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National Cancer Institute National Institutesofhealth U.S Division of Extramural Activities Annual Report 2019 National Cancer Institute U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES National Institutes of Health Immunotoxins for Cancer Therapy With the U.S. Food and Drug Administration (FDA) approval of the immunotoxin moxetumomab pasu- dotox (Lumoxiti) for treatment of drug-resistant hairy cell leukemia (HCL); https://www.fda.gov/drugs/ resources-information-approved-drugs/fda-approves-moxetumomab-pasudotox-tdfk-hairy-cell-leukemia, there is interest in using immunotoxins for treating other cancers.1 (Cover–Figure A) Immunotoxins were developed in the Laboratory of Molecular Biology (LMB), Center for Cancer Research (CCR), NCI, by the team of Drs. Ira Pastan, David Fitzgerald, Bob Kreitman, and Raffit Hassan. Immunotoxins are hybrid proteins composed of an antibody fragment (Fv or Fab) attached to a protein toxin.2 The antibody brings the toxin to the cancer cell, and the toxin enters and kills the cell. (Cover–Figure B) After internalization, the toxin is separated from the antibody by furin and travels through the Golgi to the endoplasmic reticu- lum, where it enters the cytosol and ADP-ribosylates and inactivates elongation factor 2 (EF2). The arrest of protein synthesis leads to apoptosis and cell death.2 This research group uses Pseudomonas exotoxin A (PE) as the toxin moiety and antibodies against CD22 on B cell malignancies or to mesothelin (MSLN) on solid tumors as the targeting moieties. One advantage of using a toxin to kill a cancer cell is that toxins kill cells by inhibiting protein synthesis, a different mechanism of cell killing than cytotoxic drugs used to treat cancer. This property enables immunotoxins to kill drug-resistant cells, such as those found in drug-resistant HCL. One disadvantage is that they induce anti-drug antibodies (ADAs) in patients with normal immune systems, thereby limiting the amount of the drug that can be given. The structure of immunotoxins now in clinical trials is shown on the cover. Lumoxiti binds with high affin- ity to CD22, a protein highly expressed in HCL. The Fv is attached to a 38 kDa fragment of PE. Because CD22 is not expressed on other cell types, Lumoxiti does not damage other organs. In 2018, Lumoxiti was approved by the FDA for the treatment of patients with HCL who failed purine analogue therapies.1 (Cover– Figure C) Lumoxiti was discovered and developed in the LMB, and initial clinical trials were conducted at the NIH. Lumoxiti is licensed to AstraZeneca, which performed the trials necessary for FDA approval. Cur- rently, this research group is conducting studies to determine whether Lumoxiti combined with Rituxan can be used as a first-line therapy so patients might avoid using drugs that damage the bone marrow and enhance the risk of secondary malignancies. LMB-100 is an immunotoxin that targets mesothelin, also discovered by the LMB team, and it is a popular target for antibody-based therapies because it is expressed on about 30 percent of human cancers and not in essential organs3 (Cover–Figures A and D). LMB-100 contains an anti-mesothelin Fab fused to a mutant of PE that is much less immunogenic than PE38. The PE38 payload is useful for leukemia patients with immune dysfunction, because bone marrow damage greatly diminishes the formation of ADAs. In contrast, PE38 is not useful for solid tumor patients with normal immune systems who develop ADAs. Consequently, LMB- 100 induces immunogenic cell death and, when combined with anti-CTLA-4, produced complete tumor regressions and anti-tumor immunity in mice.4 In a recent small study, patients with mesothelioma who received Pembrolizumab following treatment with LMB-100 had major tumor responses.5 (Cover–Figure E) Currently, this combination is being tested in a prospective clinical trial in patients with mesothelioma. References 1. Kreitman R.J. & Pastan I. Contextualizing the use of moxetumomab pasudotox in the treatment of relapsed or refractory hairy cell leukemia. Oncologist. 2020;25(1):e170-e177, doi:10.1634/theoncologist.2019-0370. 2. Alewine C., Hassan R., & Pastan I. Advances in anticancer immunotoxin therapy. Oncologist. 2015;20(2):176-185, doi:10.1634/ theoncologist.2014-0358. 3. Hassan R., et al. Mesothelin immunotherapy for cancer: ready for prime time? J. Clin. Oncol. 2016;34(34):4171-4179, doi:10.1200/JCO.2016.68.3672. 4. Leshem Y., et al. Combining local immunotoxins targeting mesothelin with CTLA-4 blockade synergistically eradicates murine cancer by promoting anticancer immunity. Cancer Immunol. Res. 2017;5(8):685-694, doi:10.1158/2326-6066.CIR-16-0330. 