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B. Payrastre et al. INSERM U1048, I2MC, Toulouse, France Rôles des phosphoinositides dans les pathologies cardiovasculaires PI(4,5)P2 Activated mouse platelet

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Page 1: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

B. Payrastre et al.

INSERM U1048, I2MC,

Toulouse, France

Rôles des phosphoinositides dans les

pathologies cardiovasculaires

PI(4,5)P2

Activated mouse platelet

Page 2: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

Phosphoinositides are minor constituents of cell me mbranes with a highly dynamic metabolism

PIP-K IIPI 3-KClass I, II & III

PI K II & IIIPIP-K I

PLC

CH2 CH CH2

O

O C

Arachidonic acid(20:4)

Stearic acid(18:0)

O

C

O

O -

P

O

O

O

100

50%

Relative amounts of phosphoinositides

In general their head group protrudes from the cytosolic leaflet of membranes to get

phosphorylated/dephosphorylated and to bindwith various affinity and specificity to proteins.

cytosol

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PA

PI(ER)PI synthase

CTPCDP-DAG

Inositol

CDP-DAG synthase

PPi

PACMP

PI -

TP

PLC(PM) PI PI(4,5)P2PI(4)P DAG

IP3

The PI cycle in the seventies/eighties

USA 1969 UK 1979 Japan 80’s

M. & L. HokinR. Dawson

J. Folch

M. BerridgeR.H. Michell

R. Irvine

Y. NishizukaK. Mikoshiba

Michell R.H. Biochimica Biophysica Acta 1975

Page 4: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PI(4,5)P2PI4P

PI

IP3

DAGPIP5K

Various pathways of phosphoinositide synthesis and interconversions

PI(3,4)P2

PI(3,4,5)P3PI3K identification

Nature (1988) 332, 644-646

Whitman M, Downes CP, Keeler M, Keller T & Cantley L.

PI5P

Rameh L, Tolias KF,Duckworth BC & Cantley L

PI5P identificationNature (1997) 390, 192-196

PI3P

PI(3,5)P2

Dove et al. PI(3,5)P2pathway identification

Nature (1997) 390, 187-192

Page 5: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PIP3-binding PH domainfrom Grp1

PI(3)P-binding FYVE domainfrom EEA1

PI(3)P-binding PX domain from p47phox

Phosphoinositide binding domains

Itoh T & Takenawa T, Cell Signal 2002

PIP2-binding FERM domain from radixin

PIP2-binding ENTH domainfrom epsin

PI5P-binding domainPHD from ING2

Page 6: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

Phosphoinositides define organelle identity ?

Botelho, Bioessays, 2009Bebpia et al., Nature 2005Carlton & Cullen, Trends Cell Biol 2005Balla & Varnai, Curr Protoc cell Biol 2009

PI(4,5)P2

PI(3,4)P2PI(3,4,5)P2

PI(3,5)P2

PI3P

PI4P

PI5P

PM

ER

golgi

EE

MVB/LE

Lys/vac

CCV

nucleus

CSK

PHD

PH PX

ββββ-prop

PHPX

PHENTH

GAT EEA1(FYVE)

PI3P

PXFYVE

PLCδ (PH)

PHENTH

FERM

PI(4,5)P2

Page 7: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

Phosphoinositides in the dynamics of cell organizat ion and polarity

Di Paolo & Camilli, Nature Rev 2006Sasaki et al., Progress Lipid Res 2009Gassama & Payrastre, Int Rev Cell Mol Biol 2009

AEE

Nucleus

Basolateral

Apical

BEE

Lysosome

RE

ECMPI(3,4,5)P3

PI(4,5)P2

PI3K

PTEN

Epithelial cell polarity

PIP5K

TGN PI4K

Migrating cells :- PI(3,4,5)P3 at the leading edge

Dividing cells : - PI(3,4,5)P3 at the midsection of

the cortex to properly orientatethe spindle

- PI3P at the midbody during cytokinesisto recruit cytokinesis regulatory machinery

- PI(4,5)P2 at the mitotic cortex as a spatial regulator of its stability

The regulation and localization of PI-kinases and - phosphatases is critical to ensure adequate cell response to environmental cues .

