Journal of Molecular Evolution

, Volume 84, Issue 4, pp 214–224 | Cite as

Evolutionary Analysis of the Mammalian Tuftelin Sequence Reveals Features of Functional Importance

Original Article

Abstract

Tuftelin (TUFT1) is an acidic, phosphorylated glycoprotein, initially discovered in developing enamel matrix. TUFT1 is expressed in many mineralized and non-mineralized tissues. We performed an evolutionary analysis of 82 mammalian TUFT1 sequences to identify residues and motifs that were conserved during 220 million years (Ma) of evolution. We showed that 168 residues (out of the 390 residues composing the human TUFT1 sequence) are under purifying selection. Our analyses identified several, new, putatively functional domains and confirmed previously described functional domains, such as the TIP39 interaction domain, which correlates with nuclear localization of the TUFT1 protein, that was demonstrated in several tissues. We also identified several sites under positive selection, which could indicate evolutionary changes possibly related to the functional diversification of TUFT1 during evolution in some lineages. We discovered that TUFT1 and MYZAP (myocardial zonula adherens protein) share a common ancestor that was duplicated circa 500 million years ago. Taken together, these findings expand our knowledge of TUFT1 evolution and provide new information that will be useful for further investigation of TUFT1 functions.

Keywords

Tuftelin TUFT1 MYZAP Evolution Mineralization Mammals 

Supplementary material

239_2017_9789_MOESM1_ESM.pdf (135 kb)
Supplementary material 1 (PDF 135 KB)
239_2017_9789_MOESM2_ESM.pdf (87 kb)
Supplementary material 2 (PDF 86 KB)
239_2017_9789_MOESM3_ESM.pdf (136 kb)
Supplementary material 3 (PDF 135 KB)
239_2017_9789_MOESM4_ESM.jpg (4.6 mb)
Supplementary material 4 (JPG 4705 KB)
239_2017_9789_MOESM5_ESM.pdf (207 kb)
Supplementary material 5 (PDF 207 KB)
239_2017_9789_MOESM6_ESM.pdf (56 kb)
Supplementary material 6 (PDF 55 KB)
239_2017_9789_MOESM7_ESM.pdf (52 kb)
Supplementary material 7 (PDF 51 KB)
239_2017_9789_MOESM8_ESM.pdf (665 kb)
Supplementary material 8 (PDF 665 KB)
239_2017_9789_MOESM9_ESM.pdf (6 kb)
Supplementary material 9 (PDF 6 KB)

