YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway

The Hippo signalling pathway regulates cellular proliferation and survival, thus has profound effects on normal cell fate and tumorigenesis. The pivotal effector of this pathway is YAP (yes-associated protein), a transcriptional co-activator amplified in mouse and human cancers, where it promotes ep...

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Published inNature cell biology Vol. 11; no. 12; pp. 1444 - 1450
Main Authors Overholtzer, Michael, Smolen, Gromoslaw A, Brugge, Joan S, Zhang, Jianmin, Ji, Jun-Yuan, Yu, Min, Dyson, Nicholas J, Haber, Daniel A, Wang, Rebecca
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.12.2009
Nature Publishing Group
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Abstract The Hippo signalling pathway regulates cellular proliferation and survival, thus has profound effects on normal cell fate and tumorigenesis. The pivotal effector of this pathway is YAP (yes-associated protein), a transcriptional co-activator amplified in mouse and human cancers, where it promotes epithelial to mesenchymal transition (EMT) and malignant transformation. So far, studies of YAP target genes have focused on cell-autonomous mediators; here we show that YAP-expressing MCF10A breast epithelial cells enhance the proliferation of neighbouring untransfected cells, implicating a non-cell-autonomous mechanism. We identify the gene for the epidermal growth factor receptor (EGFR) ligand amphiregulin (AREG) as a transcriptional target of YAP, whose induction contributes to YAP-mediated cell proliferation and migration, but not EMT. Knockdown of AREG or addition of an EGFR kinase inhibitor abrogates the proliferative effects of YAP expression. Suppression of the negative YAP regulators LATS1 and 2 (large tumour suppressor 1 and 2) is sufficient to induce AREG expression, consistent with physiological regulation of AREG by the Hippo pathway. Genetic interaction between the Drosophila YAP orthologue Yorkie and Egfr signalling components supports the link between these two highly conserved signalling pathways. Thus, YAP-dependent secretion of AREG indicates that activation of EGFR signalling is an important non-cell-autonomous effector of the Hippo pathway, which has implications for the regulation of both physiological and malignant cell proliferation.
AbstractList The Hippo signaling pathway regulates cellular proliferation and survival, thus exerting profound effects on normal cell fate and tumorigenesis 1 - 3 . The pivotal effector of this pathway is YAP, a transcriptional co-activator amplified in mouse and human cancers, where it promotes epithelial to mesenchymal transition (EMT) and malignant transformation 4 - 10 . To date, studies of YAP target genes have focused on cell-autonomous mediators; here we show that YAP-expressing MCF10A breast epithelial cells enhance the proliferation of neighboring untransfected cells, implicating a non-cell autonomous mechanism. We identify the epidermal growth factor receptor (EGFR) ligand, amphiregulin (AREG), as a transcriptional target of YAP, whose induction contributes to YAP-mediated cell proliferation and migration, but not EMT. Knockdown of AREG or addition of an EGFR kinase inhibitor abrogates the proliferative effects of YAP expression. Suppression of the negative YAP regulators LATS1/2 is sufficient to induce AREG expression, consistent with physiological regulation of AREG by the Hippo pathway. Genetic interaction between the Drosophila YAP orthologue Yorkie and Egfr signaling components support the link between these two highly conserved signaling pathways. Thus, YAP-dependent secretion of AREG implicates activation of EGFR signaling as an important non-cell autonomous effector of the Hippo pathway, with implications for the regulation of both physiological and malignant cell proliferation.
