Novel transglutaminase-1 mutations and genotypephenotype investigations of 104 patients with autosomal recessive congenital ichthyosis in the USA

Journal of Medical Genetics

Volumn 46, Issue 2, 2009, Pages 103-111

  Farasat, S ^a   Wei, M H ^b   Herman, M ^a   Liewehr, D J ^a   Steinberg, S M ^a   Bale, S J ^c   Fleckman, P ^d   Toro, J R ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c GENEDX   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PYROXYLIN;

ADOLESCENT; ADULT; AGED; ALOPECIA; ANHIDROSIS; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CHILD; ECTROPION; FEMALE; GENE; GENE MUTATION; GENOTYPE PHENOTYPE CORRELATION; HUMAN; ICHTHYOSIS; INFANT; MAJOR CLINICAL STUDY; MALE; MISSENSE MUTATION; PRIORITY JOURNAL; TRANSGLUTAMINASE 1 GENE;

AMINO ACID SEQUENCE; DNA MUTATIONAL ANALYSIS; GENES, RECESSIVE; GENOTYPE; HUMANS; ICHTHYOSIFORM ERYTHRODERMA, CONGENITAL; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; SEQUENCE ALIGNMENT; TRANSGLUTAMINASES; UNITED STATES;

EID: 62149121322     PISSN: 00222593     EISSN: 14686244     Source Type: Journal    
DOI: 10.1136/jmg.2008.060905     Document Type: Article

References (69)

1. Bale SJ, Doyle SZ. The genetics of ichthyosis: a primer for epidemiologists. J Invest Dermatol 1994;102:49S-50S.
2. Pigg M, Gedde-Dahl T Jr, Cox D, Hausser I, Anton-Lamprecht I, Dahl N. Strong founder effect for a transglutaminase 1 gene mutation in lamellar ichthyosis and congenital ichthyosiform erythroderma from Norway. Eur J Hum Genet 1998;6:589-96.
3. Williams ML, Elias PM. Heterogeneity in autosomal recessive ichthyosis. Clinical and biochemical differentiation of lamellar ichthyosis and nonbullous congenital ichthyosiform erythroderma. Arch Dermatol 1985;121:477-88.
4. Russell LJ, DiGiovanna JJ, Hashem N, Compton JG, Bale SJ. Linkage of autosomal recessive lamellar ichthyosis to chromosome 14q. Am J Hum Genet 1994;55:1146-52.
5. Russell LJ, DiGiovanna JJ, Rogers GR, Steinert PM, Hashem N, Compton JG, Bale SJ. Mutations in the gene for transglutaminase 1 in autosomal recessive lamellar ichthyosis. Nat Genet 1995;9:279-83.
6. Akiyama M, Takizawa Y, Kokaji T, Shimizu H. Novel mutations of TGM1 in a child with congenital ichthyosiform erythroderma. Br J Dermatol 2001;144:401-7.
7. Akiyama M, Takizawa Y, Suzuki Y, Ishiko A, Matsuo I, Shimizu H. Compound heterozygous TGM1 mutations including a novel missense mutation L204Q in a mild form of lamellar ichthyosis. J Invest Dermatol 2001;116:992-5.
8. Akiyama M, Takizawa Y, Suzuki Y, Shimizu H. A novel homozygous mutation 371delA in TGM1 leads to a classic lamellar ichthyosis phenotype. Br J Dermatol 2003;148:149-53.
9. Becker K, Csikos M, Sardy M, Szalai ZS, Horvath A, Karpati S. Identification of two novel nonsense mutations in the transglutaminase 1 gene in a Hungarian patient with congenital ichthyosiform erythroderma. Exp Dermatol 2003;12:324-9.
10. Bichakjian CK, Nair RP, Wu WW, Goldberg S, Elder JT. Prenatal exclusion of lamellar ichthyosis based on identification of two new mutations in the transglutaminase 1 gene. J Invest Dermatol 1998;110:179-82.
