A Novel Mutation of the ADAR1 Gene in a Chinese Family with Dyschromatosis Symmetrica Hereditaria and Literature Review

Hongping Ge; Na Zhang; Xinru Chen; Meiyan Wang; Tianhui Ye

doi:10.2147/CCID.S475880

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Original Research

A Novel Mutation of the ADAR1 Gene in a Chinese Family with Dyschromatosis Symmetrica Hereditaria and Literature Review

Authors Ge H , Zhang N, Chen X, Wang M, Ye T

Received 28 April 2024

Accepted for publication 23 November 2024

Published 30 November 2024 Volume 2024:17 Pages 2687—2700

DOI https://doi.org/10.2147/CCID.S475880

Checked for plagiarism Yes

Review by Single anonymous peer review

Peer reviewer comments 2

Editor who approved publication: Dr Jeffrey Weinberg

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Hongping Ge,^1,² Na Zhang,¹ Xinru Chen,^1,³ Meiyan Wang,¹ Tianhui Ye^1,³

¹Department of Dermatology, Jinhua Municipal Central Hospital (Affiliated Jinhua Hospital, Zhejiang University School of Medicine), Jinhua City, Zhejiang Province, People’s Republic of China; ²Department of Dermatology, The Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang; ³Department of Dermatology, Zhejiang Chinese Medical University, Hangzhou, Zhejiang

Correspondence: Na Zhang, Email [email protected]

Background: Dyschromatosis symmetrica hereditaria (DSH) is a rare genetic skin condition characterized by pigmented macules on the hands, feet, and sometimes the face. The ADAR1 gene is responsible for this autosomal dominant disorder.
Objective: This study aimed to analyze a three-generation Chinese family with DSH, identify a novel ADAR1 gene mutation, and conduct a comprehensive literature review of Chinese DSH families to enhance understanding of the genetic basis and clinical manifestations.
Methods: Clinical reports, mutation analysis, and literature reviews were conducted. A literature search was performed using PubMed.
Results: A novel heterozygous nonsense mutation, c.763C>T (p.Q255X), in the ADAR1 gene was identified in the proband and five other affected individuals. Literature review findings revealed prevalent mutation sites and clinical data in Chinese DSH families over the past two decades.
Limitations: The number of databases searched was limited, and the treatment outcomes for patients were not deemed satisfactory.
Conclusion: This study provides valuable insights into the genetic basis and clinical features of DSH in Chinese families, shedding light on prevalent mutation sites and clinical data. Further research is needed to explore the relationship between gene mutations and clinical phenotypes and advance therapeutic interventions for DSH.

Keywords: dyschromatosis symmetrica hereditaria, ADAR1 gene, mutation analysis

Introduction

Dyschromatosis symmetrica hereditaria (DSH: OMIM #127400, also called “reticulate acropigmentation of Dohi”), which is clinically characterized by a mixture of hyperpigmented and hypopigmented macules distributed on the dorsal aspects of their hands and feet. Some patients with DSH have freckle-like pigmented macules on the face. It is a rare autosomal dominant pigmentary genodermatosis with high penetrance. The skin lesions of this disease start in infancy or early childhood, cease spreading before adolescence, and persist throughout life. According to current literature, DSH is predominantly reported in Japan and China.¹ In 2003, Zhang et al² conducted gene detection on two Chinese DSH families and first identified the pathogenic gene for DSH located at chromosome 1q11-1q21. The gene responsible for DSH, known as the double-stranded RNA-specific adenosine deaminase (DSRAD) gene, has been located on chromosome 1q21.3 and comprises 15 exons. This gene is also referred to as the adenosine deaminase acting on RNA 1 (ADAR1) gene.³

Materials and Method

Ethical Approval

All procedures involving human participants were conducted in accordance with the ethical standards of the Ethics Committee of the Jinhua Municipal Central Hospital and the Helsinki Declaration. All patients, their normal family members, and 100 ethnically matched controls were informed about the purpose of the study and provided written consent prior to recruitment and sampling. Informed written consent for minors has been obtained from their legal guardians.

