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

  • Nawfal Al-Hashimi
  • Jean-Yves Sire
  • Sidney Delgado
Article

Abstract

Enamelin (ENAM) plays an important role in the mineralization of the forming enamel matrix. We have performed an evolutionary analysis of mammalian ENAM to identify highly conserved residues or regions that could have important function (selective pressure), to predict mutations that could be associated with amelogenesis imperfecta in humans, and to identify possible adaptive evolution of ENAM during 200 million years ago of mammalian evolution. In order to fulfil these objectives, we obtained 36-ENAM sequences that are representative of the mammalian lineages. Our results show a remarkably high conservation pattern in the region of the 32-kDa fragment of ENAM, especially its phosphorylation, glycosylation, and proteolytic sites. In primates and rodents we also identified several sites under positive selection, which could indicate recent evolutionary changes in ENAM function. Furthermore, the analysis of the unusual signal peptide provided new insights on the possible regulation of ENAM secretion, a hypothesis that should be tested in the near future. Taken together, these findings improve our understanding of ENAM evolution and provide new information that would be useful for further investigation of ENAM function as well as for the validation of mutations leading to amelogenesis imperfecta.

Keywords

Enamelin Evolution Teeth Mammals Purifying selection Positive selection 

Notes

Acknowledgments

We thank Mehboob Chilwan (Erasmus, University of Keele, UK) for English corrections. This work was supported by CNRS and UPMC (UMR 7138) Grants.

Supplementary material

239_2009_9302_MOESM1_ESM.doc (120 kb)
Amino acid alignment of the 36 mammalian ENAMs analyzed. The sequences were aligned against the human sequence and are ordered following the mammalian relationships shown in Fig. 3. The 24 complete sequences are indicated in bold characters. This alignment leads to 1,550 positions (including all gaps). The signal peptide (exons 3 and 4) is underlined. Remarkably conserved residues and motifs are on gray background.][: exon limits; (.): residue identical to human ENAM residue; (−): indel; (=): unknown amino acid; (#): the 77 residues identical in all sequences; (+): the 10 site-specific positive selection in human ENAM (see also Figs. 5 and 7).(DOC 120 kb)
239_2009_9302_MOESM2_ESM.doc (78 kb)
Comparison of the 20 nucleotides located at the 5′ and 3′ UTR, and at both splice sites of introns 3–9 in ten ENAM sequences of species representative of the main mammalian lineages. Conserved positions are indicated in bold characters. Three mutations at the splicing sites (boxed bp) are known to lead to AIH2 (see Fig. 1).(DOC 78 kb)
239_2009_9302_MOESM3_ESM.doc (70 kb)
Substitution rates calculated for 22 mammalian ENAMs taken two by two using the HyPhy program.(DOC 69 kb)

