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Trudy G. Oliver

Associate Professor of Oncological Sciences

Huntsman Cancer Institute Endowed Chair in Cancer Research

Cell Response and Regulation co-Leader

Lung Cancer Center co-Leader 

Lung Cancer, Drug Resistance, Mouse Models, Developmental Signaling Pathways, Tumor Progression, Metabolism, Immunology, Transcription Factors

oliver

 

Molecular Biology Program

Education

B.S. Oklahoma Baptist University

Ph.D. Duke University

Postdoctoral Fellowship: Massachusetts Institute of Technology

 

Research

Improving Treatment Options for Patients with Lung Cancer

The Oliver Lab focuses on mechanisms of tumor development, progression, and drug resistance in lung cancer with the goal of improving treatment options for patients with lung cancer.

Lung Cancer: Major Subtypes

Lung cancer is the leading cause of cancer-related death in the United States and is divided into two major subtypes: non-small cell lung cancer (NSCLC) and small cell lung cancer (SCLC). More than 80% of lung cancer patients have NSCLC, which are typically adenocarcinoma, squamous cell carcinoma, or large cell carcinoma.

Approximately 20% of patients have small cell lung cancer (SCLC). SCLC is highly responsive to platinum-based chemotherapy with ~80% response rate, but tumors almost always acquire rapid resistance. There are currently no targeted therapies approved for SCLC patients beyond the recent approval of immunotherapy, which only benefits a small percentage of patients. Drug resistance, both inherent and acquired, is a major problem preventing effective lung cancer treatment.

Personalizing Cancer Therapies

The Oliver Lab is interested in understanding mechanisms of therapeutic response and resistance in order to personalize cancer therapies based on the characteristics of a given tumor. Our approach is to integrate human genomics/sequencing data with mechanistic data gleaned from cell culture systems and sophisticated mouse models of lung cancer.

We use mouse models of lung cancer that closely resemble human lung cancer. Genes that are altered in human lung cancer are altered by genetic engineering in mice, or by lentiviral delivery of genes specifically to the mouse lung. We use bacterial Cre/LoxP systems and CRISPR/Cas9 systems to alter cancer genes in living mice. To monitor the therapeutic response of mouse lung tumors, we use state-of-the-art micro-CT imaging technologies. We also use cancer cell lines, as well as patient-derived xenografts from tumors and circulating tumor cells to probe the function of specific genes and signaling pathways.

Other techniques used in the lab include single-cell sequencing technologies, genomics, biochemistry, molecular and cellular biology, lentiviral technologies and high-throughput drug screening. We have numerous collaborators in the United States and internationally, and we work with pharmaceutical companies to test novel therapies in our mouse models.

Creating novel mouse models of lung cancer

Oliver
Oliver

 

Squamous cell carcinoma (SCC) of the lung is a subtype of NSCLC that leads to ~40,000 deaths each year in the US. To study SCC, we created a genetically-engineered mouse model (GEMM) combining Sox2 overexpression (one of the most frequently amplified genes in SCC) with loss of Lkb1, a regulator of the mTOR pathway (Mukhodpadhyay et al, Cell Reports, 2014). We have now created additional squamous GEMMs and demonstrated their similarity to human lung SCC at the level of biomarker expression, signaling pathway activation, and gene expression (Mollaoglu et al, Immunity, 2018). Our laboratory and others have found that squamous tumors have an altered tumor microenvironment with high infiltration of tumor-associated neutrophils (TANs) and an increase in neutrophil extracellular traps (NETs). In contrast, lung adenocarcinoma, another type of NSCLC driven by different oncogenes, typically display elevated levels of macrophages. These results suggest that the immune microenvironment has a conserved genetic basis, and may be dictated by tumor type-specific oncogenes and/or tumor suppressor genes. To test this hypothesis, we developed multiple new GEMMs to determine the role of lineage-specifiers SOX2 (associated with squamous lung cancer) and NKX2-1 (associated with adenocarcinoma) in the tumor immune microenvironment. SOX2 is highly expressed in lung SCC and largely absent in adenocarcinoma, whereas the converse is true for NKX2-1. We used lentiviral and genetic approaches to overexpress and deplete SOX2 and NKX2-1, respectively, to determine their role in TAN infiltration in vivo. We found that SOX2 is sufficient to recruit TANs and that NKX2-1 represses TAN infiltration. Furthermore, we find that both transcription factors reciprocally regulate neutrophil chemoattractant CXCL5, which is sufficient to recruit TANs, and whose homolog is upregulated in human squamous tumors (Mollaoglu et al, Immunity, 2018). Together, this work has defined how lineage specifiers dictate the tumor immune microenvironment. We are currently studying the functions of pro-tumor TANs in the tumor microenvironment, and testing therapeutic strategies that modulate neutrophil function.