Clinical Report

In this study, we investigated a three-generation Chinese family with DSH (Figure 1a). All affected individuals had typical hyperpigmented and hypopigmented macules on the dorsal aspects of hands and feet. These skin lesions are irregular in shape and size, but they are asymptomatic. The cutaneous lesions of these patients are consistent with the typical clinical manifestations of DSH. The proband, individual III1, is a 31-year-old man. He developed an asymptomatic mixture of hyperpigmented and hypopigmented macules on dorsal aspects of his hands and feet at the age of 5. (Figure 1b and c) Besides the proband, there are five other affected individuals in the family. The other affected family members all have varying degrees of hyperpigmented and hypopigmented macules located on the dorsum of the hands and feet. Onset of symptoms occurred before the age of 6 for all affected individuals. It is worth noting that the proband in the family had the most severe skin lesions, which prompted a visit to our dermatology department for comprehensive genetic testing. Additionally, according to the patient and their family’s description, there are no other related comorbidities in the family lineage. The family history conforms to an autosomal dominant inheritance pattern of hereditary symmetric dyschromatosis.

Figure 1 (a) Pedigree of the family: arrow indicates the proband. (b and c) A mixture of hyperpigmented and hypopigmented macules on the dorsal aspect of hands and feet in the proband.

Mutation Analysis

After informed consent, genomic DNA was extracted from the peripheral blood of the proband and all family members. In addition, genomic DNA samples were extracted from 100 unrelated healthy volunteers as controls to exclude the possibility that these are polymorphisms in the ADAR1 gene. In our study, we designed primers that flanked all 15 coding exons and intron-exon boundaries of the ADAR1 gene using the Primer 3.0 program. The polymerase chain reaction was performed according to the method described in the previous literature.⁴

Results

A novel heterozygous nonsense mutation, c.763C>T (p.Q255X), located in exon 2 of the ADAR1 gene, was identified in the proband through direct sequence analysis of the PCR products. The same mutation was also detected in five other affected individuals in the family. This mutation was not found in other healthy family members or in 100 unrelated controls, indicating that c.763C>T is not a common polymorphism. A mutation occurs at the 763rd nucleotide in the DNA sequence of the ADAR1 gene, changing it from C to T. This resulted in the amino acid at position 255 in the protein sequence being altered from glutamine (Q) to a premature stop codon (X), causing premature termination of protein synthesis and the production of a truncated protein. (Figure 2).

Figure 2 (a) A novel heterozygous nonsense mutation, c.763C>T (p.Q255X) mutation in exon 2 of the ADAR1 gene in proband. The red arrow indicates the mutation site. (b) The sequence of the exon 2 of the ADAR1 gene in normal individuals.

Literature Review

All the articles published in PubMed since 2003 were searched using the keywords of “dyschromatosis symmetrica hereditarian”, “adenosine deaminase acting on RNA 1 gene”, “ADAR1 gene”, “double-stranded RNA-specific adenosine deaminase gene” and “DSRAD gene”. Inclusion criteria: (1) diagnosed with DSH; (2) Chinese DSH pedigree; (3) Clinical manifestations, pedigree information and genetic testing are complete. (4) The full text is available. Exclusion criteria: (1) other ADAR gene-related diseases; (2) Non-Chinese pedigree; (3) incomplete clinical data; (4) outside the set time. Finally, 61 articles on Chinese DSH families were obtained through the above search criteria, involving 180 patients (Table 1). Ever since the identification of the pathogenic gene for DSH on chromosome 1q11-1q21 by Zhang et al in 2003, research on the detection of the ADAR gene has garnered significant attention. In this study, we conducted a review of genetic testing and clinical data pertaining to Chinese DSH families documented in the PubMed database over the past two decades. Remarkably, 86.1% of the patients exhibited a family history. Despite DSH being inherited as an autosomal dominant disorder, our cohort of 180 patients included 25 sporadic cases. According to the literature, almost all patients exhibited typical cutaneous manifestations on the dorsum of the hands and feet, which are crucial for clinical diagnosis. The face was identified as the second most common site, with some patients also presenting the macules on other areas such as the knees and elbows. Mutation analysis revealed that 36.1% (65/180) of the patients carried missense mutations, while frameshift mutations accounted for one-third of the cases (60/180) of the cases. Nonsense mutations were identified in 36 patients, and a small number of splice site mutations were also observed. Upon analyzing of the chromosomal locations where mutations occurred, we found 39 mutation sites located on chromosome 2, which may be considered as prominent mutation sites among Chinese families. (Figure 3) This paper presents a compilation of Chinese DSH families over the past 20 years, along with a summary of prevalent mutation sites and clinical manifestations, aiming to facilitate future investigations into the relationship between gene mutations and clinical phenotypes.

