Platelet generation in vivo and in vitro

2.

Gaetano

GD

,

Cerletti

C

.

Platelet adhesion and aggregation and fibrin formation in flowing blood: a historical contribution by Giulio Bizzozero

.

Platelets

.

2002

;

13

(

2

):

85

-

89

.

3.

Gremmel

T

,

Frelinger

AL

,

Michelson

AD

.

Platelet physiology

.

Semin Thromb Hemost

.

2016

;

42

(

3

):

191

-

204

.

4.

Deppermann

C

,

Kubes

P

.

Start a fire, kill the bug: the role of platelets in inflammation and infection

.

Innate Immun

.

2018

;

24

(

6

):

335

-

348

.

5.

Kaushansky

K

.

Thrombopoietin

.

N Engl J Med

.

1998

;

339

(

11

):

746

-

754

.

6.

Noetzli

LJ

,

French

SL

,

Machlus

KR

.

New insights into the differentiation of megakaryocytes from hematopoietic progenitors

.

Arterioscler Thromb Vasc Biol

.

2019

;

39

(

7

):

1288

-

1300

.

7.

Noh

J-Y

.

Megakaryopoiesis and platelet biology: roles of transcription factors and emerging clinical implications

.

Int J Mol Sci

.

2021

;

22

(

17

):

9615

.

8.

Deutsch

VR

,

Tomer

A

.

Megakaryocyte development and platelet production

.

Br J Haematol

.

2006

;

134

(

5

):

453

-

466

.

9.

Wang

H

,

He

J

,

Xu

C

, et al.

Decoding human megakaryocyte development

.

Cell Stem Cell

.

2021

;

28

(

3

):

535

-

549.e8

.

10.

Mazzi

S

,

Lordier

L

,

Debili

N

,

Raslova

H

,

Vainchenker

W

.

Megakaryocyte and polyploidization

.

Exp Hematol

.

2018

;

57

:

1

-

13

.

11.

Cunin

P

,

Nigrovic

PA

.

Megakaryocytes as immune cells

.

J Leukoc Biol

.

2019

;

105

(

6

):

1111

-

1121

.

12.

Puhm

F

,

Laroche

A

,

Boilard

E

.

Diversity of megakaryocytes

.

Arterioscler Thromb Vasc Biol

.

2023

;

43

(

11

):

2088

-

2098

.

13.

Tilburg

J

,

Stone

AP

,

Billingsley

JM

, et al.

Spatial transcriptomics of murine bone marrow megakaryocytes at single-cell resolution

.

Res Pract Thromb Haemost

.

2023

;

7

(

4

):

100158

.

14.

Tilburg

J

,

Becker

IC

,

Italiano

JE

.

Don’t you forget about me(gakaryocytes)

.

Blood

.

2022

;

139

(

22

):

3245

-

3254

.

15.

Pariser

DN

,

Hilt

ZT

,

Ture

SK

, et al.

Lung megakaryocytes are immune modulatory cells

.

J Clin Invest

.

2021

;

131

(

1

):

e137377

.

16.

Liu

H

,

Liu

J

,

Wang

L

,

Zhu

F

.

In vitro generation of megakaryocytes and platelets

.

Front Cell Dev Biol

.

2021

;

9

:

713434

.

17.

Chen

SJ

,

Hashimoto

K

,

Fujio

K

, et al.

A let-7 microRNA-RALB axis links the immune properties of iPSC-derived megakaryocytes with platelet producibility

.

Nat Commun

.

2024

;

15

(

1

):

2588

.

https://doi.org/10.21203/rs.3.rs-3576483/v1

18.

Conrad

C

,

Magnen

M

,

Tsui

J

, et al.

Decoding functional hematopoietic progenitor cells in the adult human lung

.

Res Sq

.

Preprint posted online 28 November 2023

.

19.

Mookerjee

S

,

Foster

HR

,

Waller

AK

,

Ghevaert

CJ

.

In vitro-derived platelets: the challenges we will have to face to assess quality and safety

.

Platelets

.

2020

;

31

(

6

):

724

-

730

.

20.

Aubron

C

,

Flint

AWJ

,

Ozier

Y

,

McQuilten

Z

.

