期刊论文详细信息
BMC Evolutionary Biology
Amelotin: an enamel matrix protein that experienced distinct evolutionary histories in amphibians, sauropsids and mammals
Jean-Yves Sire2  Tiphaine Davit-Béal2  Jérémie Silvent3  Ylenia Chiari1  Barbara Gasse2 
[1] Department of Biology, University of South Alabama, Mobile 36688, AL, USA;Institut de Biologie Paris-Seine, Université Pierre et Marie Curie, Evolution Paris-Seine, Paris UMR7138, France;Department of Structural Biology, Weizmann Institute of Science, Rehovot 76100, Israel
关键词: Evolution;    Gene expression;    Bioinformatics;    Tetrapods;    Amelogenesis;    Enamel;   
Others  :  1158255
DOI  :  10.1186/s12862-015-0329-x
 received in 2014-10-17, accepted in 2015-02-24,  发布年份 2015
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【 摘 要 】

Background

Amelotin (AMTN) is an ameloblast-secreted protein that belongs to the secretory calcium-binding phosphoprotein (SCPP) family, which originated in early vertebrates. In rodents, AMTN is expressed during the maturation stage of amelogenesis only. This expression pattern strongly differs from the spatiotemporal expression of other ameloblast-secreted SCPPs, such as the enamel matrix proteins (EMPs). Furthermore, AMTN was characterized in rodents only. In this study, we applied various approaches, including in silico screening of databases, PCRs and transcriptome sequencing to characterize AMTN sequences in sauropsids and amphibians, and compared them to available mammalian and coelacanth sequences.

Results

We showed that (i) AMTN is tooth (enamel) specific and underwent pseudogenization in toothless turtles and birds, and (ii) the AMTN structure changed during tetrapod evolution. To infer AMTN function, we studied spatiotemporal expression of AMTN during amelogenesis in a salamander and a lizard, and compared the results with available expression data from mouse. We found that AMTN is expressed throughout amelogenesis in non-mammalian tetrapods, in contrast to its expression limited to enamel maturation in rodents.

Conclusions

Taken together our findings suggest that AMTN was primarily an EMP. Its functions were conserved in amphibians and sauropsids while a change occurred early in the mammalian lineage, modifying its expression pattern during amelogenesis and its gene structure. These changes likely led to a partial loss of AMTN function and could have a link with the emergence of prismatic enamel in mammals.

