The evolution of the hh-signaling pathway genes: A computer-assisted study

In Silico Biology

Volumn 7, Issue 3, 2007, Pages 333-354

  Gunbin, Konstantin V ^a   Afonnikov, Dmitrij A ^a,b   Kolchanov, Nikolay A ^a  

^a INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

^b NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

Author keywords

Bilateria; Compensatory changes; Hh signaling cascade; Positive selection

Indexed keywords

SONIC HEDGEHOG PROTEIN;

AMINO ACID SUBSTITUTION; CELL DIFFERENTIATION; COMPUTER ANALYSIS; CONFERENCE PAPER; CONTROLLED STUDY; DROSOPHILA; EMBRYO DEVELOPMENT; GENETIC CODE; GENETIC CONSERVATION; MOLECULAR MECHANICS; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN DOMAIN; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TAXONOMY; XENOPUS;

ALGORITHMS; ANIMALS; COMPUTER SIMULATION; EVOLUTION, MOLECULAR; HEDGEHOG PROTEINS; HUMANS; INVERTEBRATES; PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 38949120513     PISSN: 13866338     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Conference Paper

References (99)

1. Abascal, F., Zardoya, R. and Posada, D. (2005). ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105.
2. Akimaru, H., Chen, Y., Dai, P., Hou, D.-X., Nonaka, M., Smolik, S. M., Armstrong, S., Goodman, R. H. and Ishii, S. (1997). Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature 386, 735-738.
3. Alexandre, C., Jacinto, A. and Ingham, P.W. (1996). Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev. 10, 2003-2013.
4. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
5. Ascano, M. Jr., Nybakken, K. E., Sosinski, J., Stegman, M. A. and Robbins, D. J. (2002). The carboxyl-terminal domain of the protein kinase fused can function as a dominant inhibitor of hedgehog signalling. Mol. Cell. Biol. 22, 1555-1566.
6. Ascano, M. Jr. and Robbins, D. J. (2004). An intramolecular association between two domains of the protein kinase Fused is necessary for Hedgehog signalling. Mol. Cell. Biol. 24, 10397-10405.
7. Aza-Blanc, P., Lin, H.-Y, Ruiz i Altaba, A. and Kornberg, T. B. (2000). Expression of the vertebrate Gli proteins in Drosophila reveals a distribution of activator and repressor activities. Development 127 4293-4301.
8. Barnfield, P. C., Zhang, X., Thanabalasingham V,. Yoshida, M. and Hui, C. C. (2005). Negative regulation of Gli1 and Gli2 activator function by Suppressor of fused through multiple mechanisms. Differentiation 73 397-405.
9. Benton, M. J. and Donoghue, P. C. (2007). Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24, 26-53.
10. Bijlsma, M. F., Spek, C. A. and Peppelenbosch, M. P. (2004). Hedgehog: an unusual signal transducer. Bioessays 26, 387-394.
11. Bourlat, S. J., Juliusdottir, T., Lowe, C. J., Freeman, R., Aronowicz, J., Kirschner, M., Lander, E. S., Thorndyke, M., Nakano, H., Kohn, A. B., Heyland, A., Moroz, L. L., Copley, R. R. and Telford, M. J. (2006). Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444, 85-88.
12. Burke, R., Nellen, D., Bellotto, M., Hafen, E., Senti, K.-A., Dickson, B. J. and Basler, K. (1999). Dispatched, a novel sterol-sensing domain proem dedicated to the release of cholesterol-modified hedgehog from signalling cells. Cell 99, 803-815.
13. Cardozo, T. and Pagano, M. (2004). The SCF ubiquitin ligase: Insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5, 739-751.
14. Chen, Y., Goodman, R. H. and Smolik, S. M. (2000). Cubitus interruptus requires Drosophila CREB-binding protein to activate wingless expression in the Drosophila embryo. Mol. Cell. Biol. 20, 1616-1625.
15. Dai, P., Akimaru, H., Tanaka, Y., Maekawa, T., Nakafuku, M. and Ishii, S. (1999). Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274, 8143-8152.
