Arg555Gln Mutation of TGFBI Gene in Geographical-type Reis Bücklers Corneal Dystrophy in a Chinese Family
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1 The Journal of International Medical Research 2012; 40: Arg555Gln Mutation of TGFBI Gene in Geographical-type Reis Bücklers Corneal Dystrophy in a Chinese Family MZ PIAO 1, XT ZHOU 1, LC WU 2 AND RY CHU 1 1 National Ministry of Health Key Laboratory of Myopia, Eye and ENT Hospital Affiliated to Fudan University, Shanghai, China; 2 Central Hospital of Jing an District, Shanghai, China OBJECTIVE: Mutations of the transforming growth factor b-induced (TGFBI) gene were studied in a Chinese family with Reis Bücklers corneal dystrophy (RBCD). METHODS: Six family members with RBCD and six unaffected family members were investigated. The pedigree showed a typical dominant inheritance pattern. Genomic DNA was extracted from peripheral leucocytes from all study participants. Exons 4, 12 and 14 of the TGFBI gene were analysed using polymerase chain reaction, and standard automated sequencing was performed. Corneal tissue sampled from the proband during phototherapeutic keratectomy was examined using transmission electron microscopy (TEM). RESULTS: A typical geographical pattern of fine opacities in Bowman s layer of the cornea was seen in all six s on slit-lamp examination. An Arg555Gln (R555Q) mutation of the TGFBI gene was identified in all six s but was absent in all unaffected family members. TEM revealed rodshaped bodies in Bowman s layer of the cornea. CONCLUSIONS: In this Chinese family an R555Q mutation of the TGFBI gene was associated with RBCD. As the RBCD phenotype is usually associated with an R124L mutation, this novel genotype phenotype correlation may prompt further investigation of Bowman s layer corneal dystrophy. KEY WORDS: REIS BÜCKLERS CORNEAL DYSTROPHY; GEOGRAPHICAL TYPE; TGFBI; GENE MUTATION Introduction Reis Bücklers corneal dystrophy (RBCD) is a rare type of Bowman s layer corneal dystrophy that is inherited in an autosomal dominant manner. RBCD s experience recurrent erosions of the corneal epithelium within the first decade of life and moderate impairment of eyesight with ageing. 1 The disease was first reported in 1917 by Reis 2 and described in more detail in 1949 by Bücklers, 3 who reported eosinophilic deposits that were congophilic and did not stain with periodic acid Schiff on histopathological examination. Examination by light microscope revealed rod-shaped and trapezoidal deposits in the Bowman s layer. Mutations associated with RBCD have been mapped to the transforming growth factor, β-induced (TGFBI) gene on chromosome 5q31; 4 granular corneal dystrophy, lattice corneal dystrophy, Avellino corneal dystrophy and Thiel Behnke corneal 1149
2 dystrophy (TBCD) are also associated with mutations of this gene. 5 The TGFBI gene contains 17 exons encoding 683 amino acids. To date, 33 different mutations have been identified in this gene; mutations at Arg124 6 and Arg555 5 account for more than half of all s with these corneal dystrophies. RBCD has been reported to be associated with the R124L mutation 7 or with atypical cases of F540, 8 H626R, 9 G623D 10 or R124C 11 mutations; however, reports on RBCD in Chinese s are rare. In the present study, TGFBI gene mutations were investigated in a Chinese family that included six members with RBCD. Patients and methods STUDY PARTICIPANTS Six members with RBCD and six unaffected members from one Chinese family were included in the study. The pedigree is shown in Fig. 1 and shows a typical dominant inheritance pattern. Unaffected family members with one (II 1, III 3, III 8 and III 13 ) or two (IV 2 and IV 7 ) unaffected parents were chosen for inclusion. The female proband ( III 5 ) attended the out clinic of the Eye and ENT Hospital Affiliated to Fudan University, Shanghai, China, at 39 years of age in March She had progressive visual impairment and recurring intermittent photophobia in both eyes since the age of 7 years. The current frequency of recurrence of symptoms was more than four times a year. The condition had previously been misdiagnosed as viral keratitis, which usually resolves naturally over a 2-week period. The frequency of corneal