Neuroectodermally converted human mesenchymal stromal cells provide cytoprotective effects on neural stem cells and inhibit their glial differentiation

References

• Curtis MA, Faull RL, Eriksson PS. The effect of neurodegenerative diseases on the subventricular zone. Nat Rev Neurosci. 2007;8:712–23.
   PubMedGoogle Scholar
• Jellinger KA. Cell death mechanisms in neurodegeneration. J Cell Mol Med. 2001;5:1–17.
   PubMed Web of Science ®Google Scholar
• Czyz J, Wiese C, Rolletschek A, Blyszczuk P, Cross M, Wobus AM. Potential of embryonic and adult stem cells in vitro. Biol Chem. 2003;384:1391–409.
   PubMed Web of Science ®Google Scholar
• Maherali N, Ahfeldt T, Rigamonti A, Utikal J, Cowan C, Hochedlinger K. A high-efficiency system for the generation and study of human induced pluripotent stem cells. Cell Stem Cell. 2008;3:340–5.
   PubMed Web of Science ®Google Scholar
• Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, . Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol. 2008;26:101–6.
   PubMed Web of Science ®Google Scholar
• Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.
   PubMed Web of Science ®Google Scholar
• Kang SK, Putnam LA, Ylostalo J, Popescu IR, Dufour J, Belousov A, . Neurogenesis of Rhesus adipose stromal cells. J Cell Sci. 2004;117:4289–99.
   PubMed Web of Science ®Google Scholar
• Safford KM, Safford SD, Gimble JM, Shetty AK, Rice HE. Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp Neurol. 2004; 187:319–28.
   PubMed Web of Science ®Google Scholar
• Fernandes KJ, McKenzie IA, Mill P, Smith KM, Akhavan M, Barnabe-Heider F, . A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol. 2004;6:1082–93.
   PubMed Web of Science ®Google Scholar
• Joannides A, Gaughwin P, Schwiening C, Majed H, Sterling J, Compston A, . Efficient generation of neural precursors from adult human skin: astrocytes promote neurogenesis from skin-derived stem cells. Lancet. 2004;364:172–8.
   PubMed Web of Science ®Google Scholar
• Bossolasco P, Montemurro T, Cova L, Zangrossi S, Calzarossa C, Buiatiotis S, . Molecular and phenotypic characterization of human amniotic fluid cells and their differentiation potential. Cell Res. 2006;16:329–36.
   PubMed Web of Science ®Google Scholar
• De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, . Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol. 2007;25:100–6.
   PubMed Web of Science ®Google Scholar
• Troyer DL, Weiss ML. Wharton's jelly-derived cells are a primitive stromal cell population. Stem Cells. 2008;26:591–9.
   PubMed Web of Science ®Google Scholar
• Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, . Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol. 2000; 164:247–56.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Henderson D, Blackstad M, Chen A, Miller RF, Verfaillie CM. Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc Natl Acad Sci USA. 2003;100(Suppl 1):11854–60.
   PubMedGoogle Scholar
• Buzanska L, Machaj EK, Zablocka B, Pojda Z, Domanska-Janik K. Human cord blood-derived cells attain neuronal and glial features in vitro. J Cell Sci. 2002;115:2131–8.
   PubMed Web of Science ®Google Scholar
• Sanchez-Ramos JR. Neural cells derived from adult bone marrow and umbilical cord blood. J Neurosci Res. 2002; 69:880–93.
   PubMed Web of Science ®Google Scholar
• Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res. 2000;61:364–70.
   PubMed Web of Science ®Google Scholar
• Dezawa M, Kanno H, Hoshino M, Cho H, Matsumoto N, Itokazu Y, . Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J Clin Invest. 2004;113:1701–10.
   PubMed Web of Science ®Google Scholar
• Hermann A, Gastl R, Liebau S, Popa MO, Fiedler J, Boehm BO, . Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci. 2004;117:4411–22.
   PubMed Web of Science ®Google Scholar
• Hermann A, Liebau S, Gastl R, Fickert S, Habisch HJ, Fiedler J, . Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using various conversion protocols. J Neurosci Res. 2006; 83:1502–14.
   PubMed Web of Science ®Google Scholar
• Fu L, Zhu L, Huang Y, Lee TD, Forman SJ, Shih CC. Derivation of neural stem cells from mesenchymal stem cells: evidence for a bipotential stem cell population. Stem Cells Dev. 2008;17:1109–21.
   PubMed Web of Science ®Google Scholar
• Prockop DJ. ‘Stemness’ does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin Pharmacol Ther. 2007;82:241–3.
