Conservation of dorsal ventral patterning in arthropods and chordates

Current Opinion in Genetics and Development

Volumn 6, Issue 4, 1996, Pages 424-431

  Ferguson, Edwin L ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA;

ARTHROPOD; CHORDATA; DEVELOPMENTAL GENETICS; DROSOPHILA; ECTODERM; EMBRYO; EMBRYO PATTERN FORMATION; EMBRYO POLARITY; GENE EXPRESSION REGULATION; MESODERM; NONHUMAN; PRIORITY JOURNAL; REVIEW; XENOPUS;

ARTHROPODA; CHORDATA;

EID: 0030219608     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(96)80063-3     Document Type: Article

References (72)

1. 1. Geoffrey-Saint-Hilaire E: Considérations générales sur la vertèbre. Mem du Mus Hist Nat 1822, 9:89-119. [Title translation: General observations on vertebrates.]
2. 2. Nübler-Jung K, Arendt D: Is ventral in insects dorsal in vertebrates? A history of embryological arguments favouring axis inversion in chordate ancestors. Roux Arch Dev Biol 1994, 203:357-366.
3. 3. Spemann H, Mangold H: Uber induktion von embryonalanlagen durch implantation artfremder organisatoren. Roux Arch f Entw mech 1924, 100:599-638. [Title translation: On the induction of embryonic form by implantation of organizers of foreign species.]
4. 4. St Johnston D, Nüsslein-Volhard C: The origin of pattern and polarity in the Drosophila embryo. Cell 1992, 68:201-219.
5. 5. Morisato D, Anderson KV: Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. Annu Rev Genet 1995, 29:371-399.
6. 6. Padgett RW, St Johnston RD, Gelbart WM: A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family. Nature 1987, 325:81-84.
7. 7. St Johnston RD, Gelbart WM: Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J 1987, 6:2785-2791.
8. 8. Ray RP, Arora K, Nüsslein-Volhard C, Gelbart WM: The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development 1991, 113:35-54.
9. 9. Irish VF, Gelbart WM: The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev 1987, 1:868-879.
10. 10. Ferguson EL, Anderson KV: Localized enhancement and repression of the activity of the TGF-β family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 1992, 114:583-597.
11. 11. Arora K, Nüsslein-Volhard C: Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes. Development 1992, 114:1003-1024.
12. 12. Ferguson EL, Anderson KV: Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 1992, 71:451-461.
13. 13. Wharton KA, Ray RP, Gelbart WM: An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 1993, 117:807-822.
14. 14. Nellen D, Burke R, Struhl G, Basler K: Direct and long-range action of a DPP morphogen gradient. Cell 1996, 85:357-368. Clones of cells that express dpp ectopically have long-range, dose-dependent effects on the expression of molecular markers in the developing wing. Clones of cells that express an activated dpp receptor ectopically, however, display only cell-autonomous effects on gene expression. These experiments strongly suggest that it is the cell non-autonomous effect of the dpp morphogen, and not a cascade of local cell interactions, that pattern the developing wing.
15. 15. François V, Solloway M, O'Neill JW, Emery J, Bier E: Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev 1994, 8:2602-2616.
16. 16. Holley SA, Jackson PD, Sasai Y, Lu B, De Robertis EM, Hoffmann FM, Ferguson EL: A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 1995, 376:249-253. Injection of sog mRNA promotes ventral fates in Drosophila and dorsal fates in Xenopus, whereas injection of chordin mRNA, which promotes dorsal fates in Xenopus [25], promotes ventral fates in Drosophila. Injection of dpp promotes ventral fates in Xenopus, and its effects are antagonized by injection of sog mRNA, demonstrating molecular conservation of dorsal-ventral patterning mechanisms between arthropods and chordates.
17. 17. Vincent JP, Gerhart JC: Subcortical rotation in Xenopus eggs: an early step in embryonic axis specification. Dev Biol 1987, 123:526-539.
18. 18. Boterenbrood EC, Nieuwkoop PD: The formation of the mesoderm in urodelan amphibians. V. Its regional induction by the endoderm. Wilhelm Roux Arch Dev Biol 1973, 173:319-332.
19. 19. Gimlich RL, Gerhart JC: Early cellular interactions promote embryonic axis formation in Xenopus laevis. Dev Biol 1984, 104:117-130.
20. 20. Dale L, Smith JC, Slack JMW: Mesoderm induction in Xenopus laevis: a quantitative study using a cell lineage label and tissue-specific antibodies. J Embryol Exp Morph 1985, 89:289-312.