References

  1. Aoba T, Moreno EC (1987) The enamel fluid in the early secretory stage of porcine amelogenesis: chemical composition and saturation with respect to enamel mineral. Calcif Tissue Int 41:86–94CrossRefPubMedGoogle Scholar
  2. Brookes SJ, Lyngstadaas SP, Robinson C, Shore RC, Wood SR, Kirkham J (2002) Enamelin compartmentalization in developing porcine enamel. Connect Tissue Res 43:477–481PubMedGoogle Scholar
  3. Chen Y-C, Peng G-S, Wang M-F, Tsao T-P, Yin S-J (2009) Polymorphism of ethanol-metabolism genes and alcoholism: correlation of allelic variations with the pharmacokinetic and pharmacodynamic consequences. Chem Biol Int 178:2–7CrossRefGoogle Scholar
  4. Davis MJ, Hanson KA, Clark F, Fink JL, Zhang F, Kasukawa T, Kai C, Kawai J, Carninci P, Hayashizaki Y, Teasdale RD (2006) Differential use of signal peptides and membrane domains is a common occurrence in the protein output of transcriptional units. PLoS Genet 2:e46CrossRefPubMedGoogle Scholar
  5. Davit-Béal T, Tucker T, Sire JY (2009) Loss of teeth and enamel in tetrapods: fossil record, genetic data and morphological adaptations. J Anat 214:277–501CrossRefGoogle Scholar
  6. Dayhoff MO, Schwartz R, Orcutt BC (1978) A model of evolutionary change in proteins, matrixes for detecting distant relationships. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5. National Biomedical Research Foundation, Washington, DC, pp 345–358Google Scholar
  7. Delgado S, Casane D, Bonnaud L, Laurin M, Sire JY, Girondot M (2001) Molecular evidence for Precambrian origin of amelogenin, the major protein of vertebrate enamel. Mol Biol Evol 18:2146–2153PubMedGoogle Scholar
  8. Delgado S, Girondot M, Sire JY (2005) Molecular evolution of amelogenin in mammals. J Mol Evol 60:12–30CrossRefPubMedGoogle Scholar
  9. Delgado S, Couble ML, Magloire H, Sire JY (2006) Cloning, sequencing, and expression of the amelogenin gene in two scincid lizards. J Dent Res 85:138–143CrossRefPubMedGoogle Scholar
  10. Delgado S, Ishiyama M, Sire JY (2007) Validation of amelogenesis imperfecta inferred from amelogenin evolution. J Dent Res 86:326–330CrossRefPubMedGoogle Scholar
  11. Deméré TA, McGowen MR, Berta A, Gatesy J (2008) Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Syst Biol 57:15–37CrossRefPubMedGoogle Scholar
  12. Deutsch D (1989) Structure and function of enamel gene products. Anat Rec 224:189–210CrossRefPubMedGoogle Scholar
  13. Dong J, Gu TT, Simmons D, MacDougall M (2000) Enamelin maps to human chromosome 4q21 within the autosomal dominant amelogenesis imperfecta locus. Eur J Oral Sci 108:353–358CrossRefPubMedGoogle Scholar
  14. Doron-Faigenboim A, Stern A, Mayrose I, Bacharach E, Pupko T (2005) Selecton: a server for detecting evolutionary forces at a single amino-acid site. Bioinformatics 21:2101–2103CrossRefPubMedGoogle Scholar
  15. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z (2002) Intrinsic disorder and protein function. Biochemistry 41:6573–6582CrossRefPubMedGoogle Scholar
  16. Endo T, Ikeo K, Gojobori T (1996) Large-scale search for genes on which positive selection may operate. Mol Biol Evol 13:685–690PubMedGoogle Scholar
  17. Fan D, Lakshminarayanan R, Moradian-Oldak J (2008) The 32 kDa enamelin undergoes conformational transitions upon calcium binding. J Struct Biol 163:109–115CrossRefPubMedGoogle Scholar
  18. Fisher LW, Fedarko NS (2003) Six genes expressed in bones and teeth encode the current members of the SIBLING family of proteins. Connect Tissue Res 44(Suppl 1):33–40PubMedGoogle Scholar
