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Glycogen Synthase Kinase 3
 β
(GSK3
 β
) Regulates Differentiation andProliferation in Neural Stem Cells from the Rat Subventricular Zone
Martin H. Maurer,*
,†
Jens O. Bro
 1 
mme,
†,§
Robert E. Feldmann, Jr.,
†,§
 Anne Ja 
 1 
rve,
Fatemeh Sabouri,
Heinrich F. Bu
 1 
rgers,
Dominik W. Schelshorn,
Carola Kru
 1 
ger,
 Armin Schneider,
and Wolfgang Kuschinsky 
Department of Physiology and Pathophysiology, Division of Systems Physiology, University of Heidelberg,Im Neuenheimer Feld 326, 69120 Heidelberg, Germany, and SYGNIS Pharma AG, Im Neuenheimer Feld 515,Heidelberg, Germany 
Received November 3, 2006
On the basis of its inhibition by SB216763, we identified the multifunctional enzyme Glycogen SynthaseKinase 3
 β
(GSK3
 β
) as a central regulator for differentiation and cell survival of adult neural stem cells.Detected by proteomic approaches, members of the Wnt/ 
 β
-catenin signaling pathway appear toparticipate in enhanced neuronal differentiation and activated transcription of
β
-catenin target genesduring GSK3
 β
inhibition, associated with decreased apoptosis.
Keywords:
Neural stem cell
Neurosphere
Glycogen Synthase Kinase 3
 β
Two-dimensional gel electrophoresis
Rat
Subventricular zone
Introduction
Glycogen Synthase Kinase 3
 β
(GSK3
 β
) was originally namedfor its role in glycogen metabolism. Nowadays, GSK3
 β
isconsidered a multifunctional enzyme participating in cellsurvival, formation of the cytoskeleton, cell growth and polarity,metabolism, and transcriptional control.
1
-
3
In mammals, GSK3
 β
also takes part in oncogenesis and neurological disorders.
4
During development, GSK3
 β
coordinates cell growth andpolarity.
5
-
7
GSK3
 β
is located both in the cytoplasm and the nucleus. Twofunctionally different protein isoforms have been identified: theunbound form is regulated by protein kinases, whereas thesecond form is associated with two others proteins, axin andthe adenomateous polyposis coli protein (APC), and is regu-lated by the developmental Wnt signaling pathway.
1
Of note,phosphorylation of GSK3
 β
at its serine residues results ininactivation of the enzyme, not in signaling activation. Theinactivation of GSK3
 β
results in the stabilization of its down-stream target
β
-catenin, which is otherwise ubiquitinated anddegraded in the proteasome. The stabilized
β
-catenin istransferred to the nucleus and binds to the TCF/Lef-1 tran-scription factor, activating transcription for specific targetgenes.
8
-
10
In the present study, we analyzed the molecular basis of GSK3
 β
for proliferation and differentiation of adult neural stemcells. First, we measured changes in protein levels during inhibition of GSK3
 β
to detect proteins involved in this process. After verifying the transcriptional activation by 
β
-cateninstabilization and nuclear transfer, we focused on cell viability and found an increase in neurosphere differentiation.
Materials and Methods
Neurosphere Cultures
.
Neural stem cells were isolated fromadult rat brains as described earlier.
