Journal Mobile Options
Table of Contents
Vol. 186, No. 1, 2007
Issue release date: July 2007
Cells Tissues Organs 2007;186:7–24
(DOI:10.1159/000102678)

Gene Duplication and the Evolution of Vertebrate Skeletal Mineralization

Kawasaki K. · Buchanan A.V. · Weiss K.M.
To view the fulltext, log in and/or choose pay-per-view option

Individual Users: Register with Karger Login Information

Please create your User ID & Password





Contact Information











I have read the Karger Terms and Conditions and agree.

To view the fulltext, please log in

To view the pdf, please log in

Abstract

The mineralized skeleton is a critical innovation that evolved early in vertebrate history. The tissues found in dermal skeletons of ancient vertebrates are similar to the dental tissues of modern vertebrates; both consist of a highly mineralized surface hard tissue, enamel or enameloid, more resilient body dentin, and basal bone. Many proteins regulating mineralization of these tissues are evolutionarily related and form the secretory calcium-binding phosphoprotein (SCPP) family. We hypothesize here the duplication histories of SCPP genes and their common ancestors, SPARC and SPARCL1. At around the same time that Paleozoic jawless vertebrates first evolved mineralized skeleton, SPARCL1 arose from SPARC by whole genome duplication. Then both before and after the split of ray-finned fish and lobe-finned fish, tandem gene duplication created two types of SCPP genes, each residing on the opposite side of SPARCL1. One type was subsequently used in surface tissue and the other in body tissue. In tetrapods, these two types of SCPP genes were separated by intrachromosomal rearrangement. While new SCPP genes arose by duplication, some old genes were eliminated from the genome. As a consequence, phenogenetic drift occurred: while mineralized skeleton is maintained by natural selection, the underlying genetic basis has changed.



Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Aburomia, R., O. Khaner, A. Sidow (2003) Functional evolution in the ancestral lineage of vertebrates or when genomic complexity was wagging its morphological tail. J Struct Funct Genomics 3: 45–52.
  2. Bartlett, J.D., B. Ganss, M. Goldberg, J. Moradian-Oldak, M.L. Paine, M.L. Snead, X. Wen, S.N. White, Y.L. Zhou (2006) Protein-protein interactions of the developing enamel matrix. Curr Top Dev Biol 74: 57–115.
  3. Bhattacharyya, J., K.P. Das (1999) Molecular chaperone-like properties of an unfolded protein, αS-casein. J Biol Chem 274: 15505–15509.
  4. Bouropoulos, N., J. Moradian-Oldak (2004) Induction of apatite by the cooperative effect of amelogenin and the 32-kDa enamelin. J Dent Res 83: 278–282.
  5. Bradshaw, A.D., D.C. Graves, K. Motamed, E.H. Sage (2003) SPARC-null mice exhibit increased adiposity without significant differences in overall body weight. Proc Natl Acad Sci USA 100: 6045–6050.
  6. Brekken, R.A., E.H. Sage (2000) SPARC, a matricellular protein: at the crossroads of cell-matrix. Matrix Biol 19: 569–580.
  7. Carlson, S.J. (1990) Vertebrate dental structures; in Carter, J.G. (ed): Skeletal Biomineralization: Pattern, Process and Evolutionary Trends. New York, Van Nostrand Reinhold, vol I, pp 531–556.
  8. Chun, Y.H., Y. Yamakoshi, J.W. Kim, T. Iwata, J.C. Hu, J.P. Simmer (2006) Porcine SPARC: isolation from dentin, cDNA sequence, and computer model. Eur J Oral Sci 114(suppl 1): 78–85; discussion 93–75, 379–380.
  9. Creamer, L.K., T. Richardson, D.A. Parry (1981) Secondary structure of bovine alpha s1- and beta-casein in solution. Arch Biochem Biophys 211: 689–696.
  10. Dehal, P., J.L. Boore (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3: e314.
  11. Delgado, S., D. Casane, L. Bonnaud, M. Laurin, J.Y. Sire, M. Girondot (2001) Molecular evidence for Precambrian origin of amelogenin, the major protein of vertebrate enamel. Mol Biol Evol 18: 2146–2153.
  12. Delsuc, F., H. Brinkmann, D. Chourrout, H. Philippe (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439: 965–968.
  13. Donoghue, P.C., I.J. Sansom (2002) Origin and early evolution of vertebrate skeletonization. Microsc Res Tech 59: 352–372.
  14. Donoghue, P.C., M.A. Purnell (2005) Genome duplication, extinction and vertebrate evolution. Trends Ecol Evol 20: 312–319.
  15. Donoghue, P.C., I.J. Sansom, J.P. Downs (2006) Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development. J Exp Zoolog B Mol Dev Evol 306: 278–294.

