Lack of miRNA misregulation at early pathological stages in Drosophila neurodegenerative disease models

Frontiers in Genetics

Volumn 3, Issue OCT, 2012, Pages

  Reinhardt, Anita ^a   Feuillette, Sébastien ^b,c   Cassar, Marlène ^d   Callens, Céline ^d   Thomassin, Hélène ^e   Birman, Serge ^d   Lecourtois, Magalie ^b,c   Antoniewski, Christophe ^e   Tricoire, Hervé ^a  

^a Groupe Hospitalier Pitié Salpêtrière   (France)

^b INSERM   (France)

^c UNIVERSITY OF ROUEN   (France)

^d CNRS   (France)

^e Sorbonne Universités   (France)

Author keywords

Ataxia; Deep sequencing; Frontotemporal lobar degeneration; miRNA; Neurodegenerative diseases; Parkinson disease; Polyq diseases

Indexed keywords

ANIMALIA;

EID: 84876144212     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2012.00226     Document Type: Article

References (74)

1. Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol. 11,R106.
2. Asikainen, S., Rudgalvyte, M., Heikki-nen, L., Louhiranta, K., Lakso, M., Wong, G., et al. (2010). Global microRNA expression profiling of Caenorhabditis elegans Parkinson's disease models. J. Mol. Neurosci. 41, 210-218.
3. Bak, M., Silahtaroglu, A., Møller, M., Christensen, M., Rath, M. E, Skryabin, B., et al. (2008). MicroRNA expression in the adult mouse central nervous system. RNA 14,432-444.
4. Bañez-Coronel, M., Porta, S., Kager-Bauer, B., Mateu-Huertas, E., Pantano, L., Ferrer, I., et al. (2012). A pathogenic mechanism in Hunt-ington's disease involves small CAG-repeated RNAs with neurotoxic activity. PLoS Genet. 8, e1002481. doi:10.1371/journal.pgen.1002481
5. Berezikov, E., Robine, N., Samsonova, A., Westholm, J. O., Naqvi, A., Hung, J. H., et al. (2011). Deep annotation of Drosophila melanogaster microR-NAs yields insights into their processing, modification, and emergence. Genome Res. 21,203-215.
6. Bilen, J., Liu, N., Burnett, B. G., Pittman, R. N., and Bonini, N. M. (2006). MicroRNA pathways modulate polyglutamine-induced neuro degeneration. Mol Cell 24, 157-163.
7. Brookmeyer, R., Evans, D. A., Hebert, L., Langa, K. M., Heeringa, S. G., Plassman, B. L., et al. (2011). National estimates of the prevalence of Alzheimer's disease in the United States. Alzheimers Dement. 7, 61-73.
8. Buratti, E., De Conti, L., Stuani, C., Romano, M., Baralle, M., and Bar-alle, E (2010). Nuclear factor TDP-43 can affect selected microRNA levels. FEBSJ. 277, 2268-2281.
9. Bushati, N., and Cohen, S. M. (2007). microRNA functions. Annu. Rev. Cell Dev. Biol. 23, 175-205.
10. Cannon, J. R., and Greenamyre, J. T. (2010). Neurotoxic in vivo models of Parkinson's disease recent advances. Prog. Brain Res. 184,17-33.
11. Chaudhuri, A., Bowling, K., Funder-burk, C., Lawal, H., Inamdar, A., Wang,Z.,etal. (2007). Interaction of genetic and environmental factors in a Drosophila parkinsonism mo del. J. Neurosci. 27, 2457-2467.
12. Chung, D. W., Rudnicki, D. D., Yu, L., andMargolis,R.L. (2011). Anatural antisense transcript at the Hunting-ton's disease repeat locus regulates HTT expression. Hum. Mol. Genet. 20,3467-3477.
13. Chung, W.-J., Okamura, K., Martin, R., and Lai, E. C. (2008). Endogenous RNA interference provides a somatic defense against Drosophila transposons. Curr. Biol. 18, 795-802.
14. Cuellar, T. L., Davis, T. H., Nelson, P. T., Loeb, G. B., Harfe, B. D., Ullian, E., et al. (2008). Dicer loss in stri-atal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proc. Natl. Acad. Sci. U.S.A. 105, 5614-5619.
15. Delay, C., Mandemakers, W., and Hébert, S. S. (2012). MicroRNAs in Alzheimer's disease. Neurobiol Dis. 46, 285-290.
16. Eacker, S. M., Dawson, T. M., and Dawson, V. L. (2009). Understanding microRNAs in neurodegeneration. Nat. Rev. Neurosci. 10, 837-841.
