LepR+ niche cell–derived AREG compromises hematopoietic stem cell maintenance under conditions of DNA repair deficiency and aging

2.

Himburg

HA

,

Termini

CM

,

Schlussel

L

, et al.

Distinct bone marrow sources of pleiotrophin control hematopoietic stem cell maintenance and regeneration

.

Cell Stem Cell

.

2018

;

23

(

3

):

370

-

381.e5

.

3.

Joseph

C

,

Quach

JM

,

Walkley

CR

,

Lane

SW

,

Lo Celso

C

,

Purton

LE

.

Deciphering Hematopoietic stem cells in their niches: a critical appraisal of genetic models, lineage tracing, and imaging strategies

.

Cell Stem Cell

.

2013

;

13

(

5

):

520

-

533

.

4.

Zhou

BO

,

Ding

L

,

Morrison

SJ

.

Hematopoietic stem and progenitor cells regulate the regeneration of their niche by secreting angiopoietin-1

.

eLife

.

2015

;

4

:

e05521

.

5.

Zhou

BO

,

Yu

H

,

Yue

R

, et al.

Bone marrow adipocytes promote the regeneration of stem cells and haematopoiesis by secreting SCF

.

Nat Cell Biol

.

2017

;

19

(

8

):

891

-

903

.

6.

Mendelson

A

,

Frenette

PS

.

Hematopoietic stem cell niche maintenance during homeostasis and regeneration

.

Nat Med

.

2014

;

20

(

8

):

833

-

846

.

7.

Wei

Q

,

Frenette

PS

.

Niches for hematopoietic stem cells and their progeny

.

Immunity

.

2018

;

48

(

4

):

632

-

648

.

8.

Zhou

BO

,

Yue

R

,

Murphy

MM

,

Peyer

JG

,

Morrison

SJ

.

Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow

.

Cell Stem Cell

.

2014

;

15

(

2

):

154

-

168

.

9.

Ding

L

,

Saunders

TL

,

Enikolopov

G

,

Morrison

SJ

.

Endothelial and perivascular cells maintain hematopoietic stem cells

.

Nature

.

2012

;

481

(

7382

):

457

-

462

.

10.

Ding

L

,

Morrison

SJ

.

Hematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches

.

Nature

.

2013

;

495

(

7440

):

231

-

235

.

11.

Welsh

C

,

Day

R

,

McGurk

C

,

Masters

JRW

,

Wood

RD

,

Köberle

B

.

Reduced levels of XPA, ERCC1 and XPF DNA repair proteins in testis tumour cell lines

.

Int J Cancer

.

2004

;

110

(

3

):

352

-

361

.

12.

Mendoza

J

,

Martínez

J

,

Hernández

C

, et al.

Association between ERCC1 and XPA expression and polymorphisms and the response to cisplatin in testicular germ cell tumours

.

Br J Cancer

.

2013

;

109

(

1

):

68

-

75

.

13.

Ciccia

A

,

Elledge

SJ

.

The DNA damage response: making it safe to play with knives

.

Mol Cell

.

2010

;

40

(

2

):

179

-

204

.

14.

Pan

MR

,

Li

K

,

Lin

SY

,

Hung

WC

.

Connecting the dots: from DNA damage and repair to aging

.

Int J Mol Sci

.

2016

;

17

(

5

):

685

.

15.

Naka

K

,

Hirao

A

.

Maintenance of genomic integrity in hematopoietic stem cells

.

Int J Hematol

.

2011

;

93

(

4

):

434

-

439

.

16.

Rossi

DJ

,

Bryder

D

,

Seita

J

,

Nussenzweig

A

,

Hoeijmakers

J

,

Weissman

IL

.

Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age

.

Nature

.

2007

;

447

(

7145

):

725

-

729

.

17.

Zhang

S

,

Yajima

H

,

Huynh

H

, et al.

Congenital bone marrow failure in DNA-PKcs mutant mice associated with deficiencies in DNA repair

.

J Cell Biol

.

2011

;

193

(

2

):

295

-

305

.

18.

Geiger

H

,

de Haan

G

,

Florian

MC

.

