Fragile X protein family member FXR1P is regulated by microRNAs

RNA

Volumn 16, Issue 8, 2010, Pages 1530-1539

  Cheever, Anne ^a   Blackwell, Ernest ^a,b   Ceman, Stephanie ^a,b,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

FMRP; FXR1P; miRNA; Translation regulation

Indexed keywords

DICER; FRAGILE X MENTAL RETARDATION PROTEIN; LUCIFERASE; MICRORNA; MICRORNA 25; MICRORNA 32; MICRORNA 363; MICRORNA 367; MICRORNA 92; PROTEIN FXR 1 P; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CELL LINE; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA BINDING; RNA SEQUENCE; RNA TRANSLATION; TRANSLATION REGULATION;

ANIMALS; BASE SEQUENCE; CELL LINE; DEAD-BOX RNA HELICASES; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; HELA CELLS; HUMANS; MENTAL RETARDATION; MICE; MICRORNAS; MUSCLE DEVELOPMENT; MUSCLES; MUSCULAR DYSTROPHY, FACIOSCAPULOHUMERAL; PROTEINS; RIBONUCLEASE III;

DANIO RERIO; MUS;

EID: 77955116603     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2022210     Document Type: Article

References (59)

1. Abdelmohsen K, Lal A, Kim H, Gorospe M. 2007. Post-transcriptional orchestration of an anti-apoptotic program by HuR. Cell Cycle 6: 1288-1292. (Pubitemid 47327958)
2. Abdelmohsen K, Srikantan S, Kuwano Y, Gorospe M. 2008. miR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels. Proc Natl Acad Sci 105: 20297-20302.
3. Bakker C, de Diego Oter Y, Bontekoe C, Raghoe P, Luteijn T, Hoogeveen A, Oostra B, Willemsen R. 2000. Immunocytochemical and biochemical characterization of FMRP, FXR1P, and FXR2P in the mouse. Exp Cell Res 258: 162-170. (Pubitemid 30461118)
4. Bartel D. 2004. MircroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
5. Bartel D. 2009. MircroRNAs: Target recognition and regulatory functions. Cell 136: 215-233.
6. Buerstedde J, Takeda S. 1991. Increased ratio of targeted to random integration after transfection of chicken B cell lines. Cell 67: 179-188. (Pubitemid 121001434)
7. Cheever A, Ceman S. 2009. Phosphorylation of FMRP inhibits association with Dicer. RNA 15: 1-5.
8. Chen J, Mandel E, Thomson J, Wu Q, Callis T, Hammond S, Conlon F, Wang D. 2006. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38: 228-233. (Pubitemid 43177239)
9. Chen J, Murchison E, Tang R, Callis T, Tatsuguchi M, Deng Z, Rojas M, Hammond S, Schneider M, Selzman C, et al. 2008. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc Natl Acad Sci 105: 2111-2116.
10. Chen J, Callis T, Wang D. 2009. microRNAs and muscle disorders. J Cell Sci 122: 13-20.
11. Cherry J, Karschner V, Jones H, Pekala P. 2006. HuR, an RNA-binding protein, involved in the control of cellular differentiation. In Vivo 20: 17-23.
12. Chi S, Zang J, Mele A, Darnell R. 2009. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486.
13. Coy J, Sedlacek Z, Bachner D, Hameister H, Joos S, Lichter P, Delius H, Poustka A. 1995. Highly conserved 3′ UTR and expression pattern of FXR1 points to a divergent gene regulation of FXR1 and FMR1. Hum Mol Genet 4: 2209-2218.
14. Davidovic L, Sacconi S, Bechara E, Delplace S, Allegra M, Desnuelle C, Bardoni B. 2008. Alteration of expression of muscle specific isoforms of the fragile X related protein (FXR1P) in facioscapulohumeral muscular dystrophy patients. J Med Genet 45: 679-685.
15. Devys D, Lutz Y, Rouyer N, Bellocq J, Mandel J. 1993. The FMR-1 protein is cytoplasmic, most abundant in neurons and appears normal in carriers of fragile X premutation. Nat Genet 4: 335-340. (Pubitemid 23231479)
16. Doran J, Strauss W. 2007. Bioinformatic trends for the determination of miRNA-target interactions in mammals. DNA Cell Biol 26: 353-360. (Pubitemid 46799183)