17. Evert, B. O., Araujo, J., Vieira-Saecker, A. M., de Vos, R. A., Harendza, S., Klockgether, T., et al. (2006). Ataxin-3 represses transcription via chromatin binding, interaction with histone deacetylase 3, and his-tone deacetylation. J. Neurosci. 26, 11474-11486.
18. Feany, M. B., and Bender, W. W. (2000). A Drosophila model of Parkinson's disease. Nature 404, 394-398.
19. Fernandez-Funez, P., Nino-Rosales, M. L., de Gouyon, B., She, W. C., Luchak, J. M., Martinez, P., et al. (2000). Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408, 101-106.
20. Gascon, E., and Gao, F. B. (2012). Cause or effect: misregulation of microRNA pathways in neurodegeneration. Front. Neurosci. 6:48. doi:10.3389/fnins.2012.00048
21. Geekiyanage, H., and Chan, C. (2011). MicroRNA-137/181c regulates ser-ine palmitoyltransferase and in turn amyloid beta, novel targets in sporadic Alzheimer's disease. J. Neurosci. 31,14820-14830.
22. Gehrke, S., Imai, Y., Sokol, N., and Lu, B. (2010). Pathogenic LRRK2 nega tively regulates microRNA-mediated translational repression. Nature 466, 637-641.
23. Girardot, F., Monnier, V., and Tri-coire, H. (2004). Genome wide analysis of common and specific stress responses in adult Drosophila melanogaster. BMC Genomics 5, 74. doi:10.1186/1471-2164-5-74.
24. Gregory, R. I., Yan, K. P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N., et al. (2004). The Microprocessor complex mediates the genesis of microRNAs. Nature 432,235-240.
25. Hebert, S. S., Horre, K., Nicolai, L., Papadopoulou, A. S., Mandemakers, W., Silahtaroglu, A. N., et al. (2008). Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc. Natl. Acad. Sci. U.S.A. 105, 6415-6420.
26. Hébert, S. S., Papadopoulou, A. S., Smith, P., Galas, M. C., Planel, E., Silahtaroglu, A. N., et al. (2010). Genetic ablation of Dicer in adult forebrain neurons results in abnormal tau hyperphosphoryla-tion and neurodegeneration. Hum. Mol. Genet. 19, 3959-3969.
27. Helmlinger, D., Hardy, S., Abou-Sleymane, G., Eberlin, A., Bowman, A. B., Gansmüller, A., et al. (2006).Glutamine-expanded ataxin-7 alters TFTC/STAGA recruitment and chromatin structure leading to photoreceptor dysfunction. PLoS Biol. 4, e67. doi:10.1371/journal.pbio.0040067
28. Hsu, R. J., Hsiao, K. K., Lin, M. J., Li, C. Y., Wang, L. C., Chen, L. K., et al. (2011). Long tract of untranslated CAG repeats is deleterious in trans-genic mice. PLoS One 6, e16417. doi:10.1371/journal.pone.0016417
29. Johnson, R., Zuccato, C., Belyaev, N. D., Guest, D. J., Cattaneo, E., and Buckley, N. J. (2008). A microRNA-based gene dysregulation pathway in Huntington's disease. Neurobiol. Dis. 29, 438-445.
30. Jucker, M., and Walker, L. C. (2011). Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann. Neurol. 70, 532-540.
31. Kanao, T., Venderova, K., Park, D. S., Unterman, T., Lu, B., and Imai, Y (2010). Activation of FoxO by LRRK2 induces expression of proapoptotic proteins and alters survival of postmitotic dopaminergic neuron in Drosophila. Hum. Mol. Genet. 19, 3747-3758.
32. Kapsimali, M., Kloosterman, W P., de Bruijn, E., Rosa, F., Plas-terk, R. H., and Wilson, S. W. (2007). MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biol. 8, R173.
33. Kaur, P., Armugam, A., and Jeyaseelan, K. (2012). MicroRNAs in neurotox-icity. J. Toxicol. 2012, 870150.
34. Kawahara, Y., and Mieda-Sato, A. (2012). TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc. Natl. Acad. Sci. U.S.A. 109, 3347-3352.
35. Kim, J., Inoue, K., Ishii, J., Vanti, W B., Voronov, S. V., Murchison, E., et al. (2007). A MicroRNA feedback circuit in midbrain dopamine neurons. Science 317,1220-1224.
36. Kloosterman, W P., and Plasterk, R. H. (2006). The diverse functions of microRNAs in animal development and disease. Dev. Cell 11, 441-450.