The ageing haematopoietic stem cell compartment

.

Nat Rev Immunol

.

2013

;

13

(

5

):

376

-

389

.

19.

Li

T

,

Zhou

ZW

,

Ju

Z

,

Wang

ZQ

.

DNA damage response in hematopoietic stem cell ageing

.

Genomics Proteomics Bioinformatics

.

2016

;

14

(

3

):

147

-

154

.

20.

Moehrle

BM

,

Geiger

H

.

Aging of hematopoietic stem cells: DNA damage and mutations

.

Exp Hematol

.

2016

;

44

(

10

):

895

-

901

.

21.

Doan

PL

,

Himburg

HA

,

Helms

K

, et al.

Epidermal growth factor regulates hematopoietic regeneration following radiation injury

.

Nat Med

.

2013

;

19

(

3

):

295

-

304

.

22.

Lin

Q

,

Wu

L

,

Chatla

S

, et al.

Hematopoietic stem cell regeneration through paracrine regulation of the Wnt5a/Prox1 signaling axis

.

J Clin Invest

.

2022

;

132

(

12

):

e155914

.

23.

Narod

SA

,

Foulkes

WD

.

BRCA1 and BRCA2: 1994 and beyond

.

Nat Rev Cancer

.

2004

;

4

(

9

):

665

-

676

.

24.

Yoshida

K

,

Miki

Y

.

Role of BRCA1 and BRCA2 as regulators of DNA repair, transcription, and cell cycle in response to DNA damage

.

Cancer Sci

.

2004

;

95

(

11

):

866

-

871

.

25.

Semmler

L

,

Reiter-Brennan

C

,

Klein

A

.

BRCA1 and breast cancer: a review of the underlying mechanisms resulting in the tissue-specific tumorigenesis in mutation carriers

.

J Breast Cancer

.

2019

;

22

(

1

):

1

-

14

.

26.

Venkitaraman

AR

.

How do mutations affecting the breast cancer genes BRCA1 and BRCA2 cause cancer susceptibility?

.

DNA Repair (Amst)

.

2019

;

81

:

102668

.

27.

Meyer

S

,

Tischkowitz

M

,

Chandler

K

,

Gillespie

A

,

Birch

JM

,

Evans

DG

.

Fanconi anaemia, BRCA2 mutations and childhood cancer: a developmental perspective from clinical and epidemiological observations with implications for genetic counselling

.

J Med Genet

.

2014

;

51

(

2

):

71

-

75

.

28.

Navarro

S

,

Meza

NW

,

Quintana-Bustamante

O

, et al.

Hematopoietic dysfunction in a mouse model for Fanconi anemia group D1

.

Mol Ther

.

2006

;

14

(

4

):

525

-

535

.

29.

Berasain

C

,

Avila

MA

.

Amphiregulin

.

Semin Cell Dev Biol

.

2014

;

28

:

31

-

41

.

30.

Zaiss

DMW

,

Gause

WC

,

Osborne

LC

,

Artis

D

.

Emerging functions of amphiregulin in orchestrating immunity, inflammation and tissue repair

.

Immunity

.

2015

;

42

(

2

):

216

-

226

.

31.

Arpaia

N

,

Green

JA

,

Moltedo

B

, et al.

A distinct function of regulatory T cells in tissue protection

.

Cell

.

2015

;

162

(

5

):

1078

-

1089

.

32.

Monticelli

LA

,

Sonnenberg

GF

,

Abt

MC

, et al.

Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus

.

Nat Immunol

.

2011

;

12

(

11

):

1045

-

1054

.

33.

Zaiss

DM

,

van Loosdregt

J

,

Gorlani

A

, et al.

Amphiregulin enhances regulatory T cell-suppressive function via the epidermal growth factor receptor

.

Immunity

.

2013

;

38

(

2

):

275

-

284

.

34.

Meulenbroeks

C

,

van Weelden

H

,

Schwartz

C

, et al.

Basophil-derived amphiregulin is essential for UVB irradiation-induced immune suppression

.

J Invest Dermatol

.

2015

;

135

(

1

):

222

-

228

.

