Ubiquitin-specific peptidase 8 regulates proliferation and early differentiation of sheep skeletal muscle satellite cells

https://doi.org/10.17221/105/2020-CJASCitation:

Wang S.Y., Li K., Gao H., Liu Z.P., Shi S., Tan Q., Wang Z.G. (2021): Ubiquitin-specific peptidase 8 regulates proliferation and early differentiation of sheep skeletal muscle satellite cells. Czech J. Anim. Sci., 66: 87–96.

download PDF

Ubiquitin-specific protease 8 (USP8), a member of the ubiquitin-specific protease (USP) family, was originally identified as playing a role in the regulation of growth and cell cycle. However, its functional role in myogenesis is unknown. In this study, we investigated the role of USP8 in proliferation and differentiation of sheep skeletal muscle satellite cells. The results showed that the expression level of USP8 was significantly increased on days 2 and 3 following the induction of the differentiation process. Furthermore, knocking down USP8 resulted in a significant increase in myogenin-positive cells, and promoted early differentiation of satellite cells by regulating the expression level of paired box 7 (PAX7). Additionally, knocking down USP8 suppressed muscle satellite cell proliferation, possibly explaining that the relative mRNA level of USP8 was linearly related to muscle fibre density of Hu sheep. Overall, our research demonstrates that USP8 plays a role in proliferation and early differentiation of skeletal muscle satellite cells.

References:
Bentzinger CF, Wang YX, Rudnicki MA. Building muscle: Molecular regulation of myogenesis. Cold Spring Harb Perspect Biol. 2012 Feb 1;4(2): [16 p.]. https://doi.org/10.1101/cshperspect.a008342
 
Berlin I, Higginbotham KM, Dise RS, Sierra MI, Nash PD. The deubiquitinating enzyme USP8 promotes trafficking and degradation of the chemokine receptor 4 at the sorting endosome. J Biol Chem. 2010 Nov 26;285(48):37895-908.
 
Bradford M. A rapid and sensitive method for the quantification of microgram quantities of protein utilising the principle of protein-dye binding. Anal Biochem. 1976 May 7;72(1-2):248-54. https://doi.org/10.1016/0003-2697(76)90527-3
 
Cao Z, Wu X, Yen L, Sweeney C, Carraway KL. Neuregulin-induced ErbB3 downregulation is mediated by a protein stability cascade involving the E3 ubiquitin ligase Nrdp1. Mol Cell Biol. 2007 Mar;27(6):2180-8. https://doi.org/10.1128/MCB.01245-06
 
Ceriani M, Amigoni L, D’Aloia A, Berruti G, Martegani E. The deubiquitinating enzyme UBPy/USP8 interacts with TrkA and inhibits neuronal differentiation in PC12 cells. Exp Cell Res. 2015 Apr 10;333(1):49-59. https://doi.org/10.1016/j.yexcr.2015.01.019
 
Charge SBP, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004 Jan 1;84(1):209-38. https://doi.org/10.1152/physrev.00019.2003
 
Costa ML, Escaleira R, Cataldo A, Oliveira F, Mermelstein CS. Desmin: Molecular interactions and putative functions of the muscle intermediate filament protein. Braz J Med Biol Res. 2004 Dec;37(12):1819-30.
 
Daviet L, Colland F. Targeting ubiquitin specific proteases for drug discovery. Biochimie. 2008 Feb;90(2):270-83. https://doi.org/10.1016/j.biochi.2007.09.013
 
Gu H, Shi X, Liu C, Wang C, Sui N, Zhao Y, Gong J, Wang F, Zhang H, Li W, Zhao T. USP8 maintains embryonic stem cell stemness via deubiquitination of EPG5. Nat Commun. 2019 Apr 1;10(1): [9 p.]. https://doi.org/10.1038/s41467-019-09430-4
 
Hunt LC, Stover J, Haugen B, Shaw TI, Li Y, Pagala VR, Finkelstein D, Barton ER, Fan Y, Labelle M, Peng J, Demontis F. A key role for the ubiquitin ligase UBR4 in myofiber hypertrophy in Drosophila and mice. Cell Rep. 2019 Jul 30;28(5):1268-81. https://doi.org/10.1016/j.celrep.2019.06.094
 
