Distinct genetic programs guide Drosophila circular and longitudinal visceral myoblast fusion
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  • 作者:Anja Rudolf (3) (4)
    Detlev Buttgereit (3)
    Matthias Jacobs (3)
    Georg Wolfstetter (5) (6)
    D枚rthe Kesper (3) (7)
    Michael P眉tz (3) (8)
    Susanne Berger (3) (9)
    Renate Renkawitz-Pohl (3)
    Anne Holz (5)
    Susanne F 脰nel (3)

    3. Developmental Biology
    ; Department of Biology ; Philipps-Universit盲t Marburg ; Karl-von-Frisch-Stra脽e 8 ; Marburg ; 35043 ; Germany
    4. INSERM U1016 Institut Cochin
    ; D茅partement G茅n茅tique et D茅veloppement ; 24 Rue du Faubourg Saint Jacques ; Paris ; 75014 ; France
    5. Institut f眉r Allgemeine Zoologie und Entwicklungsbiologie
    ; Justus-Liebig-Universit盲t Gie脽en ; Stephanstra脽e 24 ; Giessen ; 35390 ; Germany
    6. Department of Molecular Biology
    ; Building 6聽L ; Ume氓 University ; Ume氓 ; 90187 ; Sweden
    7. Institute of Pathobiochemistry and Molecular Diagnostics
    ; Philipps-Universit盲t Marburg ; Hans-Meerwein-Stra脽e 2 ; Marburg ; 35043 ; Germany
    8. Institute for Neurology
    ; Clinical Neurobiology ; FB20 Philipps-Universit盲t Marburg ; Baldingerstra脽e ; Marburg ; 35043 ; Germany
    9. Life and Medical Sciences Institute
    ; Universit盲t Bonn ; Carl-Troll-Stra脽e 31 ; Bonn ; 53115 ; Germany
  • 关键词:Visceral musculature ; Actin regulation ; FuRMAS ; Myoblast fusion ; Site ; specific mRNA localization ; Differential transcriptional control ; Scar/Wave ; Blow ; Rols ; Kette/Nap ; 1
  • 刊名:BMC Cell Biology
  • 出版年:2014
  • 出版时间:December 2014
  • 年:2014
  • 卷:15
  • 期:1
  • 全文大小:4,687 KB
  • 参考文献:1. Abmayr, SM, Pavlath, GK (2012) Myoblast fusion: lessons from flies and mice. Development 139: pp. 641-656 CrossRef
    2. Maqbool, T, Jagla, K (2007) Genetic control of muscle development: learning from Drosophila. J Muscle Res Cell Motil 28: pp. 397-407 CrossRef
    3. Campos-Ortega, JA, Hartenstein, V (1985) The embryonic development of Drosophila melanogaster. Springer-Verlag, Berlin CrossRef
    4. Kusch, T, Reuter, R (1999) Functions for Drosophila brachyenteron and forkhead in mesoderm specification and cell signalling. Development 126: pp. 3991-4003
    5. Goldstein, MA, Burdette, WJ (1971) Striated visceral muscle of drosophila melanogaster. J Morphol 134: pp. 315-334 CrossRef
    6. Klapper, R (2000) The longitudinal visceral musculature of Drosophila melanogaster persists through metamorphosis. Mech Dev 95: pp. 47-54 CrossRef
    7. Klapper, R, Heuser, S, Strasser, T, Janning, W (2001) A new approach reveals syncytia within the visceral musculature of Drosophila melanogaster. Development 128: pp. 2517-2524
    8. San Martin, B, Ruiz-G贸mez, M, Landgraf, M, Bate, M (2001) A distinct set of founders and fusion-competent myoblasts make visceral muscles in the Drosophila embryo. Development 128: pp. 3331-3338
    9. Sandborn, EB, Duclos, S, Messier, PE, Roberge, JJ (1967) Atypical intestinal striated muscle in Drosophila melanogaster. J Ultrastruct Res 18: pp. 695-702 CrossRef
    10. Schr枚ter, RH, Buttgereit, D, Beck, L, Holz, A, Renkawitz-Pohl, R (2006) Blown fuse regulates stretching and outgrowth but not myoblast fusion of the circular visceral muscles in Drosophila. Differentiation 74: pp. 608-621 CrossRef
    11. Klapper, R, Stute, C, Schomaker, O, Strasser, T, Janning, W, Renkawitz-Pohl, R, Holz, A (2002) The formation of syncytia within the visceral musculature of the Drosophila midgut is dependent on duf, sns and mbc. Mech Dev 110: pp. 85-96 CrossRef
    12. Azpiazu, N, Frasch, M (1993) tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev 7: pp. 1325-1340 CrossRef