  19. Fukae M, Tanabe T (1985) Separation of non-amelogenin component from purified amelogenin preparation of immature porcine enamel. Jpn J Oral Biol 27:1249–1251Google Scholar
  20. Fukae M, Tanabe T (1987) Nonamelogenin components of porcine enamel in the protein fraction free from the enamel crystals. Calcif Tissue Int 40:286–293CrossRefPubMedGoogle Scholar
  21. Fukae M, Tanabe T, Murakami C, Dohi N, Uchida T, Shimizu M (1996) Primary structure of the porcine 89-kDa enamelin. Adv Dent Res 10:111–118CrossRefPubMedGoogle Scholar
  22. Gomis-Ruth FX, Bayes A, Sotiropoulou G, Pampalakis G, Tsetsenis T, Villegas V, Aviles FX, Coll M (2002) The structure of human prokallikrein 6 reveals a novel activation mechanism for the kallikrein family. J Biol Chem 277:27273–27281CrossRefPubMedGoogle Scholar
  23. Gutierrez SJ, Chaves M, Torres DM, Briceno I (2007) Identification of a novel mutation in the enamelin gene in a family with autosomal-dominant amelogenesis imperfecta. Arch Oral Biol 52:503–506CrossRefPubMedGoogle Scholar
  24. Hart PS, Michalec MD, Seow WK, Hart TC, Wright JT (2003a) Identification of the enamelin (g.8344delG) mutation in a new kindred and presentation of a standardized ENAM nomenclature. Arch Oral Biol 48:589–596CrossRefPubMedGoogle Scholar
  25. Hart TC, Hart PS, Gorry MC, Michalec MD, Ryu OH, Uygur C, Ozdemir D, Firatli S, Aren G, Firatli E (2003b) Novel ENAM mutation responsible for autosomal recessive amelogenesis imperfecta and localised enamel defects. J Med Genet 40:900–906CrossRefPubMedGoogle Scholar
  26. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefPubMedGoogle Scholar
  27. Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266:383–402CrossRefPubMedGoogle Scholar
  28. Hiss JA, Resch E, Schreiner A, Meissner M, Starzinski-Powitz A, Schneider G (2008) Domain organization of long signal peptides of single-pass integral membrane proteins reveals multiple functional capacity. PLoS ONE 3:e2767CrossRefPubMedGoogle Scholar
  29. Hu JC, Yamakoshi Y (2003) Enamelin and autosomal-dominant amelogenesis imperfecta. Crit Rev Oral Biol Med 14:387–398CrossRefPubMedGoogle Scholar
  30. Hu C-C, Fukae M, Uchida T, Qian Q, Zhang CH, Ryu OH, Tanabe T, Yamakoshi Y, Murakami C, Dohi N, Shimizu M, Simmer JP (1997a) Cloning and characterization of porcine enamelin mRNAs. J Dent Res 76:1720–1729CrossRefPubMedGoogle Scholar
  31. Hu CC, Fukae M, Uchida T, Qian Q, Zhang CH, Ryu OH, Tanabe T, Yamakoshi Y, Murakami C, Dohi N, Shimizu M, Simmer JP (1997b) Sheathlin: cloning, cDNA/polypeptide sequences, and immunolocalization of porcine enamel sheath proteins. J Dent Res 76:648–657CrossRefPubMedGoogle Scholar
  32. Hu CC, Simmer JP, Bartlett JD, Qian Q, Zhang C, Ryu OH, Xue J, Fukae M, Uchida T, MacDougall M (1998) Murine enamelin: cDNA and derived protein sequences. Connect Tissue Res 39:47–61CrossRefPubMedGoogle Scholar
  33. Hu CC, Hart TC, Dupont BR, Chen JJ, Sun X, Qian Q, Zhang CH, Jiang H, Mattern VL, Wright JT, Simmer JP (2000) Cloning human enamelin cDNA, chromosomal localization, and analysis of expression during tooth development. J Dent Res 79:912–919CrossRefPubMedGoogle Scholar
  34. Hu JC, Zhang CH, Yang Y, Karrman-Mardh C, Forsman-Semb K, Simmer JP (2001) Cloning and characterization of the mouse and human enamelin genes. J Dent Res 80:898–902CrossRefPubMedGoogle Scholar
  35. Hu JC, Yamakoshi Y, Yamakoshi F, Krebsbach PH, Simmer JP (2005) Proteomics and genetics of dental enamel. Cells Tissues Organs 181:219–231CrossRefPubMedGoogle Scholar
