Evidence for natural antisense transcript-mediated inhibition of microRNA function

Genome Biology

Volumn 11, Issue 5, 2010, Pages

  Faghihi, Mohammad Ali ^a   Zhang, Ming ^b,c   Huang, Jia ^d   Modarresi, Farzaneh ^a   Van der Brug, Marcel P ^a   Nalls, Michael A ^e   Cookson, Mark R ^e   St Laurent III, Georges ^f   Wahlestedt, Claes ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c CENTER FOR NONLINEAR STUDIES   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^e NATIONAL INSTITUTE ON AGING   (United States)

^f BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA SECRETASE 1; COMPLEMENTARY RNA; LOCKED NUCLEIC ACID; MESSENGER RNA; MICRORNA; ASPARTIC PROTEINASE; BACE1 PROTEIN, HUMAN; BACE1 PROTEIN, MOUSE; LUCIFERASE; OLIGONUCLEOTIDE; SECRETASE; UNTRANSLATED RNA;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BACE1 GENE; BINDING SITE; BIOINFORMATICS; CONTROLLED STUDY; ENZYME REPRESSION; GENE; GENE EXPRESSION; GENE INTERACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INHIBITION KINETICS; OPEN READING FRAME; PROTEIN EXPRESSION; RNA BINDING; ANIMAL; BINDING COMPETITION; BRAIN; CELL LINE; DNA SEQUENCE; DRUG EFFECT; ENZYMOLOGY; GENETICS; HIGH THROUGHPUT SCREENING; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PATHOLOGY; REPRODUCIBILITY;

MAMMALIA;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; BASE SEQUENCE; BINDING SITES; BINDING, COMPETITIVE; BRAIN; CELL LINE; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LUCIFERASES; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES; OPEN READING FRAMES; REPRODUCIBILITY OF RESULTS; RNA, ANTISENSE; RNA, MESSENGER; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, DNA;

EID: 77952698932     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2010-11-5-r56     Document Type: Article

References (55)

1. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest AR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, Allen JE, Ambesi-Impiombato A, Apweiler R, Aturaliya RN, Bailey TL, Bansal M, Baxter L, Beisel KW, Bersano T, Bono H, et al. The transcriptional landscape of the mammalian genome. Science 2005, 309:1559-1563. 10.1126/science.1112014, 16141072.
2. Kapranov P, Drenkow J, Cheng J, Long J, Helt G, Dike S, Gingeras TR. Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays. Genome Res 2005, 15:987-997. 10.1101/gr.3455305, 1172043, 15998911.
3. Gustincich S, Sandelin A, Plessy C, Katayama S, Simone R, Lazarevic D, Hayashizaki Y, Carninci P. The complexity of the mammalian transcriptome. J Physiol 2006, 575:321-332. 10.1113/jphysiol.2006.115568, 1819450, 16857706.
4. Mehler MF, Mattick JS. Non-coding RNA in the nervous system. J Physiol 2006, 575:333-341. 10.1113/jphysiol.2006.113191, 1819441, 16809366.
5. Faghihi MA, Wahlestedt C. RNA interference is not involved in natural antisense mediated regulation of gene expression in mammals. Genome Biol 2006, 7:R38. 10.1186/gb-2006-7-5-r38, 1779516, 16684369.
6. Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet 2006, (15 Spec No 1):R17-29. 10.1093/hmg/ddl046, 16651366.
7. Wahlestedt C. Natural antisense and noncoding RNA transcripts as potential drug targets. Drug Discov Today 2006, 11:503-508. 10.1016/j.drudis.2006.04.013, 16713901.
8. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, Suzuki H, Carninci P, Hayashizaki Y, Wells C, Frith M, Ravasi T, Pang KC, Hallinan J, Mattick J, Hume DA, Lipovich L, Batalov S, Engstrom PG, Mizuno Y, Faghihi MA, Sandelin A, Chalk AM, Mottagui-Tabar S, Liang Z, Lenhard B, et al. Antisense transcription in the mammalian transcriptome. Science 2005, 309:1564-1566. 10.1126/science.1112009, 16141073.
9. Engstrom PG, Suzuki H, Ninomiya N, Akalin A, Sessa L, Lavorgna G, Brozzi A, Luzi L, Tan SL, Yang L, Kunarso G, Ng EL, Batalov S, Wahlestedt C, Kai C, Kawai J, Carninci P, Hayashizaki Y, Wells C, Bajic VB, Orlando V, Reid JF, Lenhard B, Lipovich L. Complex Loci in human and mouse genomes. PLoS Genet 2006, 2:e47. 10.1371/journal.pgen.0020047, 1449890, 16683030.
10. Faghihi MA, Modarresi F, Khalil AM, Wood DE, Sahagan BG, Morgan TE, Finch CE, St Laurent G, Kenny PJ, Wahlestedt C. Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nat Med 2008, 14:723-730. 10.1038/nm1784, 2826895, 18587408.
11. Uchida T, Rossignol F, Matthay MA, Mounier R, Couette S, Clottes E, Clerici C. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1alpha. J Biol Chem 2004, 279:14871-14878. 10.1074/jbc.M400461200, 14744852.
12. Cayre A, Rossignol F, Clottes E, Penault-Llorca F. aHIF but not HIF-1alpha transcript is a poor prognostic marker in human breast cancer. Breast Cancer Res 2003, 5:R223-230. 10.1186/bcr652, 314412, 14580258.
13. Rossignol F, Vache C, Clottes E. Natural antisense transcripts of hypoxia-inducible factor 1alpha are detected in different normal and tumour human tissues. Gene 2002, 299:135-140. 10.1016/S0378-1119(02)01049-1, 12459261.
14. Rossignol F, de Laplanche E, Mounier R, Bonnefont J, Cayre A, Godinot C, Simonnet H, Clottes E. Natural antisense transcripts of HIF-1alpha are conserved in rodents. Gene 2004, 339:121-130. 10.1016/j.gene.2004.06.029, 15363852.
15. Capaccioli S, Quattrone A, Schiavone N, Calastretti A, Copreni E, Bevilacqua A, Canti G, Gong L, Morelli S, Nicolin A. A bcl-2/IgH antisense transcript deregulates bcl-2 gene expression in human follicular lymphoma t(14;18) cell lines. Oncogene 1996, 13:105-115.
16. Leung AK, Sharp PA. Function and localization of microRNAs in mammalian cells. Cold Spring Harb Symp Quant Biol 2006, 71:29-38. 10.1101/sqb.2006.71.049, 17381277.
17. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233. 10.1016/j.cell.2009.01.002, 19167326.
