Antagonistic function of Lmd and Zfh1 fine tunes cell fate decisions in the Twi and Tin positive mesoderm of Drosophila melanogaster

Developmental Biology

Volumn 326, Issue 2, 2009, Pages 444-455

  Sellin, Julia ^a   Drechsler, Maik ^a   Nguyen, Hanh T ^b,c   Paululat, Achim ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Cardiogenesis; Dorsal vessel; Dpp; Heart; Mesoderm; Myogenesis; Notch; Odd skipped; Pericardial cells; Somatic musculature

Indexed keywords

DECAPENTAPLEGIC PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LAME DUCK; TRANSCRIPTION FACTOR ODD SKIPPED; TRANSCRIPTION FACTOR TINMAN; TRANSCRIPTION FACTOR TWI; UNCLASSIFIED DRUG; ZINC FINGER HOMEODOMAIN FACTOR;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL FATE; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; GENE MUTATION; HYPERPLASIA; INSECT DEVELOPMENT; MESODERM; MUSCLE CELL; MUSCLE DEVELOPMENT; MUTATION; MYOBLAST; NONHUMAN; PERICARDIAL DISEASE; PERICARDIUM; PHENOTYPE; PRIORITY JOURNAL; STEM CELL;

DROSOPHILA MELANOGASTER;

EID: 58649118425     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.10.041     Document Type: Article

References (79)

