Cytoskeletal remodeling during myotube assembly and guidance: Coordinating the actin and microtubule networks

Communicative and Integrative Biology

Volumn 2, Issue 5, 2009, Pages 452-457

  Guerin, Colleen M ^a   Kramer, Sunita G ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Actin; Cytoskeleton; Microtubule; Muscle; Myotube guidance

Indexed keywords

DROSOPHILA MELANOGASTER;

EID: 77951271189     PISSN: None     EISSN: 19420889     Source Type: Journal    
DOI: 10.4161/cib.2.5.9158     Document Type: Short Survey

References (68)

1. Bate M. The embryonic development of larval muscles in Drosophila. Development 1990; 110:791-804.
2. Dohrmann C, Azpiazu N, Frasch M. A new Drosophila homeo box gene is expressed in mesodermal precursor cells of distinct muscles during embryogenesis. Genes Dev 1990; 4:2098-111.
3. Ruiz-Gomez M, Romani S, Hartmann C, Jackle H, Bate M. Specific muscle identities are regulated by Kruppel during Drosophila embryogenesis. Development 1997; 124:3407-14.
4. Bate M, Rushton E. Myogenesis and muscle patterning in Drosophila. C R Acad Sci III 1993; 316:1047-61.
5. Beckett K, Baylies MK. 3D analysis of founder cell and fusion competent myoblast arrangements outlines a new model of myoblast fusion. Dev Biol 2007; 309:113-25.
6. Ruiz-Gomez M, Coutts N, Price A, Taylor MV, Bate M. Drosophila dumbfounded: a myoblast attractant essential for fusion. Cell 2000; 102:189-98.
7. Bour BA, Chakravarti M, West JM, Abmayr SM. Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev 2000; 14:1498-511.
8. Luo L, Liao YJ, Jan LY, Jan YN. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 1994; 8:1787-802.
9. Massarwa R, Carmon S, Shilo BZ, Schejter ED. WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev Cell 2007; 12:557-69.
10. Kim S, Shilagardi K, Zhang S, Hong SN, Sens KL, Bo J, et al. A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev Cell 2007; 12:571-86.
11. Richardson BE, Beckett K, Nowak SJ, Baylies MK. SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development 2007; 134:4357-67.
12. Kesper DA, Stute C, Buttgereit D, Kreiskother N, Vishnu S, Fischbach KF, et al. Myoblast fusion in Drosophila melanogaster is mediated through a fusion-restricted myogenic-adhesive structure (FuRMAS). Dev Dyn 2007; 236:404-15.
13. Schafer G, Weber S, Holz A, Bogdan S, Schumacher S, Muller A, et al. The Wiskott-Aldrich syndrome protein (WASP) is essential for myoblast fusion in Drosophila. Dev Biol 2007; 304:664-74.
14. Richardson B, Beckett K, Baylies M. Visualizing new dimensions in Drosophila myoblast fusion. Bioessays 2008; 30:423-31.
15. Abmayr SM, Zhuang S, Geisbrecht ER. Myoblast fusion in Drosophila. Methods Mol Biol 2008; 475:75-97.
16. Peckham M. Engineering a multi-nucleated myotube, the role of the actin cytoskeleton. J Microsc 2008; 231:486-93.
17. Onel SF, Renkawitz-Pohl R. FuRMAS: triggering myoblast fusion in Drosophila. Dev Dyn 2009; 238:1513-25.
18. Volk T, VijayRaghavan K. A central role for epidermal segment border cells in the induction of muscle patterning in the Drosophila embryo. Development 1994; 120:59-70.
19. Schnorrer F, Dickson BJ. Muscle building; mechanisms of myotube guidance and attachment site selection. Dev Cell 2004; 7:9-20.
20. Becker S, Pasca G, Strumpf D, Min L, Volk T. Reciprocal signaling between Drosophila epidermal muscle attachment cells and their corresponding muscles. Development 1997; 124:2615-22.
21. Vorbruggen G, Jackle H. Epidermal muscle attachment site-specific target gene expression and interference with myotube guidance in response to ectopic stripe expression in the developing Drosophila epidermis. Proc Natl Acad Sci USA 1997; 94:8606-11.
22. Lee JC, VijayRaghavan K, Celniker SE, Tanouye MA. Identification of a Drosophila muscle development gene with structural homology to mammalian early growth response transcription factors. Proc Natl Acad Sci USA 1995; 92:10344-8.
