Origin of the metazoan bodyplan: Characterization and functional testing of the promoter of the homeobox gene EmH-3 from the freshwater sponge Ephydatia muelleri in mouse 3T3 cells

Biological Chemistry

Volumn 379, Issue 10, 1998, Pages 1243-1251

  Coutinho, Cristiano C ^a,b   Seack, Jürgen ^a   Van Vyver, Gisèle De ^c   Borojevic, Radovan ^b   Müller, Werner E G ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Homeobox; Homeodomain containing proteins; Molecular evolution; Phylogeny; Porifera; Promoter; Sponges

Indexed keywords

COMPLEMENTARY DNA; LUCIFERASE; STRUCTURAL PROTEIN; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ANATOMY; ARTICLE; CELL STRAIN 3T3; DNA LIBRARY; DNA SEQUENCE; DNA TRANSFECTION; GENE EXPRESSION SYSTEM; HOMEOBOX; METAZOON; MOLECULAR CLONING; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; SPONGE (PORIFERA); TATA BOX; TRANSCRIPTION REGULATION;

EPHYDATIA MUELLERI; INVERTEBRATA; MAMMALIA; METAZOA; PORIFERA; SPONGILLIDAE;

EID: 0031786993     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/bchm.1998.379.10.1243     Document Type: Article

References (70)

