Evidence for a neuroprotective microRNA pathway in amnestic mild cognitive impairment

Frontiers in Neuroscience

Volumn 9, Issue NOV, 2015, Pages

  Weinberg, Rebecca B ^a   Mufson, Elliott J ^b   Counts, Scott E ^a,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b BARROW NEUROLOGICAL INSTITUTE   (United States)

^c St Mary's Mercy Medical Center   (United States)

Author keywords

Alzheimer's disease; Frontal cortex; Gene expression regulation; MicroRNAs; Mild cognitive impairment; MiR 212; MiR 23a; Sirtuin 1

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; MICRORNA; MICRORNA 132; MICRORNA 140 3P; MICRORNA 150; MICRORNA 181A; MICRORNA 21; MICRORNA 212; MICRORNA 23A; MICRORNA 23B; MICRORNA 498; MICRORNA 886 3P; MICRORNA LET 7D; SIRTUIN 1; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DISEASE COURSE; DOWN REGULATION; FEMALE; FRONTAL CORTEX; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE LOCATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INFERIOR TEMPORAL CORTEX; MALE; MILD COGNITIVE IMPAIRMENT; NEUROPROTECTION; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SIRT1 GENE; UPREGULATION; VERY ELDERLY;

EID: 84949562692     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00430     Document Type: Article

References (67)

