Expression and functional analysis of the Wnt/beta-catenin induced mir-135a-2 locus in embryonic forebrain development

Neural Development

Volumn 11, Issue 1, 2016, Pages

  Caronia Brown, Giuliana ^a   Anderegg, Angela ^a   Awatramani, Rajeshwar ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

beta catenin; Forebrain; Lmx1a; miR 135a; Rmst; Wnts

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; MICRORNA; MICRORNA 132A; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN; LIM HOMEODOMAIN PROTEIN; LMX1A PROTEIN, MOUSE; MIRN135 MICRORNA, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BRAIN DEVELOPMENT; CHOROID PLEXUS; EMBRYO; FEMALE; FOREBRAIN; GENE DELETION; GENOTYPE; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MOUSE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; ANIMAL; EMBRYOLOGY; METABOLISM; WNT SIGNALING PATHWAY;

ANIMALS; LIM-HOMEODOMAIN PROTEINS; MICE; MICRORNAS; PROSENCEPHALON; TGF-BETA SUPERFAMILY PROTEINS; TRANSCRIPTION FACTORS; WNT SIGNALING PATHWAY;

EID: 84962195201     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/s13064-016-0065-y     Document Type: Article

References (85)

1. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120(1):15-20. doi: 10.1016/j.cell.2004.12.035.
2. Fineberg SK, Kosik KS, Davidson BL. MicroRNAs potentiate neural development. Neuron. 2009;64(3):303-9. doi: 10.1016/j.neuron.2009.10.020.
3. Yun B, Anderegg A, Menichella D, Wrabetz L, Feltri ML, Awatramani R. MicroRNA-deficient Schwann cells display congenital hypomyelination. J Neurosci. 2010;30(22):7722-8. doi: 10.1523/JNEUROSCI.0876-10.2010. PubMed PMID: 20519547, PubMed Central PMCID: PMC2906453.
4. Chen JA, Huang YP, Mazzoni EO, Tan GC, Zavadil J, Wichterle H. Mir-17-3p controls spinal neural progenitor patterning by regulating Olig2/Irx3 cross-repressive loop. Neuron. 2011;69(4):721-35. doi: 10.1016/j.neuron.2011.01.014. PubMed PMID: 21338882, PubMed Central PMCID: PMC3062262.
5. Haramati S, Chapnik E, Sztainberg Y, Eilam R, Zwang R, Gershoni N, et al. miRNA malfunction causes spinal motor neuron disease. Proc Natl Acad Sci U S A. 2010;107(29):13111-6. doi: 10.1073/pnas.1006151107. PubMed PMID: 20616011, PubMed Central PMCID: PMC2919953.
6. Li X, Carthew RW. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell. 2005;123(7):1267-77. doi: 10.1016/j.cell.2005.10.040.
7. Lin HP, Oksuz I, Hurley E, Wrabetz L, Awatramani R. Microprocessor complex subunit DiGeorge syndrome critical region gene 8 (Dgcr8) is required for schwann cell myelination and myelin maintenance. J Biol Chem. 2015;290(40):24294-307. doi: 10.1074/jbc.M115.636407. PubMed PMID: 26272614; PubMed Central PMCID: PMCPMC4591815.
8. Nowakowski TJ, Mysiak KS, Pratt T, Price DJ. Functional dicer is necessary for appropriate specification of radial glia during early development of mouse telencephalon. PLoS One. 2011;6(8):e23013. doi: 10.1371/journal.pone.0023013. PubMed PMID: 21826226, PubMed Central PMCID: PMC3149632.
9. Kawase-Koga Y, Otaegi G, Sun T. Different timings of Dicer deletion affect neurogenesis and gliogenesis in the developing mouse central nervous system. Dev Dyn. 2009;238(11):2800-12. doi: 10.1002/dvdy.22109. PubMed PMID: 19806666, PubMed Central PMCID: PMC2831750.
10. Davis TH, Cuellar TL, Koch SM, Barker AJ, Harfe BD, McManus MT, et al. Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J Neurosci. 2008;28(17):4322-30. doi: 10.1523/JNEUROSCI.4815-07.2008.