erosion had gradually decreased and best-corrected visual acuity had worsened to 20/200 over a period of 3 years. A detailed history was taken from all the study participants. Ophthalmic examination and slit-lamp photographs were performed in the six s with RBCD. Written informed consent was obtained from all the study participants. The study protocol conformed to the Declaration of Helsinki and was approved by the Ethics Committee of the Eye and ENT Hospital Affiliated to Fudan University, Shanghai, China. I 1 2 II III IV Normal female Normal male Female Male Dead female Dead male Female proband FIGURE 1: Pedigree of a Chinese family showing those individuals affected by Reis Bücklers corneal dystrophy. The proband was III 5 (indicated by an arrow) 1150
3 DETECTION OF TGFBI MUTATIONS Venous blood samples (3 5 ml) were taken from all the study participants using 2% ethylenediaminetetra-acetic acid as anti - coagulant and they were stored at 80 C until analysed. Peripheral leucocytes were separated from the whole blood samples by centrifugation (3000 rpm for 10 min at room temperature, repeated after 10 min) and total genomic DNA was then extracted using the Wizard Genomic DNA purification kit (Promega, Beijing, China) according to the manufacturer s instructions. Putative disease-causing mutations on exon 4 (R124H, R124S and R124L), exon 12 (R555Q and R555W) 1,14 and exon 14 (G623D and F540) 10,15 were detected using polymerase chain reaction (PCR). The affected coding regions of TGFBI were amplified using the following primers: exon 4, forward 5 -CCCAGAGGCCATCCCTCCT-3, reverse 5 -CCGGGCAGACGGAGGTCATC-3 ; exon 12, forward 5 -GTTGACAGGTGACA TTTTCT-3, reverse 5 -TCTTTACCCAAGAG TCTGCT-3 ; exon 14, forward 5 -TTGCA GTGAGTCGAGATCATG-3, reverse 5 -TCCG CAAAGAGCAATGTGT-3. The PCR was performed using 10 µl PCR reaction mix (Tiangen Biotech, Beijing, China). The conditions consisted of denaturation at 95 C for 5 min, followed by 30 cycles at 95 C for 1 min, 60 C for 1 min and 72 C for 1 min, followed by an elongation step at 72 C for 10 min. The products were then purified using a gel extraction kit (Exygen, Shanghai, China), according to the manufacturer s instructions, and they were sequenced on an ABI 3730XL automated sequencer (Applied Biosystems, Foster City, CA, USA) using the same PCR forward primers. The results were verified by comparison with those of Skonier et al. 16 EXAMINATION OF CORNEAL TISSUE Bilateral excimer phototherapeutic keratectomy was performed in the proband and her son ( IV 3 ). Corneal tissue was sampled from the proband during the procedure and then fixed with Karnovsky s fixative and washed in 0.1 M phosphate buffer ph 7.2. The tissue was postfixed in 0.5% osmium tetroxide in 0.1 M phosphate buffer for 2 h before being dehydrated through a graded ethanol series and embedded in Procure 812 resin (ProSciTech, Kirwan, Australia). The resin blocks were cut into 10 µm sections and examined using transmission electron microscopy (TEM). Results The clinical characteristics of the six living family members with RBCD are shown in Table 1. The proband s father ( II 2 ), sister ( III 2 ) and son ( IV 3 ) had a history of symptoms similar to those of the proband, whereas the proband s uncle ( II 4 ) and cousin ( III 15 ) had less severe symptoms. The mean ± SD onset ages were 7.5 ± 3.9 years for erosion and 13.8 ± 5.8 years for impairment of vision. Slit-lamp examination of all six s showed a typical geographical pattern of fine opacities in Bowman s layer of the cornea; a slit-lamp photograph of an eye from the proband is shown in Fig. 2. Genomic DNA sequences for all six s with RBCD revealed a G A missense mutation in the second nucleotide position of codon 555 at exon 12, causing an Arg Gln substitution (R555Q) (Fig. 3). The results of forward and reverse sequencing were identical. The six individuals without RBCD did not show this mutation. No other putative disease-causing mutations were seen. Examination of corneal samples from the proband using TEM revealed rod-shaped bodies lining Bowman s layer (Fig. 4); these are absent in normal cornea. 1151