23. Frommer G, Vorbruggen G, Pasca G, Jackle H, Volk T. Epidermal egr-like zinc finger protein of Drosophila participates in myotube guidance. EMBO J 1996; 15:1642-9.
24. Kidd T, Bland KS, Goodman CS. Slit is the midline repellent for the robo receptor in Drosophila. Cell 1999; 96:785-94.
25. Callahan CA, Bonkovsky JL, Scully AL, Thomas JB. derailed is required for muscle attachment site selection in Drosophila. Development 1996; 122:2761-7.
26. Kramer SG, Kidd T, Simpson JH, Goodman CS. Switching repulsion to attraction: changing responses to slit during transition in mesoderm migration. Science 2001; 292:737-40.
27. Bashaw GJ, Kidd T, Murray D, Pawson T, Goodman CS. Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 2000; 101:703-15.
28. Callahan CA, Muralidhar MG, Lundgren SE, Scully AL, Thomas JB. Control of neuronal pathway selection by a Drosophila receptor protein-tyrosine kinase family member. Nature 1995; 376:171-4.
29. Fan X, Labrador JP, Hing H, Bashaw GJ. Slit stimulation recruits Dock and Pak to the roundabout receptor and increases Rac activity to regulate axon repulsion at the CNS midline. Neuron 2003; 40:113-27.
30. Wong K, Ren XR, Huang YZ, Xie Y, Liu G, Saito H, et al. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 2001; 107:209-21.
31. Bonkowsky JL, Yoshikawa S, O'Keefe DD, Scully AL, Thomas JB. Axon routing across the midline controlled by the Drosophila Derailed receptor. Nature 1999; 402:540-4.
32. Estrada B, Gisselbrecht SS, Michelson AM. The transmembrane protein Perdido interacts with Grip and integrins to mediate myotube projection and attachment in the Drosophila embryo. Development 2007; 134:4469-78.
33. Schnorrer F, Kalchhauser I, Dickson BJ. The transmembrane protein Kon-tiki couples to Dgrip to mediate myotube targeting in Drosophila. Dev Cell 2007; 12:751-66.
34. Swan LE, Wichmann C, Prange U, Schmid A, Schmidt M, Schwarz T, et al. A glutamate receptor-interacting protein homolog organizes muscle guidance in Drosophila. Genes Dev 2004; 18:223-37.
35. Swan LE, Schmidt M, Schwarz T, Ponimaskin E, Prange U, Boeckers T, et al. Complex interaction of Drosophila GRIP PDZ domains and Echinoid during muscle morphogenesis. EMBO J 2006; 25:3640-51.
36. Wei SY, Escudero LM, Yu F, Chang LH, Chen LY, Ho YH, et al. Echinoid is a component of adherens junctions that cooperates with DE-Cadherin to mediate cell adhesion. Dev Cell 2005; 8:493-504.
37. Mandai K, Nakanishi H, Satoh A, Obaishi H, Wada M, Nishioka H, et al. Afadin: A novel actin filament-binding protein with one PDZ domain localized at cadherin-based cell-to-cell adherens junction. J Cell Biol 1997; 139:517-28.
38. Bahri SM, Choy JM, Manser E, Lim L, Yang X. The Drosophila homologue of Arf-GAP GIT1, dGIT, is required for proper muscle morphogenesis and guidance during embryogenesis. Dev Biol 2009; 325:15-23.
39. Zhao ZS, Manser E, Loo TH, Lim L. Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol Cell Biol 2000; 20:6354-63.
40. Miura K, Nam JM, Kojima C, Mochizuki N, Sabe H. EphA2 engages Git1 to suppress Arf6 activity modulating epithelial cell-cell contacts. Mol Biol Cell 2009; 20:1949-59.
41. Lucanic M, Cheng HJ. A RAC/CDC-42-independent GIT/PIX/PAK signaling pathway mediates cell migration in C. elegans. PLoS Genet 2008; 4:1000269.
42. Guerin CM, Kramer SG. RacGAP50C directs perinuclear {gamma}-tubulin localization to organize the uniform microtubule array required for Drosophila myotube extension. Development 2009; 136:1411-21.
43. Volk T. A new member of the spectrin superfamily may participate in the formation of embryonic muscle attachments in Drosophila. Development 1992; 116:721-30.
44. Rosenberg-Hasson Y, Renert-Pasca M, Volk T. A Drosophila dystrophin-related protein, MSP-300, is required for embryonic muscle morphogenesis. Mech Dev 1996; 60:83-94.