1. Absalon, S., Kochanek, D. M., Raghavan, V., and Krichevsky, A. M. (2013). MiR-26b, upregulated in Alzheimer's disease, activates cell cycle entry, tau-phosphorylation, and apoptosis in postmitotic neurons. J. Neurosci. 33, 14645-14659. doi: 10.1523/JNEUROSCI.1327-13.2013.
2. Albert, M. S., Dekosky, S. T., Dickson, D., Dubois, B., Feldman, H. H., Fox, N. C., et al. (2011). The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 7, 270-279. doi: 10.1016/j.jalz.2011.03.008.
3. Alldred, M. J., Che, S., and Ginsberg, S. D. (2009). Terminal continuation (TC) RNA amplification without second strand synthesis. J. Neurosci. Methods 177, 381-385. doi: 10.1016/j.jneumeth.2008.10.027.
4. Andrews, P. W., Damjanov, I., Simon, D., Banting, G. S., Carlin, C., Dracopoli, N. C., et al. (1984). Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Differentiation in vivo and in vitro. Lab. Invest. 50, 147-162.
5. Aschrafi, A., Schwechter, A. D., Mameza, M. G., Natera-Naranjo, O., Gioio, A. E., and Kaplan, B. B. (2008). MicroRNA-338 regulates local cytochrome c oxidase IV mRNA levels and oxidative phosphorylation in the axons of sympathetic neurons. J. Neurosci. 28, 12581-12590. doi: 10.1523/JNEUROSCI.3338-08.2008.
6. Banzhaf-Strathmann, J., Benito, E., May, S., Arzberger, T., Tahirovic, S., Kretzschmar, H., et al. (2014). MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer's disease. EMBO J. 33, 1667-1680. doi: 10.15252/embj.201387576.
7. Bell, K. F., Bennett, D. A., and Cuello, A. C. (2007). Paradoxical upregulation of glutamatergic presynaptic boutons during mild cognitive impairment. J. Neurosci. 27, 10810-10817. doi: 10.1523/JNEUROSCI.3269-07.2007.
8. Bennett, D. A., Wilson, R. S., Schneider, J. A., Evans, D. A., Beckett, L. A., Aggarwal, N. T., et al. (2002). Natural history of mild cognitive impairment in older persons. Neurology 59, 198-205. doi: 10.1212/WNL.59.2.198.
9. Berchtold, N. C., Coleman, P. D., Cribbs, D. H., Rogers, J., Gillen, D. L., and Cotman, C. W. (2013). Synaptic genes are extensively downregulated across multiple brain regions in normal human aging and Alzheimer's disease. Neurobiol. Aging 34, 1653-1661. doi: 10.1016/j.neurobiolaging.2012.11.024.
10. Bonda, D. J., Lee, H. G., Camins, A., Pallas, M., Casadesus, G., Smith, M. A., et al. (2011). The sirtuin pathway in ageing and Alzheimer disease: mechanistic and therapeutic considerations. Lancet Neurol. 10, 275-279. doi: 10.1016/S1474-4422(11)70013-8.
11. Bossers, K., Wirz, K. T., Meerhoff, G. F., Essing, A. H., van Dongen, J. W., Houba, P., et al. (2010). Concerted changes in transcripts in the prefrontal cortex precede neuropathology in Alzheimer's disease. Brain 133, 3699-3723. doi: 10.1093/brain/awq258.
12. Braak, H., and Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82, 239-259. doi: 10.1007/BF00308809.
13. Brunet, A., Sweeney, L. B., Sturgill, J. F., Chua, K. F., Greer, P. L., Lin, Y., et al. (2004). Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303, 2011-2015. doi: 10.1126/science.1094637.
14. Che, H., Sun, L. H., Guo, F., Niu, H. F., Su, X. L., Bao, Y. N., et al. (2014). Expression of amyloid-associated miRNAs in both the forebrain cortex and hippocampus of middle-aged rat. Cell. Physiol. Biochem. 33, 11-22. doi: 10.1159/000356646.
15. Codocedo, J. F., Allard, C., Godoy, J. A., Varela-Nallar, L., and Inestrosa, N. C. (2012). SIRT1 regulates dendritic development in hippocampal neurons. PLoS ONE 7:e47073. doi: 10.1371/journal.pone.0047073.
16. Cogswell, J. P., Ward, J., Taylor, I. A., Waters, M., Shi, Y., Cannon, B., et al. (2008). Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimers Dis. 14, 27-41.
17. Cohen, T. J., Guo, J. L., Hurtado, D. E., Kwong, L. K., Mills, I. P., Trojanowski, J. Q., et al. (2011). The acetylation of tau inhibits its function and promotes pathological tau aggregation. Nat. Commun. 2, 252. doi: 10.1038/ncomms1255.
