Generation of Robust Left-Right Asymmetry in the Mouse Embryo Requires a Self-Enhancement and Lateral-Inhibition System

Developmental Cell

Volumn 11, Issue 4, 2006, Pages 495-504

  Nakamura, Tetsuya ^a   Mine, Naoki ^a   Nakaguchi, Etsushi ^a   Mochizuki, Atsushi ^b   Yamamoto, Masamichi ^a   Yashiro, Kenta ^a   Meno, Chikara ^a   Hamada, Hiroshi ^a  

^a OSAKA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

DEVBIO; SYSBIO

Indexed keywords

LEFTY PROTEIN; LEFTY1 PROTEIN; LEFTY2 PROTEIN; MESSENGER RNA; PROTEIN NODAL; PROTEIN SUBUNIT; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO AXIS; EMBRYO PATTERN FORMATION; GENE EXPRESSION REGULATION; GENE INTERACTION; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MOLECULAR SIZE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; QUALITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SIMULATION; THEORETICAL MODEL;

ANIMALS; BODY PATTERNING; COMPUTER SIMULATION; EMBRYO; EMBRYONIC INDUCTION; FORKHEAD TRANSCRIPTION FACTORS; GENETIC VECTORS; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; MICE, MUTANT STRAINS; MODELS, BIOLOGICAL; MODELS, THEORETICAL; ORGAN CULTURE TECHNIQUES; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 33749042595     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2006.08.002     Document Type: Article

References (40)

