The titin A-band rod domain is dispensable for initial thick filament assembly in zebrafish

Developmental Biology

Volumn 387, Issue 1, 2014, Pages 93-108

  Myhre, J Layne ^a,b   Hills, Jordan A ^a   Prill, Kendal ^a   Wohlgemuth, Serene L ^a   Pilgrim, David B ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Muscle development; Myofibrillogenesis; Myogenesis; Sarcomere; Titin; Zebrafish

Indexed keywords

ACTIN; CONNECTIN; MYOSIN; TTNA PROTEIN; UNCLASSIFIED DRUG;

A BAND ROD DOMAIN; ALLELE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE MUTATION; HEART MUSCLE; MALE; MOLECULAR MODEL; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE FIBRIL; MUSCULAR DYSTROPHY; MUTANT; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; SARCOMERE; SKELETAL MUSCLE; TTNA GENE; ZEBRA FISH; ADULT; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; EMBRYO PATTERN FORMATION; PROTEIN FUNCTION; THIN FILAMENT;

MUSCLE DEVELOPMENT; MYOFIBRILLOGENESIS; MYOGENESIS; SARCOMERE; TITIN; ZEBRAFISH;

ANIMALS; CONNECTIN; HEART; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOCARDIUM; OLIGONUCLEOTIDES, ANTISENSE; PROTEIN STRUCTURE, TERTIARY; SARCOMERES; ZEBRAFISH;

EID: 84893651445     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.12.020     Document Type: Article

References (63)

