Genome-wide expression profiling and functional network analysis upon neuroectodermal conversion of human mesenchymal stem cells suggest HIF-1 and miR-124a as important regulators

Experimental Cell Research

Volumn 316, Issue 17, 2010, Pages 2760-2778

  Maisel, Martina ^a,d   Habisch, Hans Jörg ^b   Royer, Loïc ^a   Herr, Alexander ^a   Milosevic, Javorina ^c   Hermann, Andreas ^a,e   Liebau, Stefan ^b   Brenner, Rolf ^b   Schwarz, Johannes ^c   Schroeder, Michael ^a,e   Storch, Alexander ^a,e  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF ULM   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

Gene expression profile

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; MICRORNA; MIR 124A; UNCLASSIFIED DRUG; MIRN124 MICRORNA, HUMAN;

ADULT; ARTICLE; BIOINFORMATICS; CELL POPULATION; CHROMOSOME 4; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GERM LAYER; HUMAN; HUMAN CELL; IN VITRO STUDY; MARKER GENE; MESENCHYMAL STEM CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; REGULATORY MECHANISM; UPREGULATION; ADOLESCENT; BONE MARROW CELL; CELL CULTURE; CELL LINEAGE; CYTOLOGY; GENE REGULATORY NETWORK; GENETICS; HUMAN GENOME; MESENCHYMAL STROMA CELL; NERVE CELL; NEUROECTODERM; STEM CELL; YOUNG ADULT;

ADOLESCENT; ADULT; BONE MARROW CELLS; CELL LINEAGE; CELLS, CULTURED; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENOME, HUMAN; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; MESENCHYMAL STROMAL CELLS; MICRORNAS; NEURAL PLATE; NEURONS; STEM CELLS; YOUNG ADULT;

EID: 77956883998     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.06.012     Document Type: Article

References (92)