11. Cserhalmi-Friedman PB, Milstone LM, Christiano AM. Diagnosis of autosomal recessive lamellar ichthyosis with mutations in the TGM1 gene. Br J Dermatol 2001;144:726-30.
12. Esposito G, Auricchio L, Rescigno G, Paparo F, Rinaldi M, Salvatore F. Transglutaminase 1 gene mutations in Italian patients with autosomal recessive lamellar ichthyosis. J Invest Dermatol 2001;116:809-12.
13. Esposito G, Tadini G, Paparo F, Viola A, leno L, Pennacchia W, Messina F, Giordano L, Piccirillo A, Auricchio L Transglutaminase 1 deficiency and corneocyte collapse: an indication for targeted molecular screening in autosomal recessive congenital ichthyosis. Br J Dermatol 2007;157:808-10.
14. Hennies HC, Raghunath M, Wiebe V, Vogel M, Velten F, Traupe H, Reis A. Genetic and immunohistochemical detection of mutations inactivating the keratinocyte transglutaminase in patients with lamellar ichthyosis. Hum Genet 1998;102:314-18.
15. Hennies HC, Kuster W, Wiebe V, Krebsova A, Reis A. Genotype/phenotype correlation in autosomal recessive lamellar ichthyosis. Am J Hum Genet 1998;62:1052-61.
16. Huber M, Rettler I, Bernasconi K, Frenk E, Lavrijsen SP, Ponec M, Bon A, Lautenschlager S, Schorderet DF, Hohl D. Mutations of keratinocyte transglutaminase in lamellar ichthyosis. Science 1995;267:525-8.
17. Huber M, Yee VC, Burri N, Vikerfors E, Lavrijsen AP, Paller AS, Hohl D. Consequences of seven novel mutations on the expression and structure of keratinocyte transglutaminase. J Biol Chem 1997;272:21018-26.
18. Jessen BA, Phillips MA, Hovnanian A, Rice RH. Role of Sp1 response element in transcription of the human transglutaminase 1 gene. J Invest Dermatol 2000;115:113-17.
19. Kon A, Takeda H, Sasaki H, Yoneda K, Nomura K, Ahvazi B, Steinert PM, Hanada K, Hashimoto I. Novel transglutaminase 1 gene mutations (R348X/Y365D) in a Japanese family with lamellar ichthyosis. J Invest Dermatol 2003;120:170-2.
20. Laiho E, Ignatius J, Mikkola H, Yee VC, Teller DC, Niemi KM, Saarialho-Kere U, Kere J, Palotie A. Transglutaminase 1 mutations in autosomal recessive congenital ichthyosis: private and recurrent mutations in an isolated population. Am J Hum Genet 1997;61:529-38.
21. Lugassy J, Hennies HC, Indelman M, Khamaysi Z, Bergman R, Sprecher E. Rapid detection of homozygous mutations in congenital recessive ichthyosis. Arch Dermatol Res 2008;300:81-5.
22. Mizrachi-Koren M, Shemer S, Morgan M, Indelman M, Khamaysi Z, Petronius D, Bitterman-Deutsch O, Hennies HC, Bergman R, Sprecher E. Homozygosity mapping as a screening tool for the molecular diagnosis of hereditary skin diseases in consanguineous populations. J Am Acad Dermatol 2006;55:393-401.
23. Oji V, Hautier JM, Ahvazi B, Hausser I, Aufenvenne K, Walker T, Seller N, Steijlen PM, Kuster W, Hovnanian A, Hennies HC, Traupe H. Bathing suit ichthyosis is caused by transglutaminase-1 deficiency: evidence for a temperature-sensitive phenotype. Hum Mol Genet 2006;15:3083-97.
24. Parmentier L, Blanchet-Bardon C, Nguyen S, Prud'homme JF, Dubertret L, Weissenbach J. Autosomal recessive lamellar ichthyosis: identification of a new mutation in transglutaminase 1 and evidence for genetic heterogeneity. Hum Mol Genet 1995;4:1391-5.
