Human Genetics

, Volume 120, Issue 5, pp 653–662 | Cite as

A new locus for autosomal dominant amelogenesis imperfecta on chromosome 8q24.3

  • Gustavo Mendoza
  • Trevor J. Pemberton
  • Kwanghyuk Lee
  • Raquel Scarel-Caminaga
  • Ruty Mehrian-Shai
  • Catalina Gonzalez-Quevedo
  • Vasiliki Ninis
  • Jaana Hartiala
  • Hooman Allayee
  • Malcolm L. Snead
  • Suzanne M. Leal
  • Sergio R. P. Line
  • Pragna I. Patel
Original Investigation

Abstract

Amelogenesis imperfecta (AI) is a collective term used to describe phenotypically diverse forms of defective tooth enamel development. AI has been reported to exhibit a variety of inheritance patterns, and several loci have been identified that are associated with AI. We have performed a genome-wide scan in a large Brazilian family segregating an autosomal dominant form of AI and mapped a novel locus to 8q24.3. A maximum multipoint LOD score of 7.5 was obtained at marker D8S2334 (146,101,309 bp). The disease locus lies in a 1.9 cM (2.1 Mb) region according to the Rutgers Combined Linkage-Physical map, between a VNTR marker (at 143,988,705 bp) and the telomere (146,274,826 bp). Ten candidate genes were identified based on gene ontology and microarray-facilitated gene selection using the expression of murine orthologues in dental tissue, and examined for the presence of a mutation. However, no causative mutation was identified.

Notes

Acknowledgments

This research was supported by grants DE14102 (P.I.P.) and DE06988 (M.L.S.) from the National Institute of Dental and Craniofacial Research. Genotyping services were provided by the Center for Inherited Disease Research (CIDR). CIDR is fully funded through a federal contract from the National Institutes of Health to The Johns Hopkins University, contract number N01-HG-65403. This investigation was conducted in a facility constructed with support from Research Facilities Improvement Program Grant Number C06 (RR10600-01, CA62528-01, RR14514-01) from the National Center for Research Resources, National Institutes of Health.