SCLC has molecular subsets with unique therapeutic vulnerabilities

Oliver
Oliver

 

Small cell lung cancer (SCLC) is a highly metastatic neuroendocrine lung tumor, with the worst prognosis among lung cancer subtypes. SCLC has historically been treated as a single disease in the clinic, predominantly with combination chemotherapy and radiation. Patients with SCLC initially respond very well to chemotherapy, but treatment relapse is universal, rapid, and associated with cross-resistance to additional therapies. The vast majority of patients succumb to the disease within two years, which presents an urgency to identify novel therapeutic targets. Our laboratory developed the first GEMM of Myc-driven SCLC (Mollaoglu et al, Cancer Cell, 2017). Rb1/Trp53/Myc (RPM) mice develop highly aggressive metastatic SCLC with an average survival time of six weeks. We found that Myc overexpression is sufficient to drive a unique tumor histopathology called “variant” SCLC and to activate a NEUROD1+ transcriptional program that is not observed in SCLC driven by other MYC family members (i.e. L-Myc and N-Myc). Importantly, we found that Myc-driven SCLC was preferentially sensitive to Aurora kinase inhibition (Mollaoglu et al, Cancer Cell, 2017), which accurately predicted the results of clinical trials (Owonikoko et al, JTO, 2019). This led us to re-investigate SCLC using unbiased approaches in light of these newly-appreciated molecular subsets. Together with collaborators, we found that compared to L-Myc and N-Myc-driven SCLC, Myc-high SCLC is preferentially sensitive to multiple targeted therapies including IMPDH1/2 inhibitors, MCL1 inhibitors, and depletion of extracellular arginine (Huang et al, Cell Metab, 2018; Dammert et al, Nat Comm, 2019; Chalishazar et al, Clin Can Res, 2019). These findings have contributed to a new view of SCLC not as a single disease, but comprising multiple molecular subsets, each with unique therapeutic vulnerabilities (Rudin et al, Nat Rev Can, 2019; Poirier et al, JTO, 2020).

SCLC subsets exhibit remarkable plasticity

Oliver

There are currently four recognized molecular subtypes of SCLC, each expressing a unique lineage-related transcription factor: ASCL1, NEUROD1, YAP1, or POU2F3. Recently, we have investigated what determines SCLC subtype, and we found that it is a combination of cell of origin, genetics, and cell fate plasticity. Using mouse models and human cell lines coupled with single-cell RNA-sequencing (scRNA-seq), we made the unexpected discovery that MYC can convert ASCL1+ SCLC to NEUROD1+ and YAP1+ states in a dynamic fashion (Ireland et al, Cancer Cell, 2020). Mechanistically, we found that MYC activates Notch signaling, a known driver of the neuroendocrine (NE) to non-NE transition (Lim et al, Nature, 2017), to promote SCLC subtype evolution. In addition to cell fate plasticity, we found that tumor genetics are an important determinant of SCLC subtype, because MYCL-associated mouse models only develop ASCL1+ SCLC, whereas MYC-driven tumors also express NEUROD1 and YAP1. Moreover, cell of origin is important as we observed POU2F3+ tumors only in MYC-driven models initiated from an unknown (possibly tuft) cell type, whereas the other three subtypes arose from a neuroendocrine cell of origin.

