Endocytosis Inhibition in Humans to Improve Responses to ADCC-Mediating Antibodies
A safe and controlled manipulation of endocytosis in vivo may have disruptive therapeutic potential. Here, we demonstrate that the anti-emetic/anti-psychotic prochlorperazine can be repurposed to reversibly inhibit the in vivo endocytosis of membrane proteins targeted by therapeutic monoclonal antib...
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| Published in | Cell Vol. 180; no. 5; pp. 895 - 914.e27 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
05.03.2020
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| Subjects | |
| Online Access | Get full text |
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| Abstract | A safe and controlled manipulation of endocytosis in vivo may have disruptive therapeutic potential. Here, we demonstrate that the anti-emetic/anti-psychotic prochlorperazine can be repurposed to reversibly inhibit the in vivo endocytosis of membrane proteins targeted by therapeutic monoclonal antibodies, as directly demonstrated by our human tumor ex vivo assay. Temporary endocytosis inhibition results in enhanced target availability and improved efficiency of natural killer cell-mediated antibody-dependent cellular cytotoxicity (ADCC), a mediator of clinical responses induced by IgG1 antibodies, demonstrated here for cetuximab, trastuzumab, and avelumab. Extensive analysis of downstream signaling pathways ruled out on-target toxicities. By overcoming the heterogeneity of drug target availability that frequently characterizes poorly responsive or resistant tumors, clinical application of reversible endocytosis inhibition may considerably improve the clinical benefit of ADCC-mediating therapeutic antibodies.
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•A strategy for improving the ADCC potential of therapeutic antibodies is presented•Temporary inhibition of endocytosis increases tumor cell antigen presentation•Prochlorperazine could be repurposed to enhance the efficacy of anti-tumor mAbs•Potential to reduce heterogeneity in tumor cell responses to many IgG1 antibodies
Endocytosis inhibitors, such as prochlorperazine, can be used to move tumor cell antigens that are the targets of therapeutic monoclonal antibodies but hiding inside the cell to the cell surface for improved therapeutic antibody binding and tumor cell destruction by NK cells. |
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| AbstractList | A safe and controlled manipulation of endocytosis in vivo may have disruptive therapeutic potential. Here, we demonstrate that the anti-emetic/anti-psychotic prochlorperazine can be repurposed to reversibly inhibit the in vivo endocytosis of membrane proteins targeted by therapeutic monoclonal antibodies, as directly demonstrated by our human tumor ex vivo assay. Temporary endocytosis inhibition results in enhanced target availability and improved efficiency of natural killer cell-mediated antibody-dependent cellular cytotoxicity (ADCC), a mediator of clinical responses induced by IgG1 antibodies, demonstrated here for cetuximab, trastuzumab, and avelumab. Extensive analysis of downstream signaling pathways ruled out on-target toxicities. By overcoming the heterogeneity of drug target availability that frequently characterizes poorly responsive or resistant tumors, clinical application of reversible endocytosis inhibition may considerably improve the clinical benefit of ADCC-mediating therapeutic antibodies. A safe and controlled manipulation of endocytosis in vivo may have disruptive therapeutic potential. Here, we demonstrate that the anti-emetic/anti-psychotic prochlorperazine can be repurposed to reversibly inhibit the in vivo endocytosis of membrane proteins targeted by therapeutic monoclonal antibodies, as directly demonstrated by our human tumor ex vivo assay. Temporary endocytosis inhibition results in enhanced target availability and improved efficiency of natural killer cell-mediated antibody-dependent cellular cytotoxicity (ADCC), a mediator of clinical responses induced by IgG1 antibodies, demonstrated here for cetuximab, trastuzumab, and avelumab. Extensive analysis of downstream signaling pathways ruled out on-target toxicities. By overcoming the heterogeneity of drug target availability that frequently characterizes poorly responsive or resistant tumors, clinical application of reversible endocytosis inhibition may considerably improve the clinical benefit of ADCC-mediating therapeutic antibodies. [Display omitted] •A strategy for improving the ADCC potential of therapeutic antibodies is presented•Temporary inhibition of endocytosis increases tumor cell antigen presentation•Prochlorperazine could be repurposed to enhance the efficacy of anti-tumor mAbs•Potential to reduce heterogeneity in tumor cell responses to many IgG1 antibodies Endocytosis inhibitors, such as prochlorperazine, can be used to move tumor cell antigens that are the targets of therapeutic monoclonal antibodies but hiding inside the cell to the cell surface for improved therapeutic antibody binding and tumor cell destruction by NK cells. |
