Severe myopathy in mice lacking the MEF2/SRFdependent gene leiomodin-3

Journal of Clinical Investigation

Volumn 125, Issue 4, 2015, Pages 1569-1578

  Cenik, Bercin K ^a   Garg, Ankit ^a   McAnally, John R ^a   Shelton, John M ^b   Richardson, James A ^b   Bassel Duby, Rhonda ^a   Olson, Eric N ^a   Liu, Ning ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KELCH LIKE FAMILY MEMBER 40; LEIOMODIN 3; MYOCARDIN RELATED TRANSCRIPTION FACTOR; MYOCYTE ENHANCER FACTOR 2; PROTEIN; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ACTIN; ACTIN BINDING PROTEIN; CREATINE KINASE MM; HYBRID PROTEIN; KBTBD5 PROTEIN, MOUSE; LEIOMODIN-3 PROTEIN, MOUSE; MUSCLE PROTEIN; TRANSACTIVATOR PROTEIN;

ACTIN POLYMERIZATION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; FAILURE TO THRIVE; FEMALE; GENETIC TRANSCRIPTION; IN SITU HYBRIDIZATION; MALE; MOLECULAR PATHOLOGY; MOUSE; MUSCLE DISEASE; NEMALINE MYOPATHY; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SARCOMERE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; ANIMAL; ANTIBODY SPECIFICITY; CHEMISTRY; CHLOROCEBUS AETHIOPS; CONSENSUS SEQUENCE; COS CELL LINE; DEFICIENCY; GENE EXPRESSION REGULATION; GENE SILENCING; GENE THERAPY; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUSCLE CONTRACTION; PATHOLOGY; PHYSIOLOGY; POLYMERIZATION; PROMOTER REGION; TRANSGENE; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ACTINS; ANIMALS; CERCOPITHECUS AETHIOPS; CONSENSUS SEQUENCE; COS CELLS; CREATINE KINASE, MM FORM; FAILURE TO THRIVE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENETIC THERAPY; MEF2 TRANSCRIPTION FACTORS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOPATHIES, NEMALINE; ORGAN SPECIFICITY; POLYMERIZATION; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; SARCOMERES; SERUM RESPONSE FACTOR; TRANS-ACTIVATORS; TRANSGENES;

EID: 84926321428     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI80115     Document Type: Article

References (55)

