microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7
Jian-Fu Chen, Yazhong Tao, Juan Li, Zhongliang Deng, Zhen Yan, Xiao Xiao, Da-Zhi Wang, Jian-Fu Chen, Yazhong Tao, Juan Li, Zhongliang Deng, Zhen Yan, Xiao Xiao, Da-Zhi Wang
Abstract
Skeletal muscle satellite cells are adult stem cells responsible for postnatal skeletal muscle growth and regeneration. Paired-box transcription factor Pax7 plays a central role in satellite cell survival, self-renewal, and proliferation. However, how Pax7 is regulated during the transition from proliferating satellite cells to differentiating myogenic progenitor cells is largely unknown. In this study, we find that miR-1 and miR-206 are sharply up-regulated during satellite cell differentiation and down-regulated after muscle injury. We show that miR-1 and miR-206 facilitate satellite cell differentiation by restricting their proliferative potential. We identify Pax7 as one of the direct regulatory targets of miR-1 and miR-206. Inhibition of miR-1 and miR-206 substantially enhances satellite cell proliferation and increases Pax7 protein level in vivo. Conversely, sustained Pax7 expression as a result of the loss of miR-1 and miR-206 repression elements at its 3' untranslated region significantly inhibits myoblast differentiation. Therefore, our experiments suggest that microRNAs participate in a regulatory circuit that allows rapid gene program transitions from proliferation to differentiation.
Figures
References
- Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature. 409:363–366 10.1038/35053110
- Bernstein E., Kim S.Y., Carmell M.A., Murchison E.P., Alcorn H., Li M.Z., Mills A.A., Elledge S.J., Anderson K.V., Hannon G.J. 2003. Dicer is essential for mouse development. Nat. Genet. 35:215–217 10.1038/ng1253
- Buckingham M. 2007. Skeletal muscle progenitor cells and the role of Pax genes. C. R. Biol. 330:530–533 10.1016/j.crvi.2007.03.015
- Callis T.E., Wang D.Z. 2008. Taking microRNAs to heart. Trends Mol. Med. 14:254–260 10.1016/j.molmed.2008.03.006
- Chen J.F., Mandel E.M., Thomson J.M., Wu Q., Callis T.E., Hammond S.M., Conlon F.L., Wang D.Z. 2006. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38:228–233 10.1038/ng1725
- Chen J.F., Murchison E.P., Tang R., Callis T.E., Tatsuguchi M., Deng Z., Rojas M., Hammond S.M., Schneider M.D., Selzman C.H., et al. 2008. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc. Natl. Acad. Sci. USA. 105:2111–2116 10.1073/pnas.0710228105
- Clegg C.H., Linkhart T.A., Olwin B.B., Hauschka S.D. 1987. Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor. J. Cell Biol. 105:949–956 10.1083/jcb.105.2.949
- Conboy I.M., Rando T.A. 2002. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell. 3:397–409 10.1016/S1534-5807(02)00254-X
- Crist C.G., Montarras D., Pallafacchina G., Rocancourt D., Cumano A., Conway S.J., Buckingham M. 2009. Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression. Proc. Natl. Acad. Sci. USA. 106:13383–13387 10.1073/pnas.0900210106
- Eisenberg I., Eran A., Nishino I., Moggio M., Lamperti C., Amato A.A., Lidov H.G., Kang P.B., North K.N., Mitrani-Rosenbaum S., et al. 2007. Distinctive patterns of microRNA expression in primary muscular disorders. Proc. Natl. Acad. Sci. USA. 104:17016–17021 10.1073/pnas.0708115104
- Frock R.L., Kudlow B.A., Evans A.M., Jameson S.A., Hauschka S.D., Kennedy B.K. 2006. Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev. 20:486–500 10.1101/gad.1364906
- Grez M., Akgün E., Hilberg F., Ostertag W. 1990. Embryonic stem cell virus, a recombinant murine retrovirus with expression in embryonic stem cells. Proc. Natl. Acad. Sci. USA. 87:9202–9206 10.1073/pnas.87.23.9202
- Griffiths-Jones S. 2004. The microRNA Registry. Nucleic Acids Res. 32:D109–D111 10.1093/nar/gkh023