11,12
Protocols are concor-dant with the policy on the use of animals, as endorsed by theNational Institutes of Health, and fulfill the local legal require-ments. The subventricular zones of 6 rat brains were dissected, washed in 10 mL ice-cold Dulbecco’s Phosphate Buffered Saline(DPBS) supplemented with 4.5 g/L glucose (DPBS/Glc) andcentrifuged for 5 min at 1600
 g 
at 4
°
C. The pellet wasmechanically homogenized, resuspended in 20 mL DPBS/Glc,and centrifuged for 5 min at 1600
 g 
at 4
°
C. The pellet wasenzymatically digested in 10 mL of 0.01% (w/v) papain, 0.1%(w/v) Dispase II (neutral protease), 0.01% (w/v) DNase I, and12.4 mM MgSO4 in Hank’s Balanced Salt Solution (HBSS),triturated by a plastic pipet tip, and incubated at roomtemperature for 40 min. In three washing steps, the homoge-nate was centrifuged for 5 min at 1600
 g 
at 4
°
C, and the pellet was resuspended in 10 mL Dulbecco’s Modified Eagle’s Me-dium (DMEM)-Ham’s F12 medium supplemented with 100units/mL penicillin, 100 units/mL streptomycin, and 2 mM
L
-glutamine. Cells were resuspended in 1 mL of neurobasal-B27 medium, and the cell number was counted. Cells wereplated in 2 mL dishes at 200 000 cells in B27-neurobasalmedium supplemented with 100 units/mL penicillin, 100 units/mL streptomycin, 20 ng/mL EGF, 20 ng/mL FGF-2, and 2
µ
g/mL heparin. About 4/5 of the medium was replaced weekly,
* To whom correspondence should be addressed. Dr. Martin H. Maurer,Dept. of Physiology and Pathophysiology, University of Heidelberg, ImNeuenheimer Feld 326, 69120 Heidelberg, Germany. Phone:
+
49-6221-544075. Fax:
+
49-6221-544561. E-mail: maurer@physiologie.uni-heidel-berg.de.
University of Heidelberg.
SYGNIS Pharma AG.
§
Equal cotntributions.
1198 Journal of Proteome Research
2007, 6, 1198 
-
1208 
10.1021/pr0605825 CCC: $37.00
©
2007 American Chemical SocietyPublished on Web 01/18/2007
 
and cells were passaged every 10
-
14 days. The neurospheres were cultured for 6
-
10 weeks in 5% CO
2
at 37
°
C before use.For inhibition of GSK3
 β
, cell cultures were incubated for 3days in the presence of 10
µ
M (final concentration) 3-(2,4-dichlorphenyl)-4-(1-methyl-1
-indol-3-yl)-1
-pyrrole-2,5-di-one (SB216763; Tocris, Ellisville, MO), a specific low-molecular weight inhibitor of GSK3.
13
-
15
Five cell cultures were used ineach group for comparative replicates, run in individual gels.
Two-Dimensional Gel Electrophoresis (2-DE)
.
2-DE wasperformed using standard protocols as previously described.
11,12,16
Cells were harvested, and protein extraction for 2-DE wasperformed for 60 min at room temperature in a lysis buffercontaining 7 M urea, 2 M thiourea, 4% (w/v) CHAPS, 0.5% (v/v) Triton X-100, 100 mM DTT, 0.05% IPG buffer, pH 3
-
10(Amersham Biosciences, Uppsala, Sweden), and 0.156% (w/v)Complete protease inhibitor tablets (Roche, Mannheim, Ger-many). Sample protein amounts were determined by themodified Bradford method.
17,18
 A total of 250
µ
g (5
-
10
µ
L) of the protein solution was suspended in rehydration solutionconsisting of 6 M urea, 2 M thiourea, 2% (w/v) CHAPS, 0.5%(v/v) IPG buffer, pH 3
-
10, and a few grains of bromophenolblue to give a final volume of 350
µ
L. The samples were appliedto pH 3
-
10 nonlinear gradient IEF gel strips for isoelectricfocusing in the IPGphor apparatus (Amersham Biosciences,Uppsala, Sweden). The IEF gel strips reswelled for 12 h at 30 V to remove high salt concentrations and to improve proteinentry into the gel. Then 200, 500, and 1000 V were applied for1 h each. Voltage was increased to 8000 V in 30 min and keptconstant at 8000 V for 12 h, resulting in a total of 100 300 Vh.Gel strips were equilibrated for 20 min each in an SDSequilibration buffer consisting of 50 mM Tris-HCl, pH 8.8, 6 Murea, 30% (v/v) glycerol, 2% (w/v) SDS, a few grains of bromophenol blue, and 1% (w/v) dithiothreitol or 2.5% (w/v)iodoacetamide, respectively. The second-dimension separation was performed using 12.5% polyacrylamide gels in the presenceof 0.1% (w/v) sodium dodecylsulfate. The gels were run at 30mA for 30 min and 100 mA for about 4 h in a 20 cm
×
20 cm water-cooled vertical electrophoresis apparatus (OWL, Woburn,MA). For image analysis, gels were stained by the “Blue silver”method, a sensitive Coomassie-based quantitative stain.
