Midbrain dopamine neurons in Parkinson's disease exhibit a dysregulated miRNA and target-gene network

Brain Research

Volumn 1618, Issue , 2015, Pages 111-121

  Briggs, Christine E ^a   Wang, Yulei ^b   Kong, Benjamin ^b   Woo, Tsung Ung W ^c   Iyer, Lakshmanan K ^a   Sonntag, Kai C ^c  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Life Technologies Corporation   (United States)

^c MCLEAN HOSPITAL   (United States)

Author keywords

Dopamine neurons; IPA; Laser capture microdissection; miRNAs; Parkinson's disease

Indexed keywords

MICRORNA; SMALL NUCLEOLAR RNA;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOWN REGULATION; FEMALE; GENE REGULATORY NETWORK; GENE TARGETING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; LASER CAPTURE MICRODISSECTION; MALE; MESENCEPHALON; NERVE CELL; PARKINSON DISEASE; PRIORITY JOURNAL; RNA ANALYSIS; SEX DIFFERENCE; SIGNAL TRANSDUCTION; UPREGULATION; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY;

DOPAMINERGIC NEURONS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; MALE; MESENCEPHALON; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARKINSON DISEASE; SIGNAL TRANSDUCTION;

EID: 84938149412     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.05.021     Document Type: Article

References (99)

1. P. Agarwal, R. Srivastava, A.K. Srivastava, S. Ali, and M. Datta miR-135a targets IRS2 and regulates insulin signaling and glucose uptake in the diabetic gastrocnemius skeletal muscle Biochim. Biophys. Acta 1832 2013 1294 1303
2. G. Arena, V. Gelmetti, L. Torosantucci, D. Vignone, G. Lamorte, P. De Rosa, E. Cilia, E.A. Jonas, and E.M. Valente PINK1 protects against cell death induced by mitochondrial depolarization, by phosphorylating Bcl-xL and impairing its pro-apoptotic cleavage Cell Death Differ. 20 2013 920 930
3. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
4. F. Bassil, P.O. Fernagut, E. Bezard, and W.G. Meissner Insulin, IGF-1 and GLP-1 signaling in neurodegenerative disorders: targets for disease modification? Prog. Neurobiol. 118 2014 1 18
5. F.M. Benes, B. Lim, D. Matzilevich, J.P. Walsh, S. Subburaju, and M. Minns Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars Proc. Natl. Acad. Sci. U. S. A. 104 2007 10164 10169
6. V. Berezin, P.S. Walmod, M. Filippov, and A. Dityatev Targeting of ECM molecules and their metabolizing enzymes and receptors for the treatment of CNS diseases Prog. Brain Res. 214 2014 353 388
7. H. Braak, and K. Del Tredici Invited article: nervous system pathology in sporadic Parkinson disease Neurology 70 2008 1916 1925
8. A.M. Calella, C. Nerlov, R.G. Lopez, C. Sciarretta, O. von Bohlen und Halbach, O. Bereshchenko, and L. Minichiello Neurotrophin/Trk receptor signaling mediates C/EBPalpha, -beta and NeuroD recruitment to immediate-early gene promoters in neuronal cells and requires C/EBPs to induce immediate-early gene transcription Neural Dev. 2 2007 4
9. I. Cantuti-Castelvetri, C. Keller-McGandy, B. Bouzou, G. Asteris, T.W. Clark, M.P. Frosch, and D.G. Standaert Effects of gender on nigral gene expression and parkinson disease Neurobiol. Dis. 26 2007 606 614
