6. Materials And Methods
6.1. Mesenchymal Stem Cells (MSCs) isolation and expansion
Mice were sacrificed by cervical dislocation before extracting bones (both tibias
and femurs). MSCs were isolated from bone marrow (BM), flushed out from
tibias and femurs.
BM was seeded in Complete Medium, composed by MesenCult Basal Medium
supplemented with 20% Mesenchymal Mouse Stimulatory Supplement
(StemCell Technologies) and 1% Pen-Strept (Life Technologies). Cells were
seeded and grown at 37°C in humidified atmosphere at 5% CO
2.
MSCs adhere to plastic, and such criterion was used to distinguish them from
the BM hematopoietic component, which grows in suspension. In addition, the
use of MesenCult medium ensured a proper selection of the MSC component,
since it specifically support MSCs growth. Medium was changed every 3 days.
Once adherent cells reached confluence, they were removed from the culture
dishes by using Trypsin 1x (Life Technoligies) for 6 minutes, and subsequently
spun at 1250 rpm for 5 minutes.
Cells were resuspended in Complete Medium, counted on a Burker chamber
and subsequently reseeded at 2x10^4 cells/cm
2(passage 1, p1).
A second passage in culture was adopted to further eliminate the hematopoietic
component, and to expand further the MSC population, in order to obtain a
sufficient number of cells to perform the subsequent experiments. All
experiments were started at passage 2 (p2).
6.1.1. Adipogenic differentiation
MSCs were seeded at p2 at 2x10^4 cells/cm
2. Once cells reached 80%
confluence, the Complete Medium originally used to maintain their
proliferation was replaced with Adipogenic Induction Medium, composed of
MesenCult Basal Medium supplemented with 20% Adipogenic Stimulatory
Supplement (StemCell Technologies) and 1% Pen-Strept (Life Technologies).
Cells were collected at different time points during adipogenic differentiation
(after 1, 2, 3, 5, 7 and 14 days), centrifuged at 4500 rpm for 5 minutes and their
corresponding pellets stored at -80°C.
6.1.2. Osteogenic differentiation
MSCs were seeded at p2 at 2x10^4 cells/cm
2. Once cells reached 100%
confluence, the Complete Medium initially used to maintain their proliferation
was replaced with Osteogenic Induction Medium, composed of MesenCult
Basal Medium supplemented with 20% Osteogenic Stimulatory Supplement
(StemCell Technologies) and 1% Pen-Strept (Life Technologies).
Cells were collected at different time points during osteogenic differentiation
(after 1, 2, 3, 5, 7, 14 and 21 days), centrifuged at 4500 rpm for 5 minutes and
their pellets stored at -80°C.
6.1.3. Cytochemical Staining
At the end of adipogenic and osteogenic differentiation, cells were stained to
evaluate the efficiency of their induced differentiation.
Oil Red O staining was performed on terminally differentiated adipocytes. Oil
Red O labels lipid droplets present in the cytoplasm of mature adipocytes.
A staining stock solution was prepared by dissolving 0,25g Oil Red O (Sigma)
in 50ml isopropyl alcohol. A fresh working solution was prepared each time, by
adding PBS 1x to the stock solution (3 parts of Oil Red stock + 2 parts of PBS
1x).
Alizarin Red S staining was performed on terminally differentiated osteoblasts.
Alizarin Red S dyes the calcium phosphate secreted by mature osteoblasts
during bone mineralization.
A stock/working solution was prepared by dissolving 0,5g Alizarin Red S
(Sigma) in 50 ml H
2O, and pH was brought to 4.1-4.3.
Each working solution was filtered through 0.22µm filters before use in order to
remove debris.
Cells were fixed with 4% formaldehyde for 20 minutes at Room Temperature
(RT), stained for 15 minutes in the dark, and subsequently washed with distilled
water.
6.2. RNA extraction
RNA was extracted from frozen cell pellets by using the NucleoSpin® RNA
XS kit (Macherey-Nagel), which allows for the isolation of highly concentrated
and pure RNA from small samples. This kit uses silica membrane technology.
