Transcript ppt-file

Modeling of Calcium
Signaling Pathways
Stefan Schuster and Beate Knoke
Dept. of Bioinformatics
Friedrich Schiller University Jena
Germany
1. Introduction
• Oscillations of intracellular calcium ions are
important in signal transduction both in excitable
and nonexcitable cells
• A change in agonist (hormone) level can lead to
a switch between oscillatory regimes and
stationary states  digital signal
• Moreover, analogue signal encoded in frequency
• Amplitude encoding and the importance of the
exact time pattern have been discussed;
frequency encoding is main paradigm
Ca2+ oscillations in various types of
nonexcitable cells
Hepatocytes
Oocytes
Astrocytes
Pancreatic acinar cells
Effect 1
Effect 2
Vasopressin
Calmodulin
Ca2+
oscillation
Phenylephrine
Caffeine
UTP
Calpain
PKC
…..
Bow-tie structure of signalling
How can one signal transmit several signals?
Effect 3
Scheme of main processes
Caext
H
R
vout
PLC
vin
vplc vd
PIP2
DAG IP3
vrel
+
vserca
Caer
cytosol
+
ER
vmi
Cacyt
vb,j
vmo
Cam
mitochondria
proteins
Efflux of calcium out of the endoplasmic reticulum is activated by
cytosolic calcium = calcium induced calcium release = CICR
Somogyi-Stucki model
• Is a minimalist model with only 2 independent variables:
Ca2+ in cytosol (S1) and Ca2+ in endoplasmic reticulum
(S2)
• All rate laws are linear except CICR
R. Somogyi and J.W. Stucki, J. Biol. Chem. 266 (1991) 11068
Rate laws of Somogyi-Stucki model
H
Caext
PLC
R
PIP2
v2
Influx into the cell:
v1  const .
vplc
DAG IP3
+
into ER: v4  k4 S1
Efflux out of ER through channels (CICR):
Leak out of the ER:
v6  k6S2
vmi
Cacyt=S1
ER
v6
v5 
vmo
Cam
mitochondria
Caer=S2
Efflux out of the cell: v2  k2 S1
Pumping of
cytosol
+
v5
v4
Ca2+
v1
vd
vb,j
proteins
k5S2 S14
K 4  S14
Temporal behaviour
fast movement
slow movement
Relaxation
oscillations!
Many other models…
• by A. Goldbeter, G. Dupont, J. Keizer, Y.X. Li, T. Chay
etc.
• Reviewed, e.g., in Schuster, S., M. Marhl and T. Höfer.
Eur. J. Biochem. (2002) 269, 1333-1355 and Falcke, M.
Adv. Phys. (2004) 53, 255-440.
• Most models are based on calcium-induced calcium
release.
2. Bifurcation analysis of two models of
calcium oscillations
• Biologically relevant bifurcation parameter in SomogyiStucki model: rate constant of channel, k5 (CICR),
dependent on IP3
• Low k5 : steady state; medium k5: oscillations; high k5:
steady state.
• Transition points (bifurcations) between these regimes
can here be calculated analytically, be equating the trace
of the Jacobian matrix with zero.
Usual picture of Hopf bifurcations
stable limit cycle
parameter
Subcritical Hopf bifurcation
variable
variable
Supercritical Hopf bifurcation
unstable limit cycle
stable limit cycle
parameter
Hysteresis!
Bifurcation diagram
for calcium oscillations
oscillations
Subcritical HB
From: S. Schuster &
M. Marhl, J. Biol. Syst.
9 (2001) 291-314
Supercritical HB
variable
Schematic picture of bifurcation diagram
parameter
Bifurcation
Very steep increase in amplitude.
This is likely to be physiologically advantageous because
oscillations start with a distinct amplitude and, thus,
misinterpretation of the oscillatory signal is avoided.
No hysteresis – signal is unique function of agonist level.
Global bifurcations
• Local bifurcations occur when the behaviour near a
steady state changes qualitatively
• Global bifurcations occur „out of the blue“, by a global
change
• Prominent example: homoclinic bifurcation
Homoclinic bifurcation
S2
Before bifurcation
At bifurcation
Saddle point
Unstable focus
Saddle point
Homoclinic orbit
S1
After bifurcation
Necessary condition in 2D systems:
at least 2 steady states
(in Somogyi-Stucki model,
only one steady state)
Saddle point
Limit cycle
Model including binding of Ca2+ to proteins and
effect of ER transmembrane potential
H
Caext
PLC
R
vout
vin
vd
PIP2
vplc
DAG IP3
cytosol
+
vrel
+
vserca
ER
vmi
Cacyt
Caer
vmo
Cam
mitochondria
vb,j
proteins
Marhl, Schuster, Brumen, Heinrich, Biophys. Chem. 63 (1997) 221
System equations
dCacy t
dt
 J ER, ch  J ER, pump  J ER, leak  J CaPr  J Pr
dCaER  ER