35.

Dai

K

,

Huang

L

,

Sun

X

,

Yang

L

,

Gong

Z

.

Hepatic CD206-positive macrophages express amphiregulin to promote the immunosuppressive activity of regulatory T cells in HBV infection

.

J Leukoc Biol

.

2015

;

98

(

6

):

1071

-

1080

.

36.

Xu

Q

,

Chiao

P

,

Sun

Y

.

Amphiregulin in cancer: new insights for translational medicine

.

Trends Cancer

.

2016

;

2

(

3

):

111

-

113

.

37.

Minutti

CM

,

Modak

RV

,

Macdonald

F

, et al.

A macrophage-pericyte axis directs tissue restoration via amphiregulin-induced transforming growth factor Beta activation

.

Immunity

.

2019

;

50

(

3

):

645

-

654.e6

.

38.

Ko

JH

,

Kim

HJ

,

Jeong

HJ

,

Lee

HJ

,

Oh

JY

.

Mesenchymal stem and stromal cells harness macrophage-derived amphiregulin to maintain tissue homeostasis

.

Cell Rep

.

2020

;

30

(

11

):

3806

-

3820.e6

.

39.

Schuger

L

,

Johnson

GR

,

Gilbride

K

,

Plowman

GD

,

Mandel

R

.

Amphiregulin in lung branching morphogenesis: interaction with heparan sulfate proteoglycan modulates cell proliferation

.

Development

.

1996

;

122

(

6

):

1759

-

1767

.

40.

Cook

PW

,

Mattox

PA

,

Keeble

WW

, et al.

A heparin sulfate-regulated human keratinocyte autocrine factor is similar or identical to amphiregulin

.

Mol Cell Biol

.

1991

;

11

(

5

):

2547

-

2557

.

41.

Li

S

,

Plowman

GD

,

Buckley

SD

,

Shipley

GD

.

Heparin inhibition of autonomous growth implicates amphiregulin as an autocrine growth factor for normal human mammary epithelial cells

.

J Cell Physiol

.

1992

;

153

(

1

):

103

-

111

.

42.

Kennedy-Crispin

M

,

Billick

E

,

Mitsui

H

, et al.

Human keratinocytes' response to injury upregulates CCL20 and other genes linking innate and adaptive immunity

.

J Invest Dermatol

.

2012

;

132

(

1

):

105

-

113

.

43.

Roy

S

,

Krishnan

S

,

Kumar

V

,

Kesarwani

A

,

Mukhopadhyay

A

.

Amphiregulin confers protection to murine hematopoietic progenitor cells from apoptotic death

.

SciTz Stem Cell Res Ther

.

2016

;

1

(

1

):

1001

.

44.

Jonkers

J

,

Meuwissen

R

,

van der Gulden

H

,

Peterse

H

,

van der Valk

M

,

Berns

A

.

Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer

.

Nat Genet

.

2001

;

29

(

4

):

418

-

425

.

45.

Luetteke

NC

,

Qiu

TH

,

Fenton

SE

, et al.

Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development

.

Development

.

1999

;

126

(

12

):

2739

-

2750

.

46.

Houghtaling

S

,

Timmers

C

,

Noll

M

, et al.

Epithelial cancer in Fanconi anemia complementation group D2 (Fancd2) knockout mice

.

Genes Dev

.

2003

;

17

(

16

):

2021

-

2035

.

47.

Florian

MC

,

Klose

M

,

Sacma

M

, et al.

Aging alters the epigenetic asymmetry of HSC division

.

PLoS Biol

.

2018

;

16

(

9

):

e2003389

.

48.

Leshan

RL

,

Bjornholm

M

,

Munzberg

H

,

Myers

MG

.

Leptin receptor signaling and action in the central nervous system

.

Obesity (Silver Spring)

.

2006

;

14

(

suppl 5

):

208S

-

212S

.

49.

Rodda

SJ

,

McMahon

AP

.

Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors

.

Development

.

2006

;

133

(

16

):

3231

-

3244

.

50.

Alva

JA

,

Zovein

AC

,

Monvoisin

A

, et al.