References

  1. Aldred MJ, Savarirayan R, Crawford PJM (2003) Amelogenesis imperfecta: a classification and catalogue for the 21st century. Oral Dis 9:19–23PubMedCrossRefGoogle Scholar
  2. Aubin I, Adams CP, Opsahl S, Septier D, Bishop CE, Auge N, Salvayre R, Negre-Salvayre A, Goldberg M, Guenet J-L, Poirier C (2005) A deletion in the gene encoding sphingomyelin phosphodiesterase 3 (Smpd3) results in osteogenesis and dentinogenesis imperfecta in the mouse. Nat Genet 37:803–805PubMedCrossRefGoogle Scholar
  3. Backman B, Holm AK (1986) Amelogenesis imperfecta: prevalence and incidence in a northern Swedish county. Community Dent Oral Epidemiol 14:43–47PubMedCrossRefGoogle Scholar
  4. Bartlett JD, Simmer JP, Xue J, Margolis HC, Moreno EC (1996) Molecular cloning and mRNA tissue distribution of a novel matrix metalloproteinase isolated from porcine enamel organ. Gene 183:123–128PubMedCrossRefGoogle Scholar
  5. Bartlett JD, Skobe Z, Lee DH, Wright JT, Li Y, Kulkarni AB, Gibson CW (2006) A developmental comparison of matrix metalloproteinase-20 and amelogenin null mouse enamel. Eur J Oral Sci 114:18–23PubMedCrossRefGoogle Scholar
  6. Beniash E, Skobe Z, Bartlett JD (2006) Formation of the dentino-enamel interface in enamelysin (MMP-20)-deficient mouse incisors. Eur J Oral Sci 114:24–29PubMedCrossRefGoogle Scholar
  7. Burstein E, Hoberg JE, Wilkinson AS, Rumble JM, Csomos RA, Komarck CM, Maine GN, Wilkinson JC, Mayo MW, Duckett CS (2005) COMMD proteins, a novel family of structural and functional homologs of MURR1. J Biol Chem 280:22222–22232PubMedCrossRefGoogle Scholar
  8. Caterina J, Shi J, Krakora S, Bartlett JD, Engler JA, Kozak CA, Birkedal-Hansen H (1999) Isolation, characterization, and chromosomal location of the mouse enamelysin gene. Genomics 62:308–311PubMedCrossRefGoogle Scholar
  9. Chosack A, Eidelman E, Wisotski I, Cohen T (1979) Amelogenesis imperfecta among Israeli Jews and the description of a new type of local hypoplastic autosomal recessive amelogenesis imperfecta. Oral Surg Oral Med Oral Pathol 47:148–156PubMedGoogle Scholar
  10. Coffield KD, Phillips C, Brady M, Roberts MW, Strauss RP, Wright JT (2005) The psychosocial impact of developmental dental defects in people with hereditary amelogenesis imperfecta. J Am Dent Assoc 136:620–630PubMedGoogle Scholar
  11. Cottingham RWJ, Idury RM, Schaffer AA (1993) Faster sequential genetic linkage computations. Am J Hum Genet 53:252–263PubMedGoogle Scholar
  12. Dantonel J-C, Murthy KGK, Manley JL, Tora L (1997) Transcription factor TFIID recruits factor CPSF for formation of 3′ end of mRNA. Nature 389:399–402PubMedCrossRefADSGoogle 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 108:353–358PubMedCrossRefGoogle Scholar
  14. Dong J, Amor D, Aldred MJ, Gu T, Escamilla M, MacDougall M (2005) DLX3 mutation associated with autosomal dominant amelogenesis imperfecta with taurodontism. Am J Med Genet Part A 133A:138–141CrossRefGoogle Scholar
  15. Dufner-Beattie J, Wang F, Kuo Y-M, Gitschier J, Eide D, Andrews GK (2003) The acrodermatitis enteropathica gene ZIP4 encodes a tissue-specific, zinc-regulated zinc transporter in mice. J Biol Chem 278:33474–33481PubMedCrossRefGoogle Scholar
  16. Edgar R, Domrachev M, Lash AE (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nuc Acids Res 30:207–210CrossRefGoogle Scholar
  17. Espiritu-Santo AR, Line SRP (2005) The enamel organic matrix: structure and function. Braz. J Oral Sci 4:716–724Google Scholar
  18. Fong CD, Hammarstrom L (2000) Expression of amelin and amelogenin in epithelial root sheath remnants of fully formed rat molars. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 90:218–223PubMedGoogle Scholar
  19. Fujiwara S, Takeo N, Otani Y, Parry DAD, Kunimatsu M, Lu R, Sasaki M, Matsuo N, Khaleduzzaman M, Yoshioka H (2001) Epiplakin, a novel member of the Plakin family originally identified as a 450-kDa human epidermal autoantigen. Structure and tissue localization. J Biol Chem 276:13340–13347PubMedCrossRefGoogle Scholar
  20. Gentleman R, Carey V, Bates D, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini A, Sawitzki G, Smith C, Smyth G, Tierney L, Yang J, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80PubMedCrossRefGoogle Scholar