Platelet storage duration and its clinical and transfusion outcomes: a systematic review

.

Crit Care

.

2018

;

22

(

1

):

185

.

21.

Yarovoi

HV

,

Kufrin

D

,

Eslin

DE

, et al.

Factor VIII ectopically expressed in platelets: efficacy in hemophilia A treatment

.

Blood

.

2003

;

102

(

12

):

4006

-

4013

.

22.

Poncz

M

,

Zaitsev

S

,

Ahn

H

, et al.

Packaging of supplemented urokinase into alpha-granules of in vitro-grown megakaryocytes for targeted nascent clot lysis

.

Blood Adv

.

2024

;

8

(

14

):

3798

-

3809

.

23.

Lu

Q

,

Ye

H

,

Wang

K

, et al.

Bioengineered platelets combining chemotherapy and immunotherapy for postsurgical melanoma treatment: internal core-loaded doxorubicin and external surface-anchored anti-PD-L1 antibody backpacks

.

Nano Lett

.

2022

;

22

(

7

):

3141

-

3150

.

24.

Salgado

R

,

Benoy

I

,

Bogers

J

, et al.

Platelets and vascular endothelial growth factor (VEGF): a morphological and functional study

.

Angiogenesis

.

2001

;

4

(

1

):

37

-

43

.

25.

Italiano

JE

,

Patel-Hett

S

,

Hartwig

JH

.

Mechanics of proplatelet elaboration

.

J Thromb Haemost

.

2007

;

5

(

suppl 1

):

18

-

23

.

26.

Brown

E

,

Carlin

LM

,

Nerlov

C

,

Lo Celso

C

,

Poole

AW

.

Multiple membrane extrusion sites drive megakaryocyte migration into bone marrow blood vessels

.

Life Sci Alliance

.

2018

;

1

(

2

):

e201800061

.

27.

Kosaki

G

.

In vivo platelet production from mature megakaryocytes: does platelet release occur via proplatelets?

.

Int J Hematol

.

2005

;

81

(

3

):

208

-

219

.

28.

Machlus

KR

,

Italiano

JE

.

The incredible journey: from megakaryocyte development to platelet formation

.

J Cell Biol

.

2013

;

201

(

6

):

785

-

796

.

29.

Lefrançais

E

,

Looney

MR

.

Platelet biogenesis in the lung circulation

.

Physiology

.

2019

;

34

(

6

):

392

-

401

.

30.

Potts

KS

,

Farley

A

,

Dawson

CA

, et al.

Membrane budding is a major mechanism of in vivo platelet biogenesis

.

J Exp Med

.

2020

;

217

(

9

):

e20191206

.

31.

Kosaki

G

.

Platelet production by megakaryocytes: protoplatelet theory justifies cytoplasmic fragmentation model

.

Int J Hematol

.

2008

;

88

(

3

):

255

-

267

.

32.

Patel

SR

,

Hartwig

JH

,

Italiano

JE

.

The biogenesis of platelets from megakaryocyte proplatelets

.

J Clin Invest

.

2005

;

115

(

12

):

3348

-

3354

.

33.

Thon

JN

,

Montalvo

A

,

Patel-Hett

S

, et al.

Cytoskeletal mechanics of proplatelet maturation and platelet release

.

J Cell Biol

.

2010

;

191

(

4

):

861

-

874

.

34.

Geddis

AE

.

The regulation of proplatelet production

.

Haematologica

.

2009

;

94

(

6

):

756

-

759

.

35.

Bluteau

D

,

Lordier

L

,

Di Stefano

A

, et al.

Regulation of megakaryocyte maturation and platelet formation

.

J Thromb Haemost

.

2009

;

7

(

suppl 1

):

227

-

234

.

36.

Liu

H

,

Welburn

JPI

.

A circle of life: platelet and megakaryocyte cytoskeleton dynamics in health and disease

.

Open Biol

.

2024

;

14

(

6

):

240041

.

37.

Wright

JH

.

The origin and nature of the blood plates

.

Boston Med Surg J

.

1906

;

154

(

23

):

643

-

645

.

38.

Radley

J

,

Scurfield

G

.

The mechanism of platelet release

.

Blood

.