The Hippo pathway regulates proliferation and survival in Drosophila and mammals, although shared transcriptional targets of their effectors have not been identified. Mammalian YAP controls expression of the EGFR ligand amphiregulin to regulate epithelial-to-mesenchymal transition in mammary epithelial cells, and the EGFR pathway genetically interacts with Yorkie in Drosophila. The Hippo signalling pathway regulates cellular proliferation and survival, thus has profound effects on normal cell fate and tumorigenesis 1 , 2 , 3 . The pivotal effector of this pathway is YAP (yes-associated protein), a transcriptional co-activator amplified in mouse and human cancers, where it promotes epithelial to mesenchymal transition (EMT) and malignant transformation 4 , 5 , 6 , 7 , 8 , 9 , 10 . So far, studies of YAP target genes have focused on cell-autonomous mediators; here we show that YAP-expressing MCF10A breast epithelial cells enhance the proliferation of neighbouring untransfected cells, implicating a non-cell-autonomous mechanism. We identify the gene for the epidermal growth factor receptor (EGFR) ligand amphiregulin (AREG) as a transcriptional target of YAP, whose induction contributes to YAP-mediated cell proliferation and migration, but not EMT. Knockdown of AREG or addition of an EGFR kinase inhibitor abrogates the proliferative effects of YAP expression. Suppression of the negative YAP regulators LATS1 and 2 (large tumour suppressor 1 and 2) is sufficient to induce AREG expression, consistent with physiological regulation of AREG by the Hippo pathway. Genetic interaction between the Drosophila YAP orthologue Yorkie and Egfr signalling components supports the link between these two highly conserved signalling pathways. Thus, YAP-dependent secretion of AREG indicates that activation of EGFR signalling is an important non-cell-autonomous effector of the Hippo pathway, which has implications for the regulation of both physiological and malignant cell proliferation.
The Hippo signalling pathway regulates cellular proliferation and survival, thus has profound effects on normal cell fate and tumorigenesis. The pivotal effector of this pathway is YAP (yes-associated protein), a transcriptional co-activator amplified in mouse and human cancers, where it promotes epithelial to mesenchymal transition (EMT) and malignant transformation. So far, studies of YAP target genes have focused on cell-autonomous mediators; here we show that YAP-expressing MCF10A breast epithelial cells enhance the proliferation of neighbouring untransfected cells, implicating a non-cell-autonomous mechanism. We identify the gene for the epidermal growth factor receptor (EGFR) ligand amphiregulin (AREG) as a transcriptional target of YAP, whose induction contributes to YAP-mediated cell proliferation and migration, but not EMT. Knockdown of AREG or addition of an EGFR kinase inhibitor abrogates the proliferative effects of YAP expression. Suppression of the negative YAP regulators LATS1 and 2 (large tumour suppressor 1 and 2) is sufficient to induce AREG expression, consistent with physiological regulation of AREG by the Hippo pathway. Genetic interaction between the Drosophila YAP orthologue Yorkie and Egfr signalling components supports the link between these two highly conserved signalling pathways. Thus, YAP-dependent secretion of AREG indicates that activation of EGFR signalling is an important non-cell-autonomous effector of the Hippo pathway, which has implications for the regulation of both physiological and malignant cell proliferation.
The Hippo signalling pathway regulates cellular proliferation and survival, thus has profound effects on normal cell fate and tumorigenesis (1-3). The pivotal effector of this pathway is YAP (yes-associated protein), a transcriptional co-activator amplified in mouse and human cancers, where it promotes epithelial to mesenchymal transition (EMT) and malignant transformation (4-10). So far, studies of YAP target genes have focused on cell-autonomous mediators; here we show that YAP-expressing MCF10A breast epithelial cells enhance the proliferation of neighbouring untransfected cells, implicating a non-cell-autonomous mechanism. We identify the gene for the epidermal growth factor receptor (EGFR) ligand amphiregulin (AREG) as a transcriptional target of YAP, whose induction contributes to YAP-mediated cell proliferation and migration, but not EMT. Knockdown of AREG or addition of an EGFR kinase inhibitor abrogates the proliferative effects of YAP expression. Suppression of the negative YAP regulators LATS1 and 2 (large tumour suppressor 1 and 2) is sufficient to induce AREG expression, consistent with physiological regulation of AREG by the Hippo pathway. Genetic interaction between the Drosophila YAP orthologue Yorkie and Egfr signalling components supports the link between these two highly conserved signalling pathways. Thus, YAP-dependent secretion of AREG indicates that activation of EGFR signalling is an important non-cell-autonomous effector of the Hippo pathway, which has implications for the regulation of both physiological and malignant cell proliferation.
