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

Journal of Molecular Evolution

Volumn 69, Issue 6, 2009, Pages 635-656

  Al Hashimi, Nawfal ^a   Sire, Jean Yves ^a   Delgado, Sidney ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

Enamelin; Evolution; Mammals; Positive selection; Purifying selection; Teeth

Indexed keywords

ENAMEL PROTEIN; ENAMELIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

AMELOGENESIS IMPERFECTA; AMINO ACID SEQUENCE; ARTICLE; CONSERVATION BIOLOGY; EVOLUTIONARY ADAPTATION; GLYCOSYLATION; HUMAN; MAMMAL; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMATE; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; REGULATORY MECHANISM; RODENT; VALIDATION PROCESS;

AMELOGENESIS IMPERFECTA; AMINO ACID SEQUENCE; ANIMALS; DENTAL ENAMEL; DENTAL ENAMEL PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDES; PRIMATES; PROTEIN SORTING SIGNALS; RODENTIA; SELECTION, GENETIC; TOOTH;

MAMMALIA; PRIMATES; RODENTIA;

EID: 72449159548     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-009-9302-x     Document Type: Article

References (86)

1. T Aoba EC Moreno 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 94 10.1007/BF02555250 1:CAS:528: DyaL2sXltlWltLg%3D 3115550
2. SJ Brookes SP Lyngstadaas C Robinson RC Shore SR Wood J Kirkham 2002 Enamelin compartmentalization in developing porcine enamel Connect Tissue Res 43 477 481 1:CAS:528:DC%2BD38Xmt1ahu7g%3D 12489201
3. Y-C Chen G-S Peng M-F Wang T-P Tsao S-J Yin 2009 Polymorphism of ethanol-metabolism genes and alcoholism: correlation of allelic variations with the pharmacokinetic and pharmacodynamic consequences Chem Biol Int 178 2 7 10.1016/j.cbi.2008.10.029 1:CAS:528:DC%2BD1MXhsFOjtLc%3D
4. MJ Davis KA Hanson F Clark JL Fink F Zhang T Kasukawa C Kai J Kawai P Carninci Y Hayashizaki RD Teasdale 2006 Differential use of signal peptides and membrane domains is a common occurrence in the protein output of transcriptional units PLoS Genet 2 e46 10.1371/journal.pgen.0020046 16683029
5. T Davit-Béal T Tucker JY Sire 2009 Loss of teeth and enamel in tetrapods: fossil record, genetic data and morphological adaptations J Anat 214 277 501 10.1111/j.1469-7580.2009.01060.x
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 345-358
7. S Delgado D Casane L Bonnaud M Laurin JY Sire M Girondot 2001 Molecular evidence for Precambrian origin of amelogenin, the major protein of vertebrate enamel Mol Biol Evol 18 2146 2153 1:CAS:528:DC%2BD3MXptFCrs7w%3D 11719563
8. S Delgado M Girondot JY Sire 2005 Molecular evolution of amelogenin in mammals J Mol Evol 60 12 30 10.1007/s00239-003-0070-8 1:CAS:528: DC%2BD2MXhtVShsb0%3D 15696365 (Pubitemid 40310755)
9. S Delgado ML Couble H Magloire JY Sire 2006 Cloning, sequencing, and expression of the amelogenin gene in two scincid lizards J Dent Res 85 138 143 10.1177/154405910608500205 1:CAS:528:DC%2BD28Xhs1Gjt7c%3D 16434731 (Pubitemid 43827745)