- Grishok A., Pasquinelli A.E., Conte D., Li N., Parrish S., Ha I., Baillie D.L., Fire A., Ruvkun G., Mello C.C. 2001. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell. 106:23–34 10.1016/S0092-8674(01)00431-7
- He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., Vogelstein B. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA. 95:2509–2514 10.1073/pnas.95.5.2509
- Ivey K.N., Muth A., Arnold J., King F.W., Yeh R.F., Fish J.E., Hsiao E.C., Schwartz R.J., Conklin B.R., Bernstein H.S., Srivastava D. 2008. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell. 2:219–229 10.1016/j.stem.2008.01.016
- Jaenisch R., Young R. 2008. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell. 132:567–582 10.1016/j.cell.2008.01.015
- Kim H.K., Lee Y.S., Sivaprasad U., Malhotra A., Dutta A. 2006. Muscle-specific microRNA miR-206 promotes muscle differentiation. J. Cell Biol. 174:677–687 10.1083/jcb.200603008
- Krützfeldt J., Rajewsky N., Braich R., Rajeev K.G., Tuschl T., Manoharan M., Stoffel M. 2005. Silencing of microRNAs in vivo with ‘antagomirs’. Nature. 438:685–689 10.1038/nature04303
- Kuang S., Chargé S.B., Seale P., Huh M., Rudnicki M.A. 2006. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol. 172:103–113 10.1083/jcb.200508001
- Kuang S., Gillespie M.A., Rudnicki M.A. 2008. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell. 2:22–31 10.1016/j.stem.2007.12.012
- Leung A.K., Sharp P.A. 2007. microRNAs: a safeguard against turmoil? Cell. 130:581–585 10.1016/j.cell.2007.08.010
- Lu J., McKinsey T.A., Zhang C.L., Olson E.N. 2000. Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases. Mol. Cell. 6:233–244 10.1016/S1097-2765(00)00025-3
- McFarlane C., Hennebry A., Thomas M., Plummer E., Ling N., Sharma M., Kambadur R. 2008. Myostatin signals through Pax7 to regulate satellite cell self-renewal. Exp. Cell Res. 314:317–329
- McKinsey T.A., Zhang C.L., Lu J., Olson E.N. 2000. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature. 408:106–111 10.1038/35040593
- Miller A.D., Rosman G.J. 1989. Improved retroviral vectors for gene transfer and expression. Biotechniques. 7:980–982: 984–986: 989–990
- Montarras D., Morgan J., Collins C., Relaix F., Zaffran S., Cumano A., Partridge T., Buckingham M. 2005. Direct isolation of satellite cells for skeletal muscle regeneration. Science. 309:2064–2067 10.1126/science.1114758
- Morgan J.E., Partridge T.A. 2003. Muscle satellite cells. Int. J. Biochem. Cell Biol. 35:1151–1156 10.1016/S1357-2725(03)00042-6
- Murchison E.P., Partridge J.F., Tam O.H., Cheloufi S., Hannon G.J. 2005. Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl. Acad. Sci. USA. 102:12135–12140 10.1073/pnas.0505479102
- Olguin H.C., Olwin B.B. 2004. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev. Biol. 275:375–388 10.1016/j.ydbio.2004.08.015
- Olguin H.C., Yang Z., Tapscott S.J., Olwin B.B. 2007. Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J. Cell Biol. 177:769–779 10.1083/jcb.200608122
- Oustanina S., Hause G., Braun T. 2004. Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J. 23:3430–3439 10.1038/sj.emboj.7600346
- Rao P.K., Kumar R.M., Farkhondeh M., Baskerville S., Lodish H.F. 2006. Myogenic factors that regulate expression of muscle-specific microRNAs. Proc. Natl. Acad. Sci. USA. 103:8721–8726 10.1073/pnas.0602831103
- Relaix F., Rocancourt D., Mansouri A., Buckingham M. 2005. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature. 435:948–953 10.1038/nature03594
- Relaix F., Montarras D., Zaffran S., Gayraud-Morel B., Rocancourt D., Tajbakhsh S., Mansouri A., Cumano A., Buckingham M. 2006. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 172:91–102 10.1083/jcb.200508044