16. Davidson, E. H., Peterson, K. J. and Cameron, R. A. (1995). Origin of adult bilaterian body plans. Evolution of developmental regulatory mechanisms. Science 270, 1319-1325.
17. Dunaeva, M., Michelson, P., Kogerman, P. and Toftgard, R. (2003). Characterization of the physical interaction of Gli proteins with SUFU proteins. J. Biol. Chem. 278, 5116-5122.
18. Duret, L. and Mouchiroud, D. (2000). Determinants of substitution rates in mammalian genes: Expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17, 68-74.
19. Enright, A. J., Van Dongen, S. and Ouzounis, C. A. (2002). An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30, 1575-1584.
20. Erwin, D. H. and Davidson, E. H. (2002). The last common bilaterian ancestor. Development 129, 3021-3032.
21. Fuse, N., Maiti, T., Wang, B., Porter, J. A., Hall, T. M., Leahy, D. J. and Beachy, P. A. (1999). Sonic hedgehog protein signals not as a hydrolytic enzyme but as an apparent ligand for patched. Proc. Natl. Acad. Sci. USA 96, 10992-10999.
22. Gallet, A., Rodriguez, R., Ruel, L. and Therond, P. P. (2003). Cholesterol modification of hedgehog is required for trafficking and movement, revealing an asymmetnc cellular response to hedgehog. Dev Cell 4, 191-204.
23. Grassly, N. C. and Holmes, E. C. (1997). A likelihood method for the detection of selection and recombination using nucleotide sequences. Mol. Biol. Evol. 14, 239-247.
24. Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood Syst. Biol. 52, 696-704.
25. Gunbin, K. V., Omelyanchuk, L. V. and Ananko, E. A. (2004a). Two gene networks underlying the formation of the anterior-posterior and dorso-ventral wing imaginal disc compartment boundaries in Drosophila melanogaster. In: Kolchanov, N. A. et al. (eds.), Proceedings of the forth international conference on bioinformatics of genome regulation and structure, BGRS'2004. Institute of Cytology and Genetics Press 2, 56-59. http://www.bionet.nsc.ru/meeting/bgrs2004/tom2.pdf
26. Gunbin, K. V., Suslov, V. V. Kolchanov, N. A. and Omelyanchuk, N. A. (2004b). Genetic mechanisms of morphological evolution, part 1. Siberian Journal of Ecology 11, 599-610 (in Russian).
27. Gunbin, K. V., Suslov, V. V., Kolchanov, N. A. and Omelyanchuk, N. A. (2004c). Genetic mechanisms, of morphological evolution, part 2. Siberian Journal of Ecology 11, 611-621 (in Russian).
28. Gunbin, K. V., Omelyanchuk, L. V. and Kolchanov, N. A. (2005). Aromorphoses and the adaptive molecular evolution: Hedgehog signalling cascade genes. International Workshop "Biosphere Origin and Evolution". Abstracts. Boreskov Institute of Catalysis Press, p. OP-5. http://www-sbras.nsc.ru/ws/biosphere/index.en.html
29. Hall, T. M., Porter, J. A., Young, K. E., Koonin, E. V., Beachy, P. A. and Leahy, D. J. (1997). Crystal structure of a Hedgehog autoprocessing domain: Homology between Hedgehog and self-splicing proteins. Cell 91 85-97.
30. Hartman, J. L. 4th, Garvik, B. and Hartwell, L. (2001). Principles for the buffering of geaetic variation. Science 291, 1001-1004.
31. Ho, K. S., Suyama, K., Fish, M. and Scott, M. P. (2005). Differential regulation of Hedgehog target gene transcription by Costa12 and Suppressor of Fused. Development 132, 1401-1412.
32. Huangfu, D. and Anderson, K. V. (2006). Signalling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 133, 3-14.
33. Hubbard, T., et al. (2005). Ensembl 2005. Nucleic Acids Res. 33 D447-D453.
34. Ikram, M. S., Neill, G. W., Regl, G., Eichberger, T., Frischauf, A.-M., Aberger, F., Quinn, A. and Philpott, M. (2004). GLI2 is expressed in normal human epidermis and BCC and induces GLI1 expression by binding to its promoter. J. Invest. Dermatol. 122, 1503-1509.
