Dominant negative action of an abnormal secretin receptor arising from mRNA missplicing in a gastrinoma

Gastroenterology. 2002 Feb;122(2):500-11. doi: 10.1053/gast.2002.31039.

Abstract

Background & aims: The provocative secretin-stimulation test has an important role in the diagnosis and management of gastrin-secreting neuroendocrine tumors. The aim of the present study was to explore the molecular basis for positive and false-negative secretin-stimulation test results in patients with these tumors.

Methods: One of the rare patients with this histologically proven tumor who had a normal serum gastrin level and a negative secretin-stimulation test result, and 2 more typical patients with this syndrome were investigated using immunohistochemistry, reverse-transcription polymerase chain reaction, receptor binding, and signaling assays.

Results: We confirmed the molecular nature of the secretin receptor in the gastrinomas with a positive provocative test result and identified a novel mechanism for a false-negative result. Tumor expression of the class B G protein-coupled secretin receptor mediates a positive result. The false-negative result was explained by messenger RNA missplicing, resulting in a receptor variant missing exon 3 that encodes residues 44-79 in the amino-terminal tail of the mature receptor. This variant with an in-frame deletion was shown to be synthesized and to traffic to the cell surface normally, where it could neither bind secretin nor mediate a secretin-stimulated adenosine 3',5'-cyclic monophosphate response. It was able to act as a dominant negative inhibitor of wild-type secretin receptor function.

Conclusions: These data may explain some of the atypical presentations of this syndrome and provide important insights into basic mechanisms of disease.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adult
  • Amino Acid Sequence
  • Cloning, Molecular
  • DNA Primers
  • DNA, Complementary
  • Exons
  • Gastrinoma / genetics*
  • Gastrinoma / metabolism
  • Gene Expression / physiology
  • Humans
  • Molecular Sequence Data
  • Pancreatic Neoplasms / genetics*
  • Pancreatic Neoplasms / metabolism
  • Protein Structure, Tertiary
  • Protein Transport / physiology
  • RNA Splicing / genetics*
  • RNA, Messenger / genetics
  • Receptors, G-Protein-Coupled
  • Receptors, Gastrointestinal Hormone / chemistry
  • Receptors, Gastrointestinal Hormone / genetics*
  • Receptors, Gastrointestinal Hormone / metabolism*
  • Transfection

Substances

  • DNA Primers
  • DNA, Complementary
  • RNA, Messenger
  • Receptors, G-Protein-Coupled
  • Receptors, Gastrointestinal Hormone
  • secretin receptor