The myosin ID pathway and left-right asymmetry in Drosophila

Genesis

Volumn 52, Issue 6, 2014, Pages 471-480

  Géminard, Charles ^a,b   González Morales, Nicanor ^a,b   Coutelis, Jean Baptiste ^a,b   Noselli, Stéphane ^a,b  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b CENTRE DE BIOCHIMIE   (France)

Author keywords

Asymmetric morphogenesis in invertebrates; Developmental biology; Diptera; Genetic; HOX gene Abdominal B; Invertebrates; Left right asymmetry; Morphogenesis; Symmetry breaking; Unconventional type I myosin

Indexed keywords

ABDOMINAL B PROTEIN; ALPHA CATENIN; BETA CATENIN; CADHERIN; HORMONE; HOX PROTEIN; MYOSIN I; MYOSIN IC; MYOSIN ID; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

APOPTOSIS; BRAIN; BRAIN ASYMMETRY; CELL DEATH; CELL ELONGATION; CELL JUNCTION; CELLULAR STRESS RESPONSE; EPIDIDYMIS; GENE EXPRESSION; GENETIC SCREENING; HEMISPHERIC DOMINANCE; HOX GENE; IMMUNITY; INTESTINE; LEFT RIGHT ASYMMETRY; LONG TERM MEMORY; MALPIGHIAN TUBULE; METAMORPHOSIS; MICROARRAY ANALYSIS; MOLECULAR GENETICS; MORPHOGENESIS; NONHUMAN; NUCLEAR REPROGRAMMING; ORGAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; SELF CONCEPT; SIGNAL TRANSDUCTION; TERMINALIA; TESTIS; TISSUES; VAS DEFERENS; ANIMAL; DROSOPHILA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; BODY PATTERNING; DROSOPHILA; GENE EXPRESSION REGULATION; MORPHOGENESIS; MYOSIN TYPE I; SIGNAL TRANSDUCTION;

EID: 84902682782     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22763     Document Type: Review

References (82)

