Opposing Nodal and BMP Signals Regulate Left-Right Asymmetry in the Sea Urchin Larva

PLoS Biology

Volumn 10, Issue 10, 2012, Pages

  Luo, Yi Jyun ^a   Su, Yi Hsien ^a  

^a INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; MESSENGER RNA; NODAL SIGNALING PROTEIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN;

ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MORPHOGENETIC PROTEIN GENE; CELL LINEAGE; CELL SEPARATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; EMBRYO CELL; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; LARVAL STAGE; NONHUMAN; PRIMORDIUM; PROTEIN FUNCTION; REGULATOR GENE; SEA URCHIN; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; NODAL PROTEIN; SEA URCHINS; SIGNAL TRANSDUCTION;

DEUTEROSTOMIA; ECHINOIDEA; VERTEBRATA;

EID: 84868119538     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001402     Document Type: Article

References (69)

1. Speder P, Petzoldt A, Suzanne M, Noselli S, (2007) Strategies to establish left/right asymmetry in vertebrates and invertebrates. Curr Opin Genet Dev 17: 351-358.
2. Vandenberg LN, Levin M, (2010) Far from solved: a perspective on what we know about early mechanisms of left-right asymmetry. Dev Dyn 239: 3131-3146.
3. Hashimoto M, Hamada H, (2010) Translation of anterior-posterior polarity into left-right polarity in the mouse embryo. Curr Opin Genet Dev 20: 433-437.
4. Raya A, Izpisua Belmonte JC, (2006) Left-right asymmetry in the vertebrate embryo: from early information to higher-level integration. Nat Rev Genet 7: 283-293.
5. Levin M, (2005) Left-right asymmetry in embryonic development: a comprehensive review. Mech Dev 122: 3-25.
6. Duboc V, Rottinger E, Lapraz F, Besnardeau L, Lepage T, (2005) Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev Cell 9: 147-158.
7. Grande C, Patel NH, (2009) Nodal signalling is involved in left-right asymmetry in snails. Nature 457: 1007-1011.
8. Kishigami S, Mishina Y, (2005) BMP signaling and early embryonic patterning. Cytokine Growth Factor Rev 16: 265-278.
9. Monsoro-Burq A, Le Douarin NM, (2001) BMP4 plays a key role in left-right patterning in chick embryos by maintaining Sonic Hedgehog asymmetry. Mol Cell 7: 789-799.
10. Mine N, Anderson RM, Klingensmith J, (2008) BMP antagonism is required in both the node and lateral plate mesoderm for mammalian left-right axis establishment. Development 135: 2425-2434.
11. Rodriguez Esteban C, Capdevila J, Economides AN, Pascual J, Ortiz A, et al. (1999) The novel Cer-like protein Caronte mediates the establishment of embryonic left-right asymmetry. Nature 401: 243-251.
12. Yokouchi Y, Vogan KJ, Pearse RV II, Tabin CJ, (1999) Antagonistic signaling by Caronte, a novel Cerberus-related gene, establishes left-right asymmetric gene expression. Cell 98: 573-583.
13. Katsu K, Tokumori D, Tatsumi N, Suzuki A, Yokouchi Y, (2012) BMP inhibition by DAN in Hensen's node is a critical step for the establishment of left-right asymmetry in the chick embryo. Dev Biol 363: 15-26.
14. Ramsdell AF, Yost HJ, (1999) Cardiac looping and the vertebrate left-right axis: antagonism of left-sided Vg1 activity by a right-sided ALK2-dependent BMP pathway. Development 126: 5195-5205.
15. Iijima M, Takeuchi T, Sarashina I, Endo K, (2008) Expression patterns of engrailed and dpp in the gastropod Lymnaea stagnalis. Dev Genes Evol 218: 237-251.
16. Shimizu K, Sarashina I, Kagi H, Endo K, (2011) Possible functions of Dpp in gastropod shell formation and shell coiling. Dev Genes Evol 221: 59-68.
17. Cameron RA, Fraser SE, Britten RJ, Davidson EH, (1991) Macromere cell fates during sea urchin development. Development 113: 1085-1091.
18. Gustafson T, Wolpert L, (1963) Studies on the cellular basis of morphogenesis in the sea urchin embryo. Exp Cell Res 29: 561-582.
19. Hara Y, Kuraishi R, Uemura I, Katow H, (2003) Asymmetric formation and possible function of the primary pore canal in plutei of Temnopleurus hardwicki. Dev Growth Differ 45: 295-308.
20. Ruppert EE, Balser EJ, (1986) Nephridia in the larvae of hemichordates and echinoderms. Biol Bull 171: 188-196.
21. Hyman LH (1955) The invertebrates: echinodermata, the coelomate bilateria, volume IV. New York: McGraw-Hill Book Company, Inc.