  21. Ghoul-Mazgar S, Hotton D, Lezot F, Blin-Wakkach C, Asselin A, Sautier JM, Berdal A (2005) Expression pattern of Dlx3 during cell differentiation in mineralized tissues. Bone 37:799–809PubMedCrossRefGoogle Scholar
  22. Hart PS, Hart TC, Michalec MD, Ryu OH, Simmons D, Hong S, Wright JT (2004) Mutation in kallikrein 4 causes autosomal recessive hypomaturation amelogenesis imperfecta. J Med Genet 41:545–549PubMedCrossRefGoogle Scholar
  23. Hart TC, Hart PS, Gorry MC, Michalec MD, Ryu OH, Uygur C, Ozdemir D, Firatli S, Aren G, Firatli E (2003) Novel ENAM mutation responsible for autosomal recessive amelogenesis imperfecta and localised enamel defects. J Med Genet 40:900–906PubMedCrossRefGoogle Scholar
  24. Horer J, Blum R, Feick P, Nastainczyk W, Schulz I (1999) A comparative study of rat and human Tmp21 (p23) reveals the pseudogene-like features of human Tmp21-II. DNA Seq 10:121–126PubMedGoogle Scholar
  25. Horie M, Okutomi K, Taniguchi Y, Ohbuchi Y, Suzuki M, Takahashi E-i (1998) Isolation and characterization of a new member of the human Ly6 gene family (LY6H). Genomics 53:365–368PubMedCrossRefGoogle Scholar
  26. Hu CC, Fukae M, Uchida T, Qian Q, Zhang CH, Ryu OH, Tanabe T, Yamakoshi Y, Murakami C, Dohi N, Shimizu M, Simmer JP (1997) Cloning and characterization of porcine enamelin mRNAs. J Dent Res 76:1720–1729PubMedGoogle Scholar
  27. Hu JC, Sun X, Zhang C, Liu S, Bartlett JD, Simmer JP (2002) Enamelysin and kallikrein-4 mRNA expression in developing mouse molars. Eur J Oral Sci 110:307–315PubMedCrossRefGoogle Scholar
  28. 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 80:898–902PubMedGoogle Scholar
  29. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostat 4:249–264CrossRefMATHGoogle Scholar
  30. Jang S-I, Kalinin A, Takahashi K, Marekov LN, Steinert PM (2005) Characterization of human epiplakin: RNAi-mediated epiplakin depletion leads to the disruption of keratin and vimentin IF networks. J Cell Sci 118:781–793PubMedCrossRefGoogle Scholar
  31. Kataoka K, Han S-i, Shioda S, Hirai M, Nishizawa M, Handa H (2002) MafA is a glucose-regulated and pancreatic beta-cell-specific transcriptional activator for the insulin gene. J Biol Chem 277:49903–49910PubMedCrossRefGoogle Scholar
  32. Kim J-W, Simmer JP, Lin BPL, Seymen F, Bartlett JD, Hu JCC (2006) Mutational analysis of candidate genes in 24 amelogenesis imperfecta families. Eur J Oral Sci 114:3–12PubMedCrossRefGoogle Scholar
  33. Kong X, Murphy K, Raj T, He C, White PS, Matise TC (2004) A combined linkage-physical map of the human genome. Am J Hum Genet 75:1143–1148PubMedCrossRefGoogle Scholar
  34. Lagerstrom M, Dahl N, Nakahori Y, Nakagome Y, Backman B, Landegren U, Pettersson U (1991) A deletion in the amelogenin gene (AMG) causes X-linked amelogenesis imperfecta (AIH1). Genomics 10:971–975PubMedCrossRefGoogle Scholar
  35. Lewis TB, Wood S, Michaelis EK, DuPont BR, Leach RJ (1996) Localization of a gene for a glutamate binding subunit of a NMDA receptor (GRINA) to 8q24. Genomics 32:131–133PubMedCrossRefGoogle Scholar
  36. Llano E, Pendas AM, Knauper V, Sorsa T, Salo T, Salido E, Murphy G, Simmer JP, Bartlett JD, Lopez-Otin C (1997) Identification and structural and functional characterization of human enamelysin (MMP-20). Biochemistry 36:15101–15108PubMedCrossRefGoogle Scholar
  37. Luo W, Wen X, Wang HJ, MacDougall M, Snead ML, Paine ML (2004) In vivo overexpression of Tuftelin in the enamel organic matrix. Cells Tiss Organs 177:212–220CrossRefGoogle Scholar
  38. Nagano T, Oida S, Ando H, Gomi K, Arai T, Fukae M (2003) Relative levels of mRNA encoding enamel proteins in enamel organ epithelia and odontoblasts. J Dent Res 82:982–986PubMedGoogle Scholar
  39. O’Connell JR, Weeks DE (1998) PedCheck: a program for identification of genotype incompatibilities in linkage analysis. Am J Hum Genet 63:259–266PubMedCrossRefGoogle Scholar
  40. Ohishi K, Inoue N, Maeda Y, Takeda J, Riezman H, Kinoshita T (2000) Gaa1p and Gpi8p are components of a glycosylphosphatidylinositol (GPI) transamidase that mediates attachment of GPI to proteins. Mol Biol Cell 11:1523–1533PubMedGoogle Scholar
  41. Ozdemir D, Hart PS, Ryu OH, Choi SJ, Ozdemir-Karatas M, Firatli E, Piesco N, Hart TC (2005) MMP20 active-site mutation in hypomaturation amelogenesis imperfecta. J Dent Res 84:1031–1035PubMedGoogle Scholar