37. Kosik, K. S. (2006). The neuronal microRNA system. Nat. Rev. Neurosci. 7,911-920.
38. Krol, J., Loedige, I., and Filipowicz, W. (2010). The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597-610.
39. Lam, Y. C., Bowman, A. B., Jafar-Nejad, P., Lim, J., Richman, R., Fryer, J. D., et al. (2006). ATAXIN-1 interacts with the repressor Capicua in its native complex to cause SCA1 neu-ropathology. Cell 127, 1335-1347.
40. Lanson, N. A. Jr., Maltare, A., King, H., Smith, R., Kim, J. H., Taylor, J. P., et al. (2011). A Drosophila model of FUS-related neurodegeneration reveals genetic interaction between FUS and TDP-43. Hum. Mol. Genet. 20,2510-2523.
41. Latouche, M., Lasbleiz, C., Martin, E., Monnier, V., Debeir, T., Mouatt-Prigent, A., et al. (2007). A conditional pan-neuronal Drosophila model of spinocerebellar ataxia 7 with a reversible adult phe-notype suitable for identifying modifier genes. J. Neurosci. 27, 2483-2492.
42. Lau, P., and de Strooper, B. (2010). Dys-regulated microRNAs in neurodegenerative disorders. Semin. Cell Dev. Biol. 21, 768-773.
43. Lee, Y., Samaco, R. C., Gatchel, J. R., Thaller, C., Orr, H. T., and Zoghbi, H. Y. (2008). miR-19, miR-101 and miR-130 co-regulate ATXN1 levels to potentially modulate SCA1 pathogenesis. Nat. Neurosci. 11, 1137-1139.
44. Li, L. B., Yu, Z., Teng, X., and Bonini, N. M. (2008). RNA toxicity is a component of ataxin-3 degeneration in Drosophila. Nature 453, 1107-1111.
45. Li, Y. Y., Cui, J. G., Hill, J. M., Bhat-tacharjee, S., Zhao, Y., and Lukiw, W. J. (2011). Increased expression of miRNA-146a in Alzheimer's disease transgenic mouse models. Neurosci. Lett. 487, 94-98.
46. Lukiw, W. J., and Alexandrov, P. N. (2012). Regulation of Complement Factor H (CFH) by Multiple miRNAs in Alzheimer's Disease (AD) Brain. Mol Neurobiol. PMID:22302353. [Epub ahead of print].
47. Martí, E., Pantano, L., Bañez-Coronel, M., Llorens, F., Miñones-Moyano, E., Porta, S., et al. (2010). A myriad of miRNA variants in control and Huntington's disease brain regions detected by massively parallel sequencing. Nucleic Acids Res. 38, 7219-7235.
48. Martin-Lannerée, S., Lasbleiz, C., Sanial, M., Fouix, S., Besse, F., Tricoire, H., et al. (2006). Characterization of the Drosophila myeloid leukemia factor. Genes cells 11, 1317-1335.
49. McCann, C., Holohan, E. E., Das, S., Dervan, A., Larkin, A., Lee, J. A., et al. (2011). The Ataxin-2 protein is required for microRNA function and synapse-specific long-term olfactory habituation. Proc. Natl. Acad. Sci U.S.A. 108, E655-E662.
50. Miguel, L., Avequin, T., Delarue, M., Feuillette, S., Frébourg, T., Campion, D., et al. (2012). Accumulation of insoluble forms of FUS protein correlates with toxicity in Drosophila. Neurobiol. Aging 33, 1008.e1-1008.e15.
51. Miguel, L., Frébourg, T., Campion, D., and Lecourtois, M. (2011). Both cytoplasmic and nuclear accumulations of the protein are neurotoxic in Drosophila models of TDP-43 proteinopathies. Neurobiol. Dis. 41, 398-406.
52. Minones-Moyano, E., Porta, S., Escaramis, G., Rabionet, R., Iraola, S., Kagerbauer, B., et al. (2011). MicroRNA profiling of Parkinson's disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function. Hum. Mol. Genet. 20, 3067-3078.
53. Mueller, T., Breuer, P., Schmitt, I., Walter, J., Evert, B. O., and Wüll-ner, U. (2009). CK2-dependent phosphorylation determines cellular localization and stability of ataxin-3. Hum. Mol. Genet. 18, 3334-3343.
54. Newman, M. A., and Hammond, S. M. (2010). Emerging paradigms of regulated microRNA processing. Genes Dev. 24, 1086-1092.
55. Osterwalder, T., Yoon, K. S., White, B. H., and Keshishian, H. (2001). A conditional tissue-specific transgene expression system using inducible GAL4. Proc. Natl. Acad. Sci. U.S.A. 98, 12596-12601.
