Left-right asymmetry is formed in individual cells by intrinsic cell chirality

Mechanisms of Development

Volumn 133, Issue , 2014, Pages 146-162

  Hatori, Ryo ^a,c   Ando, Tadashi ^b   Sasamura, Takeshi ^c   Nakazawa, Naotaka ^a,c   Nakamura, Mitsutoshi ^c   Taniguchi, Kiichiro ^a   Hozumi, Shunya ^a   Kikuta, Junichi ^d   Ishii, Masaru ^d   Matsuno, Kenji ^c  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

^b RIKEN   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Drosophila; Left right asymmetry; Planar cell chirality

Indexed keywords

F ACTIN; MYOSIN; MYOSIN II; MYOSIN31DF; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; MYO31DF PROTEIN, DROSOPHILA; MYOSIN I;

ANIMAL CELL; ARTICLE; CELL ELONGATION; CELL INTERACTION; CELL MUTANT; CELL SHAPE; CELL STRUCTURE; COMPUTER MODEL; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; EPITHELIUM CELL; FEMALE; MALE; NONHUMAN; PLANAR CELL CHIRALITY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; CELL POLARITY; COMPUTER SIMULATION; CYTOLOGY; DIGESTIVE SYSTEM; EMBRYOLOGY; GENE; GENETICS; MECHANOTRANSDUCTION; MORPHOGENESIS; MOSAICISM; MUTATION; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CELL POLARITY; CELL SHAPE; COMPUTER SIMULATION; DIGESTIVE SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENES, INSECT; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; MOSAICISM; MUTATION; MYOSIN TYPE I;

EID: 84908162259     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2014.04.002     Document Type: Article

References (53)