25. Petit E, Huber M, Rochat A, Bodemer C, Teillac-Hamel D, Muh JP, Revuz J, Barrandon Y, Lathrop M, de Prost Y, Hohl D, Hovnanian A. Three novel point mutations in the keratinocyte transglutaminase (TGK) gene in lamellar ichthyosis: significance for mutant transcript level, TGK immunodetection and activity. Eur J Hum Genet 1997;5:218-28.
26. Pigg M, Gedde-Dahl T Jr, Cox DW, Haugen G, Dahl N. Haplotype association and mutation analysis of the transglutaminase 1 gene for prenatal exclusion of lamellar ichthyosis. Prenat Diagn 2000;20:132-7.
27. Raghunath M, Hennies HC, Ahvazi B, Vogel M, Reis A, Steinert PM, Traupe H. Selfhealing collodion baby: a dynamic phenotype explained by a particular transglutaminase-1 mutation. J Invest Dermatol 2003;120:224-8.
28. Schorderet DF, Huber M, Laurini RN, Von Moos G, Gianadda B, Délèze G, Hohl D. Prenatal diagnosis of lamellar ichthyosis by direct mutational analysis of the keratinocyte transglutaminase gene. Prenat Diagn 1997;17:483-6.
29. Shevchenko YO, Compton JG, Toro JR, DiGiovanna JJ, Bale SJ. Splice-site mutation in TGM1 in congenital recessive ichthyosis in American families: molecular, genetic, genealogic, and clinical studies. Hum Genet 2000;106:492-9.
30. Tok J, Garzon MC, Cserhalmi-Friedman P, Lam HM, Spitz JL, Christiano AM. Identification of mutations in the transglutaminase 1 gene in lamellar ichthyosis. Exp Dermatol 1999;8:128-33.
31. Yang JM, Ahn KS, Cho MO, Yoneda K, Lee CH, Lee JH, Lee ES, Candi E, Melino G, Ahvazi B, Steinert PM. Novel mutations of the transglutaminase 1 gene in lamellar ichthyosis. J Invest Dermatol 2001;117:214-18.
32. Yotsumoto S, Akiyama M, Yoneda K, Fukushige T, Kobayashi K, Saheki T, Kanzaki T. Analyses of the transglutaminase 1 gene mutation and ultrastructural characteristics in a Japanese patient with lamellar ichthyosis. J Dermatol Sci 2000;24:119-25.
33. Rice RH, Crumrine D, Uchida Y, Gruber R, Elias PM. Structural changes in epidermal scale and appendages as indicators of defective TGM1 activity. Arch Dermatol Res 2005;297:127-33.
34. Oji V, Traupe H. Ichthyoses: differential diagnosis and molecular genetics. Eur J Dermatol 2006;16:349-59.
35. Boeshans KM, Mueser TC, Ahvazi B. A three-dimensional model of the human transglutaminase 1: insights into the understanding of lamellar ichthyosis. J Mol Model 2007;13:233-46.
36. Kim IG, McBride OW, Wang M, Kim SY, Idler WW, Steinert PM. Structure and organization of the human transglutaminase-1 gene. J Biol Chem 1992;267:7710-17.
37. Robinson NA, Lapic S, Welter JF, Eckert RL S100A11, S100A10, annexin I, desmosomal proteins, small proline-rich proteins, plasminogen activator inhibitor-2, and involucrin are components of the cornified envelope of cultured human epidermal keratinocytes. J Biol Chem 1997;272:12035-46.
38. Steinert PM, Marekov LN. The proteins elafin, filaggrin, keratin intermediate filaments, loricrin, and small proline-rich proteins 1 and 2 are isodipeptide cross-linked components of the human epidermal cornified cell envelope. J Biol Chem 1995;270:17702-11.
39. Candi E, Melino G, Lahm A, Ceci R, Rossi A, Kim IG, Ciani B, Steinert PM. Transglutaminase 1 mutations in lamellar ichthyosis. Loss of activity due to failure of activation by proteolytic processing. J Biol Chem 1998;273:13693-702.
