Proteostasis disruption in inherited bone marrow failure syndromes Available to Purchase

2.

Shimamura

A

,

Alter

BP

.

Pathophysiology and management of inherited bone marrow failure syndromes

.

Blood Rev

.

2010

;

24

(

3

):

101

-

122

.

3.

Ruggero

D

,

Shimamura

A

.

Marrow failure: a window into ribosome biology

.

Blood

.

2014

;

124

(

18

):

2784

-

2792

.

4.

Mills

EW

,

Green

R

.

Ribosomopathies: there’s strength in numbers

.

Science

.

2017

;

358

(

6363

):

eaan2755

.

5.

Sakamoto

KM

,

Shimamura

A

,

Davies

SM

.

Congenital disorders of ribosome biogenesis and bone marrow failure

.

Biol Blood Marrow Transpl

.

2010

;

16

(

suppl 1

):

S12

-

S17

.

6.

Narla

A

,

Ebert

BL

.

Ribosomopathies: human disorders of ribosome dysfunction

.

Blood

.

2010

;

115

(

16

):

3196

-

3205

.

7.

Signer

RAJ

,

Magee

JA

,

Salic

A

,

Morrison

SJ

.

Haematopoietic stem cells require a highly regulated protein synthesis rate

.

Nature

.

2014

;

509

(

7498

):

49

-

54

.

8.

Hidalgo San Jose

L

,

Sunshine

MJ

,

Dillingham

CH

, et al.

Modest declines in proteome quality impair hematopoietic stem cell self-renewal

.

Cell Rep

.

2020

;

30

(

1

):

69

-

80.e6

.

9.

Chua

BA

,

Lennan

CJ

,

Sunshine

MJ

, et al.

Hematopoietic stem cells preferentially traffic misfolded proteins to aggresomes and depend on aggrephagy to maintain protein homeostasis

.

Cell Stem Cell

.

2023

;

30

(

4

):

460

-

472.e6

.

10.

Van Galen

P

,

Kreso

A

,

Mbong

N

, et al.

The unfolded protein response governs integrity of the haematopoietic stem-cell pool during stress

.

Nature

.

2014

;

510

(

7504

):

268

-

272

.

11.

Herrejon Chavez

F

,

Luo

H

,

Cifani

P

, et al.

RNA binding protein SYNCRIP maintains proteostasis and self-renewal of hematopoietic stem and progenitor cells

.

Nat Commun

.

2023

;

14

(

1

):

2290

.

12.

Chapple

RH

,

Hu

T

,

Tseng

YJ

, et al.

ERα promotes murine hematopoietic regeneration through the ire1α-mediated unfolded protein response

.

Elife

.

2018

;

7

:

1

-

25

.

13.

Xie

SZ

,

Garcia-Prat

L

,

Voisin

V

, et al.

Sphingolipid modulation activates proteostasis programs to govern human hematopoietic stem cell self-renewal

.

Cell Stem Cell

.

2019

;

25

(

5

):

639

-

653.e7

.

14.

Chua

BA

,

Signer

RAJ

.

Hematopoietic stem cell regulation by the proteostasis network

.

Curr Opin Hematol

.

2020

;

27

(

4

):

254

-

263

.

15.

Signer

RAJ

,

Qi

L

,

Zhao

Z

, et al.

The rate of protein synthesis in hematopoietic stem cells is limited partly by 4E-BPs

.

Genes Dev

.

2016

;

30

(

15

):

1698

-

1703

.

16.

Li

C

,

Wu

B

,

Li

Y

, et al.

Amino acid catabolism regulates hematopoietic stem cell proteostasis via a GCN2-eIF2α axis

.

Cell Stem Cell

.

2022

;

29

(

7

):

1119

-

1134.e7

.

17.

Moran-Crusio

K

,

Reavie

LB

,

Aifantis

I

.

Regulation of hematopoietic stem cell fate by the ubiquitin proteasome system

.

Trends Immunol

.

2012

;

33

(

7

):

357

-

363

.

18.

Thompson

BJ

,

Jankovic

V

,

Gao

J

, et al.

Control of hematopoietic stem cell quiescence by the E3 ubiquitin ligase Fbw7

.

J Exp Med

.

2008

;

205

(

6

):

1395

-

1408

.

19.

King

B

,

Boccalatte

F

,

Moran-Crusio

K

, et al.

The ubiquitin ligase Huwe1 regulates the maintenance and lymphoid commitment of hematopoietic stem cells

.

Nat Immunol

.

2016

;

17

(

11

):

1312

-

1321

.

20.

Reavie

L

,

Della Gatta

G

,

Crusio

K

, et al.

Regulation of hematopoietic stem cell differentiation by a single ubiquitin ligase-substrate complex

.

Nat Immunol

.

2010

;

11

(

3

):

207

-

215

.

21.

Ho

TT

,

Warr

MR

,

Adelman

ER

, et al.

Autophagy maintains the metabolism and function of young and old stem cells

.

Nature

.

2017

;

543

(

7644

):

205

-

210

.

22.

Mortensen

M

,

Soilleux

EJ

,

Djordjevic

G

, et al.

The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance

.

J Exp Med

.

2011

;

208

(

3

):

455

-

467

.

23.

Borsa

M

,

Obba

S

,

Richter

FC

, et al.

Autophagy preserves hematopoietic stem cells by restraining MTORC1-mediated cellular anabolism

.

Autophagy

.

2024

;

20

(

1

):

45

-

57

.

24.

Warr

MR

,

Binnewies

M

,

Flach

J

, et al.

FOXO3A directs a protective autophagy program in haematopoietic stem cells

.

Nature

.

2013

;

494

(

7437

):

323

-

327

.

25.

Mortensen

M

,

Watson

AS

,

Simon

AK

.

Lack of autophagy in the hematopoietic system leads to loss of hematopoietic stem cell function and dysregulated myeloid proliferation

.

Autophagy

.

2011

;

7

(

9

):

1069

-

1070

.

26.

Riffelmacher

T

,

Clarke

A

,

Richter

FC

, et al.

Autophagy-dependent generation of free fatty acids is critical for normal neutrophil differentiation

.