VE-cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells

.

Dev Dyn

.

2006

;

235

(

3

):

759

-

767

.

51.

Lin

Q

,

Wu

L

,

Ma

Z

,

Chowdhury

FA

,

Mazumder

HH

,

Du

W

.

Persistent DNA damage-induced NLRP12 improves hematopoietic stem cell function

.

JCI Insight

.

2020

;

5

(

10

):

e133365

.

52.

Celeste

A

,

Difilippantonio

S

,

Difilippantonio

MJ

, et al.

H2AX haploinsufficiency modifies genomic stability and tumor susceptibility

.

Cell

.

2003

;

114

(

3

):

371

-

383

.

53.

Mao

Z

,

Hine

C

,

Tian

X

, et al.

SIRT6 promotes DNA repair under stress by activating PARP1

.

Science

.

2011

;

332

(

6036

):

1443

-

1446

.

54.

Du

W

,

Amarachintha

S

,

Wilson

AF

,

Pang

Q

.

Hyper-active non-homologous end joining selects for synthetic lethality resistant and pathological Fanconi anemia hematopoietic stem and progenitor cells

.

Sci Rep

.

2016

;

6

:

22167

.

55.

Holloman

WK

.

Unraveling the mechanism of BRCA2 in homologous recombination

.

Nat Struct Mol Biol

.

2011

;

18

(

7

):

748

-

754

.

56.

Xia

F

,

Taghian

DG

,

DeFrank

JS

, et al.

Deficiency of human BRCA2 leads to impaired homologous recombination but maintains normal nonhomologous end joining

.

Proc Natl Acad Sci U S A

.

2001

;

98

(

15

):

8644

-

8649

.

57.

Kiel

MJ

,

Yilmaz

OH

,

Iwashita

T

,

Yilmaz

OH

,

Terhorst

C

,

Morrison

SJ

.

SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells

.

Cell

.

2005

;

121

(

7

):

1109

-

1121

.

58.

Mann

M

,

Mehta

A

,

de Boer

CG

, et al.

Heterogeneous responses of hematopoietic stem cells to inflammatory stimuli are altered with age

.

Cell Rep

.

2018

;

25

(

11

):

2992

-

3005.e5

.

59.

Shen

H

,

Yu

H

,

Liang

PH

, et al.

An acute negative bystander effect of g-irradiated recipients on transplanted hematopoietic stem cells

.

Blood

.

2012

;

119

(

15

):

3629

-

3637

.

60.

Xu

Q

,

Long

Q

,

Zhu

D

, et al.

Targeting amphiregulin (AREG) derived from senescent stromal cells diminishes cancer resistance and averts programmed cell death 1 ligand (PD-L1)-mediated immunosuppression

.

Aging Cell

.

2019

;

18

(

6

):

e13027

.

61.

Fang

T

,

Zhang

Y

,

Chang

VY

, et al.

Epidermal growth factor receptor-dependent DNA repair promotes murine and human hematopoietic regeneration

.

Blood

.

2020

;

136

(

4

):

441

-

454

.

62.

Zaiss

DM

,

Yang

L

,

Shah

PR

,

Kobie

JJ

,

Urban

JF

,

Mosmann

TR

.

Amphiregulin, a TH2 cytokine enhancing resistance to nematodes

.

Science

.

2006

;

314

(

5806

):

1746

.

63.

Singh

B

,

Carpenter

G

,

Coffey

RJ

.

EGF receptor ligands: recent advances

.

F1000Res

.

2016

;

5

. F1000 Faculty Rev-2270.

64.

Koeppen

M

,

Lee

JW

,

Seo

SW

, et al.

Hypoxia-inducible factor 2-alpha-dependent induction of amphiregulin dampens myocardial ischemia-reperfusion injury

.

Nat Comm

.

2018

;

9

(

1

):

816

.

65.

Will

B

,

Vogler

TO

,

Bartholdy

B

, et al.

Satb1 regulates the self-renewal of hematopoietic stem cells by promoting quiescence and repressing differentiation commitment

.

Nat Immunol

.

2013

;

14

(

5

):

437

-

445

.