- Rosenberg M.I., Georges S.A., Asawachaicharn A., Analau E., Tapscott S.J. 2006. MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J. Cell Biol. 175:77–85 10.1083/jcb.200603039
- Rosenblatt J.D., Lunt A.I., Parry D.J., Partridge T.A. 1995. Culturing satellite cells from living single muscle fiber explants. In Vitro Cell. Dev. Biol. Anim. 31:773–779 10.1007/BF02634119
- Rossant J. 2008. Stem cells and early lineage development. Cell. 132:527–531 10.1016/j.cell.2008.01.039
- Sabourin L.A., Girgis-Gabardo A., Seale P., Asakura A., Rudnicki M.A. 1999. Reduced differentiation potential of primary MyoD−/− myogenic cells derived from adult skeletal muscle. J. Cell Biol. 144:631–643 10.1083/jcb.144.4.631
- Senoo M., Pinto F., Crum C.P., McKeon F. 2007. p63 Is essential for the proliferative potential of stem cells in stratified epithelia. Cell. 129:523–536 10.1016/j.cell.2007.02.045
- Shefer G., Yablonka-Reuveni Z. 2005. Isolation and culture of skeletal muscle myofibers as a means to analyze satellite cells. Methods Mol. Biol. 290:281–304
- Shinin V., Gayraud-Morel B., Gomès D., Tajbakhsh S. 2006. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat. Cell Biol. 8:677–687 10.1038/ncb1425
- Springer M.L., Blau H.M. 1997. High-efficiency retroviral infection of primary myoblasts. Somat. Cell Mol. Genet. 23:203–209 10.1007/BF02721371
- Tatsuguchi M., Seok H.Y., Callis T.E., Thomson J.M., Chen J.F., Newman M., Rojas M., Hammond S.M., Wang D.Z. 2007. Expression of microRNAs is dynamically regulated during cardiomyocyte hypertrophy. J. Mol. Cell. Cardiol. 42:1137–1141 10.1016/j.yjmcc.2007.04.004
- Templeton T.J., Hauschka S.D. 1992. FGF-mediated aspects of skeletal muscle growth and differentiation are controlled by a high affinity receptor, FGFR1. Dev. Biol. 154:169–181 10.1016/0012-1606(92)90057-N
- Thum T., Galuppo P., Wolf C., Fiedler J., Kneitz S., van Laake L.W., Doevendans P.A., Mummery C.L., Borlak J., Haverich A., et al. 2007. MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation. 116:258–267 10.1161/CIRCULATIONAHA.107.687947
- van Rooij E., Liu N., Olson E.N. 2008. MicroRNAs flex their muscles. Trends Genet. 24:159–166 10.1016/j.tig.2008.01.007
- Wang Y., Medvid R., Melton C., Jaenisch R., Blelloch R. 2007. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat. Genet. 39:380–385 10.1038/ng1969
- Williams A.H., Valdez G., Moresi V., Qi X., McAnally J., Elliott J.L., Bassel-Duby R., Sanes J.R., Olson E.N. 2009. MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science. 326:1549–1554 10.1126/science.1181046
- Yan Z., Choi S., Liu X., Zhang M., Schageman J.J., Lee S.Y., Hart R., Lin L., Thurmond F.A., Williams R.S. 2003. Highly coordinated gene regulation in mouse skeletal muscle regeneration. J. Biol. Chem. 278:8826–8836 10.1074/jbc.M209879200
- Yang A., Schweitzer R., Sun D., Kaghad M., Walker N., Bronson R.T., Tabin C., Sharpe A., Caput D., Crum C., McKeon F. 1999. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature. 398:714–718 10.1038/19539
- Yi R., Poy M.N., Stoffel M., Fuchs E. 2008. A skin microRNA promotes differentiation by repressing ‘stemness’. Nature. 452:225–229 10.1038/nature06642
- Zammit P.S., Golding J.P., Nagata Y., Hudon V., Partridge T.A., Beauchamp J.R. 2004. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J. Cell Biol. 166:347–357 10.1083/jcb.200312007
- Zammit P.S., Relaix F., Nagata Y., Ruiz A.P., Collins C.A., Partridge T.A., Beauchamp J.R. 2006. Pax7 and myogenic progression in skeletal muscle satellite cells. J. Cell Sci. 119:1824–1832 10.1242/jcs.02908
- Zhao Y., Ransom J.F., Li A., Vedantham V., von Drehle M., Muth A.N., Tsuchihashi T., McManus M.T., Schwartz R.J., Srivastava D. 2007. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell. 129:303–317 10.1016/j.cell.2007.03.030
Source: PubMed