Table 1 ADAR1 Mutation Spectrum in Chinese Patients with DSH

Figure 3 The relation of mutation position and mutation type.

Discussion

ADAR1 protein as an A-to-I editase, catalyzes the deamination of adenosine to inosine in double-stranded RNA substrates.⁶⁵ ADAR1 has two different isoforms: ADAR1p110 and ADAR1p150. The p150 isoform has two series of Z-DNA-binding domains (Z-α and Z-β) located in exon 2, three dsRNA-binding domains (DSRM) located in exons 2–7 and a deaminase domain (ADEAMc) located in exons 9–14. In contrast, The P110 isoform has only one Z-DNA binding domain(Z-β) located in exon 2.^15,66 To date, there is no etiologic treatment for DSH. Sun exposure exacerbates hyperpigmentation and hypopigmented macules in individuals with DSH, particularly in exposed areas such as the dorsal aspects of the hands. This can lead to significant psychosocial stress, especially among young patients. Consequently, proactive sun protection measures are effective and recommended for all individuals affected by this condition.⁶⁷ Kawakami et al⁶⁸ achieved successful treatment of a male patient in Japan through the use of 1-mm miniature punch grafting in combination with 308-nm excimer light. Many patients, including the subject of this study, expressed a strong desire for treatment. To address the skin hyperpigmentation of the patients, fractional CO2 laser, 532-nm Q-switched Nd: YAG Laser, and 694nm Q-switched ruby laser were successively employed. Meanwhile, at the site of pigmentation reduction, the 308-nm excimer laser was utilized to help restore pigment deposition. Initial observations indicated a resolution of the pigment differences within weeks following the conclusion of the treatment. However, despite multiple attempts over several months, the lesions eventually reverted to their pre-treatment state, yielding unsatisfactory results. In conclusion, this study unveiled a novel heterozygous nonsense mutation, c.763C>T (p.Q255X), within the ADAR1 gene in a multi-generational Chinese family affected by dyschromatosis symmetrica hereditaria (DSH). Simultaneously, pigment augmentation treatment was administered to the hypopigmented areas of the patient, and pigment reduction treatment was applied to the hyperpigmented areas. However, no significant improvement was observed in either case. Through an extensive review of Chinese DSH families spanning the last two decades, the study illuminated prevalent mutation sites and clinical manifestations, significantly augmenting our comprehension of the genetic underpinnings and clinical characteristics of DSH within Chinese communities. Moving forward, these insights are poised to inform future investigations into the interplay between gene mutations and clinical phenotypes in DSH, potentially paving the way for advancements in therapeutic interventions and management strategies for this condition.

Funding

This work was supported by the Jinhua Science and Technology Projects (grant number is 2021-4-019).

Disclosure

Authors declare no conflict of interests for this article.

References

1. Okamura K, Abe Y, Fukai K, et al. Mutation analyses of patients with dyschromatosis symmetrica hereditaria: ten novel mutations of the ADAR1 gene[J]. J Dermatological Sci. 2015;79(1):88–90. doi:10.1016/j.jdermsci.2015.04.004

2. J ZX, Gao M, Li M, et al. Identification of a locus for dyschromatosis symmetrica hereditaria at chromosome 1q11-1q21[J]. J Inve Derma. 2003;120(5):776–780. doi:10.1046/j.1523-1747.2003.12130.x

3. Miyamura Y, Suzuki T, Kono M, et al. Mutations of the RNA-specific adenosine deaminase gene (DSRAD) are involved in dyschromatosis symmetrica hereditaria[J]. Am J Hum Genet. 2003;73(3):693–699. doi:10.1086/378209

4. Ning X, Xiao S, Zhang Y. Identification of Two Novel Frameshift Mutations of the ADAR1 Gene in Two Chinese Families With Dyschromatosis Symmetrica Hereditaria[J]. Indian J Dermat. 2022;67(4):355–358. doi:10.4103/ijd.ijd_207_21

5. Liu X, Lei M, Xue Y, et al. Multi-dimensional Insight into the Coexistence of Pathogenic Genes for ADAR1 and TSC2: careful Consideration is Essential for Interpretation of ADAR1 Variants[J]. Biochem Genet 2023.

