Identification of a new exon 2-skipped TNFR1 transcript: regulation by three functional polymorphisms of the TNFR-associated periodic syndrome (TRAPS) gene

Ann Rheum Dis. 2014 Jan;73(1):290-7. doi: 10.1136/annrheumdis-2012-203023. Epub 2013 Mar 16.

Abstract

Background: Mutations in the TNFRSF1A gene encoding the tumour necrosis factor α cell surface receptor, TNFR1, cause TNFR-associated periodic syndrome (TRAPS) and polymorphisms in TNFRSF1A, including rs4149570, rs767455 and rs1800692, are associated with inflammatory diseases.

Objectives: To describe a new exon 2-spliced transcript-TNFR1-d2-and the impact of these three single nucleotide polymorphisms on exon 2 splicing, transcriptional activity of TNFRSF1A and TRAPS phenotype.

Methods: Expression of TNFRSF1A transcripts was performed by reverse-transcription-PCR in a range of human cells and tissues. Exon 2 splicing and transcriptional activity were analysed in HEK293T and SW480 cells by in vitro alternative splicing and luciferase assays, respectively. We constructed haplotypes containing rs4149570, rs767455 and rs1800692 in controls (n=72), patients with TRAPS (n=111) and in TRAPS-like patients (n=450) to compare their distribution and association with clinical features of TRAPS.

Results: TNFR1-d2 was expressed in a tissue-specific manner, whereas TNFR1 expression was ubiquitous. Alternative splicing assays showed that the T-A-T haplotype at rs4149570-rs767455-rs1800692 had a significantly higher expression of exon 2-skipping product (p=0.02) compared with the G-G-C haplotype. Transcriptional activity from the T-T haplotype at rs4149570-rs1800692 was increased compared with the G-C haplotype (p=0.03). In patients with TRAPS, rs1800692 T/T homozygotes were excessively rare (p<10(-4)) and TRAPS-like patients with this genotype experienced less fever.

Conclusions: Our study provides a new mechanism of TNFRSF1A regulation whereby three polymorphisms in the promoter, exon 1 and intron 4 have a functional and combined effect on exon 2 splicing, via a coupling mechanism between transcription and splicing. These polymorphisms may affect the phenotype of TRAPS and TRAPS-like patients.

Keywords: TNFR1 transcript; TRAPS; alternative splicing; autoinflammatory disease; recurrent fever.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma
  • Alternative Splicing / genetics
  • Colonic Neoplasms
  • Exons / genetics
  • Fever
  • Gene Expression Regulation / genetics*
  • Genetic Complementation Test
  • HEK293 Cells
  • Haplotypes
  • Hereditary Autoinflammatory Diseases / genetics*
  • Humans
  • Introns / genetics
  • Phenotype
  • Polymorphism, Genetic*
  • Promoter Regions, Genetic / genetics
  • Receptors, Tumor Necrosis Factor, Type I / genetics*

Substances

  • Receptors, Tumor Necrosis Factor, Type I

Supplementary concepts

  • Periodic fever, familial, autosomal dominant