The Actin Polymerization Factor Diaphanous and the Actin Severing Protein Flightless I Collaborate to Regulate Sarcomere Size

Overview

Journal Dev Biol

Publisher Elsevier

Specialties Biology
Reproductive Medicine

Date 2020 Sep 27

PMID 32980309

Citations 11

Authors

Su Deng

Ruth L Silimon

Mridula Balakrishnan

Ingo Bothe

Devin Juros

David B Soffar

Mary K Baylies

Affiliations

Soon will be listed here.

Abstract

The sarcomere is the basic contractile unit of muscle, composed of repeated sets of actin thin filaments and myosin thick filaments. During muscle development, sarcomeres grow in size to accommodate the growth and function of muscle fibers. Failure in regulating sarcomere size results in muscle dysfunction; yet, it is unclear how the size and uniformity of sarcomeres are controlled. Here we show that the formin Diaphanous is critical for the growth and maintenance of sarcomere size: Dia sets sarcomere length and width through regulation of the number and length of the actin thin filaments in the Drosophila flight muscle. To regulate thin filament length and sarcomere size, Dia interacts with the Gelsolin superfamily member Flightless I (FliI). We suggest that these actin regulators, by controlling actin dynamics and turnover, generate uniformly sized sarcomeres tuned for the muscle contractions required for flight.

Citing Articles

Human formin FHOD3-mediated actin elongation is required for sarcomere integrity in cardiomyocytes.

Valencia D, Koeberlein A, Nakano H, Rudas A, Harui A, Spencer C bioRxiv. 2024; .

PMID: 39464085 PMC: 11507729. DOI: 10.1101/2024.10.13.618125.

Atypical cadherin, Fat2, regulates axon terminal organization in the developing olfactory receptor neurons.

Vien K, Duan Q, Yeung C, Barish S, Volkan P iScience. 2024; 27(7):110340.

PMID: 39055932 PMC: 11269957. DOI: 10.1016/j.isci.2024.110340.

Peripheral thickening of the sarcomeres and pointed end elongation of the thin filaments are both promoted by SALS and its formin interaction partners.

Farkas D, Szikora S, Jijumon A, Polgar T, Patai R, Toth M PLoS Genet. 2024; 20(1):e1011117.

PMID: 38198522 PMC: 10805286. DOI: 10.1371/journal.pgen.1011117.

Role of Actin-Binding Proteins in Skeletal Myogenesis.

Nguyen M, Dash R, Jeong K, Lee W Cells. 2023; 12(21).

PMID: 37947600 PMC: 10650911. DOI: 10.3390/cells12212523.

FLII Modulates the Myogenic Differentiation of Progenitor Cells via Actin Remodeling-Mediated YAP1 Regulation.

Nguyen M, Ly Q, Kim H, Lee W Int J Mol Sci. 2023; 24(18).

PMID: 37762638 PMC: 10531566. DOI: 10.3390/ijms241814335.

References

Rosado M, Barber C, Berciu C, Feldman S, Birren S, Nicastro D . Critical roles for multiple formins during cardiac myofibril development and repair. Mol Biol Cell. 2014; 25(6):811-27. PMC: 3952851. DOI: 10.1091/mbc.E13-08-0443. View

Burkart C, Qiu F, Brendel S, Benes V, Haag P, Labeit S . Modular proteins from the Drosophila sallimus (sls) gene and their expression in muscles with different extensibility. J Mol Biol. 2007; 367(4):953-69. DOI: 10.1016/j.jmb.2007.01.059. View

Pappas C, Krieg P, Gregorio C . Nebulin regulates actin filament lengths by a stabilization mechanism. J Cell Biol. 2010; 189(5):859-70. PMC: 2878950. DOI: 10.1083/jcb.201001043. View

Sewry C, Laitila J, Wallgren-Pettersson C . Nemaline myopathies: a current view. J Muscle Res Cell Motil. 2019; 40(2):111-126. PMC: 6726674. DOI: 10.1007/s10974-019-09519-9. View

Matsubayashi Y, Coulson-Gilmer C, Millard T . Endocytosis-dependent coordination of multiple actin regulators is required for wound healing. J Cell Biol. 2015; 210(3):419-33. PMC: 4523608. DOI: 10.1083/jcb.201411037. View

