Bimolecular complementation affinity purification (BiCAP) reveals dimer-specific protein interactions for ERBB2 dimers

The dynamic assembly of multiprotein complexes is a central mechanism of many cell signaling pathways. This process is key to maintaining the spatiotemporal specificity required for an accurate, yet adaptive, response to rapidly changing cellular conditions. We describe a technique for the specific...

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Published in:Science signaling Vol. 9; no. 436; p. ra69
Main Authors: Croucher, David R, Iconomou, Mary, Hastings, Jordan F, Kennedy, Sean P, Han, Jeremy Z R, Shearer, Robert F, McKenna, Jessie, Wan, Adrian, Lau, Joseph, Aparicio, Samuel, Saunders, Darren N
Format: Journal Article
Language:English
Published: United States 12.07.2016
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ISSN:1937-9145, 1937-9145
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Abstract The dynamic assembly of multiprotein complexes is a central mechanism of many cell signaling pathways. This process is key to maintaining the spatiotemporal specificity required for an accurate, yet adaptive, response to rapidly changing cellular conditions. We describe a technique for the specific isolation and downstream proteomic characterization of any two interacting proteins, to the exclusion of their individual moieties and competing binding partners. We termed the approach bimolecular complementation affinity purification (BiCAP) because it combines the use of conformation-specific nanobodies with a protein-fragment complementation assay with affinity purification. Using BiCAP, we characterized the specific interactome of the epidermal growth factor receptor (EGFR) family member ERBB2 when in the form of a homodimer or when in the form of a heterodimer with either EGFR or ERBB3. We identified dimer-specific interaction patterns for key adaptor proteins and identified a number of previously unknown interacting partners. Functional analysis for one of these newly identified partners revealed a noncanonical mechanism of extracellular signal-regulated kinase (ERK) activation that is specific to the ERBB2:ERBB3 heterodimer and acts through the adaptor protein FAM59A in breast cancer cells.
AbstractList The dynamic assembly of multiprotein complexes is a central mechanism of many cell signaling pathways. This process is key to maintaining the spatiotemporal specificity required for an accurate, yet adaptive, response to rapidly changing cellular conditions. We describe a technique for the specific isolation and downstream proteomic characterization of any two interacting proteins, to the exclusion of their individual moieties and competing binding partners. We termed the approach bimolecular complementation affinity purification (BiCAP) because it combines the use of conformation-specific nanobodies with a protein-fragment complementation assay with affinity purification. Using BiCAP, we characterized the specific interactome of the epidermal growth factor receptor (EGFR) family member ERBB2 when in the form of a homodimer or when in the form of a heterodimer with either EGFR or ERBB3. We identified dimer-specific interaction patterns for key adaptor proteins and identified a number of previously unknown interacting partners. Functional analysis for one of these newly identified partners revealed a noncanonical mechanism of extracellular signal-regulated kinase (ERK) activation that is specific to the ERBB2:ERBB3 heterodimer and acts through the adaptor protein FAM59A in breast cancer cells.
The dynamic assembly of multiprotein complexes is a central mechanism of many cell signaling pathways. This process is key to maintaining the spatiotemporal specificity required for an accurate, yet adaptive, response to rapidly changing cellular conditions. We describe a technique for the specific isolation and downstream proteomic characterization of any two interacting proteins, to the exclusion of their individual moieties and competing binding partners. We termed the approach bimolecular complementation affinity purification (BiCAP) because it combines the use of conformation-specific nanobodies with a protein-fragment complementation assay with affinity purification. Using BiCAP, we characterized the specific interactome of the epidermal growth factor receptor (EGFR) family member ERBB2 when in the form of a homodimer or when in the form of a heterodimer with either EGFR or ERBB3. We identified dimer-specific interaction patterns for key adaptor proteins and identified a number of previously unknown interacting partners. Functional analysis for one of these newly identified partners revealed a noncanonical mechanism of extracellular signal-regulated kinase (ERK) activation that is specific to the ERBB2:ERBB3 heterodimer and acts through the adaptor protein FAM59A in breast cancer cells.The dynamic assembly of multiprotein complexes is a central mechanism of many cell signaling pathways. This process is key to maintaining the spatiotemporal specificity required for an accurate, yet adaptive, response to rapidly changing cellular conditions. We describe a technique for the specific isolation and downstream proteomic characterization of any two interacting proteins, to the exclusion of their individual moieties and competing binding partners. We termed the approach bimolecular complementation affinity purification (BiCAP) because it combines the use of conformation-specific nanobodies with a protein-fragment complementation assay with affinity purification. Using BiCAP, we characterized the specific interactome of the epidermal growth factor receptor (EGFR) family member ERBB2 when in the form of a homodimer or when in the form of a heterodimer with either EGFR or ERBB3. We identified dimer-specific interaction patterns for key adaptor proteins and identified a number of previously unknown interacting partners. Functional analysis for one of these newly identified partners revealed a noncanonical mechanism of extracellular signal-regulated kinase (ERK) activation that is specific to the ERBB2:ERBB3 heterodimer and acts through the adaptor protein FAM59A in breast cancer cells.
