Alternative polyadenylation mediates microRNA regulation of muscle stem cell function

Cell Stem Cell

Volumn 10, Issue 3, 2012, Pages 327-336

  Boutet, Stéphane C ^a   Cheung, Tom H ^a   Quach, Navaline L ^a   Liu, Ling ^a   Prescott, Sara L ^a   Edalati, Abdolhossein ^a   Iori, Kevin ^a   Rando, Thomas A ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 206; TRANSCRIPTION FACTOR PAX3; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; ENZYME REGULATION; MOUSE; MUSCLE CELL; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SATELLITE CELL; STEM CELL;

ANIMALS; CELL LINE; CELLS, CULTURED; CLONING, MOLECULAR; EMBRYO, MAMMALIAN; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICRORNAS; MODELS, BIOLOGICAL; MYOBLASTS; PAIRED BOX TRANSCRIPTION FACTORS; POLYADENYLATION; POLYMERASE CHAIN REACTION; STEM CELLS;

EID: 84863230221     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.01.017     Document Type: Article

References (45)

1. T.D. Barber, M.C. Barber, T.E. Cloutier, and T.B. Friedman PAX3 gene structure, alternative splicing and evolution Gene 237 1999 311 319 (Pubitemid 29457640)
2. S. Biressi, and T.A. Rando Heterogeneity in the muscle satellite cell population Semin. Cell Dev. Biol. 21 2010 845 854
3. F. Bladt, D. Riethmacher, S. Isenmann, A. Aguzzi, and C. Birchmeier Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud Nature 376 1995 768 771
4. E. Bober, T. Franz, H.H. Arnold, P. Gruss, and P. Tremblay Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells Development 120 1994 603 612 (Pubitemid 24071202)
5. S.C. Boutet, M.H. Disatnik, L.S. Chan, K. Iori, and T.A. Rando Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors Cell 130 2007 349 362 (Pubitemid 47081135)
6. S.C. Boutet, S. Biressi, K. Iori, V. Natu, and T.A. Rando Taf1 regulates Pax3 protein by monoubiquitination in skeletal muscle progenitors Mol. Cell 40 2010 749 761
7. J.F. Chen, E.M. Mandel, J.M. Thomson, Q. Wu, T.E. Callis, S.M. Hammond, F.L. Conlon, and D.Z. Wang The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation Nat. Genet. 38 2006 228 233 (Pubitemid 43177239)
8. J.F. Chen, Y. Tao, J. Li, Z. Deng, Z. Yan, X. Xiao, and D.Z. Wang microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7 J. Cell Biol. 190 2010 867 879
9. T.H. Cheung, N.L. Quach, G.W. Charville, L. Liu, L. Park, A. Edalati, B. Yoo, P. Hoang, and T.A. Rando Maintenance of muscle stem cell quiescence by microRNA-489 Nature 482 2012 524 528
10. I.M. Conboy, and T.A. Rando The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis Dev. Cell 3 2002 397 409
11. D.D. Cornelison, M.S. Filla, H.M. Stanley, A.C. Rapraeger, and B.B. Olwin Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration Dev. Biol. 239 2001 79 94 (Pubitemid 33052054)
12. L. Costessi, G. Devescovi, F.E. Baralle, and A.F. Muro Brain-specific promoter and polyadenylation sites of the beta-adducin pre-mRNA generate an unusually long 3′-UTR Nucleic Acids Res. 34 2006 243 253 (Pubitemid 43160047)
13. C.G. Crist, D. Montarras, G. Pallafacchina, D. Rocancourt, A. Cumano, S.J. Conway, and M. Buckingham Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression Proc. Natl. Acad. Sci. USA 106 2009 13383 13387
14. M.S. Ebert, J.R. Neilson, and P.A. Sharp MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells Nat. Methods 4 2007 721 726 (Pubitemid 47338166)
15. G. Edwalds-Gilbert, K.L. Veraldi, and C. Milcarek Alternative poly(A) site selection in complex transcription units: means to an end? Nucleic Acids Res. 25 1997 2547 2561 (Pubitemid 27298148)
16. J.A. Epstein, P. Lam, L. Jepeal, R.L. Maas, and D.N. Shapiro Pax3 inhibits myogenic differentiation of cultured myoblast cells J. Biol. Chem. 270 1995 11719 11722
17. K. Goljanek-Whysall, D. Sweetman, M. Abu-Elmagd, E. Chapnik, T. Dalmay, E. Hornstein, and A. Münsterberg MicroRNA regulation of the paired-box transcription factor Pax3 confers robustness to developmental timing of myogenesis Proc. Natl. Acad. Sci. USA 108 2011 11936 11941
18. M. Goulding, A. Lumsden, and A.J. Paquette Regulation of Pax-3 expression in the dermomyotome and its role in muscle development Development 120 1994 957 971 (Pubitemid 24111559)
19. H. Hirai, M. Verma, S. Watanabe, C. Tastad, Y. Asakura, and A. Asakura MyoD regulates apoptosis of myoblasts through microRNA-mediated down-regulation of Pax3 J. Cell Biol. 191 2010 347 365
20. Z. Ji, J.Y. Lee, Z. Pan, B. Jiang, and B. Tian Progressive lengthening of 3′ untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development Proc. Natl. Acad. Sci. USA 106 2009 7028 7033