Immunity

.

2017

;

47

(

3

):

466

-

480.e5

.

27.

Mortensen

M

,

Ferguson

DJP

,

Edelmann

M

, et al.

Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo

.

Proc Natl Acad Sci U S A

.

2010

;

107

(

2

):

832

-

837

.

28.

van Galen

P

,

Mbong

N

,

Kreso

A

, et al.

Integrated stress response activity marks stem cells in normal hematopoiesis and leukemia

.

Cell Rep

.

2018

;

25

(

5

):

1109

-

1117.e5

.

29.

Zhu

Y

,

Poyurovsky

MV

,

Li

Y

, et al.

Ribosomal protein S7 is both a regulator and a substrate of MDM2

.

Mol Cell

.

2009

;

35

(

3

):

316

-

326

.

30.

Kruta

M

,

Sunshine

MJ

,

Chua

BA

, et al.

Hsf1 promotes hematopoietic stem cell fitness and proteostasis in response to ex vivo culture stress and aging

.

Cell Stem Cell

.

2021

;

28

(

11

):

1950

-

1965.e6

.

31.

Ulirsch

JC

,

Verboon

JM

,

Kazerounian

S

, et al.

The genetic landscape of Diamond-Blackfan anemia

.

Am J Hum Genet

.

2018

;

103

(

6

):

930

-

947

.

32.

Draptchinskaia

N

,

Gustavsson

P

,

Andersson

B

, et al.

The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia

.

Nat Genet

.

1999

;

21

(

2

):

169

-

175

.

33.

Moore

JB

,

Farrar

JE

,

Arceci

RJ

,

Liu

JM

,

Ellis

SR

.

Distinct ribosome maturation defects in yeast models of Diamond-Blackfan anemia and Shwachman-Diamond syndrome

.

Haematologica

.

2010

;

95

(

1

):

57

-

64

.

34.

Garçon

L

,

Ge

J

,

Manjunath

SH

, et al.

Ribosomal and hematopoietic defects in induced pluripotent stem cells derived from Diamond Blackfan anemia patients

.

Blood

.

2013

;

122

(

6

):

912

-

921

.

35.

Ludwig

LS

,

Gazda

HT

,

Eng

JC

, et al.

Altered translation of GATA1 in Diamond-Blackfan anemia

.

Nat Med

.

2014

;

20

(

7

):

748

-

753

.

36.

Recasens-Alvarez

C

,

Alexandre

C

,

Kirkpatrick

J

, et al.

Ribosomopathy-associated mutations cause proteotoxic stress that is alleviated by TOR inhibition

.

Nat Cell Biol

.

2021

;

23

(

2

):

127

-

135

.

37.

Crétien

A

,

Hurtaud

C

,

Moniz

H

, et al.

Study of the effects of proteasome inhibitors on ribosomal protein S19 (RPS19) mutants, identified in patients with Diamond-Blackfan anemia

.

Haematologica

.

2008

;

93

(

11

):

1627

-

1634

.

38.

Doulatov

S

,

Vo

LT

,

Macari

ER

, et al.

Drug discovery for Diamond-Blackfan anemia using reprogrammed hematopoietic progenitors

.

Sci Transl Med

.

2017

;

9

(

376

):

eaah5645

.

39.

Gastou

M

,

Rio

S

,

Dussiot

M

, et al.

The severe phenotype of Diamond-Blackfan anemia is modulated by heat shock protein 70

.

Blood Adv

.

2017

;

1

(

22

):

1959

-

1976

.

40.

Weis

F

,

Giudice

E

,

Churcher

M

, et al.

Mechanism of eIF6 release from the nascent 60S ribosomal subunit

.

Nat Struct Mol Biol

.

2015

;

22

(

11

):

914

-

919

.

41.

Burwick

N

,

Coats

SA

,

Nakamura

T

,

Shimamura

A

.

Impaired ribosomal subunit association in Shwachman-Diamond syndrome

.

Blood

.

2012

;

120

(

26

):

5143

-

5152

.

42.

Sezgin

G

,

Henson

AL

,

Nihrane

A

, et al.

Impaired growth, hematopoietic colony formation, and ribosome maturation in human cells depleted of Shwachman-Diamond syndrome protein SBDS

.

Pediatr Blood Cancer

.

2013

;

60

(

2

):

281

-

286

.

43.

Tan

S

,

Kermasson

L

,

Hoslin

A

, et al.

EFL1 mutations impair eIF6 release to cause Shwachman-Diamond syndrome

.

Blood

.

2019

;

134

(

3

):

277

-

290

.

44.

Calamita

P

,

Miluzio

A

,

Russo

A

, et al.

SBDS-deficient cells have an altered homeostatic equilibrium due to translational inefficiency which explains their reduced fitness and provides a logical framework for intervention

.

Plos Genet

.

2017

;

13

(

1

):

e1006552

.

45.

Lee

S

,

Shin

CH

,

Lee

J

, et al.

Somatic uniparental disomy mitigates the most damaging EFL1 allele combination in Shwachman-Diamond syndrome

.

Blood

.

2021

;

138

(

21

):

2117

-

2128

.

46.

Wong

CC

,

Traynor

D

,

Basse

N

,

Kay

RR

,

Warren

AJ

.

Defective ribosome assembly in Shwachman-Diamond syndrome

.

Blood

.

2011

;

118

(

16

):

4305

-

4312

.

47.

Jaako

P

,

Faille

A

,

Tan

S

, et al.

eIF6 rebinding dynamically couples ribosome maturation and translation

.

Nat Commun

.

2022

;

13

(

1

):

1562

.

48.

Dhanraj

S

,

Matveev

A

,

Li

H

, et al.

Biallelic mutations in DNAJC21 cause Shwachman-Diamond syndrome

.

Blood

.

2017

;

129

(

11

):

1557

-

1562

.

49.

Tummala

H

,

Walne

AJ

,

Williams

M

, et al.

DNAJC21 mutations link a cancer-prone bone marrow failure syndrome to corruption in 60S ribosome subunit maturation

.

Am J Hum Genet

.