Page 8: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

60.00 70.00

PI(4)P

Time (min)15.00 25.00

0

500

1000

CTS

PI(3)P

PI(3,5)P2

PI(3,4)P2

PI(4,5)P2

PI(3,4,5)P3

HPLC

PIP2

PIP

origin

MP

PI

PIP3

TLC

deacylationO

CH

CH2 O

C O

C CH2OO

P

O

O

OH P04OH

O

P04

P04

Analysis of phosphoinositides: a specialized lipid biochemistry

Isotopic labelling (3H-inositol or 32Pi) followed by TLC and HPLC techniques :

B. Payrastre, Methods Mol Biol 2004

Page 9: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

Analysis of phosphoinositides : towards mass spectr ometry methods

Chemical derivation (phosphate methylation with TMS-diazomethane) coupled to HPLC-MS techniques :

J. Clark et al., Nature Methods 2011Plateau de lipidomique MétaToul

I2MC, Toulouse (http://www.i2mc.inserm.fr)

0,00

2,00

4,00

6,00

8,00

10,00

12,00

PIP

3 (n

g/10

7pl

atel

ets)

WT SHIP1 -/-

**

**

PIP3 level in WT versus SHIP1 -/- platelets:

PIP3 molecular species

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Phosphoinositide metabolism and human diseases

PI(4,5)P2PI4P

PI

IP3

DAGPIP5K

PI(3,4,5)P3

PI(3,4)P2

Pendaries et al., FEBS Lett 2003McCrea & De Camilli Physiology 2009

PI(3,5)P2

PI3P PI5P

Lowe syndrome

Myotubular myopathy&

Charcot-Marie-Tooth

oncogenesis

LCContractural S

(PIP5Kγ)γ)γ)γ)

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The Shigella flexneri effector IpgD has a motif related to the active site of mammalian phosphoinositide phosphatases

PCWNCKSGKDRTGMQDAEIKREIIRK

AAIHCKAGKG RTGVMICAYLLHRGKF

VLVHCSDGWDRTAQLTSLAML-M-LD

VLVHCSDGWDRTPQIVALAKL-L-LD

IpgD

PTEN

MTM1

MTMR3

The IpgDC438S is an inactive phosphatase

PM

Host cell

Shigella flexneriType III secretionsystem

IpgD

The Shigella flexneri effector IpgD is a PI-phosphatase

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IpgD-dependent PI(4,5)P 2 hydrolysis in Hela cellsinfected with Shigella flexneri

12000

PI(4,5)P2

PIP

origin

MP

WT

0

3000

6000

9000PIP

PI(4,5)P2

30’

origin

MP

0’ 15’

∆ ∆ ∆ ∆ IpgD

0

3000

6000

9000

12000

0’ 15’ 30’

PI(4,5)P2

PIP

PI(4,5)P2

PIP

PI5P

PI4Por ?

Time (min)40.00 45.00

0

200

400

600

800

CTS

PI4P PI5P

Time (min)40.00 45.00

0

200

400

600

800

CTS

PI4P

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The Shigella effector IpgD is sufficient to increase PI5P levels in host cells

32P-PI(4,5)P2PI5P + PIP-kinase II αααα γ32P-ATPPI4PPI3P

50

100

C IpgD

Expression of GFP-IpgDin Hela cells

IpgD-C438S

pmol

PI5

P /

mg

prot

.

32P-PI(4,5)P2

- BS176 ∆ IpgDWT

pmol

PI5

P /

mg

prot

.

0

100

200

300

400

Hela cells infected with wild typeshigella and mutants

PI5P mass assay

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Bacteria

PI5P is produced in host cells at the entry site of S. flexneri

(PHDx2 biot) (Phalloidin)PI5P F-Actin

(LPS)

Biot-GST-2XPHD probe

PHD PHD

Streptavidin-Alexa594

GSTBIOTINE

O. Gozani et al Cell 2003

Page 15: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

S. flexneri

IpgD

PI(4,5)P2 PI5P

Actin

Host cell

PI(3,4,5)P3

AKT

Host cellsurvival

Shigella flexneri injects the PI-phosphatase IpgD in the host cell through its Type III secretion system :

a model to study the role of PI5P

Niebuhr et al EMBO J. 2002Pendaries et al. EMBO J. 2006Coronas et al. Biochem Soc Symp 2007Ramel et al. BBRC 2009

?