6. Ma Q, Che L, Chen Y, et al. Identification of five novel variants of ADAR1 in dyschromatosis symmetrica hereditaria by next-generation sequencing[J]. Front Pediatr. 2023;11:1161502. doi:10.3389/fped.2023.1161502

7. Liu L, Zhang L, Huang P, et al. Case Report: aicardi-Goutières Syndrome Type 6 and Dyschromatosis Symmetrica Hereditaria With Congenital Heart Disease and Mitral Valve Calcification - Phenotypic Variants Caused by Adenosine Deaminase Acting on the RNA 1 Gene Homozygous Mutations[J]. Front Pediatr. 2022;10:852903. doi:10.3389/fped.2022.852903

8. Y WH, W WR, T CY, et al. Novel ADAR1 mutations in three cases of psoriasis coexisting with dyschromatosis symmetrica hereditaria[J]. J Eur Acad Dermatol Venereol JEADV. 2022;36(1):e54–e57. doi:10.1111/jdv.17620

9. Liu W, X WX, W LJ, et al. Mutation analyses of patients with dyschromatosis symmetrica hereditaria: five novel mutations of the ADAR1 gene[J]. Clin Exp Dermatol. 2021;46(2):347–348. doi:10.1111/ced.14355

10. Wang P, Yu S, Liu J, et al. Seven novel mutations of ADAR in multi-ethnic pedigrees with dyschromatosis symmetrica hereditaria in ChinaChina. Molecular Gene Genomic Medi. 2019;7(10):e00905. doi:10.1002/mgg3.905

11. Hu W, Shi X, Li H, et al. Four novel mutations of ADAR1 in Chinese patients with dyschromatosis symmetrica hereditaria[J]. Indian J Dermatol Venereol Leprol. 2019;85(1):69–73. doi:10.4103/ijdvl.IJDVL_66_17

12. M LS, X NM, C ZM, et al. A novel missense mutation of ADAR1 gene in a Chinese family leading to dyschromatosis symmetrica hereditaria and literature review[J]. J Genetics. 2017;96(6):1021–1026. doi:10.1007/s12041-017-0873-9

13. L TZ, Wang S, Tu C, et al. Eight Novel Mutations of the ADAR1 Gene in Chinese Patients with Dyschromatosis Symmetrica Hereditaria[J]. Genetic Test Molecu Biomark. 2018;22(2):104–108. doi:10.1089/gtmb.2017.0207

14. Chi C, Luo Y, Liu J. A novel frameshift mutation of the ADAR1 gene in a Chinese patient with dyschromatosis symmetrica hereditaria and the dermoscopic features[J]. J Eur Acad Dermatol Venereol JEADV. 2017;31(11):e484–e485. doi:10.1111/jdv.14332

15. D ZS, J FS, Nh-Tseung K, et al. Pathogenicity of ADAR1 mutation in a Chinese family with dyschromatosis symmetrica hereditaria[J]. J Eur Acad Dermatol Venereol JEADV. 2017;31(11):e483–e484. doi:10.1111/jdv.14331

16. Zhou Q, Zhang L, Zhang Y, et al. Two novel ADAR1 gene mutations in two patients with dyschromatosis symmetrical hereditaria from birth[J]. Mole Med Repo. 2017;15(6):3715–3718. doi:10.3892/mmr.2017.6427

17. R LC, Li H, X YR, et al. Novel de novo heterozygous frameshift mutation of the ADAR1 gene in heavy dyschromatosis symmetrica hereditaria[J]. Cutis. 2016;98(3):E16–E18.

18. Zhang G, Shao M, Li Z, et al. Genetic spectrum of dyschromatosis symmetrica hereditaria in Chinese patients including a novel nonstop mutation in ADAR1 gene[J]. BMC Med Genet. 2016;17:14. doi:10.1186/s12881-015-0255-1

19. W LJ, Asan SJ, Sun J, et al. Differential Diagnosis of Two Chinese Families with Dyschromatoses by Targeted Gene Sequencing[J]. Chinese Med J. 2016;129(1):33–38. doi:10.4103/0366-6999.172564

20. L LZ, Y ZG, Hui Y, et al. A novel missense mutation in ADAR1 gene causing dyschromatosis symmetrica hereditaria in a Chinese patient[J]. Indian J Dermatol Venereol Leprol. 2015;81(3):327. doi:10.4103/0378-6323.155560

21. G XX, Lv Y, L ZJ, et al. Two novel mutations of the ADAR1 gene in Chinese patients with dyschromatosis symmetrica hereditaria successfully treated with fractional CO 2 laser. J Eur Acad Dermatol Venereol JEADV. 2016;30(6):1035–1038. doi:10.1111/jdv.13090