1. Bianco P., Riminucci M., Gronthos S., Robey P.G. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 2001, 19:180-192.
2. Vogel W., Grunebach F., Messam C.A., Kanz L., Brugger W., Buhring H.J. Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells. Haematologica 2003, 88:126-133.
3. Tondreau T., Lagneaux L., Dejeneffe M., Massy M., Mortier C., Delforge A., Bron D. Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation 2004, 72:319-326.
4. Friedenstein A.J., Gorskaja J.F., Kulagina N.N. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp. Hematol. 1976, 4:267-274.
5. Reyes M., Lund T., Lenvik T., Aguiar D., Koodie L., Verfaillie C.M. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 2001, 98:2615-2625.
6. Sekiya I., Larson B.L., Smith J.R., Pochampally R., Cui J.G., Prockop D.J. Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 2002, 20:530-541.
7. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D., Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
8. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A., Verfaillie C.M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
9. Sanchez-Ramos J., Song S., Cardozo-Pelaez F., Hazzi C., Stedeford T., Willing A., Freeman T.B., Saporta S., Janssen W., Patel N., Cooper D.R., Sanberg P.R. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp. Neurol. 2000, 164:247-256.
10. Woodbury D., Schwarz E.J., Prockop D.J., Black I.B. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 2000, 61:364-370.
11. Dezawa M., Kanno H., Hoshino M., Cho H., Matsumoto N., Itokazu Y., Tajima N., Yamada H., Sawada H., Ishikawa H., Mimura T., Kitada M., Suzuki Y., Ide C. Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J. Clin. Invest. 2004, 113:1701-1710.
12. Hermann A., Gastl R., Liebau S., Popa M.O., Fiedler J., Boehm B.O., Maisel M., Lerche H., Schwarz J., Brenner R., Storch A. Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J. Cell Sci. 2004, 117:4411-4422.
13. Hermann A., Liebau S., Gastl R., Fickert S., Habisch H.J., Fiedler J., Schwarz J., Brenner R., Storch A. Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using various conversion protocols. J. Neurosci. Res. 2006, 83:1502-1514.
14. Fu L., Zhu L., Huang Y., Lee T.D., Forman S.J., Shih C.C. Derivation of neural stem cells from mesenchymal stemcells: evidence for a bipotential stem cell population. Stem Cells Dev. 2008, 17:1109-1121.
15. Zeng Z., Yuan X., Liu G., Zeng X., Zeng X., Ng H., Chen H., Jiang T., Akasaki Y., Kessey K., Black K.L., Yu J.S. Manipulation of proliferation and differentiation of human bone marrow-derived neural stem cells in vitro and in vivo. J. Neurosci. Res. 2007, 85:310-320.
16. Lee J., Elkahloun A.G., Messina S.A., Ferrari N., Xi D., Smith C.L., Cooper R., Albert P.S., Fine H.A. Cellular and genetic characterization of human adult bone marrow-derived neural stem-like cells: a potential antiglioma cellular vector. Cancer Res. 2003, 63:8877-8889.
17. Kang S.K., Putnam L.A., Ylostalo J., Popescu I.R., Dufour J., Belousov A., Bunnell B.A. Neurogenesis of Rhesus adipose stromal cells. J. Cell Sci. 2004, 117:4289-4299.
18. Bunnell B.A., Ylostalo J., Kang S.K. Common transcriptional gene profile in neurospheres-derived from pATSCs, pBMSCs, and pNSCs. Biochem. Biophys. Res. Commun. 2006, 343:762-771.
19. Yang Q., Mu J., Li Q., Li A., Zeng Z., Yang J., Zhang X., Tang J., Xie P. A simple and efficient method for deriving neurospheres from bone marrow stromal cells. Biochem. Biophys. Res. Commun. 2008, 372:520-524.
20. Sauerzweig S., Munsch T., Lessmann V., Reymann K.G., Braun H. A population of serum deprivation-induced bone marrow stem cells (SD-BMSC) expresses marker typical for embryonic and neural stem cells. Exp. Cell Res. 2009, 315:50-66.
21. Fickert S., Fiedler J., Brenner R.E. Identification, quantification and isolation of mesenchymal progenitor cells from osteoarthritic synovium by fluorescence automated cell sorting. Osteoarthritis Cartilage 2003, 11:790-800.
22. Fiedler J., Roderer G., Gunther K.P., Brenner R.E. BMP-2, BMP-4, and PDGF-bb stimulate chemotactic migration of primary human mesenchymal progenitor cells. J. Cell. Biochem. 2002, 87:305-312.
23. Toma J.G., Akhavan M., Fernandes K.J., Barnabe-Heider F., Sadikot A., Kaplan D.R., Miller F.D. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat. Cell Biol. 2001, 3:778-784.
24. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
25. Matera A.G., Terns R.M., Terns M.P. Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat. Rev. Mol. Cell Biol. 2007, 8:209-220.