Kawaguchi K, Endo A, Fukushima T, Madoka Y, Tanaka T, Komada M. Ubiquitin-specific protease 8 deubiquitinates Sec31A and decreases large COPII carriers and collagen IV secretion. Biochem Biophys Res Commun. 2018 May 15;499(3):635-41. https://doi.org/10.1016/j.bbrc.2018.03.202
 
Kitajima Y, Ono Y. Visualization of PAX7 protein dynamics in muscle satellite cells in a YFP knock-in-mouse line. Skelet Muscle. 2018 Aug 24;8(1): [11 p.]. https://doi.org/10.1186/s13395-018-0174-x
 
Kitajima Y, Suzuki N, Nunomiya A, Osana S, Yoshioka K, Tashiro Y, Takahashi R, Ono Y, Aoki M, Nagatomi R. The ubiquitin-proteasome system is indispensable for the maintenance of muscle stem cells. Stem Cell Rep. 2018 Dec 11;11(6):1523-38. https://doi.org/10.1016/j.stemcr.2018.10.009
 
Liu D, Xu J, Tong H, Li S, Yan Y. Effect of ELOVL3 expression on bovine skeletal muscle-derived satellite cell differentiation. Biochem Biophys Res Commun. 2017 Dec 2;493(4):1457-63. https://doi.org/10.1016/j.bbrc.2017.07.118
 
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001 Dec 1;25(4):402-8. https://doi.org/10.1006/meth.2001.1262
 
Mareco EA, de la Serrana DG, Johnston IA, Dal-Pai-Silva M. Characterization of the transcriptome of fast and slow muscle myotomal fibres in the pacu (Piaractus mesopotamicus). BMC Genomics. 2015 Mar 14;16(1): [13 p.]. https://doi.org/10.1186/s12864-015-1423-6
 
Mizuno E, Kitamura N, Komada M. 14-3-3-dependent inhibition of the deubiquitinating activity of UBPY and its cancellation in the M phase. Exp Cell Res. 2007 Oct 1;313(16):3624-34. https://doi.org/10.1016/j.yexcr.2007.07.028
 
Naviglio S, Matteucci C, Matoskova B, Nagase T, Nomura N, Di Fiore PP, Draetta GF. UBPY: A growth-regulated human ubiquitin isopeptidase. EMBO J. 1998 Jun 15;17(12):3241-50. https://doi.org/10.1093/emboj/17.12.3241
 
Niendorf S, Oksche A, Kisser A, Lohler J, Prinz M, Schorle H, Feller S, Lewitzky M, Horak I, Knobeloch KP. Essential role of ubiquitin-specific protease 8 for receptor tyrosine kinase stability and endocytic trafficking in vivo. Mol Cell Biol. 2007 Jul 1;27(13):5029-39. https://doi.org/10.1128/MCB.01566-06
 
Rantanen J, Hurme T, Lukka R, Heino J, Kalimo H. Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: Evidence for two different populations of satellite cells. Lab Invest. 1995 Mar 1;72(3):341-7.
 
Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell. 2000 Sep 15;102(6):777-86. https://doi.org/10.1016/S0092-8674(00)00066-0
 
Taylor MV, Hughes SM. Mef2 and the skeletal muscle differentiation program. Semin Cell Dev Biol. 2017 Dec 1;72:33-44.
 
Wiles B, Miao M, Coyne E, Larose L, Cybulsky AV, Wing SS. USP19 deubiquitinating enzyme inhibits muscle cell differentiation by suppressing unfolded-protein response signaling. Mol Biol Cell. 2015 Mar 1;26(5):913-23. https://doi.org/10.1091/mbc.E14-06-1129
 
Will K, Schering L, Albrecht E, Kalbe C, Maak S. Differentiation of bovine satellite cell-derived myoblasts under different culture conditions. In Vitro Cell Dev Biol Anim. 2015 Jun 20;51(9):885-9. https://doi.org/10.1007/s11626-015-9916-9
 
Wu H, Ren Y, Li S, Wang W, Yuan J, Guo X, Liu D, Cang M. In vitro culture and induced differentiation of sheep skeletal muscle satellite cells. Cell Biol Int. 2012 Jun;36(6):579-87. https://doi.org/10.1042/CBI20110487
 
Yablonka-Reuveni Z. The skeletal muscle satellite cell: Still young and fascinating at 50. J Histochem Cytochem. 2011 Dec 5;59(12):1041-59. https://doi.org/10.1369/0022155411426780
 
Yuan Z, Chen Y, Zhang X, Zhou X, Li M, Chen H, Wu M, Zhang Y, Mo D. Silencing myotubularin related protein 7 enhances proliferation and early differentiation of C2C12 myoblast. Biochem Biophys Res Commun. 2017 Mar 11;484(3):592-7. https://doi.org/10.1016/j.bbrc.2017.01.143
 
Yun S, Kim KK. Ubiquitin-specific protease 4 (USP4) suppresses myoblast differentiation by down regulating MyoD activity in a catalytic-independent manner. Cell Signal. 2017 Jul;35:48-60.
 
