Conserved features and evolutionary shifts of the eda signaling pathway involved in vertebrate skin appendage development

Molecular Biology and Evolution

Volumn 25, Issue 5, 2008, Pages 912-928

  Pantalacci, Sophie ^a   Chaumot, Arnaud ^b   Benoît, Gérard ^a   Sadier, Alexa ^a   Delsuc, Frédéric ^c   Douzery, Emmanuel J P ^c   Laudet, Vincent ^a  

^a UNIVERSITÉ DE LYON   (France)

^b CEMAGREF   (France)

^c INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

Comparative genomics; Ectodysplasin; EDA; Evolutionary developmental biology; Signaling pathway; Skin appendages

Indexed keywords

ECTODYSPLASIN A; ECTODYSPLASIN A1; ECTODYSPLASIN A2; EDAR ASSOCIATED DEATH DOMAIN PROTEIN; EDAR RECEPTOR; TROY RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG; XEDAR RECEPTOR; COMPLEMENTARY DNA; ECTODYSPLASIN RECEPTOR;

ARTICLE; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; GENETIC CONSERVATION; LIGAND BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PROTEIN DOMAIN; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SKIN APPENDAGE; TELEOST; VERTEBRATE; ANHIDROSIS; ANIMAL; BINDING SITE; ECTODERMAL DYSPLASIA; GENETICS; GUINEA PIG; HAMSTER; HISTOLOGY; HUMAN; INTEGUMENT; MARSUPIAL; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; SYRIAN HAMSTER;

MAMMALIA; VERTEBRATA;

ANIMALS; BINDING SITES; CRICETINAE; DNA, COMPLEMENTARY; ECTODERMAL DYSPLASIA; ECTODYSPLASINS; EVOLUTION, MOLECULAR; GUINEA PIGS; HUMANS; HYPOHIDROSIS; INTEGUMENTARY SYSTEM; MACROPODIDAE; MESOCRICETUS; MICE; MOLECULAR SEQUENCE DATA; RECEPTORS, ECTODYSPLASIN; SIGNAL TRANSDUCTION; VERTEBRATES;

EID: 50649113580     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msn038     Document Type: Article

