Development Genes and Evolution

, Volume 218, Issue 3–4, pp 203–213 | Cite as

TGFβ signaling in Tribolium: vertebrate-like components in a beetle

  • Maurijn Van der Zee
  • Rodrigo Nunes da Fonseca
  • Siegfried Roth
Original Article

Abstract

The cytokines of the TGFβ superfamily are highly conserved in evolution and elicit a diverse range of cellular responses in all metazoa. In Drosophila, the signaling pathways of the two TGFβ subfamilies, Activins and Bone Morphogenetic Proteins (BMPs), have been well studied. To address the question of whether the findings from Drosophila are representative of insects in general, we analyzed the components of TGFβ-signaling present in the genome of the beetle Tribolium castaneum. We were able to identify orthologs of the BMPs Decapentaplegic and Glass bottom boat, of the Activins Activinβ and Dawdle, as well as orthologs of the less well-known ligands Myoglianin and Maverick, together with orthologs of all TGFβ receptors and cytoplasmic signal transducers present in Drosophila. This indicates that the diversity of TGFβ signaling components is generally well conserved between Drosophila and Tribolium. However, the genome of the beetle—and of the bee Apis mellifera—lacks an ortholog of the Drosophila BMP Screw but does contain a vertebrate-like BMP10 homolog which is not found in Drosophila. Concerning BMP inhibitors, Tribolium displays an even more vertebrate-like ensemble of components. We found two orthologs of the vertebrate DAN family, Dan and Gremlin, and show embryonic expression of a vertebrate-like BAMBI ortholog, all of which are absent in Drosophila. This suggests that Tribolium might have retained a more ancestral composition of TGFβ signaling components and that TGFβ signaling underwent considerable change in the Drosophila lineage. Tribolium is an excellent model to study the function of these ancestral signaling components in insects.

Keywords

Tribolium castaneum Red flour beetle BMP signaling Activin signaling Phylogeny 

Supplementary material

427_2007_179_MOESM1_ESM.doc (64 kb)
ESM(DOC 63.5 kb)