Our discovery of subtype plasticity in SCLC predicted that individual human tumors harbor cells of not only one, but multiple subtypes. We confirmed this prediction using scRNA-seq on a human SCLC biopsy and by staining for subtype markers in human tissue (Ireland et al, Cancer Cell, 2020). Altogether, these data suggest that SCLC is remarkably heterogeneous and plastic—and due to the unique therapeutic vulnerabilities in each subtype state, we now view SCLC as a moving therapeutic target.

Finally, we have found that chemotherapy-relapsed SCLC has reduced ASCL1 expression (Wagner et al, Nature Commun, 2018), suggesting that subtype dynamics may change during treatment. We genetically deleted ASCL1 in the RPM mouse and surprisingly found that mice no longer develop neuroendocrine tumors, but instead develop bone and cartilage tumors in the lung (Olsen et al, Genes Dev, 2021). Further investigation of these tumors led us to discover that ASCL1 loss leads to a SOX9+ neural crest-stem-like state that we hypothesize precedes bone and cartilage differentiation. Importantly, ASCL1 knockdown in human SCLC cell lines also led to SOX9 induction, suggesting a conserved (likely indirect) mechanism of regulation. Together, these studies reveal SCLC’s remarkable capacity to evolve to new transcriptional states in the face of various pressures.

Oliver
Oliver

 

Current Goals

We are actively working with clinicians to translate our preclinical findings to clinical trials. Many of our ongoing projects seek to understand the key differences between SCLC subtypes at the level of cell differentiation, metabolism, immune microenvironment, and drug resistance. We aim to determine the mechanisms that regulate cell fate plasticity with the goal of constraining plasticity or directing cells toward fates that we can more effectively treat. We also have significant efforts toward identifying mechanisms of chemotherapy resistance in SCLC. Many of our findings have similarities in other cancer types like the childhood brain tumor, medulloblastoma, and in neuroendocrine prostate cancer. Together, these studies will impact diagnostic and therapeutic strategies for lung cancer and ultimately help tailor therapy to the individual patient’s disease.