Zammit PS. Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis. Semin Cell Dev Biol. 2017 Dec 1;72:19-32. https://doi.org/10.1016/j.semcdb.2017.11.011
 
Bentzinger CF, Wang YX, Rudnicki MA. Building muscle: Molecular regulation of myogenesis. Cold Spring Harb Perspect Biol. 2012 Feb 1;4(2): [16 p.].
 
Berlin I, Higginbotham KM, Dise RS, Sierra MI, Nash PD. The deubiquitinating enzyme USP8 promotes trafficking and degradation of the chemokine receptor 4 at the sorting endosome. J Biol Chem. 2010 Nov 26;285(48):37895-908. https://doi.org/10.1074/jbc.M110.129411
 
Bradford M. A rapid and sensitive method for the quantification of microgram quantities of protein utilising the principle of protein-dye binding. Anal Biochem. 1976 May 7;72(1-2):248-54. https://doi.org/10.1016/0003-2697(76)90527-3
 
Cao Z, Wu X, Yen L, Sweeney C, Carraway KL. Neuregulin-induced ErbB3 downregulation is mediated by a protein stability cascade involving the E3 ubiquitin ligase Nrdp1. Mol Cell Biol. 2007 Mar;27(6):2180-8.
 
Ceriani M, Amigoni L, D’Aloia A, Berruti G, Martegani E. The deubiquitinating enzyme UBPy/USP8 interacts with TrkA and inhibits neuronal differentiation in PC12 cells. Exp Cell Res. 2015 Apr 10;333(1):49-59. https://doi.org/10.1016/j.yexcr.2015.01.019
 
Charge SBP, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004 Jan 1;84(1):209-38. https://doi.org/10.1152/physrev.00019.2003
 
Costa ML, Escaleira R, Cataldo A, Oliveira F, Mermelstein CS. Desmin: Molecular interactions and putative functions of the muscle intermediate filament protein. Braz J Med Biol Res. 2004 Dec;37(12):1819-30.
 
Daviet L, Colland F. Targeting ubiquitin specific proteases for drug discovery. Biochimie. 2008 Feb;90(2):270-83. https://doi.org/10.1016/j.biochi.2007.09.013
 
Gu H, Shi X, Liu C, Wang C, Sui N, Zhao Y, Gong J, Wang F, Zhang H, Li W, Zhao T. USP8 maintains embryonic stem cell stemness via deubiquitination of EPG5. Nat Commun. 2019 Apr 1;10(1): [9 p.]. https://doi.org/10.1038/s41467-019-09430-4
 
Hunt LC, Stover J, Haugen B, Shaw TI, Li Y, Pagala VR, Finkelstein D, Barton ER, Fan Y, Labelle M, Peng J, Demontis F. A key role for the ubiquitin ligase UBR4 in myofiber hypertrophy in Drosophila and mice. Cell Rep. 2019 Jul 30;28(5):1268-81.
 
Kawaguchi K, Endo A, Fukushima T, Madoka Y, Tanaka T, Komada M. Ubiquitin-specific protease 8 deubiquitinates Sec31A and decreases large COPII carriers and collagen IV secretion. Biochem Biophys Res Commun. 2018 May 15;499(3):635-41. https://doi.org/10.1016/j.bbrc.2018.03.202
 
Kitajima Y, Ono Y. Visualization of PAX7 protein dynamics in muscle satellite cells in a YFP knock-in-mouse line. Skelet Muscle. 2018 Aug 24;8(1): [11 p.]. https://doi.org/10.1186/s13395-018-0174-x
 
Kitajima Y, Suzuki N, Nunomiya A, Osana S, Yoshioka K, Tashiro Y, Takahashi R, Ono Y, Aoki M, Nagatomi R. The ubiquitin-proteasome system is indispensable for the maintenance of muscle stem cells. Stem Cell Rep. 2018 Dec 11;11(6):1523-38. https://doi.org/10.1016/j.stemcr.2018.10.009
 
Liu D, Xu J, Tong H, Li S, Yan Y. Effect of ELOVL3 expression on bovine skeletal muscle-derived satellite cell differentiation. Biochem Biophys Res Commun. 2017 Dec 2;493(4):1457-63. https://doi.org/10.1016/j.bbrc.2017.07.118
 
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001 Dec 1;25(4):402-8.
 