10. S Delgado M Ishiyama JY Sire 2007 Validation of amelogenesis imperfecta inferred from amelogenin evolution J Dent Res 86 326 330 10.1177/ 154405910708600405 1:CAS:528:DC%2BD2sXltlOhtLY%3D 17384026
11. TA Deméré MR McGowen A Berta J Gatesy 2008 Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales Syst Biol 57 15 37 10.1080/10635150701884632 18266181
12. D Deutsch 1989 Structure and function of enamel gene products Anat Rec 224 189 210 10.1002/ar.1092240209 1:CAS:528:DyaL1MXkvFChsbc%3D 2672884
13. J Dong TT Gu D Simmons M MacDougall 2000 Enamelin maps to human chromosome 4q21 within the autosomal dominant amelogenesis imperfecta locus Eur J Oral Sci 108 353 358 10.1034/j.1600-0722.2000.108005353.x 1:CAS:528: DC%2BD3cXnsFGjtLo%3D 11037750
14. A Doron-Faigenboim A Stern I Mayrose E Bacharach T Pupko 2005 Selecton: a server for detecting evolutionary forces at a single amino-acid site Bioinformatics 21 2101 2103 10.1093/bioinformatics/bti259 1:CAS:528: DC%2BD2MXjsl2ns7s%3D 15647294 (Pubitemid 40668056)
15. AK Dunker CJ Brown JD Lawson LM Iakoucheva Z Obradovic 2002 Intrinsic disorder and protein function Biochemistry 41 6573 6582 10.1021/bi012159+ 1:CAS:528:DC%2BD38Xjt1aitbc%3D 12022860 (Pubitemid 34547347)
16. T Endo K Ikeo T Gojobori 1996 Large-scale search for genes on which positive selection may operate Mol Biol Evol 13 685 690 1:CAS:528: DyaK28Xis1Sms7s%3D 8676743
17. D Fan R Lakshminarayanan J Moradian-Oldak 2008 The 32 kDa enamelin undergoes conformational transitions upon calcium binding J Struct Biol 163 109 115 10.1016/j.jsb.2008.04.007 1:CAS:528:DC%2BD1cXnvVGktb4%3D 18508280
18. LW Fisher NS Fedarko 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 40 1:CAS:528:DC%2BD3sXjtlanu78%3D 12952171
19. M Fukae T Tanabe 1985 Separation of non-amelogenin component from purified amelogenin preparation of immature porcine enamel Jpn J Oral Biol 27 1249 1251 1:CAS:528:DyaL28XkslGgsrw%3D
20. M Fukae T Tanabe 1987 Nonamelogenin components of porcine enamel in the protein fraction free from the enamel crystals Calcif Tissue Int 40 286 293 10.1007/BF02555263 1:CAS:528:DyaL2sXlslSrs78%3D 3034388 (Pubitemid 19014743)
21. M Fukae T Tanabe C Murakami N Dohi T Uchida M Shimizu 1996 Primary structure of the porcine 89-kDa enamelin Adv Dent Res 10 111 118 10.1177/08959374960100020201 1:STN:280:DyaK2szltVKhtg%3D%3D 9206327
22. FX Gomis-Ruth A Bayes G Sotiropoulou G Pampalakis T Tsetsenis V Villegas FX Aviles M Coll 2002 The structure of human prokallikrein 6 reveals a novel activation mechanism for the kallikrein family J Biol Chem 277 27273 27281 10.1074/jbc.M201534200 1:CAS:528:DC%2BD38XlvV2itbs%3D 12016211 (Pubitemid 34951745)
23. SJ Gutierrez M Chaves DM Torres I Briceno 2007 Identification of a novel mutation in the enamelin gene in a family with autosomal-dominant amelogenesis imperfecta Arch Oral Biol 52 503 506 10.1016/j.archoralbio.2006.09.014 1:CAS:528:DC%2BD2sXjtFGltbo%3D 17316551 (Pubitemid 46399641)