References

  1. Pe'er D, Ogawa S, Elhanani O, Keren L, Oliver TG, Wedge D. Tumor heterogeneity. Cancer Cell. 2021 Aug 9;39(8):1015-1017. doi: 10.1016/j.ccell.2021.07.009. PubMed PMID: 34375606.
  2. Ciampricotti M, Karakousi T, Richards AL, Quintanal-Villalonga A, Karatza A, Caeser R, Costa EA, Allaj V, Manoj P, Spainhower KB, Kombak FE, Sanchez-Rivera FJ, Jaspers JE, Zavitsanou AM, Maddalo D, Ventura A, Rideout WM, Akama-Garren EH, Jacks T, Donoghue MTA, Sen T, Oliver TG, Poirier JT, Papagiannakopoulos T, Rudin CM. Rlf-Mycl gene fusion drives tumorigenesis and metastasis in a mouse model of small cell lung cancer. Cancer Discov. 2021 Aug 3; doi: 10.1158/2159-8290.CD-21-0441. [Epub ahead of print] PubMed PMID: 34344693; NIHMSID: NIHMS1732053.
  3. Olsen RR, Ireland AS, Kastner DW, Groves SM, Spainhower KB, Pozo K, Kelenis DP, Whitney CP, Guthrie MR, Wait SJ, Soltero D, Witt BL, Quaranta V, Johnson JE, Oliver TG (2021). ASCL1 represses a SOX9+ neural crest stem-like state in small cell lung cancer. Genes Dev, 2021 Jun;35(11-12): 847-869. doi: 10.1101/gad.348295.121. Epub 2021 May 20. PubMed PMID: 34016693; PubMed Central PMCID: PMC8168563.
  4. Huang F, Huffman KE, Wang Z, Wang X, Li K, Cai F, Yang C, Cai L, Shih TS, Zacharias LG, Chung A, Yang Q, Chalishazar MD, Ireland AS, Stewart CA, Cargill K, Girard L, Liu Y, Ni M, Xu J, Wu X, Zhu H, Drapkin B, Byers LA, Oliver TG, Gazdar AF, Minna JD, DeBerardinis RJ (2021). Guanosine triphosphate links MYC-dependent metabolic and ribosome programs in small-cell lung J Clin Invest, 2021 Jan 4;131(1).doi: 10.1172/JCI139929. PubMed PMID: 33079728; PubMed Central PMCID: PMC7773395.
  5. Tsabar M, Mock CS, Venkatachalam V, Reyes J, Karhohs KW, Oliver TG, Regev A, Jambhekar A, Lahav G. A Switch in p53 Dynamics Marks Cells That Escape from DSB-Induced Cell Cycle Arrest. Cell Rep. 2020 Aug 4;32(5):107995. doi: 10.1016/j.celrep.2020.107995. PubMed PMID: 32755587; PubMed Central PMCID: PMC7521664.
  6. Ireland AS, Micinski AM, Kastner DW, Guo B, Wait SJ, Spainhower KB, Conley CC, Chen OS, Guthrie MR, Soltero D, Qiao Y, Huang X, Tarapcsák S, Devarakonda S, Chalishazar MD, Gertz J, Moser JC, Marth G, Puri S, Witt BL, Spike BT, Oliver TG. MYC drives temporal evolution of small cell lung cancer subtypes by reprogramming neuroendocrine fate. Cancer Cell. 2020 Jul 13;38(1):60-78.e12. doi: 10.1016/j.ccell.2020.05.001. Epub 2020 May 30. PubMed PMID: 32473656; PubMed Central PMCID: PMC7393942.
  7. Ireland AS, Oliver TG. Neutrophils create an impeNETrable shield between tumor and cytotoxic immune cells. Immunity. 2020 May 19;52(5):729-731. doi: 10.1016/j.immuni.2020.04.009. PubMed PMID: 32433945; PubMed Central PMCID: PMC7851833.
  8. Poirier JT, George J, Owonikoko TK, Berns A, Brambilla E, Byers LA, Carbone D, Chen HJ, Christensen CL, Dive C, Farago AF, Govindan R, Hann C, Hellmann MD, Horn L, Johnson JE, Ju YS, Kang S, Krasnow M, Lee J, Lee SH, Lehman J, Lok B, Lovly C, MacPherson D, McFadden D, Minna J, Oser M, Park K, Park KS, Pommier Y, Quaranta V, Ready N, Sage J, Scagliotti G, Sos ML, Sutherland KD, Travis WD, Vakoc CR, Wait SJ, Wistuba I, Wong KK, Zhang H, Daigneault J, Wiens J, Rudin CM, Oliver TG. New approaches to small cell lung cancer therapy: From the laboratory to the clinic. J Thorac Oncol. 2020 Apr;15(4):520-540. doi: 10.1016/j.jtho.2020.01.016. Epub 2020 Feb 1. Review. PubMed PMID: 32018053; PubMed Central PMCID: PMC7263769.