22. W LW, Y WQ, Li N, et al. A novel deletion mutation of the ADAR1 gene in a Chinese patient with dyschromatosis symmetrica hereditaria[J]. Journal of Genetics. 2014;93(2):523–525. doi:10.1007/s12041-014-0392-x

23. Liu Q, Wang Z, Wu Y, et al. Five novel mutations in the ADAR1 gene associated with dyschromatosis symmetrica hereditaria[J]. BMC Med Genet. 2014;15:69. doi:10.1186/1471-2350-15-69

24. Y WQ, W LW, Li N, et al. A novel nonsense mutation of ADAR1 gene in a Chinese patient with dyschromatosis symmetrica hereditaria[J]. J Eur Acad Dermatol Venereol JEADV. 2014;28(12):1832–1833. doi:10.1111/jdv.12381

25. Zhang S, Jiang M, Zhao J. Two novel mutations in the DSRAD gene in two Chinese pedigrees with dyschromatosis symmetrica hereditaria[J]. Eur J Dermatol. 2013;23(6):782–785. doi:10.1684/ejd.2013.2236

26. Huang Y, Zhao X, Mei Q, et al. Mutation analysis of the ADAR1 gene in a Chinese Family with dyschromatosis symmetrica hereditaria[J]. The Austran J Derm. 2014;55(1):92–93. doi:10.1111/ajd.12132

27. Y ZC, J ZK, Zhou Y, et al. A novel insertion mutation in the ADAR1 gene of a Chinese family with dyschromatosis symmetrica hereditaria[J]. Genet mol re. 2013;12(3):2858–2862. doi:10.4238/2013.August.12.1

28. Y ZJ, D CX, Zhang Z, et al. The adenosine deaminase acting on RNA 1 p150 isoform is involved in the pathogenesis of dyschromatosis symmetrica hereditaria[J]. British J Derma. 2013;169(3):637–644. doi:10.1111/bjd.12401

29. L ZG, J SH, H SM, et al. Mutations in the ADAR1 gene in Chinese families with dyschromatosis symmetrica hereditaria[J]. Genet mol res. 2013;12(3):2794–2799. doi:10.4238/2013.January.4.18

30. Yuan C, Liu H, Fu X, et al. Two novel mutations of the ADAR1 gene in Chinese patients with dyschromatosis symmetrica hereditaria[J]. Indian J Dermatol Venereol Leprol. 2012;78(6):746–748. doi:10.4103/0378-6323.102375

31. L LM, J YL, H ZX, et al. A novel mutation of the DSRAD gene in a Chinese family with dyschromatosis symmetrica hereditaria[J]. Genet mol res. 2012;11(2):1731–1737. doi:10.4238/2012.June.29.5

32. Luo S, Zheng Y, Ni H, et al. Novel clinical and molecular findings in Chinese families with dyschromatosis symmetrica hereditaria[J]. J Dermatol. 2012;39(6):556–558. doi:10.1111/j.1346-8138.2011.01431.x

33. Liu Y, Liu F, Wang X, et al. Two novel frameshift mutations of the DSRAD gene in Chinese pedigrees with dyschromatosis symmetrica hereditaria[J]. Int J Dermatol. 2012;51(8):920–922. doi:10.1111/j.1365-4632.2011.05209.x

34. Liu H, A FX, X YY, et al. Identification of two novel splice mutations of the ADAR1 gene in two Chinese families with dyschromatosis symmetrica hereditaria[J]. Clin Exp Dermatol. 2011;36(7):797–799. doi:10.1111/j.1365-2230.2011.04058.x

35. J SB, Xue M, Liu Y, et al. First report of the coexistence of dyschromatosis symmetrica hereditaria and psoriasis: one novel TCT to A mutation in the double-RNA-specific adenosine deaminase gene[J]. J Eur Acad Dermatol Venereol JEADV. 2012;26(5):657–658. doi:10.1111/j.1468-3083.2011.04096.x

36. P WX, Liu Y, M WJ, et al. Two novel splice site mutations of the ADAR1 gene in Chinese families with dyschromatosis symmetrica hereditaria. J Dermatol. 2010;37(12):1051–1052. doi:10.1111/j.1346-8138.2010.00928.x

37. Pan H, Wang Z, He B, et al. Identification of a novel mutation in the DSRAD gene in a Chinese family with dyschromatosis symmetrica hereditaria[J]. J Am Acad Dermatol. 2010;63(3):529–530. doi:10.1016/j.jaad.2009.08.065