24. PS Hart MD Michalec WK Seow TC Hart JT Wright 2003 Identification of the enamelin (g.8344delG) mutation in a new kindred and presentation of a standardized ENAM nomenclature Arch Oral Biol 48 589 596 10.1016/S0003-9969(03) 00114-6 1:CAS:528:DC%2BD3sXkvVWjtr8%3D 12828988 (Pubitemid 36821063)
25. TC Hart PS Hart MC Gorry MD Michalec OH Ryu C Uygur D Ozdemir S Firatli G Aren E Firatli 2003 Novel ENAM mutation responsible for autosomal recessive amelogenesis imperfecta and localised enamel defects J Med Genet 40 900 906 10.1136/jmg.40.12.900 1:CAS:528:DC%2BD2cXht1aqsb4%3D 14684688
26. M Hasegawa H Kishino T Yano 1985 Dating of the human-ape splitting by a molecular clock of mitochondrial DNA J Mol Evol 22 160 174 10.1007/BF02101694 1:CAS:528:DyaL2MXmtFSns7g%3D 3934395 (Pubitemid 16227864)
27. DG Higgins JD Thompson TJ Gibson 1996 Using CLUSTAL for multiple sequence alignments Methods Enzymol 266 383 402 10.1016/S0076-6879(96)66024-8 1:CAS:528:DyaK28Xltl2nt7w%3D 8743695 (Pubitemid 26165878)
28. JA Hiss E Resch A Schreiner M Meissner A Starzinski-Powitz G Schneider 2008 Domain organization of long signal peptides of single-pass integral membrane proteins reveals multiple functional capacity PLoS ONE 3 e2767 10.1371/journal.pone.0002767 18648515
29. JC Hu Y Yamakoshi 2003 Enamelin and autosomal-dominant amelogenesis imperfecta Crit Rev Oral Biol Med 14 387 398 10.1177/154411130301400602 14656895
30. C-C Hu M Fukae T Uchida Q Qian CH Zhang OH Ryu T Tanabe Y Yamakoshi C Murakami N Dohi M Shimizu JP Simmer 1997 Cloning and characterization of porcine enamelin mRNAs J Dent Res 76 1720 1729 10.1177/00220345970760110201 1:CAS:528:DyaK2sXnslyltr8%3D 9372788
31. CC Hu M Fukae T Uchida Q Qian CH Zhang OH Ryu T Tanabe Y Yamakoshi C Murakami N Dohi M Shimizu JP Simmer 1997 Sheathlin: cloning, cDNA/polypeptide sequences, and immunolocalization of porcine enamel sheath proteins J Dent Res 76 648 657 10.1177/00220345970760020501 1:CAS:528:DyaK2sXitVeisrc%3D 9062558
32. CC Hu JP Simmer JD Bartlett Q Qian C Zhang OH Ryu J Xue M Fukae T Uchida M MacDougall 1998 Murine enamelin: cDNA and derived protein sequences Connect Tissue Res 39 47 61 10.3109/03008209809023911 1:STN:280:DC%2BD3crgvFKnsg%3D%3D 11062988
33. CC Hu TC Hart BR Dupont JJ Chen X Sun Q Qian CH Zhang H Jiang VL Mattern JT Wright JP Simmer 2000 Cloning human enamelin cDNA, chromosomal localization, and analysis of expression during tooth development J Dent Res 79 912 919 10.1177/00220345000790040501 1:CAS:528:DC%2BD3cXjslSksr0%3D 10831092
34. JC Hu CH Zhang Y Yang C Karrman-Mardh K Forsman-Semb JP Simmer 2001 Cloning and characterization of the mouse and human enamelin genes J Dent Res 80 898 902 10.1177/00220345010800031001 1:CAS:528:DC%2BD3MXktlWksrs%3D 11379892
35. JC Hu Y Yamakoshi F Yamakoshi PH Krebsbach JP Simmer 2005 Proteomics and genetics of dental enamel Cells Tissues Organs 181 219 231 10.1159/000091383 1:CAS:528:DC%2BD28XjsVektL0%3D 16612087