1980

;

56

(

6

):

996

-

999

.

39.

Italiano

JE

,

Lecine

P

,

Shivdasani

RA

,

Hartwig

JH

.

Blood platelets are assembled principally at the ends of proplatelet processes produced by differentiated megakaryocytes

.

J Cell Biol

.

1999

;

147

(

6

):

1299

-

1312

.

40.

Junt

T

,

Schulze

H

,

Chen

Z

, et al.

Dynamic visualization of thrombopoiesis within bone marrow

.

Science

.

2007

;

317

(

5845

):

1767

-

1770

.

41.

Kemble

S

,

Dalby

A

,

Lowe

GC

, et al.

Analysis of preplatelets and their barbell platelet derivatives by imaging flow cytometry

.

Blood Adv

.

2022

;

6

(

9

):

2932

-

2946

.

42.

Schwertz

H

,

Köster

S

,

Kahr

WHA

, et al.

Anucleate platelets generate progeny

.

Blood

.

2010

;

115

(

18

):

3801

-

3809

.

43.

Becker

RP

,

De Bruyn

PPH

.

The transmural passage of blood cells into myeloid sinusoids and the entry of platelets into the sinusoidal circulation; a scanning electron microscopic investigation

.

Am J Anat

.

1976

;

145

(

2

):

183

-

205

.

44.

Choi

ES

,

Nichol

JL

,

Hokom

MM

,

Hornkohl

AC

,

Hunt

P

.

Platelets generated in vitro from proplatelet-displaying human megakaryocytes are functional

.

Blood

.

1995

;

85

(

2

):

402

-

413

.

45.

Wang

Y

,

Hayes

V

,

Jarocha

D

, et al.

Comparative analysis of human ex vivo–generated platelets vs megakaryocyte-generated platelets in mice: a cautionary tale

.

Blood

.

2015

;

125

(

23

):

3627

-

3636

.

46.

Zhang

L

,

Orban

M

,

Lorenz

M

, et al.

A novel role of sphingosine 1-phosphate receptor S1pr1 in mouse thrombopoiesis

.

J Exp Med

.

2012

;

209

(

12

):

2165

-

2181

.

47.

Bornert

A

,

Pertuy

F

,

Lanza

F

,

Gachet

C

,

Léon

C

.

In vivo two-photon imaging of megakaryocytes and proplatelets in the mouse skull bone marrow

.

JoVE

.

2021

(

173

):

e62515

.

48.

Lefrançais

E

,

Ortiz-Muñoz

G

,

Caudrillier

A

, et al.

The lung is a site of platelet biogenesis and a reservoir for haematopoietic progenitors

.

Nature

.

2017

;

544

(

7648

):

105

-

109

.

49.

Jiang

J

,

Woulfe

DS

,

Papoutsakis

ET

.

Shear enhances thrombopoiesis and formation of microparticles that induce megakaryocytic differentiation of stem cells

.

Blood

.

2014

;

124

(

13

):

2094

-

2103

.

50.

Zhao

X

,

Alibhai

D

,

Walsh

TG

, et al.

Highly efficient platelet generation in lung vasculature reproduced by microfluidics

.

Nat Commun

.

2023

;

14

(

1

):

4026

.

51.

Ouzegdouh

Y

,

Capron

C

,

Bauer

T

, et al.

The physical and cellular conditions of the human pulmonary circulation enable thrombopoiesis

.

Exp Hematol

.

2018

;

63

:

22

-

27.e3

.

52.

Zucker-Franklin

D

,

Philipp

CS

.

Platelet production in the pulmonary capillary bed: new ultrastructural evidence for an old concept

.

Am J Pathol

.

2000

;

157

(

1

):

69

-

74

.

53.

Zucker-Franklin

D

,

Petursson

S

.

Thrombocytopoiesis--analysis by membrane tracer and freeze-fracture studies on fresh human and cultured mouse megakaryocytes

.

J Cell Biol

.

1984

;

99

(

2

):

390

-

402

.

54.

Nishimura

S

,

Nagasaki

M

,

Kunishima

S

, et al.

IL-1α induces thrombopoiesis through megakaryocyte rupture in response to acute platelet needs

.