【 授权许可】

   
2015 Gasse et al.; licensee BioMed Central.

【 预 览 】
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【 参考文献 】
  • [1]Iwasaki K, Bajenova E, Somogyi-Ganss E, Miller M, Nguyen V, Nourkeyhani H, et al.: Amelotin–a novel secreted, ameloblast-specific protein. J Dent Res 2005, 84:1127-32.
  • [2]Moffatt P, Smith CE, Sooknanan R, St-Arnaud R, Nanci A: Identification of secreted and membrane proteins in the rat incisor enamel organ using a signal-trap screening approach. Eur J Oral Sci 2006, 114:139-46.
  • [3]Moffatt P, Smith CE, St-Arnaud R, Simmons D, Wright JT, Nanci A: Cloning of rat amelotin and localization of the protein to the basal lamina of maturation stage ameloblasts and junctional epithelium. Biochem J 2006, 399:37-46.
  • [4]Moffatt P, Smith CE, St-Arnaud R, Nanci A: Characterization of Apin, a secreted protein highly expressed in tooth-associated epithelia. J Cell Biochem 2008, 103:941-56.
  • [5]Moffatt P, Wazen RM, Neves JDS, Nanci A: Characterisation of secretory calcium-binding phosphoprotein-proline-glutamine-rich 1: a novel basal lamina component expressed at cell-tooth interfaces. Cell Tissue Res 2014, 358:843-55.
  • [6]Kawasaki K, Weiss KM: Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proc Natl Acad Sci U S A 2003, 100:4060-5.
  • [7]Kawasaki K, Weiss KM: Evolutionary genetics of vertebrate tissue mineralization: the origin and evolution of the secretory calcium-binding phosphoprotein family. J Exp Zool B Mol Dev Evol 2006, 306B:295-316.
  • [8]Kawasaki K, Suzuki T, Weiss KM: Genetic basis for the evolution of vertebrate mineralized tissue. Proc Natl Acad Sci U S A 2004, 101:11356-61.
  • [9]Bertrand S, Fuentealba J, Aze A, Hudson C, Yasuo H, Torrejon M, et al.: A dynamic history of gene duplications and losses characterizes the evolution of the SPARC family in eumetazoans. Proc R Soc Lond B Biol Sci 2013, 280:20122963.
  • [10]Dehal P, Boore JL: Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 2005, 3:e314.
  • [11]Kawasaki K, Buchanan AV, Weiss KM: Gene duplication and the evolution of vertebrate skeletal mineralization. Cells Tissues Organs 2007, 186:7-24.
  • [12]Kawasaki K, Amemiya CT: SCPP genes in the coelacanth: tissue mineralization genes shared by sarcopterygians. J Exp Zool B Mol Dev Evol 2014, 322:390-402.
  • [13]Hedges SB. Vertebrates (Vertebrata). In: Hedges SB and Kumar S, editors. Timetree of Life. New York: Oxford University Press; 2009. p. 309–314.
  • [14]Kawasaki K: The SCPP gene family and the complexity of hard tissues in vertebrates. Cells Tissues Organs 2011, 194:108-12.
  • [15]Al-Hashimi N, Lafont A-G, Delgado S, Kawasaki K, Sire J-Y: The enamelin genes in lizard, crocodile, and frog and the pseudogene in the chicken provide New insights on enamelin evolution in tetrapods. Mol Biol Evol 2010, 27:2078-94.
  • [16]Huq NL, Cross KJ, Ung M, Reynolds EC: A review of protein structure and gene organisation for proteins associated with mineralised tissue and calcium phosphate stabilisation encoded on human chromosome 4. Arch Oral Biol 2005, 50:599-609.
  • [17]Gasse B, Silvent J, Sire J-Y: Evolutionary analysis suggests that AMTN is enamel-specific and a candidate for AI. J Dent Res 2012, 91:1085-9.
  • [18]Sire J-Y, Davit-Béal T, Delgado S, Gu X: The origin and evolution of enamel mineralization genes. Cells Tissues Organs 2007, 186:25-48.
  • [19]Toyosawa S, O’hUigin C, Figueroa F, Tichy H, Klein J: Identification and characterization of amelogenin genes in monotremes, reptiles, and amphibians. Proc Natl Acad Sci U S A 1998, 95:13056-61.
  • [20]Shintani S, Kobata M, Toyosawa S, Ooshima T: Identification and characterization of ameloblastin gene in an amphibian, Xenopus laevis. Gene 2003, 318:125-36.
  • [21]Somogyi-Ganss E, Nakayama Y, Iwasaki K, Nakano Y, Stolf D, McKee MD, et al.: Comparative Temporospatial expression profiling of murine amelotin protein during amelogenesis. Cells Tissues Organs 2012, 195:535-49.
  • [22]Dos Santos NJ, Wazen RM, Kuroda S, Francis Zalzal S, Moffatt P, Nanci A: Odontogenic ameloblast-associated and amelotin are novel basal lamina components. Histochem Cell Biol 2012, 137:329-38.
  • [23]Holcroft J, Ganss B: Identification of Amelotin- and ODAM-interacting enamel matrix proteins using the yeast two-hybrid system. Eur J Oral Sci 2011, 119(Suppl 1):301-6.
  • [24]Nishio C, Wazen R, Kuroda S, Moffatt P, Nanci A: Expression pattern of odontogenic ameloblast-associated and amelotin during formation and regeneration of the junctional epithelium. Eur Cell Mater 2010, 20:393-402.
  • [25]Gao Y, Wang W, Sun Y, Zhang J, Li D, Wei Y, Han T. Distribution of amelotin in mouse tooth development. Anat Rec. 2010;293:135–40.
  • [26]Lacruz RS, Nakayama Y, Holcroft J, Nguyen V, Somogyi-Ganss E, Snead ML, et al.: Targeted overexpression of amelotin disrupts the microstructure of dental enamel. PLoS One 2012, 7:e35200.