    External Resources

  16. Duboule, D., A.S. Wilkins (1998) The evolution of ‘bricolage’. Trends Genet 14: 54–59.
  17. Dunker, A.K., J.D. Lawson, C.J. Brown, R.M. Williams, P. Romero, J.S. Oh, C.J. Oldfield, A.M. Campen, C.M. Ratliff, K.W. Hipps, J. Ausio, M.S. Nissen, R. Reeves, C. Kang, C.R. Kissinger, R.W. Bailey, M.D. Griswold, W. Chiu, E.C. Garner, Z. Obradovic (2001) Intrinsically disordered protein. J Mol Graph Model 19: 26–59.
  18. Dunker, A.K., C.J. Brown, J.D. Lawson, L.M. Iakoucheva, Z. Obradovic (2002) Intrinsic disorder and protein function. Biochemistry 41: 6573–6582.
  19. Dyson, H.J., P.E. Wright (2002) Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12: 54–60.
  20. Engel, J., W. Taylor, M. Paulsson, H. Sage, B. Hogan (1987) Calcium binding domains and calcium-induced conformational transition of SPARC/BM-40/osteonectin, an extracellular glycoprotein expressed in mineralized and nonmineralized tissues. Biochemistry 26: 6958–6965.
  21. Escriva, H., L. Manzon, J. Youson, V. Laudet (2002) Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution. Mol Biol Evol 19: 1440–1450.
  22. Fincham, A.G., J. Moradian-Oldak, J.P. Simmer (1999) The structural biology of the developing dental enamel matrix. J Struct Biol 126: 270–299.
  23. Fisher, L.W., D.A. Torchia, B. Fohr, M.F. Young, N.S. Fedarko (2001) Flexible structures of SIBLING proteins, bone sialoprotein, and osteopontin. Biochem Biophys Res Commun 280: 460–465.
  24. Fitzgerald, M.C., J.E. Schwarzbauer (1998) Importance of the basement membrane protein SPARC for viability and fertility in Caenorhabditis elegans. Curr Biol 8: 1285–1288.
  25. Fong, C.D., I. Slaby, L. Hammarstrom (1996) Amelin: an enamel-related protein, transcribed in the cells of epithelial root sheath. J Bone Miner Res 11: 892–898.
  26. Force, A., W.A. Cresko, F.B. Pickett, S.R. Proulx, C. Amemiya, M. Lynch (2005) The origin of subfunctions and modular gene regulation. Genetics 170: 433–446.
  27. Force, A., M. Lynch, F.B. Pickett, A. Amores, Y.L. Yan, J. Postlethwait (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531–1545.
  28. Fukumoto, S., T. Kiba, B. Hall, N. Iehara, T. Nakamura, G. Longenecker, P.H. Krebsbach, A. Nanci, A.B. Kulkarni, Y. Yamada (2004) Ameloblastin is a cell adhesion molecule required for maintaining the differentiation state of ameloblasts. J Cell Biol 167: 973–983.
  29. Furlong, R.F., P.W. Holland (2002) Were vertebrates octoploid? Philos Trans R Soc Lond B Biol Sci 357: 531–544.
  30. Ganss, B., R.H. Kim, J. Sodek (1999) Bone sialoprotein. Crit Rev Oral Biol Med 10: 79–98.
  31. Giachelli, C.M., S. Steitz (2000) Osteopontin: a versatile regulator of inflammation and biomineralization. Matrix Biol 19: 615–622.
  32. Girard, J.P., T.A. Springer (1995) Cloning from purified high endothelial venule cells of hevin, a close relative of the antiadhesive extracellular matrix protein SPARC. Immunity 2: 113–123.