66.

Wilson

NK

,

Kent

DG

,

Buettner

F

, et al.

Combined single-cell functional and gene expression analysis resolves heterogeneity within stem cell populations

.

Cell Stem Cell

.

2015

;

16

(

6

):

712

-

724

.

67.

Du

W

,

Amarachintha

S

,

Wilson

A

,

Pang

Q

.

The immune receptor Trem1 cooperates with diminished DNA damage response to induce preleukemic stem cell expansion

.

Leukemia

.

2017

;

31

(

2

):

423

-

433

.

68.

de Haan

G

,

Lazare

SS

.

Aging of hematopoietic stem cells

.

Blood

.

2018

;

131

(

5

):

479

-

487

.

69.

Young

K

,

Borikar

S

,

Bell

R

,

Kuffler

L

,

Philip

V

,

Trowbridge

JJ

.

Progressive alterations in multipotent hematopoietic progenitors underlie lymphoid cell loss in aging

.

J Exp Med

.

2016

;

213

(

11

):

2259

-

2267

.

70.

Barlow

C

,

Hirotsune

S

,

Paylor

R

, et al.

Atm-deficient mice: a paradigm of ataxia telangiectasia

.

Cell

.

1996

;

86

(

1

):

159

-

171

.

71.

Crane

GM

,

Jeffery

E

,

Morrison

SJ

.

Adult hematopoietic stem cell niches

.

Nat Rev Immunol

.

2017

;

17

(

9

):

573

-

590

.

72.

Du

W

,

Adam

Z

,

Rani

R

,

Zhang

X

,

Pang

Q

.

Oxidative stress in Fanconi anemia hematopoiesis and disease progression

.

Antioxid Redox Signal

.

2008

;

10

(

11

):

1909

-

1921

.

73.

Longerich

S

,

Li

J

,

Xiong

Y

,

Sung

P

,

Kupfer

GM

.

Stress and DNA repair biology of the Fanconi anemia pathway

.

Blood

.

2014

;

124

(

18

):

2812

-

2819

.

74.

Zhan

S

,

Siu

J

,

Wang

Z

, et al.

Focal point of Fanconi anemia signaling

.

Int J Mol Sci

.

2021

;

22

(

23

):

12976

.

75.

Flach

J

,

Bakker

ST

,

Mohrin

M

, et al.

Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells

.

Nature

.

2014

;

512

(

7513

):

198

-

202

.

76.

Walter

D

,

Lier

A

,

Geiselhart

A

, et al.

Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells

.

Nature

.

2015

;

520

(

7548

):

549

-

552

.

77.

Martelli

AM

,

Evangelisti

C

,

Chiarini

F

, et al.

The emerging role of the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin signaling network in normal myelopoiesis and leukemogenesis

.

Biochim Biophys Acta

.

2010

;

1803

(

9

):

991

-

1002

.

78.

Manning

BD

,

Cantley

LC

.

AKT/PKB signaling: navigating downstream

.

Cell

.

2007

;

129

(

7

):

1261

-

1274

.

79.

Brugge

J

,

Hung

MC

,

Mills

GB

.

A new mutational AKTivation in the PI3K pathway

.

Cancer Cell

.

2007

;

12

(

2

):

104

-

107

.

80.

Humtsoe

JO

,

Kramer

RH

.

Differential epidermal growth factor receptor signaling regulates anchorage-independent growth by modulation of the PI3K/AKT pathway

.

Oncogene

.

2010

;

29

(

8

):

1214

-

1226

.

81.

Fang

L

,

Yu

Y

,

Li

Y

, et al.

Upregulation of AREG, EGFR, and HER2 contributes to increased VEGF expression in granulosa cells of patients with OHSS

.

Biol Reprod

.

2019

;

101

(

2

):

426

-

432

.

82.

Chen

Z

,

Chen

J

,

Gu

Y

, et al.

Aberrantly activated AREG-EGFR signaling is required for the growth and survival of CRTC1-MAML2 fusion-positive mucoepidermoid carcinoma cells

.

Oncogene

.

2014

;

33

(

29

):

3869

-

3877

.