1. Abrams J.M., White K., Fessler L.I., and Steller H. Programmed cell death during Drosophila embryogenesis. Development 117 (1993) 29-43
2. Albrecht S., Wang S., Holz A., Bergter A., and Paululat A. The ADAM metalloprotease Kuzbanian is crucial for proper heart formation in Drosophila melanogaster. Mech Dev 123 (2006) 372-387
3. Alvarez A.D., Shi W., Wilson B.A., and Skeath J.B. Pannier and PointedP2 act sequentially to regulate Drosophila heart development. Development 130 (2003) 3015-3026
4. Baker N.E. Notch signaling in the nervous system. Pieces still missing from the puzzle. BioEssays 22 (2000) 264-273
5. Baker R., and Schubiger G. Autonomous and nonautonomous Notch functions for embryonic muscle and epidermis development in Drosophila. Development 122 (1996) 617-626
6. Bate M., Rushton E., and Currie D.A. Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 113 (1991) 79-89
7. Baylies M.K., and Bate M. twist: a myogenic switch in Drosophila. Science 272 (1996) 1481-1484
8. Bodmer R. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118 (1993) 719-729
9. Borkowski O.M., Brown N.H., and Bate M. Anterior-posterior subdivision and the diversification of the mesoderm in Drosophila. Development 121 (1995) 4183-4193
10. Brand A.H., and Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 (1993) 401-415
11. Broadie K.S., and Bate M. The development of adult muscles in Drosophila: ablation of identified muscle precursor cells. Development 113 (1991) 103-118
12. Broihier H.T., Moore L.A., Van Doren M., Newman S., and Lehmann R. Zfh-1 is required for germ cell migration and gonadal mesoderm development in Drosophila. Development 125 (1998) 655-666
13. Carmena A., Murugasu-Oei B., Menon D., Jimenez F., and Chia W. Inscuteable and Numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev. 12 (1998) 304-315
14. Chartier A., Zaffran S., Astier M., Sémériva M., and Gratecos D. Pericardin, a Drosophila type IV collagen-like protein is involved in the morphogenesis and maintenance of the heart epithelium during dorsal ectoderm closure. Development 129 (2002) 3241-3253
15. Conboy I.M., Conboy M.J., Smythe G.M., and Rando T.A. Notch-mediated restoration of regenerative potential to aged muscle. Science 302 (2003) 1575-1577
16. Corbin V., Michelson A.M., Abmayr S.M., Neel V., Alcamo E., Maniatis T., and Young M.W. A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67 (1991) 311-323
17. Cripps R.M., and Olson E.N. Control of cardiac development by an evolutionarily conserved transcriptional network. Dev. Biol. 246 (2002) 14-28
18. Das D., Aradhya R., Ashoka D., and Inamdar M. Post-embryonic pericardial cells of Drosophila are required for overcoming toxic stress but not for cardiac function or adult development. Cell Tissue Res. 331 2 (2008) 565-570
19. Duan H., and Nguyen H.T. Distinct posttranscriptional mechanisms regulate the activity of the Zn finger transcription factor Lame duck during Drosophila myogenesis. Mol. Cell. Biol. 26 (2006) 1414-1423
20. Duan H., Skeath J.B., and Nguyen H.T. 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 (2001) 4489-4500
21. Dutta D., Anant S., Ruiz-Gomez M., Bate M., and VijayRaghavan K. Founder myoblasts and fibre number during adult myogenesis in Drosophila. Development 131 (2004) 3761-3772
22. Dutta D., Shaw S., Maqbool T., Pandya H., and Vijayraghavan K. Drosophila Heartless acts with Heartbroken/Dof in muscle founder differentiation. PLoS Biol. 3 (2005) e337
23. Estrada B., Choe S.E., Gisselbrecht S.S., Michaud S., Raj L., Busser B.W., Halfon M.S., Church G.M., and Michelson A.M. An integrated strategy for analyzing the unique developmental programs of different myoblast subtypes. PLoS Genet. 2 (2006) e16
24. Figeac N., Daczewska M., Marcelle C., and Jagla K. Muscle stem cells and model systems for their investigation. Dev. Dyn. 236 (2007) 3332-3342
25. Frasch M. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374 (1995) 464-467
26. Fryer C.J., White J.B., and Jones K.A. Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol. Cell 16 (2004) 509-520
27. Fuerstenberg S., and Giniger E. Multiple roles for Notch in Drosophila myogenesis. Dev. Biol. 201 (1998) 66-77
28. Fujioka M., Wessells R.J., Han Z., Liu J., Fitzgerald K., Yusibova G.L., Zamora M., Ruiz-Lozano P., Bodmer R., and Jaynes J.B. Embryonic even skipped dependent muscle and heart cell fates are required for normal adult activity, heart function, and lifespan. Circ. Res. 97 (2005) 1108-1114