1. Abbott MK, Lengyel JA. 1991. Embryonic head involution and rotation of male terminalia require the Drosophila locus head involution defective. Genetics 129:783-789.
2. Adachi-Yamada T, Fujimura-Kamada K, et al. 1999. Distortion of proximodistal information causes JNK-dependent apoptosis in Drosophila wing. Nature 400:166-169.
3. Adam G, Perrimon N, et al. 2003. The retinoic-like juvenile hormone controls the looping of left-right asymmetric organs in Drosophila. Development 130:2397-2406.
4. Adams DS, Robinson KR, et al. 2006. Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133:1657-1671.
5. Agnes F, Noselli S. 1999. [Dorsal closure in Drosophila. A genetic model for wound healing?]. C R Acad Sci III 322:5-13.
6. Agnes F, Suzanne M, et al. 1999. The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis. Development 126:5453-5462.
7. Aizawa, H. 2013. Habenula and the asymmetric development of the vertebrate brain. Anat Sci Int 88:1-9.
8. Aylsworth AS, 2001. Clinical aspects of defects in the determination of laterality. Am J Med Genet 101:345-355.
9. Barylko B, Binns DD, et al. 2000. Regulation of the enzymatic and motor activities of myosin I. Biochim Biophys Acta 1496:23-35.
10. Berg JS, Powell BC, et al. 2001. A millennial myosin census. Mol Biol Cell 12:780-794.
11. Beyenbach KW, Skaer H, et al. 2010. The developmental, molecular, and transport biology of Malpighian tubules. Annu Rev Entomol 55: 351-374.
12. Bishop DV. 2013. Cerebral asymmetry and language development: Cause, correlate, or consequence? Science 340:1230531.
13. Brody T, Cravchik A. 2000. Drosophila melanogaster G protein-coupled receptors. J Cell Biol 150: F83-88.
14. Chintapalli VR, Terhzaz S, et al. 2012. Functional correlates of positional and gender-specific renal asymmetry in Drosophila. PLoS One 7: e32577.
15. Coluccio LM. 1997. Myosin I. Am J Physiol 273: C347-359.
16. Concha ML, Wilson SW. 2001. Asymmetry in the epithalamus of vertebrates. J Anat 199(Pt 1-2):63-84.
17. Coutelis JB, Geminard C, et al. 2013. Drosophila left/right asymmetry establishment is controlled by the Hox gene abdominal-B. Dev Cell 24:89-97.
18. Coutelis JB, Petzoldt AG, et al. 2008. Left-right asymmetry in Drosophila. Semin Cell Dev Biol 19:252-262.
19. Danilchik MV, Brown EE, et al. 2006. Intrinsic chiral properties of the Xenopus egg cortex: An early indicator of left-right asymmetry? Development 133:4517-4526.
20. de Cuevas M, Matunis EL. 2011. The stem cell niche: Lessons from the Drosophila testis. Development 138:2861-2869.
21. Gettings M, Serman F, et al. 2010. JNK signalling controls remodelling of the segment boundary through cell reprogramming during Drosophila morphogenesis. PLoS Biol 8: e1000390.
22. Glise B, Bourbon H, et al. 1995. hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83:451-461.
23. Glise B, Noselli S. 1997. Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev 11:1738-1747.
24. Grether ME, Abrams JM, et al. 1995. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev 9:1694-1708.
25. Hall BL, Thummel CS. 1998. The RXR homolog ultraspiracle is an essential component of the Drosophila ecdysone receptor. Development 125:4709-4717.
26. Harmon MA, Boehm MF, et al. 1995. Activation of mammalian retinoid X receptors by the insect growth regulator methoprene. Proc Natl Acad Sci U S A 92:6157-6160.
27. Hartenstein, V. 1993. Atlas of Drosophila Development, Cold Spring Harbor Laboratory Press.
28. Hayashi T, Murakami R. 2001. Left-right asymmetry in Drosophila melanogaster gut development. Dev Growth Differ 43:239-246.
29. Holland PM, Suzanne M, et al. 1997. MKK7 is a stress-activated mitogen-activated protein kinase kinase functionally related to hemipterous. J Biol Chem 272:24994-24998.
30. Hombria JC, Brown S. 2002. The fertile field of Drosophila Jak/STAT signalling. Curr Biol 12: R569-575.
31. Hozumi S, Maeda R, et al. 2006. An unconventional myosin in Drosophila reverses the default handedness in visceral organs. Nature 440:798-802.
32. Hozumi S, Maeda R, et al. 2008. Head region of unconventional myosin I family members is responsible for the organ-specificity of their roles in left-right polarity in Drosophila. Dev Dyn 237:3528-3537.
33. Jenett A, Rubin GM, et al. 2012. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2:991-1001.
34. Jiang H, Edgar BA. 2011. Intestinal stem cells in the adult Drosophila midgut. Exp Cell Res 317:2780-2788.
35. Jiang H, Edgar BA. 2012. Intestinal stem cell function in Drosophila and mice. Curr Opin Genet Dev 22:354-360.
36. Jones G, Sharp PA. 1997. Ultraspiracle: An invertebrate nuclear receptor for juvenile hormones. Proc Natl Acad Sci USA 94:13499-13503.
37. Keisman EL, Baker BS. 2001. The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signaling to deploy dachshund sex-specifically in the genital imaginal disc. Development 128:1643-1656.
38. Kim SV, Flavell RA. 2008. Myosin I: From yeast to human. Cell Mol Life Sci 65:2128-2137.
39. Kuranaga E, Matsunuma T, et al. 2011. Apoptosis controls the speed of looping morphogenesis in Drosophila male terminalia. Development 138:1493-1499.
40. Kuroda J, Nakamura M, et al. 2012. Canonical Wnt signaling in the visceral muscle is required for left-right asymmetric development of the Drosophila midgut. Mech Dev 128:625-639.
41. Lang M, Orgogozo V. 2012. Distinct copulation positions in Drosophila pachea males with symmetric or asymmetric external genitalia. Contributions to Zoology 81:87-94.
42. Le Bras S, Van Doren M. 2006. Development of the male germline stem cell niche in Drosophila. Dev Biol 294:92-103.
43. Lengyel JA, Iwaki DD. 2002. It takes guts: The Drosophila hindgut as a model system for organogenesis. Dev Biol 243:1-19.