   PubMed Web of Science ®Google Scholar
• Habisch HJ, Fiedler J, Ludolph AC, Storch A, Brenner RE. Altered migration and adhesion potential of pro-neurally converted human bone marrow stromal cells. Cytotherapy. 2008;10:824–33.
   PubMed Web of Science ®Google Scholar
• Habisch HJ, Janowski M, Binder D, Kuzma-Kozakiewicz M, Widmann A, Habich A, . Intrathecal application of neuroectodermally converted stem cells into a mouse model of ALS: limited intraparenchymal migration and survival narrows therapeutic effects. J Neural Transm. 2007;114: 1395–40.
   PubMed Web of Science ®Google Scholar
• Janowski M, Kuzma-Kozakiewicz M, Binder D, Habisch HJ, Habich A, Lukomska B, . Neurotransplantation in mice: the concorde-like position ensures minimal cell leakage and widespread distribution of cells transplanted into the cisterna magna. Neurosci Lett. 2008;430:169–74.
   PubMedGoogle Scholar
• Habisch HJ, Schmid B, Arnim C, Ludolph AC, Brenner R, Storch A. Efficient processing of Alzheimer's disease amyloid-beta peptides by neuroectodermally converted mesenchymal stem cells. Stem Cells Dev. 2009; doi 10.1089/scd.2009.045.
   Google Scholar
• Liebau S, Vaida B, Storch A, Boeckers TM. Maturation of synaptic contacts in differentiating neural stem cells. Stem Cells. 2007;25:1720–9.
   PubMed Web of Science ®Google Scholar
• Maisel M, Herr A, Milosevic J, Hermann A, Habisch HJ, Schwarz S, . Transcription profiling of adult and fetal human neuroprogenitors identifies divergent paths to maintain the neuroprogenitor cell state. Stem Cells. 2007;25:1231–40.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402–8.
   PubMed Web of Science ®Google Scholar
• Hermann A, Maisel M, Wegner F, Liebau S, Kim DW, Gerlach M, . Multipotent neural stem cells from the adult tegmentum with dopaminergic potential develop essential properties of functional neurons. Stem Cells. 2006; 24:949–64.
   PubMed Web of Science ®Google Scholar
• Storch A, Kaftan A, Burkhardt K, Schwarz J. 6-Hydroxydopamine toxicity towards human SH-SY5Y dopaminergic neuroblastoma cells: independent of mitochondrial energy metabolism. J Neural Transm. 2000;107:281–93.
   PubMed Web of Science ®Google Scholar
• Milosevic J, Storch A, Schwarz J. Spontaneous apoptosis in murine free-floating neurospheres. Exp Cell Res. 2004; 294:9–17.
   PubMedGoogle Scholar
• Kuan CY, Schloemer AJ, Lu A, Burns KA, Weng WL, Williams MT, . Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J Neurosci. 2004;24:10763–72.
   PubMed Web of Science ®Google Scholar
• Rakic P. Adult neurogenesis in mammals: an identity crisis. J Neurosci. 2002;22:614–8.
   PubMed Web of Science ®Google Scholar
• Bauer S, Patterson PH. The cell cycle-apoptosis connection revisited in the adult brain. J Cell Biol. 2005;171: 641–50.
   PubMedGoogle Scholar
• Hamanoue M, Takemoto N, Matsumoto K, Nakamura T, Nakajima K, Kohsaka S. Neurotrophic effect of hepatocyte growth factor on central nervous system neurons in vitro. J Neurosci Res. 1996;43:554–64.
   PubMed Web of Science ®Google Scholar
• Koike H, Ishida A, Shimamura M, Mizuno S, Nakamura T, Ogihara T, . Prevention of onset of Parkinson's disease by in vivo gene transfer of human hepatocyte growth factor in rodent model: a model of gene therapy for Parkinson's disease. Gene Ther. 2006;13:1639–44.
   PubMedGoogle Scholar
• Hayashi K, Morishita R, Nakagami H, Yoshimura S, Hara A, Matsumoto K, . Gene therapy for preventing neuronal death using hepatocyte growth factor: in vivo gene transfer of HGF to subarachnoid space prevents delayed neuronal death in gerbil hippocampal CA1 neurons. Gene Ther. 2001;8:1167–73.
   PubMedGoogle Scholar
• Sun W, Funakoshi H, Nakamura T. Overexpression of HGF retards disease progression and prolongs life span in a transgenic mouse model of ALS. J Neurosci. 2002;22: 6537–48.
   PubMed Web of Science ®Google Scholar
• Forte G, Minieri M, Cossa P, Antenucci D, Sala M, Gnocchi V, . Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells. 2006;24:23–33.
   PubMed Web of Science ®Google Scholar
• Son BR, Marquez-Curtis LA, Kucia M, Wysoczynski M, Turner AR, Ratajczak J, . Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells. 2006;24:1254–64.