J Cell Biol

.

2015

;

209

(

3

):

453

-

466

.

55.

Djaldetti

M

,

Fishman

P

,

Bessler

H

,

Notti

I

.

SEM observations on the mechanism of platelet release from megakaryocytes

.

Thromb Haemost

.

1979

;

42

(

2

):

611

-

620

.

56.

Ihzumi

T

,

Hattori

A

,

Sanada

M

,

Muto

M

.

Megakaryocyte and platelet formation: a scanning electron microscope study in mouse spleen

.

Arch Histol Jpn

.

1977

;

40

(

4

):

305

-

320

.

57.

Italiano

JE

,

Bender

M

,

Merrill-Skoloff

G

,

Ghevaert

C

,

Nieswandt

B

,

Flaumenhaft

R

.

Microvesicles, but not platelets, bud off from mouse bone marrow megakaryocytes

.

Blood

.

2021

;

138

(

20

):

1998

-

2001

.

58.

Niazi

H

,

Zoghdani

N

,

Couty

L

, et al.

Murine platelet production is suppressed by S1P release in the hematopoietic niche, not facilitated by blood S1P sensing

.

Blood Adv

.

2019

;

3

(

11

):

1702

-

1713

.

59.

Fuentes

R

,

Wang

Y

,

Hirsch

J

, et al.

Infusion of mature megakaryocytes into mice yields functional platelets

.

J Clin Invest

.

2010

;

120

(

11

):

3917

-

3922

.

https://doi.org/10.1101/2024.06.04.597316

60.

Kim

H

,

Jarocha

D

,

Johnson

I

, et al.

Studies of infused megakaryocytes into mice support a “catch-and-release” model of pulmonary-centric thrombopoiesis

.

bioRxiv

.

Preprint posted online 5 June 2024

.

61.

Asquith

NL

,

Carminita

E

,

Camacho

V

, et al.

The bone marrow is the primary site of thrombopoiesis

.

Blood

.

2024

;

143

(

3

):

272

-

278

.

62.

Davis

RE

,

Stenberg

PE

,

Levin

J

,

Beckstead

JH

.

Localization of megakaryocytes in normal mice and following administration of platelet antiserum, 5-fluorouracil, or radiostrontium: evidence for the site of platelet production

.

Exp Hematol

.

1997

;

25

(

7

):

638

-

648

.

63.

Stegner

D

,

Vaneeuwijk

JMM

,

Angay

O

, et al.

Thrombopoiesis is spatially regulated by the bone marrow vasculature

.

Nat Commun

.

2017

;

8

(

1

):

127

.

64.

Kallinikos-Maniatis

A

.

Megakaryocytes and platelets in central venous and arterial blood

.

Acta Haematol

.

1969

;

42

(

6

):

330

-

335

.

65.

Pedersen

NT

.

Circulating megakaryocytes in blood from the inferior vena cava in adult rats

.

Scand J Haematol

.

1971

;

8

(

3

):

223

-

230

.

66.

Trowbridge

EA

,

Martin

JF

,

Slater

DN

,

Kishk

YT

,

Warren

CW

.

Platelet production: a computer based biological interpretation

.

Thromb Res

.

1983

;

31

(

2

):

329

-

350

.

67.

Xiao

DW

,

Yang

M

,

Yang

J

,

Hon

KL

,

Fok

FT

.

Lung damage may induce thrombocytopenia

.

Platelets

.

2006

;

17

(

5

):

347

-

349

.

68.

Mishra

N

,

Vagha

K

,

Sawhney

S

,

Murhekar

S

,

Vagha

JD

,

Javvaji

CK

.

Estimation of prevalence of thrombocytopenia in cyanotic congenital heart disease: a cross-sectional study among the pediatric population

.

Cureus

.

2024

;

16

(

3

):

e55453

.

69.

Dunois-Lardé

C

,

Capron

C

,

Fichelson

S

,

Bauer

T

,

Cramer-Bordé

E

,

Baruch

D

.

Exposure of human megakaryocytes to high shear rates accelerates platelet production

.

Blood

.

2009

;

114

(

9

):

1875

-

1883

.

70.