35. Ina, Y. (1995). New methods for estimating the numbers of synonymous and nonsynonymous substitutions. J. Mol. Evol. 40, 190-226.
36. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signalling in animal development: Paradigms and principles. Genes Dev. 15, 3059-3087.
37. Jackson, P. K. and Eldridge, A. G. (2002). The SCF ubiquitin ligase: An extended look. Mol. Cell. 9, 923-925.
38. Jia, J., Tong, C. and Jiang, J. (2003). Smoothened transduces Hedgehog signal by physically interacting with Costal2/Fused complex through its C-terminal tail. Genes Dev. 17, 2709-2720.
39. Jia, J., Tong, C., Wang, B., Luo, L. and Jiang, J. (2004). Hedgehog signalling activity of Smoothened requires phosphorylation by protein kinase A and casein kinase I. Nature 432, 1045-1050.
40. Karpen, H. E., Bukowski, J. T., Hughes, T., Gratton, J. P., Sessa, W. C. and Gailani, M. R. (2001). The sonic hedgehog receptor patched associates with caveolin-1 in cholesterol-rich microdomains of the plasma membrane. J. Biol. Chem. 276, 19503-19511.
41. Katoh, K., Kuma, K., Toh, H. and Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511-518.
42. Katoh, K., Misawa, K., Kuma, K. and Miyata, T. (2002). MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066.
43. Katoh, Y. and Katoh, M. (2004) KIF27 is one of orthologs for Drosophila Costal-2. Int. J. Oncol. 25, 1875-1880.
44. Kimura, M. (1983) The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge.
45. Knoll, A. H. and Carroll, S. B. (1999). Early animal evolution: Emerging views from comparative biology and geology. Science 284, 2129-2137.
46. Kolchanov, N. A., Suslov, V. V. and Gunbin, K. V. (2004). Biological evolution simulation: Genetic regulatory systems and biological complexity encoding. Herald of the VOGIS 8, 86-99. http://www.bionet.nsc.ru/vogis/pict.pdf/2004/29/07_Kolchanov.pdf (in Russian)
47. Kumar, S., Balczarek, K. A. and Lai, Z. C. (1996). Evolution of the hedgehog gene family. Genetics 142, 965-972.
48. Kuwabara, P. E. and Labouesse, M. (2002) The sterol-sensing domain: multiple families, a unique role? Trends Genet. 18, 193-201.
49. Lum, L. and Beachy, P. A. (2004). The Hedgehog response network: sensors, switches, and routers. Science 304, 1755-1759.
50. Lum, L., Zhang, C., Oh, S., Mann, R. K., von Kessler, D. P., Taipale, J., Weis-Garcia, F., Gong, R., Wang,-B. and Beachy, P. A. (2003). Hedgehog signal transduction via Smoothened association with a cytoplasmic complex sca.folded by the atypical kinesin, Costal-2. Mol. Cell. 12, 1261-1274.
51. Maddison, D. R. and Schulz K.-S. (eds.) (1996-2006). The Tree of Life Web Project http://tolweb.org
52. Marchler-Bauer, A., et al. (2005). CDD: A Conserved Domain Database for protein classification. Nucleic Acids Res. 33, D192-D196.
53. Martin, V., Carrillo, G., Torroja, C. and Guerrero, I. (2001). The sterol-sensing domain of Patched protein seems to control Smoothened activity through Patched vesicular trafficking. Curr Biol. 11, 601-607.
54. Merchant, M., Vajdos, F. F., Ultsch, M., Mann, H. R., Wendt, U., Cannon, I., Desmarais, W., Lazarus, R. A., de Vos, A. M. and de Sauvage, F. J. (2004). Suppressor of fused regulates Gli activity through a dual binding mechanism. Mol. Cell. Biol. 24, 8627-8641.
55. Merl, D., Escalante, A. and Prado, R. (2005). Comparison of Bayesian, maximum likelihood and parsimony methods for detecting positive selection. UCSC Department of Applied Math and Statistics Technical Reports, ams2005-03. www.ams.ucsc.edu/reports/ams2005-03.pdf.
56. Monnier, V., Ho, K. S., Sanial, M., Scott; M. P. and Plessis, A. (2002). Hedgehog signal transduction proteins: Contacts of the Fused kinase and Ci transcription factor with the kinesin-related protein Costal2. BMC Dev. Biol. 2, 4.
