Post-transcriptional regulation of myotube elongation and myogenesis by Hoi polloi

Development (Cambridge)

Volumn 140, Issue 17, 2013, Pages 3645-3656

  Johnson, Aaron N ^a,b   Mokalled, Mayssa H ^c   Valera, Juliana M ^b   Poss, Kenneth D ^c   Olson, Eric N ^a  

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

^b UNIVERSITY OF COLORADO   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Drosophila; Myogenesis; Myotube elongation; Post transcriptional regulation; Zebrafish

Indexed keywords

HOI POLLOI PROTEIN; MYOSIN HEAVY CHAIN; RNA BINDING PROTEIN; TROPOMYOSIN; UNCLASSIFIED DRUG;

ARTICLE; DROSOPHILA; EMBRYO; GENETIC SCREENING; HEART MUSCLE; MAJOR HISTOCOMPATIBILITY COMPLEX; MUSCLE DEVELOPMENT; MUSCLE DISEASE; MYOBLAST; MYOTUBE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SPLICING; SKELETAL MUSCLE; STRUCTURAL GENE; ZEBRA FISH;

DROSOPHILA; MYOGENESIS; MYOTUBE ELONGATION; POST-TRANSCRIPTIONAL REGULATION; ZEBRAFISH;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; DNA PRIMERS; DROSOPHILA; DROSOPHILA PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MUSCLE, STRIATED; MUTAGENESIS, SITE-DIRECTED; MYOSIN HEAVY CHAINS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA-BINDING PROTEINS; SARCOMERES; SEQUENCE ANALYSIS, RNA; TROPOMYOSIN; ZEBRAFISH;

EID: 84881587073     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.095596     Document Type: Article

References (74)