1. Ausubel, P.M., Brent, R., Kingston, R.E., Moore, D.D., Smith, J.A., Seidmann, J.G., and Struhl, K. (1995). Current Protocols in Molecular Biology. (New York: John Wlley and Sons).
2. Bucher, P. (1990). Weight matrix description of four eukaryotic RNA polymerase II promotor elements derived from 502 unrelated promotor sequences. J. Mol. Biol. 212, 563-578.
3. Bürglin, T.R. (1994). A comprehensive classification of homeobox genes. In: Guidebook to the Homeobox Genes. D. Duboule, ed. (Oxford, UK: A Sambrook and Tooze Publication at Oxford University Press), pp. 27-71.
4. Carroll, S.B. (1995). Homeotic genes and the evolution of arthropods and chordates. Nature 376, 479-485.
5. Cavalier-Smith, T., Allsopp, M.T.E.P, Chao, E.E., Boury-Esnault, N., and Vacelet, J. (1996). Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rRNA evidence. Can. J. Zool. 74, 2031-2045.
6. Conway Morris, S. (1993). The fossil record and the early evolution of the Metazoa. Nature 361, 219-225.
7. Coutinho, C.C., Richelle-Maurer, E., Van de Vyver G., and Visser, S. (1994). Evidence of homeobox genes in freshwater sponge Ephhydatia fluviatilis. In: Sponges in Time and Space. R.W.M. van Soest, T.M.G. Van Kempen and J.C. Braekman, eds. (Rotterdam, The Netherlands: Balkema Press), pp. 385-388.
8. Davidson, E.H. (1989). Lineage-specific gene expression and its regulative capacities of the sea urchin embryo: a proposed mechanism. Develop. 105, 421-445.
9. Davidson, E.H., Peterson, K.J., and Cameron, R.A. (1995). Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270, 1319-1325.
10. Dayhoff, M.O., Schwarte, R.M., and Orcutt, B.C. (1978). A model of evolutionary change in protein. In: Atlas of Protein Sequence and Structure, Vol. 5, Suppl. 3. M.O. Dayhoff, ed. (Washington, DC.: Nat. Biomed. Res. Foundation), pp. 345-352.
11. Degnan, B.M., Degnan, S.M., Giusti, A., and Morse, D.E. (1995). A hox/nom homeobox gene in sponges. Gene 755, 175-177.
12. Duboule, D. (ed.) (1989). Guidebook to the Homeobox Genes. A Sambrook and Tooze Publication (Oxford, UK: Oxford University Press).
13. Emery, I.F., Bedian, V., and Guild, G.M. (1994). Differential expression of Broad-Complex transcription factor. Development 120, 3275-3287.
14. Exposito, J.Y., and Garrone, R. (1990). Characterization of afibrillar collagen gene in sponges reveals the early evolutionary appearance of two collagen families. Proc. Natl. Acad. Sci. USA 87, 6669-6673.
15. Felsenstein, J. (1993). PHYLIP, ver 3.5. University of Washington, Seattle.
16. Garcia-Fernàndes, J., and Holland, P.W.H. (1994). Archetypal organisation of the amphioxus Hox gene cluster Nature 370, 563-566.
17. Gehring, W.J., Müller, M., Affolter, M., Percival-Smith, A., Billeter, M., Qian, Y.Q., Otting, G., and Wüthrich, K. (1990). The structure of the homeodomain and its functional implications. Trends Genet. 6, 323-329.
18. Han, T.M., and Runnegar, B. (1992). Megascopic eukaryotic algae from the 2.1 billion-year-old Negaunee Iron-Formation, Michigan. Science 257, 232-235.
19. Harley, V.R., Jackson, D.I., Hextall, P.J., Hawkins, U.R., Berkovitz, G.D., Sockanathan, S., Lovell-Badge, R., and Goodfellow, P.N. (1992). DNA binding activity of recombinant SRY from normal males and XYfemales. Science 255, 453-456.
20. Higashijima, S., Kojima, T., Michlue, T., Ishimaru, S., Emori, Y., and Salgo, K. (1992). Dual Bar homeo box genes of Drosophila required in two photoreceptor cells, R1 and R6, and primary pigment cells for normal eye development. Genes Dev. 6, 50-60.
21. Holland, P., Ingham P., and Krauss, S.P. (1988). Development and evolution. Mice and flies head to head. Nature 358, 687-690.
22. Kappen, C., Schughart, K., and Ruddle, F.H. (1993). Early evolutionary origin of major homeodomain sequence classes. Genomics 18, 54-70.
23. Kaufmann, E., Hoch, M., and Jäckle, H. (1994). The interaction of DNA with the DNA-binding domain encoded by the Drosophila gene fork head. Eur. J. Biochem. 223, 329-337.
24. Kennedy, M.A., Gonzales-Sarmiento, R., Kees, U.R., Lampert, F., Dear, N., Boehm, T., and Rabbitts, T.H. (1991). HOX11, a homeobox-containing T-cell oncogene on human chromosome 10q24. Proc. Natl. Acad. Sci. USA 88, 8900-8904.