22. Eaves AA, (2005) Potential for paired vestibules in plutei (Echinodermata, Echinoidea). Invertebr Biol 124: 174-184.
23. Smith MM, Cruz Smith L, Cameron RA, Urry LA, (2008) The larval stages of the sea urchin, Strongylocentrotus purpuratus. J Morphol 269: 713-733.
24. McCain ER, McClay DR, (1994) The establishment of bilateral asymmetry in sea urchin embryos. Development 120: 395-404.
25. Aihara M, Amemiya S, (2001) Left-right positioning of the adult rudiment in sea urchin larvae is directed by the right side. Development 128: 4935-4948.
26. Kitazawa C, Amemiya S, (2007) Micromere-derived signal regulates larval left-right polarity during sea urchin development. J Exp Zool A 307: 249-262.
27. Lapraz F, Rottinger E, Duboc V, Range R, Duloquin L, et al. (2006) RTK and TGF-beta signaling pathways genes in the sea urchin genome. Dev Biol 300: 132-152.
28. Angerer LM, Oleksyn DW, Logan CY, McClay DR, Dale L, et al. (2000) A BMP pathway regulates cell fate allocation along the sea urchin animal-vegetal embryonic axis. Development 127: 1105-1114.
29. Chen JH, Luo YJ, Su YH, (2011) The dynamic gene expression patterns of transcription factors constituting the sea urchin aboral ectoderm gene regulatory network. Dev Dyn 240: 250-260.
30. Duboc V, Rottinger E, Besnardeau L, Lepage T, (2004) Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev Cell 6: 397-410.
31. Lapraz F, Besnardeau L, Lepage T, (2009) Patterning of the dorsal-ventral axis in echinoderms: insights into the evolution of the BMP-chordin signaling network. PLoS Biol 7: e1000248 doi:10.1371/journal.pbio.1000248.
32. Saudemont A, Haillot E, Mekpoh F, Bessodes N, Quirin M, et al. (2010) Ancestral regulatory circuits governing ectoderm patterning downstream of Nodal and BMP2/4 revealed by gene regulatory network analysis in an echinoderm. PLoS Genet 6: e1001259 doi:10.1371/journal.pgen.1001259.
33. Su YH, Li E, Geiss GK, Longabaugh WJ, Kramer A, et al. (2009) A perturbation model of the gene regulatory network for oral and aboral ectoderm specification in the sea urchin embryo. Dev Biol 329: 410-421.
34. Davidson EH, Cameron RA, Ransick A, (1998) Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development 125: 3269-3290.
35. Tanaka S, Dan K, (1990) Study of the lineage and cell-cycle of small micromeres in embryos of the sea urchin, Hemicentrotus pulcherrimus. Dev Growth Differ 32: 145-156.
36. Voronina E, Lopez M, Juliano CE, Gustafson E, Song JL, et al. (2008) Vasa protein expression is restricted to the small micromeres of the sea urchin, but is inducible in other lineages early in development. Dev Biol 314: 276-286.
37. Juliano CE, Voronina E, Stack C, Aldrich M, Cameron AR, et al. (2006) Germ line determinants are not localized early in sea urchin development, but do accumulate in the small micromere lineage. Dev Biol 300: 406-415.
38. Yankura KA, Martik ML, Jennings CK, Hinman VF, (2010) Uncoupling of complex regulatory patterning during evolution of larval development in echinoderms. BMC Biol 8: 143.
39. Hibino T, Ishii Y, Levin M, Nishino A, (2006) Ion flow regulates left-right asymmetry in sea urchin development. Dev Genes Evol 216: 265-276.
40. Ransick A, Rast JP, Minokawa T, Calestani C, Davidson EH, (2002) New early zygotic regulators expressed in endomesoderm of sea urchin embryos discovered by differential array hybridization. Dev Biol 246: 132-147.
41. Tu Q, Brown CT, Davidson EH, Oliveri P, (2006) Sea urchin Forkhead gene family: phylogeny and embryonic expression. Dev Biol 300: 49-62.
42. Burke RD, Alvarez CM, (1988) Development of the esophageal muscles in embryos of the sea urchin Strongylocentrotus purpuratus. Cell Tissue Res 252: 411-417.
43. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, et al. (2008) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 4: 33-41.
44. Hibino T, Nishino A, Amemiya S, (2006) Phylogenetic correspondence of the body axes in bilaterians is revealed by the right-sided expression of Pitx genes in echinoderm larvae. Dev Growth Differ 48: 587-595.