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PI5P integrates membrane and cytoskeleton dynamics

Akt

Prolonged survival signaling

PI5PPP

Lysosomal degradation blockade

RTK activation

Tom1 ?

EE

Bacterial infection

PI(3,5)P2

Chicanne et al Biochem J 2012Dupuis-Coronas et al. J Biol Chem 2011Amoasii et al. PLoS Genetics 2012

PIKfyvePI3P

Directed migration

Tiam1

Rab4

Rac1GTP

Actin dynamics

Recycling

Rac1GTP

Tiam1

Rac1GTP

PI5P

Ramel et al, 2011

Oncogenes

EGF-R

Page 17: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PI3Kββββ in platelet activation and thrombus growth

Page 18: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

Plasma membrane

Kinases (Akt,PDK)Phospholipase (PLCγ )

Adaptors (Gab)GEFs (Vav, ARNO)

GrowthProliferation & Survival

MetabolismDifferentiation

Polarisation & Motility

PP

PIP2

PP

P

PIP3

Signal

CancerImmunityDiabetes

Haemostasis

A critical role for PI3K and PIP3 in cell regulatio n

Vanhaesebroeck B. et al., Nature Review 2010 Sasaki et al., Progress Lipid Res 2009Hirsch E. et al., Trends Biochem Sci 2009

PH

Increase protein concentrationto generate a steric environmentfavorable for protein interactions

Page 19: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

BLEEDING

THROMBOSIS

Adapted from Brass, Nature 2001

The key role of platelets in haemostasis and thromb osis

resting

activated

Interactions with blood cells and endothelial cells,

secretion of cytokines, growth factors and matrix proteins

- Inflammation- Atherosclerosis- Angiogenesis- Metastasis

NewsFocusScience 2010

Page 20: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

BloodFlow

GPIbα

Atherosclerotic plaque

Collagen

FGFGFGFGααααIIbIIbIIbIIbββββ3333

++++TxA2ADP

FGFGFGFG

VWF

GPVI

Platelet activation and ischemic vascular events du ring atherothrombosis

platelet

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PI3Ks are activated downstream of most activatory h uman platelet receptors

PI3Ks

Class I PI 3-kinases are drug targets in

cancer and immune diseases

(ex : XL147, XL765, INK1117)

PI3K inhibitors entering in clinic

TXA2,Thrombin

GqG12/13

Gi

ADP

P2Y12

PAR1 & 4, TP, P2Y1

PAR1 & 4, TP

Sol

uble

ago

nist

s

FcRγγγγ

Talin

Fibrinogen

Collagen

vWF

Syk

Src

ααααIIbββββ3 (GpIIbIIIa)

Adh

esiv

e m

olec

ules

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Blood platelets contain all the different PI3K

Vanhaesebroeck et al., Nat Rev Mol Cell Biol 2012Laurent P.A. et al., Advance Biol Reg 2013

p110 α, β, δα, β, δα, β, δα, β, δ

p110 γγγγ

Class Ia

Class Ib

PI3KC2 α,β,γα,β,γα,β,γα,β,γ

Vps34p

Class II

Class IIIClass III

PF4Cre-p110ββββlox/lox

PF4Cre-p110ααααlox/lox

Page 23: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PF4Cre-p110β β β β lox/lox

p110ββββ

lung

liver

kidney

platelets

p110ββββ

p110δδδδ

p110γγγγ

p110αααα

actin

platelets

Mouse model of PI3K ββββ invalidation specifically in the megakaryocyte/platelet lineage

Page 24: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

not mandatory to induce platelet aggregation in res ponse to thrombin or U46619 stimulation but required for the formation of large platelet aggregates

required for ααααIIbββββ3 -mediated platelet adhesion on fibrinogen under flo w conditions and spreading in static conditions, involved in fib rin clot retraction

PI3Kββββ in platelet activation in vitro

critical role in GPVI-mediated platelet activation (Akt activation, PLC γγγγ2 activation, Ca2+ mobilization, PKC activation, PLA2 activation & TXA2, 12-HETE, 8-HETE synthesis )

Role in vivo ?Jackson et al Nature Med 2005Ragab et al., Blood 2007Gratacap et al. Blood 2009Martin et al., Blood 2010Canobbio et al Blood 2009

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A role for PI3K ββββ in arterial thrombus formation

PI3Kββββ-null mice have a normal tail bleeding time but are protected against the formation of occlusive thrombus.