18. Conte, A., Pellegrini, S., and Tagliazucchi, D. (2003). Effect of resveratrol and catechin on PC12 tyrosine kinase activities and their synergistic protection from beta-amyloid toxicity. Drugs Exp. Clin. Res. 29, 243-255.
19. Counts, S. E., Alldred, M. J., Che, S., Ginsberg, S. D., and Mufson, E. J. (2013). Synaptic gene dysregulation within hippocampal CA1 pyramidal neurons in mild cognitive impairment. Neuropharmacology 79, 172-179. doi: 10.1016/j.neuropharm.2013.10.018.
20. Counts, S. E., He, B., Che, S., Ikonomovic, M. D., DeKosky, S. T., Ginsberg, S. D., et al. (2007). Alpha7 nicotinic receptor up-regulation in cholinergic basal forebrain neurons in Alzheimer disease. Arch. Neurol. 64, 1771-1776. doi: 10.1001/archneur.64.12.1771.
21. Counts, S. E., and Mufson, E. J. (2010). Noradrenaline activation of neurotrophic pathways protects against neuronal amyloid toxicity. J. Neurochem. 113, 649-660. doi: 10.1111/j.1471-4159.2010.06622.x.
22. Counts, S. E., Nadeem, M., Lad, S. P., Wuu, J., and Mufson, E. J. (2006). Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment. J. Neuropathol. Exp. Neurol. 65, 592-601. doi: 10.1097/00005072-200606000-00007.
23. Counts, S. E., Nadeem, M., Wuu, J., Ginsberg, S. D., Saragovi, H. U., and Mufson, E. J. (2004). Reduction of cortical TrkA but not p75(NTR) protein in early-stage Alzheimer's disease. Ann. Neurol. 56, 520-531. doi: 10.1002/ana.20233.
24. Cui, J. G., Li, Y. Y., Zhao, Y., Bhattacharjee, S., and Lukiw, W. J. (2010). Differential regulation of interleukin-1 receptor-associated kinase-1 (IRAK-1) and IRAK-2 by microRNA-146a and NF-kappaB in stressed human astroglial cells and in Alzheimer disease. J. Biol. Chem. 285, 38951-38960. doi: 10.1074/jbc. M110.178848.
25. DeKosky, S. T., Ikonomovic, M. D., Styren, S. D., Beckett, L., Wisniewski, S., Bennett, D. A., et al. (2002). Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment. Ann. Neurol. 51, 145-155. doi: 10.1002/ana.10069.
26. Doné, S. C., and Beltcheva, O. (2014). In situ hybridization detection of miRNA using LNA oligonucleotides. Methods Mol. Biol. 1182, 57-71. doi: 10.1007/978-1-4939-1062-5_6.
27. Fineberg, S. K., Kosik, K. S., and Davidson, B. L. (2009). MicroRNAs potentiate neural development. Neuron 64, 303-309. doi: 10.1016/j.neuron.2009.10.020.
28. Gao, J., Wang, W. Y., Mao, Y. W., Gräff, J., Guan, J. S., Pan, L., et al. (2010). A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466, 1105-1109. doi: 10.1038/nature09271.
29. Ginsberg, S. D. (2008). Transcriptional profiling of small samples in the central nervous system. Methods Mol. Biol. 439, 147-158. doi: 10.1007/978-1-59745-188-8_10.
30. Ginsberg, S. D., Alldred, M. J., Counts, S. E., Cataldo, A. M., Neve, R. L., Jiang, Y., et al. (2010). Microarray analysis of hippocampal CA1 neurons implicates early endosomal dysfunction during Alzheimer's disease progression. Biol. Psychiatry 68, 885-893. doi: 10.1016/j.biopsych.2010.05.030.
31. Han, Y. S., Zheng, W. H., Bastianetto, S., Chabot, J. G., and Quirion, R. (2004). Neuroprotective effects of resveratrol against beta-amyloid-induced neurotoxicity in rat hippocampal neurons: involvement of protein kinase C. Br. J. Pharmacol. 141, 997-1005. doi: 10.1038/sj.bjp.0705688.
32. Hébert, S. S., and De Strooper, B. (2009). Alterations of the microRNA network cause neurodegenerative disease. Trends Neurosci. 32, 199-206. doi: 10.1016/j.tins.2008.12.003.
33. Hébert, S. S., Horré, K., Nicolaï, 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. doi: 10.1073/pnas.0710263105.
34. 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 hyperphosphorylation and neurodegeneration. Hum. Mol. Genet. 19, 3959-3969. doi: 10.1093/hmg/ddq311.