  33. Gu, X., J. Zhang (1997) A simple method for estimating the parameter of substitution rate variation among sites. Mol Biol Evol 14: 1106–1113.
  34. Gu, X., Y. Wang, J. Gu (2002) Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat Genet 31: 205–209.
  35. Hall, B.K. (2005) Bones and Cartilage: Developmental and Evolutionary Skeletal Biology. San Diego, Elsevier.
  36. Halstead, L.B. (1974) Vertebrate Hard Tissues. London, Wykeham.
  37. Hambrock, H.O., D.P. Nitsche, U. Hansen, P. Bruckner, M. Paulsson, P. Maurer, U. Hartmann (2003) SC1/hevin. An extracellular calcium-modulated protein that binds collagen I. J Biol Chem 278: 11351–11358.
  38. Hauschka, P.V., S.A. Carr (1982) Calcium-dependent alpha-helical structure in osteocalcin. Biochemistry 21: 2538–2547.
  39. Hohenester, E., P. Maurer, C. Hohenadl, R. Timpl, J.N. Jansonius, J. Engel (1996) Structure of a novel extracellular Ca2+-binding module in BM-40. Nat Struct Biol 3: 67–73.
  40. Holland, P.W., S.J. Harper, J.H. McVey, B.L. Hogan (1987) In vivo expression of mRNA for the Ca++-binding protein SPARC (osteonectin) revealed by in situ hybridization. J Cell Biol 105: 473–482.
  41. Holland, P.W., J. Garcia-Fernandez, N.A. Williams, A. Sidow (1994) Gene duplications and the origins of vertebrate development. Dev Suppl, pp 125–133.
  42. Hu, J.C., Y. Yamakoshi (2003) Enamelin and autosomal-dominant amelogenesis imperfecta. Crit Rev Oral Biol Med 14: 387–398.
  43. Hu, J.C., Y. Yamakoshi, F. Yamakoshi, P.H. Krebsbach, J.P. Simmer (2005) Proteomics and genetics of dental enamel. Cells Tissues Organs 181: 219–231.
  44. Huq, N.L., K.J. Cross, M. Ung, E.C. Reynolds (2005) 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 50: 599–609.
  45. Iakoucheva, L.M., P. Radivojac, C.J. Brown, T.R. O’Connor, J.G. Sikes, Z. Obradovic, A.K. Dunker (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32: 1037–1049.
  46. International Chicken Genome Sequencing Consortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695–716.
  47. Isbell, D.T., S. Du, A.G. Schroering, G. Colombo, J.G. Shelling (1993) Metal ion binding to dog osteocalcin studied by 1H NMR spectroscopy. Biochemistry 32: 11352–11362.
  48. Iwasaki, K., E. Bajenova, E. Somogyi-Ganss, M. Miller, V. Nguyen, H. Nourkeyhani, Y. Gao, M. Wendel, B. Ganss (2005) Amelotin – a novel secreted, ameloblast-specific protein. J Dent Res 84: 1127–1132.
  49. Iwase, M., Y. Satta, N. Takahata (2001) Sex-chromosomal differentiation and amelogenin genes in mammals. Mol Biol Evol 18: 1601–1603.
  50. Iwase, M., Y. Satta, Y. Hirai, H. Hirai, H. Imai, N. Takahata (2003) The amelogenin loci span an ancient pseudoautosomal boundary in diverse mammalian species. Proc Natl Acad Sci USA 100: 5258–5263.
  51. Jacob, F. (1977) Evolution and tinkering. Science 196: 1161–1166.
  52. Janvier, P. (2003) Vertebrate characteristics and the Cambrian vertebrates. CR Palevol 2: 523–531.