11. Anderegg A, Lin HP, Chen JA, Caronia-Brown G, Cherepanova N, Yun B, et al. An Lmx1b-miR135a2 Regulatory Circuit Modulates Wnt1/Wnt Signaling and Determines the Size of the Midbrain Dopaminergic Progenitor Pool. PLoS Genet. 2013;9(12):e1003973. doi: 10.1371/journal.pgen.1003973. PubMed PMID: 24348261, PubMed Central PMCID: PMC3861205.
12. Inui M, Montagner M, Piccolo S. miRNAs and morphogen gradients. Curr Opin Cell Biol. 2012;24(2):194-201. doi: 10.1016/j.ceb.2011.11.013.
13. Inestrosa NC, Arenas E. Emerging roles of Wnts in the adult nervous system. Nat Rev Neurosci. 2010;11(2):77-86. doi: 10.1038/nrn2755.
14. Chenn A, Walsh CA. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science. 2002;297(5580):365-9. doi: 10.1126/science.1074192.
15. Megason SG, McMahon AP. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development. 2002;129(9):2087-98.
16. Lee SM, Tole S, Grove E, McMahon AP. A local Wnt-3a signal is required for development of the mammalian hippocampus. Development. 2000;127(3):457-67. Epub 2000/01/13.
17. McMahon AP, Joyner AL, Bradley A, McMahon JA. The midbrain-hindbrain phenotype of Wnt-1-/Wnt-1- mice results from stepwise deletion of engrailed-expressing cells by 9.5 days postcoitum. Cell. 1992;69(4):581-95.
18. Machon O, Backman M, Machonova O, Kozmik Z, Vacik T, Andersen L, et al. A dynamic gradient of Wnt signaling controls initiation of neurogenesis in the mammalian cortex and cellular specification in the hippocampus. Dev Biol. 2007;311(1):223-37. doi: 10.1016/j.ydbio.2007.08.038.
19. Tang M, Villaescusa JC, Luo SX, Guitarte C, Lei S, Miyamoto Y, et al. Interactions of Wnt/beta-catenin signaling and sonic hedgehog regulate the neurogenesis of ventral midbrain dopamine neurons. J Neurosci. 2010;30(27):9280-91. doi: 10.1523/JNEUROSCI.0860-10.2010. PubMed PMID: 20610763, PubMed Central PMCID: PMC3578394.
20. Galceran J, Farinas I, Depew MJ, Clevers H, Grosschedl R. Wnt3a-/--like phenotype and limb deficiency in Lef1(-/-)Tcf1(-/-) mice. Genes Dev. 1999;13(6):709-17. PubMed PMID: 10090727, PubMed Central PMCID: PMC316557, Epub 1999/03/25.
21. Woodhead GJ, Mutch CA, Olson EC, Chenn A. Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation. J Neurosci. 2006;26(48):12620-30. doi: 10.1523/JNEUROSCI.3180-06.2006. PubMed PMID: 17135424, PubMed Central PMCID: PMC2867669.
22. Joksimovic M, Yun BA, Kittappa R, Anderegg AM, Chang WW, Taketo MM, et al. Wnt antagonism of Shh facilitates midbrain floor plate neurogenesis. Nat Neurosci. 2009;12(2):125-31. doi: 10.1038/nn.2243. Epub 2009/01/06.
23. Joksimovic M, Awatramani R. Wnt/beta-catenin signaling in midbrain dopaminergic neuron specification and neurogenesis. J Mol Cell Biol. 2014. doi: 10.1093/jmcb/mjt043.
24. Nouri N, Patel MJ, Joksimovic M, Poulin JF, Anderegg A, Taketo MM, et al. Excessive Wnt/beta-catenin signaling promotes midbrain floor plate neurogenesis, but results in vacillating dopamine progenitors. Mol Cell Neurosci. 2015;68:131-42. doi: 10.1016/j.mcn.2015.07.002. PubMed PMID: 26164566; PubMed Central PMCID: PMCPMC4633300.
