

118

(

9

):

2578

-

2588

.

18.

Johnson

CS

,

Pourbohloul

SC

,

Furmanski

P

.

Negative regulators of in vivo erythropoiesis: interaction of IL-1 alpha and TNF-alpha and the lack of a strict requirement for T or NK cells for their activity

.

Exp Hematol

.

1991

;

19

(

2

):

101

-

105

.

19.

Rusten

LS

,

Jacobsen

SE

.

Tumor necrosis factor (TNF)-alpha directly inhibits human erythropoiesis in vitro: role of p55 and p75 TNF receptors

.

Blood

.

1995

;

85

(

4

):

989

-

996

.

20.

Johnson

CS

,

Cook

CA

,

Furmanski

P

.

In vivo suppression of erythropoiesis by tumor necrosis factor-alpha (TNF-alpha): reversal with exogenous erythropoietin (EPO)

.

Exp Hematol

.

1990

;

18

(

2

):

109

-

113

.

21.

Morceau

F

,

Dicato

M

,

Diederich

M

.

Pro-inflammatory cytokine-mediated anemia: regarding molecular mechanisms of erythropoiesis

.

Mediators Inflamm

.

2009

;

2009

:

405016

.

22.

Felli

N

,

Pedini

F

,

Zeuner

A

, et al.

Multiple members of the TNF superfamily contribute to IFN-gamma-mediated inhibition of erythropoiesis

.

J Immunol

.

2005

;

175

(

3

):

1464

-

1472

.

23.

Gardenghi

S

,

Renaud

TM

,

Meloni

A

, et al.

Distinct roles for hepcidin and interleukin-6 in the recovery from anemia in mice injected with heat-killed Brucella abortus

.

Blood

.

2014

;

123

(

8

):

1137

-

1145

.

24.

Guerra

A

,

Oikonomidou

PR

,

Sinha

S

, et al.

Lack of Gdf11 does not improve anemia or prevent the activity of RAP-536 in a mouse model of β-thalassemia

.

Blood

.

2019

;

134

(

6

):

568

-

572

.

25.

Parrow

NL

,

Li

Y

,

Feola

M

, et al.

Lobe specificity of iron binding to transferrin modulates murine erythropoiesis and iron homeostasis

.

Blood

.

2019

;

134

(

17

):

1373

-

1384

.

26.

Dholakia

U

,

Bandyopadhyay

S

,

Hod

EA

,

Prestia

KA

.

Determination of RBC survival in C57BL/6 and C57BL/6-Tg(UBC–GFP) mice

.

Comp Med

.

2015

;

65

(

3

):

196

-

201

.

27.

Chen

K

,

Liu

J

,

Heck

S

,

Chasis

JA

,

An

X

,

Mohandas

N

.

Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis

.

Proc Natl Acad Sci U S A

.

2009

;

106

(

41

):

17413

-

17418

.

28.

Purton

LE

.

Adult murine hematopoietic stem cells and progenitors: an update on their identities, functions, and assays

.

Exp Hematol

.

2022

;

116

:

1

-

14

.

29.

Chappell

ME

,

Breda

L

,

Tricoli

L

, et al.

Use of HSC-targeted LNP to generate a mouse model of lethal α-thalassemia and treatment via lentiviral gene therapy

.

Blood

.

2024

;

144

(

15

):

1633

-

1645

.

30.

Yamashita

M

,

Passegué

E

.

TNF-α coordinates hematopoietic stem cell survival and myeloid regeneration

.

Cell Stem Cell

.

2019

;

25

(

3

):

357

-

372.e7

.

31.

Ruan

B

,

Paulson

RF

.

Metabolic regulation of stress erythropoiesis, outstanding questions, and possible paradigms

.

Front Physiol

.

2022

;

13

:

1063294

.

32.

Paulson

RF

,

Hariharan

S

,

Little

JA

.

Stress erythropoiesis: definitions and models for its study

.

Exp Hematol

.

2020

;

89

:

43

-

54.e2

.

33.

Bennett

LF

,

Liao

C

,

Quickel

MD

, et al.

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

.

Sci Signal

.

2019

;

12

(

598

):

eaap7336

.

34.

Salomon

BL

,

Leclerc

M

,

Tosello

J

,

Ronin

E

,

Piaggio

E

,

Cohen

JL

.

Tumor necrosis factor α and regulatory T cells in oncoimmunology

.

Front Immunol

.

2018

;

9

:

444

.

35.

Zheng

J

,

Umikawa

M

,

Zhang

S

, et al.

Ex vivo expanded hematopoietic stem cells overcome the MHC barrier in allogeneic transplantation

.

Cell Stem Cell

.

2011

;

9

(

2

):

119

-

130

.

36.

Ma

X

.

TNF-α and IL-12:a balancing act in macrophage functioning

.

Microbes Infect

.

2001

;

3

(

2

):

121

-

129

.

37.

Masli

S

,

Turpie

B

.

Anti-inflammatory effects of tumour necrosis factor (TNF)-α are mediated via TNF-R2 (p75) in tolerogenic transforming growth factor-β-treated antigen-presenting cells

.

Immunology

.

2009

;

127

(

1

):

62

-

72

.

38.

Alam

Z

,

Devalaraja

S

,

Li

M

, et al.

Counter regulation of spic by NF-κB and STAT signaling controls inflammation and iron metabolism in macrophages

.

Cell Rep

.

2020

;

31

(

13

):

107825

.

39.

Guerra

A

,

Parhiz

H

,

Rivella

S

.

Novel potential therapeutics to modify iron metabolism and red cell synthesis in diseases associated with defective erythropoiesis

.

Haematologica

.

2023

;

108

(

10

):

2582

-

2593

.

40.

Nemeth

E

,

Valore

EV

,

Territo

M

,

Schiller

G

,

Lichtenstein

A

,

Ganz

T

.

Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein

.

Blood

.

2003

;

101

(

7

):

2461

-

2463

.

41.

Zakharova

M

,

Ziegler

HK

.

Paradoxical anti-inflammatory actions of TNF-α: inhibition of IL-12 and IL-23 via TNF receptor 1 in macrophages and dendritic cells

.

J Immunol

.

2005

;

175

(

8

):

5024

-

5033

.

42.

Speiser

DE

,

Sebzda

E

,

Ohteki

T

, et al.

Tumor necrosis factor receptor p55 mediates deletion of peripheral cytotoxic T lymphocytes in vivo

.

Eur J Immunol

.

1996

;

26

(

12

):

3055

-

3060

.

43.

Kanaly

ST

,

Nashleanas

M

,

Hondowicz

B

,

Scott

P

.

TNF receptor p55 is required for elimination of inflammatory cells following control of intracellular pathogens

.

J Immunol

.

1999

;

163

(

7

):

3883

-

3889

.

44.

Siegmund

D

,

Wajant

H

.

TNF and TNF receptors as therapeutic targets for rheumatic diseases and beyond

.

Nat Rev Rheumatol

.

2023

;

19

(

9

):

576

-

591

.

45.

Morales-Mantilla

DE

,

King

KY

.

The role of interferon-gamma in hematopoietic stem cell development, homeostasis, and disease

.

Curr Stem Cell Rep

.

2018

;

4

(

3

):

264

-

271

.

46.

Salomon

BL

.

Insights into the biology and therapeutic implications of TNF and regulatory T cells

.

Nat Rev Rheumatol

.

2021

;

17

(

8

):

487

-

504

.