Post-transcriptional regulation of satellite cell quiescence by TTP-mediated mRNA decay

eLife

Volumn 2015, Issue 4, 2015, Pages

  Hausburg, Melissa A ^b,c   Doles, Jason D ^f   Clement, Sandra L ^d   Cadwallader, Adam B ^a   Hall, Monica N ^a   Blackshear, Perry J ^d   Lykke Andersen, Jens ^e   Olwin, Bradley B ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b SWEDISH MEDICAL CENTER   (United States)

^c Ampio Pharmaceuticals Inc   (United States)

^d CALIFORNIA POLYTECHNIC STATE UNIVERSITY   (United States)

^e NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN BETA CHAIN; MITOGEN ACTIVATED PROTEIN KINASE 11; RNA BINDING PROTEIN; TRISTETRAPROLIN; MAP-KINASE-ACTIVATED KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; MYOD PROTEIN; MYOD1 MYOGENIC DIFFERENTIATION PROTEIN; PROTEIN BINDING; SIGNAL PEPTIDE; SMALL INTERFERING RNA; ZFP36 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SIGNALING ASSAY; CONTROLLED STUDY; FEMALE; GENE SILENCING; GENETIC TRANSFECTION; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION; SATELLITE CELL; SEQUENCE TAGGED SITE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRISTETRAPROLIN MEDIATED MRNA DECAY; 3' UNTRANSLATED REGION; ANIMAL; BINDING SITE; C57BL MOUSE; CELL DIFFERENTIATION; GENETICS; INJURY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; REGENERATION; RNA PROCESSING; RNA STABILITY; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; TRANSGENIC MOUSE;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MYOD PROTEIN; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN BINDING; PROTEIN SERINE-THREONINE KINASES; REGENERATION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, SMALL INTERFERING; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; TRISTETRAPROLIN;

EID: 84925955248     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03390     Document Type: Article

References (44)