( J ER, pump  J ER, ch  J ER, leak )
dt
 ER
2D model
with
J ER, ch  g~Ca
2
Cacy
t
K12
2
 Cacy
t
( ECa  )
Nonlinear equation for transmembrane potential ...
J ER, pump  kER, pumpCacyt
J Pr  kCacytPr
J ER, leak  kER, leak(CaER  Cacyt)
J CaPr  kCaPr
…this gives rise to a
homoclinic bifurcation
variable
oscillation
Hopf bifn.
Saddle point
parameter
As the velocity of the trajectory
tends to zero when it approaches
the saddle point, the oscillation
period becomes arbirtrarily long
near the bifurcation.
Schuster &
Marhl,
J. Biol. Syst.
9 (2001) 291
3. How can one second messenger
transmit more than one signal?
• One possibility: Bursting oscillations (work with Beate
Knoke and Marko Marhl)
Differential activation of
two Ca2+ - binding proteins
Prot1T * Ca 4
Prot1Ca4 
K1  Ca 4
Prot2T * Ca 4
Prot2Ca4 
 Ca 4 
4
( K 2  Ca )* 1 

K
I 

Selective activation of protein 1
Prot1
Prot2
Selective activation of protein 2
Prot2
Prot1
Simultaneous up- and
downregulation
Prot2
Prot1
S. Schuster, B. Knoke,
M. Marhl: Differential
regulation of proteins by
bursting calcium oscillations
– A theoretical study.
BioSystems 81 (2005)
49-63.
4. Finite calcium oscillations
• Of course, in living cells, only a finite number of
spikes occur
• Question: Is finiteness relevant for protein activation
(decoding of calcium oscillations)?
Intermediate velocity of binding
is best
kon = 500 s-1mM-4
kon = 15 s-1mM-4
kon = 1 s-1mM-4
koff/kon = const. = 0.01 mM4
„Finiteness resonance“
Proteins with different binding properties can be activated selectively.
This effect does not occur for infinitely long oscillations.
M. Marhl, M. Perc, S. Schuster S. A minimal model for decoding of
time-limited Ca(2+) oscillations. Biophys Chem. (2005) Dec 7, Epub ahead of print
5. Discussion
• Relatively simple models (e.g. Somogyi-Stucki) can give
rise to complex bifurcation behaviour.
• Relaxation oscillators allow jump-like increase in
amplitude at bifurcations and do not show hysteresis.
• At global bifurcations, oscillations start with a finite (often
large) amplitude.
• Physiologically advantageous because misinterpretation
of the oscillatory signal is avoided in the presence of
fluctuations.
Discussion (2)
• Near homoclinic bifurcations, oscillation period can get
arbitrarily high.
• This may be relevant for frequency encoding. Frequency
can be varied over a wide range.
• Bursting oscillations may be relevant for transmitting two
signals simultaneously – experimental proof is desirable
• Thus, complex oscillations as found in, e.g. hepatocytes,
may be of physiological importance
• Finite trains of calcium spikes show resonance in protein
activation
• Thus, selective activation of proteins is enabled
Cooperations
• Marko Marhl (University of Maribor,
Slovenia)
• Thomas Höfer (Humboldt University,
Berlin, Germany)
• Exchange with Slovenia supported by
Research Ministries of both countries.