1. Barolo, S., Castro, B. and Posakony, J. W. (2004). New Drosophila transgenic reporters: insulated P-element vectors expressing fast-maturing RFP. Biotechniques 36, 436-440, 442.
2. Bate, M. (1990). The embryonic development of larval muscles in Drosophila. Development 110, 791-804.
3. Bernstein, S. I., Mogami, K., Donady, J. J. and Emerson, C. P., Jr (1983). Drosophila muscle myosin heavy chain encoded by a single gene in a cluster of muscle mutations. Nature 302, 393-397.
4. Biedermann, B., Hotz, H. R. and Ciosk, R. (2010). The Quaking family of RNA-binding proteins: coordinators of the cell cycle and differentiation. Cell Cycle 9, 1929-1933.
5. Bloor, J. W. and Brown, N. H. (1998). Genetic analysis of the Drosophila alphaPS2 integrin subunit reveals discrete adhesive, morphogenetic and sarcomeric functions. Genetics 148, 1127-1142.
6. Bour, B. A., O'Brien, M. A., Lockwood, W. L., Goldstein, E. S., Bodmer, R., Taghert, P. H., Abmayr, S. M. and Nguyen, H. T. (1995). Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev. 9, 730-741.
7. Brown, N. H. (1994). Null mutations in the alpha PS2 and beta PS integrin subunit genes have distinct phenotypes. Development 120, 1221-1231.
8. Brown, N. H., Gregory, S. L., Rickoll, W. L., Fessler, L. I., Prout, M., White, R. A. and Fristrom, J. W. (2002). Talin is essential for integrin function in Drosophila. Dev. Cell 3, 569-579.
9. Bunch, T. A., Graner, M. W., Fessler, L. I., Fessler, J. H., Schneider, K. D., Kerschen, A., Choy, L. P., Burgess, B. W. and Brower, D. L. (1998). The PS2 integrin ligand tiggrin is required for proper muscle function in Drosophila. Development 125, 1679-1689.
10. Callahan, C. A., Bonkovsky, J. L., Scully, A. L. and Thomas, J. B. (1996). derailed is required for muscle attachment site selection in Drosophila. Development 122, 2761-2767.
11. Carmena, A., Bate, M. and Jiménez, F. (1995). Lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev. 9, 2373-2383.
12. Carrasco-Rando, M. and Ruiz-Gómez, M. (2008). Mind bomb 2, a founder myoblast-specific protein, regulates myoblast fusion and muscle stability. Development 135, 849-857.
13. Chanana, B., Graf, R., Koledachkina, T., Pflanz, R. and Vorbrüggen, G. (2007). AlphaPS2 integrin-mediated muscle attachment in Drosophila requires the ECM protein Thrombospondin. Mech. Dev. 124, 463-475.
14. Chen, E. H. and Olson, E. N. (2001). Antisocial, an intracellular adaptor protein, is required for myoblast fusion in Drosophila. Dev. Cell 1, 705-715.
15. Cléry, A., Senty-Ségault, V., Leclerc, F., Raué, H. A. and Branlant, C. (2007). Analysis of sequence and structural features that identify the B/C motif of U3 small nucleolar RNA as the recognition site for the Snu13p-Rrp9p protein pair. Mol. Cell. Biol. 27, 1191-1206.
16. de Joussineau, C., Bataillé, L., Jagla, T. and Jagla, K. (2012). Diversification of muscle types in Drosophila: upstream and downstream of identity genes. Curr. Top. Dev. Biol. 98, 277-301.
17. Dennis, G., Jr, Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C. and Lempicki, R. A. (2003). DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol. 4, 3.
18. Dobbyn, H. C. and O'Keefe, R. T. (2004). Analysis of Snu13p mutations reveals differential interactions with the U4 snRNA and U3 snoRNA. RNA 10, 308-320.
19. Elhanany-Tamir, H., Yu, Y. V., Shnayder, M., Jain, A., Welte, M. and Volk, T. (2012). Organelle positioning in muscles requires cooperation between two KASH proteins and microtubules. J. Cell Biol. 198, 833-846.
20. Estrada, B., Gisselbrecht, S. S. and Michelson, A. M. (2007). The transmembrane protein Perdido interacts with Grip and integrins to mediate myotube projection and attachment in the Drosophila embryo. Development 134, 4469-4478.
21. Folker, E. S., Schulman, V. K. and Baylies, M. K. (2012). Muscle length and myonuclear position are independently regulated by distinct Dynein pathways. Development 139, 3827-3837.
22. Frommer, G., Vorbrüggen, G., Pasca, G., Jäckle, H. and Volk, T. (1996). Epidermal egr-like zinc finger protein of Drosophila participates in myotube guidance. EMBO J. 15, 1642-1649.
23. Ge, J., Liu, H. and Yu, Y. T. (2010). Regulation of pre-mRNA splicing in Xenopus oocytes by targeted 2'-O-methylation. RNA 16, 1078-1085.
24. Gilsohn, E. and Volk, T. (2010a). Slowdown promotes muscle integrity by modulating integrin-mediated adhesion at the myotendinous junction. Development 137, 785-794.
25. Gilsohn, E. and Volk, T. (2010b). A screen for tendon-specific genes uncovers new and old components involved in muscle-tendon interaction. Fly (Austin) 4, 149-153.