2016

;

99

(

1

):

115

-

124

.

50.

In

K

,

Zaini

MA

,

Müller

C

,

Warren

AJ

,

von Lindern

M

,

Calkhoven

CF

.

Shwachman-Bodian-Diamond syndrome (SBDS) protein deficiency impairs translation re-initiation from C/EBPα and C/EBPβ mRNAs

.

Nucleic Acids Res

.

2016

;

44

(

9

):

4134

-

4146

.

51.

Rujkijyanont

P

,

Adams

SL

,

Beyene

J

,

Dror

Y

.

Bone marrow cells from patients with Shwachman-Diamond syndrome abnormally express genes involved in ribosome biogenesis and RNA processing

.

Br J Haematol

.

2009

;

145

(

6

):

806

-

815

.

52.

Ketharnathan

S

,

Pokharel

S

,

Prykhozhij

SV

, et al.

Loss of Dnajc21 leads to cytopenia and altered nucleotide metabolism in zebrafish

.

Leukemia

.

2024;

;

38

(

10

):

2115

-

2126

.

53.

Bezzerri

V

,

Lentini

L

,

Api

M

, et al.

Novel translational read-through–inducing drugs as a therapeutic option for Shwachman-Diamond syndrome

.

Biomedicines

.

2022

;

10

(

4

):

886

.

54.

Bezzerri

V

,

Bardelli

D

,

Morini

J

, et al.

Ataluren-driven restoration of Shwachman-Bodian-Diamond syndrome protein function in Shwachman-Diamond syndrome bone marrow cells

.

Am J Hematol

.

2018

;

93

(

4

):

527

-

536

.

55.

Cipolli

M

,

Boni

C

,

Penzo

M

, et al.

Ataluren improves myelopoiesis and neutrophil chemotaxis by restoring ribosome biogenesis and reducing p53 levels in Shwachman–Diamond syndrome cells

.

Br J Haematol

.

2024

;

204

(

1

):

292

-

305

.

56.

Bellanné-Chantelot

C

,

Schmaltz-Panneau

B

,

Marty

C

, et al.

Mutations in the SRP54 gene cause severe congenital neutropenia as well as Shwachman-Diamond – Like syndrome

.

Blood

.

2018

;

132

(

12

):

1318

-

1331

.

57.

Carapito

R

,

Konantz

M

,

Paillard

C

, et al.

Mutations in signal recognition particle SRP54 cause syndromic neutropenia with Shwachman-Diamond-like features

.

J Clin Invest

.

2017

;

127

(

11

):

4090

-

4103

.

58.

Necchi

V

,

Minelli

A

,

Sommi

P

, et al.

Ubiquitin-proteasome-rich cytoplasmic structures in neutrophils of patients with Shwachman-Diamond syndrome

.

Haematologica

.

2012

;

97

(

7

):

1057

-

1063

.

59.

Yoon

A

,

Peng

G

,

Brandenburg

Y

, et al.

Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita

.

Science

.

2006

;

312

(

5775

):

902

-

906

.

60.

Bellodi

C

,

Kopmar

N

,

Ruggero

D

.

Deregulation of oncogene-induced senescence and p53 translational control in X-linked dyskeratosis congenita

.

EMBO J

.

2010

;

29

(

11

):

1865

-

1876

.

61.

Knight

SW

,

Heiss

NS

,

Vulliamy

TJ

, et al.

X-linked dyskeratosis congenita is predominantly caused by missense mutations in the DKC1 gene

.

Am J Hum Genet

.

1999

;

65

(

1

):

50

-

58

.

62.

Dannenmann

B

,

Zahabi

A

,

Mir

P

, et al.

Human iPSC-based model of severe congenital neutropenia reveals elevated UPR and DNA damage in CD34+ cells preceding leukemic transformation [published correction appears in Exp Hematol. 2022;114:61]

.

Exp Hematol

.

2019

;

71

:

51

-

60

.

63.

Nanua

S

,

Murakami

M

,

Xia

J

, et al.

Activation of the unfolded protein response is associated with impaired granulopoiesis in transgenic mice expressing mutant Elane

.

Blood

.

2011

;

117

(

13

):

3539

-

3547

.

64.

Grenda

DS

,

Murakami

M

,

Ghatak

J

, et al.

Mutations of the ELA2 gene found in patients with severe congenital neutropenia induce the unfolded protein response and cellular apoptosis

.

Blood

.

2007

;

110

(

13

):

4179

-

4187

.

65.

Köllner

I

,

Sodeik

B

,

Schreek

S

, et al.

Mutations in neutrophil elastase causing congenital neutropenia lead to cytoplasmic protein accumulation and induction of the unfolded protein response

.

Blood

.

2006

;

108

(

2

):

493

-

500

.

66.

Benson

KF

,

Li

FQ

,

Person

RE

, et al.

Mutations associated with neutropenia in dogs and humans disrupt intracellular transport of neutrophil elastase

.

Nat Genet

.

2003

;

35

(

1

):

90

-

96

.

67.

Massullo

P

,

Druhan

LJ

,

Bunnell

BA

, et al.

Aberrant subcellular targeting of the G185R neutrophil elastase mutant associated with severe congenital neutropenia induces premature apoptosis of differentiating promyelocytes

.

Blood

.

2005

;

105

(

9

):

3397

-

3404

.

68.

Wiesmeier

M

,

Gautam

S

,

Kirschnek

S

,

Häcker

G

.

Characterisation of neutropenia-associated neutrophil elastase mutations in a murine differentiation model in vitro and in vivo

.

PLoS One

.

2016

;

11

(

12

):

e0168055

.

69.

Nustede

R

,

Klimiankou

M

,

Klimenkova

O

, et al.

ELANE mutant-specific activation of different UPR pathways in congenital neutropenia

.

Br J Haematol

.

2016

;

172

(

2

):

219

-

227

.

70.

Rao

S

,

Yao

Y

,

Soares de Brito

J

, et al.

Dissecting ELANE neutropenia pathogenicity by human HSC gene editing

.

Cell Stem Cell

.

2021

;

28

(

5

):

833

-

845.e5

.

71.