References (68)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics. 21:2104-2105.
2. Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ. 2004. Bmp4 and morphological variation of beaks in Darwin's finches. Science. 305:1462-1465.
3. Benton MJ, Donoghue PC. 2007. Paleontological evidence to date the tree of life. Mol Biol Evol. 24:26-53.
4. Bertrand S, Brunet FG, Escriva H, Parmentier G, Laudet V, Robinson-Rechavi M. 2004. Evolutionary genomics of nuclear receptors: from twenty-five ancestral genes to derived endocrine systems. Mol Biol Evol. 21:1923-1937.
5. Blom N, Gammeltoft S, Brunak S. 1999. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol. 294:1351-1362.
6. Bossen C, Ingold K, Tardivel A, Bodmer JL, Gaide O, Hertig S, Ambrose C, Tschopp J, Schneider P. 2006. Interactions of tumor necrosis factor (TNF) and TNF receptor family members in the mouse and human. J Biol Chem. 281:13964-13971.
7. Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, Green ED, Sidow A, Batzoglou S. 2003. LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res. 13:721-731.
8. Brugmann SA, Goodnough LH, Gregorieff A, Leucht P, ten Berge D, Fuerer C, Clevers H, Nusse R, Helms JA. 2007. Wnt signaling mediates regional specification in the vertebrate face. Development. 134:3283-3295.
9. Chassaing N, Bourthoumieu S, Cossee M, Calvas P, Vincent MC. 2006. Mutations in EDAR account for one-quarter of non-ED1-related hypohidrotic ectodermal dysplasia. Hum Mutat. 27:255-259.
10. Collette Y, Gilles A, Pontarotti P, Olive D. 2003. A co-evolution perspective of the TNFSF and TNFRSF families in the immune system. Trends Immunol. 24:387-394.
11. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G Jr, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science. 307:1928-1933.
12. Courtney JM, Blackburn J, Sharpe PT. 2005. The Ectodysplasin and NFkappaB signalling pathways in odontogenesis. Arch Oral Biol. 50:159-163.
13. Cui CY, Schlessinger D. 2006. EDA signaling and skin appendage development. Cell Cycle. 5:2477-2483.
14. Donoghue PCJ. 2002. Evolution of development of the vertebrate dermal and oral skeletons: unraveling concepts, regulatory theories, and homologies. Paleobiology. 28:474-507.
15. Drew CF, Lin CM, Jiang TX, Blunt G, Mou C, Chuong CM, Headon DJ. 2007. The Edar subfamily in feather placode formation. Dev Biol. 305:232-245.
16. Eby MT, Jasmin A, Kumar A, Sharma K, Chaudhary PM. 2000. TAJ, a novel member of the tumor necrosis factor receptor family, activates the c-Jun N-terminal kinase pathway and mediates caspase-independent cell death. J Biol Chem. 275:15336-15342.
17. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
18. Felix MA. 2005. An inversion in the wiring of an intercellular signal: evolution of Wnt signaling in the nematode vulva. Bioessays. 27:765-769.
19. Fujimoto A, Kimura R, Ohashi J, et al. (15 co-authors). 2007. A scan for genetic determinants of human hair morphology: eDAR is associated with Asian hair thickness. Hum Mol Genet. 17:835-843.
20. Galtier N, Gouy M, Gautier C. 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci. 12:543-548.
21. Gillis JA, Donoghue PCJ. 2007. The homology and phylogeny of chondrichthyan tooth enameloid. J Morphol. 268:33-49.
22. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
23. Hashimoto T, Cui CY, Schlessinger D. 2006. Repertoire of mouse ectodysplasin-A (EDA-A) isoforms. Gene. 371:42-51.
24. Hoekstra HE, Coyne JA. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evol Int J Org Evol. 61:995-1016.
25. Houghton L, Lindon C, Morgan BA. 2005. The ectodysplasin pathway in feather tract development. Development. 132:863-872.
26. Huchon D, Madsen O, Sibbald MJJB, Ament K, Stanhope MJ, Catzeflis F, de Jong WW, Douzery EJP. 2002. Rodent phylogeny and a timescale for the evolution of glires: evidence from an extensive taxon sampling using three nuclear genes. Mol Biol Evol. 19:1053-1065.
27. Hymowitz SG, Compaan DM, Yan M, Wallweber HJ, Dixit VM, Starovasnik MA, de Vos AM. 2003. The crystal structures of EDA-A1 and EDA-A2: splice variants with distinct receptor specificity. Structure. 11:1513-1520.
28. Itoh N, Ornitz DM. 2004. Evolution of the Fgf and Fgfr gene families. Trends Genet. 20:563-569.
29. Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, Johnson RL, Gates J, Scott MP, Carroll SB. 1999. Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science. 283:532-534.
30. Knecht AK, Hosemann KE, Kingsley DM. 2007. Constraints on utilization of the EDA-signaling pathway in threespine stickleback evolution. Evol Dev. 9:141-154.
31. Kojima T, Morikawa Y, Copeland NG, Gilbert DJ, Jenkins NA, Senba E, Kitamura T. 2000. TROY, a newly identified member of the tumor necrosis factor receptor superfamily, exhibits a homology with Edar and is expressed in embryonic skin and hair follicles. J Biol Chem. 275:20742-20747.
32. Kondo S, Kuwahara Y, Kondo M, Naruse K, Mitani H, Wakamatsu Y, Ozato K, Asakawa S, Shimizu N, Shima A. 2001. The medaka rs-3 locus required for scale development encodes ectodysplasin-A receptor. Curr Biol. 11:1202-1206.
33. Lavoue S, Miya M, Inoue JG, Saitoh K, Ishiguro NB, Nishida M. 2005. Molecular systematics of the gonorynchiform fishes (Teleostei) based on whole mitogenome sequences: implications for higher-level relationships within the Otocephala. Mol Phylogenet Evol. 37:165-177.
34. Levasseur A, Gouret P, Lesage-Meessen L, Asther M, Asther M, Record E, Pontarotti P. 2006. Tracking the connection between evolutionary and functional shifts using the fungal lipase/feruloyl esterase A family. BMC Evol Biol. 6:92.
