IgE-based therapeutic combination enhances anti-tumor response in preclinical models of pancreatic cancer
Pancreatic ductal adenocarcinoma (PDAC) represents 3% of all cancer cases and 7% of all cancer deaths in the United States. Late diagnosis and inadequate response to standard chemotherapies contribute to an unfavorable prognosis and an overall 5-year survival rate of less than 10% in PDAC. Despite r...
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| Published in: | Molecular cancer therapeutics Vol. 20; no. 12; pp. 2457 - 2468 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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08-10-2021
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| Online Access: | Get full text |
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| Abstract | Pancreatic ductal adenocarcinoma (PDAC) represents 3% of all cancer cases and 7% of all cancer deaths in the United States. Late diagnosis and inadequate response to standard chemotherapies contribute to an unfavorable prognosis and an overall 5-year survival rate of less than 10% in PDAC. Despite recent advances in tumor immunology, tumor-induced immunosuppression attenuates the immunotherapy response in PDAC. To date, studies have focused on IgG-based therapeutic strategies in PDAC. With the recent interest in IgE-based therapies in multiple solid tumors, we explored the MUC1-targeted IgE antibody’s potential against pancreatic cancer. Our study demonstrates the notable expression of FcεRI (receptor for IgE antibody) in tumors from PDAC patients. Our study showed that administration with a limited amount of MUC1 targeted-IgE (mouse/human chimeric anti-MUC1.IgE) antibody at intermittent levels in combination with checkpoint inhibitor (anti-PD-L1) and TLR3 agonist (PolyICLC) induces a robust anti-tumor response that is dependent on NK and CD8 T cells in pancreatic tumor-bearing mice. Subsequently, our study showed that IgE antibody’s antigen specificity plays a vital role in executing the anti-tumor response as non-specific IgE, induced by ovalbumin (OVA), failed to restrict tumor growth in pancreatic tumor-bearing mice. Utilizing the OVA-induced allergic asthma-PDAC model, we demonstrate that allergic phenotype induced by OVA cannot restrain pancreatic tumor growth in orthotopic tumor-bearing mice. Together, our data demonstrate the novel tumor protective benefits of tumor antigen-specific IgE-based therapeutics in a preclinical model of pancreatic cancer, which can open new avenues for future clinical interventions. |
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| AbstractList | Pancreatic ductal adenocarcinoma (PDAC) represents 3% of all cancer cases and 7% of all cancer deaths in the United States. Late diagnosis and inadequate response to standard chemotherapies contribute to an unfavorable prognosis and an overall 5-year survival rate of less than 10% in PDAC. Despite recent advances in tumor immunology, tumor-induced immunosuppression attenuates the immunotherapy response in PDAC. To date, studies have focused on IgG-based therapeutic strategies in PDAC. With the recent interest in IgE-based therapies in multiple solid tumors, we explored the MUC1-targeted IgE antibody’s potential against pancreatic cancer. Our study demonstrates the notable expression of FcεRI (receptor for IgE antibody) in tumors from PDAC patients. Our study showed that administration with a limited amount of MUC1 targeted-IgE (mouse/human chimeric anti-MUC1.IgE) antibody at intermittent levels in combination with checkpoint inhibitor (anti-PD-L1) and TLR3 agonist (PolyICLC) induces a robust anti-tumor response that is dependent on NK and CD8 T cells in pancreatic tumor-bearing mice. Subsequently, our study showed that IgE antibody’s antigen specificity plays a vital role in executing the anti-tumor response as non-specific IgE, induced by ovalbumin (OVA), failed to restrict tumor growth in pancreatic tumor-bearing mice. Utilizing the OVA-induced allergic asthma-PDAC model, we demonstrate that allergic phenotype induced by OVA cannot restrain pancreatic tumor growth in orthotopic tumor-bearing mice. Together, our data demonstrate the novel tumor protective benefits of tumor antigen-specific IgE-based therapeutics in a preclinical model of pancreatic cancer, which can open new avenues for future clinical interventions. |
| Author | Mehla, Kamiya Nicodemus, Christopher F. Caffrey, Thomas C. Grunkemeyer, James A. Singh, Pankaj K. Patil, Prathamesh P. Markov, Spas Dimitrov Gonzalez, Daisy Radhakrishnan, Prakash Shukla, Surendra K. Madiyalakan, Ragupathy Jaffee, Elizabeth M. Poole, Jill A. Grandgenett, Paul M. Daniels-Wells, Tracy R. Penichet, Manuel L. Shin, Simon Hollingsworth, Michael A. Vance, Krysten E. Hanson, Ryan Huang, Ying Eberle, Kirsten C. Crawford, Ayrianne J. O’Connell, Kelly A. |
