Transcriptionally inducible Pleckstrin homology-like domain, family A, member 1, attenuates ErbB receptor activity by inhibiting receptor oligomerization

Feedback control is a key mechanism in signal transduction, intimately involved in regulating the outcome of the cellular response. Here, we report a novel mechanism by which PHLDA1, Pleckstrin homology-like domain, family A, member 1, negatively regulates ErbB receptor signaling by inhibition of re...

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Published inThe Journal of biological chemistry Vol. 293; no. 6; pp. 2206 - 2218
Main Authors Magi, Shigeyuki, Iwamoto, Kazunari, Yumoto, Noriko, Hiroshima, Michio, Nagashima, Takeshi, Ohki, Rieko, Garcia-Munoz, Amaya, Volinsky, Natalia, Von Kriegsheim, Alexander, Sako, Yasushi, Takahashi, Koichi, Kimura, Shuhei, Kholodenko, Boris N., Okada-Hatakeyama, Mariko
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 09.02.2018
American Society for Biochemistry and Molecular Biology
Subjects
breast cancer
Humans
mathematical modeling
MCF-7 Cells
Models, Chemical
Neuregulin-1 - metabolism
oligomerization
Protein Multimerization
receptor tyrosine kinase
Receptor, ErbB-3 - metabolism
Signal Transduction
Single Molecule Imaging
Single-Cell Analysis
Transcription Factors - metabolism
Transcription Factors - physiology
Transcription, Genetic
mathematical modeling
breast cancer
receptor tyrosine kinase
oligomerization
signal transduction
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Abstract Feedback control is a key mechanism in signal transduction, intimately involved in regulating the outcome of the cellular response. Here, we report a novel mechanism by which PHLDA1, Pleckstrin homology-like domain, family A, member 1, negatively regulates ErbB receptor signaling by inhibition of receptor oligomerization. We have found that the ErbB3 ligand, heregulin, induces PHILDA1 expression in MCF-7 cells. Transcriptionally-induced PHLDA1 protein directly binds to ErbB3, whereas knockdown of PHLDA1 increases complex formation between ErbB3 and ErbB2. To provide insight into the mechanism for our time-course and single-cell experimental observations, we performed a systematic computational search of network topologies of the mathematical models based on receptor dimer-tetramer formation in the ErbB activation processes. Our results indicate that only a model in which PHLDA1 inhibits formation of both dimers and tetramer can explain the experimental data. Predictions made from this model were further validated by single-molecule imaging experiments. Our studies suggest a unique regulatory feature of PHLDA1 to inhibit the ErbB receptor oligomerization process and thereby control the activity of receptor signaling network.
AbstractList Feedback control is a key mechanism in signal transduction, intimately involved in regulating the outcome of the cellular response. Here, we report a novel mechanism by which PHLDA1, Pleckstrin homology-like domain, family A, member 1, negatively regulates ErbB receptor signaling by inhibition of receptor oligomerization. We have found that the ErbB3 ligand, heregulin, induces PHILDA1 expression in MCF-7 cells. Transcriptionally-induced PHLDA1 protein directly binds to ErbB3, whereas knockdown of PHLDA1 increases complex formation between ErbB3 and ErbB2. To provide insight into the mechanism for our time-course and single-cell experimental observations, we performed a systematic computational search of network topologies of the mathematical models based on receptor dimer-tetramer formation in the ErbB activation processes. Our results indicate that only a model in which PHLDA1 inhibits formation of both dimers and tetramer can explain the experimental data. Predictions made from this model were further validated by single-molecule imaging experiments. Our studies suggest a unique regulatory feature of PHLDA1 to inhibit the ErbB receptor oligomerization process and thereby control the activity of receptor signaling network.