    13. Tremml, G, Bienz, M (1989) Homeotic gene expression in the visceral mesoderm of Drosophila embryos. EMBO J 8: pp. 2677-2685
    14. Zaffran, S, K眉chler, A, Lee, HH, Frasch, M (2001) biniou (FoxF), a central component in a regulatory network controlling visceral mesoderm development and midgut morphogenesis in Drosophila. Genes Dev 15: pp. 2900-2915
    15. Englund, C, Lor茅n, CE, Grabbe, C, Varshney, GK, Deleuil, F, Hallberg, B, Palmer, RH (2003) Jeb signals through the Alk receptor tyrosine kinase to drive visceral muscle fusion. Nature 425: pp. 512-516 CrossRef
    16. Lee, HH, Norris, A, Weiss, JB, Frasch, M (2003) Jelly belly protein activates the receptor tyrosine kinase Alk to specify visceral muscle pioneers. Nature 425: pp. 507-512 CrossRef
    17. Lor茅n, CE, Englund, C, Grabbe, C, Hallberg, B, Hunter, T, Palmer, RH (2003) A crucial role for the Anaplastic lymphoma kinase receptor tyrosine kinase in gut development in Drosophila melanogaster. EMBO Rep 4: pp. 781-786 CrossRef
    18. Popichenko, D, Hugosson, F, Sj枚gren, C, Dogru, M, Yamazaki, Y, Wolfstetter, G, Sch枚nherr, C, Fallah, M, Hallberg, B, Nguyen, H, Palmer, RH (2013) Jeb/Alk signalling regulates the Lame duck GLI family transcription factor in the Drosophila visceral mesoderm. Development 140: pp. 3156-3166 CrossRef
    19. Stute, C, Schimmelpfeng, K, Renkawitz-Pohl, R, Palmer, R, Holz, A (2004) Myoblast determination in the somatic and visceral mesoderm depends on Notch signalling as well as on milliways(mili(Alk)) as receptor for Jeb signalling. Development 131: pp. 743-754 CrossRef
    20. Georgias, C, Wasser, M, Hinz, U (1997) A basic-helix-loop-helix protein expressed in precursors of Drosophila longitudinal visceral muscles. Mech Dev 69: pp. 115-124 CrossRef
    21. Ismat, A, Schaub, C, Reim, I, Kirchner, K, Schultheis, D, Frasch, M (2010) HLH54F is required for the specification and migration of longitudinal gut muscle founders from the caudal mesoderm of Drosophila. Development 137: pp. 3107-3117 CrossRef
    22. Kadam, S, Ghosh, S, Stathopoulos, A (2012) Synchronous and symmetric migration of Drosophila caudal visceral mesoderm cells requires dual input by two FGF ligands. Development 139: pp. 699-708 CrossRef
    23. Mandal, L, Dumstrei, K, Hartenstein, V (2004) Role of FGFR signaling in the morphogenesis of the Drosophila visceral musculature. Dev Dyn 231: pp. 342-348 CrossRef
    24. Reim, I, Hollfelder, D, Ismat, A, Frasch, M (2012) The FGF8-related signals Pyramus and Thisbe promote pathfinding, substrate adhesion, and survival of migrating longitudinal gut muscle founder cells. Dev Biol 368: pp. 28-43 CrossRef
    25. Bour, BA, Chakravarti, M, West, JM, Abmayr, SM (2000) Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev 14: pp. 1498-1511
    26. Ruiz-G贸mez, M, Coutts, N, Price, A, Taylor, MV, Bate, M (2000) Drosophila dumbfounded: a myoblast attractant essential for fusion. Cell 102: pp. 189-198 CrossRef
    27. Str眉nkelnberg, M, Bonengel, B, Moda, LM, Hertenstein, A, de Couet, HG, Ramos, RG, Fischbach, KF (2001) rst and its paralogue kirre act redundantly during embryonic muscle development in Drosophila. Development 128: pp. 4229-4239
    28. Kreisk枚ther, N, Reichert, N, Buttgereit, D, Hertenstein, A, Fischbach, K, Renkawitz-Pohl, R (2006) Drosophila rolling pebbles colocalises and putatively interacts with alpha-Actinin and the Sls isoform Zormin in the Z-discs of the sarcomere and with Dumbfounded/Kirre, alpha-Actinin and Zormin in the terminal Z-discs. J Muscle Res Cell Motil 27: pp. 93-106 CrossRef
    29. 脰nel, S-F, Dottermusch, C, Sickmann, A, Buttgereit, D, Renkawitz-Pohl, R Role of the actin cytoskeleton within FuRMAS during Drosophila myoblast fusion and first functionally conserved factors in vertebrates. In: Larsson, I eds. (2011) Cell Fusions: Regulation and Control. Springer, Heidelberg, Berlin, pp. 137-170