  9. Melnikova M, Wauer US, Mendus D, Hilger RA, Oliver TG, Mercer K, Gohlke BO, Erdmann K, Niederacher D, Neubauer H, Buderath P, Wimberger P, Kuhlmann JD, Thomale J. Diphenhydramine increases the therapeutic window for platinum drugs by simultaneously sensitizing tumor cells and protecting normal cells. Mol Oncol. 2020 Apr;14(4):686-703. doi: 10.1002/1878-0261.12648. Epub 2020 Mar 10. PubMed PMID: 32037720; PubMed Central PMCID: PMC7138396.
  10. Stewart CA, Gay CM, Xi Y, Sivajothi S, Sivakamasundari V, Fujimoto J, Bolisetty M, Hartsfield PM, Balasubramaniyan V, Chalishazar MD, Moran C, Kalhor N, Stewart J, Tran H, Swisher SG, Roth JA, Zhang J, de Groot J, Glisson B, Oliver TG, Heymach JV, Wistuba I, Robson P, Wang J, Byers LA. Single-cell analyses reveal increased intratumoral heterogeneity after the onset of therapy resistance in small-cell lung cancer. Nat Cancer. 2020 Apr;1:423-436. doi: 10.1038/s43018-019-0020-z. Epub 2020 Feb 17. PubMed PMID: 33521652; PubMed Central PMCID: PMC7842382. 
  11. Cable J, Finley L, Tu BP, Patti GJ, Oliver TG, Vardhana S, Mana M, Ericksen R, Khare S, DeBerardinis R, Stockwell BR, Edinger A, Haigis M, Kaelin W. Leveraging insights into cancer metabolism-a symposium report. Ann N Y Acad Sci. 2020 Feb;1462(1):5-13. doi: 10.1111/nyas.14274. Epub 2019 Dec 2. PubMed PMID: 31792987;PubMed Central PMCID: PMC7255687.
  12. Chalishazar MD, Wait SJ, Huang F, Ireland AS, Mukhopadhyay A, Lee Y, Schuman SS, Guthrie MR, Berrett KC, Vahrenkamp JM, Hu Z, Kudla M, Modzelewska K, Wang G, Ingolia NT, Gertz J, Lum DH, Cosulich SC, Bomalaski JS, DeBerardinis RJ, Oliver TG. MYC-driven small-cell lung cancer is metabolically distinct and vulnerable to arginine depletion. Clin Cancer Res. 2019 Aug 15;25(16):5107-5121. doi: 10.1158/1078-0432.CCR-18-4140. Epub 2019 Jun 4. PubMed PMID: 31164374; PubMed Central PMCID: PMC6697617.
  13. Dammert MA, Brägelmann J, Olsen RR, Böhm S, Monhasery N, Whitney CP, Chalishazar MD, Tumbrink HL, Guthrie MR, Klein S, Ireland AS, Ryan J, Schmitt A, Marx A, Ozretić L, Castiglione R, Lorenz C, Jachimowicz RD, Wolf E, Thomas RK, Poirier JT, Büttner R, Sen T, Byers LA, Reinhardt HC, Letai A, Oliver TG, Sos ML. MYC paralog-dependent apoptotic priming orchestrates a spectrum of vulnerabilities in small cell lung cancer. Nat Commun. 2019 Aug 2;10(1):3485. doi: 10.1038/s41467-019-11371-x. PubMed PMID: 31375684; PubMed Central PMCID: PMC6677768.
  14. Guo B, Oliver TG. Partners in crime: neutrophil-CTC collusion in metastasis. Trends Immunol. 2019 Jul;40(7):556-559. doi: 10.1016/j.it.2019.04.009. Epub 2019 May 15. PubMed PMID: 31101536; PubMed Central PMCID: PMC6759362.
  15. Rudin CM, Poirier JT, Byers LA, Dive C, Dowlati A, George J, Heymach JV, Johnson JE, Lehman JM, MacPherson D, Massion PP, Minna JD, Oliver TG, Quaranta V, Sage J, Thomas RK, Vakoc CR, Gazdar AF. Molecular subtypes of small cell lung cancer: a synthesis of human and mouse model data. Nat Rev Cancer. 2019 May;19(5):289-297. doi: 10.1038/s41568-019-0133-9. Review. PubMed PMID: 30926931; PubMed Central PMCID: PMC6538259.