References

  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Annes JP, Munger JS, Rifkin DB (2003) Making sense of latent TGFbeta activation. J Cell Sci 116:217–224PubMedCrossRefGoogle Scholar
  4. Arora K, Levine MS, O’Connor MB (1994) The screw gene encodes a ubiquitously expressed member of the TGF-beta family required for specification of dorsal cell fates in the Drosophila embryo. Genes Dev 8:2588–2601PubMedCrossRefGoogle Scholar
  5. Bangi E, Wharton K (2006a) Dpp and Gbb exhibit different effective ranges in the establishment of the BMP activity gradient critical for Drosophila wing patterning. Dev Biol 295:178–193PubMedCrossRefGoogle Scholar
  6. Bangi E, Wharton K (2006b) Dual function of the Drosophila Alk1/Alk2 ortholog Saxophone shapes the BMP activity gradient in the wing imaginal disc. Development 133:3295–303PubMedCrossRefGoogle Scholar
  7. Canty EG, Garrigue-Antar L, Kadler KE (2006) A complete domain structure of Drosophila tolloid is required for cleavage of short gastrulation. J Biol Chem 281:13258–13267PubMedCrossRefGoogle Scholar
  8. Capdevila J, Tsukui T, Rodriquez E.C, Zappavigna V, Izpisua Belmonte JC, (1999) Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol Cell 4:839–849PubMedCrossRefGoogle Scholar
  9. Chen H, Shi S, Acosta L, Li W, Lu J, Bao S, Chen Z, Yang Z, Schneider MD, Chien KR et al (2004) BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131:2219–31PubMedCrossRefGoogle Scholar
  10. Dorfman R, Shilo BZ (2001) Biphasic activation of the BMP pathway patterns the Drosophila embryonic dorsal region. Development 128:965–972PubMedGoogle Scholar
  11. Enomoto H, Ozaki T, Takahashi E, Nomura N, Tabata S, Takahashi H, Ohnuma N, Tanabe M, Iwai J, Yoshida H et al (1994) Identification of human DAN gene, mapping to the putative neuroblastoma tumor suppressor locus. Oncogene 9:2785–2791PubMedGoogle Scholar
  12. Feng XH, Derynck R (2005) Specificity and versatility in TGF-signaling through Smads. Annu Rev Cell Dev Biol 21:659–693PubMedCrossRefGoogle Scholar
  13. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548PubMedGoogle Scholar
  14. Gazzerro E, Pereira RC, Jorgetti V, Olson S, Economides AN, Canalis E (2005) Skeletal overexpression of gremlin impairs bone formation and causes osteopenia. Endocrinology 146:655–665PubMedCrossRefGoogle Scholar
  15. Gerlach-Bank LM, Cleveland AR, Barald KF (2004) DAN directs endolymphatic sac and duct outgrowth in the avian inner ear. Dev Dyn 229:219–230PubMedCrossRefGoogle Scholar
  16. Gilbert SF, Bolker JA (2001) Homologies of process and modular elements of embryonic construction. J Exp Zool 291:1–12PubMedCrossRefGoogle Scholar
  17. Giorgianni MW, Patel NH (2004) Patterning of the branched head appendages in Schistocerca americana and Tribolium castaneum. Evol Dev 6:402–410PubMedCrossRefGoogle Scholar
  18. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  19. Herpin A, Lelong C, Favrel P (2004) Transforming growth factor-beta-related proteins: an ancestral and widespread superfamily of cytokines in metazoans. Dev Comp Immunol 28:461–485PubMedCrossRefGoogle Scholar
  20. Hsu DR, Economides AN, Wang X, Eimon PM, Harland RM (1998) The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol Cell 1:673–683PubMedCrossRefGoogle Scholar
  21. Huse M, Chen YG, Massague J, Kuriyan J (1999) Crystal structure of the cytoplasmic domain of the type I TGF beta receptor in complex with FKBP12. Cell 96:425–436PubMedCrossRefGoogle Scholar
  22. Joubin K, Stern CD (1999) Molecular interactions continuously define the organizer during the cell movements of gastrulation. Cell 98:559–571PubMedCrossRefGoogle Scholar
  23. Kawase E, Wong MD, Ding BC, Xie T (2004) Gbb/BMP signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131:1365–1375PubMedCrossRefGoogle Scholar