| AuthorAffiliation | b OncoQuest Pharmaceuticals Inc. Edmonton, Alberta, Canada c Division of Surgical Oncology, Department of Surgery, University of California in Los Angeles (UCLA), USA a The Eppley Institute for Research in Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, Nebraska, USA e AIT Strategies, Franconia, New Hampshire, USA f Allergy and Immunology Division, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska, USA g Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA d Division of Surgical Oncology, Department of Surgery and Department of Microbiology, Immunology and Molecular Genetics; The Molecular Biology Institute; Jonsson Comprehensive Cancer Center, University of California, Los Angeles (UCLA), California, USA |
| AuthorAffiliation_xml | – name: d Division of Surgical Oncology, Department of Surgery and Department of Microbiology, Immunology and Molecular Genetics; The Molecular Biology Institute; Jonsson Comprehensive Cancer Center, University of California, Los Angeles (UCLA), California, USA – name: f Allergy and Immunology Division, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska, USA – name: e AIT Strategies, Franconia, New Hampshire, USA – name: g Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA – name: a The Eppley Institute for Research in Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, Nebraska, USA – name: b OncoQuest Pharmaceuticals Inc. Edmonton, Alberta, Canada – name: c Division of Surgical Oncology, Department of Surgery, University of California in Los Angeles (UCLA), USA |
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Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA – sequence: 17 givenname: Ragupathy surname: Madiyalakan fullname: Madiyalakan, Ragupathy organization: The Eppley Institute for Research in Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, Nebraska, USA. OncoQuest Pharmaceuticals Inc. Edmonton, Alberta, Canada. Division of Surgical Oncology, Department of Surgery, University of California in Los Angeles (UCLA), USA. Division of Surgical Oncology, Department of Surgery and Department of Microbiology, Immunology and Molecular Genetics; The Molecular Biology Institute; Jonsson Comprehensive Cancer Center, University of California, Los Angeles (UCLA), California, USA. AIT Strategies, Franconia, New Hampshire, USA. Allergy and Immunology Division, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska, USA. Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA – sequence: 18 givenname: Tracy R. surname: Daniels-Wells fullname: Daniels-Wells, Tracy R. organization: The Eppley Institute for Research in Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, Nebraska, USA. OncoQuest Pharmaceuticals Inc. Edmonton, Alberta, Canada. Division of Surgical Oncology, Department of Surgery, University of California in Los Angeles (UCLA), USA. Division of Surgical Oncology, Department of Surgery and Department of Microbiology, Immunology and Molecular Genetics; The Molecular Biology Institute; Jonsson Comprehensive Cancer Center, University of California, Los Angeles (UCLA), California, USA. AIT Strategies, Franconia, New Hampshire, USA. Allergy and Immunology Division, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska, USA. 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Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA – sequence: 20 givenname: Christopher F. surname: Nicodemus fullname: Nicodemus, Christopher F. organization: The Eppley Institute for Research in Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, Nebraska, USA. OncoQuest Pharmaceuticals Inc. Edmonton, Alberta, Canada. Division of Surgical Oncology, Department of Surgery, University of California in Los Angeles (UCLA), USA. Division of Surgical Oncology, Department of Surgery and Department of Microbiology, Immunology and Molecular Genetics; The Molecular Biology Institute; Jonsson Comprehensive Cancer Center, University of California, Los Angeles (UCLA), California, USA. AIT Strategies, Franconia, New Hampshire, USA. Allergy and Immunology Division, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska, USA. Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA – sequence: 21 givenname: Jill A. surname: Poole fullname: Poole, Jill A. organization: The Eppley Institute for Research in Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, Nebraska, USA. OncoQuest Pharmaceuticals Inc. Edmonton, Alberta, Canada. Division of Surgical Oncology, Department of Surgery, University of California in Los Angeles (UCLA), USA. Division of Surgical Oncology, Department of Surgery and Department of Microbiology, Immunology and Molecular Genetics; The Molecular Biology Institute; Jonsson Comprehensive Cancer Center, University of California, Los Angeles (UCLA), California, USA. AIT Strategies, Franconia, New Hampshire, USA. Allergy and Immunology Division, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska, USA. Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA – sequence: 22 givenname: Elizabeth M. surname: Jaffee fullname: Jaffee, Elizabeth M. organization: The Eppley Institute for Research in Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, Nebraska, USA. OncoQuest Pharmaceuticals Inc. Edmonton, Alberta, Canada. Division of Surgical Oncology, Department of Surgery, University of California in Los Angeles (UCLA), USA. Division of Surgical Oncology, Department of Surgery and Department of Microbiology, Immunology and Molecular Genetics; The Molecular Biology Institute; Jonsson Comprehensive Cancer Center, University of California, Los Angeles (UCLA), California, USA. AIT Strategies, Franconia, New Hampshire, USA. Allergy and Immunology Division, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska, USA. Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA – sequence: 23 givenname: Michael A. surname: Hollingsworth fullname: Hollingsworth, Michael A. organization: The Eppley Institute for Research in Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, Nebraska, USA. OncoQuest Pharmaceuticals Inc. Edmonton, Alberta, Canada. Division of Surgical Oncology, Department of Surgery, University of California in Los Angeles (UCLA), USA. Division of Surgical Oncology, Department of Surgery and Department of Microbiology, Immunology and Molecular Genetics; The Molecular Biology Institute; Jonsson Comprehensive Cancer Center, University of California, Los Angeles (UCLA), California, USA. AIT Strategies, Franconia, New Hampshire, USA. Allergy and Immunology Division, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska, USA. Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA – sequence: 24 givenname: Kamiya surname: Mehla fullname: Mehla, Kamiya email: kamiya.mehla@unmc.edu organization: The Eppley Institute for Research in Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, Nebraska, USA. OncoQuest Pharmaceuticals Inc. Edmonton, Alberta, Canada. Division of Surgical Oncology, Department of Surgery, University of California in Los Angeles (UCLA), USA. Division of Surgical Oncology, Department of Surgery and Department of Microbiology, Immunology and Molecular Genetics; The Molecular Biology Institute; Jonsson Comprehensive Cancer Center, University of California, Los Angeles (UCLA), California, USA. AIT Strategies, Franconia, New Hampshire, USA. Allergy and Immunology Division, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, Nebraska, USA. Bloomberg–Kimmel Institute for Cancer Immunotherapy, Johns Hopkins University School of Medicine, Baltimore MD, USA |
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| Notes | Authors’ contributions S. D. Markov: Investigation, formal analysis, data curation, methodology, writing-editing. T. C. Caffrey: Methodology, data curation, investigation, formal analysis and editing. K. A. O’Connell: Data curation, investigation and management of mice samples. J. A. Grunkemeyer: Investigation and management of mice samples. S. Shin: Investigation and data curation. R. Hanson: Data curation and formal analysis. P. P. Patil: Investigation and data curation. S. K. Shukla: Investigation and data curation. D. V. Gonzalez: Investigation and data curation. A. J. Crawford: Data curation. K. E. Vance: Data curation. Y. Huang: Investigation. K. C. Eberle: Management of human samples. P. Radhakrishnan: Investigation and writing-review-editing. P. M. Grandgenett: Resources and funding. P. K. Singh: Resources, supervision, funding and writing-review-editing. R. Madiyalakan: Conceptualization, resources and writing-review-editing. T. R. Daniels-Wells: Writing-review-editing. M. L. Penichet: Writing-review-editing. C. F. Nicodemus: Conceptualization and writing-review-editing. J. A. Poole: Funding, resources, methodology and writing-review-editing E. M. Jaffee: Conceptualization, and writing-review-editing. M. A. Hollingsworth: Conceptualization, Supervision, funding, resources and writing-review-editing. K. Mehla: Conceptualization, supervision, funding, investigation, methodology, formal analysis, writing original draft, and writing-review-editing. |
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| Snippet | Pancreatic ductal adenocarcinoma (PDAC) represents 3% of all cancer cases and 7% of all cancer deaths in the United States. Late diagnosis and inadequate... |
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| Title | IgE-based therapeutic combination enhances anti-tumor response in preclinical models of pancreatic cancer |
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