10. C. Chakraborty, C.G. Doss, S. Bandyopadhyay, and G. Agoramoorthy Influence of miRNA in insulin signaling pathway and insulin resistance: micro-molecules with a major role in type-2 diabetes Wiley Interdiscip. Rev. RNA 5 2014 697 712
11. F. Chen, S.K. Hou, H.J. Fan, and Y.F. Liu MiR-15a-16 represses Cripto and inhibits NSCLC cell progression Mol. Cell. Biochem. 391 2014 11 19
12. L. Chen, A.G. Lau, and F. Sarti Synaptic retinoic acid signaling and homeostatic synaptic plasticity Neuropharmacology 78 2014 3 12
13. Y. Chen, F. Siegel, S. Kipschull, B. Haas, H. Frohlich, G. Meister, and A. Pfeifer miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit Nat. Commun. 4 2013 1769
14. H.J. Cho, G. Liu, S.M. Jin, L. Parisiadou, C. Xie, J. Yu, L. Sun, B. Ma, J. Ding, R. Vancraenenbroeck, E. Lobbestael, V. Baekelandt, J.M. Taymans, P. He, J.C. Troncoso, Y. Shen, and H. Cai MicroRNA-205 regulates the expression of Parkinson's disease-related leucine-rich repeat kinase 2 protein Hum. Mol. Genet. 22 2013 608 620
15. S.J. Chung, S.M. Armasu, J.M. Biernacka, T.G. Lesnick, D.N. Rider, J.M. Cunningham, and D.M. Maraganore Variants in estrogen-related genes and risk of Parkinson's disease Mov. Disord. 26 2011 1234 1242
16. T. Cijsouw, J.P. Weber, J.H. Broeke, J.A. Broek, D. Schut, T. Kroon, I. Saarloos, M. Verhage, and R.F. Toonen Munc18-1 redistributes in nerve terminals in an activity- and PKC-dependent manner J. Cell Biol. 204 2014 759 775
17. E.T. Courtois, C.G. Castillo, E.G. Seiz, M. Ramos, C. Bueno, I. Liste, and A. Martinez-Serrano In vitro and in vivo enhanced generation of human A9 dopamine neurons from neural stem cells by Bcl-XL J. Biol. Chem. 285 2010 9881 9897
18. D. Crabtree, M. Dodson, X. Ouyang, M. Boyer-Guittaut, Q. Liang, M.E. Ballestas, N. Fineberg, and J. Zhang Over-expression of an inactive mutant cathepsin D increases endogenous alpha-synuclein and cathepsin B activity in SH-SY5Y cells J. Neurochem. 128 2014 950 961
19. D. Crepin, Y. Benomar, L. Riffault, H. Amine, A. Gertler, and M. Taouis The over-expression of miR-200a in the hypothalamus of ob/ob mice is linked to leptin and insulin signaling impairment Mol. Cell. Endocrinol. 384 2014 1 11
20. B. D'Haene, P. Mestdagh, J. Hellemans, and J. Vandesompele miRNA expression profiling: from reference genes to global mean normalization Methods Mol. Biol. 822 2012 261 272
21. E. Dardenne, M. Polay Espinoza, L. Fattet, S. Germann, M.P. Lambert, H. Neil, E. Zonta, H. Mortada, L. Gratadou, M. Deygas, F.Z. Chakrama, S. Samaan, F.O. Desmet, L.C. Tranchevent, M. Dutertre, R. Rimokh, C.F. Bourgeois, and D. Auboeuf RNA helicases DDX5 and DDX17 dynamically orchestrate transcription, miRNA, and splicing programs in cell differentiation Cell Rep. 7 2014 1900 1913
22. A. Deo, J. Carlsson, and A. Lindlof How to choose a normalization strategy for miRNA quantitative real-time (qPCR) arrays J. Bioinform. Comput. Biol. 9 2011 795 812