21. 21. Jones EA, Woodland HR: The development of animal cap cells in Xenopus: a measure of the start of animal cap competence to form mesoderm. Development 1987, 101:557-563.
22. 22. Slack JMW: Inducing factors in Xenopus early embryos. Curr Biol 1994, 4:116-126.
23. 23. Smith JC, Slack JMW: Dorsalization and neural induction: properties of the organizer in Xenopus laevis. J Embryol Exp Morph 1983, 78:299-317.
24. 24. Smith WC, Harland RM: Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 1992, 70:829-840.
25. 25. Sasai Y, Lu B, Steinbeisser H, Geissert D, Gont LK, De Robertis EM: Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 1994, 79:779-790.
26. 26. Smith WC, Knecht AK, Wu M, Harland RM: Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm. Nature 1993, 361:547-549.
27. 27. Lamb TM, Knecht AK, Smith WC, Stachel SE, Economides AN, Stahl N, Yancopolous GD, Harland RM: Neural induction by the secreted polypeptide noggin. Science 1993, 262:713-718.
28. 28. Sasai Y, Lu B, Steinbeisser H, De Robertis EM: Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus. Nature 1995, 376:333-336. Overexpression of chordin at the mid-blastula transition causes explanted animal caps to adopt neural fates. Furthermore, the neuralizing activity of chordin can be antagonized by injection of a plasmid that expresses Bmp4 at gastrulation. Conversely, injection of antisense Bmp4 mRNA (but not Bmp2 mRNA) can cause neural differentiation. These results indicate that Bmp4 promotes epidermal cell fates and that chordin promotes neural development by antagonizing Bmp4 activity. The results of this paper and [51•,52,54•] indicate that neuronal differentiation is the default state within the ectoderm.
29. 29. François V, Bier E: Xenopus chordin and Drosophila short gastrulation genes encode homologous proteins functioning in dorsal-ventral axis formation. Cell 1995, 80:19-20.
30. 30. De Robertis EM, Sasai Y: A unity of plan for dorso-ventral patterning in the development of animal species. Nature 1996, 380:37-40.
31. 31. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA: Novel regulators of bone formation: molecular clones and activities. Science 1988, 242:1528-1534.
32. 32. Fainsod A, Steinbeisser H, De Robertis EM: On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J 1994, 13:5015-5025.
33. 33. Schmidt JE, Suzuki A, Ueno N, Kimelman D: Localized BMP-4 mediates dorsal/ventral patterning in the early Xenopus embryo. Dev Biol 1995, 169:37-50. The authors focus on the role of Bmp4 at the early gastrula stage, examining the expression of Bmp4 and the effect of injection of Bmp4 and dominant negative Bmp4 receptors. In situ hybridization of various probes - goosecoid, myoD, Xwnt8, and Hairy II-demonstrates that alterations in Bmp4 activity perturb patterning in the gastrula and neurula stages. Strikingly, genes expressed in ventro-lateral positions of the mesoderm, such as myoD and Xwnt8, were downregulated by injection of Bmp4, suggesting that these genes may respond to a specific threshold of Bmp4 activity.
34. 34. Re'em-Kalma Y, Lamb T, Frank D: Competition between noggin and bone morphogenetic protein 4 activities may regulate dorsalization during Xenopus development. Proc Natl Acad Sci USA 1995, 92:12141-12145. Elevation of Bmp4 activity in ventral mesoderm inhibits noggin's ability to dorsalize mesoderm, however ectopic noggin downregulates Bmp4 transcription in lateral mesoderm. Thus, antagonism between noggin and Bmp4 may control the lateral extent of dorsalization within the marginal zone.
35. 35. Hemmati-Brivanlou A, Thomsen GH: Ventral mesodermal patterning in Xenopus embryos: expression patterns and activities of BMP-2 and BMP-4. Dev Genet 1995, 17:78-89.
36. 36. Köster M, Plessow S, Clement JH, Lorenz A, Tiedemann H, Knöchel W: Bone morphogenetic protein 4 (BMP-4), a member of the TGF-β family, in early embryos of Xenopus laevis: analysis of mesoderm inducing activity. Mech Dev 1991, 33:191-199.
37. 37. Dale L, Howes G, Price BM, Smith JC: Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development. Development 1992, 115:573-585.
38. 38. Jones CM, Lyons KM, Lapan PM, Wright CV, Hogan BL: DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction. Development 1992, 115:639-647.