Briefly, cells are lysed by incubation in a solution containing large amounts of
chaotropic ions. The lysis buffer immediately inactivates the RNases virtually
present in every biological sample, and creates the appropriate binding
conditions to favour absorption of RNA to the silica membrane. After lysis,
homogenization and reduction of viscosity are achieved by filtration with
NucleoSpin® Filter units. Residual genomic DNA is efficiently eliminated by
digestion with rDNase, provided by the kit. Each step of the RNA extraction
was performed according to the manufacture’s protocol.
RNA concentration was measured with NanoVue Plus Spectrophotometer.
Briefly,
1
µl
of each sample was exposed to ultraviolet light at 260 nm, and a
photo-detector measured the light passing through the sample. The more light
absorbed by the sample, the higher the nucleic acid concentration.
It is common
for nucleic acid samples to be contaminated with other molecules (i.e. proteins
or organic compounds). The ratio of the absorbance at 260 and 280nm (A
260/280)
is used to assess the purity of nucleic acids from proteins, whereas A
260/230is
used to assess the purity from carbohydrates and phenols (solvents). We always
utilized RNA of the highest purity (with reading of A
260/280=1,9 and A
260/230=
2).
6.3. cDNA sytnthesis
Reverse transcription of RNA was performed using the QuantiTect Reverse
Transcription Kit (Qiagen), accordingly to manufacture’s protocol. Purified
RNA was briefly incubated in gDNA Wipeout Buffer to effectively remove
contaminating genomic DNA. The RNA sample was then used directly in a
reverse transcription reaction, using a master mix composed of Quantiscript
Reverse Transcriptase, Quantiscript RT Buffer, and RT Primer Mix. The entire
reaction was carried out at 42°C and it was subsequently inactivated at 95°C.
6.4. Real Time qPCR
Real Time qPCR was performed by using the QuantiTect SYBR Green PCR
Kits, which contains a ready-to-use master mix, composed of HotStart Taq
DNA Polymerase, SYBR Green PCR Buffer, SYBR Green I, and dNTPs. The
fluorescent dye SYBR Green I intercalates in the minor groove of the double
DNA strand. The stronger the fluorescence released, the higher the DNA
quantity. Abalanced combination of K
+and NH
4+ions in the PCR buffer
promotes specific primer annealing and enables high PCR specificity and
sensitivity. In addition,HotStarTaq DNA Polymerase provides a stringent hot
start, preventing the formation of non-specific products.
Samples were prepared in 15 µl total volume, containing SyBR Green I Master
mix 1X, forward and reverse primers (0,3µM) specific for each gene. Primers
were designed and verified by using the Beacon Designer 5.0 and the Primer3
Software, respectively.
Real Time qPCR reaction was run on a Rotor Gene 3000 (Corbett). Data were
normalized to the levels of the housekeeping gene Hprt.
6.5. Protein Extraction
Protein extraction was performed by using a freshly prepared lysis buffer
working solution, composed of RIPA Buffer stock solution, 1%NP40 (Igepal
CA-630), 1 mM PMSF (
PhenylmethylsulfonylFluoride)
, 1% Protease Inhibitor
(ProteaseInhibitor Cocktail Tablets, cOmplete Mini, Roche). RIPA Stock
Buffer is composed of H
2O, 50mM Tris HCL, 150 mM NaCl, 1mM EDTA, 1%
SDS, 0,5% DOC, and stored at 4°C. Cell pellets were resuspended on ice in 50
µl lysis buffer working solution and incubated on ice for 30 minutes. After
incubation cells were sonicated 3 times (10 seconds @ power 7), with Misonix
Microson 22000 and centrifuged 10 minutes at 6000 rcf at 4°C. Supernatants,
which contain the protein extracts, were transferred to clean tubes, and stored at
-80°C.
Protein concentration was evaluated by using the Micro BCA
TMProtein Assay
kit (ThermoScientific), according to manufacture’s datasheet.
The Thermo Scientific Pierce Micro BCA Protein Assay can be used on a
spectrophotometer (A 562nm) to measure total protein concentration of diluted
protein solutions (ranging from 0,5 to 20µg/mL).
