Reduced cell number in the hindgut epithelium disrupts hindgut left-right asymmetry in a mutant of pebble, encoding a RhoGEF, in Drosophila embryos

Mechanisms of Development

Volumn 130, Issue 2-3, 2013, Pages 169-180

  Nakamura, Mitsutoshi ^a,b   Matsumoto, Kenjiroo ^a,b   Iwamoto, Yuta ^a,b   Muguruma, Takeshi ^a   Nakazawa, Naotaka ^a,b   Hatori, Ryo ^a,b   Taniguchi, Kiichiro ^a   Maeda, Reo ^a   Matsuno, Kenji ^b  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Drosophila; Gut development; Left right asymmetry; Pebble; RhoGEF

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL POLARITY; CELL SIZE; CONTROLLED STUDY; CYTOKINESIS; DEVELOPMENTAL STAGE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE; GENE EXPRESSION; GENE FREQUENCY; GENE MUTATION; GENETIC SCREENING; HETEROZYGOSITY; HOMOZYGOSITY; INTESTINE DEVELOPMENT; INTESTINE EPITHELIUM; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; ORGANOGENESIS; PBL GENE; PRIORITY JOURNAL;

ALLELES; ANIMALS; BODY PATTERNING; CELL COUNT; CELL POLARITY; CYTOKINESIS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIAL CELLS; EPITHELIUM; GASTROINTESTINAL TRACT; GENE DELETION; GENE EXPRESSION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HOMOZYGOTE; ORGAN SPECIFICITY; POINT MUTATION; RNA SPLICE SITES; SEQUENCE ANALYSIS, DNA;

ANIMALIA; INVERTEBRATA; MAMMALIA; VERTEBRATA;

EID: 84873524169     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2012.09.007     Document Type: Article

References (56)