1. Ryan MM, et al. Clinical course correlates poorly with muscle pathology in nemaline myopathy. Neurology. 2003;60(4):665-673.
2. Romero NB, Clarke NF. Congenital myopathies. Handb Clin Neurol. 2013;113:1321-1336.
3. Romero NB, Sandaradura SA, Clarke NF. Recent advances in nemaline myopathy. Curr Opin Neurol. 2013;26(5):519-526.
4. North KN, Ryan MM. Nemaline Myopathy. GeneReviews. Seattle, Washington, USA: University of Washington; 2002.
5. Nowak KJ, Ravenscroft G, Laing NG. Skeletal muscle alpha-actin diseases (actinopathies): pathology and mechanisms. Acta Neuropathol. 2013;125(1):19-32.
6. Garg A, et al. KLHL40 deficiency destabilizes thin filament proteins and promotes nemaline myopathy. J Clin Invest. 2014;124(8):3529-3539.
7. Ravenscroft G, et al. Mutations in KLHL40 are a frequent cause of severe autosomal-recessive nemaline myopathy. Am J Hum Genet. 2013;93(1):6-18.
8. Marttila M, et al. Nebulin interactions with actin and tropomyosin are altered by disease-causing mutations. Skelet Muscle. 2014;4:15.
9. Gupta VA, Beggs AH. Kelch proteins: emerging roles in skeletal muscle development and diseases. Skelet Muscle. 2014;4:11.
10. Yuen M, et al. Leiomodin-3 dysfunction results in thin filament disorganization nemaline myopathy. J Clin Invest. 2014;124(11):4693-4708.
11. Nworu CU, Kraft R, Schnurr DC, Gregorio CC, Krieg PA. Leiomodin 3 Tropomodulin 4 have overlapping functions during skeletal myofibrillogenesis. J Cell Sci. 2015;128(2):239-250.
12. Campellone KG, Welch MD. A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol. 2010;11(4):237-251.
13. Chereau D, et al. Leiomodin is an actin filament nucleator in muscle cells. Science. 2008;320(5873):239-243.
14. Conley CA, Fritz-Six KL, Almenar-Queralt A, Fowler VM. Leiomodins: larger members of the tropomodulin (Tmod) gene family. Genomics. 2001;73(2):127-139.
15. Tsukada T, et al. Leiomodin-2 is an antagonist of tropomodulin-1 at the pointed end of the thin filaments in cardiac muscle. J Cell Sci. 2010; 123(pt 18):3136-3145.
16. Qualmann B, Kessels MM. New players in actin polymerization - WH2-domain-containing actin nucleators. Trends Cell Biol. 2009;19(6):276-285.
17. Wang DZ, et al. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci U S A. 2002;99(23):14855-14860.
18. Kuwahara K, Barrientos T, Pipes GC, Li S, Olson EN. Muscle-specific signaling mechanism that links actin dynamics to serum response factor. Mol Cell Biol. 2005;25(8):3173-3181.
19. Olson EN, Nordheim A. Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol. 2010;11(5):353-365.
20. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell. 2003;113(3):329-342.
21. Vartiainen MK, Guettler S, Larijani B, Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science. 2007;316(5832):1749-1752.
22. Miano JM, Long X, Fujiwara K. Serum response factor: master regulator of the actin cytoskeleton and contractile apparatus. Am J Physiol Cell Physiol. 2007;292(1):C70-C81.
23. Potthoff MJ, Olson EN. MEF2: a central regulator of diverse developmental programs. Development. 2007;134(23):4131-4140.
24. Esnault C, et al. Rho-actin signaling to the MRTF coactivators dominates the immediate transcriptional response to serum in fibroblasts. Genes Dev. 2014;28(9):943-958.
25. Schnell C, Kan A, North KN. 'An artefact gone awry': identification of the first case of nemaline myopathy by Dr R.D.K. Reye. Neuromuscul Disord. 2000;10(4-5):307-312.
26. Ilkovski B, et al. Nemaline myopathy caused by mutations in the muscle a-skeletal-actin gene. Am J Hum Genet. 2001;68(6):1333-1343.
27. Grayson J, Williams RS, Yu YT, Bassel-Duby R. Synergistic interactions between heterologous upstream activation elements and specific TATA sequences in a muscle-specific promoter. Mol Cell Biol. 1995;15(4):1870-1878.
28. Leibham D, et al. Binding of TFIID and MEF2 to the TATA element activates transcription of the Xenopus MyoDa promoter. Mol Cell Biol. 1994;14(1):686-699.
29. He A, Kong SW, Ma Q, Pu WT. Co-occupancy by multiple cardiac transcription factors identifies transcriptional enhancers active in heart. Proc Natl Acad Sci U S A. 2011;108(14):5632-5637.
30. Kothary R, et al. Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development. 1989;105(4):707-714.
31. Liu N, et al. Requirement of MEF2A, C, and D for skeletal muscle regeneration. Proc Natl Acad Sci U S A. 2014;111(11):4109-4114.
32. Kuwahara K, et al. Modulation of adverse cardiac remodeling by STARS, a mediator of MEF2 signaling and SRF activity. J Clin Invest. 2007;117(5):1324-1334.
33. Malfatti E, et al. Muscle histopathology in nebulin-related nemaline myopathy: ultrastrastructural findings correlated to disease severity and genotype. Acta Neuropathol Commun. 2014;2:44.
34. Carlier MF, et al. Structure, function, and evolution of the β-thymosin/WH2 (WASP-Homology2) actin-binding module. Ann N Y Acad Sci. 2007;1112:67-75.
35. Paunola E, Mattila PK, Lappalainen P. WH2 domain: a small, versatile adapter for actin monomers. FEBS Lett. 2002;513(1):92-97.
36. Rasson AS, Bois JS, Pham DS, Yoo H, Quinlan ME. Filament assembly by spire: key residues and concerted actin binding. J Mol Biol. 2015;427(4):824-839.
37. DiFranco M, Quinonez M, Capote J, Vergara J. DNA transfection of mammalian skeletal muscles using in vivo electroporation. J Vis Exp. 2009;(32):e1520.
38. Miller JC, et al. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol. 2011;29(2):143-148.
39. Bedell VM, et al. In vivo genome editing using a high-efficiency TALEN system. Nature. 2012;491(7422):114-118.
40. Kato T, et al. Production of Sry knockout mouse using TALEN via oocyte injection. Sci Rep. 2013;3:3136.
41. Sung YH, Jin Y, Kim S, Lee HW. Generation of knockout mice using engineered nucleases. Methods. 2014;69(1):85-93.
42. Cermak T, et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 2011;39(12):e82.
43. Doyle EL, et al. TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res. 2012;40(Web Server issue):W117-W122.
44. Long C, et al. Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA. Science. 2014;345(6201):1184-1188.
45. Wang H, et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/ Cas-mediated genome engineering. Cell. 2013;153(4):910-918.
46. Kim HJ, Lee HJ, Kim H, Cho SW, Kim JS. Targeted genome editing in human cells with zinc finger nucleases constructed via modular assembly. Genome Res. 2009;19(7):1279-1288.
47. Kim MS, et al. Protein kinase D1 stimulates MEF2 activity in skeletal muscle and enhances muscle performance. Mol Cell Biol. 2008;28(11):3600-3609.
48. Naya FJ, et al. Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J Biol Chem. 2000;275(7):4545-4548.
49. Sternberg EA, et al. Identification of upstream and intragenic regulatory elements that confer cell-type-restricted and differentiation-specific expression on the muscle creatine kinase gene. Mol Cell Biol. 1988;8(7):2896-2909.
50. Cheng TC, Hanley TA, Mudd J, Merlie JP, Olson EN. Mapping of myogenin transcription during embryogenesis using transgenes linked to the myogenin control region. J Cell Biol. 1992;119(6):1649-1656.
51. Hargrave M, Koopman P. In situ hybridization of whole-mount embryos. Methods Mol Biol. 2000;123:279-289.
52. Millay DP, et al. Myomaker is a membrane activator of myoblast fusion and muscle formation. Nature. 2013;499(7458):301-305.
53. Wu H, et al. Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science. 2002;296(5566):349-352.
54. Liu N, et al. Mice lacking microRNA 133a develop dynamin 2-dependent centronuclear myopathy. J Clin Invest. 2011;121(8):3258-3268.
55. Nelson BR, et al. Skeletal muscle-specific Ttubule protein STAC3 mediates voltage-induced Ca2+ release and contractility. Proc Natl Acad Sci U S A. 2013;110(29):11881-11886.