23. M. Diedrich, L. Mao, C. Bernreuther, C. Zabel, G. Nebrich, R. Kleene, and J. Klose Proteome analysis of ventral midbrain in MPTP-treated normal and L1cam transgenic mice Proteomics 8 2008 1266 1275
24. E. Doxakis Post-transcriptional regulation of alpha-synuclein expression by mir-7 and mir-153 J. Biol. Chem. 285 2010 12726 12734
25. L. Du, and A. Pertsemlidis Cancer and neurodegenerative disorders: pathogenic convergence through microRNA regulation. J Mol. Cell. Biol. 3 2011 176 180
26. P. Du, W.A. Kibbe, and S.M. Lin lumi: a pipeline for processing Illumina microarray Bioinformatics 24 2008 1547 1548
27. M. Elstner, C.M. Morris, K. Heim, A. Bender, D. Mehta, E. Jaros, T. Klopstock, T. Meitinger, D.M. Turnbull, and H. Prokisch Expression analysis of dopaminergic neurons in Parkinson's disease and aging links transcriptional dysregulation of energy metabolism to cell death Acta Neuropathol. 122 2011 75 86
28. J.L. Esguerra, C. Bolmeson, C.M. Cilio, and L. Eliasson Differential glucose-regulation of microRNAs in pancreatic islets of non-obese type 2 diabetes model Goto-Kakizaki rat PLoS One 6 2011 e18613
29. R.J. Frost, and E.N. Olson Control of glucose homeostasis and insulin sensitivity by the Let-7 family of microRNAs Proc. Natl. Acad. Sci. U. S. A. 108 2011 21075 21080
30. F.V. Fuller-Pace The DEAD box proteins DDX5 (p68) and DDX17 (p72): multi-tasking transcriptional regulators Biochim. Biophys. Acta 1829 2013 756 763
31. Z. Gao, H.J. Fu, J.J. Xue, Z.X. Wu, and L.B. Zhao Genetic polymorphisms in VDR, ESR1 and ESR2 genes may contribute to susceptibility to Parkinson's disease: a meta-analysis Mol. Biol. Rep. 41 2014 4463 4474
32. S. Gehrke, Y. Imai, N. Sokol, and B. Lu Pathogenic LRRK2 negatively regulates microRNA-mediated translational repression Nature 466 2010 637 641
33. B.J. Gentil, and L. Cooper Molecular basis of axonal dysfunction and traffic impairments in CMT Brain Res. Bull. 88 2012 444 453
34. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, K. Hornik, T. Hothorn, W. Huber, S. Iacus, R. Irizarry, F. Leisch, C. Li, M. Maechler, A.J. Rossini, G. Sawitzki, C. Smith, G. Smyth, L. Tierney, J.Y. Yang, and J. Zhang Bioconductor: open software development for computational biology and bioinformatics Genome Biol. 5 2004 R80
35. I. Gerin, G.T. Bommer, C.S. McCoin, K.M. Sousa, V. Krishnan, and O.A. MacDougald Roles for miRNA-378/378 in adipocyte gene expression and lipogenesis Am. J. Physiol. Endocrinol. Metab. 299 2010 E198 E206
36. K.M. Giles, R.A. Brown, M.R. Epis, F.C. Kalinowski, and P.J. Leedman miRNA-7-5p inhibits melanoma cell migration and invasion Biochem. Biophys. Res Commun. 430 2013 706 710
37. B. Gurung, A.B. Muhammad, and X. Hua Menin is required for optimal processing of the microRNA let-7a J. Biol. Chem. 289 2014 9902 9908
38. G.A. Han, N.T. Malintan, B.M. Collins, F.A. Meunier, and S. Sugita Munc18-1 as a key regulator of neurosecretion J. Neurochem. 115 2010 1 10