1. Bang M.L., Centner T., Fornoff F., Geach A.J., Gotthardt M., McNabb M., Witt C.C., Labeit D., Gregorio C.C., Granzier H., Labeit S. The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ. Res. 2001, 89:1065-1072.
2. Barthel L.K., Raymond P.A. Improved method for obtaining 3-microns cryosections for immunocytochemistry. J. Histochem. Cytochem.: Official J. Histochem. Soc. 1990, 38:1383-1388.
3. Bill B.R., Petzold A.M., Clark K.J., Schimmenti L.A., Ekker S.C. A primer for morpholino use in zebrafish. Zebrafish 2009, 6:69-77.
4. Bonnemann C.G., Laing N.G. Myopathies resulting from mutations in sarcomeric proteins. Curr. Opin. Neurol. 2004, 17:529-537.
5. Bradley K.M., Elmore J.B., Breyer J.P., Yaspan B.L., Jessen J.R., Knapik E.W., Smith J.R. A major zebrafish polymorphism resource for genetic mapping. Genome. Biol. 2007, 8:R55.
6. Chen J.N., Haffter P., Odenthal J., Vogelsang E., Brand M., van Eeden F.J., Furutani-Seiki M., Granato M., Hammerschmidt M., Heisenberg C.P., Jiang Y.J., Kane D.A., Kelsh R.N., Mullins M.C., Nusslein-Volhard C. Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development 1996, 123:293-302.
7. Comyn S.A., Pilgrim D. Lack of developmental redundancy between Unc45 proteins in zebrafish muscle development. PLoS One 2012, 7:e48861.
8. Crawford G.L., Horowits R. Scaffolds and chaperones in myofibril assembly: putting the striations in striated muscle. Biophys. Rev. 2011, 3:25-32.
9. Du A., Sanger J.M., Sanger J.W. Cardiac myofibrillogenesis inside intact embryonic hearts. Dev. Biol. 2008, 318:236-246.
10. Ehler E., Gautel M. The sarcomere and sarcomerogenesis. Adv. Exp. Med. Biol. 2008, 642:1-14.
11. Etard C., Behra M., Fischer N., Hutcheson D., Geisler R., Strahle U. The UCS factor Steif/Unc-45b interacts with the heat shock protein Hsp90a during myofibrillogenesis. Dev. Biol. 2007, 308:133-143.
12. Fulton A.B., L'Ecuyer T. Cotranslational assembly of some cytoskeletal proteins: implications and prospects. J. Cell Sci. 1993, 105(Pt 4):867-871.
13. Gautel M. Cytoskeletal protein kinases: titin and its relations in mechanosensing. Pflugers Arch.: Eur. J. Physiol. 2011, 462:119-134.
14. Gazda L., Pokrzywa W., Hellerschmied D., Lowe T., Forne I., Mueller-Planitz F., Hoppe T., Clausen T. The myosin chaperone UNC-45 is organized in tandem modules to support myofilament formation in C. elegans. Cell 2013, 152:183-195.
15. Geisler R. Mapping and cloning. Zebrafish: A Practical Approach 2005, 175-212. Oxford University Press, Oxford. C. Nusslein-Volhard (Ed.).
16. Geisler R., Rauch G.J., Geiger-Rudolph S., Albrecht A., van Bebber F., Berger A., Busch-Nentwich E., Dahm R., Dekens M.P., Dooley C., Elli A.F., Gehring I., Geiger H., Geisler M., Glaser S., Holley S., Huber M., Kerr A., Kirn A., Knirsch M., Konantz M., Kuchler A.M., Maderspacher F., Neuhauss S.C., Nicolson T., Ober E.A., Praeg E., Ray R., Rentzsch B., Rick J.M., Rief E., Schauerte H.E., Schepp C.P., Schonberger U., Schonthaler H.B., Seiler C., Sidi S., Sollner C., Wehner A., Weiler C., Nusslein-Volhard C. Large-scale mapping of mutations affecting zebrafish development. BMC Genomics 2007, 8:11.
17. Ghosh C., Collodi P. Culture of cells from zebrafish (Brachydanio rerio) blastula-stage embryos. Cytotechnology 1994, 14:21-26.
18. Gongal P.A., Waskiewicz A.J. Zebrafish model of holoprosencephaly demonstrates a key role for TGIF in regulating retinoic acid metabolism. Hum. Mol. Genet. 2008, 17:525-538.
19. Granato M., van Eeden F.J., Schach U., Trowe T., Brand M., Furutani-Seiki M., Haffter P., Hammerschmidt M., Heisenberg C.P., Jiang Y.J., Kane D.A., Kelsh R.N., Mullins M.C., Odenthal J., Nusslein-Volhard C. Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 1996, 123:399-413.
20. Granzier H.L., Labeit S. The giant protein titin: a major player in myocardial mechanics, signaling, and disease. Circ. Res. 2004, 94:284-295.