40. Muramatsu S, Suga Y, Kon J, Matsuba S, Hashimoto Y, Ogawa H. A Japanese patient with a mild form of lamellar ichthyosis harbouring two missense mutations in the core domain of the transglutaminase 1 gene. Br J Dermatol 2004;150:390-2.
41. Matsuki M, Yamashita F, Ishida-Yamamoto A, Yamada K, Kinoshita C, Fushiki S, Ueda E, Morishima Y, Tabata K, Yasuno H, Hashida M, lizuka H, Ikawa M, Okabe M, Kondoh G, Kinoshita T, Takeda J, Yamanishi K. Defective stratum corneum and early neonatal death in mice lacking the gene for transglutaminase 1 (keratinocyte transglutaminase). Proc Natl Acad Sci U S A 1998;95:1044-9.
42. Akiyama M. Harlequin ichthyosis and other autosomal recessive congenital ichthyoses: the underlying genetic defects and pathomechanisms. J Dermatol Sci 2006;42:83-9.
43. Annilo T, Shulenin S, Chen ZQ, Arnould I, Prades C, Lemoine C, Maintoux-Larois C, Devaud C, Dean M, Denèfle P, Rosier M. Identification and characterization of a novel ABCA subfamily member, ABCA12, located in the lamellar ichthyosis region on 2q34. Cytogenet Genome Res 2002;98:169-76.
44. Akiyama M, Sugiyama-Nakagiri Y, Sakai K, McMillan JR, Goto M, Arita K, Tsuji-Abe Y, Tabata N, Matsuoka K, Sasaki R, Sawamura D, Shimizu H. Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. J Clin Invest 2005;115:1777- 84.
45. Kelsell DP, Norgett EE, Unsworth H, Teh MT, Cullup T, Mein CA, Dopping-Hepenstal PJ, Dale BA, Tadini G, Fleckman P, Stephens KG, Sybert VP, Mallory SB, North BV, Witt DR, Sprecher E, Taylor AE, llchyshyn A, Kennedy CT, Goodyear H, Moss C, Paige D, Harper Jl, Young BD, Leigh IM, Eady RA, O'Toole EA. Mutations in ABCA12 underlie the severe congenital skin disease harlequin ichthyosis. Am J Hum Genet 2005;76:794-803.
46. Lefèvre C, Audebert S, Jobard F, Bouadjar B, Lakhdar H, Boughdene-Stambouli O, Blanchet-Bardon C, Heilig R, Foglio M, Weissenbach J, Lathrop M, Prud'homme JF, Fischer J. Mutations in the transporter ABCA12 are associated with lamellar ichthyosis type 2. Hum Mol Genet 2003;12:2369-78.
47. Jobard F, Lefevre C, Karaduman A, Blanchet-Bardon C, Emre S, Weissenbach J, Ozgüc M, Lathrop M, Prud'homme JF, Fischer J. Lipoxygenase-3 (ALOXE3) and 12(R)-lipoxygenase (ALOX12B) are mutated in non-bullous congenital ichthyosiform erythroderma (NCIE) linked to chromosome 17p13.1. Hum Mol Genet 2002;11:107-13.
48. Lefèvre C, Bouadjar B, Karaduman A, Jobard F, Saker S, Ozguc M, Lathrop M, Prud'homme JF, Fischer J. Mutations in ichthyin a new gene on chromosome 5q33 in a new form of autosomal recessive congenital ichthyosis. Hum Mol Genet 2004;13:2473-82.
49. Lefèvre C, Bouadjar B, Ferrand V, Tadini G, Mégarbané A, Lathrop M, Prud'homme JF, Fischer J. Mutations in a new cytochrome P450 gene in lamellar ichthyosis type 3. Hum Mol Genet 2006;15:767-76.
50. Ganemo A, Pigg M, Virtanen M, Kukk T, Raudsepp H, Rossman-Ringdahl I, Westermark P, Niemi KM, Dahl N, Vahlquist A. Autosomal recessive congenital ichthyosis in Sweden and Estonia: clinical, genetic and ultrastructural findings in eighty-three patients. Acta Derm Venereol 2003;83:24-30.