  36. Hu JC, Hu Y, Smith CE, McKee MD, Wright JT, Yamakoshi Y, Papagerakis P, Hunter GK, Feng JQ, Yamakoshi F, Simmer JP (2008) Enamel defects and ameloblast-specific expression in Enam knock-out/lacz knock-in mice. J Biol Chem 283:10858–10871CrossRefPubMedGoogle Scholar
  37. Kang HY, Seymen F, Lee SK, Yildirim M, Tuna EB, Patir A, Lee KE, Kim JW (2009) Candidate gene strategy reveals ENAM mutations. J Dent Res 88:266–269PubMedGoogle Scholar
  38. Kawasaki K, Weiss KM (2003) Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proc Natl Acad Sci USA 100:4060–4065CrossRefPubMedGoogle Scholar
  39. Kawasaki K, Weiss KM (2008) SCPP gene evolution and the dental mineralization continuum. J Dent Res 87:520–531CrossRefPubMedGoogle Scholar
  40. Kelley JL, Swanson WJ (2008) Dietary change and adaptive evolution of enamelin in humans and among Primates. Genetics 178:1595–1603CrossRefPubMedGoogle Scholar
  41. Kim JW, Seymen F, Lin BP, Kiziltan B, Gencay K, Simmer JP, Hu JC (2005a) ENAM mutations in autosomal-dominant amelogenesis imperfecta. J Dent Res 84:278–282CrossRefPubMedGoogle Scholar
  42. Kim JW, Hu JCC, Lee JI, Moon SK, Kim YJ, Jang KT, Lee SH, Kim CC, Hahn SH, Simmer JP (2005b) Mutational hot spot in the DSPP gene causing dentinogenesis imperfecta type II. Hum Genet 116:186–191CrossRefPubMedGoogle Scholar
  43. Pond SLK, Frost SD (2005a) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222CrossRefGoogle Scholar
  44. Pond SLK, Frost SD (2005b) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533CrossRefPubMedGoogle Scholar
  45. Pond SLK, Frost SD, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679CrossRefPubMedGoogle Scholar
  46. Kozak M (1984) Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res 12:857–872CrossRefPubMedGoogle Scholar
  47. Kozak M (1991) A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes. Gene Expr 1:111–115PubMedGoogle Scholar
  48. Kurys G, Tagaya Y, Bamford R, Hanover JA, Waldmann TA (2000) The long signal peptide isoform and its alternative processing direct the intracellular trafficking of interleukin-15. J Biol Chem 275:30653–30659CrossRefPubMedGoogle Scholar
  49. Lu Y, Papagerakis P, Yamakoshi Y, Hu JC, Bartlett JD, Simmer JP (2008) Functions of KLK4 and MMP-20 in dental enamel formation. Biol Chem 389:695–700CrossRefPubMedGoogle Scholar
  50. Mårdh CK, Bäckman B, Holmgren G, Hu JC, Simmer JP, Forsman-Semb K (2002) A nonsense mutation in the enamelin gene causes local hypoplastic autosomal dominant amelogenesis imperfecta (AIH2). Hum Mol Genet 11(9):1069–1074CrossRefPubMedGoogle Scholar
  51. Martoglio B, Dobberstein B (1998) Signal sequences: more than just greasy peptides. Trends Cell Biol 8:410–415CrossRefPubMedGoogle Scholar
  52. Masuya H, Shimizu K, Sezutsu H, Sakuraba Y, Nagano J, Shimizu A, Fujimoto N, Kawai A, Miura I, Kaneda H, Kobayashi K, Ishijima J, Maeda T, Gondo Y, Noda T, Wakana S, Shiroishi T (2005) Enamelin (Enam) is essential for amelogenesis: ENU-induced mouse mutants as models for different clinical subtypes of human amelogenesis imperfecta (AI). Hum Mol Genet 14:575–583CrossRefPubMedGoogle Scholar
  53. Ozdemir D, Hart PS, Firatli E, Aren G, Ryu OH, Hart TC (2005) Phenotype of ENAM mutations is dosage-dependent. J Dent Res 84:1036–1041CrossRefPubMedGoogle Scholar
  54. Patthy L (1999) Genome evolution and the evolution of exon-shuffling—a review. Gene 238:103–114CrossRefPubMedGoogle Scholar
  55. Rajpar MH, Harley K, Laing C, Davies RM, Dixon MJ (2001) Mutation of the gene encoding the enamel-specific protein, enamelin, causes autosomal-dominant amelogenesis imperfecta. Hum Mol Genet 10:1673–1677CrossRefPubMedGoogle Scholar