   PubMed Web of Science ®Google Scholar
• Neuss S, Becher E, Woltje M, Tietze L, Jahnen-Dechent W. Functional expression of HGF and HGF receptor/c-met in adult human mesenchymal stem cells suggests a role in cell mobilization, tissue repair, and wound healing. Stem Cells. 2004;22:405–14.
   PubMed Web of Science ®Google Scholar
• Wang M, Crisostomo PR, Herring C, Meldrum KK, Meldrum DR. Human progenitor cells from bone marrow or adipose tissue produce VEGF, HGF, and IGF-I in response to TNF by a p38 MAPK-dependent mechanism. Am J Physiol Regul Integr Comp Physiol. 2006;291:R880–4.
   PubMed Web of Science ®Google Scholar
• Chen X, Li Y, Wang L, Katakowski M, Zhang L, Chen J, . Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology. 2002;22:275–9.
   PubMed Web of Science ®Google Scholar
• Munoz JR, Stoutenger BR, Robinson AP, Spees JL, Prockop DJ. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci USA. 2005;102:18171–6.
   PubMed Web of Science ®Google Scholar
• Kato M, Yoshimura S, Kokuzawa J, Kitajima H, Kaku Y, Iwama T, . Hepatocyte growth factor promotes neuronal differentiation of neural stem cells derived from embryonic stem cells. Neuroreport. 2004;15:5–8.
   PubMedGoogle Scholar
• Hermann A, Maisel M, Liebau S, Gerlach M, Kleger A, Schwarz J, . Mesodermal cell types induce neurogenesis from adult human hippocampal progenitor cells. J Neurochem. 2006;98:629–40.
   PubMed Web of Science ®Google Scholar
• Croft AP, Przyborski SA. Mesenchymal stem cells expressing neural antigens instruct a neurogenic cell fate on neural stem cells. Exp Neurol. 2009;216:329–41.
   Google Scholar
• Wislet-Gendebien S, Bruyere F, Hans G, Leprince P, Moonen G, Rogister B. Nestin-positive mesenchymal stem cells favour the astroglial lineage in neural progenitors and stem cells by releasing active BMP4. BMC Neurosci. 2004;5:33.
   PubMed Web of Science ®Google Scholar
• Rivera FJ, Couillard-Despres S, Pedre X, Ploetz S, Caioni M, Lois C, . Mesenchymal stem cells instruct oligodendrogenic fate decision on adult neural stem cells. Stem Cells. 2006;24:2209–19.
   PubMed Web of Science ®Google Scholar
• Hokari M, Kuroda S, Shichinohe H, Yano S, Hida K, Iwasaki Y. Bone marrow stromal cells protect and repair damaged neurons through multiple mechanisms. J Neurosci Res. 2008;86:1024–35.
   PubMed Web of Science ®Google Scholar
• Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA. 2002;99:11946–50.
   PubMed Web of Science ®Google Scholar
• Azzouz M, Ralph GS, Storkebaum E, Walmsley LE, Mitrophanous KA, Kingsman SM, . VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature. 2004;429:413–7.
   PubMed Web of Science ®Google Scholar
• Yasuhara T, Shingo T, Kobayashi K, Takeuchi A, Yano A, Muraoka K, . Neuroprotective effects of vascular endothelial growth factor (VEGF) upon dopaminergic neurons in a rat model of Parkinson's disease. Eur J Neurosci. 2004;19:1494–504.
   PubMed Web of Science ®Google Scholar
• Schänzer A, Wachs FP, Wilhelm D, Acker T, Cooper-Kuhn C, Beck H, . Direct stimulation of adult neural stem cells in vitro and neurogenesis in vivo by vascular endothelial growth factor. Brain Pathol. 2004;14:237–48.
   PubMed Web of Science ®Google Scholar
• Ben-Ami I, Freimann S, Armon L, Dantes A, Ron-El R, Amsterdam A. Novel function of ovarian growth factors: combined studies by DNA microarray, biochemical and physiological approaches. Mol Hum Reprod. 2006;12:413–9.
   PubMedGoogle Scholar
• Xian CJ. Roles of epidermal growth factor family in the regulation of postnatal somatic growth. Endocr Rev. 2007;28:284–96.
   PubMed Web of Science ®Google Scholar
• Falk A, Frisen J. Amphiregulin is a mitogen for adult neural stem cells. J Neurosci Res. 2002;69:757–62.
   PubMedGoogle Scholar
• Kimura H, Schubert D. Schwannoma-derived growth factor promotes the neuronal differentiation and survival of PC12 cells. J Cell Biol. 1992;116:777–83.
   PubMed Web of Science ®Google Scholar