29. Furlong E.E., Andersen E.C., Null B., White K.P., and Scott M.P. Patterns of gene expression during Drosophila mesoderm development. Science 293 (2001) 1629-1633
30. Giebel B. The Notch signaling pathway is required to specify muscle progenitor cells in Drosophila. Mech. Dev. 86 (1999) 137-145
31. Glise B., and Noselli S. Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev. 11 (1997) 1738-1747
32. Han Z., and Bodmer R. Myogenic cells fates are antagonized by Notch only in asymmetric lineages of the Drosophila heart, with or without cell division. Development 130 (2003) 3039-3051
33. Han Z., Fujioka M., Su M., Liu M., Jaynes J.B., and Bodmer R. Transcriptional integration of competence modulated by mutual repression generates cell-type specificity within the cardiogenic mesoderm. Dev. Biol. 252 (2002) 225-240
34. Hartenstein A.Y., Rugendorff A., Tepass U., and Hartenstein V. The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116 (1992) 1203-1220
35. Hummel T., Schimmelpfeng K., and Klämbt C. Commissure formation in the embryonic CNS of Drosophila. Dev. Biol. 209 (1999) 381-398
36. Irvine K.D., and Rauskolb C. Boundaries in development: formation and function. Annu. Rev. Cell Dev. Biol. 17 (2001) 189-214
37. Jagla K., Frasch M., Jagla T., Dretzen G., Bellard F., and Bellard M. ladybird, a new component of the cardiogenic pathway in Drosophila required for diversification of heart precursors. Development 124 (1997) 3471-3479
38. Jagla T., Bellard F., Lutz Y., Dretzen G., Bellard M., and Jagla K. ladybird determines cell fate decisions during diversification of Drosophila somatic muscles. Development 125 (1998) 3699-3708
39. Johnson A.N., Bergman C.M., Kreitman M., and Newfeld S.J. Embryonic enhancers in the dpp disk region regulate a second round of Dpp signaling from the dorsal ectoderm to the mesoderm that represses Zfh-1 expression in a subset of pericardial cells. Dev. Biol. 262 (2003) 137-151
40. Johnson A.N., Burnett L.A., Sellin J., Paululat A., and Newfeld S.J. Defective Decapentaplegic signaling results in heart overgrowth and reduced cardiac output in Drosophila. Genetics 176 (2007) 1609-1624
41. Kiefer J.C., Jarman A., and Johnson J. Pro-neural factors and neurogenesis. Dev. Dyn. 234 (2005) 808-813
42. Kosman D., Small S., and Reinitz J. Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev. Genes Evol. 208 (1998) 290-294
43. Kraut R., Chia W., Jan L.Y., Jan Y.N., and Knoblich J.A. Role of Inscuteable in orienting asymmetric cell divisions in Drosophila. Nature 383 (1996) 50-55
44. Lai Z.C., Fortini M.E., and Rubin G.M. The embryonic expression patterns of zfh-1 and zfh-2, two Drosophila genes encoding novel zinc-finger homeodomain proteins. Mech. Dev. 34 (1991) 123-134
45. Lai Z.C., Rushton E., Bate M., and Rubin G.M. Loss of function of the Drosophila zfh-1 gene results in abnormal development of mesodermally derived tissues. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 4122-4126
46. Leiss D., Hinz U., Gasch A., Mertz R., and Renkawitz-Pohl R. Beta 3 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis. Development 104 (1988) 525-531
47. Lieber T., Kidd S., and Young M.W. Kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev. 16 (2002) 209-221
48. Liotta D., Han J., Elgar S., Garvey C., Han Z., and Taylor M.V. The him gene reveals a balance of inputs controlling muscle differentiation in Drosophila. Curr. Biol. 17 (2007) 1409-1413
49. Liu M., Su M., Lyons G.E., and Bodmer R. Functional conservation of zinc-finger homeodomain gene zfh1/SIP1 in Drosophila heart development. Dev. Genes Evol. 216 (2006) 683-693
50. Lockwood W.K., and Bodmer R. The patterns of Wingless, Decapentaplegic, and Tinman position the Drosophila heart. Mech. Dev. 114 (2002) 13-26
51. Mandal L., Banerjee U., and Hartenstein V. Evidence for a fruit fly hemangioblast and similarities between lymph-gland hematopoiesis in fruit fly and mammal aorta-gonadal-mesonephros mesoderm. Nat. Gene 36 9 (2004) 1019-1023
52. Nose A., Isshiki T., and Takeichi M. Regional specification of muscle progenitors in Drosophila: the role of the msh homeobox gene. Development 125 (1998) 215-223
53. Pan D., and Rubin G.M. Kuzbanian controls proteolytic processing of Notch and mediates lateral inhibition during Drosophila and vertebrate neurogenesis. Cell 90 (1997) 271-280
54. Park M., Yaich L.E., and Bodmer R. Mesodermal cell fate decisions in Drosophila are under the control of the lineage genes numb, Notch, and sanpodo. Mech. Dev. 75 (1998) 117-126