51. Laiho E, Niemi KM, Ignatius J, Kere J, Palotie A, Saarialho-Kere U. Clinical and morphological correlations for transglutaminase 1 gene mutations in autosomal recessive congenital ichthyosis. Eur J Hum Genet 1999;7:625-32.
52. Richards B, Skoletsky J, Shuber AP, Balfour R, Stern RC, Dorkin HL, Parad RB, Witt D, Klinger KW. Multiplex PCR amplification from the CFTR gene using DNA prepared from buccal brushes/swabs. Hum Mol Genet 1993;2:159-63.
53. Mehta CR, Patel NR. A network algorithm for performing Fisher's exact test in r × c contingency tables. J Am Stat Assoc 1983;78:427-34.
54. Agresti A. Categorical data analysis. New York: Johns Wiley and Sons, Inc., 1990.
55. Hollander M, Wolfe DA. Nonparametric statistical analysis, 2nd ed. New York: John Wiley and Sons Inc., 1999.
56. Arita K, Jacyk WK, Wessagowit V, van Rensburg EJ, Chaplin T, Mein CA, Akiyama M, Shimizu H, Happle R, McGrath JA. The South African "bathing suit ichthyosis" is a form of lamellar ichthyosis caused by a homozygous missense mutation, p.R315L, in transglutaminase 1. J Invest Dermatol 2007;127:490-3.
57. Shawky RM, Sayed NS, Elhawary NA. Mutations in transglutaminase 1 gene in autosomal recessive congenital ichthyosis in Egyptian families. Dis Markers 2004;20:325-32.
58. Huber M, Rettler I, Bernasconi K, Wyss M, Hohl D. Lamellar ichthyosis is genetically heterogeneous-cases with normal keratinocyte transglutaminase. J Invest Dermatol 1995;105:653-4.
59. Atschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389-3402.
60. Vitkup D, Sander C, Church GM. The amino-acid mutational spectrum of human genetic disease. Genome Biol 2003;4:R72.
61. Cooper DN, Youssoufian H. The CpG dinucleotide and human genetic disease. Hum Genet 1988;78:151-5.
62. Krawczak M, Ball EV, Cooper DN. Neighboring-nucleotide effects on the rates of germ-line single-base-pair substitution in human genes. Am J Hum Genet 1998;63:474-88.
63. Lüleyap HU, Alptekin D, Pazarbasi A, Kasap M, Kasap H, Demirhindi H, Mungan N, Ozer G, Froster UG. The importance of arginine mutation for the evolutionary structure and function of phenylalanine hydroxylase gene. Mutat Res 2006;601:39-45.
64. Letai A, Coulombe PA, McCormick MB, Yu QC, Hutton E, Fuchs E. Disease severity correlates with position of keratin point mutations in patients with epidermolysis bullosa simplex. Proc Natl Acad Sci U S A 1993;90:3197-201.
65. Yoneda K, Akiyama M, Morita K, Shimizu H, Imamura S, Kim SY. Expression of transglutaminase 1 in human hair follicles, sebaceous glands and sweat glands, Br J Dermiatol 1998;138:37-44.
66. Mcintosh I, Hamosh A, Dietz HC. Nonsense mutations and diminished mRNA levels. Nat Genet 1993;4:219.
67. Maquat LE. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 2004;5:89-99.
68. Phillips MA, Baden HP. Ichthyosiform dermatoses. In: Fitzpatrick TB, Eisen AZ, Wolff K, Freedberg IM, Austen KF, eds. Dermatology in general medicine, 4th ed. New York: McGraw-Hill, Inc., 1993:531-44.
69. Rossmann-Ringdahl I, Anton-Lamprecht I, Swanbeck G. A mother and two children with nonbullous congenital ichthyosiform erythroderma. Arch Dermatol 1986;122:559-64.