Elsevier

Gene

Volume 571, Issue 1, 15 October 2015, Pages 43-51
Gene

Research paper
Novel genes and variants associated with IgA nephropathy by co-segregating with the disease phenotypes in 10 IgAN families

https://doi.org/10.1016/j.gene.2015.06.041Get rights and content

Highlights

  • We discovered 3 variants in 3 novel genes associated with familial IgAN and three novel vaiations in a reported gene.

  • Exome sequencing and bioinformatics were used to explore variation.

  • Sanger sequencing, co-segregation, and haplotype analysis were employed to confirm results.

Abstract

Background

Previously, a large proportion of the genetic components predisposing individuals to IgA nephropathy (IgAN) have been unidentified. Familial IgAN is enriched with genetic variations predisposing individuals to the disease. Whole exome sequencing is an effective way to explore disease-causing genes and gene variants.

Methods

We performed exome sequencing on the probands from each of ten IgAN families, and on one of the unaffected member from 7 of the families. Sanger sequencing, bioinformatics and co-segregation analysis were performed for all available family members to detect deleterious genetic variation. The relatedness of the families was tested by haplotype analyses.

Results

Six deleterious variants in 4 genes were observed to be associated with IgA nephropathy by co-segregating with the disease phenotypes in study families. MYCT1 p.Asp22Glufs*34 was associated with IgAN by co-segregating with its phenotypes in families 2, 7, and 9; DEFA4 p.Ala8Pro, p.Ala8Val, c.172 + 1G>T co-segregated in families 1, 2, and 3; ZNF543 p.Pro226Ala co-segregated in families 3, 5, and 6 and CARD8 p.Val98Lysfs*26 co-segregated in families 7 and 8. Among these genes, MYCT1, CARD8 and ZNF543 are novel. Our haplotype analyses showed that families in which the same variation(s) were co-segregating with IgAN were unrelated, except for DEFA4. Of the families carrying DEFA4, families 2 and 3 were possibly related, but not family 1, indicating that common genes/variations in these families were not due to the same founder. Interfamilial sharing of different co-segregating genes was also observed, demonstrating the polygenic nature of this disease.

Conclusions

We discovered 6 deleterious variants in 4 genes associated with familial IgAN. These genes are good candidate genes that appear to be causally related to IgAN and warrant further study.

Introduction

IgA nephropathy (IgAN) is the most prevalent primary glomerulonephritis worldwide. Approximately 20% to 30% of individuals with IgAN develop end-stage renal disease (ESRD) within 10 to 20 years following initial diagnosis (Bisceglia et al., 2006, Le et al., 2012, Wyatt and Julian, 2013). Despite varying clinical presentations, IgAN is diagnosed by immunohistochemical analysis on renal biopsies and is characterized by predominant mesangial IgA deposition. The etiology of IgAN remains unclear. Genetic contribution to the etiology is implicated by the presence of large extended IgAN families and familial aggregation of IgAN. Evidence for a genetic component is further revealed by genome-wide association studies and candidate association studies (Klein et al., 2005, Feehally et al., 2010, Kiryluk et al., 2010, Kiryluk et al., 2014, Gharavi et al., 2011, Yu et al., 2012, Xie et al., 2013). Intriguingly, the prevalence of IgAN varies greatly among different ethnicities, being higher in Asians (especially among Chinese and Japanese) but lower in Africans (Hall et al., 2004, Kiryluk et al., 2010, Kiryluk et al., 2012).

IgAN families are enriched in genetic components predisposing individuals to IgAN. Next-generation sequencing has been proven to be an effective way to interrogate the whole exome or the whole genome to identify genes and gene variants that underlie both monogenic and complex diseases. We performed exome sequencing on individuals from 10 families with IgAN (9 families were unrelated) and identified 6 variations in 4 genes that co-segregated with the IgAN disease phenotype. These variants are good candidates for the genes causing IgAN.

Section snippets

Study subjects

Ten families with at least two members that had IgAN as demonstrated by a biopsy, were recruited from the Queen Mary Hospital, University of Hong Kong (Fig. 1). A total of 20 IgAN subjects were included in this cohort. Detailed clinical and laboratory investigations were performed on each of the family members available for the study. IgAN was diagnosed following the WHO criteria on renal biopsy, with the exclusion of systemic lupus erythematosis, Henoch–Schonlein purpura and hepatic diseases

Ten IgAN families were recruited

Ten families comprising 20 patients with IgAN and a total of 34 unaffected family members were included in this study. Each family had two patients with IgAN confirmed by biopsy following the WHO standards (Maisonneuve et al., 2000, Li et al., 2004, Wyatt and Julian, 2013). Eighteen IgAN patients and 11 unaffected family members were available for the study (Fig. 1). Clinical data for the IgAN patients are shown in Supplementary Table 2. We followed up with the unaffected family members for a

Discussion

We examined 7 genetic variants of 5 genes in ten IgAN families using exome sequencing, bioinformatics tools, genotype–phenotype co-segregation analysis and haplotype construction. We reported 6 deleterious variants in 4 genes, which co-segregated with the IgAN disease phenotype in the study families. The MYCT1, CARD8 and ZNF543 genes were novel. We also confirmed an association between one of the DEFA cluster genes, DEFA4, with IgAN (Yu et al., 2012, Kiryluk et al., 2014, Xu et al., 2014) and

Conflict of interest statement

None to declare.

Acknowledgments

The project is supported by the National Natural Science Foundation of China (31271342, 31471193), China Medical Board in New York (050827), the Doctoral Program of the Ministry of Education (20110171110047), Basic Research Funds of the Key Universities (10ykjc07), and Doctoral grant of the Ministry of Education (50000-3191016).

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    These authors contributed equally to this work.

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