    External Resources

  53. Johanson, Z., M.M. Smith (2005) Origin and evolution of gnathostome dentitions: a question of teeth and pharyngeal denticles in placoderms. Biol Rev Camb Philos Soc 80: 303–345.
  54. Kawasaki, K., K.M. Weiss (2003) Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proc Natl Acad Sci USA 100: 4060–4065.
  55. Kawasaki, K., T. Suzuki, K.M. Weiss (2004) Genetic basis for the evolution of vertebrate mineralized tissue. Proc Natl Acad Sci USA 101: 11356–11361.
  56. Kawasaki, K., T. Suzuki, K.M. Weiss (2005) Phenogenetic drift in evolution: the changing genetic basis of vertebrate teeth. Proc Natl Acad Sci USA 102: 18063–18068.
  57. Kawasaki, K., K.M. Weiss (2006) Evolutionary genetics of vertebrate tissue mineralization: the origin and evolution of the secretory calcium-binding phosphoprotein family. J Exp Zoolog B Mol Dev Evol 306: 295–316.

    External Resources

  58. Kawasaki, K., K.M. Weiss (2007) Genetic basis for the evolution of vertebrate mineralized tissue; in Bäuerlein, E. (ed): Handbook of Biomineralization. Weinheim, Wiley-VCH, vol I, pp 331–347.
  59. Kim, J.W., J.C. Hu, J.I. Lee, S.K. Moon, Y.J. Kim, K.T. Jang, S.H. Lee, C.C. Kim, S.H. Hahn, J.P. Simmer (2005) Mutational hot spot in the DSPP gene causing dentinogenesis imperfecta type II. Hum Genet 116: 186–191.
  60. Kumar, S., M. Nei (2000) Molecular Evolution and Phylogenetics. New York, Oxford University Press.
  61. Kumar, S., K. Tamura, M. Nei (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150–163.
  62. Le, T.Q., M. Gochin, J.D. Featherstone, W. Li, P.K. DenBesten (2006) Comparative calcium binding of leucine-rich amelogenin peptide and full-length amelogenin. Eur J Oral Sci 114(suppl 1): 320–326.
  63. Linding, R., L.J. Jensen, F. Diella, P. Bork, T.J. Gibson, R.B. Russell (2003) Protein disorder prediction: implications for structural proteomics. Structure 11: 1453–1459.
  64. Lundin, L.G., D. Larhammar, F. Hallböök (2003) Numerous groups of chromosomal regional paralogies strongly indicate two genome doublings at the root of the vertebrates. J Struct Funct Genomics 3: 53–63.
  65. Margolis, H.C., E. Beniash, C.E. Fowler (2006) Role of macromolecular assembly of enamel matrix proteins in enamel formation. J Dent Res 85: 775–793.
  66. Martinek, N., R. Zou, M. Berg, J. Sodek, M. Ringuette (2002) Evolutionary conservation and association of SPARC with the basal lamina in Drosophila. Dev Genes Evol 212: 124–133.
  67. Matsushima, N., Y. Izumi, T. Aoba (1998) Small-angle X-ray scattering and computer-aided molecular modeling studies of 20 kDa fragment of porcine amelogenin: does amelogenin adopt an elongated bundle structure? J Biochem (Tokyo) 123: 150–156.
  68. Maurer, P., E. Hohenester, J. Engel (1996) Extracellular calcium-binding proteins. Curr Opin Cell Biol 8: 609–617.
  69. McLysaght, A., K. Hokamp, K.H. Wolfe (2002) Extensive genomic duplication during early chordate evolution. Nat Genet 31: 200–204.
  70. Meinke, D.K., K.S. Thomson (1983) The distribution and significance of enamel and enameloid in the dermal skeleton of osteolepiform rhipidistian fishes. Paleobiology 9: 138–149.
  71. Metsäranta, M., M.F. Young, M. Sandberg, J. Termine, E. Vuorio (1989) Localization of osteonectin expression in human fetal skeletal tissues by in situ hybridization. Calcif Tissue Int 45: 146–152.
  72. Meyer, A., Y. Van de Peer (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27: 937–945.
  73. Moffatt, P., C.E. Smith, R. Sooknanan, R. St-Arnaud, A. Nanci (2006a) Identification of secreted and membrane proteins in the rat incisor enamel organ using a signal-trap screening approach. Eur J Oral Sci 114(suppl 1): 139–146.
  74. Moffatt, P., C.E. Smith, R. St-Arnaud, D. Simmons, J.T. Wright, A. Nanci (2006b) Cloning of rat amelotin and localization of the protein to the basal lamina of maturation stage ameloblasts and junctional epithelium. Biochem J 399: 37–46.
  75. Moradian-Oldak, J., M. Goldberg (2005) Amelogenin supra-molecular assembly in vitro compared with the architecture of the forming enamel matrix. Cells Tissues Organs 181: 202–218.