1. Al-Ahmadi, W., M. Al-Ghamdi, L. Al-Haj, M. Al-Saif, and K.S.A. Khabar. 2009. Alternative polyadenylation variants of the RNA binding protein, HuR: abundance, role of AU-rich elements and auto-Regulation. Nucleic Acids Res 37:3612-3624.
2. Bernet, J. D., J.D. Doles, J.K. Hall, K. Kelly Tanaka, T.A. Carter, and B.B. Olwin. 2014. p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat Med 20:265-271.
3. Boutet, S. C., T.H. Cheung, N.L. Quach, L. Liu, S.L. Prescott, A. Edalati, K. Iori, and T.A. Rando. 2012. Alternative polyadenylation mediates microRNA regulation of muscle stem cell function. Cell Stem Cell 10:327-336.
4. Brook, M., C.R. Tchen, T. Santalucia, J. McIlrath, J.S.C. Arthur, J. Saklatvala, and A.R. Clark. 2006. Posttranslational regulation of tristetraprolin subcellular localization and protein stability by p38 mitogen-activated protein kinase and extracellular signal-regulated kinase pathways. Mol Cell Biol 26:2408-2418.
5. Brooks, S. A., and P.J. Blackshear. 2013. Tristetraprolin (TTP): interactions with mRNA and proteins, and current thoughts on mechanisms of action. Biochim Biophys Acta 1829:666-679.
6. Cao, H., J.S. Tuttle, and P.J. Blackshear. 2004. Immunological characterization of tristetraprolin as a low abundance, inducible, stable cytosolic protein. J Biol Chem 279:21489-21499.
7. Carballo, E., H. Cao, W.S. Lai, E.A. Kennington, D. Campbell, and P.J. Blackshear. 2001. Decreased sensitivity of tristetraprolin-deficient cells to p38 inhibitors suggests the involvement of tristetraprolin in the p38 signaling pathway. J Biol Chem 276:42580-42587.
8. Cheung, T. H., N.L. Quach, G.W. Charville, L. Liu, L. Park, A. Edalati, B. Yoo, P. Hoang, and T.A. Rando. 2012. Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482:524-528.
9. Clement, S. L., and J. Lykke-Andersen. 2008. A tethering approach to study proteins that activate mRNA turnover in human cells. Methods Mol Biol 419:121-133.
10. Clement, S. L., C. Scheckel, G. Stoecklin, and J. Lykke-Andersen. 2011. Phosphorylation of TTP by MK2 impairs ARE mRNA decay by preventing deadenylase recruitment. Molecular and Cellular Biology:256-266.
11. Cornelison, D. D., M.S. Filla, H.M. Stanley, A.C. Rapraeger, and B.B. Olwin. 2001. Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 239:79-94.
12. Cornelison, D. D. W., S.A. Wilcox-Adelman, P.F. Goetinck, H. Rauvala, A.C. Rapraeger, and B.B. Olwin. 2004. Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev 18:2231-2236.
13. Cosgrove, B. D., P.M. Gilbert, E. Porpiglia, F. Mourkioti, S.P. Lee, S.Y. Corbel, M.E. Llewellyn, S.L. Delp, and H.M. Blau. 2014. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nature Medicine 20:255-264.
14. Crist, C. G., D. Montarras, and M. Buckingham. 2012. Muscle satellite cells are primed for myogenesis but maintain quiescence with sequestration of Myf5 mRNA targeted by microRNA-31 in mRNP granules. Cell Stem Cell 11:118-126.
15. Farina, N. H., M. Hausburg, N. Dalla Betta, C. Pulliam, D. Srivastava, D.D. Cornelison, and B.B. Olwin. 2012. A role for RNA post-transcriptional regulation in satellite cell activation. Skelet Muscle 2:21.
16. Farina, N. H., M. Hausburg, N. Dalla Betta, C. Pulliam, D. Srivastava, D.D. Cornelison, and B.B. Olwin. 2012. A role for RNA post-transcriptional regulation in satellite cell activation. Skelet Muscle 2:21.
17. Figueroa, A., A. Cuadrado, J. Fan, U. Atasoy, G.E. Muscat, P. Muñoz-Canoves, M. Gorospe, and A. Muñoz. 2003. Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol Cell Biol 23:4991-5004.
18. Flanagan-Steet, H., K. Hannon, M.J. McAvoy, R. Hullinger, and B.B. Olwin. 2000. Loss of FGF receptor 1 signaling reduces skeletal muscle mass and disrupts myofiber organization in the developing limb. Dev Biol 218:21-37.
19. Hall, J. K., G.B. Banks, J.S. Chamberlain, and B.B. Olwin. 2010. Prevention of muscle aging by myofiber-associated satellite cell transplantation. Sci Transl Med 2:57ra83.
20. Harpavat, S., and C.L. Cepko. 2006. RCAS-RNAi: a loss-of-function method for the developing chick retina. BMC Dev Biol 6:2.
21. Hughes, S. H. 2004. The RCAS vector system. Folia Biol (Praha) 50:107-119.
22. Jones, N. C., K.J. Tyner, L. Nibarger, H.M. Stanley, D.D.W. Cornelison, Y.V. Fedorov, and B.B. Olwin. 2005. The p38{alpha}/{beta} MAPK functions as a molecular switch to activate the quiescent satellite cell. J Cell Biol 169:105-116.