56. Packer, A. N., Xing, Y., Harper, S. Q., Jones, L., and Davidson, B. L. (2008). The bifunctional microRNA miR-9/miR-9 regulates REST and CoREST and is downregulated in Huntington's disease. J. Neurosci. 28, 14341-14346.
57. Pandey, U. B., Nie, Z., Batlevi, Y., McCray, B. A., Ritson, G. P., Nedel-sky, N. B., et al. (2007). HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447, 859-863.
58. Pereira, J. A., Baumann, R., Norrmén, C., Somandin, C., Miehe, M., Jacob, C., et al. (2010). Dicer in Schwann cells is required for myelination and axonal integrity. J. Neurosci. 30, 6763-6775.
59. Rogers, I., Kerr, F., Martinez, P., Hardy, J., Lovestone, S., and Partridge, L. (2012). Ageing increases vulnerability to aβ42 toxicity in Drosophila. PLoS One 7, e40569. doi:10.1371/journal.pone. 0040569
60. Schonrock, N., Ke, Y. D., Humphreys, D., Staufenbiel, M., Ittner, L. M., Preiss, T., et al. (2010). Neuronal microRNA deregulation in response to Alzheimer's disease amyloid-beta. PLoS One 5, e1 1070. doi: 10.1371/journal.pone.0011070
61. Schaefer, A., O'Carroll, D., Tan, C. L., Hillman, D., Sugimori, M., Lli-nas, R., et al. (2007). Cerebellar neurodegeneration in the absence of microRNAs. J. Exp. Med. 204, 1553-1558.
62. Sethi, P., and Lukiw, W. J. (2009). Micro-RNA abundance and stability in human brain: specific alterations in Alzheimer's disease temporal lobe neocortex. Neurosci. Lett. 459, 100-104.
63. Shin, D., Shin, J. Y., McManus, M. T., Ptácek, L. J., and Fu, Y. H. (2009). Dicer ablation in oligodendrocytes provokes neuronal impairment in mice. Ann. Neurol. 66, 843-857.
64. Shioya, M., Obayashi, S., Tabunoki, H., Arima, K., Saito, Y., Ishida, T., et al. (2010). Aberrant microRNA expression in the brains of neurodegenerative diseases: miR-29a decreased in Alzheimer disease brains targets neurone navigator 3. Neuropathol. Appl. Neurobiol. 36, 320-330.
65. Siomi, H., and Siomi, M. C. (2010). Posttranscriptional regulation of microRNA biogenesis in animals. Mol. Cell 38, 323-332.
66. Smith, P., Al Hashimi, A., Girard, J., Delay, C., and Hebert, S. S. (2011). In vivo regulation of amyloid precursor protein neuronal splicing by microRNAs. J. Neurochem. 116, 240-247.
67. Sofola, O., Kerr, F., Rogers, I., Killick, R., Augustin,H.,Gandy,C.,etal. (2010). Inhibition of GSK-3 ameliorates Abeta pathology in an adult-onset Drosophila model of Alzheimer's disease. PLoS Genet. 6, e1001087. doi:10.1371/journal.pgen. 1001087
68. Tanner, C. M., Kamel, F., Ross, G. W., Hoppin, J. A., Goldman, S. M., Korell, M., et al. (2011). Rotenone, paraquat, and Parkinson's disease. Environ. Health Perspect. 119,866-872.
69. Tao, J., Wu, H., Lin, Q., Wei, W., Lu, X., Cantle, J. P., et al. (2011). Deletion of astroglial Dicer causes non-cell-autonomous neuronal dysfunction and degeneration. J. Neurosci. 31,8306-8319.
70. Wang, L. C., Chen, K. Y., Pan, H., Wu, C., Chen, P. H., Liao, Y., et al. (2011). Muscleblind participates in RNA toxicity of expanded CAG and CUG repeats in Caenorhabdi-tis elegans. Cell. Mol. Life Sci. 68, 1255-1267.
71. Wang, X., Liu, P., Zhu, H., Xu, Y., Ma, C., Dai, X., et al. (2009). miR-34a, a microRNA up-regulated in a double transgenic mouse model of Alzheimer's disease, inhibits bcl2 translation. Brain. Res. Bull. 80, 268-273.
72. Wittmann, C. W., Wszolek, M. F., Shulman, J. M., Salvaterra, P. M., Lewis, J., Hutton, M., et al. (2001). Tauopathy in Drosophila: neurodegeneration without neu-rofibrillary tangles. Science 293, 711-714.
73. Yankner, B. A., Lu, T., and Loerch, P. (2008). The aging brain. Annu. Rev. Pathol. 3,41-66.
74. Zou, S., Meadows, S., Sharp, L., Jan, L. Y., and Jan, Y N. (2000). Genome-wide study of aging and oxidative stress response in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 97, 13726-13731.