Prothyrotropin-releasing hormone targets its processing products to different vesicles of the secretory pathway

J Biol Chem. 2008 Jul 18;283(29):19936-47. doi: 10.1074/jbc.M800732200. Epub 2008 May 12.

Abstract

Prothyrotropin-releasing hormone (pro-TRH) is initially cleaved by the prohormone convertase-1/3 (PC1/3) in the trans-Golgi network generating N- and C-terminal intermediate forms that are then packed into secretory vesicles. However, it is not known whether these peptides are differentially sorted within the secretory pathway. This is of key importance because the processing products of several prohormones fulfill different biological functions. Using AtT20 cells stably transfected with prepro-TRH cDNA, we found that two specific N- and C-terminal peptides were located in different vesicles. Furthermore, the C-terminal pro-TRH-derived peptides were more efficiently released in response to KCl and norepinephrine, a natural secretagogue of TRH. Similar sorting and secretion of N- and C-terminal peptides occurs in vivo. When we blocked the initial proteolytic processing by a mutagenic approach, the differential sorting and secretion of these peptides were prevented. In summary, our data show that pro-TRH-derived peptides are differentially sorted within the secretory pathway and that the initial cleavage in the trans-Golgi network is key to this process. This could be a common mechanism used by neuroendocrine cells to regulate independently the secretion of different bioactive peptides derived from the same gene product.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Hypothalamus / metabolism
  • Male
  • Microscopy, Immunoelectron
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Protein Precursors / genetics
  • Protein Precursors / metabolism*
  • Pyrrolidonecarboxylic Acid / analogs & derivatives*
  • Pyrrolidonecarboxylic Acid / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Thyrotropin-Releasing Hormone / genetics
  • Thyrotropin-Releasing Hormone / metabolism*

Substances

  • Peptide Fragments
  • Protein Precursors
  • Thyrotropin-Releasing Hormone
  • pro-thyrotropin releasing hormone
  • Pyrrolidonecarboxylic Acid