36. JC Hu Y Hu CE Smith MD McKee JT Wright Y Yamakoshi P Papagerakis GK Hunter JQ Feng F Yamakoshi JP Simmer 2008 Enamel defects and ameloblast-specific expression in Enam knock-out/lacz knock-in mice J Biol Chem 283 10858 10871 10.1074/jbc.M710565200 1:CAS:528:DC%2BD1cXksFagtbo%3D 18252720
37. HY Kang F Seymen SK Lee M Yildirim EB Tuna A Patir KE Lee JW Kim 2009 Candidate gene strategy reveals ENAM mutations J Dent Res 88 266 269 1:CAS:528:DC%2BD1MXltVOiu7Y%3D 19329462
38. K Kawasaki KM Weiss 2003 Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster Proc Natl Acad Sci USA 100 4060 4065 10.1073/pnas.0638023100 1:CAS:528:DC%2BD3sXivFSqu74%3D 12646701 (Pubitemid 36418157)
39. K Kawasaki KM Weiss 2008 SCPP gene evolution and the dental mineralization continuum J Dent Res 87 520 531 10.1177/154405910808700608 1:CAS:528:DC%2BD1cXnvFSjtLk%3D 18502959
40. JL Kelley WJ Swanson 2008 Dietary change and adaptive evolution of enamelin in humans and among Primates Genetics 178 1595 1603 10.1534/genetics.107.077123 1:CAS:528:DC%2BD1cXltFahurw%3D 18245370
41. JW Kim F Seymen BP Lin B Kiziltan K Gencay JP Simmer JC Hu 2005 ENAM mutations in autosomal-dominant amelogenesis imperfecta J Dent Res 84 278 282 10.1177/154405910508400314 1:CAS:528:DC%2BD2MXis1Wlurk%3D 15723871 (Pubitemid 43822038)
42. JW Kim JCC Hu JI Lee SK Moon YJ Kim KT Jang SH Lee CC Kim SH Hahn JP Simmer 2005 Mutational hot spot in the DSPP gene causing dentinogenesis imperfecta type II Hum Genet 116 186 191 10.1007/s00439-004-1223-6 1:CAS:528:DC%2BD2MXntF2ntg%3D%3D 15592686 (Pubitemid 40174004)
43. SLK Pond SD Frost 2005 Not so different after all: a comparison of methods for detecting amino acid sites under selection Mol Biol Evol 22 1208 1222 10.1093/molbev/msi105 1:CAS:528:DC%2BD2MXjvVKitbw%3D (Pubitemid 40577758)
44. SLK Pond SD Frost 2005 Datamonkey: rapid detection of selective pressure on individual sites of codon alignments Bioinformatics 21 2531 2533 10.1093/bioinformatics/bti320 1:CAS:528:DC%2BD2MXktl2ru7g%3D 15713735 (Pubitemid 40731616)
45. SLK Pond SD Frost SV Muse 2005 HyPhy: hypothesis testing using phylogenies Bioinformatics 21 676 679 10.1093/bioinformatics/bti079 1:CAS:528:DC%2BD2MXhslSlurs%3D 15509596 (Pubitemid 40424796)
46. M Kozak 1984 Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs Nucleic Acids Res 12 857 872 10.1093/nar/12.2.857 1:CAS:528:DyaL2cXpslGkuw%3D%3D 6694911
47. M Kozak 1991 A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes Gene Expr 1 111 115 1:STN:280:DyaK38zhsVKqug%3D%3D 1820208
48. G Kurys Y Tagaya R Bamford JA Hanover TA Waldmann 2000 The long signal peptide isoform and its alternative processing direct the intracellular trafficking of interleukin-15 J Biol Chem 275 30653 30659 10.1074/jbc.M002373200 1:CAS:528:DC%2BD3cXnt1agtLk%3D 10869346
49. Y Lu P Papagerakis Y Yamakoshi JC Hu JD Bartlett JP Simmer 2008 Functions of KLK4 and MMP-20 in dental enamel formation Biol Chem 389 695 700 10.1515/BC.2008.080 1:CAS:528:DC%2BD1cXos1ehu7Y%3D 18627287 (Pubitemid 352009413)