    30. Sens, KL, Zhang, S, Jin, P, Duan, R, Zhang, G, Luo, F, Parachini, L, Chen, EH (2010) An invasive podosome-like structure promotes fusion pore formation during myoblast fusion. J Cell Biol 191: pp. 1013-1027 CrossRef
    31. Jin, P, Duan, R, Luo, F, Zhang, G, Hong, SN, Chen, EH (2011) Competition between Blown fuse and WASP for WIP binding regulates the dynamics of WASP-dependent actin polymerization in vivo. Dev Cell 20: pp. 623-638 CrossRef
    32. Kesper, D, Stute, C, Buttgereit, D, Kreisk枚ther, N, Vishnu, S, Fischbach, K, Renkawitz-Pohl, R (2007) Myoblast fusion in Drosophila melanogaster is mediated through a fusion-restricted myogenic-adhesive structure (FuRMAS). Dev Dyn 236: pp. 404-415 CrossRef
    33. Sch盲fer, G, Weber, S, Holz, A, Bogdan, S, Schumacher, S, M眉ller, A, Renkawitz-Pohl, R, Onel, S (2007) The Wiskott-Aldrich syndrome protein (WASP) is essential for myoblast fusion in Drosophila. Dev Biol 304: pp. 664-674 CrossRef
    34. Schr枚ter, R, Lier, S, Holz, A, Bogdan, S, Kl盲mbt, C, Beck, L, Renkawitz-Pohl, R (2004) kette and blown fuse interact genetically during the second fusion step of myogenesis in Drosophila. Development 131: pp. 4501-4509 CrossRef
    35. Richardson, BE, Beckett, K, Nowak, SJ, Baylies, MK (2007) SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development 134: pp. 4357-4367 CrossRef
    36. Berger, S, Sch盲fer, G, Kesper, D, Holz, A, Eriksson, T, Palmer, R, Beck, L, Kl盲mbt, C, Renkawitz-Pohl, R, Onel, S (2008) WASP and SCAR have distinct roles in activating the Arp2/3 complex during myoblast fusion. J Cell Sci 121: pp. 1303-1313 CrossRef
    37. Gildor, B, Massarwa, R, Shilo, BZ, Schejter, ED (2009) The SCAR and WASp nucleation-promoting factors act sequentially to mediate Drosophila myoblast fusion. EMBO Rep 10: pp. 1043-1050 CrossRef
    38. Eriksson, T, Varshney, G, Aspenstrom, P, Palmer, RH (2010) Characterisation of the role of Vrp1 in cell fusion during the development of visceral muscle of Drosophila melanogaster. BMC Dev Biol 10: pp. 86 CrossRef
    39. Bonn, BR, Rudolf, A, Hornbruch-Freitag, C, Daum, G, Kuckwa, J, Kastl, L, Buttgereit, D, Renkawitz-Pohl, R (2013) Myosin heavy chain-like localizes at cell contact sites during Drosophila myoblast fusion and interacts in vitro with Rolling pebbles 7. Exp Cell Res 319: pp. 402-416 CrossRef
    40. Chen, EH, Olson, EN (2001) Antisocial, an intracellular adaptor protein, is required for myoblast fusion in Drosophila. Dev Cell 1: pp. 705-715 CrossRef
    41. Menon, SD, Chia, W (2001) Drosophila rolling pebbles: a multidomain protein required for myoblast fusion that recruits D-Titin in response to the myoblast attractant Dumbfounded. Dev Cell 1: pp. 691-703 CrossRef
    42. 脰nel, S, Renkawitz-Pohl, R (2009) FuRMAS: triggering myoblast fusion in Drosophila. Dev Dyn 238: pp. 1513-1525 CrossRef
    43. Rau, A, Buttgereit, D, Holz, A, Fetter, R, Doberstein, SK, Paululat, A, Staudt, N, Skeath, J, Michelson, AM, Renkawitz-Pohl, R (2001) rolling pebbles (rols) is required in Drosophila muscle precursors for recruitment of myoblasts for fusion. Development 128: pp. 5061-5073
    44. Doberstein, SK, Fetter, RD, Mehta, AY, Goodman, CS (1997) Genetic analysis of myoblast fusion: blown fuse is required for progression beyond the prefusion complex. J Cell Biol 136: pp. 1249-1261 CrossRef
    45. Hummel, T, Leifker, K, Kl盲mbt, C (2000) The Drosophila HEM-2/NAP1 homolog KETTE controls axonal pathfinding and cytoskeletal organization. Genes Dev 14: pp. 863-873