  76. Mothe, A.J., I.R. Brown (2001) Differential mRNA expression of the related extracellular matrix glycoproteins SC1 and SPARC in the rat embryonic nervous system and skeletal structure. Brain Res 892: 27–41.
  77. Nadeau, J.H., D. Sankoff (1997) Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. Genetics 147: 1259–1266.
  78. Nagano, T., S. Oida, H. Ando, K. Gomi, T. Arai, M. Fukae (2003) Relative levels of mRNA encoding enamel proteins in enamel organ epithelia and odontoblasts. J Dent Res 82: 982–986.
  79. Nakamura, S., T. Terashima, T. Yoshida, S. Iseki, Y. Takano, I. Ishikawa, T. Shinomura (2005) Identification of genes preferentially expressed in periodontal ligament: specific expression of a novel secreted protein, FDC-SP. Biochem Biophys Res Commun 338: 1197–1203.
  80. Nanci, A. (2003) Ten Cate’s Oral Histology, ed 6. St. Louis, Mosby.
  81. Nei, M. (2005) Selectionism and neutralism in molecular evolution. Mol Biol Evol 22: 2318–2342.
  82. Nei, M., A.P. Rooney (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39: 121–152.
  83. Ogbureke, K.U., L.W. Fisher (2004) Expression of SIBLINGs and their partner MMPs in salivary glands. J Dent Res 83: 664–670.
  84. Ogbureke, K.U., L.W. Fisher (2005) Renal expression of SIBLING proteins and their partner matrix metalloproteinases (MMPs). Kidney Int 68: 155–166.
  85. Ohno, S. (1970) Evolution by Gene Duplication. New York, Springer.
  86. Ohta, Y., W. Goetz, M.Z. Hossain, M. Nonaka, M.F. Flajnik (2006) Ancestral organization of the MHC revealed in the amphibian Xenopus. J Immunol 176: 3674–3685.
  87. Oritani, K., Y. Kanakura, K. Aoyama, T. Yokota, N.G. Copeland, D.J. Gilbert, N.A. Jenkins, Y. Tomiyama, Y. Matsuzawa, P.W. Kincade (1997) Matrix glycoprotein SC1/ECM2 augments B lymphopoiesis. Blood 90: 3404–3413.
  88. Paine, M.L., M.L. Snead (2005) Tooth developmental biology: disruptions to enamel-matrix assembly and its impact on biomineralization. Orthod Craniofac Res 8: 239–251.
  89. Papagerakis, P., M. MacDougall, D. Hotton, I. Bailleul-Forestier, M. Oboeuf, A. Berdal (2003) Expression of amelogenin in odontoblasts. Bone 32: 228–240.
  90. Peyer, B. (1968) Comparative Odontology. Chicago, University of Chicago Press.
  91. Philippe, H., N. Lartillot, H. Brinkmann (2005) Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Mol Biol Evol 22: 1246–1253.
  92. Poole, D.F.G. (1967) Phylogeny of tooth tissues: enameloid and enamel in recent vertebrates with a note in the history of cementum; in Miles AEW (ed): Structural and Chemical Organization of Teeth. New York, Academic Press, vol I, pp 111–149.
  93. Porter, P.L., E.H. Sage, T.F. Lane, S.E. Funk, A.M. Gown (1995) Distribution of SPARC in normal and neoplastic human tissue. J Histochem Cytochem 43: 791–800.
  94. Qin, C., O. Baba, W.T. Butler (2004) Post-translational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit Rev Oral Biol Med 15: 126–136.
  95. Radivojac, P., Z. Obradovic, D.K. Smith, G. Zhu, S. Vucetic, C.J. Brown, J.D. Lawson, A.K. Dunker (2004) Protein flexibility and intrinsic disorder. Protein Sci 13: 71–80.
  96. Rajpar, M.H., M.J. Koch, R.M. Davies, K.T. Mellody, C.M. Kielty, M.J. Dixon (2002) Mutation of the signal peptide region of the bicistronic gene DSPP affects translocation to the endoplasmic reticulum and results in defective dentine biomineralization. Hum Mol Genet 11: 2559–2565.
  97. Rath, A., A.R. Davidson, C.M. Deber (2005) The structure of ‘unstructured’ regions in peptides and proteins: role of the polyproline II helix in protein folding and recognition. Biopolymers 80: 179–185.
  98. Reif, W.E., M. Richter (2001) Revisiting the lepidomorial and the odontode regulation theories of dermo-skeletal morphogenesis. N Jb Geol Paläont Abh 219: 285–304.
  99. Rijnkels, M., L. Elnitski, W. Miller, J.M. Rosen (2003) Multispecies comparative analysis of a mammalian-specific genomic domain encoding secretory proteins. Genomics 82: 417–432.
  100. Robinson, C. (2006) Discussion of session 8: amelogenin assembly and function. Eur J Oral Sci 114(suppl 1): 327–329.