35. Lind LK, Stecksen-Blicks C, Lejon K, Schmitt-Egenolf M. 2006. EDAR mutation in autosomal dominant hypohidrotic ectodermal dysplasia in two Swedish families. BMC Med Genet. 7:80.
36. Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA, Pachter LS, Dubchak I. 2000. VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics. 16:1046-1047.
37. Mikkola ML. 2007. Genetic basis of skin appendage development. Semin Cell Dev Biol. 18:225-236.
38. Mikkola ML, Thesleff I. 2003. Ectodysplasin signaling in development. Cytokine Growth Factor Rev. 14:211-224.
39. Monreal AW, Ferguson BM, Headon DJ, Street SL, Overbeek PA, Zonana J. 1999. Mutations in the human homologue of mouse dl cause autosomal recessive and dominant hypohidrotic ectodermal dysplasia. Nat Genet. 22:366-369.
40. Murphy WJ, Eizirik E, O'Brien SJ, et al. 2001. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science. 294:2348-2351 (11 co-authors).
41. Newton K, French DM, Yan M, Frantz GD, Dixit VM. 2004. Myodegeneration in EDA-A2 transgenic mice is prevented by XEDAR deficiency. Mol Cell Biol. 24:1608-1613.
42. Oakley TH. 2007. Today's multiple choice exam. (a) gene duplication; (b) structural mutation; (c) co-option; (d) regulatory mutation; (e) all of the above. Evol Dev. 9:523-524.
43. Ohazama A, Courtney JM, Tucker AS, Naito A, Tanaka S, Inoue J, Sharpe PT. 2004. Traf6 is essential for murine tooth cusp morphogenesis. Dev Dyn. 229:131-135.
44. Peterkova R, Lesot H, Peterka M. 2006. Phylogenetic memory of developing mammalian dentition. J Exp Zoolog B Mol Dev Evol. 306:234-250.
45. Pires-daSilva A, Sommer RJ. 2003. The evolution of signalling pathways in animal development. Nat Rev Genet. 4:39-49.
46. Pispa J, Mikkola ML, Mustonen T, Thesleff I. 2003. Ectodysplasin, Edar and TNFRSF19 are expressed in complementary and overlapping patterns during mouse embryogenesis. Gene Expr Patterns. 3:675-679.
47. Popovici C, Roubin R, Coulier F, Birnbaum D. 2005. An evolutionary history of the FGF superfamily. Bioessays. 27:849-857.
48. Prud'homme B, Gompel N, Carroll SB. 2007. Emerging principles of regulatory evolution. Proc Natl Acad Sci USA. 104(Suppl 1)):8605-8612.
49. Reif WE. 1982. Evolution of dermal skeleton and dentition in vertebrates - the odontode regulation theory. Evol Biol. 15:287-368.
50. Sabeti PCP, Varilly B, Fry J, Lohmueller E, Hostetter C, et al. 2007. Genome-wide detection and characterization of positive selection in human populations. Nature. 449:913-918 (222 co-authors).
51. Schneider P, Street SL, Gaide O, Hertig S, Tardivel A, Tschopp J, Runkel L, Alevizopoulos K, Ferguson BM, Zonana J. 2001. Mutations leading to X-linked hypohidrotic ectodermal dysplasia affect three major functional domains in the tumor necrosis factor family member ectodysplasin-A. J Biol Chem. 276:18819-18827.
52. Shao Z, Browning JL, Lee X, et al. (14 co-authors). 2005. TAJ/ TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron. 45:353-359.
53. Sharpe PT. 2001. Fish scale development: hair today, teeth and scales yesterday? Curr Biol. 11:R751-R752.
54. Sinha SK, Zachariah S, Quinones HI, Shindo M, Chaudhary PM. 2002. Role of TRAF3 and -6 in the activation of the NF-kappa B and JNK pathways by X-linked ectodermal dysplasia receptor. J Biol Chem. 277:44953-44961.
55. Stock DW. 2001. The genetic basis of modularity in the development and evolution of the vertebrate dentition. Philos Trans R Soc Lond B Biol Sci. 356:1633-1653.
56. Tao R, Jin B, Guo SZ, et al. (11 co-authors). 2006. A novel missense mutation of the EDA gene in a Mongolian family with congenital hypodontia. J Hum Genet. 51:498-502.
57. Thesleff I, Mikkola ML. 2002. Death receptor signaling giving life to ectodermal organs. Sci STKE. 2002:PE22.
58. Vincent MC, Biancalana V, Ginisty D, Mandel JL, Calvas P. 2001. Mutational spectrum of the ED1 gene in X-linked hypohidrotic ectodermal dysplasia. Eur J Hum Genet. 9:355-363.
59. Visinoni AF, de Souza RL, Freire-Maia N, Gollop TR, Chautard-Freire-Maia EA. 2003. X-linked hypohidrotic ectodermal dysplasia mutations in Brazilian families. Am J Med Genet A. 122:51-55.
60. Williamson SH, Hubisz MJ, Clark AG, Payseur BA, Bustamante CD, Nielsen R. 2007. Localizing recent adaptive evolution in the human genome. PLoS Genet. 3:e90.
61. Wray GA. 2007. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet. 8:206-216.
62. Wu P, Hou L, Plikus M, Hughes M, Scehnet J, Suksaweang S, Widelitz R, Jiang TX, Chuong CM. 2004. Evo-Devo of amniote integuments and appendages. Int J Dev Biol. 48:249-270.
63. Yan M, Wang LC, Hymowitz SG, Schilbach S, Lee J, Goddard A, de Vos AM, Gao WQ, Dixit VM. 2000. Two-amino acid molecular switch in an epithelial morphogen that regulates binding to two distinct receptors. Science. 290:523-527.
64. Yan M, Zhang Z, Brady JR, Schilbach S, Fairbrother WJ, Dixit VM. 2002. Identification of a novel death domain-containing adaptor molecule for ectodysplasin-A receptor that is mutated in crinkled mice. Curr Biol. 12:409-413.
65. Yang ZH. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
66. Yang ZH, Wong WSW, Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol. 22:1107-1118.
67. Zhang JZ, Nielsen R, Yang ZH. 2005. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol. 22:2472-2479.
68. Zonana J, Elder ME, Schneider LC, et al. (11 co-authors). 2000. A novel X-linked disorder of immune deficiency and hypohidrotic ectodermal dysplasia is allelic to incontinentia pigmenti and due to mutations in IKK-gamma (NEMO). Am J Hum Genet. 67:1555-1562.