50. CK Mårdh B Bäckman G Holmgren JC Hu JP Simmer K Forsman-Semb 2002 A nonsense mutation in the enamelin gene causes local hypoplastic autosomal dominant amelogenesis imperfecta (AIH2) Hum Mol Genet 11 9 1069 1074 10.1093/hmg/11.9.1069 11978766
51. B Martoglio B Dobberstein 1998 Signal sequences: more than just greasy peptides Trends Cell Biol 8 410 415 10.1016/S0962-8924(98)01360-9 1:CAS:528:DyaK1cXmvFWjurw%3D 9789330 (Pubitemid 28458707)
52. H Masuya K Shimizu H Sezutsu Y Sakuraba J Nagano A Shimizu N Fujimoto A Kawai I Miura H Kaneda K Kobayashi J Ishijima T Maeda Y Gondo T Noda S Wakana T Shiroishi 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 14 575 583 10.1093/hmg/ddi054 1:CAS:528: DC%2BD2MXhsFSgs7o%3D 15649948 (Pubitemid 40309583)
53. D Ozdemir PS Hart E Firatli G Aren OH Ryu TC Hart 2005 Phenotype of ENAM mutations is dosage-dependent J Dent Res 84 1036 1041 10.1177/154405910508401113 1:CAS:528:DC%2BD2MXht1Git73P 16246937 (Pubitemid 43828152)
54. L Patthy 1999 Genome evolution and the evolution of exon-shuffling-a review Gene 238 103 114 10.1016/S0378-1119(99)00228-0 1:CAS:528: DyaK1MXntFKnurk%3D 10570989 (Pubitemid 29436102)
55. MH Rajpar K Harley C Laing RM Davies MJ Dixon 2001 Mutation of the gene encoding the enamel-specific protein, enamelin, causes autosomal-dominant amelogenesis imperfecta Hum Mol Genet 10 1673 1677 10.1093/hmg/10.16.1673 1:CAS:528:DC%2BD3MXmtFagtrg%3D 11487571
56. A Rambaut L Bromham 1998 Estimating divergence dates from molecular sequences Mol Biol Evol 15 442 448 1:CAS:528:DyaK1cXitlKiu70%3D 9549094
57. RM Ravindranath J Moradian-Oldak AG Fincham 1999 Tyrosyl motif in amelogenins binds N-acetyl-D-glucosamine J Biol Chem 274 2464 2471 10.1074/jbc.274.4.2464 1:CAS:528:DyaK1MXovVGqsw%3D%3D 9891017 (Pubitemid 29061409)
58. HH Ravindranath LS Chen M Zeichner-David R Ishima RM Ravindranath 2004 Interaction between the enamel matrix proteins amelogenin and ameloblastin Biochem Biophys Res Commun 323 1075 1083 10.1016/j.bbrc.2004.08.207 1:CAS:528:DC%2BD2cXnslKmtbw%3D 15381109 (Pubitemid 39243428)
59. M Reuter J Engelstadter P Fontanillas LD Hurst 2008 A test of the null model for 5′ UTR evolution based on GC content Mol Biol Evol 25 801 804 10.1093/molbev/msn044 1:CAS:528:DC%2BD1cXlvVKhtbY%3D 18296414
60. OH Ryu AG Fincham CC Hu C Zhang Q Qian JD Bartlett JP Simmer 1999 Characterization of recombinant pig enamelysin activity and cleavage of recombinant pig and mouse amelogenins J Dent Res 78 743 750 10.1177/ 00220345990780030601 1:CAS:528:DyaK1MXitFCjtL4%3D 10096449
61. IJ Sansom MP Smith HA Armstrong MM Smith 1992 Presence of the earliest vertebrate hard tissue in conodonts Science 256 1308 1311 10.1126/science. 1598573 1:STN:280:DyaK383osFKqsg%3D%3D 1598573
62. K Schmid Z Yang 2008 The trouble with sliding windows and the selective pressure in BRCA1 PLoS ONE 3 11 e3746 10.1371/journal.pone.0003746 19015730