39. R. Havekes, D.A. Canton, A.J. Park, T. Huang, T. Nie, J.P. Day, L.A. Guercio, Q. Grimes, V. Luczak, I.H. Gelman, G.S. Baillie, J.D. Scott, and T. Abel Gravin orchestrates protein kinase A and beta2-adrenergic receptor signaling critical for synaptic plasticity and memory J. Neurosci. 32 2012 18137 18149
40. S.M. Heman-Ackah, M. Hallegger, M.S. Rao, and M.J. Wood RISC in PD: the impact of microRNAs in Parkinson's disease cellular and molecular pathogenesis Front. Mol. Neurosci. 6 2013 40
41. N.T. Hertz, A. Berthet, M.L. Sos, K.S. Thorn, A.L. Burlingame, K. Nakamura, and K.M. Shokat A neo-substrate that amplifies catalytic activity of parkinson's-disease-related kinase PINK1 Cell 154 2013 737 747
42. P. Hulley, M. Schachner, and H. Lubbert L1 neural cell adhesion molecule is a survival factor for fetal dopaminergic neurons J. Neurosci. Res. 53 1998 129 134
43. M. Ishtiaq, D. Campos-Melo, K. Volkening, and M.J. Strong Analysis of novel NEFL mRNA targeting microRNAs in amyotrophic lateral sclerosis PLoS One 9 2014 e85653
44. L.C. Jellen, L. Lu, X. Wang, E.L. Unger, C.J. Earley, R.P. Allen, R.W. Williams, and B.C. Jones Iron deficiency alters expression of dopamine-related genes in the ventral midbrain in mice Neuroscience 252 2013 13 23
45. E. Junn, K.W. Lee, B.S. Jeong, T.W. Chan, J.Y. Im, and M.M. Mouradian Repression of alpha-synuclein expression and toxicity by microRNA-7 Proc. Natl. Acad. Sci. U. S. A. 106 2009 13052 13057
46. S. Kabaria, D.C. Choi, A.D. Chaudhuri, M.M. Mouradian, and E. Junn Inhibition of miR-34b and miR-34c enhances alpha-synuclein expression in Parkinson's disease FEBS Lett. 589 2015 319 325
47. R. Kang, H.J. Zeh, M.T. Lotze, and D. Tang The Beclin 1 network regulates autophagy and apoptosis Cell Death Differ. 18 2011 571 580
48. G. Keilhoff, S. Wiegand, and H. Fansa Vav deficiency impedes peripheral nerve regeneration in mice Restor. Neurol. Neurosci. 30 2012 463 479
49. J. Kim, K. Inoue, J. Ishii, W.B. Vanti, S.V. Voronov, E. Murchison, G. Hannon, and A. Abeliovich A MicroRNA feedback circuit in midbrain dopamine neurons Science 317 2007 1220 1224
50. W. Kim, Y. Lee, N.D. McKenna, M. Yi, F. Simunovic, Y. Wang, B. Kong, R.J. Rooney, H. Seo, R.M. Stephens, and K.C. Sonntag miR-126 contributes to Parkinson's disease by dysregulating the insulin-like growth factor/phosphoinositide 3-kinase signaling Neurobiol. Aging 35 2014 1712 1721
51. W. Kim, H. Noh, Y. Lee, J. Jeon, A. Shanmugavadivu, D.L. McPhie, K.S. Kim, B.M. Cohen, H. Seo, and K.C. Sonntag MiR-126 regulates growth factor activities and vulnerability to toxic insult in neurons Mol Neurobiol. 2014 17 [Epub ahead of print]
52. M. Klauzinska, N.P. Castro, M.C. Rangel, B.T. Spike, P.C. Gray, D. Bertolette, F. Cuttitta, and D. Salomon The multifaceted role of the embryonic gene Cripto-1 in cancer, stem cells and epithelial-mesenchymal transition Semin. Cancer Biol. 29C 2014 51 58
53. A. Kramer, J. Green, J. Pollard Jr., and S. Tugendreich Causal analysis approaches in ingenuity pathway analysis Bioinformatics 30 2014 523 530
54. H. Lang, Z. Ai, Z. You, Y. Wan, W. Guo, J. Xiao, and X. Jin Characterization of miRNA218/322-Stxbp1 pathway in the process of insulin secretion J. Mol. Endocrinol. 2014