Carotideinjury by FeCl3

Thrombus formation in vivo:(carotide injury and monitoring of blood flow)

Cre- P110ββββ-null

(9) (10)

% o

f a

nim

als

fo

rmin

g t

hro

mb

us

Stable occlusion

Unstable partial occlusion

No occlusion (<25%)

1

Flow probe(transonic)

Ble

edin

g tim

e (s

)

P110β-nullWild-type0

100

200

300

> 1800

Tail bleeding time :

Page 26: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PI3Kββββ regulates thrombus growth and stability under high shear rate

PI3Kβ plays a key role in thrombus stability

Laurent et al., submitted

Laser

Laser injury of mesenteric arteriole

and intravital microscopy :

LP ko

0 120 240 360 480 6000

10000

20000

30000

40000

50000

Time (s)T

hrom

bus

area

(µm

²)0 120 240 360 480 600

0

10000

20000

30000

40000

50000

Time (s)

Thro

mbu

s ar

ea (

µm²)

WT p110βnull

8 s 80 s

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McFadyen & Jackson, Thromb Haemost 2013

Thrombus growth and stability is a highly dynamic p rocess

High shear stress

Blood flow

Study of platelet adhesive interactions and thrombus growth in whole blood

under flow conditions micro-capillary coatted with collagen, vWF or

endothelial cells

aspiration

pomp

Ulratfastimagingsystem

Fluorescentplatelets

(whole blood)

Whole blood Flow

Page 28: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

Physiological shear (22.5 dyn/cm2)

*

*

22.5 dyn/cm2 (120 s) Thrombus formed

PI3Kββββ regulates thrombus stability under high shear rate

High shear (180 dyn/cm 2)120s 180s

p110ββββnull

WT

180 dyn/cm2 (60 s)Imaging/quantification

180 dyn/cm2 (60s)

wt p110ββββnull0

50000

100000

150000

200000

250000

**

thro

mbi

vol

ume

(µm

3)

wt p110ββββnull0

20

40

60

80

*su

rfac

e co

vera

ge (

%)

Laurent et al., submitted

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Flow 22.5 dyn/cm2

(2 min)

p110ββββ-null

control

p-GSK-3 αααα (Ser21)

p-GSK-3 ββββ (Ser9)

p-Akt (Ser473)

WT p110ββββnull

actin

GSK-3ββββ

Akt

PI3Kββββ is required for GSK3 αααα/ββββ inhibitory phosphorylationwithin the thrombus

120sAkt

GSK3αααα/ββββ

PI3Kβ

P

P

P

PDK1/2

Laurent et al., submitted

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0

100000

200000

300000

400000

CHIR-99021 (1µM) - + - +

p110ββββnullWT

thro

mbi

vol

ume

(µm

3 )

0

20

40

60

80

CHIR-99021 (1µM) - + - +

p110ββββnullWT

surf

ace

cove

rage

(%

)

180 dyne/cm 2 180 dyne/cm 2

** **

Thrombus formed

at 22.5 dyne/cm2

(120 s)

180 dyn/cm2

(60 s)

Imaging/quantification

Inhibition of GSK3 restores thrombus stability of P I3Kββββ null platelet mice under high shear stress

Laurent et al., submitted

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Inhibition of PI3K has little effect on primary hae mostasis and bleeding but

affects thrombus growth and stability in high shear stress conditions.

Targeting PI3K ββββ as a novel antithrombotic strategy ?

PI3Kββββ is expressed in many cell types suggesting potentia l side effects (a

recent phase I clinical trial with AZD6482 by Astra has shown little or no

adverse effect J Thromb Haemost 2012)

PI3Kββββ inhibition destabilizes platelet thrombi leading to the formation of

platelet emboli (distal embolization ?).