57. Müller, B. and Basler, K. (2000). The repressor and activator forms of Cubitus interruptus control Hedgehog target genes through common generic gli-binding sites. Development 127, 2999-3007.
58. Murone, M., Luoh, S. M., Stone, D., Li, W., Gurney, A., Armanini, M., Grey, C., Rosenthal, A. and de Sauvage, F., J. (2000). Gli regulation by the opposing activities of fused and suppressor of fused. Nat. Cell Biol. 2, 310-312.
59. Nakano, Y., Nystedt, S., Shivdasani, A. A., Strutt, H., Thomas, C. and Ingham, P. W. (2004). Fanctional domains and sub-cellular distribution of the Hedgehog transducing protein Smoothened in Drosophila. Mech. Dev. 121, 507-518.
60. Nakayama, K. I. and Nakayama, K. (2005). Regulation of the cell cycle by SCF-type ubiquitin ligases. Semin. Cell Dev. Biol. 16, 323-333.
61. Nei, M. and Gojobori, T. (1986). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418-426.
62. Nei, M., Kumar, S. and Takahashi, K. (1998). The optimization principle in phylogenetic analysis tends to give incorrect topologies when the number of nucleotides or amino acids used is small. Proc. Natl. Acad. Sci. USA 95, 12390-12397.
63. Notredame, C., Higgins, D. G. and Heringa, J. (2000). T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217.
64. Nybakken, K. and Perrimon, N. (2002). Hedgehog signal transducticn: recent findings. Curr. Opin. Genet. Dev. 12, 503-511.
65. Ogden, S. K., Ascano, M. Jr., Stegman, M. A., Suber, L. M., Hooper, J. E. and Robbins, D. J. (2003). Identification of a functional interaction between the transmembrane protein Smoothened and the kinesin-related protein Costal2. Curr Biol. 13, 1998-2003.
66. Peltier, M. R., Raley, L. C., Liberles, D. A., Benner, S. A. and Hansen, P. J. (2000). Evolutionary history of the uterine serpins. J. Exp. Zool. 288, 165-174.
67. Peters, C., Wolf, A., Wagner, M., Kuhlmaun, J. and Waldmann, H. (2004). The cholesterol membrane anchor of the Hedgehog protein confers stable membrane association to lipid-modified proteins. Proc. Natl. Acad. Sci USA 101, 8531-8536.
68. Peterson, K. J., Cameron, R. A. and Davidson, E. H. (2000). Bilaterian Origins: Significance of new experimental observations. Dev. Biol. 219, 147.
69. Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J. and McPeek, M. A. (2004). Estimating metazoan divergence times with a molecular clock. Proc. Natl. Acad. Sci. USA 101, 6536-6541.
70. Petretti, C. and Prigent, C. (2005). The Protein Kinase Resource: everything you always wanted to know about protein kinases but were afraid to ask. Biol. Cell. 97, 113-118.
71. Pires-daSilva A. and Sommer R.J. (2003). The evolution of signalling pathways in animal development. Nat. Rev. Genet. 4, 39-49.
72. Pruitt, K. D., Tatusova, T. and Maglott, D. R. (2005). NCBI Reference Sequence (RefSeq): A curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 33, D501-D504.
73. Raff, R. A. (1996). The Shape of Life: Genes, Development, and the Evolution of Animal Form. University of Chicago Press, Chicago.
74. Ruel, L., Rodriguez, R., Gallet, A., Lavenant-Staccini, L. and Thérond, P. P.(2003). Stability and association of Smoothened, Costal2 and Fused with Cubitus interruptus are regulated by Hedgehog. Nat. Cell Biol. 5, 907-913.
75. Salazar-Ciudad, I. and Jernvall, J. (2004). How different types of pattern formation mechanisms affect the evolution of form and development. Evol. Dev. 6, 6-16.
76. Salazar-Ciudad, I., Jernvall, J. and Newman, S. A. (2003). Mechanisms of pattern formation in development and evolution. Development 130, 2027-2037.
