Brief Article
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World J Gastroenterol. Dec 14, 2013; 19(46): 8659-8670
Published online Dec 14, 2013. doi: 10.3748/wjg.v19.i46.8659
Synergistic effect of interleukin-10-receptor variants in a case of early-onset ulcerative colitis
Martina Galatola, Erasmo Miele, Caterina Strisciuglio, Lorella Paparo, Daniela Rega, Paolo Delrio, Francesca Duraturo, Massimo Martinelli, Giovanni Battista Rossi, Annamaria Staiano, Paola Izzo, Marina De Rosa
Martina Galatola, Lorella Paparo, Francesca Duraturo, Paola Izzo, Marina De Rosa, Department of Molecular Medicine and Medical Biotechnology and CEINGE Biotecnologie Avanzate, University of Naples “Federico II”, 80131 Naples, Italy
Martina Galatola, Erasmo Miele, Caterina Strisciuglio, Massimo Martinelli, Annamaria Staiano, Department of Translational Medical Sciences, Section of Pediatrics, University of Naples “Federico II”, 80131 Naples, Italy
Daniela Rega, Paolo Delrio, Colorectal Surgical Oncology - Abdominal Oncology Department, Istituto Nazionale per lo studio e la cura dei tumori, “Fondazione Giovanni Pascale” IRCCS-80131 Naples, Italy
Giovanni Battista Rossi, Endoscopy Unit, Istituto Nazionale per lo studio e la cura dei tumori, “Fondazione Giovanni Pascale” IRCCS-80131 Naples, Italy
Author contributions: Izzo P and De Rosa M contributed equally to this work; Galatola M, Duraturo F and Paparo L performed the majority of the experiments; Miele E, Strisciuglio C, Martinelli M, Rega D, Delrio P and Rossi GB provided the collection of all the human material and vital reagents and were also involved in editing the manuscript; Staiano A provided the collection of all the human material and the financial support for this work; Izzo P and De Rosa M coordinated and provided the financial support for this work, designed the study and wrote the manuscript.
Supported by A grant from Ministero Salute - Ricerca Oncologica - RECAM-2006-353005; PRIN 2007-prot. 2007EN8F7T-004; Convenzione CEINGE-Regione Campania. POR Campania FSE 2007-2013, Project CREME; PRIN 2010-2011-prot. 2010K34C45_006
Correspondence to: Marina De Rosa, PhD, Department of Molecular Medicine and Medical Biotechnology and CEINGE Biotecnologie Avanzate, University of Naples “Federico II”, 80131 Naples, Italy. marina.derosa@unina.it
Telephone: +39-81-7463136 Fax: +39-81-7464359
Received: May 8, 2013
Revised: July 26, 2013
Accepted: August 17, 2013
Published online: December 14, 2013
Processing time: 224 Days and 4.8 Hours
Abstract

AIM: To investigated the molecular cause of very early-onset ulcerative colitis (UC) in an 18-mo-old affected child.

METHODS: We analysed the interleukin-10 (IL10) receptor genes at the DNA and RNA level in the proband and his relatives. Beta catenin and tumor necrosis factor-α (TNFα) receptors were analysed in the proteins extracted from peripheral blood cells of the proband, his relatives and familial adenomatous polyposis (FAP) and PTEN hamartoma tumor syndrome (PHTS) patients. Samples were also collected from the proband’s inflamed colorectal mucosa and compared to healthy and tumour mucosa collected from a FAP patient and patients affected by sporadic colorectal cancer (CRC). Finally, we examined mesalazine and azathioprine effects on primary fibroblasts stabilised from UC and FAP patients.

RESULTS: Our patient was a compound heterozygote for the IL10RB E47K polymorphism, inherited from his father, and for a novel point mutation within the IL10RA promoter (the -413G->T), inherited from his mother. Beta catenin and tumour necrosis factor α receptors-I (TNFRI) protein were both over-expressed in peripheral blood cells of the proband’s relatives more than the proband. However, TNFRII was over-expressed only in the proband. Finally, both TNFα-receptors were shown to be under-expressed in the inflamed colon mucosa and colorectal cancer tissue compared to healthy colon mucosa. Consistent with this observation, mesalazine and azathioprine induced, in primary fibroblasts, IL10RB and TNFRII over-expression and TNFRI and TNFα under-expression. We suggest that β-catenin and TNFRI protein expression in peripheral blood cells could represent molecular markers of sub-clinical disease in apparently healthy relatives of patients with early-onset UC.

CONCLUSION: A synergistic effect of several variant alleles of the IL10 receptor genes, inherited in a Mendelian manner, is involved in UC onset in this young child.

Keywords: Inflammatory bowel disease; Ulcerative colitis; Interleukin 10 receptors; Tumour necrosis factor α receptors; Beta catenin

Core tip: We identified a novel point mutation within the interleukin-10 (IL10) receptor genes promoter (the -413G->T), associated with mRNA under-expression. We propose that this mutation has a synergistic effect with other variant alleles of IL10 receptor genes in very-early ulcerative colitis (UC) onset in this young child. β-catenin and tumour necrosis factor α receptors-I (TNFRI) protein were both over-expressed in peripheral blood cells of proband relatives, whereas TNFRII was over-expressed only in the proband. We suggest that β-catenin and TNFRI protein expression could represent molecular markers of sub-clinical disease in apparently healthy relatives of patients with early-onset UC.