    46. Nose, A, Isshiki, T, Takeichi, M (1998) Regional specification of muscle progenitors in Drosophila: the role of the msh homeobox gene. Development 125: pp. 215-223
    47. Haralalka, S, Shelton, C, Cartwright, HN, Katzfey, E, Janzen, E, Abmayr, SM (2011) Asymmetric Mbc, active Rac1 and F-actin foci in the fusion-competent myoblasts during myoblast fusion in Drosophila. Development 138: pp. 1551-1562 CrossRef
    48. Morin, X, Daneman, R, Zavortink, M, Chia, W (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci U S A 98: pp. 15050-15055 CrossRef
    49. Susic-Jung, L, Hornbruch-Freitag, C, Kuckwa, J, Rexer, KH, Lammel, U, Renkawitz-Pohl, R (2012) Multinucleated smooth muscles and mononucleated as well as multinucleated striated muscles develop during establishment of the male reproductive organs of Drosophila melanogaster. Dev Biol 370: pp. 86-97 CrossRef
    50. Massarwa, R, Carmon, S, Shilo, BZ, Schejter, ED (2007) WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev Cell 12: pp. 557-569 CrossRef
    51. Patel, NH, Snow, PM, Goodman, CS (1987) Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 48: pp. 975-988 CrossRef
    52. Leiss, D, Hinz, U, Gasch, A, Mertz, R, Renkawitz-Pohl, R (1988) Beta 3 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis. Development 104: pp. 525-531
    53. Nguyen, HT, Bodmer, R, Abmayr, SM, McDermott, JC, Spoerel, NA (1994) D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryogenesis. Proc Natl Acad Sci U S A 91: pp. 7520-7524 CrossRef
    54. L茅cuyer, E, Parthasarathy, N, Krause, HM (2008) Fluorescent in situ hybridization protocols in Drosophila embryos and tissues. Methods Mol Biol 420: pp. 289-302 CrossRef
    55. Michiels, F, Gasch, A, Kaltschmidt, B, Renkawitz-Pohl, R, Michiels, F, Gasch, A, Kaltschmidt, B, Renkawitz-Pohl, R (1989) A 14 bp promotor element directs the testis specificity of the Drosophila beta 2 tubulin. Gene. EMBO J 8: pp. 1559-1565
    56. Thummel, CS, Boulet, AM, Lipshitz, HD (1988) Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene 74: pp. 445-456 CrossRef
    57. Kulke, M, Neagoe, C, Kolmerer, B, Minajeva, A, Hinssen, H, Bullard, B, Linke, WA (2001) Kettin, a major source of myofibrillar stiffness in Drosophila indirect flight muscle. J Cell Biol 154: pp. 1045-1057 CrossRef
    58. Lakey, A, Labeit, S, Gautel, M, Ferguson, C, Barlow, DP, Leonard, K, Bullard, B (1993) Kettin, a large modular protein in the Z-disc of insect muscles. EMBO J 12: pp. 2863-2871
    59. van Straaten, M, Goulding, D, Kolmerer, B, Labeit, S, Clayton, J, Leonard, K, Bullard, B (1999) Association of kettin with actin in the Z-disc of insect flight muscle. J Mol Biol 285: pp. 1549-1562 CrossRef
    60. Friedrich, MV, Schneider, M, Timpl, R, Baumgartner, S (2000) Perlecan domain V of Drosophila melanogaster. Sequence, recombinant analysis and tissue expression. Eur J Biochem 267: pp. 3149-3159 CrossRef
    61. Urbano, JM, Dom铆nguez-Gim茅nez, P, Estrada, B, Mart铆n-Bermudo, MD (2011) PS integrins and laminins: key regulators of cell migration during Drosophila embryogenesis. PLoS One 6: pp. e23893 CrossRef
    62. Wolfstetter, G, Holz, A (2011) The role of LamininB2 (LanB2) during mesoderm differentiation in Drosophila. Cell Mol Life Sci 69: pp. 267-282 CrossRef
    63. Duan, H, Skeath, JB, Nguyen, HT (2001) Drosophila Lame duck, a novel member of the Gli superfamily, acts as a key regulator of myogenesis by controlling fusion-competent myoblast development. Development 128: pp. 4489-4500
    64. Ismail, AM, Padrick, SB, Chen, B, Umetani, J, Rosen, MK (2009) The WAVE regulatory complex is inhibited. Nat Struct Mol Biol 16: pp. 561-563 CrossRef