45. Saitoh O, Arai T, Obinata T. Distribution of microtubules and other cytoskeletal filaments during myotube elongation as revealed by fluorescence microscopy. Cell Tissue Res 1988; 252:263-73.
46. Tassin AM, Maro B, Bornens M. Fate of microtubule-organizing centers during myogenesis in vitro. J Cell Biol 1985; 100:35-46.
47. Bugnard E, Zaal KJ, Ralston E. Reorganization of microtubule nucleation during muscle differentiation. Cell Motil Cytoskel 2005; 60:1-13.
48. Cottam DM, Tucker JB, Rogers-Bald MM, Mackie JB, Macintyre J, Scarborough JA, et al. Non-centrosomal microtubule-organising centres in cold-treated cultured Drosophila cells. Cell Motil Cytoskel 2006; 63:88-100.
49. Musa H, Orton C, Morrison EE, Peckham M. Microtubule assembly in cultured myoblasts and myotubes following nocodazole induced microtubule depolymerisation. J Muscle Res Cell Motil 2003; 24:301-8.
50. Clark IE, Jan LY, Jan YN. Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 1997; 124:461-70.
51. Hirose K, Kawashima T, Iwamoto I, Nosaka T, Kitamura T. MgcRacGAP is involved in cytokinesis through associating with mitotic spindle and midbody. J Biol Chem 2001; 276:5821-8.
52. Rushton E, Drysdale R, Abmayr SM, Michelson AM, Bate M. Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 1995; 121:1979-88.
53. Machesky LM, Insall RH. Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr Biol 1998; 8:1347-56.
54. Machesky LM, Mullins RD, Higgs HN, Kaiser DA, Blanchoin L, May RC, et al. Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc Natl Acad Sci USA 1999; 96:3739-44.
55. Yu TW, Hao JC, Lim W, Tessier-Lavigne M, Bargmann CI. Shared receptors in axon guidance: SAX-3/Robo signals via UNC-34/Enabled and a Netrin-independent UNC-40/DCC function. Nat Neurosci 2002; 5:1147-54.
56. Lee C, Scherr HM, Wallingford JB. Shroom family proteins regulate gamma-tubulin distribution and microtubule architecture during epithelial cell shape change. Development 2007; 134:1431-41.
57. Hagens O, Ballabio A, Kalscheuer V, Kraehenbuhl JP, Schiaffino MV, Smith P, et al. A new standard nomenclature for proteins related to Apx and Shroom. BMC Cell Biol 2006; 7:18.
58. Castrillon DH, Wasserman SA. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 1994; 120:3367-77.
59. McCartney BM, Dierick HA, Kirkpatrick C, Moline MM, Baas A, Peifer M, et al. Drosophila APC2 is a cytoskeletally-associated protein that regulates wingless signaling in the embryonic epidermis. J Cell Biol 1999; 146:1303-18.
60. Burnette DT, Ji L, Schaefer AW, Medeiros NA, Danuser G, Forscher P. Myosin II activity facilitates microtubule bundling in the neuronal growth cone neck. Dev Cell 2008; 15:163-9.
61. Pawson C, Eaton BA, Davis GW. Formin-dependent synaptic growth: evidence that Dlar signals via Diaphanous to modulate synaptic actin and dynamic pioneer microtubules. J Neurosci 2008; 28:11111-23.
62. Somers WG, Saint R. A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. Dev Cell 2003; 4:29-39.
63. Mishima M, Kaitna S, Glotzer M. Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev Cell 2002; 2:41-54.
64. Adams RR, Tavares AA, Salzberg A, Bellen HJ, Glover DM. pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev 1998; 12:1483-94.
65. Jantsch-Plunger V, Gonczy P, Romano A, Schnabel H, Hamill D, Schnabel R, et al. CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J Cell Biol 2000; 149:1391-404.
66. Zavortink M, Contreras N, Addy T, Bejsovec A, Saint R. Tum/RacGAP50C provides a critical link between anaphase microtubules and the assembly of the contractile ring in Drosophila melanogaster. J Cell Sci 2005; 118:5381-92.
67. Gregory SL, Ebrahimi S, Milverton J, Jones WM, Bejsovec A, Saint R. Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr Biol 2008; 18:25-9.
68. D'Avino PP, Takeda T, Capalbo L, Zhang W, Lilley KS, Laue ED, et al. Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J Cell Sci 2008.