Audience Academic
Author Smolen, Gromoslaw A
Haber, Daniel A
Dyson, Nicholas J
Zhang, Jianmin
Wang, Rebecca
Brugge, Joan S
Ji, Jun-Yuan
Overholtzer, Michael
Yu, Min
AuthorAffiliation 2 Howard Hughes Medical Institute, Harvard Medical School, Boston MA 02115
1 Massachusetts General Hospital Cancer Center, Harvard Medical School, Charlestown, MA 02129
3 Department of Cell Biology, Harvard Medical School, Boston MA 02115
AuthorAffiliation_xml – name: 1 Massachusetts General Hospital Cancer Center, Harvard Medical School, Charlestown, MA 02129
– name: 3 Department of Cell Biology, Harvard Medical School, Boston MA 02115
– name: 2 Howard Hughes Medical Institute, Harvard Medical School, Boston MA 02115
Author_xml – givenname: Michael
  surname: Overholtzer
  fullname: Overholtzer, Michael
  organization: Department of Cell Biology, Harvard Medical School
– givenname: Gromoslaw A
  surname: Smolen
  fullname: Smolen, Gromoslaw A
  organization: Massachusetts General Hospital Cancer Center, Harvard Medical School
– givenname: Joan S
  surname: Brugge
  fullname: Brugge, Joan S
  organization: Department of Cell Biology, Harvard Medical School
– givenname: Jianmin
  surname: Zhang
  fullname: Zhang, Jianmin
  organization: Massachusetts General Hospital Cancer Center, Harvard Medical School
– givenname: Jun-Yuan
  surname: Ji
  fullname: Ji, Jun-Yuan
  organization: Massachusetts General Hospital Cancer Center, Harvard Medical School Department of Molecular and Cellular Medicine, Texas A & M Health Science Center
– givenname: Min
  surname: Yu
  fullname: Yu, Min
  organization: Massachusetts General Hospital Cancer Center, Harvard Medical School Howard Hughes Medical Institute
– givenname: Nicholas J
  surname: Dyson
  fullname: Dyson, Nicholas J
  organization: Massachusetts General Hospital Cancer Center, Harvard Medical School
– givenname: Daniel A
  surname: Haber
  fullname: Haber, Daniel A
  organization: Massachusetts General Hospital Cancer Center, Harvard Medical School Howard Hughes Medical Institute
– givenname: Rebecca
  surname: Wang
  fullname: Wang, Rebecca
  organization: Massachusetts General Hospital Cancer Center, Harvard Medical School
BackLink https://www.ncbi.nlm.nih.gov/pubmed/19935651$$D View this record in MEDLINE/PubMed
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Snippet The Hippo signalling pathway regulates cellular proliferation and survival, thus has profound effects on normal cell fate and tumorigenesis. The pivotal...
The Hippo pathway regulates proliferation and survival in Drosophila and mammals, although shared transcriptional targets of their effectors have not been...
The Hippo signalling pathway regulates cellular proliferation and survival, thus has profound effects on normal cell fate and tumorigenesis (1-3). The pivotal...
The Hippo signaling pathway regulates cellular proliferation and survival, thus exerting profound effects on normal cell fate and tumorigenesis 1 - 3 . The...
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StartPage 1444
SubjectTerms Amphiregulin
Animals
Biomedical and Life Sciences
Cancer cells
Cancer Research
Carcinogenesis
Causes of
Cell Biology
Cell Cycle Proteins
Cell growth
Cell Line, Tumor
Cellular signal transduction
Developmental Biology
Drosophila melanogaster - genetics
Drosophila melanogaster - metabolism
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
EGF Family of Proteins
Epidermal growth factor
ErbB Receptors - genetics
ErbB Receptors - metabolism
Female
Genetic aspects
Glycoproteins - genetics
Glycoproteins - metabolism
Health aspects
Humans
Intercellular Signaling Peptides and Proteins - genetics
Intercellular Signaling Peptides and Proteins - metabolism
Intracellular Signaling Peptides and Proteins - genetics
Intracellular Signaling Peptides and Proteins - metabolism
Kinases
letter
Life Sciences
Nuclear Proteins - genetics
Nuclear Proteins - metabolism
Physiological aspects
Physiology
Protein Serine-Threonine Kinases - genetics
Protein Serine-Threonine Kinases - metabolism
Proteins
Receptors, Invertebrate Peptide - metabolism
Signal Transduction
Stem Cells
Trans-Activators - genetics
Trans-Activators - metabolism
Transcription Factors - genetics
Transcription Factors - metabolism
YAP-Signaling Proteins
Title YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway
URI http://dx.doi.org/10.1038/ncb1993
https://link.springer.com/article/10.1038/ncb1993
https://www.ncbi.nlm.nih.gov/pubmed/19935651
https://www.proquest.com/docview/222375020
https://search.proquest.com/docview/733131387
https://pubmed.ncbi.nlm.nih.gov/PMC2819909
Volume 11
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