Increased expression of MicroRNA-29a in ALS mice: Functional analysis of its inhibition

Journal of Molecular Neuroscience

Volumn 53, Issue 2, 2014, Pages 231-241

  Nolan, Katie ^a   Mitchem, Mollie R ^a   Jimenez Mateos, Eva M ^a   Henshall, David C ^a   Concannon, Caoimhín G ^a   Prehn, Jochen H M ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

Amyotrophic lateral sclerosis; Antagomir; MicroRNA; Neurodegeneration; SOD1

Indexed keywords

ANTAGOMIR; MICRORNA 29A; COPPER ZINC SUPEROXIDE DISMUTASE; MICRORNA; MIRN29 MICRORNA, MOUSE; OLIGORIBONUCLEOTIDE; SUPEROXIDE DISMUTASE;

3' UNTRANSLATED REGION; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DISEASE COURSE; DISEASE MARKER; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION; IN VIVO STUDY; LIFESPAN; MALE; MOTOR PERFORMANCE; MOUSE; MSOD1 MOUSE; MULTIGENE FAMILY; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SPINAL CORD; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; C57BL MOUSE; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY;

MUS; MUS MUSCULUS;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BRAIN; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; OLIGORIBONUCLEOTIDES; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 84901411067     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-014-0290-y     Document Type: Article

References (50)