  56. Rambaut A, Bromham L (1998) Estimating divergence dates from molecular sequences. Mol Biol Evol 15:442–448PubMedGoogle Scholar
  57. Ravindranath RM, Moradian-Oldak J, Fincham AG (1999) Tyrosyl motif in amelogenins binds N-acetyl-D-glucosamine. J Biol Chem 274:2464–2471CrossRefPubMedGoogle Scholar
  58. Ravindranath HH, Chen LS, Zeichner-David M, Ishima R, Ravindranath RM (2004) Interaction between the enamel matrix proteins amelogenin and ameloblastin. Biochem Biophys Res Commun 323:1075–1083CrossRefPubMedGoogle Scholar
  59. Reuter M, Engelstadter J, Fontanillas P, Hurst LD (2008) A test of the null model for 5′ UTR evolution based on GC content. Mol Biol Evol 25:801–804CrossRefPubMedGoogle Scholar
  60. Ryu OH, Fincham AG, Hu CC, Zhang C, Qian Q, Bartlett JD, Simmer JP (1999) Characterization of recombinant pig enamelysin activity and cleavage of recombinant pig and mouse amelogenins. J Dent Res 78:743–750CrossRefPubMedGoogle Scholar
  61. Sansom IJ, Smith MP, Armstrong HA, Smith MM (1992) Presence of the earliest vertebrate hard tissue in conodonts. Science 256:1308–1311CrossRefPubMedGoogle Scholar
  62. Schmid K, Yang Z (2008) The trouble with sliding windows and the selective pressure in BRCA1. PLoS ONE 3(11):e3746CrossRefPubMedGoogle Scholar
  63. Seedorf H, Klaften M, Eke F, Fuchs H, Seedorf U, Hrabe de Angelis M (2007) A mutation in the enamelin gene in a mouse model. J Dent Res 86:764–768CrossRefPubMedGoogle Scholar
  64. Sire JY, Delgado S, Fromentin D, Girondot M (2005) Amelogenin: lessons from evolution. Arch Oral Biol 50:205–212CrossRefPubMedGoogle Scholar
  65. Sire JY, Delgado S, Girondot M (2006) The amelogenin story: origin and evolution. Eur J Oral Sci 114(Suppl 1):64–77CrossRefPubMedGoogle Scholar
  66. Sire JY, Davit-Béal T, Delgado S, Gu X (2007) The origin and evolution of enamel mineralization genes. Cells Tissues Organs 186:25–48CrossRefPubMedGoogle Scholar
  67. Sire JY, Delgado S, Girondot M (2008) Hen’s teeth with enamel cap: from dream to impossibility. BMC Evol Biol 8:e246CrossRefGoogle Scholar
  68. Springer MS, Murphy WJ (2007) Mammalian evolution and biomedicine: new views from phylogeny. Biol Rev Camb Philos Soc 82:375–392CrossRefPubMedGoogle Scholar
  69. Stern A, Doron-Faigenboim A, Erez E, Martz E, Bacharach E, Pupko T (2007) Selecton 2007: advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res 35:W506–W511CrossRefPubMedGoogle Scholar
  70. Subramanian S, Kumar S (2006) Evolutionary anatomies of positions and types of disease-associated and neutral amino acid mutations in the human genome. BMC Genomics 7:e306CrossRefGoogle Scholar
  71. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  72. Tanabe T, Aoba T, Moreno EC, Fukae M, Shimuzu M (1990) Properties of phosphorylated 32 kd nonamelogenin proteins isolated from porcine secretory enamel. Calcif Tissue Int 46:205–215CrossRefPubMedGoogle Scholar
  73. Tanabe T, Fukae M, Shimizu M (1994) Degradation of enamelins by proteinases found in porcine secretory enamel in vitro. Arch Oral Biol 39:277–281CrossRefPubMedGoogle Scholar
  74. Termine JD, Belcourt AB, Christner PJ, Conn KM, Nylen MU (1980) Properties of dissociatively extracted fetal tooth matrix proteins. I. Principal molecular species in developing bovine enamel. J Biol Chem 255:9760–9768PubMedGoogle Scholar
  75. Tsunoyama K, Gojobori T (1998) Evolution of nicotinic acetylcholine receptor subunits. Mol Biol Evol 15:518–527PubMedGoogle Scholar