4 TABLE 1: Clinical characteristics of the six living individuals from a Chinese family who were affected by Reis Bücklers corneal dystrophy Age at onset Age at onset Age Corneal of corneal erosion of visual impairment Phototherapeutic Patient (years) Sex erosion a (years) (years) Corneal opacity b keratectomy II 2 75 Male II 4 68 Male III 2 43 Female III 5 (proband) 40 Female Both eyes III Female IV 3 16 Male Both eyes a +, rarely occurs; ++, sometimes occurs (two or three times per year); +++, frequently occurs (four or more times per year). b +, opacity in centre, iris and pupil visible; ++, opacity reaching limbus, iris and pupil still visible; +++, opacity reaching limbus, iris and pupil not visible. Discussion The TGFBI gene has been implicated in the pathogenesis of most types of corneal dystrophy, including RBCD, 4 Avellino corneal dystrophy, granular corneal dystrophy, lattice corneal dystrophy and TBCD. 5 Thiel and Behnke 17 first described TBCD in 1967 as an autosomal dominant corneal dystrophy similar to RBCD that presented with recurrent erosions, moderately reduced visual acuity and honeycomb-shaped opacities in Bowman s layer. Differentiating between RBCD and TBCD can be difficult, but a report by Küchle et al. 18 proposed that they are two distinct entities that differ markedly in their slit-lamp appearance, associated degree of visual loss, histopathological findings and TEM features. In RBCD, geographical opacification is seen in Bowman s layer on slit-lamp examination, band-shaped granular, subepithelial deposits that stain intensely red with Masson trichrome are seen histopathologically, and TEM reveals rodshaped bodies. In contrast, in TBCD, honeycomb-shaped opacities are seen on slit-lamp examination, a subepithelial fibrocellular layer is interposed between the epithelium and stroma and staining with Masson s trichrome is weak histopathologically, and TEM reveals curly fibres measuring 9 15 nm in diameter. Visual loss is early and serious in RBCD, but late and moderate in TBCD. According to the different patterns of corneal opacity and pathological changes, Bowman s layer corneal dystrophy can, therefore, be divided into a geographical form (RBCD) and a honeycomb form (TBCD). 18 The TBCD phenotype is thought to be associated with the R555Q mutation and the RBCD phenotype with the R124L mutation. 11,19 The s in the family described in the 1152
5 FIGURE 2: Slit-lamp photograph of an eye from the proband illustrating corneal opacity in Reis Bücklers corneal dystrophy (original magnification 10; diffuse illumination) A B FIGURE 3: Portion of the TGFBI gene showing the second nucleotide position of codon 555 at exon 12 (arrows): (A) heterozygous G A transition (Arg555Gln) in the sense strand in an affected family member with Reis Bücklers corneal dystrophy; (B) absence of this transition in an unaffected individual from the same family 1153
6 A B 1 µm 1 µm FIGURE 4: Transmission electron microscope images of corneal tissue from the proband: (A) epithelium, showing degenerating basal epithelial cells (arrow); (B) subepithelial layer (Bowman s layer and anterior part of stromal layer), showing subepithelial rod-shaped deposits consisting of irregular aggregates of fibrils (arrow) present study demonstrated several clinical characteristics consistent with RBCD: erosion symptoms first appearing at an early age, corneal opacity in Bowman s layer with a geographical pattern, and impairment of visual acuity from a young age. Excimer laser phototherapeutic keratectomy was successfully performed on the proband with a promising early postoperative result, although repeat procedures are likely to be required. 20 TEM of a specimen taken during surgery showed rod-shaped deposits in Bowman s layer, which is consistent with a diagnosis of RBCD. This novel association of the RBCD phenotype with the R555Q genotype challenges current knowledge about phenotype specificity. 