Mareco EA, de la Serrana DG, Johnston IA, Dal-Pai-Silva M. Characterization of the transcriptome of fast and slow muscle myotomal fibres in the pacu (Piaractus mesopotamicus). BMC Genomics. 2015 Mar 14;16(1): [13 p.]. https://doi.org/10.1186/s12864-015-1423-6
 
Mizuno E, Kitamura N, Komada M. 14-3-3-dependent inhibition of the deubiquitinating activity of UBPY and its cancellation in the M phase. Exp Cell Res. 2007 Oct 1;313(16):3624-34. https://doi.org/10.1016/j.yexcr.2007.07.028
 
Naviglio S, Matteucci C, Matoskova B, Nagase T, Nomura N, Di Fiore PP, Draetta GF. UBPY: A growth-regulated human ubiquitin isopeptidase. EMBO J. 1998 Jun 15;17(12):3241-50. https://doi.org/10.1093/emboj/17.12.3241
 
Niendorf S, Oksche A, Kisser A, Lohler J, Prinz M, Schorle H, Feller S, Lewitzky M, Horak I, Knobeloch KP. Essential role of ubiquitin-specific protease 8 for receptor tyrosine kinase stability and endocytic trafficking in vivo. Mol Cell Biol. 2007 Jul 1;27(13):5029-39. https://doi.org/10.1128/MCB.01566-06
 
Rantanen J, Hurme T, Lukka R, Heino J, Kalimo H. Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: Evidence for two different populations of satellite cells. Lab Invest. 1995 Mar 1;72(3):341-7.
 
Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell. 2000 Sep 15;102(6):777-86. https://doi.org/10.1016/S0092-8674(00)00066-0
 
Taylor MV, Hughes SM. Mef2 and the skeletal muscle differentiation program. Semin Cell Dev Biol. 2017 Dec 1;72:33-44. https://doi.org/10.1016/j.semcdb.2017.11.020
 
Wiles B, Miao M, Coyne E, Larose L, Cybulsky AV, Wing SS. USP19 deubiquitinating enzyme inhibits muscle cell differentiation by suppressing unfolded-protein response signaling. Mol Biol Cell. 2015 Mar 1;26(5):913-23. https://doi.org/10.1091/mbc.E14-06-1129
 
Will K, Schering L, Albrecht E, Kalbe C, Maak S. Differentiation of bovine satellite cell-derived myoblasts under different culture conditions. In Vitro Cell Dev Biol Anim. 2015 Jun 20;51(9):885-9. https://doi.org/10.1007/s11626-015-9916-9
 
Wu H, Ren Y, Li S, Wang W, Yuan J, Guo X, Liu D, Cang M. In vitro culture and induced differentiation of sheep skeletal muscle satellite cells. Cell Biol Int. 2012 Jun;36(6):579-87. https://doi.org/10.1042/CBI20110487
 
Yablonka-Reuveni Z. The skeletal muscle satellite cell: Still young and fascinating at 50. J Histochem Cytochem. 2011 Dec 5;59(12):1041-59.
 
Yuan Z, Chen Y, Zhang X, Zhou X, Li M, Chen H, Wu M, Zhang Y, Mo D. Silencing myotubularin related protein 7 enhances proliferation and early differentiation of C2C12 myoblast. Biochem Biophys Res Commun. 2017 Mar 11;484(3):592-7. https://doi.org/10.1016/j.bbrc.2017.01.143
 
Yun S, Kim KK. Ubiquitin-specific protease 4 (USP4) suppresses myoblast differentiation by down regulating MyoD activity in a catalytic-independent manner. Cell Signal. 2017 Jul;35:48-60. https://doi.org/10.1016/j.cellsig.2017.03.008
 
Zammit PS. Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis. Semin Cell Dev Biol. 2017 Dec 1;72:19-32.
 
download PDF

© 2021 Czech Academy of Agricultural Sciences | Prohlášení o přístupnosti