    External Resources

  101. Romero, P., Z. Obradovic, X. Li, E.C. Garner, C.J. Brown, A.K. Dunker (2001) Sequence complexity of disordered protein. Proteins 42: 38–48.
  102. Sabatini, L.M., T. Ota, E.A. Azen (1993) Nucleotide sequence analysis of the human salivary protein genes HIS1 and HIS2, and evolution of the STATH/HIS gene family. Mol Biol Evol 10: 497–511.
  103. Sanetra, M., G. Begemann, M.B. Becker, A. Meyer (2005) Conservation and co-option in developmental programmes: the importance of homology relationships. Front Zool 2: 15.

    External Resources

  104. Sasagawa, I. (1995) Fine structure of tooth germs during the formation of enameloid matrix in Tilapia nilotica, a teleost fish. Arch Oral Biol 40: 801–814.
  105. Sasagawa, I. (1998) Mechanisms of mineralization in the enameloid of elasmobranchs and teleosts. Connect Tissue Res 39: 207–214; discussion 221–225.
  106. Sasagawa, I. (2002) Mineralization patterns in elasmobranch fish. Microsc Res Tech 59: 396–407.
  107. Schaeffer, B. (1977) The dermal skeleton in fishes; in Andrews, S.M., R.S. Miles, A.D. Walker (eds): Problems in Vertebrate Evolution. London, Academic Press, pp 25–52.
  108. Schmidt, H.A., K. Strimmer, M. Vingron, A. von Haeseler (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.
  109. Shellis, R.P., A.E.W. Miles (1974) Autoradiographic study of the formation of enameloid and dentine matrices in teleost fishes using tritiated amino acids. Proc R Soc Lond B 185: 51–72.

    External Resources

  110. Shintani, S., M. Kobata, S. Toyosawa, T. Fujiwara, A. Sato, T. Ooshima (2002) Identification and characterization of ameloblastin gene in a reptile. Gene 283: 245–254.
  111. Shintani, S., M. Kobata, S. Toyosawa, T. Ooshima (2003) Identification and characterization of ameloblastin gene in an amphibian, Xenopus laevis. Gene 318: 125–136.
  112. Shintani, S., M. Kobata, S. Toyosawa, T. Ooshima (2006) Expression of ameloblastin during enamel formation in a crocodile. J Exp Zoolog B Mol Dev Evol 306: 126–133.

