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DEA 2009 Annual Report Contents Foreword Division of Extramural Activities Annual Report 2009 Human Glioblastoma (GBM) GSC GBM Xenograft Patient-Derived Glioma Stem Cells: A Better Model National Cancer Institute Cancer National GSC Neurospheres GBM Differentiation GBM Genomics GBM Drug Screening U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES National Institutes of Health Glioblastoma-Derived Tumor Stem Cells Glioblastoma (GBM) is the most common malignant primary brain tumor and one of the most lethal of all human cancers with a median survival of little more than 14 months. Along with its rapid proliferative capacity, the lethality of GBM is in large part a result of its highly infiltrative nature with individual glioma cells invading deep into surrounding eloquent areas of the brain. Standard glioma xenografts grow as balls within the brain of immunodeficient animals and do not recapitulate the most critical aspect of human GBM biology, making them poor model systems for biological study and testing of new therapies. Not only are new therapies desperately needed in GBM, but also better model systems are needed. Recently a new model of tumor growth, called the cancer stem cell hypothesis, has generated growing interest. This model suggests that tumors actually possess only a small subpopulation of cells with truly tumorigenic potential and that these cells have characteristics similar to that of normal tissue-restricted stem cells. Several years ago, we began a search for such cells in primary patient-derived human GBMs, resulting in a series of observations that we hope will change the way we study these tumors and treat patients with malignant gliomas: • We demonstrated using whole genomic single nucleotide polymorphism (SNP) scanning and gene expression arrays that the standard glioma cell lines that scientists have been studying for more than 20 years do not resemble primary human GBMs at all. In fact, they look more like any other long-established cancer cell line than they do GBMs. Additionally, the few standard glioma cell lines that form tumors in immunodeficient mice are non-invasive and do not recapitulate human GBM histology. Standard glioma cell lines are therefore very poor models for human GBMs (and other gliomas) and raise the concern for the relevance of these cells in studying GBM biology and for screening new therapeutic agents. • We demonstrated that by using novel culturing techniques we could derive a population of cells that had normal neural stem cell (NSC)-like features; however, unlike NSC, these cells also possessed all of the genomic anomalies that the parental human GBM contained, were clonogenic in vitro, and could form highly invasive tumors in vivo that were histologically identical to the original patient’s GBMs. Additionally, these cells and their resultant tumors maintained the unique genomic landscape and had gene expression profiles very similar to the parental tumor. These cells therefore meet the criteria of tumor/glioma stem cells (TSC/GSC) and suggest that GBMs are derived from a population of TSC. Furthermore, glioma TSC represent a much more promising model system for studying human GBM and may help identify novel molecular targets (i.e., stem cell pathways and for screening novel therapeutics). • The CD133 surface marker was widely accepted as a marker for glioma TSCs, but unfortunately this marker is found in only a minority of tumor samples. We demonstrated that the embryonic and early neural stem cell marker CD15 (SSEA-1) allowed us to identify subpopulations of glioma TSC/GSC more efficiently in a significant percentage of tumors that were negative for CD133 cells, therefore allowing the generation of patient-derived glioma TSC/GSC lines from a greater number of patients. • Glioma TSCs from different patients are highly heterogeneous and patient-specific in their biological behavior and genomic/epigenomic landscape, modeling the great heterogeneity seen genomically and clinically in human GBMs. • It can be shown that many glioma TSC/GSC lines can be terminally differentiated along both glial and neuronal lin- eages; however, several glioma TSC/GSC lines are refractory to terminal differentiation. We have identified a subgroup of GBMs that do not terminally differentiate to normal developmental cues secondary to polycomb repressor complex- mediated hypermethylation and subsequent downregulation of the bone-morphogenic protein receptor-1b (BMPR1B). Demethylation of the promoter and subsequent re-expression of the BMPR1b gene by treatment of the TSC with the demethylating agent, 5-azacytidine, induced terminal differentiation of the TSC and tumorigenecity, opening up the possibility of epigenetic-targeted differentiation therapies in patients with GBM. • We have identified connective tissue growth factor (CTGF), through its activation of TrkA, as a potent inducer of glioma cell invasion and demonstrate that reactive astrocytes that surround glioma cells secrete CTGF, establishing a host-derived, pro-invasive microenvironment for glioma invasion. Accordingly, small