63. H Seedorf M Klaften F Eke H Fuchs U Seedorf M Hrabe de Angelis 2007 A mutation in the enamelin gene in a mouse model J Dent Res 86 764 768 10.1177/154405910708600815 1:CAS:528:DC%2BD2sXpsF2quro%3D 17652207
64. JY Sire S Delgado D Fromentin M Girondot 2005 Amelogenin: lessons from evolution Arch Oral Biol 50 205 212 10.1016/j.archoralbio.2004.09.004 1:CAS:528:DC%2BD2MXhtlGjsLo%3D 15721151 (Pubitemid 40252941)
65. JY Sire S Delgado M Girondot 2006 The amelogenin story: origin and evolution Eur J Oral Sci 114 Suppl 1 64 77 10.1111/j.1600-0722.2006.00297.x 1:CAS:528:DC%2BD28XlvF2gsr4%3D 16674665
66. JY Sire T Davit-Béal S Delgado X Gu 2007 The origin and evolution of enamel mineralization genes Cells Tissues Organs 186 25 48 10.1159/000102679 17627117 (Pubitemid 47026715)
67. JY Sire S Delgado M Girondot 2008 Hen's teeth with enamel cap: from dream to impossibility BMC Evol Biol 8 e246 10.1186/1471-2148-8-246
68. MS Springer WJ Murphy 2007 Mammalian evolution and biomedicine: new views from phylogeny Biol Rev Camb Philos Soc 82 375 392 10.1111/j.1469-185X.2007. 00016.x 17624960 (Pubitemid 47052387)
69. A Stern A Doron-Faigenboim E Erez E Martz E Bacharach T Pupko 2007 Selecton 2007: advanced models for detecting positive and purifying selection using a Bayesian inference approach Nucleic Acids Res 35 W506 W511 10.1093/nar/gkm382 17586822
70. S Subramanian S Kumar 2006 Evolutionary anatomies of positions and types of disease-associated and neutral amino acid mutations in the human genome BMC Genomics 7 e306 10.1186/1471-2164-7-306 (Pubitemid 46017446)
71. K Tamura M Nei 1993 Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees Mol Biol Evol 10 512 526 1:CAS:528:DyaK3sXks1CksL4%3D 8336541
72. T Tanabe T Aoba EC Moreno M Fukae M Shimuzu 1990 Properties of phosphorylated 32 kd nonamelogenin proteins isolated from porcine secretory enamel Calcif Tissue Int 46 205 215 10.1007/BF02555046 1:CAS:528: DyaK3cXkslGgsbo%3D 2106381
73. T Tanabe M Fukae M Shimizu 1994 Degradation of enamelins by proteinases found in porcine secretory enamel in vitro Arch Oral Biol 39 277 281 10.1016/0003-9969(94)90117-1 1:CAS:528:DyaK2MXhs1amsg%3D%3D 8024491
74. JD Termine AB Belcourt PJ Christner KM Conn MU Nylen 1980 Properties of dissociatively extracted fetal tooth matrix proteins. I. Principal molecular species in developing bovine enamel J Biol Chem 255 9760 9768 1:CAS:528:DyaL3cXlvF2murY%3D 7430099
75. K Tsunoyama T Gojobori 1998 Evolution of nicotinic acetylcholine receptor subunits Mol Biol Evol 15 518 527 1:CAS:528:DyaK1cXislens7o%3D 9580980
76. T Uchida T Tanabe M Fukae M Shimizu M Yamada K Miake S Kobayashi 1991 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 96 129 138 10.1007/BF00315983 1:CAS:528:DyaK3MXkvV2ls7g%3D 1917569
77. T Uchida T Tanabe M Fukae M Shimizu 1991 Immunocytochemical and immunochemical detection of a 32 kDa nonamelogenin and related proteins in porcine tooth germs Arch Histol Cytol 54 527 538 10.1679/aohc.54.527 1:STN:280:DyaK387nt1Gguw%3D%3D 1793666