44. Levin, M., Johnson RL, et al. 1995. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82:803-814.
45. Levin M, Thorlin T, et al. 2002. Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111:77-89.
46. Loveland KL, Hime G. 2005. TGFbeta superfamily members in spermatogenesis: Setting the stage for fertility in mouse and Drosophila. Cell Tissue Res 322:141-146.
47. Macias A, Romero NM, et al. 2004. PVF1/PVR signaling and apoptosis promotes the rotation and dorsal closure of the Drosophila male terminalia. Int J Dev Biol 48:1087-1094.
48. Maeda R, Hozumi S, et al. 2007. Roles of single-minded in the left-right asymmetric development of the Drosophila embryonic gut. Mech Dev 124:204-217.
49. Maeda RK, Karch F. 2006. The ABC of the BX-C: The bithorax complex explained. Development 133:1413-1422.
50. Manjon C, Sanchez-Herrero E, et al. 2007. Sharp boundaries of Dpp signalling trigger local cell death required for Drosophila leg morphogenesis. Nat Cell Biol 9:57-63.
51. Manner, J. 2009. The anatomy of cardiac looping: A step towards the understanding of the morphogenesis of several forms of congenital cardiac malformations. Clin Anat 22:21-35.
52. Mercola M, Levin M. 2001. Left-right asymmetry determination in vertebrates. Annu Rev Cell Dev Biol 17: 779-805.
53. Micchelli CA. 2012. The origin of intestinal stem cells in Drosophila. Dev Dyn 241:85-91.
54. Micchelli CA, Perrimon N. 2006. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439:475-479.
55. Morgan D, Turnpenny L, et al. 1998. Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse. Nat Genet 20:149-156.
56. Morton BE. 2013. Behavioral laterality of the brain: Support for the binary construct of hemisity. Front Psychol 4: 683.
57. Myat MM. 2005. Making tubes in the Drosophila embryo. Dev Dyn 232:617-632.
58. Nakamura M, Matsumoto K, et al. 2013. Reduced cell number in the hindgut epithelium disrupts hindgut left-right asymmetry in a mutant of pebble, encoding a RhoGEF, in Drosophila embryos. Mech Dev 130:169-180.
59. Noselli S, Agnes F. 1999. Roles of the JNK signaling pathway in Drosophila morphogenesis. Curr Opin Genet Dev 9:466-472.
60. Nurnberger J, Bacallao RL, et al. 2002. Inversin forms a complex with catenins and N-cadherin in polarized epithelial cells. Mol Biol Cell 13:3096-3106.
61. Ohlstein B, Spradling A. 2006. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470-474.
62. Okumura T, Fujiwara H, et al. 2010. Left-right asymmetric morphogenesis of the anterior midgut depends on the activation of a non-muscle myosin II in Drosophila. Dev Biol 344:693-706.
63. Okumura T, Utsuno H, et al. 2008. The development and evolution of left-right asymmetry in invertebrates: Lessons from Drosophila and snails. Dev Dyn 237:3497-3515.
64. Pascual A, Huang KL, et al. 2004. Neuroanatomy: Brain asymmetry and long-term memory. Nature 427:605-606.
65. Petzoldt AG, Coutelis JB, et al. 2012. DE-Cadherin regulates unconventional Myosin ID and Myosin IC in Drosophila left-right asymmetry establishment. Development 139:1874-1884.
66. Pyrpassopoulos S, Feeser EA, et al. 2012. Membrane-bound myo1c powers asymmetric motility of actin filaments. Curr Biol 22:1688-1692.
67. Raya A, Izpisua Belmonte JC. 2008. Insights into the establishment of left-right asymmetries in vertebrates. Birth Defects Res C Embryo Today 84:81-94.
68. Richards TA, Cavalier-Smith T. 2005. Myosin domain evolution and the primary divergence of eukaryotes. Nature 436:1113-1118.
69. Rousset R, Bono-Lauriol S, et al. 2010. The Drosophila serine protease homologue Scarface regulates JNK signalling in a negative-feedback loop during epithelial morphogenesis. Development 137:2177-2186.
70. Roussigne M, Blader P, et al. 2012. Breaking symmetry: The zebrafish as a model for understanding left-right asymmetry in the developing brain. Dev Neurobiol 72:269-281.
71. Santos AC, Lehmann R. 2004. Germ cell specification and migration in Drosophila and beyond. Curr Biol 14: R578-589.
72. Speder P, Adam G, et al. 2006. Type ID unconventional myosin controls left-right asymmetry in Drosophila. Nature 440:803-807.
73. Speder P, Noselli S. 2007. Left-right asymmetry: Class I myosins show the direction. Curr Opin Cell Biol 19:82-87.
74. Speder P, Petzoldt A, et al. 2007. Strategies to establish left/right asymmetry in vertebrates and invertebrates. Curr Opin Genet Dev 17:351-358.
75. Suzanne M, Petzoldt AG, et al. 2010. Coupling of apoptosis and L/R patterning controls stepwise organ looping. Curr Biol 20:1773-1778.
76. Tabin, C. 2005. Do we know anything about how left-right asymmetry is first established in the vertebrate embryo? J Mol Histol 36:317-323.
77. Takashima S, Younossi-Hartenstein A, et al. 2011. A novel tissue in an established model system: The Drosophila pupal midgut. Dev Genes Evol 221:69-81.
78. Taniguchi K, Hozumi S, et al. 2007. D-JNK signaling in visceral muscle cells controls the laterality of the Drosophila gut. Dev Biol 311:251-263.
79. Taniguchi K, Maeda R, et al. 2011. Chirality in planar cell shape contributes to left-right asymmetric epithelial morphogenesis. Science 333:339-341.
80. Thomas C, Rousset R, et al. 2009. JNK signalling influences intracellular trafficking during Drosophila morphogenesis through regulation of the novel target gene Rab30. Dev Biol 331:250-260.
81. Vandenberg LN, Levin M. 2013. A unified model for left-right asymmetry? Comparison and synthesis of molecular models of embryonic laterality. Dev Biol 379:1-15.
82. Zeitlinger J, Bohmann D. 1999. Thorax closure in Drosophila: Involvement of Fos and the JNK pathway. Development 126:3947-3956.