Transplantation of Neural Precursors Derived from Induced Pluripotent Cells Preserve Perineuronal Nets and Stimulate Neural Plasticity in ALS Rats
Abstract
:1. Introduction
2. Results
2.1. Differentiation of NP-iPS in Culture
2.2. NP-iPS Transplantation Improves Motor Activity and Extends the Survival of SOD1 Rats
2.3. Spinally Grafted NP-iPS Are Neuroprotective and Do Not Cause Tumors
2.4. NP-iPS Graft Modifies Spinal PNN-, Neurotrophic-, and Apoptosis-Related Gene Expression
2.5. Intraspinally Grafted NP-iPS Normalizes Expression of PNN-Related Chondroitin Sulfate Proteoglycans in Terminal SOD1 Rats
3. Discussion
4. Materials and Methods
4.1. Culture of Human Induced Pluripotent Stem Cell-Derived Neural Precursors
4.2. Animals
4.3. Behavioral Testing
4.3.1. Grip Strength Test (GrST)
4.3.2. BBB Test
4.3.3. Rotarod
4.3.4. Thirty Second Test
- (I)
- NP-iPS transplantation into asymptomatic SOD1 rats (n = 9)
- (II)
- NP-iPS transplantation into symptomatic SOD1 rats (n = 14)
- (III)
- vehicle injection into SOD1symptomatic rats (n = 13)
- (IV)
- vehicle injection into wild type (WT) littermates (n = 7)
4.4. Intraspinal Transplantation of NP-iPS
4.5. Postoperative Care
4.6. Tissue Processing and Immunohistochemistry
4.7. Quantification of Motoneuron Staining in the Spinal Ventral Horns
4.8. Immunocytochemistry
4.9. Electrophoresis and Western Blotting (WB)
4.10. Gene Expression
4.11. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Abbreviations
acan | Aggrecan |
ALS | Amyotrophic lateral sclerosis |
BDNF | Brain derived neurotrophic factor |
Bcan | Brevican |
Casp-3 | Caspase-3 |
Casp-7 | Caspase-7 |
CSPGs | Chondroitin sulfate proteoglycans |
EAAT2 | Excitatory amino acid transporter2 |
EGF | Epidermal growth factor |
ECM | Extracellular matrix |
FGF | Fibroblast growth factor |
GFAP | Glial fibrillary acidic protein |
GRNP | Glial-rich neural precursor |
GrST | Grip strength test |
Has 1 | Hyaluronan synthase-1 |
ICC | Immunocytochemistry |
IHC | Immunohistochemistry |
iPSC | Induced pluripotent stem cells |
IGF-1 | Insulin growth factor-1 |
hapln-1 | Hyaluronan and proteoglycan link protein-1 |
MMP | Matrix metalloproteinase |
ADAMST-4 | Metalloproteinase with thrombospondin motifs four |
MNs | Motoneurons |
NF | Neurofilaments |
NGF | Nerve growth factor |
NP-iPS | Neural precursors derived from induced pluripotent stem cells |
PNN | Perineuronal nets |
SR | Serotonin |
SC | Stem cells |
SOD1 | Superoxide dismutase-1 |
TnR | Tenascin-R |
Tg | Transgenic animals |
VEGF | Vascular endothelial growth factor |
vcan | Versican |
WB | Western Blot |
WT | Wild type animal |
Appendix A
Weeks | BBB | Rotarod | GRST | Weight |
---|---|---|---|---|