Advantage :

Potential disadvantages :

The PI3Kββββ/Akt/GSK3 axis is critical for thrombus stability u nder high shear stress condition

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WT

Sepsis Sham

p110ββββnull

PI3Kββββ null platelet mice are protected against thrombus f ormation in lung microcirculation upon peritonitis-induced seps is

liver

Intestine

WT p110ββββnull

Peritonitis-induced severe sepsis in mice

1515

6

Num

ber

of th

rom

bi/n

umbe

r of

ves

sels

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P2Y1

TP

Thrombus growthThrombus growthLA

T

Syk

FcRγGPVI

Gq

Gi

PAR1

PAR4

P2Y12

Gi

Gq

G12/13

G12/13

αIIββββ3

SFKPLCγ2

PLCγ2

PI3Kαααα PI3Kββββ

PI3Kββββ

PI3KββββGSK3Thrombus growth and stability under

high shear rate

PI3Kαααα and PI3K ββββ have distinct and important roles in platelet activation and thrombus stability

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“Platelet production and function,sign aling and phosphoinositides ”

Inserm U563, Toulouse, France

Collaborations :B. Van Haesebroeck

C. GachetP. Sansonetti

S. SeverinJ. ViaudF. BoalP.A. LaurentA. Antkowiak(D. Ramel & F. Lagarigue)

B. PayrastreF. Gaits-IacovoniH. TronchèreM.P. GratacapA.D. TerrisseG. ChicanneA. RagabJ.M. Xuereb

Animal , lipidomic and Cell Imaging Facilities

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Acides biliaires (bile)

Lipoprotéines• Eicosanoides• Phospholipides• Céramides,

Sphingomyéline• Stérol C4• PIP3• Sphingosine-

Phosphate• Isoprostanes• LPA,PA,LPC

• Sphinganine, sphingosine

• Céramides• Sphingomyéline• Ganglioside,

GluCer, GalCer

Instruments analytiques et

molécules analysées

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Instruments analytiques et

molécules analysées

• Oestradiol• Stérols• Oxystérols• Acides gras

hydroxylés (non conventionnels)

Lipides neutres- TG- DG- Cholestérol- Chol esters

Acides Gras libres et Totaux

DéveloppementsEssais

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� Le personnel du plateau

� Les membres du conseil scientifique

Bernard Payrastre (Président), Xavier Collet, Thierry Levade, Marc Poirot, Hervé Guillou, Nicolas Cénac, Joost Schanstra, Nathalie Auge, François Tercé, Jean Sébastien Saulnier-Blache

Véronique ROQUESTechnicienne UPS

PaulineLE FAOUDER

CDD IR

Aude DUPUYCDD IE

Fabien RIOLSCDD IE

Justine BERTRAND MICHEL

IR, responsable plateau

MetaToul-Lipidomique

Plateau de lipidomique MétaToulI2MC, Toulouse (http://www.i2mc.inserm.fr)

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Thrombin 0.5IU/ml

U46619 1µM

Control p110 ββββ-null

0 1 2 3 4 5 6 7

Time (min)

0

50

100

0

50

100

Agg

rega

tion

(%)

Agg

rega

tion

(%)

Control p110ββββ-null

Thrombin0.5 IU/ml0.3 IU/ml0.2 IU/ml

U466191 µM0.5 µM0.25 µM

U46619

0 1 2 3 4 5 6 7

Time (min)

PI3Kβ is necessary for the formation of large aggregates upon thrombin and TXA2 stimulation and is critical for GPVI-induced platelet activation

Role of PI3K ββββ in platelet aggregation in response to various agon ists

Control p110ββββ-null

0

50

100

0

50

100

Agg

rega

tion

(%)

Agg

rega

tion

(%)

Collagen10 µg/ml5 µg/ml2.5 µg/ml

Convulxin

15 nM10 nM

0 1 2 3 4 5 6 7

Time (min)0 1 2 3 4 5 6 7 0 1 2 3 4 5 6 7

Time (min)

Collagen 10µg/ml

Control p110 ββββ-null

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GpVI

YP

YP

Fcγγγγ−−−−Chain

Src

ITA

M

CollagenCVX

Syk

SH

2S

H2

Y 175Y 195Y 235

Y 136

An important role of PI3K ββββ in GPVI-mediated platelet activation

PLCγγγγ2pY

Secreted ADP

P2Y12

Giraft

Secretion / Aggregation

PKC

Ca2+

DAG

IP3

Ragab et al., Blood 2007Gratacap et al. Blood 2009Martin et al., Blood 2010

PI3Kββββ

PIP

2

PIP

3Akt

PIP

3 pr

oduc

tion

(Fol

d in

crea

se)