    External Resources

  113. Sidow, A. (1996) Gen(om)e duplications in the evolution of early vertebrates. Curr Opin Genet Dev 6: 715–722.
  114. Simmer, J.P., J.C. Hu (2002) Expression, structure, and function of enamel proteinases. Connect Tissue Res 43: 441–449.
  115. Sire, J.Y., S. Delgado, D. Fromentin, M. Girondot (2005) Amelogenin: lessons from evolution. Arch Oral Biol 50: 205–212.
  116. Sire, J.Y., S. Delgado, M. Girondot (2006) The amelogenin story: origin and evolution. Eur J Oral Sci 114(suppl 1): 64–77; discussion 93–95, 379–380.
  117. Smith, M.M. (1995) Heterochrony in the evolution of enamel in vertebrates; in McNamara KJ (ed): Evolutionary Change and Heterochrony. Chichester, Wiley, pp 125–150.
  118. Smith, M.M., B.K. Hall (1990) Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol Rev Camb Philos Soc 65: 277–373.
  119. Spring, J. (1997) Vertebrate evolution by interspecific hybridisation – are we polyploid? FEBS Lett 400: 2–8.
  120. Suga, H., D. Hoshiyama, S. Kuraku, K. Katoh, K. Kubokawa, T. Miyata (1999) Protein tyrosine kinase cDNAs from amphioxus, hagfish, and lamprey: isoform duplications around the divergence of cyclostomes and gnathostomes. J Mol Evol 49: 601–608.
  121. Sullivan, M.M., E.H. Sage (2004) Hevin/SC1, a matricellular glycoprotein and potential tumor-suppressor of the SPARC/BM-40/Osteonectin family. Int J Biochem Cell Biol 36: 991–996.
  122. Termine, J.D., H.K. Kleinman, S.W. Whitson, K.M. Conn, M.L. McGarvey, G.R. Martin (1981) Osteonectin, a bone-specific protein linking mineral to collagen. Cell 26: 99–105.
  123. Timpl, R. (1996) Macromolecular organization of basement membranes. Curr Opin Cell Biol 8: 618–624.
  124. Toyosawa, S., C. O’hUigin, F. Figueroa, H. Tichy, J. Klein (1998) Identification and characterization of amelogenin genes in monotremes, reptiles, and amphibians. Proc Natl Acad Sci USA 95: 13056–13061.
  125. True, J.R., E.S. Haag (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3: 109–119.
  126. Uversky, V.N., J.R. Gillespie, A.L. Fink (2000) Why are ‘natively unfolded’ proteins unstructured under physiologic conditions? Proteins 41: 415–427.
  127. Veis, A. (2003) Mineralization in organic matrix frameworks. Rev Mineral Geochem 54: 249–289.
  128. Vienne, A., J. Rasmussen, L. Abi-Rached, P. Pontarotti, A. Gilles (2003) Systematic phylogenomic evidence of en bloc duplication of the ancestral 8p11.21-8p21.3-like region. Mol Biol Evol 20: 1290–1298.
  129. Ward, J.J., L.J. McGuffin, K. Bryson, B.F. Buxton, D.T. Jones (2004) The DISOPRED server for the prediction of protein disorder. Bioinformatics 20: 2138–2139.
  130. Weiss, K.M., A.V. Buchanan (2004) Genetics and the Logic of Evolution. Hoboken, Wiley.
  131. Weiss, K.M., S.M. Fullerton (2000) Phenogenetic drift and the evolution of genotype-phenotype relationships. Theor Popul Biol 57: 187–195.
  132. Williamson, M.P. (1994) The structure and function of proline-rich regions in proteins. Biochem J 297(Pt 2): 249–260.
  133. Wolfe, K.H. (2001) Yesterday’s polyploids and the mystery of diploidization. Nat Rev Genet 2: 333–341.
  134. Wright, J.T., P.S. Hart, M.J. Aldred, K. Seow, P.J. Crawford, S.P. Hong, C.W. Gibson, T.C. Hart (2003) Relationship of phenotype and genotype in X-linked amelogenesis imperfecta. Connect Tissue Res 44(suppl 1): 72–78.
  135. Yan, Q., E.H. Sage (1999) SPARC, a matricellular glycoprotein with important biological functions. J Histochem Cytochem 47: 1495–1506.
  136. Zeichner-David, M., T. Diekwisch, A. Fincham, E. Lau, M. MacDougall, J. Moradian-Oldak, J. Simmer, M. Snead, H.C. Slavkin (1995) Control of ameloblast differentiation. Int J Dev Biol 39: 69–92.
  137. Zeichner-David, M., K. Oishi, Z. Su, V. Zakartchenko, L.S. Chen, H. Arzate, P. Bringas, Jr. (2003) Role of Hertwig’s epithelial root sheath cells in tooth root development. Dev Dyn 228: 651–663.
  138. Zhang, J. (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18: 292–298.


Pay-per-View Options
Direct payment This item at the regular price: USD 38.00
Payment from account With a Karger Pay-per-View account (down payment USD 150) you profit from a special rate for this and other single items.
This item at the discounted price: USD 26.50