78. T van Rheede T Bastiaans DN Boone SB Hedges WW de Jong O Madsen 2006 The platypus is in its place: nuclear genes and indels confirm the sister group relation of monotremes and therians Mol Biol Evol 23 587 597 10.1093/molbev/msj064 16291999 (Pubitemid 43278270)
79. G von Heijne 1985 Signal sequences: the limits of variation J Mol Biol 184 99 105 10.1016/0022-2836(85)90046-4 (Pubitemid 15068265)
80. WC Warren LW Hillier JA Marshall Graves E Birney CP Ponting F Grutzner K Belov W Miller L Clarke AT Chinwalla SP Yang A Heger DP Locke P Miethke PD Waters F Veyrunes L Fulton B Fulton T Graves J Wallis XS Puente C Lopez-Otin GR Ordonez EE Eichler L Chen Z Cheng JE Deakin A Alsop K Thompson P Kirby AT Papenfuss MJ Wakefield T Olender D Lancet GA Huttley AF Smit A Pask P Temple-Smith MA Batzer JA Walker MK Konkel RS Harris CM Whittington ES Wong NJ Gemmell E Buschiazzo IM Vargas Jentzsch A Merkel J Schmitz A Zemann G Churakov JO Kriegs J Brosius EP Murchison R Sachidanandam C Smith GJ Hannon E Tsend-Ayush D McMillan R Attenborough W Rens M Ferguson-Smith CM Lefevre JA Sharp KR Nicholas DA Ray M Kube R Reinhardt TH Pringle J Taylor RC Jones B Nixon JL Dacheux H Niwa Y Sekita X Huang A Stark P Kheradpour M Kellis P Flicek Y Chen C Webber R Hardison J Nelson K Hallsworth-Pepin K Delehaunty C Markovic P Minx Y Feng C Kremitzki M Mitreva J Glasscock T Wylie P Wohldmann P Thiru MN Nhan CS Pohl SM Smith S Hou MB Renfree 2008 Genome analysis of the platypus reveals unique signatures of evolution Nature 453 175 183 10.1038/nature06936 1:CAS:528:DC%2BD1cXls12msLs%3D 18464734 (Pubitemid 351667983)
81. S Weiner 1986 Organization of extracellularly mineralized tissues: a comparative study of biological crystal growth CRC Crit Rev Biochem 20 365 408 10.3109/10409238609081998 1:CAS:528:DyaL28XlsVyhtrs%3D 3524990
82. Y Yamakoshi 1995 Carbohydrate moieties of porcine 32 kDa enamelin Calcif Tissue Int 56 323 330 10.1007/BF00318054 1:CAS:528:DyaK2MXks1ent7g%3D 7767845
83. Y Yamakoshi FH Pinheiro T Tanabe M Fukae M Shimizu 1998 Sites of asparagine-linked oligosaccharides in porcine 32 kDa enamelin Connect Tissue Res 39 39 46 10.3109/03008209809023910 1:STN:280:DC%2BD3crgvFKguw%3D%3D 11062987
84. Y Yamakoshi JC Hu S Liu C Zhang S Oida M Fukae JP Simmer 2003 Characterization of porcine dentin sialoprotein (DSP) and dentin sialophosphoprotein (DSPP) cDNA clones Eur J Oral Sci 111 60 67 10.1034/j.1600-0722.2003.00009.x 1:CAS:528:DC%2BD3sXhvV2iur8%3D 12558809 (Pubitemid 37465299)
85. Y Yamakoshi JC Hu M Fukae F Yamakoshi JP Simmer 2006 How do enamelysin and kallikrein 4 process the 32-kDa enamelin? Eur J Oral Sci 114 Suppl 1 45 51 10.1111/j.1600-0722.2006.00281.x 1:CAS:528:DC%2BD28XlvF2hu7o%3D 16674662
86. H Yoon G Laxmikanthan J Lee SI Blaber A Rodriguez JM Kogot IA Scarisbrick M Blaber 2007 Activation profiles anad regulatory cascades of the human kallikrein-related peptidases J Biol Chem 282 31852 31864 10.1074/jbc.M705190200 1:CAS:528:DC%2BD2sXht1WlsrbF 17823117 (Pubitemid 350106429)