Loss of Smyhc1 or Hsp90α1 function results in different effects on myofibril organization in skeletal muscles of zebrafish embryos

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Codina, Marta ^a,b   Li, Junling ^a   Gutiérrez, Joaquim ^b   Kao, Joseph P Y ^a,c   Du, Shao Jun ^a,c  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME INHIBITOR; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 ALPHA 1; MYOSIN; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN 1; SULFONAMIDE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE MUTATION; LOSS OF FUNCTION MUTATION; MUSCLE FIBRIL; MYOFILAMENT; NONHUMAN; PHENOTYPE; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; SARCOMERE; SKELETAL MUSCLE; THIN FILAMENT; ZEBRA FISH; ANIMAL; GENE SILENCING; GENETICS; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT;

DANIO RERIO;

ANIMALS; GENE KNOCKDOWN TECHNIQUES; HSP90 HEAT-SHOCK PROTEINS; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; ZEBRAFISH;

EID: 77649136075     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008416     Document Type: Article

References (46)

1. Agarkova I, Perriard JC (2005) The M-band: an elastic web that crosslinks thick filaments in the center of the sarcomere. Trends Cell Biol 15: 477-485.
2. Boateng SY, Goldspink PH (2008) Assembly and maintenance of the sarcomere night and day. Cardiovasc Res 77: 667-675.
3. Clark KA, McElhinny AS, Beckerle MC, Gregorio CC (2002) Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol 18: 637-706.
4. Frank D, Kuhn C, Katus HA, Frey N (2006) The sarcomeric Z-disc: a nodal point in signalling and disease. J Mol Med 84: 446-468.
5. Gregorio CC, Granzier H, Sorimachi H, Labeit S (1999) Muscle assembly: a titanic achievement? Curr Opin Cell Biol 11: 18-25.
6. Squire JM (1997) Architecture and function in the muscle sarcomere. Curr Opin Struct Biol 7: 247-257.
7. Sanger JW, Chowrashi P, Shaner NC, Spalthoff S, Wang J, et al. (2002) Myofibrillogenesis in skeletal muscle cells. Clin Orthop Relat Res. pp S153-162.
8. Epstein HF, Fischman DA (1991) Molecular analysis of protein assembly in muscle development. Science 251: 1039-1044.
9. Sparrow JC, Schock F (2009) The initial steps of myofibril assembly: integrins pave the way. Nat Rev Mol Cell Biol 10: 293-298.
10. Barral JM, Bauer CC, Ortiz I, Epstein HF (1998) Unc-45 mutations in Caenorhabditis elegans implicate a CRO1/She4p-like domain in myosin assembly. J Cell Biol 143: 1215-1225.
11. Epstein HF, Bernstein SI (1992) Genetic approaches to understanding muscle development. Dev Biol 154: 231-244.
12. Epstein HF, Thomson JN (1974) Temperature-sensitive mutation affecting myofilament assembly in Caenorhabditis elegans. Nature 250: 579-580.
13. Landsverk ML, Epstein HF (2005) Genetic analysis of myosin II assembly and organization in model organisms. Cell Mol Life Sci 62: 2270-2282.
14. Moerman DG, Williams BD (2006) Sarcomere assembly in C. elegans muscle. WormBook. pp 1-16.
15. Du SJ, Li H, Bian Y, Zhong Y (2008) Heat-shock protein 90alpha1 is required for organized myofibril assembly in skeletal muscles of zebrafish embryos. Proc Natl Acad Sci U S A 105: 554-559.
16. Etard C, Behra M, Fischer N, Hutcheson D, Geisler R, et al. (2007) The UCS factor Steif/Unc-45b interacts with the heat shock protein Hsp90a during myofibrillogenesis. Dev Biol 308: 133-143.
17. Hawkins TA, Haramis AP, Etard C, Prodromou C, Vaughan CK, et al. (2008) The ATPase-dependent chaperoning activity of Hsp90a regulates thick filament formation and integration during skeletal muscle myofibrillogenesis. Development 135: 1147-1156.
18. Srikakulam R, Winkelmann DA (2004) Chaperone-mediated folding and assembly of myosin in striated muscle. J Cell Sci 117: 641-652.
19. Sass JB, Martin CC, Krone PH (1999) Restricted expression of the zebrafish hsp90alpha gene in slow and fast muscle fiber lineages. Int J Dev Biol 43: 835-838.
20. Bryson-Richardson RJ, Daggett DF, Cortes F, Neyt C, Keenan DG, et al. (2005) Myosin heavy chain expression in zebrafish and slow muscle composition. Dev Dyn 233: 1018-1022.
21. Elworthy S, Hargrave M, Knight R, Mebus K, Ingham PW (2008) Expression of multiple slow myosin heavy chain genes reveals a diversity of zebrafish slow twitch muscle fibres with differing requirements for Hedgehog and Prdm1 activity. Development 135: 2115-2126.