25. Kojima, T., Ishimaru, S., Higashijima, S., Takayama, E., Akimaru, H., Sone, M., Emori, Y., and Saigo, K. (1991). Identification of a different-type homeobox gene, BarH1, possibly causing Bar (B) and Om (1D) mutations in Drosophila. Proc. Natl. Acad. Sci. USA 88, 4343-4347.
26. Kozak, M. (1991). An analysis of vertebrate mRNA sequences: Intimations of translational control. J. Cell Biol. 115, 887-903.
27. Koziol, C., Borojevic, R., Steffen, R., and Müller, W.E.G. (1998). Sponges (Porifera) model systems to study the shift from immortal- to senescent somatic cells: the telomerase activity in somatic cells. Mech. Ageing Develop. 100, 107-120.
28. Lévi, C. (1956). Etude des Halisarca de Roscoff. Embryologie et systematique des demosponges. Arch. Zool. Exp. Gén. 93, 1-181.
29. Lu, M., Gong, Z.Y. and Ho, A.D. (1991).The tcl-3proto-oncogene altered by chromosomal translocation in T-cell leukemia codes for a homeobox protein. EMBO J. 10, 2905-2910.
30. Maas, R. (1983). An Improved colony hybridisation method with significantly increased sensitivity for detection of single genes. Plasmid 10, 296-298.
31. Margalit, Y., Yarus, S., Shapira, E., Gruenbaum, Y., and Fainsod, A. (1993). Isolation and characterization of the target sequences of the chicken CdxA homeobox gene. Nucl. Acids Res. 21, 4915-4922.
32. Martin, D.I., and Orkin, S.H. (1990). Transcription and DNA binding by the erythroid factor GF-1/NF-E1/Eryf 1. Genes Dev. 4, 1886-1898.
33. McGinnis, W., and Krumlauf, R. (1992). Homeobox genes and axial patterning. Cell 68, 283-302.
34. Mehlhorn, H. (ed.) (1989). Grundriβ der Zoologie. (Stuttgart, Germany: G. Fischer).
35. Merika, M., and Orkin, S.H. (1993). DNA-specificity of GATA family transcription factors. Mol. Cell. Biol. 13, 3999-4010.
36. Molnar, A., and Georgopoulos, K. (1994). The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol. Cell. Biol. 14, 8292-8303.
37. Müller, W.E.G. (1995). Molecular phylogeny of metazoa [animals]: monophyletic origin. Naturwiss. 82, 321-329.
38. Müller, W.E.G. (1998a). Molecular phylogeny of Eumetazoa: experimental evidence for monophyly of animals based on genes in sponges [Porifera]. Progr. Molec. Subcell. Biol. 19, 89-132.
39. Müller, W.E.G. (ed.) (1998b). Molecular Evolution: Evidence for Monophyly of Metazoa. Progr. Molec. Subcell. Biol. Vol. 19 (Berlin, Germany: Springer), pp. 89-132.
40. Müller, W.E.G., Perovic, S., Krasko, A., and Meesters, E. (1997). Nachweis neuronaler Elemente in Zellen des Meeresschwammes Geodia cydonium, BioSpektrum3, 81-83.
41. Müller, W.E.G., Coutinho, C.C., Müller, I.M., Gamulin, V., Kavsan, V., Kruse, M., and Skorokhod, A. (1998). Monophyly of Metazoa: Phylogenetic analyses of genes encoding Ser/Thr-kinases and a receptor Tyr-kinase from Porifera [sponges]. 7th Senckenberg Symp. - Courier Research Institute Senckenberg (C.F.S.), in press.
42. Nicholas, K.B., and Nicholas, H.B. Jr. (1996). GeneDoc version 1.1.004.
43. Overdier, D.G., Porcella, A., and Costa, R.H. (1994). The DNA-binding specificity of the hepatocyte nuclear factor 3/forkhead domain is influenced by amino-acid residues adjacent to the recognition helix. Mol. Cell. Biol. 14, 2755-2766.
44. Pahler, S., Krasko, A., Schütze, J., Müller, I.M., and Müller, W.E.G. (1998). Isolation and characterization of a cDNA encoding a potential morphogen from the marine sponge Geodia cydonium, that is conserved in higher metazoans. Royal Society Lond., B 265, 421-425.
45. Pancer, Z., Kruse, M., Müller, I., and Müller, W.E.G. (1997a). On the origin of adhesion receptors of metazoa: cloning of the integrin α subunit cDNA from the sponge Geodia cydonium. Molec. Biol. Evol. 74, 391-398.
46. Pancer, Z., Münkner, J., Müller, I., and Müller, W.E.G. (1997b). A novel member of an ancient superfamily: sponge (Geodia cydonium, Porifera) putative protein that features scavenger receptor cysteine-rich repeats. Gene 793, 211-218.
47. Parikh, H., Shah, S., Hilt, D., and Peterkofshy, A. (1995). Organization, sequence and regulation of expression of the murine Hoxa-7 gene. Gene 754, 237-242.
