Dynamic Activity of miR-125b and miR-93 during Murine Neural Stem Cell Differentiation In Vitro and in the Subventricular Zone Neurogenic Niche

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Lattanzi, Annalisa ^a,b   Gentner, Bernhard ^a   Corno, Daniela ^a   Di Tomaso, Tiziano ^a   Mestdagh, Pieter ^c   Speleman, Frank ^c   Naldini, Luigi ^a,d   Gritti, Angela ^a  

^a SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^b UNIVERSITY OF PERUGIA   (Italy)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

^d VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

LENTIVIRUS VECTOR; MICRORNA; MICRORNA 124; MICRORNA 125B; MICRORNA 23A; MICRORNA 93; UNCLASSIFIED DRUG; MIRN125 MICRORNA, MOUSE; MIRN93 MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL POPULATION; CELL SPECIFICITY; CELL TYPE; CONTROLLED STUDY; FEMALE; GENE ACTIVITY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MACROGLIA; MALE; MONITORING; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS TISSUE; NEURAL STEM CELL; NEWBORN; NONHUMAN; SENSITIVITY AND SPECIFICITY; SUBVENTRICULAR ZONE; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; GENE EXPRESSION PROFILING; GENETICS; LATERAL BRAIN VENTRICLE; METABOLISM; NERVE CELL; PHYSIOLOGY; STEM CELL NICHE;

MURINAE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; FEMALE; GENE EXPRESSION PROFILING; IN VITRO TECHNIQUES; LATERAL VENTRICLES; MALE; MICE; MICRORNAS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; STEM CELL NICHE;

EID: 84879508240     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067411     Document Type: Article

References (68)

1. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, et al. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773.
2. Kawahara H, Imai T, Okano H, (2012) MicroRNAs in Neural Stem Cells and Neurogenesis. Front Neurosci 6: 30.
3. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
4. Cao X, Yeo G, Muotri AR, Kuwabara T, Gage FH, (2006) Noncoding RNAs in the mammalian central nervous system. Annu Rev Neurosci 29: 77-103.
5. Maiorano NA, Mallamaci A, (2010) The pro-differentiating role of miR-124: indicating the road to become a neuron. RNA Biol 7: 528-533.
6. Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS, (2003) A microRNA array reveals extensive regulation of microRNAs during brain development. Rna 9: 1274-1281.
7. Zhao C, Sun G, Li S, Lang MF, Yang S, et al. (2010) MicroRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling. Proc Natl Acad Sci U S A 107: 1876-1881.
8. Mansfield JH, Harfe BD, Nissen R, Obenauer J, Srineel J, et al. (2004) MicroRNA-responsive 'sensor' transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression. Nat Genet 36: 1079-1083.
9. Nishino J, Kim I, Chada K, Morrison SJ, (2008) Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell 135: 227-239.
10. Shi Y, Zhao X, Hsieh J, Wichterle H, Impey S, et al. (2010) MicroRNA regulation of neural stem cells and neurogenesis. J Neurosci 30: 14931-14936.
11. Lang MF, Shi Y, (2012) Dynamic Roles of microRNAs in Neurogenesis. Front Neurosci 6: 71.
12. Visvanathan J, Lee S, Lee B, Lee JW, Lee SK, (2007) The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev 21: 744-749.
13. Yu JY, Chung KH, Deo M, Thompson RC, Turner DL, (2008) MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp Cell Res 314: 2618-2633.
14. Cheng LC, Pastrana E, Tavazoie M, Doetsch F, (2009) miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 12: 399-408.
15. Akerblom M, Sachdeva R, Barde I, Verp S, Gentner B, et al. (2012) MicroRNA-124 Is a Subventricular Zone Neuronal Fate Determinant. J Neurosci 32: 8879-8889.
16. Rybak A, Fuchs H, Hadian K, Smirnova L, Wulczyn EA, et al. (2009) The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. Nat Cell Biol 11: 1411-1420.
17. Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, et al. (2004) Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol 5: R13.
18. Stappert L, Borghese L, Roese-Koerner B, Weinhold S, Koch P, et al. (2013) MicroRNA-Based Promotion of Human Neuronal Differentiation and Subtype Specification. PLoS One 8: e59011.
19. Deo M, Yu JY, Chung KH, Tippens M, Turner DL, (2006) Detection of mammalian microRNA expression by in situ hybridization with RNA oligonucleotides. Dev Dyn 235: 2538-2548.
20. Thompson RC, Deo M, Turner DL, (2007) Analysis of microRNA expression by in situ hybridization with RNA oligonucleotide probes. Methods 43: 153-161.
21. Brown BD, Gentner B, Cantore A, Colleoni S, Amendola M, et al. (2007) Endogenous microRNA can be broadly exploited to regulate transgene expression according to tissue, lineage and differentiation state. Nat Biotechnol 25: 1457-1467.
22. Colin A, Faideau M, Dufour N, Auregan G, Hassig R, et al. (2009) Engineered lentiviral vector targeting astrocytes in vivo. Glia 57: 667-679.
23. Sachdeva R, Jonsson ME, Nelander J, Kirkeby A, Guibentif C, et al. (2010) Tracking differentiating neural progenitors in pluripotent cultures using microRNA-regulated lentiviral vectors. Proc Natl Acad Sci U S A 107: 11602-11607.
24. Di Stefano B, Maffioletti SM, Gentner B, Ungaro F, Schira G, et al. (2011) A microRNA-based system for selecting and maintaining the pluripotent state in human induced pluripotent stem cells. Stem Cells 29: 1684-1695.
25. Amendola M, Venneri MA, Biffi A, Vigna E, Naldini L, (2005) Coordinate dual-gene transgenesis by lentiviral vectors carrying synthetic bidirectional promoters. Nat Biotechnol 23: 108-116.
26. Gentner B, Visigalli I, Hiramatsu H, Lechman E, Ungari S, et al. (2010) Identification of hematopoietic stem cell-specific miRNAs enables gene therapy of globoid cell leukodystrophy. Sci Transl Med 2: 58ra84.
27. Gritti A, Dal Molin M, Foroni C, Bonfanti L, (2009) Effects of developmental age, brain region, and time in culture on long-term proliferation and multipotency of neural stem cell populations. J Comp Neurol 517: 333-349.
28. Lattanzi A, Neri M, Maderna C, di Girolamo I, Martino S, et al. (2010) Widespread Enzymatic Correction of Cns Tissues by a Single Intracerebral Injection of Therapeutic Lentiviral Vector in Leukodystrophy Mouse Models. Hum Mol Genet 19: 2208-2227.
29. Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, et al. (2009) A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol 10: R64.
30. Mestdagh P, Feys T, Bernard N, Guenther S, Chen C, et al. (2008) High-throughput stem-loop RT-qPCR miRNA expression profiling using minute amounts of input RNA. Nucleic Acids Res 36: e143.
31. Reynolds BA, Rietze RL, (2005) Neural stem cells and neurospheres-re-evaluating the relationship. Nat Methods 2: 333-336.
32. Cavazzin C, Ferrari D, Facchetti F, Russignan A, Vescovi AL, et al. (2006) Unique expression and localization of aquaporin- 4 and aquaporin-9 in murine and human neural stem cells and in their glial progeny. Glia.
33. Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R, et al. (2005) Regulation of miRNA expression during neural cell specification. Eur J Neurosci 21: 1469-1477.
34. Farrell BC, Power EM, Mc Dermott KW, (2011) Developmentally regulated expression of Sox9 and microRNAs 124, 128 and 23 in neuroepithelial stem cells in the developing spinal cord. Int J Dev Neurosci 29: 31-36.