38. Li M, Jin C, Yang L, et al. A novel complex insertion–deletion mutation in ADAR1 gene in a Chinese family with dyschromatosis symmetrica hereditaria. J Eur Acad Dermatol Venereol JEADV. 2011;25(6):743–746. doi:10.1111/j.1468-3083.2010.03773.x

39. peng WX, Juan WW, min WJ, et al. Four novel and two recurrent mutations of the ADAR1 gene in Chinese patients with dyschromatosis symmetrica hereditaria[J]. J Dermatological Sci. 2010;58(3):217–218. doi:10.1016/j.jdermsci.2010.03.021

40. Dong Y, Xiao S, Ren J, et al. Double-stranded RNA-specific adenosine deaminase (DSRAD) gene mutation in a Chinese family with dyschromatosis symmetrica hereditaria (DSH)[J]. Int J Dermatol. 2011;50(3):375–378. doi:10.1111/j.1365-4632.2009.04346.x

41. R LC, L XX, J SX, et al. Two new mutations of the ADAR1 gene associated with dyschromatosis symmetrica hereditaria[J]. Arch Dermatological Res. 2010;302(6):477–480. doi:10.1007/s00403-010-1037-4

42. Li M, Yang L, Li C, et al. Mutational spectrum of the ADAR1 gene in dyschromatosis symmetrica hereditaria[J]. Arch Dermatological Res. 2010;302(6):469–476. doi:10.1007/s00403-010-1039-2

43. Xu Q, Xiao S, Huo J, et al. Identification of two novel DSRAD mutations in two Chinese families with dyschromatosis symmetrica hereditaria[J]. Arch Dermatological Res. 2010;302(3):235–236. doi:10.1007/s00403-009-1027-6

44. Dong Y, Xiao S, Ren J, et al. A novel missense mutation of the DSRAD gene in a Chinese family with dyschromatosis symmetrica hereditaria[J]. Eur J Dermatol. 2009;19(3):270–272. doi:10.1684/ejd.2009.0639

45. Li M, Yang LJ, Zhu XH. Identification of a novel DSRAD gene mutation in a Chinese family with dyschromatosis symmetrica hereditaria[J]. Clin Exp Dermatol. 2008;33(5):644–646. doi:10.1111/j.1365-2230.2008.02887.x

46. W RJ, J LS, H PZ, et al. Novel frameshift mutation of the DSRAD gene in a Chinese family with dyschromatosis symmetrica hereditaria. J Eur Acad Dermatol Venereol JEADV. 2008;22(11):1375–1376. doi:10.1111/j.1468-3083.2008.02632.x

47. Zhang F, Liu H, Jiang D, et al. Six novel mutations of the ADAR1 gene in Chinese patients with dyschromatosis symmetrica hereditaria[J]. J Dermatological Sci. 2008;50(2):109–114. doi:10.1016/j.jdermsci.2007.11.011

48. Li M, J YL, X SY, et al. A novel missense mutation in DSRAD in a family with dyschromatosis symmetrica hereditaria[J]. Arch Dermatological Res. 2007;299(5–6):273–275. doi:10.1007/s00403-007-0762-9

49. Xing Q, Shu A, Yu L, et al. Novel deletion mutation of DSRAD in a Chinese family with Dyschromatosis Symmetrica Hereditaria (DSH)[J]. European j Dermat. 2007;17(3):247–248. doi:10.1684/ejd.2007.0161

50. Hou Y, Chen J, Gao M, et al. Five novel mutations of RNA-specific adenosine deaminase gene with dyschromatosis symmetrica hereditaria[J]. Acta Dermato-Venereologica. 2007;87(1):18–21. doi:10.2340/00015555-0168

51. Liu Y, Xiao S, Peng Z, et al. A new mutation of the double-stranded RNA-specific adenosine deaminase gene in a family with dyschromatosis symmetrica hereditaria[J]. Dermatology. 2006;213(3):200–203. doi:10.1159/000095036

52. Lu J, Liao Z, Chen J, et al. Identification of two novel DSRAD mutations in two Chinese families with dyschromatosis symmetrica hereditaria[J]. Arch Dermatological Res. 2006;298(7):357–360. doi:10.1007/s00403-006-0701-1