21. Gregorio C.C., Trombitas K., Centner T., Kolmerer B., Stier G., Kunke K., Suzuki K., Obermayr F., Herrmann B., Granzier H., Sorimachi H., Labeit S. The NH2 terminus of titin spans the Z-disc: its interaction with a novel 19-kD ligand (T-cap) is required for sarcomeric integrity. J. Cell Biol. 1998, 143:1013-1027.
22. Guo W., Bharmal S.J., Esbona K., Greaser M.L. Titin diversity - alternative splicing gone wild. J. Biomed. Biotechnol. 2010, 2010:753675.
23. Hackman J.P., Vihola A.K., Udd A.B. The role of titin in muscular disorders. Ann. Med. 2003, 35:434-441.
24. Johnson S.L., Zon L.I. Genetic backgrounds and some standard stocks and strains used in zebrafish developmental biology and genetics. Methods Cell Biol. 1999, 60:357-359.
25. Kettleborough R.N., Busch-Nentwich E.M., Harvey S.A., Dooley C.M., de Bruijn E., van Eeden F., Sealy I., White R.J., Herd C., Nijman I.J., Fenyes F., Mehroke S., Scahill C., Gibbons R., Wali N., Carruthers S., Hall A., Yen J., Cuppen E., Stemple D.L. A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature 2013, 496:494-497.
26. Kim J., Lowe T., Hoppe T. Protein quality control gets muscle into shape. Trends Cell Biol. 2008, 18:264-272.
27. Kontrogianni-Konstantopoulos A., Ackermann M.A., Bowman A.L., Yap S.V., Bloch R.J. Muscle giants: molecular scaffolds in sarcomerogenesis. Physiol. Rev. 2009, 89:1217-1267.
28. Laing N.G., Nowak K.J. When contractile proteins go bad: the sarcomere and skeletal muscle disease. Bioessays 2005, 27:809-822.
29. Lange S., Xiang F., Yakovenko A., Vihola A., Hackman P., Rostkova E., Kristensen J., Brandmeier B., Franzen G., Hedberg B., Gunnarsson L.G., Hughes S.M., Marchand S., Sejersen T., Richard I., Edstrom L., Ehler E., Udd B., Gautel M. The kinase domain of titin controls muscle gene expression and protein turnover. Science 2005, 308:1599-1603.
30. Lisse T.S., Thiele F., Fuchs H., Hans W., Przemeck G.K., Abe K., Rathkolb B., Quintanilla-Martinez L., Hoelzlwimmer G., Helfrich M., Wolf E., Ralston S.H., Hrabe de Angelis M. ER stress-mediated apoptosis in a new mouse model of osteogenesis imperfecta. PLoS Genet. 2008, 4:e7.
31. Mayans O., van der Ven P.F., Wilm M., Mues A., Young P., Furst D.O., Wilmanns M., Gautel M. Structural basis for activation of the titin kinase domain during myofibrillogenesis. Nature 1998, 395:863-869.
32. Miller G., Musa H., Gautel M., Peckham M. A targeted deletion of the C-terminal end of titin, including the titin kinase domain, impairs myofibrillogenesis. J. Cell Sci. 2003, 116:4811-4819.
33. Musa H., Meek S., Gautel M., Peddie D., Smith A.J., Peckham M. Targeted homozygous deletion of M-band titin in cardiomyocytes prevents sarcomere formation. J. Cell Sci. 2006, 119:4322-4331.
34. Myhre J.L., Pilgrim D.B. Cellular differentiation in primary cell cultures from single zebrafish embryos as a model for the study of myogenesis. Zebrafish 2010, 7:255-266.
35. Obermann W.M., Gautel M., Weber K., Furst D.O. Molecular structure of the sarcomeric M band: mapping of titin and myosin binding domains in myomesin and the identification of a potential regulatory phosphorylation site in myomesin. EMBO J. 1997, 16:211-220.
36. Paulus J.D., Willer G.B., Willer J.R., Gregg R.G., Halloran M.C. Muscle contractions guide rohon-beard peripheral sensory axons. J. Neurosci. 2009, 29:13190-13201.
37. Peckham M., Young P., Gautel M. Constitutive and variable regions of Z-disk titin/connectin in myofibril formation: a dominant-negative screen. Cell Struct. Funct. 1997, 22:95-101.
38. Peng J., Raddatz K., Labeit S., Granzier H., Gotthardt M. Muscle atrophy in titin M-line deficient mice. J. Muscle Res. Cell Motil. 2005, 26:381-388.
39. Person V., Kostin S., Suzuki K., Labeit S., Schaper J. Antisense oligonucleotide experiments elucidate the essential role of titin in sarcomerogenesis in adult rat cardiomyocytes in long-term culture. J. Cell Sci. 2000, 113(Pt 21):3851-3859.
40. Puchner E.M., Alexandrovich A., Kho A.L., Hensen U., Schafer L.V., Brandmeier B., Grater F., Grubmuller H., Gaub H.E., Gautel M. Mechanoenzymatics of titin kinase. Proc. Natl. Acad. Sci. USA 2008, 105:13385-13390.