1. Acevedo-Arozena A, Kalmar B, Essa S, Ricketts T, Joyce P, Kent R, Rowe C, Parker A, Gray A, Hafezparast M, Thorpe JR, Greensmith L, Fisher EM (2011) A comprehensive assessment of the SOD1G93A low-copy transgenic mouse, which models human amyotrophic lateral sclerosis. Dis Model Mech 4:686-700
2. Ambros V (2004) The functions of animal microRNAs. Nature 431:350-355
3. Ayala V, Granado-Serrano AB, Cacabelos D, Naudi A, Ilieva EV, Boada J, Caraballo-Miralles V, Llado J, Ferrer I, Pamplona R, Portero-Otin M (2011) Cell stress induces TDP-43 pathological changes associated with ERK1/2 dysfunction: implications in ALS. Acta Neuropathol 122:259-270
4. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297
5. Bouchie A (2013) First microRNA mimic enters clinic. Nat Biotechnol 31:577
6. Brown JA, Min J, Staropoli JF, Collin E, Bi S, Feng X, Barone R, Cao Y, O'Malley L, Xin W, Mullen TE, Sims KB (2012) SOD1, ANG, TARDBP and FUS mutations in amyotrophic lateral sclerosis: a United States clinical testing lab experience. Amyotroph Lateral Scler 13:217-222
7. Bruijn LI, Houseweart MK, Kato S, Anderson KL, Anderson SD, Ohama E, Reaume AG, Scott RW, Cleveland DW (1998) Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 281:1851-1854 (Pubitemid 28450505)
8. Buck CR, Seburn KL, Cope TC (2000) Neurotrophin expression by spinal motoneurons in adult and developing rats. J Comp Neurol 416:309-318 (Pubitemid 30027129)
9. Byrne S, Walsh C, Lynch C, Bede P, Elamin M, Kenna K, McLaughlin R, Hardiman O (2011) Rate of familial amyotrophic lateral sclerosis: a systematic review andmeta-analysis. J Neurol Neurosurg Psychiatry 82:623-627
10. Choi CI, Lee YD, Gwag BJ, Cho SI, Kim SS, Suh-Kim H (2008) Effects of estrogen on lifespan andmotor functions in female hSOD1 G93A transgenic mice. J Neurol Sci 268:40-47 (Pubitemid 351389466)
11. Cleveland DW, Rothstein JD (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2:806-819 (Pubitemid 33674062)
12. Farg MA, Soo KY, Walker AK, Pham H, Orian J, Horne MK, Warraich ST, Williams KL, Blair IP, Atkin JD (2012) Mutant FUS induces endoplasmic reticulum stress in amyotrophic lateral sclerosis and interacts with protein disulfide-isomerase. Neurobiol Aging 33:2855-2868
13. Gould TW, Buss RR, Vinsant S, Prevette D, Sun W, Knudson CM, Milligan CE, Oppenheim RW (2006) Complete dissociation of motor neuron death from motor dysfunction by Bax deletion in a mouse model of ALS. J Neurosci 26:8774-8786 (Pubitemid 44319413)
14. Gurney ME (1994) Transgenic-mouse model of amyotrophic lateral sclerosis. N Engl J Med 331:1721-1722
15. Hebert SS, Horre K, Nicolai L, Papadopoulou AS, Mandemakers W, Silahtaroglu AN, Kauppinen S, De Delacourte A, Strooper B (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 (Pubitemid 351758360)
16. Janssen HL, Reesink HW, Lawitz EJ, Zeuzem S, Rodriguez-Torres M, Patel K, van der Meer AJ, Patick AK, Chen A, Zhou Y, Persson R, King BD, Kauppinen S, Levin AA, Hodges MR (2013) Treatment of HCV infection by targeting microRNA. N Engl J Med 368:1685-1694
17. Jimenez-Mateos EM, Engel T, Merino-Serrais P, McKiernan RC, Tanaka K, Mouri G, Sano T, O'Tuathaigh C, Waddington JL, Prenter S, Delanty N, Farrell MA, O'Brien DF, Conroy RM, Stallings RL, DeFelipe J, Henshall DC (2012) Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat Med 18:1087-1094
18. Kanekura K, Suzuki H, Aiso S, Matsuoka M (2009) ER stress and unfolded protein response in amyotrophic lateral sclerosis. Mol Neurobiol 39:81-89
19. Kieran D, Woods I, Villunger A, Strasser A, Prehn JH (2007) Deletion of the BH3-only protein puma protects motoneurons from ER stress-induced apoptosis and delays motoneuron loss in ALS mice. Proc Natl Acad Sci U S A 104:20606-20611