References

  1. Al-Hashimi N, Sire JY, Delgado S (2009) 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 69(6):635–656CrossRefPubMedGoogle Scholar
  2. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38(Web Server issue):W529–W533Google Scholar
  3. Bashir MM, Abrams WR, Tucker T, Sellinger B, Budarf M, Emanuel B, Rosenbloom J (1998) Molecular cloning and characterization of the bovine and human tuftelin genes. Connect Tissue Res 39:13–24CrossRefPubMedGoogle Scholar
  4. Celniker G, Nimrod G, Ashkenazy H, Glaser F, Martz E, Mayrose I, Pupko T, Ben-Tal N (2013) ConSurf: using evolutionary data to raise testable hypotheses about protein function. Isr J Chem 53:199–206CrossRefGoogle Scholar
  5. Chan HC, Mai L, Oikonomopoulou A, Chan HL, Richardson AS, Wang SK, Simmer JP, Hu JC (2010) Altered enamelin phosphorylation site causes amelogenesis imperfecta. J Dent Res 89:695–699CrossRefPubMedPubMedCentralGoogle Scholar
  6. Deutsch D (1989) Structure and function of enamel gene products. Anat Rec 224:189–210CrossRefPubMedGoogle Scholar
  7. Deutsch D, Palmon A, Fisher LW, Kolodny N, Termine JD, Young MF (1991) Sequencing of bovine enamelin (“tuftelin”) a novel acidic enamel protein. J Biol Chem 266:16021–16028PubMedGoogle Scholar
  8. Deutsch D, Palmon A, Dafni L, Mao Z, Leytin V, Young M, Fisher LW (1998) Tuftelin – aspects of protein and gene structure. Eur J Oral Sci 106(Suppl. 1):315–323CrossRefPubMedGoogle Scholar
  9. Deutsch D, Shay B, Rosenfeld E, Leiser Y, Fermon E, Taylor A, Charuvi K, Cohen Y, Haze A, Fuks A, Dafni L, Mao Z (2002) The human tuftelin gene and the expression of tuftelin in mineralizing and nonmineralizing tissues. Connect Tissue Res 43:425–434CrossRefPubMedGoogle Scholar
  10. Deutsch D, Silverstein N, Shilo D, Lecht S, Lazarovici P, Blumenfeld A (2011) Biphasic influence of hypoxia on tuftelin expression in mouse mesenchymal C3H10T1/2 stem cells. Eur J Oral Sci 119(suppl. 1):55–61CrossRefPubMedGoogle Scholar
  11. Dinkel H, Van Roey K, Michael S, Kumar M, Uyar B, Altenberg B, Milchevskaya V, Schneider M, Kühn H, Behrendt A, Dahl SL, Damerell V, Diebel S, Kalman S, Klein S, Knudsen AC, Mäder C, Merrill S, Staudt A, Thiel V, Welti L, Davey NE, Diella F, Gibson TJ (2016) ELM 2016-data update and new functionality of the eukaryotic linear motif resource. Nucleic Acids Res 44(D1):D294–D300CrossRefPubMedGoogle Scholar
  12. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  13. Endo T, Ikeo K, Gojobori T (1996) Large-scale search for genes on which positive selection may operate. Mol Biol Evol 13:685–690CrossRefPubMedGoogle Scholar
  14. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22(2):160–174Google Scholar
  15. Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266:383–402Google Scholar
  16. Jeremias FL, Koruyucu M, Küchler EC, Bayram M, Tuna EB, Deeley K, Pierri RA, Souza JF, Fragelli CM, Paschoal MA, Gencay K, Seymen F, Caminaga RM, dos Santos-Pinto L, Vieira AR (2013) Genes expressed in dental enamel development are associated with molar-incisor hypomineralization. Arch Oral Biol 58:1434–1442CrossRefPubMedPubMedCentralGoogle Scholar
  17. Leiser Y, Blumenfeld A, Haze A, Dafni L, Taylor AL, Rosenfeld E, Fermon E, Gruenbaum-Cohen Y, Shay B, Deutsch D (2007) Localization, quantification, and characterization of tuftelin in soft tissues. Anat Rec 290:449–454CrossRefGoogle Scholar
  18. Leiser Y, Silverstein NC, Blumenfeld A, Shilo D, Haze A, Rosenfeld E, Shay B, Tabakman R, Lecht S, Lazarovici P, Deutsch D (2010) The induction of tuftelin expression in PC12 cell line during hypoxia and NGF induced differentiation. J Cell Physiol 226:165–172CrossRefGoogle Scholar
  19. MacDougall M, Simmons D, Dodds A, Knight C, Luan X, Zeichner-David M, Zhang C, Ryu OH, Qian Q, Simmer JP, Hu C-C (1998) Cloning, characterization, and tissue expression pattern of mouse tuftelin cDNA. J Dent Res 77:1970–1978CrossRefPubMedGoogle Scholar