Van Nieuwenhove

E

,

Barber

JS

,

Neumann

J

, et al.

Defective Sec61α1 underlies a novel cause of autosomal dominant severe congenital neutropenia

.

J Allergy Clin Immunol

.

2020

;

146

(

5

):

1180

-

1193

.

72.

Doll

L

,

Welte

K

,

Skokowa

J

,

Bajoghli

B

.

A JAGN1-associated severe congenital neutropenia zebrafish model revealed an altered G-CSFR signaling and UPR activation

.

Blood Adv

.

2024

;

8

(

15

):

4050

-

4065

.

73.

Williams

SA

,

Longerich

S

,

Sung

P

,

Vaziri

C

,

Kupfer

GM

.

The E3 ubiquitin ligase RAD18 regulates ubiquitylation and chromatin loading of FANCD2 and FANCI

.

Blood

.

2011

;

117

(

19

):

5078

-

5087

.

74.

Parmar

K

,

Kim

J

,

Sykes

SM

, et al.

Hematopoietic stem cell defects in mice with deficiency of Fancd2 or Usp1

.

Stem Cells

.

2010

;

28

(

7

):

1186

-

1195

.

75.

Kovuru

N

,

Mochizuki-kashio

M

,

Menna

T

, et al.

Deregulated protein homeostasis constrains fetal hematopoietic stem cell pool expansion in Fanconi anemia

.

Nat Commun

.

2024

;

15

(

1

):

1852

.

76.

Gueiderikh

A

,

Maczkowiak-Chartois

F

,

Rouvet

G

, et al.

Fanconi anemia A protein participates in nucleolar homeostasis maintenance and ribosome biogenesis

.

Sci Adv

.

2021

;

7

(

1

):

eabb5414

.

77.

Oda

T

,

Hayano

T

,

Miyaso

H

,

Takahashi

N

,

Yamashita

T

.

Hsp90 regulates the Fanconi anemia DNA damage response pathway

.

Blood

.

2007

;

109

(

11

):

5016

-

5026

.

78.

Karras

GI

,

Yi

S

,

Sahni

N

, et al.

HSP90 shapes the consequences of human genetic variation

.

Cell

.

2017

;

168

(

5

):

856

-

866.e12

.

79.

Sondalle

SB

,

Longerich

S

,

Ogawa

LM

,

Sung

P

,

Baserga

SJ

.

Fanconi anemia protein FANCI functions in ribosome biogenesis

.

Proc Natl Acad Sci U S A

.

2019

;

116

(

7

):

2561

-

2570

.

80.

Zhang

F

,

Ji

Q

,

Chaturvedi

J

, et al.

Human SAMD9 is a poxvirus-activatable anticodon nuclease inhibiting codon-specific protein synthesis

.

Sci Adv

.

2023

;

9

(

23

):

eadh8502

.

81.

Thomas

ME

,

Abdelhamed

S

,

Hiltenbrand

R

, et al.

Pediatric MDS and bone marrow failure-associated germline mutations in SAMD9 and SAMD9L impair multiple pathways in primary hematopoietic cells

.

Leukemia

.

2021

;

35

(

11

):

3232

-

3244

.

82.

Sivan

G

,

Glushakow-Smith

SG

,

Katsafanas

GC

,

Americo

JL

,

Moss

B

.

Human host range restriction of the vaccinia virus C7/K1 double deletion mutant is mediated by an atypical mode of translation inhibition

.

J Virol

.

2018

;

92

(

23

):

e01329-18

.

83.

Allenspach

EJ

,

Soveg

F

,

Finn

LS

, et al.

Germline SAMD9L truncation variants trigger global translational repression

.

J Exp Med

.

2021

;

218

(

5

):

e20201195

.

84.

Necchi

V

,

Balduini

A

,

Noris

P

, et al.

Ubiquitin/proteasome-rich particulate cytoplasmic structures (PaCSs) in the platelets and megakaryocytes of ANKRD26-related thrombocytopenia

.

Thromb Haemost

.

2013

;

109

(

2

):

263

-

271

.

85.

Cai

X

,

Gao

L

,

Teng

L

, et al.

Runx1 deficiency decreases ribosome biogenesis and confers stress resistance to hematopoietic stem and progenitor cells

.

Cell Stem Cell

.

2015

;

17

(

2

):

165

-

177

.

86.

Wlodarski

MW

,

Vlachos

A

,

Farrar

JE

, et al.

Diagnosis, treatment, and surveillance of Diamond-Blackfan anaemia syndrome: international consensus statement

.

Lancet Haematol

.

2024

;

11

(

5

):

e368

-

e382

.

87.

Magee

JA

,

Signer

RAJ

.

Developmental stage-specific changes in protein synthesis differentially sensitize hematopoietic stem cells and erythroid progenitors to impaired ribosome biogenesis

.

Stem Cell Rep

.

2021

;

16

(

1

):

20

-

28

.

88.

Gazda

HT

,

Kho

AT

,

Sanoudou

D

, et al.

Defective ribosomal protein gene expression alters transcription, translation, apoptosis, and oncogenic pathways in Diamond-Blackfan anemia

.

Stem Cells

.

2006

;

24

(

9

):

2034

-

2044

.

89.

Khajuria

RK

,

Munschauer

M

,

Ulirsch

JC

, et al.

Ribosome levels selectively regulate translation and lineage commitment in human hematopoiesis

.

Cell

.

2018

;

173

(

1

):

90

-

103.e19

.

90.

Iskander

D

,

Wang

G

,

Heuston

EF

, et al.

Single-cell profiling of human bone marrow progenitors reveals mechanisms of failing erythropoiesis in Diamond-Blackfan anemia

.

Sci Transl Med

.

2021

;

13

(

610

):

eabf0113

.

91.

Dai

MS

,

Lu

H

.

Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5

.

J Biol Chem

.

2004

;

279

(

43

):

44475

-

44482

.

92.

Lohrum

MAE

,

Ludwig

RL

,

Kubbutat

MHG

,

Hanlon

M

,

Vousden

KH

.

Regulation of HDM2 activity by the ribosomal protein L11

.

Cancer Cell

.