1. Adams D.S., Robinson K.R., Fukumoto T., Yuan S., Albertson R.C., 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.
2. Aigouy B., Farhadifar R., Staple D.B., Sagner A., Röper J.C., Jülicher F., Eaton S. Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 2010, 142:773-786.
3. Baarsma H.A., Königshoff M., Gosens R. The WNT signaling pathway from ligand secretion to gene transcription: molecular mechanisms and pharmacological targets. Pharmacol. Ther. 2013, 138:66-83.
4. Bachmann A., Knust E. The use of P-element transposons to generate transgenic flies. Methods Mol. Biol. 2008, 420:61-77.
5. Blankenship J.T., Backovic S.T., Sanny J.S., Weitz O., Zallen J.A. Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev. Cell 2006, 11:459-470.
6. Borghi N., Sorokina M., Shcherbakova O.G., Weis W.I., Pruitt B.L., Nelson W.J., Dunn A.R. E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch. Proc. Natl. Acad. Sci. USA 2012, 109:12568-12573.
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. Briscoe J., Thérond P.P. The mechanisms of Hedgehog signalling and its roles in development and disease. Nat. Rev. Mol. Cell Biol. 2013, 14:416-429.
9. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., Tsien R.Y. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 2002, 99:7877-7882.
10. Chen T.H., Hsu J.J., Zhao X., Guo C., Wong M.N., Huang Y., Li Z., Garfinkel A., Ho C.M., Tintut Y., Demer L.L. Left-right symmetry breaking in tissue morphogenesis via cytoskeletal mechanics. Circ. Res. 2012, 110:551-559.
11. Essner J.J., Amack J.D., Nyholm M.K., Harris E.B., Yost H.J. Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 2005, 132:1247-1260.
12. Gorfinkiel N., Blanchard G.B. Dynamics of actomyosin contractile activity during epithelial morphogenesis. Curr. Opin. Cell Biol. 2011, 23:531-539.
13. Gros J., Feistel K., Viebahn C., Blum M., Tabin C.J. Cell movements at Hensen's node establish left/right asymmetric gene expression in the chick. Science 2009, 324:941-944.
14. Hayashi T., Murakami R. Left-right asymmetry in Drosophila melanogaster gut development. Dev. Growth Differ. 2001, 43:239-246.
15. Heisenberg C.P., Bellaïche Y. Forces in tissue morphogenesis and patterning. Cell 2013, 153:948-962.
16. 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.
17. Hozumi S., Maeda R., Taniguchi-Kanai M., Okumura T., Taniguchi K., Kawakatsu Y., Nakazawa N., Hatori R., Matsuno K. 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. 2008, 237:3528-3537.
18. Huveneers S., de Rooij J. Mechanosensitive systems at the cadherin-F-actin interface. J. Cell Sci. 2013, 126:403-413.
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. Krebs L.T., Iwai N., Nonaka S., Welsh I.C., Lan Y., Jiang R., Saijoh Y., O'Brien T.P., Hamada H., Gridley T. Notch signaling regulates left-right asymmetry determination by inducing Nodal expression. Genes Dev. 2003, 17:1207-1212.
21. 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. 2012, 128:625-639.
22. Kuroda R., Endo B., Abe M., Shimizu M. Chiral blastomere arrangement dictates zygotic left-right asymmetry pathway in snails. Nature 2009, 462:790-794.
23. Larkins C.E., Long A.B., Caspary T. Defective Nodal and Cerl2 expression in the Arl13b(hnn) mutant node underlie its heterotaxia. Dev. Biol. 2012, 367:15-24.
24. Lengyel J.A., Iwaki D.D. It takes guts: the Drosophila hindgut as a model system for organogenesis. Dev. Biol. 2002, 243:1-19.
25. Levin M., Thorlin T., Robinson K.R., Nogi T., Mercola M. Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 2002, 111:77-89.
26. Levin M. Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 2005, 122:3-25.
27. Maeda S., Tsukihara T. Structure of the gap junction channel and its implications for its biological functions. Cell. Mol. Life Sci. 2011, 68:1115-1129.
28. Meshcheriakov V.N. Dyssymmetrical cytotomy and orientation of the spindles in early isolated blastomeres of gastropod molluscs. Ontogenez 1976, 7:558-565.
29. Nagai T., Honda H. A dynamic cell model for the formation of epithelial tissues. Philos. Mag. B 2001, 81:699-719.
30. Nakamura M., Matsumoto K., Iwamoto Y., Muguruma T., Nakazawa N., Hatori R., Taniguchi K., Maeda R., Matsuno K. 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. 2013, 130:169-180.
31. Nakamura T., Hamada H. Left-right patterning: conserved and divergent mechanisms. Development 2012, 139:3257-3262.
32. Nakazawa N., Taniguchi K., Okumura T., Maeda R., Matsuno K. A novel Cre/loxP system for mosaic gene expression in the Drosophila embryo. Dev. Dyn. 2012, 241:965-974.
33. Nonaka S., Tanaka Y., Okada Y., Takeda S., Harada A., Kanai Y., Kido M., Hirokawa N. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 1998, 95:829-837.
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. 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.
36. Olguín P., Glavic A., Mlodzik M. Intertissue mechanical stress affects Frizzled-mediated planar cell polarity in the Drosophila notum epidermis. Curr. Biol. 2011, 21:236-242.
37. Palmer A.R. Symmetry breaking and the evolution of development. Science 2004, 306:828-833.
38. Pascual A., Huang K.L., Neveu J., Préat T. Neuroanatomy: brain asymmetry and long-term memory. Nature 2004, 427:605-606.
39. Petzoldt A.G., Coutelis J.B., Géminard C., Spéder P., Suzanne M., Cerezo D., Noselli S. DE-Cadherin regulates unconventional Myosin ID and Myosin IC in Drosophila left-right asymmetry establishment. Development 2012, 139:1874-1884.
40. Pohl C., Bao Z. Chiral forces organize left-right patterning in C. elegans by uncoupling midline and anteroposterior axis. Dev. Cell 2010, 19:402-412.
41. Rauzi M., Lenne P.F., Lecuit T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 2010, 468:1110-1114.
42. 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.
43. Shiratori H., Hamada H. The left-right axis in the mouse: from origin to morphology. Development 2006, 133:2095-2104.
44. Spéder P., Adám G., Noselli S. Type ID unconventional myosin controls left-right asymmetry in Drosophila. Nature 2006, 440:803-807.
45. 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.
46. Toyama Y., Peralta X.G., Wells A.R., Kiehart D.P., Edwards G.S. Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 2008, 321:1683-1686.
47. Trepat X., Fredberg J.J. Plithotaxis and emergent dynamics in collective cellular migration. Trends Cell Biol. 2011, 21:638-646.
48. Vandenberg L.N., Levin M. A unified model for left-right asymmetry? Comparison and synthesis of molecular models of embryonic laterality. Dev. Biol. 2013, 379:1-15.
49. 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.
50. Wells R.E., Barry J.D., Warrington S.J., Cuhlmann S., Evans P., Huber W., Strutt D., Zeidler M.P. Control of tissue morphology by Fasciclin III-mediated intercellular adhesion. Development 2013, 140:3858-3868.
51. 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.
52. Yost H.J. Left-right asymmetry: nodal cilia make and catch a wave. Curr. Biol. 2003, 13:R808-R809.
53. Zhang L., Ward R.E. Distinct tissue distributions and subcellular localizations of differently phosphorylated forms of the myosin regulatory light chain in Drosophila. Gene Expr. Patterns 2011, 11:93-104.