26. Milosevic J., Schwarz S.C., Maisel M., Poppe-Wagner M., Dieterlen M.T., Storch A., Schwarz J. Dopamine D2/D3 receptor stimulation fails to promote dopaminergic neurogenesis of murine and human midbrain-derived neural precursor cells in vitro. Stem Cells Dev. 2007, 16:625-635.
27. Milosevic J., Adler I., Manaenko A., Schwarz S.C., Walkinshaw G., Arend M., Flippin L.A., Storch A., Schwarz J. Non-hypoxic stabilization of hypoxia-inducible factor alpha (HIF-alpha): relevance in neural progenitor/stem cells. Neurotox. Res. 2009, 15:367-380.
28. Su A.I., Cooke M.P., Ching K.A., Hakak Y., Walker J.R., Wiltshire T., Orth A.P., Vega R.G., Sapinoso L.M., Moqrich A., Patapoutian A., Hampton G.M., Schultz P.G., Hogenesch J.B. Large-scale analysis of the human and mouse transcriptomes. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:4465-4470.
29. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., Speed T.P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
30. Tusher V.G., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5116-5121.
31. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., Sturn A., Snuffin M., Rezantsev A., Popov D., Ryltsov A., Kostukovich E., Borisovsky I., Liu Z., Vinsavich A., Trush V., Quackenbush J. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
32. Maisel M., Herr A., Milosevic J., Hermann A., Habisch H.J., Schwarz S., Kirsch M., Antoniadis G., Brenner R., Hallmeyer-Elgner S., Lerche H., Schwarz J., Storch A. Transcription profiling of adult and fetal human neuroprogenitors identifies divergent paths to maintain the neuroprogenitor cell state. Stem Cells 2007, 25:1231-1240.
33. Kent W.J., Sugnet C.W., Furey T.S., Roskin K.M., Pringle T.H., Zahler A.M., Haussler D. The human genome browser at UCSC. Genome Res. 2002, 12:996-1006.
34. Matys V., Kel-Margoulis O.V., Fricke E., Liebich I., Land S., Barre-Dirrie A., Reuter I., Chekmenev D., Krull M., Hornischer K., Voss N., Stegmaier P., Lewicki-Potapov B., Saxel H., Kel A.E., Wingender E. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 2006, 34:D108-D110.
35. Royer L., Reimann M., Andreopoulos B., Schroeder M. Unraveling protein networks with power graph analysis. PLoS Comput. Biol. 2008, 4:e1000108.
36. Mishra G.R., Suresh M., Kumaran K., Kannabiran N., Suresh S., Bala P., Shivakumar K., Anuradha N., Reddy R., Raghavan T.M., Menon S., Hanumanthu G., Gupta M., Upendran S., Gupta S., Mahesh M., Jacob B., Mathew P., Chatterjee P., Arun K.S., Sharma S., Chandrika K.N., Deshpande N., Palvankar K., Raghavnath R., Krishnakanth R., Karathia H., Rekha B., Nayak R., Vishnupriya G., Kumar H.G., Nagini M., Kumar G.S., Jose R., Deepthi P., Mohan S.S., Gandhi T.K., Harsha H.C., Deshpande K.S., Sarker M., Prasad T.S., Pandey A. Human protein reference database-2006 update. Nucleic Acids Res. 2006, 34:D411-D414.
37. Moodbidri M.S., Shirsat N.V. Induction of BAALC and down regulation of RAMP3 in astrocytes treated with differentiation inducers. Cell Biol. Int. 2006, 30:210-213.
38. Marcinkiewicz M., Touraine P., Chretien M. Pan-neuronal mRNA expression of the secretory polypeptide 7B2. Neurosci. Lett. 1994, 177:91-94.
39. Werner H., Dimou L., Klugmann M., Pfeiffer S., Nave K.A. Multiple splice isoforms of proteolipid M6B in neurons and oligodendrocytes. Mol. Cell. Neurosci. 2001, 18:593-605.
40. Maxwell P.H., Wiesener M.S., Chang G.W., Clifford S.C., Vaux E.C., Cockman M.E., Wykoff C.C., Pugh C.W., Maher E.R., Ratcliffe P.J. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399:271-275.
41. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., Kaelin W.G. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001, 292:464-468.
42. Cheng L.C., Pastrana E., Tavazoie M., Doetsch F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 2009, 12:399-408.
43. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., Bartel D.P., Linsley P.S., Johnson J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
44. Visvanathan J., Lee S., Lee B., Lee J.W., Lee S.K. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 2007, 21:744-749.
45. Baroukh N.N., Van Obberghen E. Function of microRNA-375 and microRNA-124a in pancreas and brain. FEBS J. 2009, 276:6509-6521.
46. Baroukh N., Ravier M.A., Loder M.K., Hill E.V., Bounacer A., Scharfmann R., Rutter G.A., Van Obberghen E. MicroRNA-124a regulates Foxa2 expression and intracellular signaling in pancreatic beta-cell lines. J. Biol. Chem. 2007, 282:19575-19588.