CVX15 nM

Resting

Control

p110ββββ-null

*

PIP3

Mbr/Csk boundPLCγ2

total PLCγ2

0 30 60 30 60 (s)

p110βnull

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A role for PI3K αααα in arterial thrombus formation in vivo

0 30 60 90 120 150 1800

100

200

300

400

500

Time (s)

Thro

mbu

s ar

ea (

µm²)

WT KO0

100

200

300

400

500 *

Thro

mbu

s ar

ea (

µm²)

Area at 30s

Superficial lesion

WT

p110α

0 120 240 360 480 6000

5000

10000

15000

20000

25000

30000

Time (s)

Thr

ombu

s ar

ea (

µm²)

Deep lesion

WT

p110α

WT KO0

2.0××××106

4.0××××106

6.0××××106

8.0××××106

1.0××××107ns

AU

C (

µm2 x

min

)

PI3Kαααα is implicated in thrombus growth in vivo upon superficial arterial injury and is not involved in thrombus sta bility

Laser

Laser injury of mesenteric arteriole

and intravital microscopy :

Page 41: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

Thrombin : (IU/ml)

PI3Kα partially contributes to ITAM-mediated Akt activation

P-Akt (Ser473)

actin

- -0.02 0.020.03 0.03

- -0.2 0.20.25 0.250.5 0.5

P-Akt (Ser473)

actin

U46619 :(µM)

p110ααααnullWT

- 1 1.5 2 - 1 1.5 2

P-Akt (Ser473)

actin

CRP :(µg/ml)

Role of PI3K αααα in Akt activation

Page 42: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

GpVI

YP

YP

Fcγγγγ−−−−ChainpY

Src/BTK

Src

ITA

M

CollagenCVX

Syk

SH

2S

H2 PLCγγγγ2

PIP

2

Secretion / Aggregation

PIP

2

IP3

DAG PKC

Ca2+

Y PY PY P

Y P

Nieswandt & Watson, Blood 2003

Mechanism of platelet activation via the collagen receptor GPVI

Page 43: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

Integrin GpIIbIIIa ( αΙΙαΙΙαΙΙαΙΙbββββ3) signaling is essential for platelet aggregation

ααααIIb ββββ3

(Closed!)

(occupied!)

Inside-out signaling

Primary agonists

Signaling cascade 1

Integrin regulatorsCytoskeletonchanges

Fibrinogen

P

P

Signaling cascade 2

Outside-in signalingFormation of large aggregates

with thightly associated platelets

Page 44: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PI3Kββββ is involved in integrin GpIIbIIIa signaling

Controlp110ββββ-null

0 30 60 120Time (min)

**

***

Delay in the clot retraction : potential role of p110ββββ in organizing an efficient GpIIbIIIa-mediated contractility

Fibrin clot retractionC

lot r

etra

ctio

n (%

ser

um e

xtru

ded

from

clo

t)

***

***

*

Control

p110ββββ-null

Sur

face

cov

ered

(%

)

***

PI3Kββββ is required for GpIIbIIIa-mediated platelet adhesio n on fibrinogen under flow conditions and spreading i n static conditions

Controlp110ββββ-null

Platelet adhesion on fibrinogenunder flow conditions (1500 s-1)

Platelet adhesion on fibrinogen(static conditions)

actintubulin

Control p110β-null

30 60 1200

Time (min)

Page 45: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

P-Akt (Ser473)

total Akt

- -0.2 0.20.3 0.30.5 0.5

- -0.25 0.250.5 0.51 1

P-Akt (Ser473)

total Akt

Thrombin : (IU/ml)

U46619 :(µM)

p110ββββnullWT

PI3Kβ plays an essential role in Aktactivation induced by both ITAM and GPCR

-mediated platelet signaling

- 1 1.5 2 - 1 1.5 2

P-Akt (Ser473)

total Akt

CRP :(µg/ml)