23 | p ≤ 0.0221 | p = 0.054 | p = 0.08 | p = 0.2 |
24 | p ≤ 0.003 | p ≤ 0.0018 | p ≤ 0.024 | p = 0.055 |
25 | p ≤ 0.003 | p ≤ 0.0000004 | p ≤ 0.000061 | p = 0.10 |
26 | p ≤ 0.003 | p ≤ 0.0000004 | p ≤ 0.000061 | p = 0.20 |
27 | p ≤ 0.004 | p ≤ 0.0035 | p ≤ 0.000013 | p = 0.09 |
28 | p ≤ 0.024 | p ≤ 0.04 | p ≤ 0.022 | p = 0.1 |
29 | p ≤ 0.05 | p ≤ 0.014 | p ≤ 0.04 | p = 0.2 |
Weeks | BBB | Rotarod | GRST | Weight |
---|---|---|---|---|
23 | p = 0.2 | p = 0.53 | p = 0.37 | p = 0.6 |
24 | p ≤ 0.037 | p ≤ 0.21 | p ≤ 0.053 | p = 0.2 |
25 | p ≤ 0.021 | p ≤ 0.002 | p ≤ 0.011 | p = 0.5 |
26 | p ≤ 0.02 | p ≤ 0.032 | p ≤ 0.04 | p = 0.2 |
27 | p ≤ 0.0019 | p = 0.053 | p ≤ 0.0028 | p = 0.1 |
28 | p ≤ 0.012 | p ≤ 0.011 | p ≤ 0.012 | p = 0.5 |
29 | p ≤ 0.01 | p ≤ 0.026 | p ≤ 0.03 | p = 0.2 |
Appendix B
Appendix C
AB Name | Protein of Interest/Application | Species & Antibody Type | Concentrations | Manufacturer |
---|---|---|---|---|
AB1031 | Aggrecan/WB, IHC | Rabbit Polyclonal | 1:1000 | Millipore, Burlington, MA, USA |
12C5 | Versican/WB, IHC | Mouse monoclonal | 1:100 | DSHB, Iowa city, IA, USA |
Anti-Tenascin-R | Tenascin-R/WB, IHC | Goat polyclonal | 1:1000 | R&D Systems, Minneapolis, MN, USA |
1F6 | Neurocan/WB, IHC | Mouse monoclonal | 1:100 | DHSB |
Anti-Brevican | Brevican/WB, IHC | Mouse polyclonal | 1:100 | Abcam, Cambridge, MA, USA |
3F8 | Phosphacan/WB, IHC | Mouse monoclonal | 1:1000 | DHSB |
Anti-Crtl1 | Link protein-1/WB, IHC | Goat monoclonal | 1:1000 | R&D Systems |
Anti-NF200 | Neural filaments 200 kDa/IHC | Mouse monoclonal | 1:200 | Sigma-Aldrich, St. Louis, MO, USA |
SMI-32 | Nonphosphorylated neurofilament H/IHC | Mouse monoclonal | 1:1000 | Covance, Princeton, NJ, USA |
Anti-NeuN | Neural DNA/IHC | Rabbit monoclonal | 1:200 | Millipore |
Anti-MTC02 | Non-glycosylated protein component of human mitochondria/IHC | Mouse monoclonal | 1:200 | Abcam |
Anti-β-III tubulin | β-tubulin isotype III/IHC | Mouse monoclonal | Sigma-Aldrich | |
Anti-S100β | β chain/IHC/ICC | Rabbit polyclonal | 1:400 | DAKO Denmark, Glostrup, Denmark |
Anti-l-type Ca2+ CP α1C | L-type Ca2+ CP α1C/ICC | Rabbit polyclonal | 1:200 | Alomone Labs, Jerusalem, Israel |
Anti-N type Ca2+ CP α1B | N type Ca2+ CP α1B/ICC | Rabbit polyclonal | 1:200 | Alomone Labs |
Anti-P/Q-type Ca2+ CP α1A | P/Q-type Ca2+ CP α1A/ICC | Rabbit polyclonal | 1:200 | Alomone Labs |
Anti-Ryanodine Receptor 1 | Ryanodine Receptor 1/ICC | Rabbit polyclonal | 1:200 | Alomone Labs |
Anti-Ryanodine Receptor 2 | Ryanodine Receptor 2/ICC | Rabbit polyclonal | 1:200 | Alomone Labs |
Anti-Ryanodine Receptor 3 | Ryanodine Receptor 3/ICC | Rabbit polyclonal | 1:100 | Alomone Labs |
Anti-ORAI Receptor 1 | ORAI Receptor 1/ICC | Rabbit polyclonal | 1:200 | Alomone Labs |