Author Lau, Joseph
Iconomou, Mary
Han, Jeremy Z R
Hastings, Jordan F
McKenna, Jessie
Aparicio, Samuel
Kennedy, Sean P
Croucher, David R
Shearer, Robert F
Wan, Adrian
Saunders, Darren N
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  surname: Croucher
  fullname: Croucher, David R
  email: d.croucher@garvan.org.au, d.saunders@unsw.edu.au
  organization: The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, New South Wales 2010, Australia. St. Vincent's Hospital Clinical School, University of New South Wales, Sydney, New South Wales 2052, Australia. School of Medicine, University College Dublin, Belfield, Dublin D4, Ireland. d.croucher@garvan.org.au d.saunders@unsw.edu.au
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  surname: Iconomou
  fullname: Iconomou, Mary
  organization: The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, New South Wales 2010, Australia
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  givenname: Jordan F
  surname: Hastings
  fullname: Hastings, Jordan F
  organization: The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, New South Wales 2010, Australia
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  givenname: Sean P
  surname: Kennedy
  fullname: Kennedy, Sean P
  organization: The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, New South Wales 2010, Australia. Systems Biology Ireland, University College Dublin, Belfield, Dublin D4, Ireland
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  surname: Han
  fullname: Han, Jeremy Z R
  organization: The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, New South Wales 2010, Australia
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  surname: Shearer
  fullname: Shearer, Robert F
  organization: The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, New South Wales 2010, Australia
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  surname: McKenna
  fullname: McKenna, Jessie
  organization: The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, New South Wales 2010, Australia
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  givenname: Adrian
  surname: Wan
  fullname: Wan, Adrian
  organization: Department of Molecular Oncology, British Columbia Cancer Research Centre, Vancouver, British Columbia V5Z 1L3, Canada
– sequence: 9
  givenname: Joseph
  surname: Lau
  fullname: Lau, Joseph
  organization: Department of Molecular Oncology, British Columbia Cancer Research Centre, Vancouver, British Columbia V5Z 1L3, Canada
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  givenname: Samuel
  surname: Aparicio
  fullname: Aparicio, Samuel
  organization: Department of Molecular Oncology, British Columbia Cancer Research Centre, Vancouver, British Columbia V5Z 1L3, Canada. Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
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  givenname: Darren N
  surname: Saunders
  fullname: Saunders, Darren N
  email: d.croucher@garvan.org.au, d.saunders@unsw.edu.au
  organization: The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, New South Wales 2010, Australia. School of Medical Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia. d.croucher@garvan.org.au d.saunders@unsw.edu.au
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Snippet The dynamic assembly of multiprotein complexes is a central mechanism of many cell signaling pathways. This process is key to maintaining the spatiotemporal...
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SubjectTerms Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Female
HEK293 Cells
Humans
MAP Kinase Signaling System
MCF-7 Cells
Protein Multimerization
Receptor, Epidermal Growth Factor - isolation & purification
Receptor, Epidermal Growth Factor - metabolism
Receptor, ErbB-2 - isolation & purification
Receptor, ErbB-2 - metabolism
Receptor, ErbB-3 - isolation & purification
Receptor, ErbB-3 - metabolism
Title Bimolecular complementation affinity purification (BiCAP) reveals dimer-specific protein interactions for ERBB2 dimers
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