39. 39. Jones CM, Dale L, Hogan BLM, Wright CVE, Smith JC: Bone morphogenetic protein-4 (BMP-4) acts during gastrula stages to cause ventralization of Xenopus embryos. Development 1996, 122:1545-1554. The authors use three criteria to demonstrate that Bmp4 acts during the gastrula stage to promote ventral fates within the mesoderm. First, activation of organizer-specific genes occurs normally after Bmp4 mRNA injection but the organizer genes are then rapidly downregulated. Second, Spemann's organizer grafts cannot rescue embryos ventralized with Bmp4 mRNA. Third, the dorsalizing effects of the organizer can be counteracted by Bmp4 mRNA injection. These results establish that Bmp4 is involved in patterning preexisting mesoderm, rather than inducing mesoderm with a ventral character.
40. 40. Padgett RW, Wozney JM, Gelbart WM: Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc Natl Acad Sci USA 1993, 90:2905-2909.
41. 41. Schmidt JE, François V, Bier E, Kimelman D: Drosophila short gastrulation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning. Development 1995, 121:4319-4328. Injection of sog mRNA into Xenopus embryos expands neurogenic and dorsal mesodermal cell tissues, as evidenced by changes in the pattern of gene expression at the gastrula stage, and can induce a partial secondary axis. These results, in conjunction with [16••], demonstrate conservation of the system for dorsal-ventral patterning between arthropods and chordates.
42. 42. Staehling-Hampton K, Hoffmann FM, Baylies MK, Rushton E, Bate M: dpp induces mesodermal gene expression in Drosophila. Nature 1994, 372:783-786.
43. 43. Frasch M: Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 1995, 374:464-467.
44. 44. Gerhart J: Johannes Holtfreter's contributions to ongoing studies of the organizer. Dev Dyn 1996, 205:245-256.
45. 45. Graff JM, Thies RS, Song JJ, Celeste AJ, Melton DA: Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 1994, 79:169-179.
46. 46. Suzuki A, Thies RS, Yamaji N, Song JJ, Wozney JM, Murakami K, Ueno N: A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc Natl Acad Sci USA 1994, 91:10255-10259.
47. 47. Maeno M, Ong RC, Suzuki A, Ueno N, Kung HF: A truncated bone morphogenetic protein 4 receptor alters the fate of ventral mesoderm to dorsal mesoderm: roles of animal pole tissue in the development of ventral mesoderm. Proc Natl Acad Sci USA 1994, 91:10260-10264.
48. 48. Steinbeisser H, Fainsod A, Niehrs C, Sasai Y, De Robertis EM: The role of gsc and BMP-4 in dorsal-ventral patterning of the marginal zone in Xenopus: a loss of function study using antisense RNA. EMBO J 1995, 14:5230-5243. Injection of antisense Bmp4 mRNA rescues axis development in ventralized embryos and dorsalizes wild-type embryos. Antisense Bmp4 constructs dorsalize ventral marginal zone explants, causing them to express lateral muscle-specific markers while repressing expression of more ventral markers, such as globin.
49. 49. Godsave SF, Slack JM: Clonal analysis of mesoderm induction in Xenopus laevis. Dev Biol 1989, 134:486-490.
50. 50. Grunz H, Tacke L: Neural differentiation of Xenopus laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. Cell Diff Devel 1989, 28:211-217.
51. 51. Wilson PA, Hemmati-Brivanlou A: Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 1995, 376:331-333. Application of BMP4 protein to disassociated animal cap cells, which would normally adopt a neural fate, causes these cells to become epidermis. These results indicate that disassociation of animal cap cells abrogates endogenous Bmp4 activity and directly demonstrate that BMP4 induces epidermal fates. This paper also shows that dominant-negative activin receptors, which promote neural fates, do so by blocking Bmp4 signaling.
52. 52. Suzuki A, Shioda N, Ueno N: Bone morphogenetic protein acts as a ventral mesoderm modifier in early Xenopus embryos. Dev Growth Diff 1995, 37:581-588.
53. 53. Xu RH, Kim J, Taira M, Zhan S, Sredni D, Kung HF: A dominant negative bone morphogenetic protein 4 receptor causes neuralization in Xenopus ectoderm. Biochem Biophys Res Commun 1995, 212:212-219.
54. 54. Hawley SHB, Wünnenberg-Stapleton K, Hashimoto C, Laurent MN, Watabe T, Blumberg BW, Cho KWY: Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev 1995, 9:2923-2935. Injection of mRNAs encoding dominant negative forms of Bmp4 or Bmp7 (but not activin) proteins with mutated cleavage sites caused formation of a second body axis in whole embryos and formation of neural structures in explanted animal caps. These results extend the observations of [45,46] that loss of Bmp4 activity promotes dorsal mesodermal structures in the absence of the organizer and directly demonstrate that Bmp4 activity is required for the production of epidermal fates within animal cap ectoderm.