35. Hébert, S. S., Wang, W. X., Zhu, Q., and Nelson, P. T. (2013). A study of small RNAs from cerebral neocortex of pathology-verified Alzheimer's disease, dementia with lewy bodies, hippocampal sclerosis, frontotemporal lobar dementia, and non-demented human controls. J. Alzheimers Dis. 35, 335-348. doi: 10.3233/JAD-122350.
36. Herskovits, A. Z., and Guarente, L. (2014). SIRT1 in neurodevelopment and brain senescence. Neuron 81, 471-483. doi: 10.1016/j.neuron.2014.01.028.
37. Hyman, B. T., Phelps, C. H., Beach, T. G., Bigio, E. H., Cairns, N. J., Carrillo, M. C., et al. (2012). National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease. Alzheimers Dement. 8, 1-13. doi: 10.1016/j.jalz.2011.10.007.
38. Imai, S., Armstrong, C. M., Kaeberlein, M., and Guarente, L. (2000). Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403, 795-800. doi: 10.1038/35001622.
39. Karuppagounder, S. S., Pinto, J. T., Xu, H., Chen, H. L., Beal, M. F., and Gibson, G. E. (2009). Dietary supplementation with resveratrol reduces plaque pathology in a transgenic model of Alzheimer's disease. Neurochem. Int. 54, 111-118. doi: 10.1016/j.neuint.2008.10.008.
40. Kim, D., Nguyen, M. D., Dobbin, M. M., Fischer, A., Sananbenesi, F., Rodgers, J. T., et al. (2007). SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer's disease and amyotrophic lateral sclerosis. EMBO J. 26, 3169-3179. doi: 10.1038/sj.emboj.7601758.
41. Kosik, K. S. (2006). The neuronal microRNA system. Nat. Rev. Neurosci. 7, 911-920. doi: 10.1038/nrn2037.
42. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. (2001). Identification of novel genes coding for small expressed RNAs. Science 294, 853-858. doi: 10.1126/science.1064921.
43. Lau, P., Bossers, K., Janky, R., Salta, E., Frigerio, C. S., Barbash, S., et al. (2013). Alteration of the microRNA network during the progression of Alzheimer's disease. EMBO Mol. Med. 5, 1613-1634. doi: 10.1002/emmm.201201974.
44. Li, Y. Y., Alexandrov, P. N., Pogue, A. I., Zhao, Y., Bhattacharjee, S., and Lukiw, W. J. (2012). miRNA-155 upregulation and complement factor H deficits in Down's syndrome. Neuroreport 23, 168-173. doi: 10.1097/WNR.0b013e32834f4eb4.
45. Lukiw, W. J., Cui, J. G., Yuan, L. Y., Bhattacharjee, P. S., Corkern, M., Clement, C., et al. (2010). Acyclovir or Abeta42 peptides attenuate HSV-1-induced miRNA-146a levels in human primary brain cells. Neuroreport 21, 922-927. doi: 10.1097/WNR.0b013e32833da51a.
46. Ma, L., and Weinberg, R. A. (2008). Micromanagers of malignancy: role of microRNAs in regulating metastasis. Trends Genet. 24, 448-456. doi: 10.1016/j.tig.2008.06.004.
47. Magill, S. T., Cambronne, X. A., Luikart, B. W., Lioy, D. T., Leighton, B. H., Westbrook, G. L., et al. (2010). microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc. Natl. Acad. Sci. U.S.A. 107, 20382-20387. doi: 10.1073/pnas.1015691107.
48. McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., and Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA work group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34, 939-944. doi: 10.1212/WNL.34.7.939.
49. Michán, S., Li, Y., Chou, M. M., Parrella, E., Ge, H., Long, J. M., et al. (2010). SIRT1 is essential for normal cognitive function and synaptic plasticity. J. Neurosci. 30, 9695-9707. doi: 10.1523/JNEUROSCI.0027-10.2010.
50. Min, S. W., Cho, S. H., Zhou, Y., Schroeder, S., Haroutunian, V., Seeley, W. W., et al. (2010). Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron 67, 953-966. doi: 10.1016/j.neuron.2010.08.044.
51. Mirra, S. S., Heyman, A., McKeel, D., Sumi, S. M., Crain, B. J., Brownlee, L. M., et al. (1991). The consortium to establish a registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41, 479-486. doi: 10.1212/WNL.41.4.479.