47. Shin S., Sun Y., Liu Y., Khaner H., Svant S., Cai J., Xu Q.X., Davidson B.P., Stice S.L., Smith A.K., Goldman S.A., Reubinoff B.E., Zhan M., Rao M.S., Chesnut J.D. Whole genome analysis of human neural stem cells derived from embryonic stem cells and stem and progenitor cells isolated from fetal tissue. Stem Cells 2007, 25:1298-1306.
48. Krichevsky A.M., Sonntag K.C., Isacson O., Kosik K.S. Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 2006, 24:857-864.
49. Wang G.L., Jiang B.H., Rue E.A., Semenza G.L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:5510-5514.
50. MacKenzie E.D., Selak M.A., Tennant D.A., Payne L.J., Crosby S., Frederiksen C.M., Watson D.G., Gottlieb E. Cell-permeating alpha-ketoglutarate derivatives alleviate pseudohypoxia in succinate dehydrogenase-deficient cells. Mol. Cell. Biol. 2007, 27:3282-3289.
51. Hermann A., Maisel M., Liebau S., Gerlach M., Kleger A., Schwarz J., Kim K.S., Antoniadis G., Lerche H., Storch A. Mesodermal cell types induce neurogenesis from adult human hippocampal progenitor cells. J. Neurochem. 2006, 98:629-640.
52. Cadet N., Paquin J. Conversion and storage of somatostatin are established before response to secretagogue stimuli in P19 neurons. Brain Res. Dev. Brain Res. 2000, 120:211-221.
53. Korshunova I., Novitskaya V., Kiryushko D., Pedersen N., Kolkova K., Kropotova E., Mosevitsky M., Rayko M., Morrow J.S., Ginzburg I., Berezin V., Bock E. GAP-43 regulates NCAM-180-mediated neurite outgrowth. J. Neurochem. 2007, 100:1599-1612.
54. Zhang P.L., Izrael M., Ainbinder E., Ben-Simchon L., Chebath J., Revel M. Increased myelinating capacity of embryonic stem cell derived oligodendrocyte precursors after treatment by interleukin-6/soluble interleukin-6 receptor fusion protein. Mol. Cell. Neurosci. 2006, 31:387-398.
55. Tanner S.M., Austin J.L., Leone G., Rush L.J., Plass C., Heinonen K., Mrozek K., Sill H., Knuutila S., Kolitz J.E., Archer K.J., Caligiuri M.A., Bloomfield C.D., de La Chapelle A. BAALC, the human member of a novel mammalian neuroectoderm gene lineage, is implicated in hematopoiesis and acute leukemia. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13901-13906.
56. Zetterstrom R.H., Solomin L., Jansson L., Hoffer B.J., Olson L., Perlmann T. Dopamine neuron agenesis in Nurr1-deficient mice. Science 1997, 276:248-250.
57. Wada K., Nakajima A., Katayama K., Kudo C., Shibuya A., Kubota N., Terauchi Y., Tachibana M., Miyoshi H., Kamisaki Y., Mayumi T., Kadowaki T., Blumberg R.S. Peroxisome proliferator-activated receptor gamma-mediated regulation of neural stem cell proliferation and differentiation. J. Biol. Chem. 2006, 281:12673-12681.
58. Ohnishi S., Yasuda T., Kitamura S., Nagaya N. Effect of hypoxia on gene expression of bone marrow-derived mesenchymal stem cells and mononuclear cells. Stem Cells 2007, 25:1166-1177.
59. Chambeyron S., Bickmore W.A. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev. 2004, 18:1119-1130.
60. Muller W.G., Walker D., Hager G.L., McNally J.G. Large-scale chromatin decondensation and recondensation regulated by transcription from a natural promoter. J. Cell Biol. 2001, 154:33-48.
61. Asensio V.C., Campbell I.L. Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci. 1999, 22:504-512.
62. Simpson J.E., Newcombe J., Cuzner M.L., Woodroofe M.N. Expression of the interferon-gamma-inducible chemokines IP-10 and Mig and their receptor, CXCR3, in multiple sclerosis lesions. Neuropathol. Appl. Neurobiol. 2000, 26:133-142.
63. Junier M.P. What role(s) for TGFalpha in the central nervous system?. Prog. Neurobiol. 2000, 62:443-473.
64. Luo Q., Kang Q., Si W., Jiang W., Park J.K., Peng Y., Li X., Luu H.H., Luo J., Montag A.G., Haydon R.C., He T.C. Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J. Biol. Chem. 2004, 279:55958-55968.
65. Mbikay M., Seidah N.G., Chretien M. Neuroendocrine secretory protein 7B2: structure, expression and functions. Biochem. J. 2001, 357:329-342.
66. Hou Q.L., Gao X., Lu Q., Zhang X.H., Tu Y.Y., Jin M.L., Zhao G.P., Yu L., Jing N.H., Li B.M. SNAP-25 in hippocampal CA3 region is required for long-term memory formation. Biochem. Biophys. Res. Commun. 2006, 347:955-962.
67. Erlandsson A., Enarsson M., Forsberg-Nilsson K. Immature neurons from CNS stem cells proliferate in response to platelet-derived growth factor. J. Neurosci. 2001, 21:3483-3491.
68. Jackson E.L., Garcia-Verdugo J.M., Gil-Perotin S., Roy M., Quinones-Hinojosa A., VandenBerg S., Alvarez-Buylla A. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006, 51:187-199.