19
Briefly, gels were soaked overnight in 0.12% Coomassie BlueG-250, 10% phosphoric acid, 10% ammonium sulfate, and 20%methanol and destained the next day for 5
-
6 h.
Gel Image Analysis and Mass Spectrometry 
.
Gels werescanned, and images were analyzed using the Phoretix 2DExpression software (Nonlinear Dynamics, Newcastle-upon-Tyne, U.K.). Image analysis was performed as described.
20
Normalized spot volumes defined as integral of spot areamultiplied by optical densities were compared to normalizedmeans
(
standard deviations from 3 gels of each group by Student’s
test for unpaired data.
21
Spots of interest wereexcised and digested by trypsin for mass spectrometry (Centrefor Molecular Medicine, ZMMK, University of Cologne, Ger-many), and mass spectra were identified by searching the NCBInonredundant protein database with Mascot
22
(http:// www.matrixscience.com) as described elsewhere in detail.
23
Briefly, trypsinized protein samples were loaded onto prespot-ted AnchorChip targets which are stainless steel supportscoated with hydrophobic material equipped with an array of 384 circular interruptions (anchors) of 600 mm diameter(Bruker-Daltonics, Bremen, Germany). They were preparedusing 
R
-cyano-4-hydroxycinnamic acid (HCCA) as matrix, whereby 0.3 mL of analyte solution and 1.2 mL of matrix solution (0.3 g/L HCCA in ethanol/acetone
)
2:1) were appliedonto the anchors using an Investigator ProMS MALDI Spotting Robot (Genomic Solutions, Ann Arbor, MI). Samples wereallowed to air-dry at room temperature. Peptide mass spectra were obtained using an Ultraflex TOF/TOF (Bruker-Daltonics)in the fully automated reflectron TOF mode operated by theflexControl software. The mass spectrometer was equipped witha SCOUT-MALDI source for multisample handling, a pulsedUV laser, a two-stage gridless reflector, a 2 GHz digitizer, a LIFT-TOF/TOF unit to analyze fragment ions of selected peptide ions(see below), and multichannel-plate detectors for linear andreflector mode measurements. All measurements were carriedout in positive ionization mode using a reflector voltage of 20kV. The external instrument calibration was achieved using signals from [M 1 H]1 ions of the following reference standards(
m
/
): Bradykinin clip (1
-
7) mono 757.39916; Angiotensin IImono 1046.5418; Angiotensin I mono 1296.6848; Substance Pmono 1347.7354; Bombesin mono 1619.8223; Renin substratemono 1758.93261; adrenocorticotropic hormone (ACTH) clip(1
-
17) mono 2093.0862; ACTH clip (18
-
39) mono 2465.1983;and Somatostatin clip (28) mono 3147.4710. Fragment
m
/
spectra were obtained by integration over up to 2000 successivelaser pulses (
 f 
)
50 Hz). The spectra were calibrated using autodigestion peptide signals for trypsin (
m
/
842.5094,1045.5637, 2211.1040, and 2283.1802) as reference values and were the basis of mining the NCBI nonredundant database forprotein identification via Mascot query (Matrix Science, Lon-don, U.K.) with the following parameters: enzyme, trypsin;missed cleavages, 1; allowed modifications, carbamidomethyl(fixed) and methionine oxidation (variable); tolerance, 75 ppm,that is, mass measurement accuracies were typically 
(
75 ppm.The Mascot-delivered probability based score was regarded asa quality parameter for the correct identification.