25. Furuta Y, Piston DW, Hogan BL. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development. 1997;124(11):2203-12.
26. Liem Jr KF, Tremml G, Jessell TM. A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord. Cell. 1997;91(1):127-38. Epub 1997/10/23 22:32.
27. Augsburger A, Schuchardt A, Hoskins S, Dodd J, Butler S. BMPs as mediators of roof plate repulsion of commissural neurons. Neuron. 1999;24(1):127-41. Epub 2000/02/17.
28. Samanta J, Burke GM, McGuire T, Pisarek AJ, Mukhopadhyay A, Mishina Y, et al. BMPR1a signaling determines numbers of oligodendrocytes and calbindin-expressing interneurons in the cortex. J Neurosci. 2007;27(28):7397-407.
29. Hebert JM, Mishina Y, McConnell SK. BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron. 2002;35(6):1029-41. Epub 2002/10/02.
30. See J, Mamontov P, Ahn K, Wine-Lee L, Crenshaw 3rd EB, Grinspan JB. BMP signaling mutant mice exhibit glial cell maturation defects. Mol Cell Neurosci. 2007;35(1):171-82.
31. Choe Y, Kozlova A, Graf D, Pleasure SJ. Bone morphogenic protein signaling is a major determinant of dentate development. J Neurosci. 2013;33(16):6766-75. doi: 10.1523/JNEUROSCI.0128-13.2013. PubMed PMID: 23595735, PubMed Central PMCID: PMC3684166.
32. Doan LT, Javier AL, Furr NM, Nguyen KL, Cho KW, Monuki ES. A Bmp reporter with ultrasensitive characteristics reveals that high Bmp signaling is not required for cortical hem fate. PLoS One. 2012;7(9):e44009. doi: 10.1371/journal.pone.0044009. PubMed PMID: 22984456, PubMed Central PMCID: PMC3439469.
33. Hu JS, Doan LT, Currle DS, Paff M, Rheem JY, Schreyer R, et al. Border formation in a Bmp gradient reduced to single dissociated cells. Proc Natl Acad Sci U S A. 2008;105(9):3398-403. doi: 10.1073/pnas.0709100105. PubMed PMID: 18292231, PubMed Central PMCID: PMC2265170.
34. Itasaki N, Hoppler S. Crosstalk between Wnt and bone morphogenic protein signaling: a turbulent relationship. Dev Dyn. 2010;239(1):16-33. doi: 10.1002/dvdy.22009.
35. Subramanian L, Remedios R, Shetty A, Tole S. Signals from the edges: the cortical hem and antihem in telencephalic development. Semin Cell Dev Biol. 2009;20(6):712-8. doi: 10.1016/j.semcdb.2009.04.001. Epub 2009/05/19. PubMed PMID: 19446478; PubMed Central PMCID: PMC2791850.
36. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW. The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development. 1998;125(12):2315-25.
37. Monuki ES, Porter FD, Walsh CA. Patterning of the dorsal telencephalon and cerebral cortex by a roof plate-Lhx2 pathway. Neuron. 2001;32(4):591-604. Epub 2001/11/24doi: S0896-6273(01)00504-9 [pii].
38. Tole S, Grove EA. Detailed field pattern is intrinsic to the embryonic mouse hippocampus early in neurogenesis. J Neurosci. 2001;21(5):1580-9. Epub 2001/02/27.
39. Mangale VS, Hirokawa KE, Satyaki PR, Gokulchandran N, Chikbire S, Subramanian L, et al. Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science. 2008;319(5861):304-9. doi: 10.1126/science.1151695. PubMed PMID: 18202285, PubMed Central PMCID: PMC2494603.
40. Zhou CJ, Zhao C, Pleasure SJ. Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. J Neurosci. 2004;24(1):121-6. doi: 10.1523/JNEUROSCI.4071-03.2004. Epub 2004/01/13. PubMed PMID: 14715945.
41. Grove EA, Tole S. Patterning events and specification signals in the developing hippocampus. Cereb Cortex. 1999;9(6):551-61. Epub 1999/09/25.