  16. Mollaoglu G, Jones A, Wait SJ, Mukhopadhyay A, Jeong S, Arya R, Camolotto SA, Mosbruger TL, Stubben CJ, Conley CJ, Bhutkar A, Vahrenkamp JM, Berrett KC, Cessna MH, Lane TE, Witt BL, Salama ME, Gertz J, Jones KB, Snyder EL, Oliver TG. The lineage-defining transcription factors SOX2 and NKX2-1 determine lung cancer cell fate and shape the tumor immune microenvironment. Immunity. 2018 Oct 16;49(4):764-779.e9. doi: 10.1016/j.immuni.2018.09.020. PubMed PMID: 30332632; PubMed Central PMCID: PMC6197489.
  17. Wagner AH, Devarakonda S, Skidmore ZL, Krysiak K, Ramu A, Trani L, Kunisaki J, Masood A, Waqar SN, Spies NC, Morgensztern D, Waligorski J, Ponce J, Fulton RS, Maggi LB Jr, Weber JD, Watson MA, O'Conor CJ, Ritter JH, Olsen RR, Cheng H, Mukhopadhyay A, Can I, Cessna MH, Oliver TG, Mardis ER, Wilson RK, Griffith M, Griffith OL, Govindan R. Recurrent WNT pathway alterations are frequent in relapsed small cell lung cancer. Nat Commun. 2018 Sep 17;9(1):3787. doi: 10.1038/s41467-018-06162-9. PubMed PMID: 30224629; PubMed Central PMCID: PMC6141466.
  18. Huang F, Ni M, Chalishazar MD, Huffman KE, Kim J, Cai L, Shi X, Cai F, Zacharias LG, Ireland AS, Li K, Gu W, Kaushik AK, Liu X, Gazdar AF, Oliver TG, Minna JD, Hu Z, DeBerardinis RJ. Inosine monophosphate dehydrogenase dependence in a subset of small cell lung cancers. Cell Metab. 2018 Sep 4;28(3):369-382.e5. doi: 10.1016/j.cmet.2018.06.005. Epub 2018 Jun 28. PubMed PMID: 30043754; PubMed Central PMCID: PMC6125205.
  19. Zhang W, Girard L, Zhang YA, Haruki T, Papari-Zareei M, et al. Small cell lung cancer tumors and preclinical models display heterogeneity of neuroendocrine phenotypes. Transl Lung Cancer Res. 2018 Feb;7(1):32-49. PubMed PMID: 29535911; PubMed Central PMCID: PMC5835590.
  20. Cardnell RJ, Li L, Sen T, Bara R, Tong P, et al. Protein expression of TTF1 and cMYC define distinct molecular subgroups of small cell lung cancer with unique vulnerabilities to aurora kinase inhibition, DLL3 targeting, and other targeted therapies. Oncotarget. 2017 Sep 26;8(43):73419-73432. PubMed PMID: 29088717; PubMed Central PMCID: PMC5650272.
  21. Brägelmann J, Böhm S, Guthrie MR, Mollaoglu G, Oliver TG, et al. Family matters: how MYC family oncogenes impact small cell lung cancer. Cell Cycle. 2017 Aug 18;16(16):1489-1498. PubMed PMID: 28737478; PubMed Central PMCID: PMC5584863.
  22. Mollaoglu G, Guthrie MR, Böhm S, Brägelmann J, Can I, et al. MYC drives progression of small cell lung cancer to a variant neuroendocrine subtype with vulnerability to aurora kinase inhibition. Cancer Cell. 2017 Feb 13;31(2):270-285. PubMed PMID: 28089889; PubMed Central PMCID: PMC5310991.
  23. Terry MR, Arya R, Mukhopadhyay A, Berrett KC, Clair PM, et al. Caspase-2 impacts lung tumorigenesis and chemotherapy response in vivo. Cell Death Differ. 2015 May;22(5):719-30. PubMed PMID: 25301067; PubMed Central PMCID: PMC4392070.
  24. Mukhopadhyay A, Oliver TG. Mighty mouse breakthroughs: a Sox2-driven model for squamous cell lung cancer. Mol Cell Oncol. 2015 Apr-Jun;2(2):e969651. PubMed PMID: 27308419; PubMed Central PMCID: PMC4904963.
  25. Oliver TG, Patel J, Akerley W. Squamous non-small cell lung cancer as a distinct clinical entity. Am J Clin Oncol. 2015 Apr;38(2):220-6. PubMed PMID: 25806712.