55. Y. Li, and X. Shi MicroRNAs in the regulation of TLR and RIG-I pathways Cell. Mol. Immunol. 10 2013 65 71
56. W. Lin, N.L. Wadlington, L. Chen, X. Zhuang, J.R. Brorson, and U.J. Kang Loss of PINK1 attenuates HIF-1alpha induction by preventing 4E-BP1-dependent switch in protein translation under hypoxia J. Neurosci. 34 2014 3079 3089
57. L. Ma, L. Wei, F. Wu, Z. Hu, Z. Liu, and W. Yuan Advances with microRNAs in Parkinson's disease research Drug Des. Dev. Ther. 7 2013 1103 1113
58. A.K. Mankan, M.W. Lawless, S.G. Gray, D. Kelleher, and R. McManus NF-kappaB regulation: the nuclear response J. Cell. Mol. Med. 13 2009 631 643
59. P. Mestdagh, P. Van Vlierberghe, A. De Weer, D. Muth, F. Westermann, F. Speleman, and J. Vandesompele A novel and universal method for microRNA RT-qPCR data normalization Genome Biol. 10 2009 R64
60. J. Michels, O. Kepp, L. Senovilla, D. Lissa, M. Castedo, G. Kroemer, and L. Galluzzi Functions of BCL-X L at the interface between cell death and metabolism Int. J. Cell Biol. 2013 2013 705294
61. E. Minones-Moyano, S. Porta, G. Escaramis, R. Rabionet, S. Iraola, B. Kagerbauer, Y. Espinosa-Parrilla, I. Ferrer, X. Estivill, and E. Marti MicroRNA profiling of Parkinson's disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function Hum. Genet. 20 2011 3067 3078
62. P.T. Nelson, W.X. Wang, and B.W. Rajeev MicroRNAs (miRNAs) in neurodegenerative diseases Brain Pathol. 18 2008 130 138
63. A.T. Nies, G. Jedlitschky, J. Konig, C. Herold-Mende, H.H. Steiner, H.P. Schmitt, and D. Keppler Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain Neuroscience 129 2004 349 360
64. J.M. Palacios, G. Mengod, M.T. Vilaro, and P. Ramm Recent trends in receptor analysis techniques and instrumentation J. Chem. Neuroanat. 4 1991 343 353
65. N. Palacios, M. Weisskopf, K. Simon, X. Gao, M. Schwarzschild, and A. Ascherio Polymorphisms of caffeine metabolism and estrogen receptor genes and risk of Parkinson's disease in men and women Parkinsonism Relat. Disord. 16 2010 370 375
66. M. Parsanejad, Y. Zhang, D. Qu, I. Irrcher, M.W. Rousseaux, H. Aleyasin, F. Kamkar, S. Callaghan, R.S. Slack, T.W. Mak, S. Lee, D. Figeys, and D.S. Park Regulation of the VHL/HIF-1 pathway by DJ-1 J. Neurosci. 34 2014 8043 8050
67. E. Pena-Altamira, E. Polazzi, E. Moretto, M. Lauriola, and B. Monti The transcription factor CCAAT enhancer-binding protein beta protects rat cerebellar granule neurons from apoptosis through its transcription-activating isoforms Eur. J. Neurosci. 39 2014 176 185
68. J.P. Pierce, T. Mayer, and J.B. McCarthy Evidence for a satellite secretory pathway in neuronal dendritic spines Curr. Biol. 11 2001 351 355
69. C.Y. Pietersen, M.P. Lim, L. Macey, T.U. Woo, and K.C. Sonntag Neuronal type-specific gene expression profiling and laser-capture microdissection Methods Mol. Biol. 755 2011 327 343
70. W.J. Poppinga, P. Munoz-Llancao, C. Gonzalez-Billault, and M. Schmidt A-kinase anchoring proteins: cAMP compartmentalization in neurodegenerative and obstructive pulmonary diseases Br. J. Pharmacol. 171 2014 5603 5623