48. Pfeifer, K., Haasemann, M., Gamulin, V., Bretting, H., Fahrenholz, F., and Mutier, W.E.G. (1993). S-type lectins occur also in inver- tebrates: high conservation of the carbohydrate recognition domain in the lectin genes from the marine sponge Geodia cydonium. Glycobiol. 3, 179-184.
49. Pontiggia, A., Rimini, R., Harley, V.R., Goodfellow, P.N., Lovell-Badge, R., and Bianchi, M.E. (1994). Sex-reversing mutations affect the architecture of SRY-DNA complexes. EMBO J. 13, 6115-6124.
50. Richelle-Maurer, E., Van de Vyver, G., Visser, S., and Coutinho, C.C. (1998). Homeobox-containlng genes In freshwater sponges: characterization, expression, and phylogeny. Progr. Molec. Subcell. Biol. 79, 157-175.
51. Rocancourt, D., Bonnerot, C., Jouin, H., Emerman, M., and Nicolas, J.F. (1990). Activation of a beta-galactosidase recombinant provirus: application to titration of human Immunodeficiency virus (HIV) and HIV-infected cells. J. Virol. 64, 2660-2668.
52. Runnegar, B. (1985). Collagen gene construction and evolution. J. Mol. Evol. 22, 141-149.
53. Sanger, F., Nicklen, S., and Coulson, A.R. (1977). DMA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463-5457.
54. Schäcke, H., Müller, W.E.G., Gamulin, V., and Rinkevich, B. (1994a). The Ig superfamily includes members from the lowest invertebrates to the highest vertebrates. Immunology Today 15, 497-498.
55. Schacke, H., Rinkevich, B., Gamulin, V., Müller, I.M., and Müller, W.E.G. (1994b). Immunoglobulin-llke domain is present in the extracellular part of the receptor tyrosine kinase from the marine sponge Geodia cydonium. J. Molec. Recognition 7, 272-276.
56. Scheffer, U., Krasko, A., Pancer, Z., and Müller, W.E.G. (1997). Isolation and characterization of the cDNA clone encoding the serum response factor homolog in the marine sponge Geodia cydonium: high conservation of this transcription factor within Metazoa. Biol J. Linnean Soc. 61, 127-137.
57. Schubert, F.R., Nieselt-Struwe, K., and Gruss, P. (1993). The Antennapedia-type homeobox genes have evolved from three precursors separately early in metazoan evolution. Proc. Natl. Acad. Sci. USA 90, 143-147.
58. Schummer, M., Scheurlen, I., Schaller, C., and Galliot, B. (1992). HOM/HOX homeobox genes are present in hydra (Chlorohydra viridis) and are differentially expressed during regeneration. EMBO J. 11, 1815-1823.
59. Seack, J., Kruse, M., and Müller, W.E.G. (1998). Evolutionary analysis of G-proteins in early metazoans: Cloning of α- and β-subunits from the sponge Geodia cydonium. Biochim. Biophys. Acta 1401, 93-103.
60. Seimiya, M., Ishiguro, H., Miura, K., Watanabe, Y., and Kurosawa, Y. (1994). Homeobox-containing genes in the most primitive Metazoa, the sponge. Eur. J. Biochem. 227, 219-225.
61. Seimiya, M., Naito, M., Watanabe, Y., and Kurosawa, Y (1998). Homeobox genes in the freshwater sponge Ephydatia fluviatilis. Progr. Molec. Subcell. Biol. 19, 133-155.
62. Simpson, T.L. (1984). The Cell Biology of Sponges. (New York: Springer).
63. Slack, J.M.W. (1987). Morphogenetic gradients - past and present. Trends Biochem. Sci. 12, 200-204.
64. Steiner, M., Mehl, D., Reitner, J., and Erdtmann, B.D. (1993). Oldest entirely preserved sponges and other fossils from the Lowermost Cambrian and a new facies reconstruction of the Yangtze Platform (China). Berliner Geowiss. Abh. (E) 9, 293-329.
65. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nuc. Acids Res. 22, 4673-4680.
66. Tissier-Seta, J.P., Muchielli, M.L., Mark, M., Mattei, M.G., Goridls, C., and Brunet, J.F. (1995). Barx1, a new mouse homeodomain transcription factor expressed in cranio-facial ectomes-enchyme and the stomach. Mech. Dev. 51, 3-15.
67. Valentine, J.W. (1994). Late precambrian bilaterians: grades and clades. Proc. Natl. Acad. Sci. USA 91, 6751-6757.
68. von Kalm, L., Crossgrove, K., Seggern, D. v., Guild, G.M., and Beckendorf, S.K. (1994). The Broad-Complex directly controls a tissue-specific response to the steroid hormone receptor at the onset of Drosophila melanogaster. EMBO J. 13, 3505-3516.
69. Willmer, P. (1994). Invertebrate Relationships. (Cambridge, UK: Cambridge University Press).
70. Wray, G.A., Levinton, J.S., and Shapiro, L.H. (1996). Molecular evidence for deep Precambrian divergences among metazoan phyla. Science 274, 568-573.