21. H.K. Kim, Y.S. Lee, U. Sivaprasad, A. Malhotra, and A. Dutta Muscle-specific microRNA miR-206 promotes muscle differentiation J. Cell Biol. 174 2006 677 687 (Pubitemid 44306724)
22. F. Le Grand, A.E. Jones, V. Seale, A. Scim, and M.A. Rudnicki Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells Cell Stem Cell 4 2009 535 547
23. C. Lepper, S.J. Conway, and C.M. Fan Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements Nature 460 2009 627 631
24. D.D. Licatalosi, and R.B. Darnell RNA processing and its regulation: global insights into biological networks Nat. Rev. Genet. 11 2010 75 87
25. C.S. Lutz Alternative polyadenylation: a twist on mRNA 3′ end formation ACS Chem. Biol. 3 2008 609 617
26. T. Maniatis, and R. Reed An extensive network of coupling among gene expression machines Nature 416 2002 499 506 (Pubitemid 34288845)
27. C. Mayr, and D.P. Bartel Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells Cell 138 2009 673 684
28. S. Millevoi, and S. Vagner Molecular mechanisms of eukaryotic pre-mRNA 3′ end processing regulation Nucleic Acids Res. 38 2010 2757 2774
29. D. Montarras, J. Morgan, C. Collins, F. Relaix, S. Zaffran, A. Cumano, T. Partridge, and M. Buckingham Direct isolation of satellite cells for skeletal muscle regeneration Science 309 2005 2064 2067 (Pubitemid 41362326)
30. C.J. Parker, S.G. Shawcross, H. Li, Q.Y. Wang, C.S. Herrington, S. Kumar, R.M. MacKie, W. Prime, I.G. Rennie, K. Sisley, and P. Kumar Expression of PAX 3 alternatively spliced transcripts and identification of two new isoforms in human tumors of neural crest origin Int. J. Cancer 108 2004 314 320 (Pubitemid 37541789)
31. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res. 29 2001 e45
32. C. Pritchard, G. Grosveld, and A.D. Hollenbach Alternative splicing of Pax3 produces a transcriptionally inactive protein Gene 305 2003 61 69 (Pubitemid 36197866)
33. N.L. Quach, and T.A. Rando Focal adhesion kinase is essential for costamerogenesis in cultured skeletal muscle cells Dev. Biol. 293 2006 38 52
34. P.K. Rao, R.M. Kumar, M. Farkhondeh, S. Baskerville, and H.F. Lodish Myogenic factors that regulate expression of muscle-specific microRNAs Proc. Natl. Acad. Sci. USA 103 2006 8721 8726 (Pubitemid 43878086)
35. F. Relaix, D. Montarras, S. Zaffran, B. Gayraud-Morel, D. Rocancourt, S. Tajbakhsh, A. Mansouri, A. Cumano, and M. Buckingham Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells J. Cell Biol. 172 2006 91 102 (Pubitemid 43042632)
36. J.D. Rosenblatt, A.I. Lunt, D.J. Parry, and T.A. Partridge Culturing satellite cells from living single muscle fiber explants In Vitro Cell. Dev. Biol. Anim. 31 1995 773 779
37. R. Sandberg, J.R. Neilson, A. Sarma, P.A. Sharp, and C.B. Burge Proliferating cells express mRNAs with shortened 3′ untranslated regions and fewer microRNA target sites Science 320 2008 1643 1647 (Pubitemid 351931255)
38. D. Sweetman, K. Goljanek, T. Rathjen, S. Oustanina, T. Braun, T. Dalmay, and A. Münsterberg Specific requirements of MRFs for the expression of muscle specific microRNAs, miR-1, miR-206 and miR-133 Dev. Biol. 321 2008 491 499
39. K.K. Tanaka, J.K. Hall, A.A. Troy, D.D. Cornelison, S.M. Majka, and B.B. Olwin Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration Cell Stem Cell 4 2009 217 225
40. H. Tian, H.J. Chen, T.H. Cross, and H.J. Edenberg Alternative splicing and promoter use in the human GABRA2 gene Brain Res. Mol. Brain Res. 137 2005 174 183 (Pubitemid 40798900)
41. M. Tranter, R.N. Helsley, W.R. Paulding, M. McGuinness, C. Brokamp, L. Haar, Y. Liu, X. Ren, and W.K. Jones Coordinated post-transcriptional regulation of Hsp70.3 gene expression by microRNA and alternative polyadenylation J. Biol. Chem. 286 2011 29828 29837
42. Q. Wang, S. Kumar, M. Slevin, and P. Kumar Functional analysis of alternative isoforms of the transcription factor PAX3 in melanocytes in vitro Cancer Res. 66 2006 8574 8580 (Pubitemid 44449171)
43. J. Winter, M. Kunath, S. Roepcke, S. Krause, R. Schneider, and S. Schweiger Alternative polyadenylation signals and promoters act in concert to control tissue-specific expression of the Opitz Syndrome gene MID1 BMC Mol. Biol. 8 2007 105
44. X.M. Yang, K. Vogan, P. Gros, and M. Park Expression of the met receptor tyrosine kinase in muscle progenitor cells in somites and limbs is absent in Splotch mice Development 122 1996 2163 2171 (Pubitemid 26235816)
45. J. Zhao, L. Hyman, and C. Moore Formation of mRNA 3′ ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis Microbiol. Mol. Biol. Rev. 63 1999 405 445 (Pubitemid 29264977)