Genome-Wide Association Study Identifies 4 Novel Risk Loci for Small Intestinal Neuroendocrine Tumors Including a Missense Mutation in LGR5

Gastroenterology. 2023 Oct;165(4):861-873. doi: 10.1053/j.gastro.2023.06.031. Epub 2023 Jul 14.

Abstract

Background & aims: Small intestinal neuroendocrine tumor (SI-NET) is a rare disease, but its incidence has increased over the past 4 decades. Understanding the genetic risk factors underlying SI-NETs can help in disease prevention and may provide clinically beneficial markers for diagnosis. Here the results of the largest genome-wide association study of SI-NETs performed to date with 405 cases and 614,666 controls are reported.

Methods: Samples from 307 patients with SI-NETs and 287,137 controls in the FinnGen study were used for the identification of SI-NET risk-associated genetic variants. The results were also meta-analyzed with summary statistics from the UK Biobank (n = 98 patients with SI-NET and n = 327,529 controls).

Results: We identified 6 genome-wide significant (P < 5 × 10-8) loci associated with SI-NET risk, of which 4 (near SEMA6A, LGR5, CDKAL1, and FERMT2) are novel and 2 (near LTA4H-ELK and in KIF16B) have been reported previously. Interestingly, the top hit (rs200138614; P = 1.80 × 10-19) was a missense variant (p.Cys712Phe) in the LGR5 gene, a bona-fide marker of adult intestinal stem cells and a potentiator of canonical WNT signaling. The association was validated in an independent Finnish collection of 70 patients with SI-NETs, as well as in the UK Biobank exome sequence data (n = 92 cases and n = 392,814 controls). Overexpression of LGR5 p.Cys712Phe in intestinal organoids abolished the ability of R-Spondin1 to support organoid growth, indicating that the mutation perturbed R-Spondin-LGR5 signaling.

Conclusions: Our study is the largest genome-wide association study to date on SI-NETs and reported 4 new associated genome-wide association study loci, including a novel missense mutation (rs200138614, p.Cys712Phe) in LGR5, a canonical marker of adult intestinal stem cells.

Keywords: CDKAL1; FERMT2; FinnGen; SEMA6A; SI-NET.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Genome-Wide Association Study
  • Humans
  • Intestinal Neoplasms* / genetics
  • Intestinal Neoplasms* / pathology
  • Kinesins / genetics
  • Mutation, Missense
  • Neuroendocrine Tumors* / genetics
  • Neuroendocrine Tumors* / pathology
  • Pancreatic Neoplasms
  • Receptors, G-Protein-Coupled / genetics
  • Stomach Neoplasms

Substances

  • LGR5 protein, human
  • Receptors, G-Protein-Coupled
  • KIF16B protein, human
  • Kinesins

Supplementary concepts

  • Gastro-enteropancreatic neuroendocrine tumor