Yamamoto

K

,

de Waard

V

,

Fearns

C

,

Loskutoff

DJ

.

Tissue distribution and regulation of murine von Willebrand factor gene expression in vivo

.

Blood

.

1998

;

92

(

8

):

2791

-

2801

.

71.

Poirault-Chassac

S

,

Nguyen

KA

,

Pietrzyk

A

, et al.

Terminal platelet production is regulated by von Willebrand factor

.

PLoS One

.

2013

;

8

(

5

):

e63810

.

72.

Valet

C

,

Magnen

M

,

Qiu

L

, et al.

Sepsis promotes splenic production of a protective platelet pool with high CD40 ligand expression

.

J Clin Invest

.

2022

;

132

(

7

):

e153920

.

73.

Lim

HI

,

Cuker

A

.

Thrombocytopenia and liver disease: pathophysiology and periprocedural management

.

Hematology

.

2022

;

2022

(

1

):

296

-

302

.

74.

Thomson

JA

,

Itskovitz-Eldor

J

,

Shapiro

SS

, et al.

Embryonic stem cell lines derived from human blastocysts

.

Science

.

1998

;

282

(

5391

):

1145

-

1147

.

75.

Yu

J

,

Vodyanik

MA

,

Smuga-Otto

K

, et al.

Induced pluripotent stem cell lines derived from human somatic cells

.

Science

.

2007

;

318

(

5858

):

1917

-

1920

.

76.

Takahashi

K

,

Tanabe

K

,

Ohnuki

M

, et al.

Induction of pluripotent stem cells from adult human fibroblasts by defined factors

.

Cell

.

2007

;

131

(

5

):

861

-

872

.

77.

Thon

JN

,

Dykstra

BJ

,

Beaulieu

LM

.

Platelet bioreactor: accelerated evolution of design and manufacture

.

Platelets

.

2017

;

28

(

5

):

472

-

477

.

78.

Matsunaga

T

,

Tanaka

I

,

Kobune

M

, et al.

Ex vivo large-scale generation of human platelets from cord blood CD34⁺ cells

.

Stem Cell

.

2006

;

24

(

12

):

2877

-

2887

.

79.

Takayama

N

,

Nishikii

H

,

Usui

J

, et al.

Generation of functional platelets from human embryonic stem cells in vitro via ES-sacs, VEGF-promoted structures that concentrate hematopoietic progenitors

.

Blood

.

2008

;

111

(

11

):

5298

-

5306

.

80.

Lu

S-J

,

Li

F

,

Yin

H

, et al.

Platelets generated from human embryonic stem cells are functional in vitro and in the microcirculation of living mice

.

Cell Res

.

2011

;

21

(

3

):

530

-

545

.

81.

Sullenbarger

B

,

Bahng

JH

,

Gruner

R

,

Kotov

N

,

Lasky

LC

.

Prolonged continuous in vitro human platelet production using three-dimensional scaffolds

.

Exp Hematol

.

2009

;

37

(

1

):

101

-

110

.

82.

Lasky

LC

,

Sullenbarger

B

.

Manipulation of oxygenation and flow-induced shear stress can increase the in vitro yield of platelets from cord blood

.

Tissue Eng Part C Methods

.

2011

;

17

(

11

):

1081

-

1088

.

83.

Blin

A

,

Le Goff

A

,

Magniez

A

, et al.

Microfluidic model of the platelet-generating organ: beyond bone marrow biomimetics

.

Sci Rep

.

2016

;

6

(

1

):

21700

.

84.

Ito

Y

,

Nakamura

S

,

Sugimoto

N

, et al.

Turbulence activates platelet biogenesis to enable clinical scale ex vivo production

.

Cell

.

2018

;

174

(

3

):

636

-

648.e18

.

85.

Strassel

C

,

Brouard

N

,

Mallo

L

, et al.

Aryl hydrocarbon receptor–dependent enrichment of a megakaryocytic precursor with a high potential to produce proplatelets

.

Blood

.

2016

;

127

(

18

):

2231

-

2240

.

86.

Pongérard

A

,

Mallo

L

,

Do Sacramento

V

, et al.

Development of an efficient, ready to use, blood platelet-release device based on two new flow regime parameters: the periodic hydrodynamic loading and the shear stress accumulation

.