  76. Uchida T, Tanabe T, Fukae M, Shimizu M, Yamada M, Miake K, Kobayashi S (1991a) Immunochemical and immunohistochemical studies, using antisera against porcine 25 kDa amelogenin, 89 kDa enamelin and the 13–17 kDa nonamelogenins, on immature enamel of the pig and rat. Histochemistry 96:129–138CrossRefPubMedGoogle Scholar
  77. Uchida T, Tanabe T, Fukae M, Shimizu M (1991b) Immunocytochemical and immunochemical detection of a 32 kDa nonamelogenin and related proteins in porcine tooth germs. Arch Histol Cytol 54:527–538CrossRefPubMedGoogle Scholar
  78. van Rheede T, Bastiaans T, Boone DN, Hedges SB, de Jong WW, Madsen O (2006) The platypus is in its place: nuclear genes and indels confirm the sister group relation of monotremes and therians. Mol Biol Evol 23:587–597CrossRefPubMedGoogle Scholar
  79. von Heijne G (1985) Signal sequences: the limits of variation. J Mol Biol 184:99–105CrossRefGoogle Scholar
  80. Warren WC, Hillier LW, Marshall Graves JA, Birney E, Ponting CP, Grutzner F, Belov K, Miller W, Clarke L, Chinwalla AT, Yang SP, Heger A, Locke DP, Miethke P, Waters PD, Veyrunes F, Fulton L, Fulton B, Graves T, Wallis J, Puente XS, Lopez-Otin C, Ordonez GR, Eichler EE, Chen L, Cheng Z, Deakin JE, Alsop A, Thompson K, Kirby P, Papenfuss AT, Wakefield MJ, Olender T, Lancet D, Huttley GA, Smit AF, Pask A, Temple-Smith P, Batzer MA, Walker JA, Konkel MK, Harris RS, Whittington CM, Wong ES, Gemmell NJ, Buschiazzo E, Vargas Jentzsch IM, Merkel A, Schmitz J, Zemann A, Churakov G, Kriegs JO, Brosius J, Murchison EP, Sachidanandam R, Smith C, Hannon GJ, Tsend-Ayush E, McMillan D, Attenborough R, Rens W, Ferguson-Smith M, Lefevre CM, Sharp JA, Nicholas KR, Ray DA, Kube M, Reinhardt R, Pringle TH, Taylor J, Jones RC, Nixon B, Dacheux JL, Niwa H, Sekita Y, Huang X, Stark A, Kheradpour P, Kellis M, Flicek P, Chen Y, Webber C, Hardison R, Nelson J, Hallsworth-Pepin K, Delehaunty K, Markovic C, Minx P, Feng Y, Kremitzki C, Mitreva M, Glasscock J, Wylie T, Wohldmann P, Thiru P, Nhan MN, Pohl CS, Smith SM, Hou S, Renfree MB (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature 453:175–183CrossRefPubMedGoogle Scholar
  81. Weiner S (1986) Organization of extracellularly mineralized tissues: a comparative study of biological crystal growth. CRC Crit Rev Biochem 20:365–408CrossRefPubMedGoogle Scholar
  82. Yamakoshi Y (1995) Carbohydrate moieties of porcine 32 kDa enamelin. Calcif Tissue Int 56:323–330CrossRefPubMedGoogle Scholar
  83. Yamakoshi Y, Pinheiro FH, Tanabe T, Fukae M, Shimizu M (1998) Sites of asparagine-linked oligosaccharides in porcine 32 kDa enamelin. Connect Tissue Res 39:39–46CrossRefPubMedGoogle Scholar
  84. Yamakoshi Y, Hu JC, Liu S, Zhang C, Oida S, Fukae M, Simmer JP (2003) Characterization of porcine dentin sialoprotein (DSP) and dentin sialophosphoprotein (DSPP) cDNA clones. Eur J Oral Sci 111:60–67CrossRefPubMedGoogle Scholar
  85. Yamakoshi Y, Hu JC, Fukae M, Yamakoshi F, Simmer JP (2006) How do enamelysin and kallikrein 4 process the 32-kDa enamelin? Eur J Oral Sci 114(Suppl 1):45–51CrossRefPubMedGoogle Scholar
  86. Yoon H, Laxmikanthan G, Lee J, Blaber SI, Rodriguez A, Kogot JM, Scarisbrick IA, Blaber M (2007) Activation profiles anad regulatory cascades of the human kallikrein-related peptidases. J Biol Chem 282:31852–31864CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Nawfal Al-Hashimi
    • 1
  • Jean-Yves Sire
    • 1
  • Sidney Delgado
    • 1
  1. 1.Université Pierre et Marie Curie, UMR 7138—Systématique, Adaptation, EvolutionParisFrance

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