Anti-ORAI Receptor 2 | ORAI Receptor 2/ICC | Rabbit polyclonal | 1:200 | Alomone Labs |
Anti-ORAI Receptor 3 | ORAI Receptor 3/ICC | Rabbit polyclonal | 1:1000 | Sigma-Aldrich |
Anti-Hepcidin | Hepcidin | Goat monoclonal | 1:200 | Dr. Raha-Chowdhury |
Anti-HB9 | HB9 homeobox transcription factor | Goat polyclonal | 1:200 | Santa Cruz Inc., Dallas, TX, USA |
Anti-SR | Serotonin | Goat polyclonal | 1:600 | Abcam |
Anti-ParAlb | PV 25 Rabbit anti Parvalbumin | Rabbit | 1.2000 | Swant, Marly, Switzerland |
NKx6.1 | NK homeodomain protein, Nkx6.1 | Mouse monoclonal | 1:20 | DSHB |
Anti-Islet1 | Islet 1- Neural Stem Cell Marker | Rabbit polyclonal | 1:500 | Abcam |
Anti-Islet2 | GST fusion from E. coli linker region of protein | Mouse | 1:20 | DSHB |
Anti-CHAT | Choline Acetyltransferase | Chicken polyclonal | 1:50 | Abcam |
Anti-Nestin | Anti-NESTIN | Mouse monoclonal | 1:2500 | Millipore, |
Anti-GFAP | Anti-glial fibrillary acidic protein | Mouse monoclonal | 1:1000 | Cell Signaling, Danvers, MA, USA |
Assay | Gene Name |
---|---|
Rn00573424_m1 | aggrecan |
Rn00581331_m1 | neurocan |
Rn00563814_m1 | brevican |
Rn00564869_m1 | tenascin-R |
Rn01493755_m1 | versican |
Rn00569884_m1 | hapln1 |
Rn99999125_m1 | bcl2 |
Rn00563902_m1 | casp3 |
Rn00573917_m1 | casp7 |
Rn01480161_g1 | bax |
Rn01533872_m1 | ngf |
Rn02531967_s1 | bdnf |
Rn 00710306_m1 | igf-1 |
Rn 00580526_m1 | ncam |
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Forostyak, S.; Forostyak, O.; Kwok, J.C.F.; Romanyuk, N.; Rehorova, M.; Kriska, J.; Dayanithi, G.; Raha-Chowdhury, R.; Jendelova, P.; Anderova, M.; et al. Transplantation of Neural Precursors Derived from Induced Pluripotent Cells Preserve Perineuronal Nets and Stimulate Neural Plasticity in ALS Rats. Int. J. Mol. Sci. 2020, 21, 9593. https://doi.org/10.3390/ijms21249593
Forostyak S, Forostyak O, Kwok JCF, Romanyuk N, Rehorova M, Kriska J, Dayanithi G, Raha-Chowdhury R, Jendelova P, Anderova M, et al. Transplantation of Neural Precursors Derived from Induced Pluripotent Cells Preserve Perineuronal Nets and Stimulate Neural Plasticity in ALS Rats. International Journal of Molecular Sciences. 2020; 21(24):9593. https://doi.org/10.3390/ijms21249593
Chicago/Turabian StyleForostyak, Serhiy, Oksana Forostyak, Jessica C. F. Kwok, Nataliya Romanyuk, Monika Rehorova, Jan Kriska, Govindan Dayanithi, Ruma Raha-Chowdhury, Pavla Jendelova, Miroslava Anderova, and et al. 2020. "Transplantation of Neural Precursors Derived from Induced Pluripotent Cells Preserve Perineuronal Nets and Stimulate Neural Plasticity in ALS Rats" International Journal of Molecular Sciences 21, no. 24: 9593. https://doi.org/10.3390/ijms21249593