  42. Paine ML, Wang H-J, Luo W, Krebsbach PH, Snead ML (2003) A Transgenic animal model resembling amelogenesis imperfecta related to ameloblastin overexpression. J Biol Chem 278:19447–19452PubMedCrossRefGoogle Scholar
  43. Paine ML, White SN, Luo W, Fong H, Sarikaya M, Snead ML (2001) Regulated gene expression dictates enamel structure and tooth function. Mat Biol 20:273–292CrossRefGoogle Scholar
  44. Papagerakis P, MacDougall M, Hotton D, Bailleul-Forestier I, Oboeuf M, Berdal A (2003) Expression of amelogenin in odontoblasts. Bone 32:228–240PubMedCrossRefGoogle Scholar
  45. Platenik J, Kuramoto N, Yoneda Y (2000) Molecular mechanisms associated with long-term consolidation of the NMDA signals. Life Sci 67:335–364PubMedCrossRefGoogle Scholar
  46. Price JA, Bowden DW, Wright JT, Pettenati MJ, Hart TC (1998) Identification of a mutation in DLX3 associated with tricho-dento-osseous (TDO) syndrome. Hum Molec Genet 7:563–569PubMedCrossRefGoogle Scholar
  47. Price JA, Wright JT, Walker SJ, Crawford PJM, Aldred MJ, Hart TC (1999) Tricho-dento-osseous syndrome and amelogenesis imperfecta with taurodontism are genetically distinct conditions. Clin Genet 56:35–40PubMedCrossRefGoogle Scholar
  48. Raiborg C, Rusten TE, Stenmark H (2003) Protein sorting into multivesicular endosomes. Curr Opin Cell Biol 15:446–455PubMedCrossRefGoogle Scholar
  49. 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 10:1673–1677PubMedCrossRefGoogle Scholar
  50. Schuler GD (1997) Sequence Mapping by Electronic PCR. Genome Res 7:541–550PubMedGoogle Scholar
  51. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article 3Google Scholar
  52. Snead ML, Luo W, Lau EC, Slavkin HC (1988) Spatial- and temporal-restricted pattern for amelogenin gene expression during mouse molar tooth organogenesis. Development 104:77–85PubMedGoogle Scholar
  53. Sobel E, Lange K (1996) Descent graphs in pedigree analysis: applications to haplotyping, location scores, and marker-sharing statistics. Am J Hum Genet 58:1323–1337PubMedGoogle Scholar
  54. Solban N, Jia H-P, Richard S, Tremblay S, Devlin AM, Peng J, Gossard F, Guo D-F, Morel G, Hamet P, Lewanczuk R, Tremblay J (2000) HCaRG, a novel calcium-regulated gene coding for a nuclear protein, is potentially involved in the regulation of cell proliferation. J Biol Chem 275:32234–32243PubMedCrossRefGoogle Scholar
  55. Stephanopoulos G, Garefalaki ME, Lyroudia K (2005) Genes and related proteins involved in amelogenesis imperfecta. J Dent Res 84:1117–1126PubMedCrossRefGoogle Scholar
  56. Sundell S (1986) Hereditary amelogenesis imperfecta. An epidemiological, genetic and clinical study in a Swedish child population. Swed Dent J Suppl 31:1–38PubMedADSGoogle Scholar
  57. Witkop CJ (1976) Clinical aspects of dental anomalies. Int Dent J 26:378–390PubMedGoogle Scholar
  58. Wright JT, Daly B, Simmons D, Hong S, Hart SP, Hart TC, Atsawasuwan P, Yamauchi M (2006) Human enamel phenotype associated with amelogenesis imperfecta and a kallikrein-4 (g.2142G > A) proteinase mutation. Eur J Oral Sci 114:13–17PubMedCrossRefGoogle Scholar
  59. Wright JT, Hall K, Yamauchi M (1997) The protein composition of normal and developmentally defective enamel. Ciba Found Symp 205:85–99PubMedGoogle Scholar
  60. Zhou S, Zawel L, Lengauer C, Kinzler KW, Vogelstein B (1998) Characterization of Human FAST-1, a TGF[beta] and Activin Signal Transducer. Mol Cell 2:121–127PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Gustavo Mendoza
    • 1
  • Trevor J. Pemberton
    • 1
  • Kwanghyuk Lee
    • 2
  • Raquel Scarel-Caminaga
    • 3
  • Ruty Mehrian-Shai
    • 1
  • Catalina Gonzalez-Quevedo
    • 1
  • Vasiliki Ninis
    • 4
  • Jaana Hartiala
    • 1
  • Hooman Allayee
    • 1
  • Malcolm L. Snead
    • 5
  • Suzanne M. Leal
    • 2
  • Sergio R. P. Line
    • 6
  • Pragna I. Patel
    • 1
    • 5
  1. 1.Institute for Genetic MedicineUniversity of Southern CaliforniaLos AngelesUSA
  2. 2.Department of Molecular and Human GeneticsBaylor College of MedicineHoustonUSA
  3. 3.School of DentistryUniversity of São Paulo State, UNESPAraraquaraBrazil
  4. 4.Department of NeurologyBaylor College of MedicineHoustonUSA
  5. 5.Center for Craniofacial Molecular BiologyUniversity of Southern CaliforniaLos AngelesUSA
  6. 6.Faculty of Odontology of PiracicabaUNICAMPCampinasBrazil

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