2003

;

3

(

6

):

577

-

587

.

93.

Zhang

Y

,

Wolf

GW

,

Bhat

K

, et al.

Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway

.

Mol Cell Biol

.

2003

;

23

(

23

):

8902

-

8912

.

94.

Bhat

KP

,

Itahana

K

,

Jin

A

,

Zhang

Y

.

Essential role of ribosomal protein L11 in mediating growth inhibition-induced p53 activation

.

EMBO J

.

2004

;

23

(

12

):

2402

-

2412

.

95.

Jin

A

,

Itahana

K

,

O’Keefe

K

,

Zhang

Y

.

Inhibition of HDM2 and activation of p53 by ribosomal protein L23

.

Mol Cell Biol

.

2004

;

24

(

17

):

7669

-

7680

.

96.

Dai

M-S

,

Zeng

SX

,

Jin

Y

,

Sun

XX

,

David

L

,

Lu

H

.

Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition

.

Mol Cell Biol

.

2004

;

24

(

17

):

7654

-

7668

.

97.

Chen

D

,

Zhang

Z

,

Li

M

, et al.

Ribosomal protein S7 as a novel modulator of p53-MDM2 interaction: binding to MDM2, stabilization of p53 protein, and activation of p53 function

.

Oncogene

.

2007

;

26

(

35

):

5029

-

5037

.

98.

Yadavilli

S

,

Mayo

LD

,

Higgins

M

,

Lain

S

,

Hegde

V

,

Deutsch

WA

.

Ribosomal protein S3: a multi-functional protein that interacts with both p53 and MDM2 through its KH domain

.

DNA Repair (Amst)

.

2009

;

8

(

10

):

1215

-

1224

.

99.

Ofir-Rosenfeld

Y

,

Boggs

K

,

Michael

D

,

Kastan

MB

,

Oren

M

.

Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26

.

Mol Cell

.

2008

;

32

(

2

):

180

-

189

.

100.

Gazda

HT

,

Preti

M

,

Sheen

MR

, et al.

Frameshift mutation in p53 regulator RPL26 is associated with multiple physical abnormalities and a specific pre-ribosomal RNA processing defect in Diamond-Blackfan anemia

.

Hum Mutat

.

2012

;

33

(

7

):

1037

-

1044

.

101.

Dutt

S

,

Narla

A

,

Lin

K

, et al.

Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells

.

Blood

.

2011

;

117

(

9

):

2567

-

2576

.

102.

Bhoopalan

SV

,

Yen

JS

,

Mayuranathan

T

, et al.

An RPS19-edited model for Diamond-Blackfan anemia reveals TP53-dependent impairment of hematopoietic stem cell activity

.

JCI Insight

.

2023

;

8

(

1

):

e161810

.

103.

O’Donohue

MF

,

Da Costa

L

,

Lezzerini

M

, et al.

HEATR3 variants impair nuclear import of uL18 (RPL5) and drive Diamond-Blackfan anemia

.

Blood

.

2022

;

139

(

21

):

3111

-

3126

.

104.

Jia

Q

,

Zhang

Q

,

Zhang

Z

, et al.

Transcriptome analysis of the zebrafish model of Diamond-Blackfan anemia from RPS19 deficiency via p53-dependent and -independent pathways

.

PLoS One

.

2013

;

8

(

8

):

e71782

.

105.

Giménez

Y

,

Palacios

M

,

Sánchez-Domínguez

R

, et al.

Lentivirus-mediated gene therapy corrects ribosomal biogenesis and shows promise for Diamond Blackfan anemia

.

JCI Insight

.

2024

;

9

(

10

):

e171650

.

106.

Payne

EM

,

Virgilio

M

,

Narla

A

, et al.

L-leucine improves the anemia and developmental defects associated with Diamond-Blackfan anemia and del(5q) MDS by activating the mTOR pathway

.

Blood

.

2012

;

120

(

11

):

2214

-

2224

.

107.

Kimball

SR

,

Shantz

LM

,

Horetsky

RL

,

Jefferson

LS

.

Leucine regulates translation of specific mRNAs in L6 myoblasts through mTOR-mediated changes in availability of eIF4E and phosphorylation of ribosomal protein S6

.

J Biol Chem

.

1999

;

274

(

17

):

11647

-

11652

.

108.

Narla

A

,

Payne

EM

,

Abayasekara

N

, et al.

L-Leucine improves the anaemia in models of Diamond Blackfan anaemia and the 5q- syndrome in a TP53-independent way

.

Br J Haematol

.

2014

;

167

(

4

):

524

-

528

.

109.

Jaako

P

,

Debnath

S

,

Olsson

K

,

Bryder

D

,

Flygare

J

,

Karlsson

S

.

Dietary L-leucine improves the anemia in a mouse model for Diamond-Blackfan anemia

.

Blood

.

2012

;

120

(

11

):

2225

-

2228

.

110.

Vlachos

A

,

Atsidaftos

E

,

Lababidi

ML

, et al.

L-leucine improves anemia and growth in patients with transfusion-dependent Diamond-Blackfan anemia: results from a multicenter pilot phase I/II study from the Diamond-Blackfan Anemia Registry

.

Pediatr Blood Cancer

.

2020

;

67

(

12

):

e28748

.

111.

Dror

Y

,

Freedman

MH

.

Shwachman-Diamond syndrome

.

Br J Haematol

.

2002

;

118

(

3

):

701

-

713

.

112.

Boocock

GRB

,

Morrison

JA

,

Popovic

M

, et al.

Mutations in SBDS are associated with Shwachman-Diamond syndrome

.

Nat Genet

.

2003

;

33

(

1

):

97

-

101

.

113.

Woloszynek

JR

,

Rothbaum

RJ

,

Rawls

AS

, et al.

Mutations of the SBDS gene are present in most patients with Shwachman-Diamond syndrome

.

Blood

.

2004

;

104

(

12

):

3588

-

3590

.

114.

Menne

TF

,

Goyenechea

B

,

Sánchez-Puig

N

, et al.

The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast

.

Nat Genet

.

2007

;

39

(

4

):

486

-

495

.