  26. Masin M, Vazquez J, Rossi S, Groeneveld S, Samson N, et al. GLUT3 is induced during epithelial-mesenchymal transition and promotes tumor cell proliferation in non-small cell lung cancer. Cancer Metab. 2014;2:11. PubMed PMID: 25097756; PubMed Central PMCID: PMC4122054.
  27. Mukhopadhyay A, Berrett KC, Kc U, Clair PM, Pop SM, et al. Sox2 cooperates with Lkb1 loss in a mouse model of squamous cell lung cancer. Cell Rep. 2014 Jul 10;8(1):40-9. PubMed PMID: 24953650; PubMed Central PMCID: PMC4410849.
  28. Curry NL, Mino-Kenudson M, Oliver TG, Yilmaz OH, Yilmaz VO, et al. Pten-null tumors cohabiting the same lung display differential AKT activation and sensitivity to dietary restriction. Cancer Discov. 2013 Aug;3(8):908-21. PubMed PMID: 23719831; PubMed Central PMCID: PMC3743121.
  29. Xue W, Meylan E, Oliver TG, Feldser DM, Winslow MM, et al. Response and resistance to NF-κB inhibitors in mouse models of lung adenocarcinoma. Cancer Discov. 2011 Aug;1(3):236-47. PubMed PMID: 21874163; PubMed Central PMCID: PMC3160630.
  30. Oliver TG, Meylan E, Chang GP, Xue W, Burke JR, et al. Caspase-2-mediated cleavage of Mdm2 creates a p53-induced positive feedback loop. Mol Cell. 2011 Jul 8;43(1):57-71. PubMed PMID: 21726810; PubMed Central PMCID: PMC3160283.
  31. Doles J, Oliver TG, Cameron ER, Hsu G, Jacks T, et al. Suppression of Rev3, the catalytic subunit of Pol{zeta}, sensitizes drug-resistant lung tumors to chemotherapy. Proc Natl Acad Sci U S A. 2010 Nov 30;107(48):20786-91. PubMed PMID: 21068376; PubMed Central PMCID: PMC2996428.
  32. Oliver TG, Mercer KL, Sayles LC, Burke JR, Mendus D, et al. Chronic cisplatin treatment promotes enhanced damage repair and tumor progression in a mouse model of lung cancer. Genes Dev. 2010 Apr 15;24(8):837-52. PubMed PMID: 20395368; PubMed Central PMCID: PMC2854397.
  33. Cowley DO, Rivera-Pérez JA, Schliekelman M, He YJ, Oliver TG, et al. Aurora-A kinase is essential for bipolar spindle formation and early development. Mol Cell Biol. 2009 Feb;29(4):1059-71. PubMed PMID: 19075002; PubMed Central PMCID: PMC2643803.
  34. Schliekelman M, Cowley DO, O'Quinn R, Oliver TG, Lu L, et al. Impaired Bub1 function in vivo compromises tension-dependent checkpoint function leading to aneuploidy and tumorigenesis. Cancer Res. 2009 Jan 1;69(1):45-54. PubMed PMID: 19117986; PubMed Central PMCID: PMC4770788.
  35. Fogarty MP, Emmenegger BA, Grasfeder LL, Oliver TG, Wechsler-Reya RJ. Fibroblast growth factor blocks sonic hedgehog signaling in neuronal precursors and tumor cells. Proc Natl Acad Sci U S A. 2007 Feb 20;104(8):2973-8. PubMed PMID: 17299056; PubMed Central PMCID: PMC1815291.
  36. Oliver TG, Read TA, Kessler JD, Mehmeti A, Wells JF, et al. Loss of patched and disruption of granule cell development in a pre-neoplastic stage of medulloblastoma. Development. 2005 May;132(10):2425-39. PubMed PMID: 15843415.
  37. Oliver TG, Wechsler-Reya RJ. Getting at the root and stem of brain tumors. Neuron. 2004 Jun 24;42(6):885-8. PubMed PMID: 15207233.
  38. Oliver TG, Grasfeder LL, Carroll AL, Kaiser C, Gillingham CL, et al. Transcriptional profiling of the sonic hedgehog response: a critical role for n-myc in proliferation of neuronal precursors. Proc Natl Acad Sci U S A. 2003 Jun 10;100(12):7331-6. PubMed PMID: 12777630; PubMed Central PMCID: PMC165875. 
Last Updated: 9/7/21