71. C. Quevedo, V. Sauzeau, M. Menacho-Marquez, A. Castro-Castro, and X.R. Bustelo Vav3-deficient mice exhibit a transient delay in cerebellar development Mol. Biol. Cell 21 2010 1125 1139
72. H. Rakshit, N. Rathi, and D. Roy Construction and analysis of the protein-protein interaction networks based on gene expression profiles of Parkinson's disease PLoS One 9 2014 e103047
73. H. Ren, K. Fu, C. Mu, X. Zhen, and G. Wang L166P mutant DJ-1 promotes cell death by dissociating Bax from mitochondrial Bcl-XL Mol. Neurodegener. 7 2012 40
74. V. Rottiers, S.H. Najafi-Shoushtari, F. Kristo, S. Gurumurthy, L. Zhong, Y. Li, D.E. Cohen, R.E. Gerszten, N. Bardeesy, R. Mostoslavsky, and A.M. Naar MicroRNAs in metabolism and metabolic diseases Cold Spring Harb. Symp. Quant. Biol. 76 2011 225 233
75. M.M. Salama Huwe1: a possible role in PD Med. Hypotheses 79 2012 419
76. M. Sang, L. Ma, M. Sang, X. Zhou, W. Gao, and C. Geng LIM-domain-only proteins: multifunctional nuclear transcription coregulators that interacts with diverse proteins Mol. Biol. Rep. 41 2014 1067 1073
77. V. Sauzeau, J.A. Horta-Junior, A.S. Riolobos, G. Fernandez, M.A. Sevilla, D.E. Lopez, M.J. Montero, B. Rico, and X.R. Bustelo Vav3 is involved in GABAergic axon guidance events important for the proper function of brainstem neurons controlling cardiovascular, respiratory, and renal parameters Mol. Biol. Cell. 21 2010 4251 4263
78. A.H. Schapira, and P. Jenner Etiology and pathogenesis of Parkinson's disease Mov. Disord. 26 2011 1049 1055
79. C. Schiesling, N. Kieper, K. Seidel, and R. Kruger Review: familial Parkinson's disease - genetics, clinical phenotype and neuropathology in relation to the common sporadic form of the disease Neuropathol. Appl. Neurobiol. 34 2008 255 271
80. E.G. Seiz, M. Ramos-Gomez, E.T. Courtois, J. Tonnesen, M. Kokaia, I. Liste Noya, and A. Martinez-Serrano Human midbrain precursors activate the expected developmental genetic program and differentiate long-term to functional A9 dopamine neurons in vitro. Enhancement by Bcl-X(L) Exp. Cell. Res. 318 2012 2446 2459
81. I. Shaked, A. Meerson, Y. Wolf, R. Avni, D. Greenberg, A. Gilboa-Geffen, and H. Soreq MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesterase Immunity 31 2009 965 973
82. T. Shathasivam, T. Kislinger, and A.O. Gramolini Genes, proteins and complexes: the multifaceted nature of FHL family proteins in diverse tissues J Cell Mol Med. 14 2010 2702 2720
83. F. Simunovic, M. Yi, Y. Wang, L. Macey, L.T. Brown, A.M. Krichevsky, S.L. Andersen, R.M. Stephens, F.M. Benes, and K.C. Sonntag Gene expression profiling of substantia nigra dopamine neurons: further insights into Parkinson's disease pathology Brain 132 2009 1795 1809
84. F. Simunovic, M. Yi, Y. Wang, R. Stephens, and K.C. Sonntag Evidence for gender-specific transcriptional profiles of nigral dopamine neurons in Parkinson disease PLoS One 5 2010 e8856