77. Sanderson, M. J. and Shaffer, H. B. (2002). Troubleshooting molecular phylogenetic analyses. Annu. Rev. Ecol. Syst. 33, 49-72.
78. Schmidt, H. A., Shimmer, K., Vingron, M. and von Haeseler, A. (2002). TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502-504.
79. Shimeld, S. M. (1999). The evolution of the hedgehog gene family in chordates: Insights from amphioxus hedgehog. Dev. Genes Evol. 209, 40-47.
80. Sepkoski, J. J. Jr. Fossil marine animals. Stratigraphic distribution; taxonomy. 1996. Programming: Markov A., 1999. http://macroevolution.narod.ru/dblist.htm (in Russian)
81. Shu, D. G., Morris, S. C., Han, J., Li, Y., Zhang, X. L., Hua, H., Zhang, Z. F., Liu, J. N., Guo, J. F., Yao, Y. and Yasui, K. (2006). Lower Cambrian vendobionts from China and early diploblast evolution. Science 312, 731-734.
82. Sole, R. V., Fernandez, P. and Kauffman, S. A. (2003). Adaptive walks in a gene network model of morphogenesis: Insights into the Cambrian explosion. Int. J. Dev. Biol. 47, 685-693.
83. Suslov, V. V., Gunbin, K. V. and Kolchanov, N. A. (2004). Genetic mechanisms of biological complexity encoding. Ecological genetic 2 13-26 (in Russian).
84. Suzuki, Y. (2004). New methods for detecting positive selection at single amino acid sites. J. Mol. Evol. 59, 11-19.
85. Suzuki, Y., Gojobori, T. and Nei, M. (2001). ADAPTSITE: Detecting natural selection at single amino acid sites. Bioinformatics 17, 660-661.
86. Tang, H. and Wa, C. I. (2006). A new method for estimating nonsynonymous substitutions and its applications to detecting positive selection. Mol. Biol. Evol. 23, 372-379.
87. Tay, S. Y., Ingham, P. W. and Roy, S. (2005). A homologne of the Drosophila kinesin-like protein Costal2 regulates Hedgehog signal transduction in the vertebrate embryo. Development 132, 625-634.
88. 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. Nucleic Acids Res. 22, 4673-4680.
89. Thompson, J. D., Plewniak, F. and Poch, O. (1999). A comprehensive comparison of multiple sequence alignment programs. Nucleic Acids Res. 27, 2682-2690.
90. Thompson, J. D., Thierry, J. C. and Poch, O. (2003). RASCAL: Rapid scanning and correction of multiple sequence alignments. Bioinformatics 19, 1155-1161.
91. Tseng, T. T., Gratwick, K. S., Kollman, J., Park, D., Nies, D. H., Goffeau, A. and Saier, M. H. Jr. (1999). The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J. Mol. Microbiol. Biotechnol. 1, 107-125.
92. Tyurina, O. V., Guner, B., Popova, E., Feng, J., Schier, A. F., Kohtz, J. D. and Karlstrom, R. O. (2005). Zebrafish Gli3 functions as both an activator and a repressor in Hedgehog signalling. Dev. Biol. 277, 537-556.
93. Tzeng, Y. H., Pan, R. and Li, W. H. (2004). Comparison of three methods for estimating rates of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 21, 2290-2298.
94. Vorontsov, N. N. (1967). Evolutsia Pishchevaritelnoy Systemy Mysheobraznykh Gryzunov. Nauka, (In Russian). English translation (1979). Evolution of the Alimentary System in Myomorph Rodents. Smithsonian Institution, Washington D.C. & Nat. Sci. Foundation (Translated by the Indian Documentation Centre, New Delhi)
95. Wang, G. and Jiang, J. (2004). Multiple Cos2/Ci interactions regulate Ci subcellular localization through microtubule dependent and independent mechanisms. Dev. Biol. 268, 493-505.
96. Whelan, S. and Goldman, N. (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691-699.
97. Whittam, T. S. and Nei, M. (1991). Neutral mutation hypothesis test. Nature 354, 115-116.
98. Yang, Z. (1997). PAML: A program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555-556.
99. Yang, Z. and Nielsen, R. (2000). Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17, 32-43.