18. Laird FM, Cai H, Savonenko AV, Farah MH, He K, Melnikova T, Wen H, Chiang HC, Xu G, Koliatsos VE, Borchelt DR, Price DL, Lee HK, Wong PC. BACE1, a major determinant of selective vulnerability of the brain to amyloid-beta amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. J Neurosci 2005, 25:11693-11709. 10.1523/JNEUROSCI.2766-05.2005, 2564291, 16354928.
19. Hu X, Hicks CW, He W, Wong P, Macklin WB, Trapp BD, Yan R. Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 2006, 9:1520-1525. 10.1038/nn1797, 17099708.
20. Willem M, Garratt AN, Novak B, Citron M, Kaufmann S, Rittger A, DeStrooper B, Saftig P, Birchmeier C, Haass C. Control of peripheral nerve myelination by the beta-secretase BACE1. Science 2006, 314:664-666. 10.1126/science.1132341, 16990514.
21. Roberson ED, Mucke L. 100 years and counting: prospects for defeating Alzheimer's disease. Science 2006, 314:781-784. 10.1126/science.1132813, 17082448.
22. Vassar R. Beta-secretase (BACE) as a drug target for Alzheimer's disease. Adv Drug Deliv Rev 2002, 54:1589-1602. 10.1016/S0169-409X(02)00157-6, 12453676.
23. Vassar R. The beta-secretase, BACE: a prime drug target for Alzheimer's disease. J Mol Neurosci 2001, 17:157-170. 10.1385/JMN:17:2:157, 11816789.
24. Ghosh AK, Kumaragurubaran N, Tang J. Recent developments of structure based beta-secretase inhibitors for Alzheimer's disease. Curr Top Med Chem 2005, 5:1609-1622. 10.2174/156802605775009711, 16375745.
25. Zimmermann M, Gardoni F, Di Luca M. Molecular rationale for the pharmacological treatment of Alzheimer's disease. Drugs Aging 2005, 22(Suppl 1):27-37. 10.2165/00002512-200522001-00003, 16506440.
26. Li R, Lindholm K, Yang LB, Yue X, Citron M, Yan R, Beach T, Sue L, Sabbagh M, Cai H, Wong P, Price D, Shen Y. Amyloid beta peptide load is correlated with increased beta-secretase activity in sporadic Alzheimer's disease patients. Proc Natl Acad Sci USA 2004, 101:3632-3637. 10.1073/pnas.0205689101, 373514, 14978286.
27. Holsinger RM, McLean CA, Collins SJ, Masters CL, Evin G. Increased beta-Secretase activity in cerebrospinal fluid of Alzheimer's disease subjects. Ann Neurol 2004, 55:898-899. 10.1002/ana.20144, 15174031.
28. Fukumoto H, Cheung BS, Hyman BT, Irizarry MC. Beta-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch Neurol 2002, 59:1381-1389. 10.1001/archneur.59.9.1381, 12223024.
29. Rossner S, Sastre M, Bourne K, Lichtenthaler SF. Transcriptional and translational regulation of BACE1 expression - implications for Alzheimer's disease. Prog Neurobiol 2006, 79:95-111. 10.1016/j.pneurobio.2006.06.001, 16904810.
30. Holsinger RM, McLean CA, Beyreuther K, Masters CL, Evin G. Increased expression of the amyloid precursor beta-secretase in Alzheimer's disease. Ann Neurol 2002, 51:783-786. 10.1002/ana.10208, 12112088.
31. Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibe B, Bouix J, Caiment F, Elsen JM, Eychenne F, Larzul C, Laville E, Meish F, Milenkovic D, Tobin J, Charlier C, Georges M. A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet 2006, 38:813-818. 10.1038/ng1810, 16751773.
32. Chin LJ, Ratner E, Leng S, Zhai R, Nallur S, Babar I, Muller RU, Straka E, Su L, Burki EA, Crowell RE, Patel R, Kulkarni T, Homer R, Zelterman D, Kidd KK, Zhu Y, Christiani DC, Belinsky SA, Slack FJ, Weidhaas JB. A SNP in a let-7 microRNA complementary site in the KRAS 3' untranslated region increases non-small cell lung cancer risk. Cancer Res 2008, 68:8535-8540. 10.1158/0008-5472.CAN-08-2129, 2672193, 18922928.
33. Mishra PJ, Humeniuk R, Longo-Sorbello GS, Banerjee D, Bertino JR. A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance. Proc Natl Acad Sci USA 2007, 104:13513-13518. 10.1073/pnas.0706217104, 1948927, 17686970.
34. Mishra PJ, Banerjee D, Bertino JR. MiRSNPs or MiR-polymorphisms, new players in microRNA mediated regulation of the cell: introducing microRNA pharmacogenomics. Cell Cycle 2008, 7:853-858.
35. Abelson JF, Kwan KY, O'Roak BJ, Baek DY, Stillman AA, Morgan TM, Mathews CA, Pauls DL, Rasin MR, Gunel M, Davis NR, Ercan-Sencicek AG, Guez DH, Spertus JA, Leckman JF, Dure L, Kurlan R, Singer HS, Gilbert DL, Farhi A, Louvi A, Lifton RP, Sestan N, State MW. Sequence variants in SLITRK1 are associated with Tourette's syndrome. Science 2005, 310:317-320. 10.1126/science.1116502, 16224024.