  24. Kingsley DM (1994) The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 8:133–146PubMedCrossRefGoogle Scholar
  25. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  26. Lee-Hoeflich ST, Zhao X, Mehra A, Attisano L (2005) The Drosophila type II receptor, Wishful thinking, binds BMP and myoglianin to activate multiple TGFbeta family signaling pathways. FEBS Lett 579:4615–4621PubMedCrossRefGoogle Scholar
  27. Lele Z, Nowak M, Hammerschmidt M (2001) Zebrafish admp is required to restrict the size of the organizer and to promote posterior and ventral development. Dev Dyn 222:681–687PubMedCrossRefGoogle Scholar
  28. Lo RS, Chen YG, Shi Y, Pavletich NP, Massague J (1998) The L3 loop: a structural motif determining specific interactions between SMAD proteins and TGF-beta receptors. EMBO J 17:996–1005PubMedCrossRefGoogle Scholar
  29. Lopez-Coviella I, Follettie MT, Mellott TJ, Kovacheva VP, Slack BE, Diesl V, Berse B, Thies RS, Blusztajn JK (2005) Bone morphogenetic protein 9 induces the transcriptome of basal forebrain cholinergic neurons. Proc Natl Acad Sci USA 102:6984–6989PubMedCrossRefGoogle Scholar
  30. Lopez-Coviella I, Mellott TM, Kovacheva VP, Berse B, Slack BE, Zemelko V, Schnitzler A, Blusztajn JK (2006) Developmental pattern of expression of BMP receptors and Smads and activation of Smad1 and Smad5 by BMP9 in mouse basal forebrain. Brain Res 1088:49–56PubMedCrossRefGoogle Scholar
  31. Lowe CJ, Terasaki M, Wu M, Freeman RM, Jr., Runft L, Kwan K, Haigo S, Aronowicz J, Lander E, Gruber C et al (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol 9:e291CrossRefGoogle Scholar
  32. Lu MM, Yang H, Zhang L, Shu W, Blair DG, Morrisey, EE (2001) The bone morphogenic protein antagonist gremlin regulates proximal–distal patterning of the lung. Dev Dyn 222:667–680PubMedCrossRefGoogle Scholar
  33. Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–W331PubMedCrossRefGoogle Scholar
  34. Marques G (2005) Morphogens and synaptogenesis in Drosophila. J Neurobiol 64:417–434PubMedCrossRefGoogle Scholar
  35. Massague J, Chen YG (2000) Controlling TGF-beta signaling. Genes Dev 14:627–644PubMedGoogle Scholar
  36. Massague J, Seoane J, Wotton D (2005) Smad transcription factors. Genes Dev 19:2783–2810PubMedCrossRefGoogle Scholar
  37. Merino R, Rodriguez-Leon J, Macias D, Ganan Y, Economides AN, Hurle JM (1999) The BMP antagonist Gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb. Development 126:5515–5522PubMedGoogle Scholar
  38. Mizutani CM, Nie Q, Wan FY, Zhang YT, Vilmos P, Sousa-Neves R, Bier E, Marsh JL, Lander AD (2005) Formation of the BMP activity gradient in the Drosophila embryo. Dev Cell 8:915–924PubMedCrossRefGoogle Scholar
  39. Moos M, Jr., Wang S, Krinks M (1995) Anti-dorsalizing morphogenetic protein is a novel TGF-beta homolog expressed in the Spemann organizer. Development 121:4293–4301PubMedGoogle Scholar
  40. Newfeld SJ, Wisotzkey RG, Kumar S (1999) Molecular evolution of a developmental pathway: phylogenetic analyses of transforming growth factor-beta family ligands, receptors and Smad signal transducers. Genetics 152:783–795PubMedGoogle Scholar
  41. Nguyen M, Parker L, Arora K (2000) Identification of Maverick, a novel member of the TGF-beta superfamily in Drosophila. Mech Dev 95:201–206PubMedCrossRefGoogle Scholar
  42. Nguyen T, Jamal J, Shimell MJ, Arora K, O’Connor MB (1994) Characterization of tolloid-related-1: a BMP-1-like product that is required during larval and pupal stages of Drosophila development. Dev Biol 166:569–586PubMedCrossRefGoogle Scholar
  43. Nicoli S, Gilardelli CN, Pozzoli O, Presta M, Cotelli F (2005) Regulated expression pattern of gremlin during zebrafish development. Gene Expr Patterns 5:539–544PubMedCrossRefGoogle Scholar