52. Mufson, E. J., Chen, E. Y., Cochran, E. J., Beckett, L. A., Bennett, D. A., and Kordower, J. H. (1999). Entorhinal cortex beta-amyloid load in individuals with mild cognitive impairment. Exp. Neurol. 158, 469-490. doi: 10.1006/exnr.1999.7086.
53. Nelson, P. T., Wang, W. X., and Rajeev, B. W. (2008). MicroRNAs (miRNAs) in neurodegenerative diseases. Brain Pathol. 18, 130-138. doi: 10.1111/j.1750-3639.2007.00120.x.
54. North, B. J., and Verdin, E. (2004). Sirtuins: Sir2-related NAD-dependent protein deacetylases. Genome Biol. 5:224. doi: 10.1186/gb-2004-5-5-224.
55. Petersen, R. C., Doody, R., Kurz, A., Mohs, R. C., Morris, J. C., Rabins, P. V., et al. (2001). Current concepts in mild cognitive impairment. Arch. Neurol. 58, 1985-1992. doi: 10.1001/archneur.58.12.1985.
56. Qin, W., Yang, T., Ho, L., Zhao, Z., Wang, J., Chen, L., et al. (2006). Neuronal SIRT1 activation as a novel mechanism underlying the prevention of Alzheimer disease amyloid neuropathology by calorie restriction. J. Biol. Chem. 281, 21745-21754. doi: 10.1074/jbc. M602909200.
57. Qin, W., Zhao, W., Ho, L., Wang, J., Walsh, K., Gandy, S., et al. (2008). Regulation of forkhead transcription factor FoxO3a contributes to calorie restriction-induced prevention of Alzheimer's disease-type amyloid neuropathology and spatial memory deterioration. Ann. N.Y. Acad. Sci. 1147, 335-347. doi: 10.1196/annals.1427.024.
58. Rajasethupathy, P., Fiumara, F., Sheridan, R., Betel, D., Puthanveettil, S. V., Russo, J. J., et al. (2009). Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63, 803-817. doi: 10.1016/j.neuron.2009.05.029.
59. Sabirzhanov, B., Zhao, Z., Stoica, B. A., Loane, D. J., Wu, J., Borroto, C., et al. (2014). Downregulation of miR-23a and miR-27a following experimental traumatic brain injury induces neuronal cell death through activation of proapoptotic Bcl-2 proteins. J. Neurosci. 34, 10055-10071. doi: 10.1523/JNEUROSCI.1260-14.2014.
60. Schratt, G. M., Tuebing, F., Nigh, E. A., Kane, C. G., Sabatini, M. E., Kiebler, M., et al. (2006). A brain-specific microRNA regulates dendritic spine development. Nature 439, 283-289. doi: 10.1038/nature04367.
61. Vingtdeux, V., Giliberto, L., Zhao, H., Chandakkar, P., Wu, Q., Simon, J. E., et al. (2010). AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J. Biol. Chem. 285, 9100-9113. doi: 10.1074/jbc. M109.060061.
62. Walsh, D. M., Hartley, D. M., Kusumoto, Y., Fezoui, Y., Condron, M. M., Lomakin, A., et al. (1999). Amyloid beta-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 274, 25945-25952. doi: 10.1074/jbc.274.36.25945.
63. Wang, R. Y., Phang, R. Z., Hsu, P. H., Wang, W. H., Huang, H. T., and Liu, I. Y. (2013). In vivo knockdown of hippocampal miR-132 expression impairs memory acquisition of trace fear conditioning. Hippocampus 23, 625-633. doi: 10.1002/hipo.22123.
64. Wang, W. X., Rajeev, B. W., Stromberg, A. J., Ren, N., Tang, G., Huang, Q., et al. (2008). The expression of microRNA miR-107 decreases early in Alzheimer's disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. J. Neurosci. 28, 1213-1223. doi: 10.1523/JNEUROSCI.5065-07.2008.
65. Williams, C., Mehrian Shai, R., Wu, Y., Hsu, Y. H., Sitzer, T., Spann, B., et al. (2009). Transcriptome analysis of synaptoneurosomes identifies neuroplasticity genes overexpressed in incipient Alzheimer's disease. PLoS ONE 4:e4936. doi: 10.1371/journal.pone.0004936.
66. Wong, H. K., Veremeyko, T., Patel, N., Lemere, C. A., Walsh, D. M., Esau, C., et al. (2013). De-repression of FOXO3a death axis by microRNA-132 and-212 causes neuronal apoptosis in Alzheimer's disease. Hum. Mol. Genet. 22, 3077-3092. doi: 10.1093/hmg/ddt164.
67. Yaffe, K., Petersen, R. C., Lindquist, K., Kramer, J., and Miller, B. (2006). Subtype of mild cognitive impairment and progression to dementia and death. Dement. Geriatr. Cogn. Disord. 22, 312-319. doi: 10.1159/000095427.