| Author | Rae, James Frazer, Ian H. Panizza, Benedict Walpole, Euan De Lima, Priscila O. Simpson, Fiona Gonzalez Cruz, Jazmina L. Hu, Lingbo Lum, Benedict O’Donnell, Jake S. Martin, Jennifer H. King, Brigid Robinson, Phillip J. Okano, Satomi Foote, Matthew Cuff, Katharine Wells, James W. Barry, Rachael Souza-Fonseca-Guimaraes, Fernando Parton, Robert G. Moi, Davide Dolcetti, Riccardo Thomas, Ranjeny Mazzieri, Roberta Chew, Hui Yi Saunders, Nicholas A. Banushi, Blerida McCluskey, Adam Echejoh, Godwins Merida de Long, Lilia Joseph, Shannon R. |
| Author_xml | – sequence: 1 givenname: Hui Yi surname: Chew fullname: Chew, Hui Yi organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 2 givenname: Priscila O. surname: De Lima fullname: De Lima, Priscila O. organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 3 givenname: Jazmina L. surname: Gonzalez Cruz fullname: Gonzalez Cruz, Jazmina L. organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 4 givenname: Blerida surname: Banushi fullname: Banushi, Blerida organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 5 givenname: Godwins surname: Echejoh fullname: Echejoh, Godwins organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 6 givenname: Lingbo surname: Hu fullname: Hu, Lingbo organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 7 givenname: Shannon R. surname: Joseph fullname: Joseph, Shannon R. organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 8 givenname: Benedict surname: Lum fullname: Lum, Benedict organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 9 givenname: James surname: Rae fullname: Rae, James organization: Cell Biology and Molecular Medicine Division, Institute for Molecular Bioscience, University of Queensland, St Lucia QLD 4072, Australia – sequence: 10 givenname: Jake S. surname: O’Donnell fullname: O’Donnell, Jake S. organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 11 givenname: Lilia surname: Merida de Long fullname: Merida de Long, Lilia organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 12 givenname: Satomi surname: Okano fullname: Okano, Satomi organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 13 givenname: Brigid surname: King fullname: King, Brigid organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 14 givenname: Rachael surname: Barry fullname: Barry, Rachael organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 15 givenname: Davide surname: Moi fullname: Moi, Davide organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 16 givenname: Roberta surname: Mazzieri fullname: Mazzieri, Roberta organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 17 givenname: Ranjeny surname: Thomas fullname: Thomas, Ranjeny organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 18 givenname: Fernando surname: Souza-Fonseca-Guimaraes fullname: Souza-Fonseca-Guimaraes, Fernando organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 19 givenname: Matthew surname: Foote fullname: Foote, Matthew organization: Princess Alexandra Hospital, Brisbane QLD 4102, Australia – sequence: 20 givenname: Adam surname: McCluskey fullname: McCluskey, Adam organization: Centre for Chemistry, Biology and Clinical Pharmacology, The University of Newcastle, Callaghan NSW 2308, Australia – sequence: 21 givenname: Phillip J. surname: Robinson fullname: Robinson, Phillip J. organization: Cell Signaling Unit, Children’s Medical Research Institute, The University of Sydney, Sydney NSW 2145, Australia – sequence: 22 givenname: Ian H. surname: Frazer fullname: Frazer, Ian H. organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 23 givenname: Nicholas A. surname: Saunders fullname: Saunders, Nicholas A. organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 24 givenname: Robert G. surname: Parton fullname: Parton, Robert G. organization: Cell Biology and Molecular Medicine Division, Institute for Molecular Bioscience, University of Queensland, St Lucia QLD 4072, Australia – sequence: 25 givenname: Riccardo surname: Dolcetti fullname: Dolcetti, Riccardo organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 26 givenname: Katharine surname: Cuff fullname: Cuff, Katharine organization: Princess Alexandra Hospital, Brisbane QLD 4102, Australia – sequence: 27 givenname: Jennifer H. surname: Martin fullname: Martin, Jennifer H. organization: Princess Alexandra Hospital, Brisbane QLD 4102, Australia – sequence: 28 givenname: Benedict surname: Panizza fullname: Panizza, Benedict organization: Princess Alexandra Hospital, Brisbane QLD 4102, Australia – sequence: 29 givenname: Euan surname: Walpole fullname: Walpole, Euan organization: Princess Alexandra Hospital, Brisbane QLD 4102, Australia – sequence: 30 givenname: James W. surname: Wells fullname: Wells, James W. organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia – sequence: 31 givenname: Fiona surname: Simpson fullname: Simpson, Fiona email: f.simpson@uq.edu.au organization: The University of Queensland Diamantina Institute, University of Queensland, Woolloongabba QLD 4102, Australia |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32142680$$D View this record in MEDLINE/PubMed |
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| Keywords | trastuzumab prochlorperazine antibody-dependent cellular cytotoxicity avelumab epidermal growth factor receptor endocytosis cetuximab programmed death ligand 1 monoclonal antibody therapy natural killer cell |
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| Title | Endocytosis Inhibition in Humans to Improve Responses to ADCC-Mediating Antibodies |
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