42. Caronia G, Wilcoxon J, Feldman P, Grove EA. Bone morphogenetic protein signaling in the developing telencephalon controls formation of the hippocampal dentate gyrus and modifies fear-related behavior. J Neurosci. 2010;30(18):6291-301. doi: 10.1523/JNEUROSCI.0550-10.2010. Epub 2010/05/07.
43. Yoshida M, Assimacopoulos S, Jones KR, Grove EA. Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development. 2006;133(3):537-45. doi: 10.1242/dev.02209.
44. Caronia-Brown G, Yoshida M, Gulden F, Assimacopoulos S, Grove EA. The cortical hem regulates the size and patterning of neocortex. Development. 2014;141(14):2855-65. doi: 10.1242/dev.106914.
45. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, Oshima M, et al. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 1999;18(21):5931-42. doi: 10.1093/emboj/18.21.5931. PubMed PMID: 10545105, PubMed Central PMCID: PMC1171659.
46. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, et al. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development. 2001;128(8):1253-64.
47. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci. 2002;22(15):6309-14. doi: 20026564.
48. Park CY, Jeker LT, Carver-Moore K, Oh A, Liu HJ, Cameron R, et al. A resource for the conditional ablation of microRNAs in the mouse. Cell Reports. 2012;1(4):385-91. doi: 10.1016/j.celrep.2012.02.008. PubMed PMID: 22570807, PubMed Central PMCID: PMC3345170.
49. Awatramani R, Soriano P, Rodriguez C, Mai JJ, Dymecki SM. Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat Genet. 2003;35(1):70-5. doi: 10.1038/ng1228.
50. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet. 1999;23(1):99-103. doi: 10.1038/12703.
51. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101-8.
52. Vlachos IS, Kostoulas N, Vergoulis T, Georgakilas G, Reczko M, Maragkakis M, et al. DIANA miRPath v.2.0: investigating the combinatorial effect of microRNAs in pathways. Nucleic Acids Res. 2012;40(Web Server issue):W498-504. doi: 10.1093/nar/gks494. PubMed PMID: 22649059; PubMed Central PMCID: PMC3394305.
53. Uhde CW, Vives J, Jaeger I, Li M. Rmst is a novel marker for the mouse ventral mesencephalic floor plate and the anterior dorsal midline cells. PLoS One. 2010;5(1):e8641. doi: 10.1371/journal.pone.0008641. PubMed PMID: 20062813, PubMed Central PMCID: PMC2799666.
54. Backman M, Machon O, Mygland L, van den Bout CJ, Zhong W, Taketo MM, et al. Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev Biol. 2005;279(1):155-68. doi: 10.1016/j.ydbio.2004.12.010. Epub 2005/02/15.
55. Kim AS, Lowenstein DH, Pleasure SJ. Wnt receptors and Wnt inhibitors are expressed in gradients in the developing telencephalon. Mech Dev. 2001;103(1-2):167-72. Epub 2001/05/04.
56. Bulchand S, Grove EA, Porter FD, Tole S. LIM-homeodomain gene Lhx2 regulates the formation of the cortical hem. Mech Dev. 2001;100(2):165-75.
57. Willert J, Epping M, Pollack JR, Brown PO, Nusse R. A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Dev Biol. 2002;2:8. PubMed PMID: 12095419, PubMed Central PMCID: PMC117803.
58. Chizhikov VV, Lindgren AG, Mishima Y, Roberts RW, Aldinger KA, Miesegaes GR, et al. Lmx1a regulates fates and location of cells originating from the cerebellar rhombic lip and telencephalic cortical hem. Proc Natl Acad Sci U S A. 2010;107(23):10725-30. doi: 10.1073/pnas.0910786107. Epub 2010/05/26. PubMed PMID: 20498066; PubMed Central PMCID: PMC2890798.
59. Quan M, Chen J, Zhang D. Exploring the secrets of long noncoding RNAs. Int J Mol Sci. 2015;16(3):5467-96. doi: 10.3390/ijms16035467. PubMed PMID: 25764159; PubMed Central PMCID: PMCPMC4394487.