Bi W, Saifi G, Shaw C, Walz K, Fonseca P, Wilson M . Mutations of RAI1, a PHD-containing protein, in nondeletion patients with Smith-Magenis syndrome. Hum Genet. 2004; 115(6):515-24. DOI: 10.1007/s00439-004-1187-6. View

Taniguchi K, Takeya R, Suetsugu S, Kan-O M, Narusawa M, Shiose A . Mammalian formin fhod3 regulates actin assembly and sarcomere organization in striated muscles. J Biol Chem. 2009; 284(43):29873-81. PMC: 2785617. DOI: 10.1074/jbc.M109.059303. View

Pizon V, Iakovenko A, van der Ven P, Kelly R, Fatu C, Furst D . Transient association of titin and myosin with microtubules in nascent myofibrils directed by the MURF2 RING-finger protein. J Cell Sci. 2002; 115(Pt 23):4469-82. DOI: 10.1242/jcs.00131. View

Daou P, Hasan S, Breitsprecher D, Baudelet E, Camoin L, Audebert S . Essential and nonredundant roles for Diaphanous formins in cortical microtubule capture and directed cell migration. Mol Biol Cell. 2014; 25(5):658-68. PMC: 3937091. DOI: 10.1091/mbc.E13-08-0482. View

10.

Kremneva E, Makkonen M, Skwarek-Maruszewska A, Gateva G, Michelot A, Dominguez R . Cofilin-2 controls actin filament length in muscle sarcomeres. Dev Cell. 2014; 31(2):215-26. PMC: 4223631. DOI: 10.1016/j.devcel.2014.09.002. View

11.

Deng S, Bothe I, Baylies M . The Formin Diaphanous Regulates Myoblast Fusion through Actin Polymerization and Arp2/3 Regulation. PLoS Genet. 2015; 11(8):e1005381. PMC: 4546610. DOI: 10.1371/journal.pgen.1005381. View

12.

Nowotarski S, McKeon N, Moser R, Peifer M . The actin regulators Enabled and Diaphanous direct distinct protrusive behaviors in different tissues during Drosophila development. Mol Biol Cell. 2014; 25(20):3147-65. PMC: 4196866. DOI: 10.1091/mbc.E14-05-0951. View

13.

Fowler V . Thin filaments elongate from their pointed ends during myofibril assembly in Drosophila indirect flight muscle. J Cell Biol. 2001; 155(6):1043-53. PMC: 2150893. DOI: 10.1083/jcb.200108026. View

14.

Straub K, Stella M, Leptin M . The gelsolin-related flightless I protein is required for actin distribution during cellularisation in Drosophila. J Cell Sci. 1996; 109 ( Pt 1):263-70. DOI: 10.1242/jcs.109.1.263. View

15.

Malfatti E, Romero N . Nemaline myopathies: State of the art. Rev Neurol (Paris). 2016; 172(10):614-619. DOI: 10.1016/j.neurol.2016.08.004. View

16.

Iskratsch T, Reijntjes S, Dwyer J, Toselli P, Degano I, Dominguez I . Two distinct phosphorylation events govern the function of muscle FHOD3. Cell Mol Life Sci. 2012; 70(5):893-908. PMC: 3696992. DOI: 10.1007/s00018-012-1154-7. View

17.

Dhanyasi N, VijayRaghavan K, Shilo B, Schejter E . Microtubules provide guidance cues for myofibril and sarcomere assembly and growth. Dev Dyn. 2020; 250(1):60-73. DOI: 10.1002/dvdy.227. View

18.

Afshar K, Stuart B, Wasserman S . Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development. 2000; 127(9):1887-97. DOI: 10.1242/dev.127.9.1887. View

19.

DE Couet H, Fong K, Weeds A, McLaughlin P, Miklos G . Molecular and mutational analysis of a gelsolin-family member encoded by the flightless I gene of Drosophila melanogaster. Genetics. 1995; 141(3):1049-59. PMC: 1206829. DOI: 10.1093/genetics/141.3.1049. View

20.

Orfanos Z, Leonard K, Elliott C, Katzemich A, Bullard B, Sparrow J . Sallimus and the dynamics of sarcomere assembly in Drosophila flight muscles. J Mol Biol. 2015; 427(12):2151-8. DOI: 10.1016/j.jmb.2015.04.003. View