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Research Article
EGFRvIII uses intrinsic and extrinsic mechanisms to reduce glioma adhesion and increase migration
Afsheen Banisadr, Mariam Eick, Pranjali Beri, Alison D. Parisian, Benjamin Yeoman, Jesse K. Placone, Adam J. Engler, Frank Furnari
Journal of Cell Science 2020 133: jcs247189 doi: 10.1242/jcs.247189 Published 24 December 2020
Afsheen Banisadr
1Biomedical Sciences Program, UC San Diego, La Jolla, CA 92093, USA
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Mariam Eick
2Department of Bioengineering, UC San Diego, La Jolla, CA 92093, USA
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Pranjali Beri
2Department of Bioengineering, UC San Diego, La Jolla, CA 92093, USA
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Alison D. Parisian
1Biomedical Sciences Program, UC San Diego, La Jolla, CA 92093, USA
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Benjamin Yeoman
2Department of Bioengineering, UC San Diego, La Jolla, CA 92093, USA
3Department of Mechanical Engineering, San Diego State University, San Diego, CA 92182, USA
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Jesse K. Placone
2Department of Bioengineering, UC San Diego, La Jolla, CA 92093, USA
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Adam J. Engler
1Biomedical Sciences Program, UC San Diego, La Jolla, CA 92093, USA
4Sanford Consortium for Regenerative Medicine, La Jolla, CA 92037, USA
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  • ORCID record for Adam J. Engler
  • For correspondence: aengler@ucsd.edu ffurnari@ucsd.edu
Frank Furnari
1Biomedical Sciences Program, UC San Diego, La Jolla, CA 92093, USA
5Ludwig Institute for Cancer Research, La Jolla, CA 92037, USA
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  • For correspondence: aengler@ucsd.edu ffurnari@ucsd.edu

Handling Editor: Andrew Ewald

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ABSTRACT

A lack of biological markers has limited our ability to identify the invasive cells responsible for glioblastoma multiforme (GBM). To become migratory and invasive, cells must downregulate matrix adhesions, which could be a physical marker of invasive potential. We engineered murine astrocytes with common GBM mutations, e.g. Ink4a (Ink) or PTEN deletion and expressing a constitutively active EGF receptor truncation (EGFRvIII), to elucidate their effect on adhesion. While loss of Ink or PTEN did not affect adhesion, counterparts expressing EGFRvIII were significantly less adhesive. EGFRvIII reduced focal adhesion size and number, and these cells – with more labile adhesions – displayed enhanced migration. Regulation appears to depend not on physical receptor association to integrins but, rather, on the activity of the receptor kinase, resulting in transcriptional integrin repression. Interestingly, EGFRvIII intrinsic signals can be propagated by cytokine crosstalk to cells expressing wild-type EGFR, resulting in reduced adhesion and enhanced migration. These data identify potential intrinsic and extrinsic mechanisms that gliomas use to invade surrounding parenchyma.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: A.J.E., F.F.; Methodology: A.B., A.J.E., F.F.; Software: A.B.; Validation: A.B.; Formal analysis: A.B., P.B., A.D.P., B.Y., J.K.P.; Investigation: A.B., M.E., P.B., A.D.P., B.Y., J.K.P.; Resources: A.J.E., F.F.; Writing - original draft: A.B., A.J.E., F.F.; Writing - review & editing: A.B., A.J.E., F.F.; Supervision: A.J.E., F.F.; Project administration: A.J.E., F.F.; Funding acquisition: A.J.E., F.F.

  • Funding

    Funding was provided by direct support from the Ludwig Institute for Cancer Research, National Institutes of Health (grant numbers: R01CA206880 and R21CA217735 to A.J.E., R01NS080939 to F.F., and R01NS116802 to A.J.E. and F.F.), the National Science Foundation (grant number: CMMI-1763139 to A.J.E.) and the National Science Foundation Graduate Research Fellowship program (to A.B.). Deposited in PMC for release after 12 months.

  • Supplementary information

    Supplementary information available online at https://jcs.biologists.org/lookup/doi/10.1242/jcs.247189.supplemental

  • Received April 3, 2020.
  • Accepted November 9, 2020.
  • © 2020. Published by The Company of Biologists Ltd
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Keywords

  • Cancer
  • Extracellular matrix
  • Adhesion
  • Invasion

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Research Article
EGFRvIII uses intrinsic and extrinsic mechanisms to reduce glioma adhesion and increase migration
Afsheen Banisadr, Mariam Eick, Pranjali Beri, Alison D. Parisian, Benjamin Yeoman, Jesse K. Placone, Adam J. Engler, Frank Furnari
Journal of Cell Science 2020 133: jcs247189 doi: 10.1242/jcs.247189 Published 24 December 2020
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Research Article
EGFRvIII uses intrinsic and extrinsic mechanisms to reduce glioma adhesion and increase migration
Afsheen Banisadr, Mariam Eick, Pranjali Beri, Alison D. Parisian, Benjamin Yeoman, Jesse K. Placone, Adam J. Engler, Frank Furnari
Journal of Cell Science 2020 133: jcs247189 doi: 10.1242/jcs.247189 Published 24 December 2020

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