60. Tan JY, Sirey T, Honti F, Graham B, Piovesan A, Merkenschlager M, et al. Corrigendum: Extensive microRNA-mediated crosstalk between lncRNAs and mRNAs in mouse embryonic stem cells. Genome Res. 2015;25(9):1410.1. PubMed PMID: 26330573; PubMed Central PMCID: PMCPMC4561499.
61. Jalali S, Bhartiya D, Lalwani MK, Sivasubbu S, Scaria V. Systematic transcriptome wide analysis of lncRNA-miRNA interactions. PLoS One. 2013;8(2):e53823. doi: 10.1371/journal.pone.0053823. PubMed PMID: 23405074; PubMed Central PMCID: PMCPMC3566149.
62. Jeggari A, Marks DS, Larsson E. miRcode: a map of putative microRNA target sites in the long non-coding transcriptome. Bioinformatics. 2012;28(15):2062-3. doi: 10.1093/bioinformatics/bts344. PubMed PMID: 22718787; PubMed Central PMCID: PMCPMC3400968.
63. Fischer S, Handrick R, Aschrafi A, Otte K. Unveiling the principle of microRNA-mediated redundancy in cellular pathway regulation. RNA Biol. 2015;12(3):238-47. doi: 10.1080/15476286.2015.1017238.
64. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell. 2012;148(6):1172-87. doi: 10.1016/j.cell.2012.02.005. PubMed PMID: 22424228, PubMed Central PMCID: PMC3308137.
65. Caronia-Brown G, Grove EA. Timing of Cortical Interneuron Migration Is Influenced by the Cortical Hem. Cereb Cortex. 2010. doi: 10.1093/cercor/bhq142. Epub 2010/08/18.
66. Galceran J, Miyashita-Lin EM, Devaney E, Rubenstein JL, Grosschedl R. Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development. 2000;127(3):469-82. Epub 2000/01/13.
67. Qiu L, Rivera-Perez JA, Xu Z. A non-specific effect associated with conditional transgene expression based on Cre-loxP strategy in mice. PLoS One. 2011;6(5):e18778. doi: 10.1371/journal.pone.0018778. PubMed PMID: 21572998, PubMed Central PMCID: PMC3091857.
68. Hodge RD, Garcia III AJ, Elsen GE, Nelson BR, Mussar KE, Reiner SL, et al. Tbr2 expression in Cajal-Retzius cells and intermediate neuronal progenitors is required for morphogenesis of the dentate gyrus. J Neurosci. 2013;33(9):4165-80. doi: 10.1523/JNEUROSCI.4185-12.2013. PubMed PMID: 23447624; PubMed Central PMCID: PMCPMC3623668.
69. Konno D, Iwashita M, Satoh Y, Momiyama A, Abe T, Kiyonari H, et al. The mammalian DM domain transcription factor Dmrta2 is required for early embryonic development of the cerebral cortex. PLoS One. 2012;7(10):e46577. doi: 10.1371/journal.pone.0046577. PubMed PMID: 23056351; PubMed Central PMCID: PMCPMC3462758.
70. Li Q, Bian S, Hong J, Kawase-Koga Y, Zhu E, Zheng Y, et al. Timing specific requirement of microRNA function is essential for embryonic and postnatal hippocampal development. PLoS One. 2011;6(10):e26000. doi: 10.1371/journal.pone.0026000. PubMed PMID: 21991391; PubMed Central PMCID: PMCPMC3186801.
71. Lavado A, He Y, Pare J, Neale G, Olson EN, Giovannini M, et al. Tumor suppressor Nf2 limits expansion of the neural progenitor pool by inhibiting Yap/Taz transcriptional coactivators. Development. 2013;140(16):3323-34. doi: 10.1242/dev.096537. PubMed PMID: 23863479; PubMed Central PMCID: PMCPMC3737715.