55. Petcherski A.G., and Kimble J. Mastermind is a putative activator for Notch. Curr. Biol. 10 (2000) R471-473
56. Popichenko D., and Paululat A. Cell fate decisions in the Drosophila dorsal vessel depend on the multiadapter protein Inscuteable. Genesis 40 (2004) 218-222
57. Postigo A.A., and Dean D.C. ZEB, a vertebrate homolog of Drosophila Zfh-1, is a negative regulator of muscle differentiation. Embo J. 16 (1997) 3935-3943
58. Postigo A.A., Ward E., Skeath J.B., and Dean D.C. zfh-1, the Drosophila homologue of ZEB, is a transcriptional repressor that regulates somatic myogenesis. Mol. Cell. Biol. 19 (1999) 7255-7263
59. Postigo A.A., Depp J.L., Taylor J.J., and Kroll K.L. Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins. Embo J. 22 (2003) 2453-2462
60. Riechmann V., Irion U., Wilson R., Grosskortenhaus R., and Leptin M. Control of cell fates and segmentation in the Drosophila mesoderm. Development 124 (1997) 2915-2922
61. Rooke J., Pan D., Xu T., and Rubin G.M. KUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis. Science 273 (1996) 1227-1231
62. Ruiz-Gómez M., and Bate M. Segregation of myogenic lineages in Drosophila requires Numb. Development 124 (1997) 4857-4866
63. Ruiz-Gómez M., Coutts N., Suster M.L., Landgraf M., and Bate M. myoblasts incompetent encodes a zinc finger transcription factor required to specify fusion-competent myoblasts in Drosophila. Development 129 (2002) 133-141
64. Rusconi J.C., and Corbin V. Evidence for a novel Notch pathway required for muscle precursor selection in Drosophila. Mech. Dev. 79 (1998) 39-50
65. Ryan K.M., Hoshizaki D.K., and Cripps R.M. Homeotic selector genes control the patterning of seven-up expressing cells in the Drosophila dorsal vessel. Mech. Dev. 122 (2005) 1023-1033
66. Sellin J., Albrecht S., Kölsch V., and Paululat A. Dynamics of heart differentiation, visualized utilizing heart enhancer elements of the Drosophila melanogaster bHLH transcription factor Hand. Gene Expr. Patterns 6 (2006) 360-375
67. St Johnston R.D., Hoffmann F.M., Blackman R.K., Segal D., Grimaila R., Padgett R.W., Irick H.A., and Gelbart W.M. Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev. 4 (1990) 1114-1127
68. Su M.T., Fujioka M., Goto T., and Bodmer R. The Drosophila homeobox genes zfh-1 and even-skipped are required for cardiac-specific differentiation of a Numb-dependent lineage decision. Development 126 (1999) 3241-3251
69. Tio M., Zavortink M., Yang X., and Chia W. A functional analysis of inscuteable and its roles during Drosophila asymmetric cell divisions. J. Cell. Sci. 112 Pt 10 (1999) 1541-1551
70. Tögel M., Pass G., and Paululat A. The Drosophila wing hearts originate from pericardial cells and are essential for wing maturation. Dev. Biol. 318 (2008) 29-37
71. Ward E.J., and Coulter D.E. odd-skipped is expressed in multiple tissues during Drosophila embryogenesis. Mech. Dev. 96 (2000) 233-236
72. Ward E.J., and Skeath J.B. Characterization of a novel subset of cardiac cells and their progenitors in the Drosophila embryo. Development 127 (2000) 4959-4969
73. Weavers H., Prieto-Sánchez S., Grawe F., Garcia-López A., Artero R., Wilsch-Bräuninger M., Ruiz-Gómez M., Skaer H., and Denholm B. The insect nephrocyte is a podocyte-like cell with a filtration slit diaphragm. Nature (2008) 10.1038/nature07526 (Epub ahead of print).
74. Wiersdorff V., Lecuit T., Cohen S.M., and Mlodzik M. Mad acts downstream of Dpp receptors, revealing a differential requirement for Dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development 122 (1996) 2153-2162
75. Xu X., Yin Z., Hudson J.B., Ferguson E.L., and Frasch M. Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev. 12 (1998) 2354-2370
76. Yedvobnick B., Kumar A., Chaudhury P., Opraseuth J., Mortimer N., and Bhat K.M. Differential effects of Drosophila mastermind on asymmetric cell fate specification and neuroblast formation. Genetics 166 (2004) 1281-1289
77. Yin Z., and Frasch M. Regulation and function of tinman during dorsal mesoderm induction and heart specification in Drosophila. Dev. Genet. 22 (1998) 187-200
78. Yin Z., Xu X.L., and Frasch M. Regulation of the Twist target gene tinman by modular cis-regulatory elements during early mesoderm development. Development 124 (1997) 4971-4982
79. Zaffran S., and Frasch M. Early signals in cardiac development. Circ. Res. 91 (2002) 457-469