The E3 Ubiquitin Ligase Specificity Subunit ASB2beta is a Novel Regulator of Muscle Differentiation That Targets Filamin B to Proteasomal Degradation

Overview

Journal Cell Death Differ

Specialty Cell Biology

Date 2009 Mar 21

PMID 19300455

Citations 34

Authors

N F Bello

I Lamsoul

M L Heuze

A Metais

G Moreaux

D A Calderwood

D Duprez

C Moog-Lutz

P G Lutz

Affiliations

Soon will be listed here.

Abstract

Ubiquitin-mediated protein degradation is the main mechanism for controlled proteolysis, which is crucial for muscle development and maintenance. The ankyrin repeat-containing protein with a suppressor of cytokine signaling box 2 gene (ASB2) encodes the specificity subunit of an E3 ubiquitin ligase complex involved in differentiation of hematopoietic cells. Here, we provide the first evidence that a novel ASB2 isoform, ASB2beta, is important for muscle differentiation. ASB2beta is expressed in muscle cells during embryogenesis and in adult tissues. ASB2beta is part of an active E3 ubiquitin ligase complex and targets the actin-binding protein filamin B (FLNb) for proteasomal degradation. Thus, ASB2beta regulates FLNb functions by controlling its degradation. Knockdown of endogenous ASB2beta by shRNAs during induced differentiation of C2C12 cells delayed FLNb degradation as well as myoblast fusion and expression of muscle contractile proteins. Finally, knockdown of FLNb in ASB2beta knockdown cells restores myogenic differentiation. Altogether, our results suggest that ASB2beta is involved in muscle differentiation through the targeting of FLNb to destruction by the proteasome.

Citing Articles

Novel Candidate Genes Involved in an Initial Stage of White Striping Development in Broiler Chickens.

Padilha S, Ibelli A, Peixoto J, Cantao M, Moreira G, Fernandes L Animals (Basel). 2024; 14(16).

PMID: 39199913 PMC: 11350825. DOI: 10.3390/ani14162379.

Differential transcriptomic changes in the central nervous system and urinary bladders of mice infected with a coronavirus.

Clarkson T, Iguchi N, Xie A, Malykhina A PLoS One. 2022; 17(12):e0278918.

PMID: 36490282 PMC: 9733897. DOI: 10.1371/journal.pone.0278918.

Time-resolved phosphoproteome and proteome analysis reveals kinase signaling on master transcription factors during myogenesis.

Xiao D, Caldow M, Kim H, Blazev R, Koopman R, Manandi D iScience. 2022; 25(6):104489.

PMID: 35721465 PMC: 9198430. DOI: 10.1016/j.isci.2022.104489.

Dynamics of skeletal muscle-resident stem cells during myogenesis in fibrodysplasia ossificans progressiva.

Stanley A, Tichy E, Kocan J, Roberts D, Shore E, Mourkioti F NPJ Regen Med. 2022; 7(1):5.

PMID: 35031614 PMC: 8760285. DOI: 10.1038/s41536-021-00201-8.

Epigenetics of Skeletal Muscle-Associated Genes in the , , , and Gene Families.

Ehrlich K, Lacey M, Ehrlich M Epigenomes. 2021; 4(1).

PMID: 34968235 PMC: 8594701. DOI: 10.3390/epigenomes4010001.

References

Dedieu S, Poussard S, Mazeres G, Grise F, Dargelos E, Cottin P . Myoblast migration is regulated by calpain through its involvement in cell attachment and cytoskeletal organization. Exp Cell Res. 2004; 292(1):187-200. DOI: 10.1016/j.yexcr.2003.08.014. View

McDaneld T, Hannon K, Moody D . Ankyrin repeat and SOCS box protein 15 regulates protein synthesis in skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2006; 290(6):R1672-82. DOI: 10.1152/ajpregu.00239.2005. View

Nastasi T, Bongiovanni A, Campos Y, Mann L, Toy J, Bostrom J . Ozz-E3, a muscle-specific ubiquitin ligase, regulates beta-catenin degradation during myogenesis. Dev Cell. 2004; 6(2):269-82. DOI: 10.1016/s1534-5807(04)00020-6. View

Spencer J, Eliazer S, Ilaria Jr R, Richardson J, Olson E . Regulation of microtubule dynamics and myogenic differentiation by MURF, a striated muscle RING-finger protein. J Cell Biol. 2000; 150(4):771-84. PMC: 2175279. DOI: 10.1083/jcb.150.4.771. View