molecule Trk-A inhibitors potently inhibit glioma cell invasion in vitro and in vivo. Tumor stem cells represent a potential paradigm change in how we think about and study GBMs. Furthermore, the fact that glioma TSC/GSCs appear to represent a much improved and clinically relevant model of primary human GBMs has opened up the door to developing novel therapeutics directed at intrinsic stem cell signaling pathways (i.e., notch, wnt) as well as to such important GBM properties as terminal differentiation (i.e., 5-azacytidine) and invasion (i.e., Trk-A inhibitors) that could not have been appropriately studied or targeted using our old GBM models. References: Lee J, et al. Cancer Cell. 2006;9(5):391-403. Son MJ, et al. Cell Stem Cell. 2009;4(5):440-52. Li A, et al. Mol Cancer Res. 2008;6(1):21-30. Woolard K, Fine HA. Cell Stem Cell. 2009;4(6):466-7. Lee J, et al. Cancer Cell. 2008;13(1):69-80. Fine HA. Cancer Cell. 2009;15(4):247-9. Division of Extramural Activities Annual Report 2009 Human Glioblastoma (GBM) GSC GBM Xenograft Patient-Derived Glioma Stem Cells: A Better Model National Cancer Institute Cancer National GSC Neurospheres GBM Differentiation GBM Genomics GBM Drug Screening Cover Images: The generation of tumor stem cell-derived neurospheres from patient-derived glioblastoma tissue. The neurospheres are transplanted back into immunodeficient mice generating tumor xenografts with the biological, radiographic, and clinical characteristics of the primary human tumor. Neurosphere- derived tumor stem cells can be used to study properties such as tumor cell differentiation and genomics as well as for screening new therapeutic agents. Images and narrative are courtesy of Dr. Howard A. Fine, Neuro-Oncology Branch, National Cancer Institute, NIH. U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES National Institutes of Health ii NCI DEA 2009 Annual Report Contents Foreword . v 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 . 5 Grant Referral: A First Point of Contact for NCI Grant Applicants and Applications . 6 Peer Review—The Next Step . 8 NCI Grant and RFA Funding . 19 American Recovery and Reinvestment Act . 21 Supporting Peer Review Consultants . 23 DEA’s Role in Advisory Activities . 25 Committee Management Activities . 33 Portfolio Tracking and Analysis . 35 Information Resources Management . 36 Organizational Structure of the Division of Extramural Activities . 38 Tables _______________________________________________________________________________ Table 1a. Requests for Applications (RFAs) Published by the NCI in FY2009, Sorted by Date of Publication . 50 Table 1b. Requests for Applications (RFAs) Published by the NCI in FY2009, Sorted by Division, Office, and Center . 51 Table 2. NCI Participation in Trans-NIH Requests for Applications (RFAs) in FY2009, Sorted by Date of Publication . 52 Table 3a. Program Announcements (PAs) Published by the NCI in FY2009, Sorted by Date of Publication . 53 Table 3b. Program Announcements (PAs) Published by the NCI in FY2009, Sorted by Division, Office, and Center . 55 Table 4. NCI Participation in Trans-NIH Program Announcements (PAs) in FY2009, Sorted by Date of Publication . 57 Table 5. Applications Received for Referral by the NCI/DEA in FY2009, Sorted by Mechanism . 59 Table 6. Grant and Cooperative Agreement Applications Reviewed by the NCI/DEA in FY2009, Sorted by Mechanism . 61 Table 7. Applications Reviewed by NCI Initial Review Group (IRG) Subcommittees and Special Emphasis Panels (SEPs) in FY2009 . 62 Table 8. Summary of Investigator-Initiated P01 Applications Reviewed, Sorted by NCAB Meeting, in FY2009 . 63 Table 9. Summary of Investigator-Initiated P01 Applications Reviewed, Sorted by NCI Program Division, in FY2009 . 63 Table 10. Requests for Applications (RFAs) Reviewed by the NCI/DEA in FY2009 . 64 Table 11. Program Announcements (PAs) Reviewed by the NCI/DEA in FY2009 . 66 Table 12. Requests for Proposals (RFPs) Reviewed by the NCI/DEA in FY2009 . 68 Table 13. Summary of NCI Grant Awards by Mechanism in FY2009 . 70 Table 14. Average Total Cost and Number of Research Project Grant Awards Sorted by Division, Office, Center, and Mechanism From FY2005 - FY2009 . 72 Table 15. NCI Organ and Related Site-Specific Dollars for FY2005 - FY2009 – Annual Percent Change . 75 Table 16. NCI Special Interest Category (SIC) Dollars for FY2005 - FY2009 – Annual Percent Change . 77 Table 17. NCI Funding (in Thousands) of Foreign Research Grants in FY2009 . 82 Table 18. Foreign Components of U.S. Domestic Research Grants in FY2009 . 83 Table 19. NCI Participation in Trans-NIH ARRA Requests for Applications (RFAs) in FY2009, Sorted by Date of Publication . 85 Table 20. ARRA Solicited Applications Received for Referral by the NCI/DEA in FY2009, Sorted by Mechanism . 86 NCI DEA 2009 Annual Report iii Table 21. ARRA Solicited Grant and Cooperative Applications Reviewed by the NCI/DEA in FY2009, Sorted by Mechanism . 87 Table 22. ARRA Funding Opportunity Announcements (FOA) Reviewed by the NCI/DEA in FY2009 . 88 Table 23. NCI ARRA Dollars by Anatomical Site for FY2009 .
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