36. Arteaga-Vazquez M, Caballero-Perez J, Vielle-Calzada JP. A family of microRNAs present in plants and animals. Plant Cell 2006, 18:3355-3369. 10.1105/tpc.106.044420, 1785418, 17189346.
37. Lytle JR, Yario TA, Steitz JA. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR. Proc Natl Acad Sci USA 2007, 104:9667-9672. 10.1073/pnas.0703820104, 1887587, 17535905.
38. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. Prediction of plant microRNA targets. Cell 2002, 110:513-520. 10.1016/S0092-8674(02)00863-2, 12202040.
39. Forman JJ, Legesse-Miller A, Coller HA. A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc Natl Acad Sci USA 2008, 105:14879-14884. 10.1073/pnas.0803230105, 2567461, 18812516.
40. Duursma AM, Kedde M, Schrier M, le Sage C, Agami R. miR-148 targets human DNMT3b protein coding region. RNA 2008, 14:872-877. 10.1261/rna.972008, 2327368, 18367714.
41. Prasanth KV, Prasanth SG, Xuan Z, Hearn S, Freier SM, Bennett CF, Zhang MQ, Spector DL. Regulating gene expression through RNA nuclear retention. Cell 2005, 123:249-263. 10.1016/j.cell.2005.08.033, 16239143.
42. Leung AK, Sharp PA. microRNAs: a safeguard against turmoil?. Cell 2007, 130:581-585. 10.1016/j.cell.2007.08.010, 17719533.
43. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 2006, 125:1111-1124. 10.1016/j.cell.2006.04.031, 16777601.
44. St Laurent G, Wahlestedt C. Noncoding RNAs: couplers of analog and digital information in nervous system function?. Trends Neurosci 2007, 30:612-621. 10.1016/j.tins.2007.10.002, 17996312.
45. Borghi R, Patriarca S, Traverso N, Piccini A, Storace D, Garuti A, Cirmena G, Odetti P, Tabaton M. The increased activity of BACE1 correlates with oxidative stress in Alzheimer's disease. Neurobiol Aging 2007, 28:1009-1014. 10.1016/j.neurobiolaging.2006.05.004, 16769154.
46. Tong Y, Zhou W, Fung V, Christensen MA, Qing H, Sun X, Song W. Oxidative stress potentiates BACE1 gene expression and Abeta generation. J Neural Transm 2005, 112:455-469. 10.1007/s00702-004-0255-3, 15614428.
47. Tamagno E, Bardini P, Guglielmotto M, Danni O, Tabaton M. The various aggregation states of beta-amyloid 1-42 mediate different effects on oxidative stress, neurodegeneration, and BACE-1 expression. Free Radic Biol Med 2006, 41:202-212. 10.1016/j.freeradbiomed.2006.01.021, 16814100.
48. Harkany T, Abraham I, Konya C, Nyakas C, Zarandi M, Penke B, Luiten PG. Mechanisms of beta-amyloid neurotoxicity: perspectives of pharmacotherapy. Rev Neurosci 2000, 11:329-382.
49. Yatin SM, Aksenova M, Aksenov M, Markesbery WR, Aulick T, Butterfield DA. Temporal relations among amyloid beta-peptide-induced free-radical oxidative stress, neuronal toxicity, and neuronal defensive responses. J Mol Neurosci 1998, 11:183-197. 10.1385/JMN:11:3:183, 10344789.
50. Li Y, Zhou W, Tong Y, He G, Song W. Control of APP processing and Abeta generation level by BACE1 enzymatic activity and transcription. Faseb J 2006, 20:285-292. 10.1096/fj.05-4986com, 16449801.
51. McConlogue L, Buttini M, Anderson JP, Brigham EF, Chen KS, Freedman SB, Games D, Johnson-Wood K, Lee M, Zeller M, Liu W, Motter R, Sinha S. Partial reduction of BACE1 has dramatic effects on Alzheimer plaque and synaptic pathology in APP transgenic mice. J Biol Chem 2007, 282:26326-26334. 10.1074/jbc.M611687200, 17616527.
52. Hackenberg M, Sturm M, Langenberger D, Falcon-Perez JM, Aransay AM. miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments. Nucleic Acids Res 2009, 37:W68-76. 10.1093/nar/gkp347, 2703919, 19433510.
53. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 2008, 36:D154-158. 10.1093/nar/gkm952, 2238936, 17991681.
54. Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol 2000, 7:203-214. 10.1089/10665270050081478, 10890397.
55. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human microRNA targets. PLoS Biol 2004, 2:e363. 10.1371/journal.pbio.0020363, 521178, 15502875.