85. G.K. Smyth limma: linear models for microarray data R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, W. Huber, Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005 397 420
86. K.C. Sonntag MicroRNAs and deregulated gene expression networks in neurodegeneration Brain Res. 1338 2010 48 57
87. K.C. Sonntag, T.U. Woo, and A.M. Krichevsky Converging miRNA functions in diverse brain disorders: a case for miR-124 and miR-126 Exp. Neurol. 235 2012 427 435
88. A. Tsujimura, K. Taguchi, Y. Watanabe, H. Tatebe, T. Tokuda, T. Mizuno, and M. Tanaka Lysosomal enzyme cathepsin B enhances the aggregate forming activity of exogenous alpha-synuclein fibrils Neurobiol. Dis. 73C 2014 244 253
89. S. Venkataraman, D.K. Birks, I. Balakrishnan, I. Alimova, P.S. Harris, P.R. Patel, M.H. Handler, A. Dubuc, M.D. Taylor, N.K. Foreman, and R. Vibhakar MicroRNA 218 acts as a tumor suppressor by targeting multiple cancer phenotype-associated genes in medulloblastoma J. Biol. Chem. 288 2013 1918 1928
90. G. Wang, J.M. van der Walt, G. Mayhew, Y.J. Li, S. Zuchner, W.K. Scott, E.R. Martin, and J.M. Vance Variation in the miRNA-433 binding site of FGF20 confers risk for Parkinson disease by overexpression of alpha-synuclein Am. J. Hum. Genet. 82 2008 283 289
91. F. Wen, Y. Yang, D. Jin, J. Sun, X. Yu, and Z. Yang MiRNA-145 is involved in the development of resistin-induced insulin resistance in HepG2 cells Biochem. Biophys. Res. Commun. 445 2014 517 523
92. K. Wirdefeldt, H.O. Adami, P. Cole, D. Trichopoulos, and J. Mandel Epidemiology and etiology of Parkinson's disease: a review of the evidence Eur. J. Epidemiol. 26 Suppl 1 2011 S1 58
93. G. Wong, and R. Nass miRNAs and their putative roles in the development and progression of Parkinson's disease Front. Genet. 3 2012 315
94. Q. Wu, Z. Yang, L. Xia, Y. Nie, K. Wu, Y. Shi, and D. Fan Methylation of miR-129-5p CpG island modulates multi-drug resistance in gastric cancer by targeting ABC transporters Oncotarget 5 2014 11552 11563
95. Y. Wu, X. Li, W. Xie, J. Jankovic, W. Le, and T. Pan Neuroprotection of deferoxamine on rotenone-induced injury via accumulation of HIF-1 alpha and induction of autophagy in SH-SY5Y cells Neurochem. Int. 57 2010 198 205
96. D. Yang, T. Li, Y. Wang, Y. Tang, H. Cui, Y. Tang, X. Zhang, D. Chen, N. Shen, and W. Le miR-132 regulates the differentiation of dopamine neurons by directly targeting Nurr1 expression J. Cell. Sci. 125 2012 1673 1682
97. J. Zhou, Q. Liu, M. Mao, and Y. Tong Huwe1 as a therapeutic target for neural injury Genet. Mol. Res. 13 2014 4320 4325
98. H. Zhu, N. Shyh-Chang, A.V. Segre, G. Shinoda, S.P. Shah, W.S. Einhorn, A. Takeuchi, J.M. Engreitz, J.P. Hagan, M.G. Kharas, A. Urbach, J.E. Thornton, R. Triboulet, R.I. Gregory, D. Consortium, M. Investigators, D. Altshuler, and G.Q. Daley The Lin28/let-7 axis regulates glucose metabolism Cell 147 2011 81 94
99. Y. Zhu, F. Yu, Y. Jiao, J. Feng, W. Tang, H. Yao, C. Gong, J. Chen, F. Su, Y. Zhang, and E. Song Reduced miR-128 in breast tumor-initiating cells induces chemotherapeutic resistance via Bmi-1 and ABCC5 Clin. Cancer Res. 17 2011 7105 7115