41. Rhee D., Sanger J.M., Sanger J.W. The premyofibril: evidence for its role in myofibrillogenesis. Cell Motil. Cytoskel. 1994, 28:1-24.
42. Sanger J.W., Kang S., Siebrands C.C., Freeman N., Du A., Wang J., Stout A.L., Sanger J.M. How to build a myofibril. J. Muscle Res. Cell Motil. 2005, 26:343-354.
43. Sanger J.W., Wang J., Fan Y., White J., Sanger J.M. Assembly and dynamics of myofibrils. J. Biomed. Biotechnol. 2010, 2010:858606.
44. Sanger J.W., Wang J.S., Holloway B., Du A.P., Sanger J.M. Myofibrillogenesis in skeletal muscle cells in zebrafish. Cell Motil. Cytoskel. 2009, 66:556-566.
45. Seeley M., Huang W., Chen Z., Wolff W.O., Lin X., Xu X. Depletion of zebrafish titin reduces cardiac contractility by disrupting the assembly of Z-discs and A-bands. Circ. Res. 2007, 100:238-245.
46. Selcen D., Engel A.G. Myofibrillar myopathy 1993, GeneReviews, Seattle, WA. R.A. Pagon, T.D. Bird, C.R. Dolan, K. Stephens, M.P. Adam (Eds.).
47. Sparrow J.C., Schock F. The initial steps of myofibril assembly: integrins pave the way. Nat. Rev. Mol. Cell Biol. 2009, 10:293-298.
48. Steffen L.S., Guyon J.R., Vogel E.D., Howell M.H., Zhou Y., Weber G.J., Zon L.I., Kunkel L.M. The zebrafish runzel muscular dystrophy is linked to the titin gene. Dev. Biol. 2007, 309:180-192.
49. Streisinger G., Walker C., Dower N., Knauber D., Singer F. Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 1981, 291:293-296.
50. Tokuyasu K.T. Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryos. III. Generation of fasciae adherentes and costameres. J. Cell Biol. 1989, 108:43-53.
51. Tskhovrebova L., Trinick J. Role of titin in vertebrate striated muscle. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2002, 357:199-206.
52. Tskhovrebova L., Trinick J. Titin: properties and family relationships. Nat. Rev. Mol. Cell Biol. 2003, 4:679-689.
53. Turnacioglu K.K., Mittal B., Dabiri G.A., Sanger J.M., Sanger J.W. Zeugmatin is part of the Z-band targeting region of titin. Cell Struct. Funct. 1997, 22:73-82.
54. Udd B. Distal myopathies - new genetic entities expand diagnostic challenge. Neuromuscul. Disord. 2012, 22:5-12.
55. van Eeden F.J., Granato M., Schach U., Brand M., Furutani-Seiki M., Haffter P., Hammerschmidt M., Heisenberg C.P., Jiang Y.J., Kane D.A., Kelsh R.N., Mullins M.C., Odenthal J., Warga R.M., Allende M.L., Weinberg E.S., Nusslein-Volhard C. Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 1996, 123:153-164.
56. Vleminckx V., Van Damme P., Goffin K., Delye H., Van Den Bosch L., Robberecht W. Upregulation of HSP27 in a transgenic model of ALS. J. Neuropathol. Exp. Neurol, 2002, 61:968-974.
57. Vogel B., Meder B., Just S., Laufer C., Berger I., Weber S., Katus H.A., Rottbauer W. In vivo characterization of human dilated cardiomyopathy genes in zebrafish. Biochem. Biophys. Res. Commun. 2009, 390:516-522.
58. Weinert S., Bergmann N., Luo X., Erdmann B., Gotthardt M. M line-deficient titin causes cardiac lethality through impaired maturation of the sarcomere. J. Cell Biol. 2006, 173:559-570.
59. Westerfield M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio) 2000, University of Oregon Press, Eugene, OR.
60. Whiting A., Wardale J., Trinick J. Does titin regulate the length of muscle thick filamentsα. J. Mol. Biol. 1989, 205:263-268.
61. Wohlgemuth S.L., Crawford B.D., Pilgrim D.B. The myosin co-chaperone UNC-45 is required for skeletal and cardiac muscle function in zebrafish. Dev. Biol. 2007, 303:483-492.
62. Xu X., Meiler S.E., Zhong T.P., Mohideen M., Crossley D.A., Burggren W.W., Fishman M.C. Cardiomyopathy in zebrafish due to mutation in an alternatively spliced exon of titin. Nat. Genet. 2002, 30:205-209.
63. Zou P., Gautel M., Geerlof A., Wilmanns M., Koch M.H., Svergun D.I. Solution scattering suggests cross-linking function of telethonin in the complex with titin. J. Biol. Chem. 2003, 278:2636-2644.