5. Jiang Q., et al. Enhanced efficacy of mesothelin-targeted immunotoxin LMB-100 and anti-PD1 antibody in patients with mesothelioma and mouse tumor models. Sci. Transl. Med. 2020;12(550):eaaz7252, doi:10.1126/scitranslmed.aaz7252. The cover images and narrative are courtesy of Dr. Ira Pastan, co-Chief, Laboratory of Molecular Biology (LMB), NIH Dis- tinguished Investigator, Head, Molecular Biology Section, Center for Cancer Research (CCR), NCI. Division of Extramural Activities Annual Report 2019 National Cancer Institute U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES National Institutes of Health ii NCI DEA 2017 Annual Report Contents Introduction ...................................................................1 Overview of the Division of Extramural Activities ......................................3 Special Activities in the Office of the Director, DEA ....................................4 Program Coordination: A Resource for New Funding Initiatives ............................6 Grant Referral: A First Point of Contact for NCI Grantees and Applications...................7 Peer Review—The Next Step ......................................................9 NCI Grant and RFA Funding .....................................................17 Supporting Peer Review Consultants ...............................................19 DEA’s Role in Advisory Activities ..................................................20 Committee Management Activities.................................................22 Portfolio Tracking and Analysis ....................................................24 Information Resources Management................................................28 Organizational Structure of the Division of Extramural Activities .........................30 Figures ______________________________________________________________________________ Figure 1. Receipt and Referral of NCI Grant Applications, FY2015 – 2019 ...................7 Figure 2. DEA Review Workload, Grants and Contracts Reviewed in FY2015 – 2019 .........10 Figure 3. Program Project (P01), SPORE, and Other Multi-Project Research Applications Reviewed in FY2015 – 2019 ...................................11 Figure 4. Numbers of Career Development (CD) and Training and Education (T&E) Applications Reviewed in FY2015 – 2019 ...................................13 Figure 5. Technology Initiatives Applications Reviewed in FY2015 – 2019 ..................15 Figure 6. NCI Grant and RFA/Cooperative Agreement Funding Percentages by Concept Area, FY2018 ..................................................17 Figure 7. NCI Grant and RFA/Cooperative Agreement Funding Percentages by Concept Area, FY2019 ..................................................18 Figure 8. BSA-Approved RFA/Cooperative Agreement Concept Set-Asides by Division/Office......................................................18 Figure 9. FY2019 Success Rates for Applications in High Incidence Cancer .................26 Figure 10. FY2019 Success Rates for Applications in Selected Special Interest Categories .......27 Tables _______________________________________________________________________________ Table 1a. Requests for Applications (RFAs) Published by the NCI in FY2019, Sorted by Date of Publication .............................................40 Table 1b. Requests for Applications (RFAs) Published by the NCI in FY2019, Sorted by Division, Office, and Center ......................................43 Table 2. NCI Participation in Trans-NIH Requests for Applications (RFAs) in FY2019, Sorted by Date of Publication .............................................46 Table 3a. Program Announcements (PAs) Published by the NCI in FY2019, Sorted by Date of Publication .............................................49 NCI DEA 2019 Annual Report iii Table 3b. Program Announcements (PAs) Published by the NCI in FY2019, Sorted by Division, Office, and Center ......................................52 Table 4. NCI Participation in Trans-NIH Program Announcements (PAs/PARs) in FY2019, Sorted by Date of Publication .............................................55 Table 5. Applications Received for Referral by the NCI/DEA in FY2019, Sorted by Activity Code . .59 Table 6. Grant and Cooperative Agreement Applications Reviewed by the NCI/DEA in FY2019, Sorted by Activity Code . 61 Table 7. Applications Reviewed by NCI IRG Subcommittees and Special Emphasis Panels (SEPs) in FY2019 . 62 Table 8. Summary of Investigator-Initiated P01 Applications Reviewed in FY2019, Sorted by NCAB Meeting ................................................62 Table 9. Summary of Unsolicited P01 Applications Reviewed in FY2019, Sorted by NCI Program Division ..........................................62 Table 10. Requests for Applications (RFAs) Reviewed by the NCI/DEA in FY2019 ...........63 Table 11. Program Announcements (PAs) Reviewed by the NCI/DEA in FY2019.............66 Table 12. SBIR Topics and Requests for Proposals (RFPs) Reviewed by
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