26. Guerin, C. M. and Kramer, S. G. (2009a). Cytoskeletal remodeling during myotube assembly and guidance: coordinating the actin and microtubule networks. Commun. Integr. Biol. 2, 452-457.
27. Guerin, C. M. and Kramer, S. G. (2009b). RacGAP50C directs perinuclear gamma-tubulin localization to organize the uniform microtubule array required for Drosophila myotube extension. Development 136, 1411-1421.
28. Gurkan, C., Lapp, H., Alory, C., Su, A. I., Hogenesch, J. B. and Balch, W. E. (2005). Large-scale profiling of Rab GTPase trafficking networks: the membrome. Mol. Biol. Cell 16, 3847-3864.
29. Hess, N. K., Singer, P. A., Trinh, K., Nikkhoy, M. and Bernstein, S. I. (2007). Transcriptional regulation of the Drosophila melanogaster muscle myosin heavy-chain gene. Gene Expr. Patterns 7, 413-422.
30. Higashijima, S., Okamoto, H., Ueno, N., Hotta, Y. and Eguchi, G. (1997). High-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Dev. Biol. 192, 289-299.
31. Jagla, T., Bellard, F., Lutz, Y., Dretzen, G., Bellard, M. and Jagla, K. (1998). ladybird determines cell fate decisions during diversification of Drosophila somatic muscles. Development 125, 3699-3708.
32. Jia, Y., Mu, J. C. and Ackerman, S. L. (2012). Mutation of a U2 snRNA gene causes global disruption of alternative splicing and neurodegeneration. Cell 148, 296-308.
33. Johnson, A. N., Burnett, L. A., Sellin, J., Paululat, A. and Newfeld, S. J. (2007). Defective decapentaplegic signaling results in heart overgrowth and reduced cardiac output in Drosophila. Genetics 176, 1609-1624.
34. Johnson, A. N., Mokalled, M. H., Haden, T. N. and Olson, E. N. (2011). JAK/Stat signaling regulates heart precursor diversification in Drosophila. Development 138, 4627-4638.
35. Kania, A., Salzberg, A., Bhat, M., D'Evelyn, D., He, Y., Kiss, I. and Bellen, H. J. (1995). P-element mutations affecting embryonic peripheral nervous system development in Drosophila melanogaster. Genetics 139, 1663-1678.
36. Kiehart, D. P. and Feghali, R. (1986). Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol. 103, 1517-1525.
37. Kosman, D., Small, S. and Reinitz, J. (1998). Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev. Genes Evol. 208, 290-294.
38. Kramer, S. G., Kidd, T., Simpson, J. H. and Goodman, C. S. (2001). Switching repulsion to attraction: changing responses to slit during transition in mesoderm migration. Science 292, 737-740.
39. Kronert, W. A., O'Donnell, P. T. and Bernstein, S. I. (1994). A charge change in an evolutionarily-conserved region of the myosin globular head prevents myosin and thick filament accumulation in Drosophila. J. Mol. Biol. 236, 697-702.
40. Li, W. and Gao, F. B. (2003). Actin filament-stabilizing protein tropomyosin regulates the size of dendritic fields. J. Neurosci. 23, 6171-6175.
41. Lilly, B., Zhao, B., Ranganayakulu, G., Paterson, B. M., Schulz, R. A. and Olson, E. N. (1995). Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267, 688-693.
42. Martin-Bermudo, M. D. and Brown, N. H. (2000). The localized assembly of extracellular matrix integrin ligands requires cell-cell contact. J. Cell Sci. 113, 3715-3723.
43. Mokalled, M. H., Johnson, A., Kim, Y., Oh, J. and Olson, E. N. (2010). Myocardin-related transcription factors regulate the Cdk5/Pctaire1 kinase cascade to control neurite outgrowth, neuronal migration and brain development. Development 137, 2365-2374.
44. Nagaraj, R. and Adler, P. N. (2012). Dusky-like functions as a Rab11 effector for the deposition of cuticle during Drosophila bristle development. Development 139, 906-916.
45. Nose, A., Isshiki, T. and Takeichi, M. (1998). Regional specification of muscle progenitors in Drosophila: the role of the msh homeobox gene. Development 125, 215-223.
46. Nottrott, S., Hartmuth, K., Fabrizio, P., Urlaub, H., Vidovic, I., Ficner, R. and Lührmann, R. (1999). Functional interaction of a novel 15.5kD [U4/U6.U5] tri-snRNP protein with the 5' stem-loop of U4 snRNA. EMBO J. 18, 6119-6133.
47. Prokopenko, S. N., He, Y., Lu, Y. and Bellen, H. J. (2000). Mutations affecting the development of the peripheral nervous system in Drosophila: a molecular screen for novel proteins. Genetics 156, 1691-1715.
48. Reim, I., Mohler, J. P. and Frasch, M. (2005). Tbx20-related genes, mid and H15, are required for tinman expression, proper patterning, and normal differentiation of cardioblasts in Drosophila. Mech. Dev. 122, 1056-1069.
49. Robinson, J. T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G. and Mesirov, J. P. (2011). Integrative genomics viewer. Nat. Biotechnol. 29, 24-26.
50. Rosenberg-Hasson, Y., Renert-Pasca, M. and Volk, T. (1996). A Drosophila dystrophin-related protein, MSP-300, is required for embryonic muscle morphogenesis. Mech. Dev. 60, 83-94.