  44. O’Connor MB, Umulis D, Othmer HG, Blair SS (2006) Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133:183–193PubMedCrossRefGoogle Scholar
  45. Ober KA, Jockusch EL (2006) The roles of wingless and decapentaplegic in axis and appendage development in the red flour beetle, Tribolium castaneum. Dev Biol 294: 391–405PubMedCrossRefGoogle Scholar
  46. Onichtchouk D, Chen YG, Dosch R, Gawantka V, Delius H, Massague J, Niehrs C (1999) Silencing of TGF-beta signalling by the pseudoreceptor BAMBI. Nature 401:480–485PubMedCrossRefGoogle Scholar
  47. Parker L, Ellis JE, Nguyen MQ, Arora K (2006) The divergent TGF-{beta} ligand Dawdle utilizes an activin pathway to influence axon guidance in Drosophila. Development 133:4981–4991PubMedCrossRefGoogle Scholar
  48. Parker L, Stathakis DG, Arora K (2004) Regulation of BMP and activin signaling in Drosophila. Prog Mol Subcell Biol 34:73–101PubMedGoogle Scholar
  49. Persson U, Izumi H, Souchelnytskyi S, Itoh S, Grimsby S, Engstrom U, Heldin CH, Funa K, ten Dijke P (1998) The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation. FEBS Lett 434:83–87PubMedCrossRefGoogle Scholar
  50. Prpic NM, Janssen R, Wigand B, Klingler M, Damen WG (2003) Gene expression in spider appendages reveals reversal of exd/hth spatial specificity, altered leg gap gene dynamics, and suggests divergent distal morphogen signaling. Dev Biol 264:119–140PubMedCrossRefGoogle Scholar
  51. Ralston A, Blair SS (2005) Long-range Dpp signaling is regulated to restrict BMP signaling to a crossvein competent zone. Dev Biol 280:187–200PubMedCrossRefGoogle Scholar
  52. Rentzsch F, Anton R, Saina M, Hammerschmidt M, Holstein TW, Technau U (2006) Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. Dev Biol 296:375–387PubMedCrossRefGoogle Scholar
  53. Richards S (2008) The genome of the developmental model beetle and pest Tribolium castaneum. Nature, in pressGoogle Scholar
  54. Rodriguez EC, Capdevila J, Economides AN, Pascual J, Ortiz A, Izpisua Belmonte JC (1999) The novel Cer-like protein Caronte mediates the establishment of embryonic left–right asymmetry. Nature 401:243–251CrossRefGoogle Scholar
  55. Rosen V (2006) BMP and BMP inhibitors in bone. Ann NY Acad Sci 1068:19–25PubMedCrossRefGoogle Scholar
  56. Ross JJ, Shimmi O, Vilmos P, Petryk A, Kim H, Gaudenz K, Hermanson S, Ekker S C, O’Connor MB, Marsh JL (2001) Twisted gastrulation is a conserved extracellular BMP antagonist. Nature 410:479–483PubMedCrossRefGoogle Scholar
  57. Sanchez-Salazar J, Pletcher MT, Bennett RL, Brown S, Dandamudi TJ, Denell R, Doctor JS (1996) The Tribolium decapentaplegic gene is similar in sequence, structure and expression to the Drosophila dpp gene. Dev Genes Evol 206:237–246CrossRefGoogle Scholar
  58. Savard J, Tautz D, Richards S, Weinstock GM, Gibbs RA, Werren JH, Tettelin H, Lercher MJ (2006) Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res 16:1334–1338PubMedCrossRefGoogle Scholar
  59. Schmidt-Ott U (2000) The amnioserosa is an apomorphic character of cyclorrhaphan flies. Dev Genes Evol 210:373–376PubMedCrossRefGoogle Scholar
  60. Scott IC, Blitz IL, Pappano WN, Maas SA, Cho KW, Greenspan DS (2001) Homologues of Twisted gastrulation are extracellular cofactors in antagonism of BMP signalling. Nature 410:475–478PubMedCrossRefGoogle Scholar
  61. Serpe M, O’Connor MB (2006) The metalloprotease Tolloid-related and its TGF-{beta}-like substrate Dawdle regulate Drosophila motoneuron axon guidance. Development 133:4969–4979PubMedCrossRefGoogle Scholar
  62. Serpe M, Ralston A, Blair SS, O’Connor MB (2005) Matching catalytic activity to developmental function: tolloid-related processes Sog in order to help specify the posterior crossvein in the Drosophila wing. Development 132:2645–2656PubMedCrossRefGoogle Scholar
