Integration of mTOR and estrogen-ERK2 signaling in lymphangioleiomyomatosis pathogenesis

Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):14960-5. doi: 10.1073/pnas.1309110110. Epub 2013 Aug 27.

Abstract

Lymphangioleiomyomatosis (LAM) is a destructive lung disease of women associated with the metastasis of tuberin-null cells with hyperactive mammalian target of rapamycin complex 1 (mTORC1) activity. Clinical trials with the mTORC1 inhibitor rapamycin have revealed partial efficacy but are not curative. Pregnancy appears to exacerbate LAM, suggesting that estrogen (E2) may play a role in the unique features of LAM. Using a LAM patient-derived cell line (bearing biallelic Tuberin inactivation), we demonstrate that E2 stimulates a robust and biphasic activation of ERK2 and transcription of the late response-gene Fra1 associated with epithelial-to-mesenchymal transition. In a carefully orchestrated collaboration, activated mTORC1/S6K1 signaling enhances the efficiency of Fra1 translation of Fra1 mRNA transcribed by the E2-ERK2 pathway, through the phosphorylation of the S6K1-dependent eukaryotic translation initiation factor 4B. Our results indicate that targeting the E2-ERK pathway in combination with the mTORC1 pathway may be an effective combination therapy for LAM.

Keywords: EMT; ERK signaling; estrogen signaling; mTORC1 signaling.

Publication types

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

MeSH terms

  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Cell Line, Tumor
  • Cell Movement
  • Epithelial-Mesenchymal Transition
  • Estradiol / metabolism*
  • Eukaryotic Initiation Factors / metabolism
  • Female
  • Gene Knockdown Techniques
  • Humans
  • Lymphangioleiomyomatosis / etiology*
  • Lymphangioleiomyomatosis / genetics
  • Lymphangioleiomyomatosis / metabolism*
  • MAP Kinase Signaling System
  • Mechanistic Target of Rapamycin Complex 1
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 1 / genetics
  • Mitogen-Activated Protein Kinase 1 / metabolism*
  • Multiprotein Complexes / antagonists & inhibitors
  • Multiprotein Complexes / metabolism
  • Neoplasm Invasiveness
  • Pregnancy
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Neoplasm / genetics
  • RNA, Neoplasm / metabolism
  • Ribosomal Protein S6 Kinases, 70-kDa / metabolism
  • Signal Transduction / drug effects
  • Sirolimus / pharmacology
  • TOR Serine-Threonine Kinases / antagonists & inhibitors
  • TOR Serine-Threonine Kinases / metabolism*

Substances

  • Arabidopsis Proteins
  • Eukaryotic Initiation Factors
  • FRA1 protein, Arabidopsis
  • Microtubule-Associated Proteins
  • Multiprotein Complexes
  • RNA, Messenger
  • RNA, Neoplasm
  • eIF-4B
  • Estradiol
  • MTOR protein, human
  • Mechanistic Target of Rapamycin Complex 1
  • Ribosomal Protein S6 Kinases, 70-kDa
  • TOR Serine-Threonine Kinases
  • ribosomal protein S6 kinase, 70kD, polypeptide 1
  • MAPK1 protein, human
  • Mitogen-Activated Protein Kinase 1
  • Sirolimus