53. Liu Y, X XS, H PZ, et al. Two frameshift mutations of the double-stranded RNA-specific adenosine deaminase gene in Chinese pedigrees with dyschromatosis symmetrica hereditaria[J]. British J Derma. 2006;155(2):473–476. doi:10.1111/j.1365-2133.2006.07223.x

54. Liu Q, Jiang L, Liu WL, et al. Two novel mutations and evidence for haploinsufficiency of the ADAR gene in dyschromatosis symmetrica hereditaria[J]. British J Derma. 2006;154(4):636–642. doi:10.1111/j.1365-2133.2006.07133.x

55. C CS, Y LJY, M SH, et al. A novel deletion mutation of the DSRAD gene in a Taiwanese patient with dyschromatosis symmetrica hereditaria[J]. British J Derma. 2005;153(5):1064–1066. doi:10.1111/j.1365-2133.2005.06874.x

56. Li M, Li C, Hua H, et al. Identification of two novel mutations in Chinese patients with Dyschromatosis symmetrica hereditaria[J]. Arch Dermatological Res. 2005;297(5):196–200. doi:10.1007/s00403-005-0595-3

57. Xing Q, Wang M, Chen X, et al. Identification of a novel ADAR mutation in a Chinese family with dyschromatosis symmetrica hereditaria (DSH)[J]. Arch Dermatological Res. 2005;297(3):139–142. doi:10.1007/s00403-005-0589-1

58. K SX, E XA, F CJ, et al. The double-RNA-specific adenosine deaminase (DSRAD) gene in dyschromatosis symmetrica hereditaria patients: two novel mutations and one previously described[J]. British J Derma. 2005;153(2):342–345. doi:10.1111/j.1365-2133.2005.06572.x

59. Cui Y, Wang J, Yang S, et al. Identification of a novel mutation in the DSRAD gene in a Chinese pedigree with dyschromatosis symmetrica hereditaria[J]. Arch Dermatological Res. 2005;296(11):543–545. doi:10.1007/s00403-005-0546-z

60. Gao M, G WP, Yang S, et al. Two frameshift mutations in the RNA-specific adenosine deaminase gene associated with dyschromatosis symmetrica hereditaria[J]. Arch Dermatol. 2005;141(2):193–196. doi:10.1001/archderm.141.2.193

61. R LC, Li M, J MH, et al. A new arginine substitution mutation of DSRAD gene in a Chinese family with dyschromatosis symmetrica hereditaria[J]. J Dermatological Sci. 2005;37(2):95–99. doi:10.1016/j.jdermsci.2004.11.004

62. Li M, X JY, B LJ, et al. A novel mutation of the DSRAD gene in a Chinese family with dyschromatosis symmetrica hereditaria[J]. Clin Exp Dermatol. 2004;29(5):533–535. doi:10.1111/j.1365-2230.2004.01548.x

63. J ZX, P HP, Li M, et al. Seven novel mutations of the ADAR gene in Chinese families and sporadic patients with dyschromatosis symmetrica hereditaria (DSH)[J]. Human Mutation. 2004;23(6):629–630. doi:10.1002/humu.9246

64. Liu Q, Liu W, Jiang L, et al. Novel mutations of the RNA-specific adenosine deaminase gene (DSRAD) in Chinese families with dyschromatosis symmetrica hereditaria[J]. J Inve Derma. 2004;122(4):896–899. doi:10.1111/j.0022-202X.2004.22429.x

65. Suzuki N, Suzuki T, Inagaki K, et al. Ten Novel Mutations of the ADAR1 Gene in Japanese Patients with Dyschromatosis Symmetrica Hereditaria[J]. J Invest Dermatol. 2007;127(2):309–311. doi:10.1038/sj.jid.5700528

66. Hayashi M, Suzuki T. Dyschromatosis symmetrica hereditaria[J]. J Dermatol. 2013;40(5):336–343. doi:10.1111/j.1346-8138.2012.01661.x

67. Kono M, Okamoto T, Takeichi T, et al. Dyschromatosis symmetrica hereditaria may be successfully controlled by topical sunscreen[J]. Eur J Dermatol. 2018;28(6):840–841. doi:10.1684/ejd.2018.3415

68. Kawakami T, Otaguchi R, Kyoya M, et al. Patient with dyschromatosis symmetrica hereditaria treated with miniature punch grafting, followed by excimer light therapy[J]. J Dermatol. 2013;40(9):771–772. doi:10.1111/1346-8138.12205

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