  63. Shi W, Zhao J, Anderson KD, Warburton D (2001) Gremlin negatively modulates BMP-4 induction of embryonic mouse lung branching morphogenesis. Am J Physiol Lung Cell Mol Physiol 280:L1030–L1039PubMedGoogle Scholar
  64. Shimell MJ, Ferguson EL, Childs SR, O’Connor MB (1991) The Drosophila dorsal–ventral patterning gene tolloid is related to human bone morphogenetic protein 1. Cell 67:469–481PubMedCrossRefGoogle Scholar
  65. Shimmi O, Umulis D, Othmer H, O’Connor MB (2005) Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell 120:873–886PubMedCrossRefGoogle Scholar
  66. Shivdasani AA, Ingham PW (2003) Regulation of stem cell maintenance and transit amplifying cell proliferation by tgf-beta signaling in Drosophila spermatogenesis. Curr Biol 13:2065–2072PubMedCrossRefGoogle Scholar
  67. Song X, Wong MD, Kawase E, Xi R, Ding BC, McCarthy JJ, Xie T (2004) BMP signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131:1353–1364PubMedCrossRefGoogle Scholar
  68. Stauber M, Prell A, Schmidt-Ott U (2002) A single Hox3 gene with composite bicoid and zerknullt expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci USA 99:274–279PubMedCrossRefGoogle Scholar
  69. Sun J, Zhuang FF, Mullersman JE, Chen H, Robertson EJ, Warburton D, Liu YH, Shi W (2006) BMP4 activation and secretion are negatively regulated by an intracellular gremlin–BMP4 interaction. J Biol Chem 281(39):29349–29356PubMedCrossRefGoogle Scholar
  70. Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81–85PubMedCrossRefGoogle Scholar
  71. Tzahor E, Kempf H, Mootoosamy RC, Poon AC, Abzhanov A, Tabin CJ, Dietrich S, Lassar AB (2003) Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle. Genes Dev 17:3087–3099PubMedCrossRefGoogle Scholar
  72. van der Zee M, Stockhammer O, von Levetzow C, Nunes da Fonseca R, Roth S (2006) Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect. Proc Natl Acad Sci USA 103:16307–16312PubMedCrossRefGoogle Scholar
  73. Vilmos P, Sousa-Neves R, Lukacsovich T, Marsh JL (2005) Crossveinless defines a new family of Twisted-gastrulation-like modulators of bone morphogenetic protein signalling. EMBO Rep 6:262–267PubMedCrossRefGoogle Scholar
  74. Wang YC, Ferguson EL (2005) Spatial bistability of Dpp-receptor interactions during Drosophila dorsal–ventral patterning. Nature 434:229–234PubMedCrossRefGoogle Scholar
  75. Weber M (2006) Bone Morphogenetic Proteins (BMP) in der Embryonalentwicklung von Tribolium castaneum, vol. Ph.D. University of Munich, MünchenGoogle Scholar
  76. Whiting MF (2004) Phylogeny of the holometabolous insects. In: Cracraft J, Donoghue MJ (ed) Assembling the tree of life. Oxford University Press, OxfordGoogle Scholar
  77. Yamamoto Y, Oelgeschlager M (2004) Regulation of bone morphogenetic proteins in early embryonic development. Naturwissenschaften 91:519–534PubMedCrossRefGoogle Scholar
  78. Yamanishi T, Katsu K, Funahashi J, Yumoto E, Yokouchi Y (2007) Dan is required for normal morphogenesis and patterning in the developing chick inner ear. Dev Growth Differ 49:13–26PubMedGoogle Scholar
  79. Zdobnov EM, Bork P (2007) Quantification of insect genome divergence. Trends Genet 23:16–20PubMedCrossRefGoogle Scholar
  80. Zheng X, Zugates CT, Lu Z, Shi L, Bai JM, Lee T (2006) Baboon/dSmad2 TGF-beta signaling is required during late larval stage for development of adult-specific neurons. EMBO J 25:615–627PubMedCrossRefGoogle Scholar
  81. Zuniga A, Haramis AP, McMahon AP, Zeller R (1999) Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature 401:598–602PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Maurijn Van der Zee
    • 1
  • Rodrigo Nunes da Fonseca
    • 2
  • Siegfried Roth
    • 2
  1. 1.Institute for GeneticsUniversity of CologneCologneGermany
  2. 2.Institute for Developmental BiologyUniversity of CologneCologneGermany

Personalised recommendations