51. Rui, Y., Bai, J. and Perrimon, N. (2010). Sarcomere formation occurs by the assembly of multiple latent protein complexes. PLoS Genet. 6, e1001208.
52. Schejter, E. D. and Baylies, M. K. (2010). Born to run: creating the muscle fiber. Curr. Opin. Cell Biol. 22, 566-574.
53. Schnorrer, F. and Dickson, B. J. (2004). Muscle building; mechanisms of myotube guidance and attachment site selection. Dev. Cell 7, 9-20.
54. Schnorrer, F., Kalchhauser, I. and Dickson, B. J. (2007). The transmembrane protein Kon-tiki couples to Dgrip to mediate myotube targeting in Drosophila. Dev. Cell 12, 751-766.
55. Schottenfeld-Roames, J. and Ghabrial, A. S. (2012). Whacked and Rab35 polarize dynein-motor-complex-dependent seamless tube growth. Nat. Cell Biol. 14, 386-393.
56. Schultz, A., Nottrott, S., Watkins, N. J. and Lührmann, R. (2006). Proteinprotein and protein-RNA contacts both contribute to the 15.5K-mediated assembly of the U4/U6 snRNP and the box C/D snoRNPs. Mol. Cell. Biol. 26, 5146-5154.
57. Small, E. M., Warkman, A. S., Wang, D. Z., Sutherland, L. B., Olson, E. N. and Krieg, P. A. (2005). Myocardin is sufficient and necessary for cardiac gene expression in Xenopus. Development 132, 987-997.
58. Steigemann, P., Molitor, A., Fellert, S., Jäckle, H. and Vorbrüggen, G. (2004). Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signaling. Curr. Biol. 14, 225-230.
59. Subramanian, A., Wayburn, B., Bunch, T. and Volk, T. (2007). Thrombospondin-mediated adhesion is essential for the formation of the myotendinous junction in Drosophila. Development 134, 1269-1278.
60. Swan, L. E., Wichmann, C., Prange, U., Schmid, A., Schmidt, M., Schwarz, T., Ponimaskin, E., Madeo, F., Vorbrüggen, G. and Sigrist, S. J. (2004). A glutamate receptor-interacting protein homolog organizes muscle guidance in Drosophila. Genes Dev. 18, 223-237.
61. Swan, L. E., Schmidt, M., Schwarz, T., Ponimaskin, E., Prange, U., Boeckers, T., Thomas, U. and Sigrist, S. J. (2006). Complex interaction of Drosophila GRIP PDZ domains and Echinoid during muscle morphogenesis. EMBO J. 25, 3640-3651.
62. Thisse, B. and Thisse, C. (2001). Fast Release Clones: A High Throughput Expression Analysis. ZFIN Direct Data Submission. http://zfin.org
63. Toledano-Katchalski, H., Nir, R., Volohonsky, G. and Volk, T. (2007). Posttranscriptional repression of the Drosophila midkine and pleiotrophin homolog miple by HOW is essential for correct mesoderm spreading. Development 134, 3473-3481.
64. Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., Salzberg, S. L., Wold, B. J. and Pachter, L. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515.
65. Venkatesh, T. V., Park, M., Ocorr, K., Nemaceck, J., Golden, K., Wemple, M. and Bodmer, R. (2000). Cardiac enhancer activity of the homeobox gene tinman depends on CREB consensus binding sites in Drosophila. Genesis 26, 55-66.
66. Vidovic, I., Nottrott, S., Hartmuth, K., Lührmann, R. and Ficner, R. (2000). Crystal structure of the spliceosomal 15.5kD protein bound to a U4 snRNA fragment. Mol. Cell 6, 1331-1342.
67. Watkins, N. J., Dickmanns, A. and Lührmann, R. (2002). Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5K protein, for the hierarchical assembly of the box C/D snoRNP. Mol. Cell. Biol. 22, 8342-8352.
68. Wayburn, B. and Volk, T. (2009). LRT, a tendon-specific leucine-rich repeat protein, promotes muscle-tendon targeting through its interaction with Robo. Development 136, 3607-3615.
69. Wei, Q., Rong, Y. and Paterson, B. M. (2007). Stereotypic founder cell patterning and embryonic muscle formation in Drosophila require nautilus (MyoD) gene function. Proc. Natl. Acad. Sci. USA 104, 5461-5466.
70. Wells, L., Edwards, K. A. and Bernstein, S. I. (1996). Myosin heavy chain isoforms regulate muscle function but not myofibril assembly. EMBO J. 15, 4454-4459.
71. Yarnitzky, T., Min, L. and Volk, T. (1998). An interplay between two EGF-receptor ligands, Vein and Spitz, is required for the formation of a subset of muscle precursors in Drosophila. Mech. Dev. 79, 73-82.
72. Zhai, R. G., Hiesinger, P. R., Koh, T. W., Verstreken, P., Schulze, K. L., Cao, Y., Jafar-Nejad, H., Norga, K. K., Pan, H., Bayat, V. et al. (2003). Mapping Drosophila mutations with molecularly defined P element insertions. Proc. Natl. Acad. Sci. USA 100, 10860-10865.
73. Zhang, S. and Bernstein, S. I. (2001). Spatially and temporally regulated expression of myosin heavy chain alternative exons during Drosophila embryogenesis. Mech. Dev. 101, 35-45.
74. Zimyanin, V. L., Belaya, K., Pecreaux, J., Gilchrist, M. J., Clark, A., Davis, I. and St Johnston, D. (2008). In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134, 843-853.