22
Protein spotsthat could not successfully be identified with the previousmethod were additionally analyzed by peptide sequencing withthe same device, Ultraflex MALDI LIFT-TOF/TOF. Therefore,a high-resolution timed ion selector to separate selectedpeptide ions, a LIFT device for raising the potential energy of fragment ions, a velocity focusing stage with subsequentpostacceleration, and a postLIFT metastable suppressor device were used. For the analysis, up to five precursor ions wereselected. The ions were subjected initially to acceleration with8 kV in mass spectrometer step one, then selected using a timedion-gate, and finally energy-lifted to a voltage of 19 kV.Fragmentized ion species were then accelerated in the secondion source and analyzed in mass spectrometer step two,running in reflector mode. Mascot analysis of the obtainedspectra was performed with 0.8 Da tolerance, one missedcleavage, and carbamidomethyl and methionine oxidation asallowed modifications.
Reverse Transcription-Polymerase Chain Reaction (RT-PCR).
Neurospheres were harvested for total RNA extractionusing the RNeasy kit (Qiagen, Hilden, Germany). RNA wasreversely transcribed using the Omniscript RT kit (Qiagen,Hilden, Germany). Specific cDNA target sequences for GlycogenSynthase Kinase 3
β
(GSK3
 β
; NM_032080), forward, 5
-GGATCTGCCATCGAGACATT-3
; reverse, 5
-CCAACTGATCCA-CACCACTG-3
; Wnt5a (NM_022631), forward, 5
-TGGAGTGG-TAAATGCCATGA-3
; reverse, 5
-ATACTGTCCTGCGACCTGCT-3
; Wnt7a (XM_342723), forward, 5
-CCCGAACCCTCATGAACTTA-3
; reverse, 5
-TAGCCTGAGGGGCTGTCTTA-3
; and Bone Mor-phogenic Protein 4 (BMP4; NM_012827), forward, 5
-CC-TGGTAACCGAATGCTGAT-3
; reverse, 5
-TCCTCACAGTGTTG-
GSK3 
 β
Regulates Neural Stem Cell Differentiation
research articles
Journal of Proteome Research
Vol. 6, No. 3, 2007
1199
 
GCTCTG-3
were amplified by quantitative RT-PCR in theLightCycler 2.0 system (Roche, Mannheim, Germany) using theDNA Master SYBR Green I kit.
24
The amplification protocol was5 min initial denaturation at 94
°
C, 50 cycles of 5 s denaturation
Figure 1.
(A) Comparison of two-dimensional electropherograms of neurospheres in the presence of the GSK3
 β
inhibitor SB216763(green spots) compared to neurospheres differentiated in vitro (red spots). Overlaid spot images result in yellow spot color. Somedistinct protein isoforms are solely expressed in either of the groups, others are differentially expressed. (B) Three-dimensional close-up of spots identified as isoforms of the Collapsin response mediator protein-2 (CRMP-2). Whereas the main spot decreases, there isan isoform shift for other isoforms of CRMP-2: spot no. 76 decreases and spot no. 1392 appears at a new p
, indicating changes inphosphorylation.
Table 1.
Differentially Expressed Proteins during in Vitro Differentiation of Neurospheres Which Are Related to GSK3
 β
in the WntSignaling Pathway
GenBank annotationproteinabbrev.UniProtaccessionnumber remarkstheoreticalp
theoreticalMW (Da)fold-change(inhibitedvs control)
RuvB-like protein 1; Pontin 52 Ruvbl1 P60123 binds
β
-catenin 6.02 50524 1.47Proteasome subunit, alpha type 1 Psa1 P18420 degradates
β
-catenin 6.14 29784 1.6Rho GDP-dissociation inhibitor 1 Gdir Q99PT1 binds rho 5.12 23450 1.5Proteasome subunit, alpha type 6 Psa6 P34062 degradates
β
-catenin 6.35 27838 1.3Microtubule-associated proteinRP/EB family member 1Mare1 Q66HR2 binds APC 5.02 30168
-
2.3
a
Proteins were identified by two-dimensional gel electrophoresis and mass spectrometry (Figure 1). Spot volumes were compared by statistical tests (
<
0.05,
)
5 gels in each group). Results of the Hierarchical Cluster Analysis showed that 3 of the proteins (Ruvbl1, Psa1, and Psa6) are found in the samecluster.
researcharticles
Maurer et al.
1200 Journal of Proteome Research
Vol. 6, No. 3, 2007
of 00

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