115.

Finch

AJ

,

Hilcenko

C

,

Basse

N

, et al.

Uncoupling of GTP hydrolysis from eIF6 release on the ribosome causes Shwachman-Diamond syndrome

.

Genes Dev

.

2011

;

25

(

9

):

917

-

929

.

116.

Stepensky

P

,

Chacón-Flores

M

,

Kim

KH

, et al.

Mutations in EFL1, an SBDS partner, are associated with infantile pancytopenia, exocrine pancreatic insufficiency and skeletal anomalies in a Shwachman-Diamond like syndrome

.

J Med Genet

.

2017

;

54

(

8

):

558

-

566

.

117.

Senger

B

,

Lafontaine

DLJ

,

Graindorge

JS

, et al.

The nucle(ol)ar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis

.

Mol Cell

.

2001

;

8

(

6

):

1363

-

1373

.

118.

Schürch

C

,

Schaefer

T

,

Müller

JS

, et al.

SRP54 mutations induce congenital neutropenia via dominant-negative effects on XBP1 splicing

.

Blood

.

2021

;

137

(

10

):

1340

-

1352

.

119.

Robertson

N

,

Shchepachev

V

,

Wright

D

, et al.

A disease-linked lncRNA mutation in RNase MRP inhibits ribosome synthesis

.

Nat Commun

.

2022

;

13

(

1

):

649

.

120.

Williams

MS

,

Ettinger

RS

,

Hermanns

P

, et al.

The natural history of severe anemia in cartilage-hair hypoplasia

.

Am J Med Genet A

.

2005

;

138

(

1

):

35

-

40

.

121.

Mäkitie

O

,

Rajantie

J

,

Kaitila

I

.

Anaemia and macrocytosis—unrecognized features in cartilage-hair hypoplasia

.

Acta Paediatr

.

1992

;

81

(

12

):

1026

-

1029

.

122.

Skokowa

J

,

Dale

DC

,

Touw

IP

,

Zeidler

C

,

Welte

K

.

Severe congenital neutropenias

.

Nat Rev Dis Primers

.

2017

;

3

:

17032

.

123.

Sigurdsson

V

,

Takei

H

,

Soboleva

S

, et al.

Bile acids protect expanding hematopoietic stem cells from unfolded protein stress in fetal liver

.

Cell Stem Cell

.

2016

;

18

(

4

):

522

-

532

.

124.

Chen

MZ

,

Moily

NS

,

Bridgford

JL

, et al.

A thiol probe for measuring unfolded protein load and proteostasis in cells

.

Nat Commun

.

2017

;

8

(

1

):

474

.

125.

Mehta

PA

,

Ebens

C

. Fanconi Anemia. [updated 2021 Jun 3]. In:

Adam

MP

,

Feldman

J

,

Mirzaa

GM

,

Pagon

RA

,

Wallace

SE

,

Amemiya

A

, eds.

GeneReviews [Internet]

.

Seattle (WA)

:

University of Washington, Seattle

;

2002 Feb 14

:

1993

-

2025

.

126.

Domenech

C

,

Maillard

L

,

Rousseau

A

, et al.

Studies in an early development window unveils a severe HSC defect in both murine and human Fanconi anemia

.

Stem Cell Rep

.

2018

;

11

(

5

):

1075

-

1091

.

127.

Kamimae-Lanning

AN

,

Goloviznina

NA

,

Kurre

P

.

Fetal origins of hematopoietic failure in a murine model of Fanconi anemia

.

Blood

.

2013

;

121

(

11

):

2008

-

2012

.

128.

Haneline

BLS

,

Gobbett

TA

,

Carreau

M

, et al.

Loss of FancC function results in decreased hematopoietic

.

Stem Cell Repopulating Ability

.

1999

;

94

(

1

):

1

-

8

.

129.

Carreau

M

,

Gan

OI

,

Liu

L

,

Doedens

M

,

Dick

JE

,

Buchwald

M

.

Hematopoietic compartment of Fanconi anemia group C null mice contains fewer lineage-negative CD34+ primitive hematopoietic cells and shows reduced reconstitution ability

.

Exp Hematol

.

1999

;

27

(

11

):

1667

-

1674

.

130.

Zhang

QS

,

Marquez-Loza

L

,

Eaton

L

, et al.

Fancd2-/- mice have hematopoietic defects that can be partially corrected by resveratrol

.

Blood

.

2010

;

116

(

24

):

5140

-

5148

.

131.

Suzuki

S

,

Racine

RR

,

Manalo

NA

,

Cantor

SB

,

Raffel

GD

.

Impairment of fetal hematopoietic stem cell function in the absence of Fancd2

.

Exp Hematol

.

2017

;

48

:

79

-

86

.

132.

Vasanthakumar

A

,

Arnovitz

S

,

Marquez

R

, et al.

Brca1 deficiency causes bone marrow failure and spontaneous hematologic malignancies in mice

.

Blood

.

2015

;

126

(

23

):

295

. 295.

133.

Mgbemena

VE

,

Signer

RAJ

,

Wijayatunge

R

,

Laxson

T

,

Morrison

SJ

,

Ross

TS

.

Distinct Brca1 mutations differentially reduce hematopoietic stem cell function

.

Cell Rep

.

2017

;

18

(

4

):

947

-

960

.

134.

Ceccaldi

R

,

Parmar

K

,

Mouly

E

, et al.

Bone marrow failure in fanconi anemia is triggered by an exacerbated p53/p21 DNA damage response that impairs hematopoietic stem and progenitor cells

.

Cell Stem Cell

.

2012

;

11

(

1

):

36

-

49

.

135.

Zhang

H

,

Kozono

DE

,

O’Connor

KW

, et al.

TGF-β inhibition rescues hematopoietic stem cell defects and bone marrow failure in Fanconi anemia

.

Cell Stem Cell

.

2016

;

18

(

5

):

668

-

681

.

136.

Rodríguez

A

,

Zhang

K

,

Färkkilä

A

, et al.

MYC promotes bone marrow stem cell dysfunction in Fanconi anemia

.

Cell Stem Cell

.