Feedback control is a key mechanism in signal transduction, intimately involved in regulating the outcome of the cellular response. Here, we report a novel mechanism by which PHLDA1, Pleckstrin homology-like domain, family A, member 1, negatively regulates ErbB receptor signaling by inhibition of receptor oligomerization. We have found that the ErbB3 ligand, heregulin, induces PHILDA1 expression in MCF-7 cells. Transcriptionally-induced PHLDA1 protein directly binds to ErbB3, whereas knockdown of PHLDA1 increases complex formation between ErbB3 and ErbB2. To provide insight into the mechanism for our time-course and single-cell experimental observations, we performed a systematic computational search of network topologies of the mathematical models based on receptor dimer-tetramer formation in the ErbB activation processes. Our results indicate that only a model in which PHLDA1 inhibits formation of both dimers and tetramer can explain the experimental data. Predictions made from this model were further validated by single-molecule imaging experiments. Our studies suggest a unique regulatory feature of PHLDA1 to inhibit the ErbB receptor oligomerization process and thereby control the activity of receptor signaling network.
Feedback control is a key mechanism in signal transduction, intimately involved in regulating the outcome of the cellular response. Here, we report a novel mechanism by which PHLDA1, Pleckstrin homology-like domain, family A, member 1, negatively regulates ErbB receptor signaling by inhibition of receptor oligomerization. We have found that the ErbB3 ligand, heregulin, induces expression in MCF-7 cells. Transcriptionally-induced PHLDA1 protein directly binds to ErbB3, whereas knockdown of increases complex formation between ErbB3 and ErbB2. To provide insight into the mechanism for our time-course and single-cell experimental observations, we performed a systematic computational search of network topologies of the mathematical models based on receptor dimer-tetramer formation in the ErbB activation processes. Our results indicate that only a model in which PHLDA1 inhibits formation of both dimers and tetramer can explain the experimental data. Predictions made from this model were further validated by single-molecule imaging experiments. Our studies suggest a unique regulatory feature of PHLDA1 to inhibit the ErbB receptor oligomerization process and thereby control the activity of receptor signaling network.
Author Nagashima, Takeshi
Iwamoto, Kazunari
Okada-Hatakeyama, Mariko
Volinsky, Natalia
Kimura, Shuhei
Ohki, Rieko
Kholodenko, Boris N.
Yumoto, Noriko
Von Kriegsheim, Alexander
Takahashi, Koichi
Garcia-Munoz, Amaya
Sako, Yasushi
Hiroshima, Michio
Magi, Shigeyuki
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  surname: Yumoto
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  givenname: Rieko
  surname: Ohki
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  organization: Division of Rare Cancer Research, National Cancer Center Research Institute, Tsukiji 5-1-1, Chuo-ku, Tokyo 104-0045, Japan
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  givenname: Amaya
  surname: Garcia-Munoz
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  surname: Takahashi
  fullname: Takahashi, Koichi
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  email: mokada@protein.osaka-u.ac.jp
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Keywords mathematical modeling
breast cancer
receptor tyrosine kinase
oligomerization
signal transduction
Language English
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2018 by The American Society for Biochemistry and Molecular Biology, Inc.
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Both authors contributed equally to this work.
Supported by MEXT SPIRE Supercomputational Life Science.
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Snippet Feedback control is a key mechanism in signal transduction, intimately involved in regulating the outcome of the cellular response. Here, we report a novel...
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StartPage 2206
SubjectTerms breast cancer
Humans
mathematical modeling
MCF-7 Cells
Models, Chemical
Neuregulin-1 - metabolism
oligomerization
Protein Multimerization
receptor tyrosine kinase
Receptor, ErbB-3 - metabolism
Signal Transduction
Single Molecule Imaging
Single-Cell Analysis
Transcription Factors - metabolism
Transcription Factors - physiology
Transcription, Genetic
Title Transcriptionally inducible Pleckstrin homology-like domain, family A, member 1, attenuates ErbB receptor activity by inhibiting receptor oligomerization
URI https://dx.doi.org/10.1074/jbc.M117.778399
https://www.ncbi.nlm.nih.gov/pubmed/29233889
https://search.proquest.com/docview/1976440259
https://pubmed.ncbi.nlm.nih.gov/PMC5808779
Volume 293
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