N Biotechnol

.

2023

;

77

:

68

-

79

.

87.

Nakagawa

Y

,

Nakamura

S

,

Nakajima

M

, et al.

Two differential flows in a bioreactor promoted platelet generation from human pluripotent stem cell–derived megakaryocytes

.

Exp Hematol

.

2013

;

41

(

8

):

742

-

748

.

88.

Avanzi

MP

,

Oluwadara

OE

,

Cushing

MM

,

Mitchell

ML

,

Fischer

S

,

Mitchell

WB

.

A novel bioreactor and culture method drives high yields of platelets from stem cells

.

Transfusion

.

2016

;

56

(

1

):

170

-

178

.

89.

Martinez

AF

,

McMahon

RD

,

Horner

M

,

Miller

WM

.

A uniform-shear rate microfluidic bioreactor for real-time study of proplatelet formation and rapidly-released platelets

.

Biotechnol Prog

.

2017

;

33

(

6

):

1614

-

1629

.

90.

Tozzi

L

,

Laurent

PA

,

Di Buduo

CA

, et al.

Multi-channel silk sponge mimicking bone marrow vascular niche for platelet production

.

Biomaterials

.

2018

;

178

:

122

-

133

.

91.

Di Buduo

CA

,

Wray

LS

,

Tozzi

L

, et al.

Programmable 3D silk bone marrow niche for platelet generation ex vivo and modeling of megakaryopoiesis pathologies

.

Blood

.

2015

;

125

(

14

):

2254

-

2264

.

92.

Pallotta

I

,

Lovett

M

,

Kaplan

DL

,

Balduini

A

.

Three-dimensional system for the in vitro study of megakaryocytes and functional platelet production using silk-based vascular tubes

.

Tissue Eng Part C Methods

.

2011

;

17

(

12

):

1223

-

1232

.

93.

Thon

JN

,

Mazutis

L

,

Wu

S

, et al.

Platelet bioreactor-on-a-chip

.

Blood

.

2014

;

124

(

12

):

1857

-

1867

.

94.

Fujiyama

S

,

Hori

N

,

Sato

T

,

Enosawa

S

,

Murata

M

,

Kobayashi

E

.

Development of an ex vivo xenogeneic bone environment producing human platelet-like cells

.

PLoS One

.

2020

;

15

(

4

):

e0230507

.

95.

Metcalf

D

.

Blood. Thrombopoietin--at last

.

Nature

.

1994

;

369

(

6481

):

519

-

520

.

96.

Thon

JN

,

Medvetz

DA

,

Karlsson

SM

,

Italiano

JE

.

Road blocks in making platelets for transfusion

.

J Thromb Haemost

.

2015

;

13

(

suppl 1

):

S55

-

S62

.

97.

Do Sacramento

V

,

Mallo

L

,

Freund

M

, et al.

Functional properties of human platelets derived in vitro from CD34⁺ cells

.

Sci Rep

.

2020

;

10

(

1

):

914

.

98.

Strassel

C

,

Gachet

C

,

Lanza

F

.

On the way to in vitro platelet production

.

Front Med

.

2018

;

5

:

239

.

99.

Lambert

MP

,

Sullivan

SK

,

Fuentes

R

,

French

DL

,

Poncz

M

.

Challenges and promises for the development of donor-independent platelet transfusions

.

Blood

.

2013

;

121

(

17

):

3319

-

3324

.

100.

Sugimoto

N

,

Eto

K

.

Generation and manipulation of human iPSC-derived platelets

.

Cell Mol Life Sci

.

2021

;

78

(

7

):

3385

-

3401

.

101.

Sim

X

,

Poncz

M

,

Gadue

P

,

French

DL

.

Understanding platelet generation from megakaryocytes: implications for in vitro-derived platelets

.

Blood

.

2016

;

127

(

10

):

1227

-

1233

.

102.

Sugimoto

N

,

Kanda

J

,

Nakamura

S

, et al.

iPLAT1: the first-in-human clinical trial of iPSC-derived platelets as a phase 1 autologous transfusion study

.

Blood

.

2022

;

140

(

22

):

2398

-

2402

.