Caveolin-1-deficient mice show accelerated mammary gland development during pregnancy, premature lactation, and hyperactivation of the Jak-2/STAT5a signaling cascade

Mol Biol Cell. 2002 Oct;13(10):3416-30. doi: 10.1091/mbc.02-05-0071.

Abstract

It is well established that mammary gland development and lactation are tightly controlled by prolactin signaling. Binding of prolactin to its cognate receptor (Prl-R) leads to activation of the Jak-2 tyrosine kinase and the recruitment/tyrosine phosphorylation of STAT5a. However, the mechanisms for attenuating the Prl-R/Jak-2/STAT5a signaling cascade are just now being elucidated. Here, we present evidence that caveolin-1 functions as a novel suppressor of cytokine signaling in the mammary gland, akin to the SOCS family of proteins. Specifically, we show that caveolin-1 expression blocks prolactin-induced activation of a STAT5a-responsive luciferase reporter in mammary epithelial cells. Furthermore, caveolin-1 expression inhibited prolactin-induced STAT5a tyrosine phosphorylation and DNA binding activity, suggesting that caveolin-1 may negatively regulate the Jak-2 tyrosine kinase. Because the caveolin-scaffolding domain bears a striking resemblance to the SOCS pseudosubstrate domain, we examined whether Jak-2 associates with caveolin-1. In accordance with this homology, we demonstrate that Jak-2 cofractionates and coimmunoprecipitates with caveolin-1. We next tested the in vivo relevance of these findings using female Cav-1 (-/-) null mice. If caveolin-1 normally functions as a suppressor of cytokine signaling in the mammary gland, then Cav-1 null mice should show premature development of the lobuloalveolar compartment because of hyperactivation of the prolactin signaling cascade via disinhibition of Jak-2. In accordance with this prediction, Cav-1 null mice show accelerated development of the lobuloalveolar compartment, premature milk production, and hyperphosphorylation of STAT5a (pY694) at its Jak-2 phosphorylation site. In addition, the Ras-p42/44 MAPK cascade is hyper-activated. Because a similar premature lactation phenotype is observed in SOCS1 (-/-) null mice, we conclude that caveolin-1 is a novel suppressor of cytokine signaling.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Carrier Proteins / genetics
  • Caveolin 1
  • Caveolins / genetics
  • Caveolins / metabolism*
  • Cell Line
  • Cell Membrane / metabolism
  • DNA-Binding Proteins / metabolism*
  • Down-Regulation / physiology
  • Enzyme Activation
  • Epithelial Cells / metabolism
  • Estrogens / metabolism
  • Female
  • Genes, Reporter
  • Janus Kinase 2
  • Lactation Disorders*
  • Mammary Glands, Animal / cytology
  • Mammary Glands, Animal / growth & development*
  • Mammary Glands, Animal / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Milk Proteins / biosynthesis
  • Mitogen-Activated Protein Kinases / metabolism
  • Molecular Sequence Data
  • Pregnancy
  • Progesterone / metabolism
  • Prolactin / metabolism
  • Protein-Tyrosine Kinases / metabolism*
  • Proteins / genetics
  • Proto-Oncogene Proteins*
  • Repressor Proteins*
  • STAT5 Transcription Factor
  • Sequence Alignment
  • Signal Transduction / physiology*
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Trans-Activators / metabolism*
  • Transcription Factors*

Substances

  • Carrier Proteins
  • Cav1 protein, mouse
  • Caveolin 1
  • Caveolins
  • DNA-Binding Proteins
  • Estrogens
  • Milk Proteins
  • Proteins
  • Proto-Oncogene Proteins
  • Repressor Proteins
  • STAT5 Transcription Factor
  • Socs1 protein, mouse
  • Socs3 protein, mouse
  • Stat5a protein, mouse
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Trans-Activators
  • Transcription Factors
  • Progesterone
  • Prolactin
  • Protein-Tyrosine Kinases
  • Jak2 protein, mouse
  • Janus Kinase 2
  • Mitogen-Activated Protein Kinases