20. Kikuchi H, Almer G, Yamashita S, Guegan C, Nagai M, Xu Z, Sosunov AA, McKhann GM II, Przedborski S (2006) Spinal cord endoplasmic reticulum stress associated with a microsomal accumulation of mutant superoxide dismutase-1 in an ALS model. Proc Natl Acad Sci U S A 103:6025-6030
21. Koval ED, Shaner C, Zhang P, du Maine X, Fischer K, Tay J, Chau BN, Wu GF, Miller TM (2013) Method for widespread microRNA-155 inhibition prolongs survival in ALS-model mice. Hum Mol Genet 22:4127-4135
22. Lee ST, Chu K, Im WS, Yoon HJ, Im JY, Park JE, Park KH, Jung KH, Lee SK, Kim M, Roh JK (2011) Altered microRNA regulation in Huntington's disease models. Exp Neurol 227:172-179
23. Lindholm D, Wootz H, Korhonen L (2006) ER stress and neurodegenerative diseases. Cell Death Differ 13:385-392
24. Liu P, He K, Li Y, Wu Q, Yang P, Wang D (2012) Exposure to mercury causes formation of male-specific structural deficits by inducing oxidative damage in nematodes. Ecotoxicol Environ Saf 79:90-100
25. Mackenzie IR, Bigio EH, Ince PG, Geser F, Neumann M, Cairns NJ, Kwong LK, Forman MS, Ravits J, Stewart H, Eisen A, McClusky L, Kretzschmar HA, Monoranu CM, Highley JR, Kirby J, Siddique T, Shaw PJ, Lee VM, Trojanowski JQ (2007) Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1mutations. Ann Neurol 61:427-434 (Pubitemid 46878770)
26. Majounie E, Renton AE, Mok K, Dopper EG, Waite A, Rollinson S, Chio A, Restagno G, Nicolaou N, Simon-Sanchez J, van Swieten JC, Abramzon Y, Johnson JO, Sendtner M, Pamphlett R, Orrell RW, Mead S, Sidle KC, Houlden H, Rohrer JD, Morrison KE, Pall H, Talbot K, Ansorge O, Hernandez DG, Arepalli S, Sabatelli M, Mora G, Corbo M, Giannini F, Calvo A, Englund E, Borghero G, Floris GL, Remes AM, Laaksovirta H, McCluskey L, Trojanowski JQ, Van Deerlin VM, Schellenberg GD, Nalls MA, Drory VE, Lu CS, Yeh TH, Ishiura H, Takahashi Y, Tsuji S, Le Ber I, Brice A, Drepper C, Williams N, Kirby J, Shaw P, Hardy J, Tienari PJ, Heutink P, Morris HR, Pickering-Brown S, Traynor BJ (2012) Frequency of the C9orf72 hexanucleotide repeat expansion in patients with amyotrophic lateral sclerosis and frontotemporal dementia: a cross-sectional study. Lancet Neurol 11:323-330
27. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10:615-622 (Pubitemid 46652435)
28. Nishitoh H, Kadowaki H, Nagai A, Maruyama T, Yokota T, Fukutomi H, Noguchi T, Matsuzawa A, Takeda K, Ichijo H (2008) ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev 22:1451-1464 (Pubitemid 351793080)
29. Nolan K, Gallagher R, Germain M, Slack R, Concannon CG, Prehn JHM (2012) MicroRNA-29a targeting Mcl-1 controls controls ER stress induced apoptosis and autophagy. Program No. 61.11. 2012. Neuroscience Meeting Planner. Society for Neuroscience, New Orleans, Online
30. Ouyang YB, Xu L, Lu Y, Sun X, Yue S, Xiong XX, Giffard RG (2013) Astrocyte-enriched miR-29a targets PUMA and reduces neuronal vulnerability to forebrain ischemia. Glia 61:1784-1794
31. Padhi AK, Jayaram B, Gomes J (2013) Prediction of functional loss of human angiogenin mutants associated with ALS by molecular dynamics simulations. Sci Rep 3:1225
32. Pasinelli P, Brown RH (2006) Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 7:710-723 (Pubitemid 44267495)
33. Pilati N, Barker M, Panteleimonitis S, Donga R, Hamann M (2008) A rapid method combining Golgi and Nissl staining to study neuronal morphology and cytoarchitecture. J Histochem Cytochem 56:539-550 (Pubitemid 351702298)
34. Prell T, Lautenschlager J, Witte OW, Carri MT, Grosskreutz J (2012) The unfolded protein response in models of human mutant G93A amyotrophic lateral sclerosis. Eur J Neurosci 35:652-660