McCarthy J, Andrews J, McDearmon E, Campbell K, Barber B, Miller B . Identification of the circadian transcriptome in adult mouse skeletal muscle. Physiol Genomics. 2007; 31(1):86-95. PMC: 6080860. DOI: 10.1152/physiolgenomics.00066.2007. View

Witt S, Granzier H, Witt C, Labeit S . MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: towards understanding MURF-dependent muscle ubiquitination. J Mol Biol. 2005; 350(4):713-22. DOI: 10.1016/j.jmb.2005.05.021. View

Guibal F, Moog-Lutz C, Smolewski P, Di Gioia Y, Darzynkiewicz Z, Lutz P . ASB-2 inhibits growth and promotes commitment in myeloid leukemia cells. J Biol Chem. 2001; 277(1):218-24. DOI: 10.1074/jbc.M108476200. View

Sun L, Trausch-Azar J, Ciechanover A, Schwartz A . Ubiquitin-proteasome-mediated degradation, intracellular localization, and protein synthesis of MyoD and Id1 during muscle differentiation. J Biol Chem. 2005; 280(28):26448-56. DOI: 10.1074/jbc.M500373200. View

Calderwood D, Huttenlocher A, Kiosses W, Rose D, Woodside D, Schwartz M . Increased filamin binding to beta-integrin cytoplasmic domains inhibits cell migration. Nat Cell Biol. 2002; 3(12):1060-8. DOI: 10.1038/ncb1201-1060. View

10.

Andres V, Walsh K . Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J Cell Biol. 1996; 132(4):657-66. PMC: 2199863. DOI: 10.1083/jcb.132.4.657. View

11.

Heuze M, Guibal F, Banks C, Conaway J, Conaway R, Cayre Y . ASB2 is an Elongin BC-interacting protein that can assemble with Cullin 5 and Rbx1 to reconstitute an E3 ubiquitin ligase complex. J Biol Chem. 2004; 280(7):5468-74. DOI: 10.1074/jbc.M413040200. View

12.

Edom F, Mouly V, Barbet J, Fiszman M, Butler-Browne G . Clones of human satellite cells can express in vitro both fast and slow myosin heavy chains. Dev Biol. 1994; 164(1):219-29. DOI: 10.1006/dbio.1994.1193. View

13.

Solomon V, GOLDBERG A . Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. J Biol Chem. 1996; 271(43):26690-7. DOI: 10.1074/jbc.271.43.26690. View

14.

Moog-Lutz C, Cave-Riant F, Guibal F, Breau M, Di Gioia Y, Couraud P . JAML, a novel protein with characteristics of a junctional adhesion molecule, is induced during differentiation of myeloid leukemia cells. Blood. 2003; 102(9):3371-8. DOI: 10.1182/blood-2002-11-3462. View

15.

Hilton D, Richardson R, Alexander W, Viney E, Willson T, Sprigg N . Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc Natl Acad Sci U S A. 1998; 95(1):114-9. PMC: 18144. DOI: 10.1073/pnas.95.1.114. View

16.

Chomczynski P, Sacchi N . Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987; 162(1):156-9. DOI: 10.1006/abio.1987.9999. View

17.

Tozer S, Bonnin M, Relaix F, Di Savino S, Garcia-Villalba P, Coumailleau P . Involvement of vessels and PDGFB in muscle splitting during chick limb development. Development. 2007; 134(14):2579-91. DOI: 10.1242/dev.02867. View

18.

Menko A, Boettiger D . Occupation of the extracellular matrix receptor, integrin, is a control point for myogenic differentiation. Cell. 1987; 51(1):51-7. DOI: 10.1016/0092-8674(87)90009-2. View

19.

McElhinny A, Perry C, Witt C, Labeit S, Gregorio C . Muscle-specific RING finger-2 (MURF-2) is important for microtubule, intermediate filament and sarcomeric M-line maintenance in striated muscle development. J Cell Sci. 2004; 117(Pt 15):3175-88. DOI: 10.1242/jcs.01158. View

20.

Lindon C, Montarras D, Pinset C . Cell cycle-regulated expression of the muscle determination factor Myf5 in proliferating myoblasts. J Cell Biol. 1998; 140(1):111-8. PMC: 2132595. DOI: 10.1083/jcb.140.1.111. View