Thyrocyte-specific deletion of insulin and IGF-1 receptors induces papillary thyroid carcinoma-like lesions through EGFR pathway activation

Int J Cancer. 2018 Nov 15;143(10):2458-2469. doi: 10.1002/ijc.31779. Epub 2018 Sep 22.

Abstract

Insulin and insulin-like growth factor (IGF)-1 signaling in the thyroid are thought to be permissive for the coordinated regulation by thyroid-stimulating hormone (TSH) of thyrocyte proliferation and hormone production. However, the integrated role of insulin receptor (IR) and IGF-1 receptor (IGF-1R) in thyroid development and function has not been explored. Here, we generated thyrocyte-specific IR and IGF-1R double knockout (DTIRKO) mice to precisely evaluate the coordinated functions of these receptors in the thyroid of neonates and adults. Neonatal DTIRKO mice displayed smaller thyroids, paralleling defective folliculogenesis associated with repression of the thyroid-specific transcription factor Foxe1. By contrast, at postnatal day 14, absence of IR and IGF-1R paradoxically induced thyrocyte proliferation, which was mediated by mTOR-dependent signaling pathways. Furthermore, we found elevated production of TSH during the development of follicular hyperplasia at 8 weeks of age. By 50 weeks, all DTIRKO mice developed papillary thyroid carcinoma (PTC)-like lesions that correlated with induction of the ErbB pathway. Taken together, these data define a critical role for IR and IGF-1R in neonatal thyroid folliculogenesis. They also reveal an important reciprocal relationship between IR/IGF-1R and TSH/ErbB signaling in the pathogenesis of thyroid follicular hyperplasia and, possibly, of papillary carcinoma.

Keywords: IGF-1 receptor; folliculogenesis; hyperplasia; insulin receptor; thyroid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • ErbB Receptors / metabolism*
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Receptor, IGF Type 1 / deficiency*
  • Receptor, IGF Type 1 / genetics
  • Receptor, IGF Type 1 / metabolism
  • Receptor, Insulin / deficiency*
  • Receptor, Insulin / genetics
  • Receptor, Insulin / metabolism
  • Signal Transduction
  • Thyroid Cancer, Papillary / metabolism*
  • Thyroid Cancer, Papillary / pathology
  • Thyroid Epithelial Cells / metabolism*
  • Thyroid Epithelial Cells / pathology
  • Thyroid Neoplasms / metabolism*
  • Thyroid Neoplasms / pathology
  • Thyrotropin / biosynthesis
  • Thyrotropin / metabolism

Substances

  • Thyrotropin
  • ErbB Receptors
  • Receptor, IGF Type 1
  • Receptor, Insulin