17. Dube M, Huot M, Khandjian E. 2000. Muscle specific fragile X related protein 1 isoforms are sequestered in the nucleus of undifferentiated myoblast. BMC Genet 1: 4. doi: 10.1186/1471-2156-1-4.
18. Eisenberg I, Alexander M, Kunkel L. 2009. miRNAs in normal and diseased skeletal muscle. J Cell Mol Med 13: 2-11.
19. Feng Y, Absher D, Eberhart DE, Brown V, Malter HE, Warren ST. 1997. FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol Cell 1: 109-118. (Pubitemid 127376398)
20. Filipowicz W, Bhattacharyya S, Sonenberg N. 2008. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nature 9: 102-114.
21. Fukagawa T, Nogami M, Yoshikawa M, Ikeno M, Okazaki T, Takami Y, Nakayama T, Oshimura M. 2004. Dicer is essential for formation of the heterochromatin structure of vertebrate cells. Nat Cell Biol 6: 784-791. (Pubitemid 39144485)
22. Gorospe M. 2003. HuR in the mammalian genotoxic response: Posttranscriptional multitasking. Cell Cycle 2: 412-414.
23. Grimson A, Farh K, Johnston W, Garrett-Engele P, Lim L, Bartel D. 2007. MicroRNA targeting specificity in mammals: Determinants beyond seed pairing. Mol Cell 27: 91-105. (Pubitemid 46991392)
24. Gu S, Jin L, Zhang F, Sarnow P, Kay M. 2009. Biological basis for restriction of microRNA targets to the 3′ untranslated region in mammalian mRNAs. Nat Struct Mol Biol 16: 144-150.
25. Hendrickson D, Hogan D, Herschlag D, Ferrell J, Brown P. 2008. Systematic identification of mRNAs recruited to argonaute 2 by specific microRNAs and corresponding changes in transcript abundance. PLoS One 3: e2126. doi: 10.1371/journal.pone.0002126.
26. Huot M, Bisson N, Davidovic L, Mazroui R, Labelle Y, Moss T, Khandjian E. 2005. The RNA-binding protein fragile X-related 1 regulates somite formation in Xenopus laevis. Mol Biol Cell 16: 4350-4361. (Pubitemid 41262902)
27. Hurteau G, Carlson J, Spivack S, Brock G. 2007. Overespression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res 67: 7972-7976. (Pubitemid 47395127)
28. Hutvagner G, McLachlan J, Pasquinelli A, Balint E, Tuschl T, Zamore P. 2001. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293: 834-838. (Pubitemid 32743968)
29. Jackson A, Burchard J, Schelter J, Chau B, Cleary M, Lim L, Linsley P. 2009. Widespread siRNA 'off-target' transcript silencing mediated by seed region sequence complementarity. RNA 12: 1179-1187.
30. Jin P, Zarnescu D, Ceman S, Nakamoto M, Mowrey J, Jongens T, Nelson D, Moses K, Warren S. 2004. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat Neurosci 7: 113-117.
31. Khandjian E, Fortin A, Thibodeau A, Tremblay S, Cote F, Devys D, Mandel J, Rousseau F. 1995. A heterogeneous set of FMR1 proteins is widely distributed in mouse tissues and is modulated in cell culture. Hum Mol Genet 4: 783-789.
32. Khandjian E, Corbin F, Woerly S, Rousseau F. 1996. The fragile X mental retardation protein is associated with ribosomes. Nat Genet 12: 91-93. (Pubitemid 26013158)
33. Khandjian EW, Bardoni B, Corbin F, Sittler A, Giroux S, Heitz D, Tremblay S, Pinset C, Montarras D, Rousseau F, et al. 1998. Novel isoforms of the fragile X related protein FXR1P are expressed during myogenesis. Hum Mol Genet 7: 2121-2128.
34. Kirkpatrick L, McIlwain K, Nelson D. 1999. Alternative splicing in the murine and human FXR1 genes. Genomics 59: 193-202. (Pubitemid 29365350)
35. Kirkpatrick L, Mcllwain K, Nelson D. 2001. Comparative genomic sequence analysis of the FXR gene family: FMR1, FXR1, and FXR1. Genomics 78: 169-177. (Pubitemid 34001420)
36. Lal A, Navarro F, Maher C, Maliszewski L, Yan N, O'Day E, Chowdhury D, Dykxhoorn D, Tsai P, Hofmann O, et al. 2009. miR-24 inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to 'seedless' 3′UTR microRNA recognition elements. Mol Cell 35: 610-625.
37. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst A, Landthaler M, et al. 2007. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129: 1401-1414.
38. Lewis B, Burge C, Bartel D. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20. (Pubitemid 40094598)
39. Lopez de Silanes I, Lal A, Gorospe M. 2005. HuR: Post-transcriptional paths to malignancy. RNA Biol 2: 11-13.
40. Lytle J, Yario T, Steitz J. 2007. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR. Proc Natl Acad Sci 104: 9667-9672.
41. Majoros W, Ohler U. 2007. Spatial preferences of microRNA targets in 3′ untranslated regions. BMC Genomics 8: 152. doi: 10.1186/1471-2164-8- 152.
42. Mazroui R, Huot M, Tremblay S, Boilard N, Labelle Y, Khandjian E. 2003. Fragile X Mental Retardation protein determinants required for its association with polyribosomal mRNPs. Hum Mol Genet 12: 3087-3096. (Pubitemid 37508881)
43. Mientjes E, Willemsen R, Kirkpatrick L, Nieuwenhuizen I, Hoogeveen-Westerveld M, Verweij M, Reis S, Bardoni B, Hoogeveen A, Oostra B, et al. 2004. Fxr1 knockout mice show a striated muscle phenotype: implications for Fxr1p function in vivo. Hum Mol Genet 13: 1291-1302.
44. Nilsen T. 2007. Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet 23: 243-249. (Pubitemid 46628981)
45. Padje S, Chaudhry B, Severijnen L-A, Linde H, Mientjes E, Oostra B, Willemsen R. 2009. Reduction in fragile X related 1 protein causes cardiomyopathy and mucular dystrophy in zebrafish. J Exp Biol 212: 2564-2570.
46. Price D, Zhang F, Ashley C, Warren S. 1996. The chicken FMR1 gene is highly conserved with a CCT 5′-untranslated repeat and encodes an RNA-binding protein. Genomics 31: 3-12.
47. Rigoutsos I. 2009. New tricks for animal microRNAs: Targeting of amino acid coding regions at conserved and nonconserved sites. Cancer Res 69: 3245-3248.
48. Ruan H, Brown C, Morris D. 1997. Analysis of ribosome loading onto mRNA species: Implications for translational control. In mRNA formulation and function (ed. J Richter), pp. 305-321. Academic, New York.
49. Scott G, Goga A, Bhaumik D, Berger C, Sullivan C, Benz C. 2007. Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem 282: 1479-1486. (Pubitemid 47076526)
50. Siomi M, Siomi H, Sauer W, Srinivasan S, Nussbaum R, Dreyfuss G. 1995. FXR1, and autosomal homolog of the fragile X mental retardation gene. EMBO J 14: 2401-2408.
51. Stetler A, Winograd C, Sayegh J, Cheever A, Patton E, Zhang X, Clarke S, Ceman S. 2006. Identification and characterization of the methyl arginines in the fragile X mental retardation protein Fmrp. Hum Mol Genet 15: 87-96. (Pubitemid 43020107)
52. Terracciano A, Chiurazzi P, Neri G. 2005. Fragile X syndrome. Semin Med Genet 137C: 32-37.
53. Vasudevan S, Steitz J. 2007. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 128: 1105-1118. (Pubitemid 46427873)
54. Vasudevan S, Tong Y, Steitz J. 2007. Switching from repression to activation: MicroRNAs can up-regulate translation. Science 318: 1931-1934.
55. Wienholds E, Plasterk R. 2005. MicroRNA function in animal development. FEBS Lett 579: 5911-5922.
56. Winograd C, Clayton D, Ceman S. 2008. Expression of fragile X mental retardation protein within the vocal control system of developing and adult male zebra finches. Neuroscience 157: 132-142.
57. Xiao C, Calado D, Galler G, Thai T, Patterson H, Wang J, Rajewsky N, Bender T, Rajewsky K. 2007. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131: 146-159. (Pubitemid 47498525)
58. Yekta S, Shih I, Bartel D. 2004. MicroRNA-directed cleavage of HOXB8 mRNA. Science 304: 594-596.
59. Zhang Y, O'Connor J, Siomi M, Srinivasan S, Dutra A, Nussbaum R, Dreyfuss G. 1995. The fragile X mental retardation syndrome protein interacts with novel homologs FXR1 and FXR2. EMBO J 14: 5358-5366.