35. Renton AE, Majounie E, Waite A, Simon-Sanchez J, Rollinson S, Gibbs JR, Schymick JC, Laaksovirta H, van Swieten JC, Myllykangas L, Kalimo H, Paetau A, Abramzon Y, Remes AM, Kaganovich A, Scholz SW, Duckworth J, Ding J, Harmer DW, Hernandez DG, Johnson JO, Mok K, Ryten M, Trabzuni D, Guerreiro RJ, Orrell RW, Neal J, Murray A, Pearson J, Jansen IE, Sondervan D, Seelaar H, Blake D, Young K, Halliwell N, Callister JB, Toulson G, Richardson A, Gerhard A, Snowden J, Mann D, Neary D, Nalls MA, Peuralinna T, Jansson L, Isoviita VM, Kaivorinne AL, Holtta-Vuori M, Ikonen E, Sulkava R, Benatar M, Wuu J, Chio A, Restagno G, Borghero G, Sabatelli M, Heckerman D, Rogaeva E, Zinman L, Rothstein JD, Sendtner M, Drepper C, Eichler EE, Alkan C, Abdullaev Z, Pack SD, Dutra A, Pak E, Hardy J, Singleton A, Williams NM, Heutink P, Pickering-Brown S, Morris HR, Tienari PJ, Traynor BJ (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72:257-268
36. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX et al (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62 (Pubitemid 23087289)
37. Saxena S, Cabuy E, Caroni P (2009) A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat Neurosci 12:627-636
38. Schroder M, Kaufman RJ (2005) ER stress and the unfolded protein response. Mutat Res 569:29-63 (Pubitemid 39643256)
39. Shioya M, Obayashi S, Tabunoki H, Arima K, Saito Y, Ishida T, Satoh J (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
40. Stenvang J, Petri A, Lindow M, Obad S, Kauppinen S (2012) Inhibition of microRNA function by antimiR oligonucleotides. Silence 3:1
41. Traynor BJ, Codd MB, Corr B, Forde C, Frost E, Hardiman O (1999) Incidence and prevalence of ALS in Ireland, 1995-1997: a population-based study. Neurology 52:504-509 (Pubitemid 29075594)
42. Turner MR, Bowser R, Bruijn L, Dupuis L, Ludolph A, McGrath M, Manfredi G, Maragakis N, Miller RG, Pullman SL, Rutkove SB, Shaw PJ, Shefner J, Fischbeck KH (2013) Mechanisms, models and biomarkers in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 14(Suppl 1):19-32
43. van Es MA, Schelhaas HJ, van Vught PW, Ticozzi N, Andersen PM, Groen EJ, Schulte C, Blauw HM, Koppers M, Diekstra FP, Fumoto K, LeClerc AL, Keagle P, Bloem BR, Scheffer H, van Nuenen BF, van Blitterswijk M, van Rheenen W, Wills AM, Lowe PP, Hu GF, Yu W, Kishikawa H, Wu D, Folkerth RD, Mariani C, Goldwurm S, Pezzoli G, Van Damme P, Lemmens R, Dahlberg C, Birve A, Fernandez-Santiago R, Waibel S, Klein C, Weber M, van der Kooi AJ, de Visser M, Verbaan D, van Hilten JJ, Heutink P, Hennekam EA, Cuppen E, Berg D, Brown RH Jr, Silani V, Gasser T, Ludolph AC, Robberecht W, Ophoff RA, Veldink JH, Pasterkamp RJ, de Bakker PI, Landers JE, van de Warrenburg BP, van den Berg LH (2011) Angiogenin variants in Parkinson disease and amyotrophic lateral sclerosis. Ann Neurol 70:964-973
44. Van Janssens J, Broeckhoven C (2013) Pathological mechanisms underlying TDP-43 driven neurodegeneration in FTLD-ALS spectrum disorders. Hum Mol Genet 22:R77-R87
45. Veldink JH, Bar PR, Joosten EA, Otten M, van den Wokke JH, Berg LH (2003) Sexual differences in onset of disease and response to exercise in a transgenic model of ALS. Neuromuscul Disord 13:737-743 (Pubitemid 37258345)
46. Vinsant S, Mansfield C, Jimenez-Moreno R, Del Gaizo Moore V, Yoshikawa M, Hampton TG, Prevette D, Caress J, Oppenheim RW, Milligan C (2013) Characterisation of early pathogenesis in the SOD1G93A mouse model of ALS: part II, results and discussion. Brain and Behaviour 2:431-457
47. Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086
48. Weydt P, Hong SY, Kliot M, Moller T (2003) Assessing disease onset and progression in the SOD1 mouse model of ALS. Neuroreport 14:1051-1054 (Pubitemid 36829789)
49. Williams KL, Fifita JA, Vucic S, Durnall JC, Kiernan MC, Blair IP, Nicholson GA (2013) Pathophysiological insights into ALS with C9ORF72 expansions. J Neurol Neurosurg Psychiatry 84:931-935
50. Wong ML, Medrano JF (2005) Real-time PCR for mRNA quantitation. Biotechniques 39:75-85