22. Devoto SH, Melancon E, Eisen JS, Westerfield M (1996) Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122: 3371-3380.
23. McGuigan K, Phillips PC, Postlethwait JH (2004) Evolution of sarcomeric myosin heavy chain genes: evidence from fish. Mol Biol Evol 21: 1042-1056.
24. Cheung A, Dantzig JA, Hollingworth S, Baylor SM, Goldman YE, et al. (2002) A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4: 83-88.
25. Kagawa M, Sato N, Obinata T (2006) Effects of BTS (N-benzyl-p-toluene sulphonamide), an inhibitor for myosin-actin interaction, on myofibrillogenesis in skeletal muscle cells in culture. Zoolog Sci 23: 969-975.
26. Dou Y, Andersson-Lendahl M, Arner A (2008) Structure and function of skeletal muscle in zebrafish early larvae. J Gen Physiol 131: 445-453.
27. Hayashi T, Silver RB, Ip W, Cayer ML, Smith DS (1977) Actin-myosin interaction. Self-assembly into a bipolar "contractile unit". J Mol Biol 111: 159-171.
28. Chun M, Falkenthal S (1988) Ifm(2)2 is a myosin heavy chain allele that disrupts myofibrillar assembly only in the indirect flight muscle of Drosophila melanogaster. J Cell Biol 107: 2613-2621.
29. Dibb NJ, Brown DM, Karn J, Moerman DG, Bolten SL, et al. (1985) Sequence analysis of mutations that affect the synthesis, assembly and enzymatic activity of the unc-54 myosin heavy chain of Caenorhabditis elegans. J Mol Biol 183: 543-551.
30. Li H, Randall WR, Du SJ (2009) skNAC (skeletal Naca), a muscle-specific isoform of Naca (nascent polypeptide-associated complex alpha), is required for myofibril organization. Faseb J 23: 1988-2000.
31. Funatsu T, Higuchi H, Ishiwata S (1990) Elastic filaments in skeletal muscle revealed by selective removal of thin filaments with plasma gelsolin. J Cell Biol 110: 53-62.
32. Funatsu T, Kono E, Higuchi H, Kimura S, Ishiwata S, et al. (1993) Elastic filaments in situ in cardiac muscle: deep-etch replica analysis in combination with selective removal of actin and myosin filaments. J Cell Biol 120: 711-724.
33. Kontrogianni-Konstantopoulos A, Catino DH, Strong JC, Sutter S, Borisov AB, et al. (2006) Obscurin modulates the assembly and organization of sarcomeres and the sarcoplasmic reticulum. Faseb J 20: 2102-2111.
34. van der Ven PF, Bartsch JW, Gautel M, Jockusch H, Furst DO (2000) A functional knock-out of titin results in defective myofibril assembly. J Cell Sci 113(Pt 8): 1405-1414.
35. Witt CC, Burkart C, Labeit D, McNabb M, Wu Y, et al. (2006) Nebulin regulates thin filament length, contractility, and Z-disk structure in vivo. Embo J 25: 3843-3855.
36. Soeno Y, Shimada Y, Obinata T (1999) BDM (2,3-butanedione monoxime), an inhibitor of myosin-actin interaction, suppresses myofibrillogenesis in skeletal muscle cells in culture. Cell Tissue Res 295: 307-316.
37. Ramachandran I, Terry M, Ferrari MB (2003) Skeletal muscle myosin crossbridge cycling is necessary for myofibrillogenesis. Cell Motil Cytoskeleton 55: 61-72.
38. Shaw MA, Ostap EM, Goldman YE (2003) Mechanism of inhibition of skeletal muscle actomyosin by N-benzyl-p-toluenesulfonamide. Biochemistry 42: 6128-6135.
39. Bejsovec A, Anderson P (1988) Myosin heavy-chain mutations that disrupt Caenorhabditis elegans thick filament assembly. Genes Dev 2: 1307-1317.
40. Lowey S, Slayter HS, Weeds AG, Baker H (1969) Substructure of the myosin molecule. I. Subfragments of myosin by enzymic degradation. J Mol Biol 42: 1-29.
41. Cripps RM, Suggs JA, Bernstein SI (1999) Assembly of thick filaments and myofibrils occurs in the absence of the myosin head. Embo J 18: 1793-1804.
42. Zhao R, Davey M, Hsu YC, Kaplanek P, Tong A, et al. (2005) Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 120: 715-27.
43. Granato M, van Eeden FJ, Schach U, Trowe T, Brand M, et al. (1996) Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 123: 399-413.
44. Ali MM, Roe SM, Vaughan CK, Meyer P, Panaretou B, et al. (2006) Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440: 1013-1017.
45. Urasaki A, Morvan G, Kawakami K (2006) Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics 174: 639-49.
46. Tan X, Rotllant J, Li H, De Deyne P, Du SJ (2006) SmyD1, a histone methyltransferase, is required for myofibril organization and muscle contraction in zebrafish embryos. Proc Natl Acad Sci U S A 103: 2713-2718.