6.6. Western Blot
After protein extraction 30µg of the protein homogenates were mixed with
Loading Buffer (Loading Buffer 4x was composed of Tris-HCl pH 6.8,
β-mercaptoethanol, SDS, Glycerol, bromophenol blue, Milli-Q-H
2O) and
incubated at 99°C for 10 minutes. This incubation allows for protein
denaturation, which is necessary to obtain a correct separation by
electrophoresis. Proteic lysates were then separated by SDS-PAGE (Sodium
Dodecyl Sulfate-Polyacrylamide Gel Electrophoresis) and transferred to PVDF
membranes (at 200mA for 2 hours). Upon incubation with primary and
secondary antibodies, immunoreactive bands were detected by ECL reaction
(Millipore), according to manufacturer’s datasheet.
-The primary antibodies utilized in our study were:
Mouse anti-Prep1 (Santa Cruz Biotechnology sc-25282, 200µg/ml), dilution
1:1000.
Rabbit anti-Pbx1 (Santa Cruz Biotechnology, sc-889, 200µg/ml), dilution
1:500.
Goat anti-Meis1/2 (Santa Cruz Biotechnology, sc-10599, 200µg/ml), dilution
1:500.
Rabbit anti-Cytoskeletal Actin (Bethyl Laboratories A300-485A, 1mg/ml),
dilution 1:10000.
-the secondary antibodies utilized in our study were:
Goat Anti-Mouse HRP (Santa Cruz Biotechnology, sc-2005, 200µg/0,5ml),
dilution 1:1000
Goat Anti-Rabbit HRP (Santa Cruz Biotechnology, sc-2004, 400µg/ml),
dilution 1:1500
Donkey Anti-Goat HRP (Santa Cruz Biotechnology, sc-2033, 200µg/0,5ml),
dilution 1:2000
Upon development of the films, pixel intensity of the resulting bands was
quantified by using ImageJ Software.
6.7. Flow Cytometry Analysis
Flow cytometry analysis was performed on a FACSCalibur
TMflow cytometer.
Cells were resuspended in staining solution (PBS 1X, 1% FBS (Fetal Bovine
Serum) and stained with Phycoerythrin (PE) conjugated anti-mouse Kit-PE
(1:10) (Anti-Mouse CD117-PE 0,2mg/ml eBioscience, #12-1171)
Cells were stained for 30 minutes at 4°C in the dark, then washed twice with
PBS 1x and analyzed by flow cytometry.
Results were analyzed by using FlowJo Software.
6.8. Detection of apoptosis
In order to quantify apoptotic cells we took advantage of two different
tecniques, namely the TUNEL assay and Annexin V- PI staining (FACS
analysis), as explained below.
6.8.1. TUNEL assay:
The In Situ Cell Death Detection Kit Fluorescein (Roche) is based on the
detection of single- and double-stranded DNA breaks that occur at the early
stages of apoptosis. Apoptotic cells are fixed and permeabilized. Subsequently,
cells are incubated with the TUNEL reaction mixture that contains TdT and
fluorescein-dUTP. During this incubation period, TdT catalyzes the addition of
fluorescein-dUTP to the free 3'-OH groups of single- and double-stranded
DNA. After washing, the label incorporated at the damaged sites of the DNA is
visualized by fluorescence microscopy.
6.8.2. Annexin V and PI staining
Apoptosis was detect by using a detection Kit purchased from BD Pharmingen
(FITC Annexin V Apoptosis Kit). In apoptotic cells, the membrane
phospholipid phosphatidylserine (PS) is translocated from the inner to the outer
leaflet of the plasma membrane, thereby exposing PS to the external cellular
environment. Annexin V (conjugated to the fluorochromes FITC) is a 35-36
kDa Ca2
+-dependent phospholipid-binding protein with high affinity to PS,
binding therefore cells with exposed PS, thus constituting a sensitive probe for
flow cytometric analysis of apoptotic cells. Briefly, cells are incubated for 15
minutes in the dark at room temperature with the staining solution (Binding
Buffer 1X, FITC Annexin V and Propidium Iodide (PI)) and then analyzed on a
cytometer (FACSCalibur
TM). FITC Annexin V stains both early apoptotic and
completely apoptotic cells. Viable cells with intact membranes exclude PI,
whereas the membranes of dead and damaged cells are permeable to PI. Cells
that are considered viable are FITC Annexin V and PI negative; cells that are in
early apoptosis are Annexin V positive and PI negative; and cells that are in late
apoptosis or already dead are double positive for Annexin V and PI.
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