Respective roles of PI3-kinases αααα and ββββ in Akt activation

PI3Kβ

Page 46: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

ααααIIbββββ3

Fibrinogen

P-MLC

Ca2+-calmodulin

MLCK

PI3KββββSHIP1SHIP1 PtdIns(3,4,5)P3

PtdIns(3,4)P2

PI 3K ββββ and SHIP1 play an important role in the formation o flarge aggregates

Formation of large aggregates with tightly associated platelets

TXA2ADP

TXA2 ADP

CAMs

Eph kinases/Ephrine

GPCR

cytoskeletonorganization

mec

hani

cal

forc

e

Adapted from Brass et al. J. Clin. Invest. 2005

?

Page 47: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PI5P production increases the colocalization of EGFR with early endosome markers

EndosomeEEA1

P P

P

P

P

P

SNX1

Col

ocal

isat

ion

EG

FR

/EE

A1

GFP -IpgD WT

GFP

*

0%

20%

40%

60%

80%

100%

GFP -IpgD WT

GFP

Col

ocal

isat

ion

EG

FR

/SN

X1 *

C EGFP EEA1 EGFR Merge

EGFP

EGFP

-Ipg

D-W

T

A EGFP SNX1 EGFR Merge

EGFP

EGFP

-IpgD

-WT

Page 48: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

controle IpgD

IpgD-inducible MEF cells

Page 49: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

P-EGFR Y1173

P-EGFR Y1068

EGFR

P-Akt S473

Akt

Ectopic expression of IpgD and PI5P generation acti vate EGFR

IpgD-inducible MEF cells

IpgD

Ctrl

Inp54PI(4,5)P2 PI4P

IpgDPI(4,5)P2 PI5P

Page 50: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

GFP -IpgD WT

GFP

Colocalisation P-EGFR/EEA1

0%

20%

40%

60%

80%

100% *

GFP -IpgD WT

GFP

Colocalisation EGFR/P-Akt

0%

20%

40%

60%

80%

100% *

A EGFP EEA1 P-EGFR Y1173 Merge

EGFP

EGFP

-IpgD

-WT

C EGFP EGFRP-Akt S473 Merge

EGFP

EGFP

-IpgD

-WT

PI5P production increases the colocalization of the active EGFR with early endosome markers

Gorvel et al. Cell 1991

- +EE

- +LE

0

5

10

15

20

25

IpgD :

EEA1

BHK cells

Endosome isolationand

biochemical analysis

PI5

P(f

old

incr

ease

)

0

0.5

1

PI3

P(f

old

incr

ease

) 1.5

P-EGFR

P-Akt

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PI5P PI(4,5)P2Type II PIP4Ks

PIPLIP ?

(PTPMT1)

PI(3,5)P2

3-P

ME

PI3

K (

I)

Eukaryotic cells have the machinery to produce PI5P

Bacterial phosphatase

PI5

P p

mol

/5x1

09ce

lls

60

30

Emptyplasmid

*

*

0MTM1

WTMTM1C375S

S. Cerevisiae ymr1∆

Bertazzi et al. PLoS Genetics 2012

4-PME(Type I & II 4-PME)

Myotubularins

PI(3,5)P2

MTMR2

Page 52: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

IpgD

PI5PPI(4,5)P2

Nucleus

Cell Survival

PI3K

FKHR

P70-S6KGSK3

Akt

?

PI5P-mediated Akt activation requires EGFR

EGFR

Host cell

P-Akt S473

Total Akt

Control IpgD WT

EGFR siRNA (nM): 0 0100 100

EGFR

Control siRNA (nM): 0 0100 100

P-Akt S473

Total Akt

Control IpgD WT

AG 1478 (10 nM): - + - +

P-Akt T308

Page 53: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

EGFR

Actin

GFP

IpgD WT

GFP-PI5P4KIIββββ

0’ 60’

EGF Stimulation (200 ng/ml)

- +

- -

+

+

- +

- -

+

+

PI5P production protects EGFR from degradation

EE

LE

Ly

EEA1

SNX1

LAMP-1

Page 54: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PI5P production accumulates the fluid phase markerrhodamine-dextran in early endosomes

0%

20%

40%

60%

80%

100%

GFP -IpgD WT

GFP

Dextran/EEA1

*

0%

20%

40%

60%

80%

100%

GFP -IpgD WT

GFP

Dextran/Lamp1

*

A EGFP Dextran EEA1 Merge

EG

FPE

GFP

-IpgD

-WT

EGFP Dextran Lamp1 Merge

EGFP

EGFP

-IpgD

-WT

C

Pulse-chaseexperiments

Page 55: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PI5P is a new player in trafficking that regulates signal persistence in Shigella flexneri infected cells

IpgD

PI5PPI(4,5)P2

Nucleus

Cell Survival

PI3K

FKHRP70-S6K

GSK3

Akt

?