1. Asai R., Taguchi E., Kume Y., Saito M., and Kondo S. Zebrafish leopard gene as a component of the putative reaction-diffusion system. Mech. Dev. 89 (1999) 87-92
2. Belenkaya T.Y., Han C., Yan D., Opoka R.J., Khodoun M., Liu H., and Lin X. Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 119 (2004) 231-244
3. Brennan J., Norris D.P., and Robertson E.J. Nodal activity in the node governs left-right asymmetry. Genes Dev. 16 (2002) 2339-2344
4. Chen Y., and Schier A.F. The zebrafish Nodal signal Squint functions as a morphogen. Nature 411 (2001) 607-610
5. Chen Y., and Schier A.F. Lefty proteins are long-range inhibitors of squint-mediated nodal signaling. Curr. Biol. 12 (2002) 2124-2128
6. Collignon J., Varlet I., and Robertson E.J. Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature 381 (1996) 155-158
7. Danos M.C., and Yost H.J. Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev. Biol. 177 (1996) 96-103
8. Entchev E.V., Schwabedissen A., and Gonzalez-Gaitan M. Gradient formation of the TGF-β homolog Dpp. Cell 103 (2000) 981-991
9. Essner J.J., Amack J.D., Nyholm M.K., Harris E.B., and 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 132 (2005) 1247-1260
10. Greco V., Hannus M., and Eaton S. Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell 106 (2001) 633-645
11. Hamada H., Meno C., Watanabe D., and Saijoh Y. Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet. 3 (2002) 103-113
12. Hou J., Yashiro K., Okazaki Y., Saijoh Y., Hayashizaki Y., and Hamada H. Identification of a novel left-right asymmetrically expressed gene in the mouse belonging to the BPI/PLUNC superfamily. Dev. Dyn. 229 (2004) 373-379
13. Huangfu D., Liu A., Rakeman A.S., Murcia N.S., Niswander L., and Anderson K.V. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426 (2003) 83-87
14. Juan H., and Hamada H. Roles of nodal-lefty regulatory loops in embryonic patterning of vertebrates. Genes Cells 6 (2001) 923-930
15. Kondo S. The reaction-diffusion system: a mechanism for autonomous pattern formation in the animal skin. Genes Cells 7 (2002) 535-541
16. Lee H.X., Ambrosio A.L., Reversade B., and De Robertis E.D. Embryonic dorsal-ventral signaling: secreted frizzled-related proteins as inhibitors of tolloid proteinases. Cell 124 (2006) 147-159
17. Levin M. Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 122 (2005) 3-25
18. Lowe L.A., Supp D.M., Sampath K., Yokoyama T., Wright C.V., Potter S.S., Overbeek P., and Kuehn M.R. Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature 381 (1996) 158-161
19. Meinhardt H. Organizer and axes formation as a self-organizing process. Int. J. Dev. Biol. 45 (2001) 177-188
20. Meinhardt H., and Gierer A. Pattern formation by local self-activation and lateral inhibition. Bioessays 22 (2000) 753-760
21. Meno C., Shimono A., Saijoh Y., Yashiro K., Mochida K., Ohishi S., Noji S., Kondoh H., and Hamada H. lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal. Cell 94 (1998) 287-297
22. Meno C., Takeuchi J., Sakuma R., Koshiba-Takeuchi K., Ohishi S., Saijoh Y., Miyazaki J., ten Dijke P., Ogura T., and Hamada H. Diffusion of nodal signaling activity in the absence of the feedback inhibitor Lefty2. Dev. Cell 1 (2001) 127-138
23. Morgan D., Turnpenny L., Goodship J., Dai W., Majumder K., Matthews L., Gardner A., Schuster G., Vien L., Harrison W., et al. Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse. Nat. Genet. 20 (1998) 149-156
24. Murcia N.S., Richards W.G., Yoder B.K., Mucenski M.L., Dunlap J.R., and Woychik R.P. The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 127 (2000) 2347-2355
25. Nonaka S., Tanaka Y., Okada Y., Takeda S., Harada A., Kanai Y., Kido M., and 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 95 (1998) 829-837
26. Okada Y., Nonaka S., Tanaka Y., Saijoh Y., Hamada H., and Hirokawa N. Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol. Cell 4 (1999) 459-468
27. Okada Y., Takeda S., Tanaka Y., Belmonte J.C., and Hirokawa N. Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 121 (2005) 633-644
28. Panakova D., Sprong H., Marois E., Thiele C., and Eaton S. Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435 (2005) 58-65
29. Pearce J.J., Penny G., and Rossant J. A mouse cerberus/Dan-related gene family. Dev. Biol. 209 (1999) 98-110
30. Saijoh Y., Adachi H., Sakuma R., Yeo C.Y., Yashiro K., Watanabe M., Hashiguchi H., Mochida K., Ohishi S., Kawabata M., et al. Left-right asymmetric expression of lefty2 and nodal is induced by a signaling pathway that includes the transcription factor FAST2. Mol. Cell 5 (2000) 35-47
31. Saijoh Y., Oki S., Ohishi S., and Hamada H. Left-right patterning of the mouse lateral plate requires nodal produced in the node. Dev. Biol. 256 (2003) 160-172
32. Saijoh Y., Oki S., Tanaka C., Nakamura T., Adachi H., Yan Y.T., Shen M.M., and Hamada H. Two nodal-responsive enhancers control left-right asymmetric expression of Nodal. Dev. Dyn. 232 (2005) 1031-1036
33. Sakuma R., Ohnishi Yi Y., Meno C., Fujii H., Juan H., Takeuchi J., Ogura T., Li E., Miyazono K., and Hamada H. Inhibition of Nodal signalling by Lefty mediated through interaction with common receptors and efficient diffusion. Genes Cells 7 (2002) 401-412
34. Shiratori H., Sakuma R., Watanabe M., Hashiguchi H., Mochida K., Sakai Y., Nishino J., Saijoh Y., Whitman M., and Hamada H. Two-step regulation of left-right asymmetric expression of Pitx2: initiation by nodal signaling and maintenance by Nkx2. Mol. Cell 7 (2001) 137-149
35. Supp D.M., Witte D.P., Potter S.S., and Brueckner M. Mutation of an axonemal dynein affects left-right asymmetry in inversus viscerum mice. Nature 389 (1997) 963-966
36. Tabin C. Do we know anything about how left-right asymmetry is first established in the vertebrate embryo?. J. Mol. Histol. 36 (2005) 317-323
37. Turing A.M. The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. B237 (1952) 37-72
38. Whitman M. Smads and early developmental signaling by the TGFβ superfamily. Genes Dev. 12 (1998) 2445-2462
39. Yamamoto M., Mine N., Mochida K., Sakai Y., Saijoh Y., Meno C., and Hamada H. Nodal signaling induces the midline barrier by activating Nodal expression in the lateral plate. Development 130 (2003) 1795-1804
40. Yamamoto M., Saijoh Y., Perea-Gomez A., Shawlot W., Behringer R.R., Ang S.L., Hamada H., and Meno C. Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428 (2004) 387-392