2021

;

28

(

1

):

33

-

47.e8

.

137.

Laurenti

E

,

Varnum-Finney

B

,

Wilson

A

, et al.

Hematopoietic stem cell function and survival depend on c-Myc and N-Myc activity

.

Cell Stem Cell

.

2008

;

3

(

6

):

611

-

624

.

138.

Cunningham

L

,

Merguerian

M

,

Calvo

KR

, et al.

Natural history study of patients with familial platelet disorder with associated myeloid malignancy

.

Blood

.

2023

;

142

(

25

):

2146

-

2158

.

139.

Narla

A

,

Vlachos

A

,

Nathan

DG

.

Diamond Blackfan anemia treatment: past, present, and future

.

Semin Hematol

.

2011

;

48

(

2

):

117

-

123

.

140.

Gutierrez-Rodrigues

F

,

Sahoo

SS

,

Wlodarski

MW

,

Young

NS

.

Somatic mosaicism in inherited bone marrow failure syndromes

.

Best Pract Res Clin Haematol

.

2021

;

34

(

2

):

101279

.

141.

Alter

BP

,

Giri

N

,

Savage

SA

,

Rosenberg

PS

.

Cancer in the national cancer institute inherited bone marrow failure syndrome cohort after fifteen years of follow-up

.

Haematologica

.

2018

;

103

(

1

):

30

-

39

.

142.

Alter

BP

,

Giri

N

,

Savage

SA

, et al.

Malignancies and survival patterns in the National Cancer Institute inherited bone marrow failure syndromes cohort study

.

Br J Haematol

.

2010

;

150

(

2

):

179

-

188

.

143.

Savage

SA

,

Dufour

C

.

Classical inherited bone marrow failure syndromes with high risk for myelodysplastic syndrome and acute myelogenous leukemia

.

Semin Hematol

.

2017

;

54

(

2

):

105

-

114

.

144.

Attardi

E

,

Corey

SJ

,

Wlodarski

MW

.

Clonal hematopoiesis in children with predisposing conditions

.

Semin Hematol

.

2024

;

61

(

1

):

35

-

42

.

145.

Pasca

S

,

Gondek

LP

.

Clonal hematopoiesis and bone marrow failure syndromes

.

Best Pract Res Clin Haematol

.

2021

;

34

(

2

):

101273

.

146.

Farrar

JE

,

Vlachos

A

,

Atsidaftos

E

, et al.

Ribosomal protein gene deletions in Diamond-Blackfan anemia

.

Blood

.

2011

;

118

(

26

):

6943

-

6951

.

147.

Garelli

E

,

Quarello

P

,

Giorgio

E

, et al.

Spontaneous remission in a Diamond-Blackfan anaemia patient due to a revertant uniparental disomy ablating a de novo RPS19 mutation

.

Br J Haematol

.

2019

;

185

(

5

):

994

-

998

.

148.

Venugopal

P

,

Moore

S

,

Lawrence

DM

, et al.

Self-reverting mutations partially correct the blood phenotype in a Diamond Blackfan anemia patient

.

Haematologica

.

2017

;

102

(

12

):

e506

-

e509

.

149.

Arbiv

OA

,

Cuvelier

G

,

Klaassen

RJ

, et al.

Molecular analysis and genotype-phenotype correlation of Diamond-Blackfan anemia

.

Clin Genet

.

2018

;

93

(

2

):

320

-

328

.

150.

Cole

S

,

Giri

N

,

Alter

BP

,

Gianferante

DM

.

Variable clinical features in a large family with Diamond Blackfan anemia caused by a pathogenic missense mutation in RPS19

.

Front Genet

.

2022

;

13

:

914141

.

151.

Gianferante

DM

,

Wlodarski

MW

,

Atsidaftos

E

, et al.

Genotype-phenotype association and variant characterization in Diamond Blackfan anemia caused by pathogenic variants in RPL35A

.

Haematologica

.

2021

;

106

(

5

):

1303

-

1310

.

152.

Tan

S

,

Kermasson

L

,

Hilcenko

C

, et al.

Somatic genetic rescue of a germline ribosome assembly defect [published correction appears in Nat Commun. 2022;13(1):3574]

.

Nat Commun

.

2021

;

12

(

1

):

5044

.

153.

Kennedy

AL

,

Myers

KC

,

Bowman

J

, et al.

Distinct genetic pathways define pre-malignant versus compensatory clonal hematopoiesis in Shwachman-Diamond syndrome

.

Nat Commun

.

2021

;

12

(

1

):

1334

.

154.

Machado

HE

,

Øbro

NF

,

Williams

N

, et al.

Convergent somatic evolution commences in utero in a germline ribosomopathy

.

Nat Commun

.

2023

;

14

(

1

):

5092

.

155.

Quentin

S

,

Cuccuini

W

,

Ceccaldi

R

, et al.

Myelodysplasia and leukemia of fanconi anemia are associated with a specific pattern of genomic abnormalities that includes cryptic RUNX1/AML1 lesions

.

Blood

.

2011

;

117

(

15

):

e161

-

e170

.

156.

Skokowa

J

,

Steinemann

D

,

Katsman-Kuipers

JE

, et al.

Cooperativity of RUNX1 and CSF3R mutations in severe congenital neutropenia: a unique pathway in myeloid leukemogenesis

.

Blood

.

2014

;

123

(

14

):

2229

-

2237

.

157.

Sin

CF

,

Man

PHM

.

The role of proteasome inhibitors in treating acute lymphoblastic leukaemia

.

Front Oncol

.

2021

;

11

:

802832

.

158.

Khateb

A

,

Ronai

ZA

.

Unfolded protein response in leukemia: from basic understanding to therapeutic opportunities

.

Trends Cancer

.

2020

;

6

(

11

):

960

-

973

.

159.

Martelli

AM

,

Paganelli

F

,

Chiarini

F

,

Evangelisti

C

,

McCubrey

JA

.

The unfolded protein response: a novel therapeutic target in acute leukemias

.

Cancers (Basel)

.

2020

;

12

(

2

):

333

.

https://doi.org/10.1101/2024.09.24.614781

160.