35. Edbauer D, Neilson JR, Foster KA, Wang CF, Seeburg DP, et al. (2010) Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65: 373-384.
36. Le MT, Shyh-Chang N, Khaw SL, Chin L, Teh C, et al. (2011) Conserved regulation of p53 network dosage by microRNA-125b occurs through evolving miRNA-target gene pairs. PLoS Genet 7: e1002242.
37. Cui Y, Xiao Z, Han J, Sun J, Ding W, et al. (2012) MiR-125b orchestrates cell proliferation, differentiation and migration in neural stem/progenitor cells by targeting Nestin. BMC Neurosci 13: 116.
38. Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T, et al. (2005) A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci U S A 102: 16426-16431.
39. Klein C, Butt SJ, Machold RP, Johnson JE, Fishell G, (2005) Cerebellum- and forebrain-derived stem cells possess intrinsic regional character. Development 132: 4497-4508.
40. Kawashima H, Numakawa T, Kumamaru E, Adachi N, Mizuno H, et al. (2010) Glucocorticoid attenuates brain-derived neurotrophic factor-dependent upregulation of glutamate receptors via the suppression of microRNA-132 expression. Neuroscience 165: 1301-1311.
41. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, et al. (2008) Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132: 875-886.
42. Brett JO, Renault VM, Rafalski VA, Webb AE, Brunet A, (2011) The microRNA cluster miR-106b∼25 regulates adult neural stem/progenitor cell proliferation and neuronal differentiation. Aging (Albany NY) 3: 108-124.
43. Jovicic A, Roshan R, Moisoi N, Pradervand S, Moser R, et al. (2013) Comprehensive Expression Analyses of Neural Cell-Type-Specific miRNAs Identify New Determinants of the Specification and Maintenance of Neuronal Phenotypes. J Neurosci 33: 5127-5137.
44. Brown BD, Cantore A, Annoni A, Sergi LS, Lombardo A, et al. (2007) A microRNA-regulated lentiviral vector mediates stable correction of hemophilia B mice. Blood 110: 4144-4152.
45. Mukherji S, Ebert MS, Zheng GX, Tsang JS, Sharp PA, et al. (2011) MicroRNAs can generate thresholds in target gene expression. Nat Genet 43: 854-859.
46. Mullokandov G, Baccarini A, Ruzo A, Jayaprakash AD, Tung N, et al. (2012) High-throughput assessment of microRNA activity and function using microRNA sensor and decoy libraries. Nat Methods 9: 840-846.
47. Neri M, Ricca A, di Girolamo I, Alcala'-Franco B, Cavazzin C, et al. (2011) Neural stem cell gene therapy ameliorates pathology and function in a mouse model of globoid cell leukodystrophy. Stem Cells 29: 1559-1571.
48. Gentner B, Schira G, Giustacchini A, Amendola M, Brown BD, et al. (2009) Stable knockdown of microRNA in vivo by lentiviral vectors. Nat Methods 6: 63-66.
49. Bonfanti L, Peretto P, (2011) Adult neurogenesis in mammals-a theme with many variations. Eur J Neurosci 34: 930-950.
50. Ihrie RA, Alvarez-Buylla A, (2011) Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70: 674-686.
51. Lemasson M, Saghatelyan A, Olivo-Marin JC, Lledo PM, (2005) Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J Neurosci 25: 6816-6825.
52. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, et al. (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11: 1153-1161.
53. Gao FB, (2010) Context-dependent functions of specific microRNAs in neuronal development. Neural Dev 5: 25.
54. Mendell JT, (2008) miRiad roles for the miR-17-92 cluster in development and disease. Cell 133: 217-222.
55. Pogue AI, Cui JG, Li YY, Zhao Y, Culicchia F, et al. (2010) Micro RNA-125b (miRNA-125b) function in astrogliosis and glial cell proliferation. Neurosci Lett 476: 18-22.
56. Ihrie RA, Alvarez-Buylla A, (2008) Cells in the astroglial lineage are neural stem cells. Cell Tissue Res 331: 179-191.
57. Ivanovska I, Ball AS, Diaz RL, Magnus JF, Kibukawa M, et al. (2008) MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol 28: 2167-2174.
58. Mestdagh P, Bostrom AK, Impens F, Fredlund E, Van Peer G, et al. (2010) The miR-17-92 microRNA cluster regulates multiple components of the TGF-beta pathway in neuroblastoma. Mol Cell 40: 762-773.
59. Bian S, Hong J, Li Q, Schebelle L, Pollock A, et al. (2013) MicroRNA Cluster miR-17-92 Regulates Neural Stem Cell Expansion and Transition to Intermediate Progenitors in the Developing Mouse Neocortex. Cell Rep.
60. Foshay KM, Gallicano GI, (2009) miR-17 family miRNAs are expressed during early mammalian development and regulate stem cell differentiation. Dev Biol 326: 431-443.
61. Wang Y, Blelloch R, (2009) Cell cycle regulation by MicroRNAs in embryonic stem cells. Cancer Res 69: 4093-4096.
62. Li MA, He L, (2012) microRNAs as novel regulators of stem cell pluripotency and somatic cell reprogramming. Bioessays 34: 670-680.
63. Li Z, Yang CS, Nakashima K, Rana TM, (2011) Small RNA-mediated regulation of iPS cell generation. Embo J 30: 823-834.
64. Gao Z, Ding P, Hsieh J, (2012) Profiling of REST-Dependent microRNAs Reveals Dynamic Modes of Expression. Front Neurosci 6: 67.
65. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A, (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36: 1021-1034.
66. Buffo A, Rite I, Tripathi P, Lepier A, Colak D, et al. (2008) Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A 105: 3581-3586.
67. Laywell ED, Rakic P, Kukekov VG, Holland EC, Steindler DA, (2000) Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci U S A 97: 13883-13888.
68. Silver DJ, Steindler DA, (2009) Common astrocytic programs during brain development, injury and cancer. Trends Neurosci 32: 303-311.