45. Hao J, Daleo MA, Murphy CK, Yu PB, Ho JN, et al. (2008) Dorsomorphin, a selective small molecule inhibitor of BMP signaling, promotes cardiomyogenesis in embryonic stem cells. PLoS One 3: e2904 doi:.
46. Vogt J, Traynor R, Sapkota GP, (2011) The specificities of small molecule inhibitors of the TGFb and BMP pathways. Cell Signal 23: 1831-1842.
47. Morcos PA, Li Y, Jiang S, (2008) Vivo-Morpholinos: a non-peptide transporter delivers Morpholinos into a wide array of mouse tissues. Biotechniques 45: 613-614, 616, 618 passim.
48. Chablais F, Jazwinska A, (2010) IGF signaling between blastema and wound epidermis is required for fin regeneration. Development 137: 871-879.
49. Kowalik L, Hudspeth AJ, (2011) A search for factors specifying tonotopy implicates DNER in hair-cell development in the chick's cochlea. Dev Biol 354: 221-231.
50. Pehrson JR, Cohen LH, (1986) The fate of the small micromeres in sea urchin development. Dev Biol 113: 522-526.
51. Fujii T, Sakamoto N, Ochiai H, Fujita K, Okamitsu Y, et al. (2009) Role of the nanos homolog during sea urchin development. Dev Dyn 238: 2511-2521.
52. Juliano CE, Yajima M, Wessel GM, (2010) Nanos functions to maintain the fate of the small micromere lineage in the sea urchin embryo. Dev Biol 337: 220-232.
53. Boorman CJ, Shimeld SM, (2002) The evolution of left-right asymmetry in chordates. Bioessays 24: 1004-1011.
54. Yu JK, Holland LZ, Holland ND, (2002) An amphioxus nodal gene (AmphiNodal) with early symmetrical expression in the organizer and mesoderm and later asymmetrical expression associated with left-right axis formation. Evol Dev 4: 418-425.
55. Monteiro R, van Dinther M, Bakkers J, Wilkinson R, Patient R, et al. (2008) Two novel type II receptors mediate BMP signalling and are required to establish left-right asymmetry in zebrafish. Dev Biol 315: 55-71.
56. Furtado MB, Solloway MJ, Jones VJ, Costa MW, Biben C, et al. (2008) BMP/SMAD1 signaling sets a threshold for the left/right pathway in lateral plate mesoderm and limits availability of SMAD4. Genes Dev 22: 3037-3049.
57. Fujiwara T, Dehart DB, Sulik KK, Hogan BL, (2002) Distinct requirements for extra-embryonic and embryonic bone morphogenetic protein 4 in the formation of the node and primitive streak and coordination of left-right asymmetry in the mouse. Development 129: 4685-4696.
58. Schlange T, Arnold HH, Brand T, (2002) BMP2 is a positive regulator of Nodal signaling during left-right axis formation in the chicken embryo. Development 129: 3421-3429.
59. Piedra ME, Ros MA, (2002) BMP signaling positively regulates Nodal expression during left right specification in the chick embryo. Development 129: 3431-3440.
60. Chocron S, Verhoeven MC, Rentzsch F, Hammerschmidt M, Bakkers J, (2007) Zebrafish Bmp4 regulates left-right asymmetry at two distinct developmental time points. Dev Biol 305: 577-588.
61. Yajima M, Wessel GM, (2011) Small micromeres contribute to the germline in the sea urchin. Development 138: 237-243.
62. Sato K, Hayashi Y, Ninomiya Y, Shigenobu S, Arita K, et al. (2007) Maternal Nanos represses hid/skl-dependent apoptosis to maintain the germ line in Drosophila embryos. Proc Natl Acad Sci U S A 104: 7455-7460.
63. Suzuki H, Tsuda M, Kiso M, Saga Y, (2008) Nanos3 maintains the germ cell lineage in the mouse by suppressing both Bax-dependent and-independent apoptotic pathways. Dev Biol 318: 133-142.
64. Lai F, Singh A, King ML, (2012) Xenopus Nanos1 is required to prevent endoderm gene expression and apoptosis in primordial germ cells. Development 139: 1476-1486.
65. Wang HM, Tsang BK, (2007) Nodal signalling and apoptosis. Reproduction 133: 847-853.
66. Munir S, Xu G, Wu Y, Yang B, Lala PK, et al. (2004) Nodal and ALK7 inhibit proliferation and induce apoptosis in human trophoblast cells. J Biol Chem 279: 31277-31286.
67. Cameron RA, Samanta M, Yuan A, He D, Davidson E, (2009) SpBase: the sea urchin genome database and web site. Nucleic Acids Res 37: D750-D754.
68. Lasko PF, Ashburner M, (1990) Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev 4: 905-921.
69. Longabaugh WJ, Davidson EH, Bolouri H, (2009) Visualization, documentation, analysis, and communication of large-scale gene regulatory networks. Biochim Biophys Acta 1789: 363-374.