  • [27]Abbarin N, Miguel SS, Holcroft J, Iwasaki K, Ganss B. The enamel protein amelotin is a promoter of hydroxyapatite mineralization. J Bone Miner Res. 2014; doi:10.1002/jbmr.2411.
  • [28]Ensembl [http://www.ensembl.org/index.html]
  • [29]NCBI [http://www.ncbi.nlm.nih.gov]
  • [30]UniDPlot [http://www.ese.u-psud.fr/epc/conservation/UniDPlot/]
  • [31]Sire J-Y, Delgado SC, Girondot M: Hen’s teeth with enamel cap: from dream to impossibility. BMC Evol Biol 2008, 8:246. BioMed Central Full Text
  • [32]Jean-Yves SIRE personal website. [http://jysire.free.fr/]
  • [33]Primer3 v.0.4.0 [http://frodo.wi.mit.edu/primer3/]
  • [34]Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-86.
  • [35]Gayral P, Weinert L, Chiari Y, Tsagkogeorga G, Ballenghien M, Galtier N: Next-generation sequencing of transcriptomes: a guide to RNA isolation in nonmodel animals. Mol Ecol Resour 2011, 11:650-61.
  • [36]MBB platform [http://mbb.univ-montp2.fr/MBB//index.php]
  • [37]Se-Al v2.0a11 [http://tree.bio.ed.ac.uk/software/seal]
  • [38]SignalP 4.1 [http://www.cbs.dtu.dk/services/SignalP]
  • [39]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-6.
  • [40]Prosite [http://prosite.expasy.org/]
  • [41]Sigrist CJA, De Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, et al.: New and continuing developments at PROSITE. Nucleic Acids Res 2013, 41:D344-7.
  • [42]Gallien L, Durocher M: Table chronologique du développement chez Pleurodeles waltlii Michah. Bull Biol Fr Belg 1957, 91:97-114.
  • [43]Wang X, Wang S, Lu Y, Gibson MP, Liu Y, Yuan B, et al.: FAM20C plays an essential role in the formation of murine teeth. J Biol Chem 2012, 287:35934-42.
  • [44]TimeTree [http://www.timetree.net]
  • [45]Madsen O: Mammals (Mammalia). In The timetree of life. Edited by Hedges SB, Kumar S. Oxford University Press, New York; 2009:459-61.
  • [46]Cannatella DC, Vieitesb DR, Zhangb P, Wakeb MH, Wakeb DB: Amphibians (Lissamphibia). In The timetree of life. Edited by Hedges SB, Kumar S. Oxford University Press, New York; 2009:353-6.
  • [47]Shedlock AM, Edwards SV: Amniotes (amniota). In The timetree of life. Edited by Hedges SB, Kumar S. Oxford University Press, New York; 2009:375-9.
  • [48]Ruoslahti E: Rgd and other recognition sequences for integrins. Annu Rev Cell Dev Biol 1996, 12:697-715.
  • [49]Davit-Béal T, Tucker AS, Sire J-Y. Loss of teeth and enamel in tetrapods: fossil rcord, genetic data and morphological adaptations. J Anat. 2009;214:477–501.
  • [50]Al-Hashimi N, Sire J-Y, Delgado S: Evolutionary analysis of mammalian enamelin, the largest enamel protein, supports a crucial role for the 32-kDa peptide and reveals selective adaptation in rodents and primates. J Mol Evol 2009, 69:635-56.
  • [51]Delgado S, Davit-Béal T, Allizard F, Sire J-Y: Tooth development in a scincid lizard, Chalcides viridanus (Squamata), with particular attention to enamel formation. Cell Tissue Res 2005, 319:71-89.
  • [52]Delgado S, Couble M-L, Magloire H, Sire J-Y: Cloning, sequencing, and expression of the amelogenin gene in Two scincid lizards. J Dent Res 2006, 85:138-43.
  • [53]Davit-Béal T, Allizard F, Sire J-Y: Enameloid/enamel transition through successive tooth replacements in Pleurodeles waltl (Lissamphibia, Caudata). Cell Tissue Res 2007, 328:167-83.
  • [54]Sasagawa I, Ferguson MW: The development of enamel tubules during the formation of enamel in the marsupial Monodelphis domestica. J Anat 1991, 179:47-58.
  • [55]Assaraf-Weill N, Gasse B, Al-Hashimi N, Delgado S, Sire J-Y, Davit-Béal T: Conservation of amelogenin gene expression during tetrapod evolution. J Exp Zool B Mol Dev Evol 2013, 320:200-9.
  • [56]Davit-Béal T, Allizard F, Sire J-Y: Morphological variations in a tooth family through ontogeny in Pleurodeles waltl (Lissamphibia, Caudata). J Morphol 2006, 267:1048-65.
  • [57]Davit-Béal T, Chisaka H, Delgado S, Sire J-Y: Amphibian teeth: current knowledge, unanswered questions, and some directions for future research. Biol Rev 2007, 82:49-81.
  • [58]Sawada T, Yamazaki T, Shibayama K, Kumazawa K, Yamaguchi Y, Ohshima M: Expression and localization of laminin 5, laminin 10, type IV collagen, and amelotin in adult murine gingiva. J Mol Histol 2014, 45:293-302.
  • [59]Nishio C, Wazen R, Kuroda S, Moffatt P, Nanci A: Disruption of periodontal integrity induces expression of apin by epithelial cell rests of Malassez. J Periodontal Res 2010, 45:709-13.
  • [60]Meredith RW, Gatesy J, Springer MS: Molecular decay of enamel matrix protein genes in turtles and other edentulous amniotes. BMC Evol Biol 2013, 13:20. BioMed Central Full Text
  • [61]Louchart A, Viriot L: From snout to beak: the loss of teeth in birds. Trends Ecol Evol 2011, 26:663-73.
  • [62]Chiari Y, Cahais V, Galtier N, Delsuc F: Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria). BMC Biol 2012, 10:65. BioMed Central Full Text
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