    65. Zallen, JA, Cohen, Y, Hudson, AM, Cooley, L, Wieschaus, E, Schejter, ED (2002) SCAR is a primary regulator of Arp2/3-dependent morphological event in Drosophila. J Cell Biol 156: pp. 689-701 CrossRef
    66. Erickson, MR, Galletta, BJ, Abmayr, SM (1997) Drosophila myoblast city encodes a conserved protein that is essential for myoblast fusion, dorsal closure, and cytoskeletal organization. J Cell Biol 138: pp. 589-603 CrossRef
    67. Rushton, E, Drysdale, R, Abmayr, SM, Michelson, AM, Bate, M (1995) Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 121: pp. 1979-1988
    68. Menon, SD, Osman, Z, Chenchill, K, Chia, W (2005) A positive feedback loop between Dumbfounded and Rolling pebbles leads to myotube enlargement in Drosophila. J Cell Biol 169: pp. 909-920 CrossRef
    69. Kim, S, Shilagardi, K, Zhang, S, Hong, SN, Sens, KL, Bo, J, Gonzalez, GA, Chen, EH (2007) A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev Cell 12: pp. 571-586 CrossRef
    70. Dettman, RW, Turner, FR, Raff, EC (1996) Genetic analysis of the Drosophila beta3-tubulin gene demonstrates that the microtubule cytoskeleton in the cells of the visceral mesoderm is required for morphogenesis of the midgut endoderm. Dev Biol 177: pp. 117-135 CrossRef
    71. P眉tz, M, Kesper, D, Buttgereit, D, Renkawitz-Pohl, R (2005) In Drosophila melanogaster, the rolling pebbles isoform 6 (Rols6) is essential for proper Malpighian tubule morphology. Mech Dev 122: pp. 1206-1217 CrossRef
  • 刊物主题:Cell Biology; Biological Microscopy; Life Sciences, general;
  • 出版者:BioMed Central
  • ISSN:1471-2121
文摘
Background The visceral musculature of Drosophila larvae comprises circular visceral muscles tightly interwoven with longitudinal visceral muscles. During myogenesis, the circular muscles arise by one-to-one fusion of a circular visceral founder cell (FC) with a visceral fusion-competent myoblast (FCM) from the trunk visceral mesoderm, and longitudinal muscles arise from FCs of the caudal visceral mesoderm. Longitudinal FCs migrate anteriorly under guidance of fibroblast growth factors during embryogenesis; it is proposed that they fuse with FCMs from the trunk visceral mesoderm to give rise to syncytia containing up to six nuclei. Results Using fluorescence in situ hybridization and immunochemical analyses, we investigated whether these fusion events during migration use the same molecular repertoire and cellular components as fusion-restricted myogenic adhesive structure (FuRMAS), the adhesive signaling center that mediates myoblast fusion in the somatic mesoderm. Longitudinal muscles were formed by the fusion of one FC with Sns-positive FCMs, and defects in FCM specification led to defects in longitudinal muscle formation. At the fusion sites, Duf/Kirre and the adaptor protein Rols7 accumulated in longitudinal FCs, and Blow and F-actin accumulated in FCMs. The accumulation of these four proteins at the fusion sites argues for FuRMAS-like adhesion and signaling centers. Longitudinal fusion was disturbed in rols and blow single, and scar wip double mutants. Mutants of wasp or its interaction partner wip had no defects in longitudinal fusion. Conclusions Our results indicated that all embryonic fusion events depend on the same cell-adhesion molecules, but that the need for Rols7 and regulators of F-actin distinctly differs. Rols7 was required for longitudinal visceral and somatic myoblast fusion but not for circular visceral fusion. Importantly, longitudinal fusion depended on Kette and SCAR/Wave but was independent of WASp-dependent Arp2/3 activation. Thus, the complexity of the players involved in muscle formation increases from binucleated circular muscles to longitudinal visceral muscles to somatic muscles.

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