Lam

K

,

Kim

YJ

,

Ong

CM

, et al.

The proteostasis network is a therapeutic target in acute myeloid leukemia

.

bioRxiv

.

Preprint posted online 26 September 2024

.

161.

Leclerc

GM

,

Zheng

S

,

Leclerc

GJ

,

DeSalvo

J

,

Swords

RT

,

Barredo

JC

.

The NEDD8-activating enzyme inhibitor pevonedistat activates the eIF2α and mTOR pathways inducing UPR-mediated cell death in acute lymphoblastic leukemia

.

Leuk Res

.

2016

;

50

:

1

-

10

.

162.

Lawson

H

,

Holt-Martyn

JP

,

Dembitz

V

, et al.

The selective prolyl hydroxylase inhibitor IOX5 stabilizes HIF-1α and compromises development and progression of acute myeloid leukemia

.

Nat Cancer

.

2024

;

5

(

6

):

916

-

937

.

163.

Sjövall

D

,

Ghosh

S

,

Fernandez-Fuentes

N

, et al.

Defective ribosome assembly impairs leukemia progression in a murine model of acute myeloid leukemia

.

Cell Rep

.

2024

;

43

(

11

):

114864

.

164.

Liu

B

,

Zhang

X

,

Zhou

Y

, et al.

USP4 regulates ribosome biogenesis and protein synthesis for hematopoietic stem cell regeneration and leukemia progression

.

Leukemia

.

2024

;

38

(

11

):

2466

-

2478

.

165.

Gausdal

G

,

Gjertsen

BT

,

McCormack

E

, et al.

Abolition of stress-induced protein synthesis sensitizes leukemia cells to anthracycline-induced death

.

Blood

.

2008

;

111

(

5

):

2866

-

2877

.

166.

Mill

CP

,

Fiskus

W

,

DiNardo

CD

, et al.

Effective therapy for AML with RUNX1 mutation by cotreatment with inhibitors of protein translation and BCL2

.

Blood

.

2022

;

139

(

6

):

907

-

921

.

167.

Tang

R

,

Faussat

AM

,

Majdak

P

, et al.

Semisynthetic homoharringtonine induces apoptosis via inhibition of protein synthesis and triggers rapid myeloid cell leukemia-1 down-regulation in myeloid leukemia cells

.

Mol Cancer Ther

.

2006

;

5

(

3

):

723

-

731

.

168.

Tamburini

J

,

Green

AS

,

Bardet

V

, et al.

Protein synthesis is resistant to rapamycin and constitutes a promising therapeutic target in acute myeloid leukemia

.

Blood

.

2009

;

114

(

8

):

1618

-

1627

.

169.

Cowan

AJ

,

Green

DJ

,

Kwok

M

, et al.

Diagnosis and management of multiple myeloma: a review

.

JAMA

.

2022

;

327

(

5

):

464

-

477

.

170.

Barna

M

,

Pusic

A

,

Zollo

O

, et al.

Suppression of Myc oncogenic activity by ribosomal protein haploinsufficiency

.

Nature

.

2008

;

456

(

7224

):

971

-

975

.

171.

Barton

BM

,

Son

F

,

Verma

A

, et al.

IRE1α – XBP1 safeguards hematopoietic stem and progenitor cells by restricting pro-leukemogenic gene programs

.

Nat Immunol

.

2025

;

26

(

2

):

200

-

214

.

172.

Dong

Q

,

Xiu

Y

,

Wang

Y

, et al.

HSF1 is a driver of leukemia stem cell self-renewal in acute myeloid leukemia

.

Nat Commun

.

2022

;

13

(

1

):

6107

.

173.

Dai

C

.

The heat-shock, or HSF1-mediated proteotoxic stress, response in cancer: from proteomic stability to oncogenesis

.

Phil Trans R Soc B

.

2018

;

373

(

1738

):

20160525

.

174.

Santagata

S

,

Mendillo

ML

,

Tang

YC

, et al.

Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state

.

Science

.

2013

;

341

(

6143

):

1238303

.

175.

Nishida

Y

,

Zhao

R

,

Heese

LE

, et al.

Inhibition of translation initiation factor eIF4a inactivates heat shock factor 1 (HSF1) and exerts anti-leukemia activity in AML

.

Leukemia

.

2021

;

35

(

9

):

2469

-

2481

.

176.

Eroglu

B

,

Pang

J

,

Jin

X

,

Xi

C

,

Moskophidis

D

,

Mivechi

NF

.

HSF1-mediated control of cellular energy metabolism and mTORC1 activation drive acute T-cell lymphoblastic leukemia progression

.

Mol Cancer Res

.

2020

;

18

(

3

):

463

-

476

.

177.

Grey

W

,

Rio-Machin

A

,

Casado

P

, et al.

CKS1 inhibition depletes leukemic stem cells and protects healthy hematopoietic stem cells in acute myeloid leukemia

.

Sci Transl Med

.

2022

;

14

(

650

):

eabn3248

.

178.

Hidalgo San Jose

L

,

Signer

RAJ

.

Cell-type-specific quantification of protein synthesis in vivo

.

Nat Protoc

.

2019

;

14

(

2

):

441

-

460

.

179.

Liu

J

,

Xu

Y

,

Stoleru

D

,

Salic

A

.

Imaging protein synthesis in cells and tissues with an alkyne analog of puromycin

.

Proc Natl Acad Sci U S A

.

2012

;

109

(

2

):

413

-

418

.

180.

Taylor

AM

,

Macari

ER

,

Chan

IT

, et al.

Calmodulin inhibitors improve erythropoiesis in Diamond-Blackfan anemia

.

Sci Transl Med

.

2020

;

12

(

566

):

eabb5831

.

181.

Park

SG

,

Schimmel

P

,

Kim

S

.

Aminoacyl tRNA synthetases and their connections to disease

.

Proc Natl Acad Sci U S A

.

2008

;

105

(

32

):

11043

-

11049

.

182.

Wilson

A

,

Murphy

MJ

,

Oskarsson

T

, et al.

c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation

.

Genes Dev

.

2004

;

18

(

22

):

2747

-

2763

.