55. 55. Kingsley DM: The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 1994, 8:133-146.
56. 56. Massagué J, Attisano L, Wrana JL: The TGF-β family and its composite receptors. Trends Cell Biol 1994, 4:172-178.
57. 57. Wrana JL, Attisano L, Wieser R, Ventura F, Massagué J: Mechanism of activation of the TGF-β receptor. Nature 1994, 370:341-347.
58. 58. Letsou A, Arora K, Wrana JL, Simin K, Twombly V, Jamal J, Staehling-Hampton K, Hoffmann FM, Gelbart WM, Massagué J, O'Connor MB: Drosophila Dpp signaling is mediated by the punt gene product: a dual ligand-binding type II receptor of the TGF-β receptor family. Cell 1995, 80:899-908.
59. 59. Ruberte E, Marty T, Nellen D, Affolter M, Basler K: An absolute requirement for both the type II and type I receptors, punt and thick veins, for dpp signaling in vivo. Cell 1995, 80:889-897.
60. 60. Brummel TJ, Twombly V, Marques G, Wrana JL, Newfeld SJ, Attisano L, Massagué J, O'Connor MB, Gelbart WM: Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 1994, 78:251-261.
61. 61. Nellen D, Affolter M, Basler K: Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 1994, 78:225-237.
62. 62. Penton A, Chen Y, Staehling-Hampton K, Wrana JL, Attisano L, Szidonya J, Cassill JA, Massagué J, Hoffmann FM: Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor. Cell 1994, 78:239-250.
63. 63. Xie T, Finelli AL, Padgett RW: The Drosophila saxophone gene: a serine-threonine kinase receptor of the TGF-β superfamily. Science 1994, 263:1756-1759.
64. 64. Arora K, Levine MS, O'Connor MB: The screw gene encodes a ubiquitously expressed member of the TGF-β family required for specification of dorsal cell fates in the Drosophila embryo. Genes Dev 1994, 8:2588-2601.
65. 65. Raftery LA, Twombly V, Wharton K, Gelbart WM: Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics 1995, 139:241-254.
66. 66. Sekelsky JJ, Newfeld SJ, Raftery LA, Chartoff EH, Gelbart WM: Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 1995, 139:1347-1358.
67. 67. Savage C, Das P, Finelli A, Townsend S, Sun C, Baird S, Padgett R: Caenorhabditis elegans genes sma-2, sma-3, and sma-4 define a conserved family of TGF-β pathway components. Proc Natl Acad Sci USA 1996, 93:790-794.
68. 68. Hahn SA, Schutte M, Hoque ATMS, Moskaluk CA, Da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH, Kern SE: DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 1996, 271:350-353.
69. 69. Graff JM, Bansal A, Melton DA: Xenopus Mad proteins transduce distinct subsets of signals for the TGFβ superfamily. Cell 1996, 85:479-487. Using PCR technology, the authors identify multiple homologues of the Drosophila Mad gene in Xenopus. They then demonstrate that certain Mad homologues promote dorsal development, as assayed by gene expression after mRNA injection, whereas other homologues promote ventral development. Because different TGF-β family members promote dorsal and ventral development in Xenopus, the authors speculate that individual MAD-like proteins may transduce signals from individual TGF-β family members during embryogenesis.
70. 70. Newfeld SJ, Chartoff EH, Graff JM, Melton DA, Gelbart WM: Mothers against dpp encodes a conserved cytoplasmic protein required in DPP/TGF-β responsive cells. Development 1996, in press.
71. 71. Hoodless PA, Haerry T, Abdollah S, Stapleton M, O'Connor MB, Attisano L, Wrana JL: MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 1996, 85:489-500. Mad mutations partially suppress the phenotypes caused by constitutively-active forms of the dpp receptor, strongly suggesting that Mad acts downstream of the dpp receptor. A vertebrate MAD-related protein, MADR1, is rapidly phosphorylated upon Bmp2 receptor activation. Furthermore, mutant analysis indicates that phosphorylation is essential for function. MADR1 translocates from the cytoplasm to the nucleus after receptor activation, and thus Mad may encode one of the most downstream genes in the TGF-β signaling pathway.
72. 72. Slack JMW, Holland PWH, Graham CF: The zootype and the phylotypic stage. Nature 1993, 361:490-492.