72. Shi Y, Zhao X, Hsieh J, Wichterle H, Impey S, Banerjee S, et al. MicroRNA regulation of neural stem cells and neurogenesis. J Neurosci. 2010;30(45):14931-6. doi: 10.1523/JNEUROSCI.4280-10.2010. PubMed PMID: 21068294, PubMed Central PMCID: PMC3071711.
73. Johnson MB, Wang PP, Atabay KD, Murphy EA, Doan RN, Hecht JL, et al. Single-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex. Nat Neurosci. 2015;18(5):637-46. doi: 10.1038/nn.3980.
74. Nagel R, le Sage C, Diosdado B, van der Waal M, Oude Vrielink JA, Bolijn A, et al. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res. 2008;68(14):5795-802. doi: 10.1158/0008-5472.CAN-08-0951.
75. Leung CO, Deng W, Ye TM, Ngan HY, Tsao SW, Cheung AN, et al. miR-135a leads to cervical cancer cell transformation through regulation of beta-catenin via a SIAH1-dependent ubiquitin proteosomal pathway. Carcinogenesis. 2014;35(9):1931-40. doi: 10.1093/carcin/bgu032.
76. Gokhale A, Kunder R, Goel A, Sarin R, Moiyadi A, Shenoy A, et al. Distinctive microRNA signature of medulloblastomas associated with the WNT signaling pathway. J Cancer Res Ther. 2010;6(4):521-9. doi: 10.4103/0973-1482.77072.
77. Chen C, Peng Y, Peng Y, Peng J, Jiang S. miR-135a-5p inhibits 3T3-L1 adipogenesis through activation of canonical Wnt/beta-catenin signaling. J Mol Endocrinol. 2014;52(3):311-20. doi: 10.1530/JME-14-0013.
78. Yang X, Wang X, Nie F, Liu T, Yu X, Wang H, et al. miR-135 family members mediate podocyte injury through the activation of Wnt/beta-catenin signaling. Int J Mol Med. 2015;36(3):669-77. doi: 10.3892/ijmm.2015.2259. PubMed PMID: 26134897; PubMed Central PMCID: PMCPMC4533775.
79. Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature. 2005;438(7068):685-9. doi: 10.1038/nature04303.
80. Ebert MS, Sharp PA. MicroRNA sponges: progress and possibilities. RNA. 2010;16(11):2043-50. doi: 10.1261/rna.2414110. PubMed PMID: 20855538, PubMed Central PMCID: PMC2957044.
81. Park CY, Choi YS, McManus MT. Analysis of microRNA knockouts in mice. Hum Mol Genet. 2010;19(R2):R169-75. doi: 10.1093/hmg/ddq367. PubMed PMID: 20805106, PubMed Central PMCID: PMC2981466.
82. Bertero T, Grosso S, Robbe-Sermesant K, Lebrigand K, Henaoui IS, Puissegur MP, et al. "Seed-Milarity" confers to hsa-miR-210 and hsa-miR-147b similar functional activity. PLoS One. 2012;7(9):e44919. doi: 10.1371/journal.pone.0044919. PubMed PMID: 23028679; PubMed Central PMCID: PMC3441733.
83. Clevers H, Nusse R. Wnt/beta-catenin signaling and disease. Cell. 2012;149(6):1192-205. doi: 10.1016/j.cell.2012.05.012.
84. Chung S, Leung A, Han BS, Chang MY, Moon JI, Kim CH, et al. Wnt1-lmx1a forms a novel autoregulatory loop and controls midbrain dopaminergic differentiation synergistically with the SHH-FoxA2 pathway. Cell Stem Cell. 2009;5(6):646-58. doi: 10.1016/j.stem.2009.09.015. PubMed PMID: 19951692, PubMed Central PMCID: PMC2788512.
85. Hoekstra EJ, von Oerthel L, van der Heide LP, Kouwenhoven WM, Veenvliet JV, Wever I, et al. Lmx1a encodes a rostral set of mesodiencephalic dopaminergic neurons marked by the Wnt/B-catenin signaling activator R-spondin 2. PLoS One. 2013;8(9):e74049. doi: 10.1371/journal.pone.0074049. PubMed PMID: 24066094, PubMed Central PMCID: PMC3774790.