23. Kim, H. H., K. Abdelmohsen, and M. Gorospe. 2010. Regulation of HuR by DNA Damage Response Kinases. J Nucleic Acids 2010.
24. Lai, W. S., E.A. Kennington, and P.J. Blackshear. 2002. Interactions of CCCH zinc finger proteins with mRNA: non-binding tristetraprolin mutants exert an inhibitory effect on degradation of AU-rich element-containing mRNAs. J Biol Chem 277:9606-9613.
25. Lai, W. S., E. Carballo, J.M. Thorn, E.A. Kennington, and P.J. Blackshear. 2000. Interactions of CCCH zinc finger proteins with mRNA. Binding of tristetraprolin-related zinc finger proteins to Au-rich elements and destabilization of mRNA. J Biol Chem 275:17827-17837.
26. Liu, L., T.H. Cheung, G.W. Charville, B.M.C. Hurgo, T. Leavitt, J. Shih, A. Brunet, and T.A. Rando. 2013. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep 4:189-204.
27. Lykke-Andersen, J., M.D. Shu, and J.A. Steitz. 2000. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103:1121-1131.
28. Lykke-Andersen, J., M.D. Shu, and J.A. Steitz. 2001. Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293:1836-1839.
29. Mahtani, K. R., M. Brook, J.L. Dean, G. Sully, J. Saklatvala, and A.R. Clark. 2001. Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor alpha mRNA stability. Mol Cell Biol 21:6461-6469.
30. Parker, R., and H. Song. 2004. The enzymes and control of eukaryotic mRNA turnover. Nature structural & molecular biology 11:121-127.
31. Pisconti, A., D.D.W. Cornelison, H.C. Olguín, T.L. Antwine, and B.B. Olwin. 2010. Syndecan-3 and Notch cooperate in regulating adult myogenesis. J Cell Biol 190:427-441.
32. Sachidanandan, C., R. Sambasivan, and J. Dhawan. 2002. Tristetraprolin and LPS-inducible CXC chemokine are rapidly induced in presumptive satellite cells in response to skeletal muscle injury. J Cell Sci 115:2701-2712.
33. Schultz, E. 1976. Fine structure of satellite cells in growing skeletal muscle. Am J Anat 147:49-70.
34. Seidler, B., A. Schmidt, U. Mayr, H. Nakhai, R.M. Schmid, G. Schneider, and D. Saur. 2008. A Cre-loxP-based mouse model for conditional somatic gene expression and knockdown in vivo by using avian retroviral vectors. Proc Natl Acad Sci U S A 105:10137-10142.
35. Stoecklin, G., T. Stubbs, N. Kedersha, S. Wax, W.F.C. Rigby, T.K. Blackwell, and P. Anderson. 2004. MK2-induced tristetraprolin:14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J 23:1313-1324.
36. Stumpo, D. J., W.S. Lai, and P.J. Blackshear. 2010. Inflammation: cytokines and RNA-based regulation. Wiley Interdiscip Rev RNA 1:60-80.
37. Taylor, G. A., E. Carballo, D.M. Lee, W.S. Lai, M.J. Thompson, D.D. Patel, D.I. Schenkman, G.S. Gilkeson, H.E. Broxmeyer, B.F. Haynes, and P.J. Blackshear. 1996. A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4:445-454.
38. Tchen, C. R., M. Brook, J. Saklatvala, and A.R. Clark. 2004. The stability of tristetraprolin mRNA is regulated by mitogen-activated protein kinase p38 and by tristetraprolin itself. J Biol Chem 279:32393-32400.
39. Tiedje, C., N. Ronkina, M. Tehrani, S. Dhamija, K. Laass, H. Holtmann, A. Kotlyarov, and M. Gaestel. 2012. The p38/MK2-driven exchange between tristetraprolin and HuR regulates AU-rich element-dependent translation. PLoS Genet 8:e1002977.
40. Troy, A., A.B. Cadwallader, Y. Fedorov, K. Tyner, K.K. Tanaka, and B.B. Olwin. 2012. Coordination of Satellite Cell Activation and Self-Renewal by Par-Complex-Dependent Asymmetric Activation of p38α/β MAPK. Cell Stem Cell 11:541-553.
41. Van der Giessen, K., S. Di-Marco, E. Clair, and I.E. Gallouzi. 2003. RNAi-mediated HuR depletion leads to the inhibition of muscle cell differentiation. J Biol Chem 278:47119-47128.
42. Von Werder, A., B. Seidler, R.M. Schmid, G. Schneider, and D. Saur. 2012. Production of avian retroviruses and tissue-specific somatic retroviral gene transfer in vivo using the RCAS/TVA system. Nat Protoc 7:1167-1183.
43. Wakayama, Y., D.L. Schotland, E. Bonilla, and E. Orecchio. 1979. Quantitative ultrastructural study of muscle satellite cells in Duchenne dystrophy. Neurology 29:401-407.
44. Weller, B., G. Karpati, and S. Carpenter. 1990. Dystrophin-deficient mdx muscle fibers are preferentially vulnerable to necrosis induced by experimental lengthening contractions. J Neurol Sci 100:9-13.