11,19 The difference in phenotype between this pedigree and those described in previous research may be due to a modifying genetic or environmental mechanism. As the RBCD phenotype is usually associated with an R124L mutation, the novel association between the R555Q mutation and the RBCD phenotype suggests striking phenotype variability with TGFBI mutations and may prompt further investigation of Bowman s layer corneal dystrophy. Acknowledgements This work was partially supported by the National Natural Science Foundation (Grant No ), the Key Project of Science and Technology Committee of Shanghai (Grant No. 11JC ), the Foundation of Health Science Research of the Health Bureau of Shanghai (Grant No ) and Shi-Bai-Qian Plans of the Jing-An District Health Bureau, Shanghai (Grant No ). Conflicts of interest The authors had no conflicts of interest to declare in relation to this article. Received for publication 27 February 2012 Accepted subject to revision 7 March 2012 Revised accepted 8 May 2012 Copyright 2012 Field House Publishing LLP References 1 Zhao XC, Nakamura H, Subramanyam S, et al: Spontaneous and inheritable R555Q mutation in the TGFBI/BIGH3 gene in two unrelated 1154
7 families exhibiting Bowman s layer corneal dystrophy. Ophthalmology 2007; 114: e39 e46. 2 Reis W: Fämiliare, fleckige Hornhautetartung. Dtsch Med Wochenschr 1917; 43: 575 [in German]. 3 Bücklers M: Ueber eine weitere familiare Hornhautdystrophie (Reis). Klin Monatsbl Augenheilkd 1949; 114: [in German]. 4 Stone EM, Mathers WD, Rosenwasser GO, et al: Three autosomal dominant corneal dystrophies map to chromosome 5q. Nat Genet 1994; 6: Munier FL, Korvatska E, Djemaï A, et al: Keratoepithelin mutations in four 5q31-linked corneal dystrophies. Nat Genet 1997; 15: Mashima Y, Nakamura Y, Noda K, et al: A novel mutation at codon 124 (R124L) in the BIGH3 gene is associated with a superficial variant of granular corneal dystrophy. Arch Ophthalmol 1999; 117: Tian X, Liu ZG, Li Q, et al: Analysis of gene mutation in Chinese s with Reis Bücklers corneal dystrophy. Zhonghua Yan Ke Za Zhi 2005; 41: [in Chinese, English abstract]. 8 Rozzo C, Fossarello M, Galleri G, et al: A common beta ig-h3 gene mutation (delta f540) in a large cohort of Sardinian Reis Bücklers corneal dystrophy s. Mutations in brief no Online. Hum Mutat 1998; 12: Munier FL, Frueh BE, Othenin-Girard P, et al: BIGH3 mutation spectrum in corneal dystrophies. Invest Ophthalmol Vis Sci 2002; 43: Afshari NA, Mullally JE, Afshari MA, et al: Survey of s with granular, lattice, Avellino, and Reis Bücklers corneal dystrophies for mutations in the BIGH3 and gelsolin genes. Arch Ophthalmol 2001; 119: Ma K, Liu G, Yang Y, et al: TGFBI gene mutation analysis in a Chinese pedigree of Reis Bücklers corneal dystrophy. Mol Vis 2010; 16: Konishi M, Yamada M, Nakamura Y, et al: Varied appearance of cornea of s with corneal dystrophy associated with R124H mutation in the BIGH3 gene. Cornea 1999; 18: Kim HS, Yoon SK, Cho BJ, et al: BIGH3 gene mutations and rapid detection in Korean s with corneal dystrophy. Cornea 2001; 20: Konishi M, Mashima Y, Yamada M, et al: The classic form of granular corneal dystrophy associated with R555W mutation in the BIGH3 gene is rare in Japanese s. Am J Ophthalmol 1998; 126: Wheeldon CE, de Karolyi BH, Patel DV, et al: A novel phenotype genotype relationship with a TGFBI exon 14 mutation in a pedigree with a unique corneal dystrophy of Bowman s layer. Mol Vis 2008; 18: Skonier J, Neubauer M, Madisen L, et al: cdna cloning and sequence analysis of beta ig-h3, a novel gene induced in a human adenocarcinoma cell line after treatment with transforming growth factor-beta. DNA Cell Biol 1992; 11: Thiel HJ, Behnke H: Ein bisher unbekannte, subepitheliale hereditäre Hornhautdystrophie. Klin Monbl Augenheilkd 1967; 150: [in German]. 18 Küchle M, Green WR, Völcker HE, et al: Reevaluation of corneal dystrophies of Bowman s layer and the anterior stroma (Reis Bücklers and Thiel Behnke types): a light and electron microscopic study of eight corneas and a review of the literature. Cornea 1995; 14: Okada M, Yamamoto S, Tsujikawa M, et al: Two distinct kerato-epithelin mutations in Reis Bücklers corneal dystrophy Am J Ophthalmol 1998; 126: Ellies P, Bejjani RA, Bourges JL, et al: Phototherapeutic keratectomy for BIGH3-linked corneal dystrophy recurring after penetrating keratoplasty. Ophthalmology 2003; 110: Author s address for correspondence Dr Ren-Yuan Chu Eye and ENT Hospital Affiliated to Fudan University, 83 FenYang Road, Shanghai, China. churenyuan@hotmail.com 1155
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