  20. Mao Z, Shay B, Hekmati M, Fermon E, Taylor A, Dafni L, Heikenheimo K, Lustmann J, Fisher LW, Young MF, Deutsch D (2001) The human tuftelin gene: cloning and characterization. Gene 279:181–196CrossRefPubMedGoogle Scholar
  21. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ (2011) Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334(6055):521–524CrossRefPubMedGoogle Scholar
  22. Paine CT, Paine ML, Luo W, Okamoto CT, Lyngstadaas SP, Snead ML (2000) A tuftelin-interacting protein (TIP39) localizes tothe apical secretory pole of mouse ameloblasts. J Biol Chem 275:22284–22292CrossRefPubMedGoogle Scholar
  23. Patir A, Seymen F, Yildirim M, Deeley K, Cooper ME, Marazita ML, Vieira AR (2008) Enamel formation genes are associated with high caries experience in Turkish children. Caries Res 42:394–400CrossRefPubMedPubMedCentralGoogle Scholar
  24. Pieperhoff S, Rickelt S, Heid H, Claycomb WC, Zimbelmann R, Kuhn C, Winter-Simanowski S, Kuhn C, Frey N, Franke WW (2012) The plaque protein myozap identified as a novel major component of adhering junctions in endothelia of the blood and the lymph vascular systems. J Cell Mol Med 16:1709–1719CrossRefPubMedPubMedCentralGoogle Scholar
  25. Pond SLK, Frost SDW (2005) A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol Biol Evol 22:478–485CrossRefPubMedGoogle Scholar
  26. Pond SLK, Muse SV (2005) HyPhy: Hypothesis testing using Phylogenies. In Statistical Methods for Molecular Evolution. Statistics for Biology and Health, Part II. Springer, New York, p 125–181CrossRefGoogle Scholar
  27. Pond SLK, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679CrossRefPubMedGoogle Scholar
  28. Rickelt S, Kuhn C, Winter-Simanowski S, Zimbelmann R, Frey N, Franke WW (2011) Protein myozapa late addition to the molecular ensembles of various kinds of adherens junctions. Cell Tissue Res 346:347–359CrossRefPubMedGoogle Scholar
  29. Schmid K, Yang Z (2008) The trouble with sliding windows and the selective pressure in BRCA1. PLoS ONE 3:e3746CrossRefPubMedPubMedCentralGoogle Scholar
  30. Shay B, Gruenbaum-Cohen Y, Tucker AS, Taylor AL, Rosenfeld E, Haze A, Dafni L, Leiser Y, Fermon E, Danieli T, Blumenfeld A, Deutsch D (2009) High yield expression of biologically active recombinant full length human tuftelin protein in baculovirus-infected insect cells. Protein Expr Purif 68:90–98CrossRefPubMedGoogle Scholar
  31. Sigrist CJA, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38(Database issue):D161–D166CrossRefPubMedGoogle Scholar
  32. Silvent J, Sire JY, Delgado S (2013) The Dentin matrix acidic phosphoprotein 1 (DMP1) in the light of mammalian evolution. J Mol Evol 76(1–2):59–70CrossRefPubMedGoogle Scholar
  33. Stanek D, Pridalova-Hnilicova J, Novotny I, Huranova M, Blazikova M, Wen X, Sapra AK, Neugebauer KM (2008) Spliceosomal small nuclear ribonucleoprotein particles repeatedly cycle through Cajal bodies. Mol Biol Cell 19:2534–2543CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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(Web Server issue):W506–W511Google Scholar
  35. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  36. Tsunoyama K, Gojobori T (1998) Evolution of nicotinic acetylcholine receptor subunits. Mol Biol Evol 15:518–527CrossRefPubMedGoogle Scholar
  37. Wen X, Lei Y-P, Zhou YL, Okamoto CT, Snead ML, Paine ML (2005) Structural organization and cellular localization of tuftelin-interacting protein 11 (TFIP11). Cell Mol Life Sci 62:1038–1046CrossRefPubMedGoogle Scholar
  38. Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449Google Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Evolution et Développement du Squelette, UMR7138- Evolution Paris-Seine, Institut de Biologie (IBPS)Université Pierre et Marie CurieParisFrance
  2. 2.Dental Research Laboratory, Faculty of Dental Medicine, Institute of Dental SciencesThe Hebrew University of Jerusalem-HadassahJerusalemIsrael

Personalised recommendations