69. Johnson R., Teh C.H., Kunarso G., Wong K.Y., Srinivasan G., Cooper M.L., Volta M., Chan S.S., Lipovich L., Pollard S.M., Karuturi R.K., Wei C.L., Buckley N.J., Stanton L.W. REST regulates distinct transcriptional networks in embryonic and neural stem cells. PLoS Biol. 2008, 6:e256.
70. Bruick R.K., McKnight S.L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001, 294(5545):1337-1340.
71. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., Kaelin W.G. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001, 292(5516):464-468.
72. Jaakkola P. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001, 292(5516):468-472.
73. Wenger R.H. Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J. 2002, 16:1151-1162.
74. Tanaka H., Yamamoto M., Hashimoto N., Miyakoshi M., Tamakawa S., Yoshie M., Tokusashi Y., Yokoyama K., Yaginuma Y., Ogawa K. Hypoxia-independent overexpression of hypoxia-inducible factor 1alpha as an early change in mouse hepatocarcinogenesis. Cancer Res. 2006, 66:11263-11270.
75. Conte C., Riant E., Toutain C., Pujol F., Arnal J.F., Lenfant F., Prats A.C. FGF2 translationally induced by hypoxia is involved in negative and positive feedback loops with HIF-1alpha. PLoS ONE 2008, 3:e3078.
76. D'Ippolito G., Diabira S., Howard G.A., Roos B.A., Schiller P.C. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 2006, 39:513-522.
77. Fehrer C., Brunauer R., Laschober G., Unterluggauer H., Reitinger S., Kloss F., Gully C., Gassner R., Lepperdinger G. Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell 2007, 6:745-757.
78. Tomita S., Ueno M., Sakamoto M., Kitahama Y., Ueki M., Maekawa N., Sakamoto H., Gassmann M., Kageyama R., Ueda N., Gonzalez F.J., Takahama Y. Defective brain development in mice lacking the Hif-1alpha gene in neural cells. Mol. Cell. Biol. 2003, 23:6739-6749.
79. Milosevic J., Maisel M., Wegner F., Leuchtenberger J., Wenger R.H., Gerlach M., Storch A., Schwarz J. Lack of hypoxia-inducible factor-1{alpha} impairs midbrain neural precursor cells involving vascular endothelial growth factor signaling. J. Neurosci. 2007, 27(2):412-421.
80. Chen H.L., Pistollato F., Hoeppner D.J., Ni H.T., McKay R.D., Panchision D.M. Oxygen tension regulates survival and fate of mouse central nervous system precursors at multiple levels. Stem Cells 2007, 25:2291-2301.
81. Pacary E., Legros H., Valable S., Duchatelle P., Lecocq M., Petit E., Nicole O., Bernaudin M. Synergistic effects of CoCl2 and ROCK inhibition on mesenchymal stem cell differentiation into neuron-like cells. J. Cell Sci. 2006, 119(13):2667-2678.
82. Pacary E., Petit E., Bernaudin M. Concomitant inhibition of prolyl hydroxylases and ROCK initiates differentiation of mesenchymal stem cells and PC12 towards the neuronal lineage. Biochem. Biophys. Res. Commun. 2008, 377:400-406.
83. Pacary E., Tixier E., Coulet F., Roussel S., Petit E., Bernaudin M. Crosstalk between HIF-1 and ROCK pathways in neuronal differentiation of mesenchymal stem cells, neurospheres and in PC12 neurite outgrowth. Mol. Cell. Neurosci. 2007, 35(3):409-423.
84. Poy M.N., Eliasson L., Krutzfeldt J., Kuwajima S., Ma X., Macdonald P.E., Pfeffer S., Tuschl T., Rajewsky N., Rorsman P., Stoffel M. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004, 432:226-230.
85. Krichevsky A.M., King K.S., Donahue C.P., Khrapko K., Kosik K.S. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 2003, 9:1274-1281.
86. Suh M.R., Lee Y., Kim J.Y., Kim S.K., Moon S.H., Lee J.Y., Cha K.Y., Chung H.M., Yoon H.S., Moon S.Y., Kim V.N., Kim K.S. Human embryonic stem cells express a unique set of microRNAs. Dev. Biol. 2004, 270:488-498.
87. Conaco C., Otto S., Han J.J., Mandel G. Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2422-2427.
88. De Pietri Tonelli D., Pulvers J.N., Haffner C., Murchison E.P., Hannon G.J., Huttner W.B. miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development 2008, 135:3911-3921.
89. Maiorano N.A., Mallamaci A. Promotion of embryonic cortico-cerebral neuronogenesis by miR-124. Neural Dev. 2009, 4:40.
90. Smirnova L., Grafe A., Seiler A., Schumacher S., Nitsch R., Wulczyn F.G. Regulation of miRNA expression during neural cell specification. Eur. J. Neurosci. 2005, 21:1469-1477.
91. Papagiannakopoulos T., Kosik K.S. MicroRNA-124: micromanager of neurogenesis. Cell Stem Cell 2009, 4:375-376.
92. Makeyev E.V., Zhang J., Carrasco M.A., Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 2007, 27:435-448.