Host cell

PI5P production via IpgD activatesEGF-R and blocks its degradation to maintain

Akt-mediated survival signals

EGFRProlonged

survivalsignals

LE

RE

Golgi

EE

Ly

PtdIns5P

EGFR

Active EGFR

B

Retrograde pathway

PM

Recycling

Retrograde pathway

Ramel et al, 2011

Page 56: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

IpgD

PI5PPI(4,5)P2

Nucleus

Cell Survival

PI3K

FKHR

P70-S6KGSK3

Akt

?

PI5P-mediated Akt activation requires EGFR

EGFR

Host cell

P-Akt S473

Total Akt

Control IpgD WT

EGFR siRNA (nM): 0 0100 100

EGFR

Control siRNA (nM): 0 0100 100

P-Akt S473

Total Akt

Control IpgD WT

AG 1478 (10 nM): - + - +

P-Akt T308

Page 57: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

PF4Cre-p110β β β β lox/lox

p110ββββ

lung

liver

kidney

platelets

p110ββββ

p110δδδδ

p110γγγγ

p110αααα

actin

platelets

Mouse model of PI3-kinases αααα and ββββ invalidation specifically in the megakaryocyte/platelet lineage

PI3Kβ

PF4Cre-p110α α α α lox/lox

p110ββββ

p110δδδδ

p110γγγγ

p110αααα

actin

platelets

lung

liver

kidney

platelets

p110αααα

PI3Kα

Page 58: Rôles des phosphoinositides dans les pathologies ...ae2bm.org/wp-content/uploads/2013/09/BP_Strasbourg2013.pdf · PI - TP PLC (PM) PI PI(4,5)P PI(4)P 2 DAG IP3 The PI cycle in the

P-Akt (Ser473)

total Akt

- -0.2 0.20.3 0.30.5 0.5

- -0.25 0.250.5 0.51 1

P-Akt (Ser473)

total Akt

Thrombin : (IU/ml)

U46619 :(µM)

p110ββββnullWT

PI3Kβ plays an essential role in Aktactivation induced by both ITAM and GPCR

-mediated platelet signaling

- 1 1.5 2 - 1 1.5 2

P-Akt (Ser473)

total Akt

CRP :(µg/ml)

Respective roles of PI3-kinases αααα and ββββ in Akt activation

PI3Kβ

Thrombin : (IU/ml)

PI3Kα partially contributes to ITAM-mediated Akt activation

P-Akt (Ser473)

actin

- -0.02 0.020.03 0.03

- -0.2 0.20.25 0.250.5 0.5

P-Akt (Ser473)

actin

U46619 :(µM)

p110ααααnullWT

- 1 1.5 2 - 1 1.5 2

P-Akt (Ser473)

actin

CRP :(µg/ml)

PI3Kα

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Stimulation of PI3K ββββ : Tyrosine kinases and G ββββ/γγγγ subunits

RTK

P

PP

P P

P

PIP2

P

PP

PIP3

GTP

α

β/γ

SH3

SH2

SH2

P110ββββ

p85α/β

Ras

PI3-kinase ββββ is activated via GPCR (Guillermet-Guibert et al. PNAS 2008) and/or the

association of the 2 pathways, GPCR & RTK (Hazeki et al. Life Sci 1998; Maier et al. JBC

1999; Tang & Downes JBC 1997; Kubo et al. BJ 2005; Dbouk et al. Science Signaling 2012)

PI3Kββββ

β/γ

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The integrine GpIIbIIIa ( ααααIIbβ3)β3)β3)β3) is essential for platelet aggregation and thrombus growth

ITA

M