1. Adám G., Perrimon N., Noselli S. The retinoic-like juvenile hormone controls the looping of left-right asymmetric organs in Drosophila. Development 2003, 130:2397-2406.
2. Adams D., Robinson K., Fukumoto T., Yuan S., Albertson R., Yelick P., Kuo L., McSweeney M., Levin M. Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 2006, 133:1657-1671.
3. Asami T., Gittenberger E., Falkner G. Whole-body enantiomorphy and maternal inheritance of chiral reversal in the pond snail Lymnaea stagnalis. J. Hered. 2008, 99:552-557.
4. Ashburner M. Drosophila 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
5. Baum B. Left-right asymmetry: actin-myosin through the looking glass. Curr. Biol. 2006, 16:R502-R504.
6. Bergmann D., Lee M., Robertson B., Tsou M., Rose L., Wood W. Embryonic handedness choice in C. elegans involves the Galpha protein GPA-16. Development 2003, 130:5731-5740.
7. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
8. Burdine R., Schier A. Conserved and divergent mechanisms in left-right axis formation. Genes Dev. 2000, 14:763-776.
9. Duronio R.J., O'Farrell P.H. Developmental control of a G1-S transcriptional program in Drosophila. Development 1994, 120:1503-1515.
10. Gleichauf R. Anatomy and variability of sexual organs of Drosophila melanogaster (Meigen). Zeitschrift für Wissenschartliche Zoologie 1936, 148:1-66.
11. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
12. Hamada H., Meno C., Watanabe D., Saijoh Y. Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet. 2002, 3:103-113.
13. Hayashi T., Murakami R. Left-right asymmetry in Drosophila melanogaster gut development. Dev. Growth Differ. 2001, 43:239-246.
14. Hayashi M., Aono H., Ishihara J., Oshima S., Yamamoto H., Nakazato Y., Kobayashi S. Left-right asymmetry in the alimentary canal of the Drosophila embryo. Dev. Growth Differ. 2005, 47:457-460.
15. Hirokawa N., Tanaka Y., Okada Y., Takeda S. Nodal flow and the generation of left-right asymmetry. Cell 2006, 125:33-45.
16. Horne-Badovinac S., Munro E. Developmental biology. Tubular transformations. Science 2011, 333:294-295.
17. Hozumi S., Maeda R., Taniguchi K., Kanai M., Shirakabe S., Sasamura T., Spéder P., Noselli S., Aigaki T., Murakami R., Matsuno K. An unconventional myosin in Drosophila reverses the default handedness in visceral organs. Nature 2006, 440:798-802.
18. Iwaki D.D., Lengyel J.A. A Delta-Notch signaling border regulated by engrailed/invected repression specifies boundary cells in the Drosophila hindgut. Mech. Dev. 2002, 114:71-84.
19. Iwaki D.D., Johansen K.A., Singer J.B., Lengyel J.A. Drumstick, bowl, and lines are required for patterning and cell rearrangement in the Drosophila embryonic hindgut. Dev. Biol. 2001, 240:611-626.
20. Jiang J., Kosman D., Ip Y.T., Levine M. The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos. Genes Dev. 1991, 5:1881-1891.
21. Knust E., Bossinger O. Composition and formation of intercellular junctions in epithelial cells. Science 2002, 298:1955-1959.
22. Kuroda J., Nakamura M., Yoshida M., Yamamoto H., Maeda T., Taniguchi K., Nakazawa N., Hatori R., Ishio A., Ozaki A., Shimaoka S., Ito T., Iida H., Okumura T., Maeda R., Matsuno K. Canonical Wnt signaling in the visceral muscle is required for left-right asymmetric development of the Drosophila midgut. Mech. Dev. 2011, 128:625-639.
23. Levin M. Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 2004, 122:3-25.
24. Levin M., Palmer A. Left-right patterning from the inside out: widespread evidence for intracellular control. Bioessays 2007, 29:271-287.
25. Ligoxygakis P., Strigini M., Averof M. Specification of left-right asymmetry in the embryonic gut of Drosophila. Development 2001, 128:1171-1174.
26. Lin D.M., Goodman C.S. Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 1994, 13:507-523.
27. Liu X., Ohno S., Miki T. Nucleotide exchange factor ECT2 regulates epithelial cell polarity. Cell. Signal. 2006, 18:1604-1615.
28. Maeda R., Hozumi S., Taniguchi K., Sasamura T., Murakami R., Matsuno K. Roles of single-minded in the left-right asymmetric development of the Drosophila embryonic gut. Mech. Dev. 2007, 124:204-217.
29. Martin-Bermudo M.D., Dunin-Borkowski O.M., Brown N.H. Specificity of PS integrin function during embryogenesis resides in the alpha subunit extracellular domain. EMBO J. 1997, 16:4184-4193.
30. Michelson A.M. Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. Development 1994, 120:755-768.
31. Morita K., Hirono K., Han M. The Caenorhabditis elegans ect-2 RhoGEF gene regulates cytokinesis and migration of epidermal P cells. EMBO Rep. 2005, 6:1163-1168.
32. Oda H., Uemura T., Harada Y., Iwai Y., Takeichi M. A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell-cell adhesion. Dev. Biol. 1994, 165:716-726.
33. Okumura T., Utsuno H., Kuroda J., Gittenberger E., Asami T., Matsuno K. The development and evolution of left-right asymmetry in invertebrates: lessons from Drosophila and snails. Dev. Dyn. 2008, 237:3497-3515.
34. Okumura T., Fujiwara H., Taniguchi K., Kuroda J., Nakazawa N., Nakamura M., Hatori R., Ishio A., Maeda R., Matsuno K. Left-right asymmetric morphogenesis of the anterior midgut depends on the activation of a non-muscle myosin II in Drosophila. Dev. Biol. 2010, 344:693-706.
35. Pascual A., Huang K., Neveu J., Préat T. Neuroanatomy: brain asymmetry and long-term memory. Nature 2004, 427:605-606.
36. Prokopenko S., Brumby A., O'Keefe L., Prior L., He Y., Saint R., Bellen H. A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila. Genes Dev. 1999, 13:2301-2314.
37. Prokopenko S., Saint R., Bellen H. Tissue distribution of PEBBLE RNA and pebble protein during Drosophila embryonic development. Mech. Dev. 2000, 90:269-273.
38. Sanson B., White P., Vincent J.P. Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 1996, 383:627-630.
39. Schumacher S., Gryzik T., Tannebaum S., Müller H. The RhoGEF Pebble is required for cell shape changes during cell migration triggered by the Drosophila FGF receptor heartless. Development 2004, 131:2631-2640.
40. Shibazaki Y., Shimizu M., Kuroda R. Body handedness is directed by genetically determined cytoskeletal dynamics in the early embryo. Curr. Biol. 2004, 14:1462-1467.
41. Shiratori H., Hamada H. The left-right axis in the mouse: from origin to morphology. Development 2006, 133:2095-2104.
42. Smallhorn M., Murray M., Saint R. The epithelial-mesenchymal transition of the Drosophila mesoderm requires the Rho GTP exchange factor Pebble. Development 2004, 131:2641-2651.
43. Somers W., 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.
44. Sullivan W., Ashburner M., Hawley R.S. Drosophila Protocols 2000, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. Symons M., Settleman J. Rho family GTPases: more than simple switches. Trends Cell Biol. 2000, 10:415-419.
46. Tabin C. The key to left-right asymmetry. Cell 2006, 127:27-32.
47. Tabin C., Vogan K. A two-cilia model for vertebrate left-right axis specification. Genes Dev. 2003, 17:1-6.
48. Takashima S., Murakami R. Regulation of pattern formation in the Drosophila hindgut by wg, hh, dpp, and en. Mech. Dev. 2001, 101:79-90.
49. Taniguchi K., Hozumi S., Maeda R., Okumura T., Matsuno K. Roles of type I myosins in Drosophila handedness. Fly (Austin) 2007, 1:287-290.
50. Taniguchi K., Hozumi S., Maeda R., Ooike M., Sasamura T., Aigaki T., Matsuno K. D-JNK signaling in visceral muscle cells controls the laterality of the Drosophila gut. Dev. Biol. 2007, 311:251-263.
51. Taniguchi K., Maeda R., Ando T., Okumura T., Nakazawa N., Hatori R., Nakamura M., Hozumi S., Fujiwara H., Matsuno K. Chirality in planar cell shape contributes to left-right asymmetric epithelial morphogenesis. Science 2011, 333:339-341.
52. Tatsumoto T., Xie X., Blumenthal R., Okamoto I., Miki T. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J. Cell Biol. 1999, 147:921-928.
53. van Impel A., Schumacher S., Draga M., Herz H., Grosshans J., Müller H. Regulation of the Rac GTPase pathway by the multifunctional Rho GEF Pebble is essential for mesoderm migration in the Drosophila gastrula. Development 2009, 136:813-822.
54. Wan L.Q., Ronaldson K., Park M., Taylor G., Zhang Y., Gimble J.M., Vunjak-Novakovic G. Micropatterned mammalian cells exhibit phenotype-specific left-right asymmetry. Proc. Natl. Acad. Sci. USA 2011, 108:12295-12300.
55. Xu J., Van Keymeulen A., Wakida N.M., Carlton P., Berns M.W., Bourne H.R. Polarity reveals intrinsic cell chirality. Proc. Natl. Acad. Sci. USA 2007, 104:9296-9300.
56. Yao K.M., White K. Neural specificity of elav expression: defining a Drosophila promoter for directing expression to the nervous system. J. Neurochem. 1994, 63:41-51.