DHODH is an independent prognostic marker and potent therapeutic target in neuroblastoma

被引:15
作者
Olsen, Thale Kristin [1 ,2 ]
Dyberg, Cecilia [1 ]
Embaie, Bethel Tesfai [1 ]
Alchahin, Adele [1 ]
Milosevic, Jelena [3 ]
Ding, Jane [4 ]
Otte, Jorg [1 ]
Tummler, Conny [1 ]
Myrberg, Ida Hed [1 ]
Westerhout, Ellen M. [5 ]
Koster, Jan [5 ]
Versteeg, Rogier [5 ]
Ding, Han-Fei [4 ]
Kogner, Per [1 ]
Johnsen, John Inge [1 ]
Sykes, David B. [3 ,6 ]
Baryawno, Ninib [1 ]
机构
[1] Karolinska Inst, Dept Womens & Childrens Hlth, Div Pediat Oncol & Pediat Surg, Stockholm, Sweden
[2] Uppsala Univ, Dept Immunol Genet & Pathol, Uppsala, Sweden
[3] Massachusetts Gen Hosp, Ctr Regenerat Med, Boston, MA 02114 USA
[4] Univ Alabama Birmingham, Dept Pathol, Div Mol & Cellular Pathol, Heersink Sch Med, Birmingham, AL 35294 USA
[5] Univ Amsterdam, Dept Oncogen, Amsterdam UMC, Amsterdam, Netherlands
[6] Harvard Stem Cell Inst, Cambridge, MA USA
关键词
MULTICENTER PHASE-II; BREQUINAR SODIUM; CELL; DIFFERENTIATION; MYC; METABOLISM; EXPRESSION; LANDSCAPE; PROGRESS; TRIAL;
D O I
10.1172/jci.insight.153836
中图分类号
R-3 [医学研究方法]; R3 [基础医学];
学科分类号
1001 ;
摘要
Despite intensive therapy, children with high-risk neuroblastoma are at risk of treatment failure. We applied a multiomic system approach to evaluate metabolic vulnerabilities in human neuroblastoma. We combined metabolomics, CRISPR screening, and transcriptomic data across more than 700 solid tumor cell lines and identified dihydroorotate dehydrogenase (DHODH), a critical enzyme in pyrimidine synthesis, as a potential treatment target. Of note, DHODH inhibition is currently under clinical investigation in patients with hematologic malignancies. In neuroblastoma, DHODH expression was identified as an independent risk factor for aggressive disease, and high DHODH levels correlated to worse overall and event-free survival. A subset of tumors with the highest DHODH expression was associated with a dismal prognosis, with a 5-year survival of less than 10%. In xenograft and transgenic neuroblastoma mouse models treated with the DHODH inhibitor brequinar, tumor growth was dramatically reduced, and survival was extended. Furthermore, brequinar treatment was shown to reduce the expression of MYC targets in 3 neuroblastoma models in vivo. A combination of brequinar and temozolomide was curative in the majority of transgenic TH-MYCN neuroblastoma mice, indicating a highly active clinical combination therapy. Overall, DHODH inhibition combined with temozolomide has therapeutic potential in neuroblastoma, and we propose this combination for clinical testing.
引用
收藏
页数:19
相关论文
共 58 条
[21]   Inhibition of the de novo pyrimidine biosynthesis pathway limits ribosomal RNA transcription causing nucleolar stress in glioblastoma cells [J].
Lafita-Navarro, M. Carmen ;
Venkateswaran, Niranjan ;
Kilgore, Jessica A. ;
Kanji, Suman ;
Han, Jungsoo ;
Barnes, Spencer ;
Williams, Noelle S. ;
Buszczak, Michael ;
Burma, Sandeep ;
Conacci-Sorrell, Maralice .
PLOS GENETICS, 2020, 16 (11)
[22]   The landscape of cancer cell line metabolism [J].
Li, Haoxin ;
Ning, Shaoyang ;
Ghandi, Mahmoud ;
Kryukov, Gregory V. ;
Gopal, Shuba ;
Deik, Amy ;
Souza, Amanda ;
Pierce, Kerry ;
Keskula, Paula ;
Hernandez, Desiree ;
Ann, Julie ;
Shkoza, Dojna ;
Apfel, Verena ;
Zou, Yilong ;
Vazquez, Francisca ;
Barretina, Jordi ;
Pagliarini, Raymond A. ;
Galli, Giorgio G. ;
Root, David E. ;
Hahn, William C. ;
Tsherniak, Aviad ;
Giannakis, Marios ;
Schreiber, Stuart L. ;
Clish, Clary B. ;
Garraway, Levi A. ;
Sellers, William R. .
NATURE MEDICINE, 2019, 25 (05) :850-+
[23]   Identification of DHODH as a therapeutic target in small cell lung cancer [J].
Li, Leanne ;
Ng, Sheng Rong ;
Colon, Caterina I. ;
Drapkin, Benjamin J. ;
Hsu, Peggy P. ;
Li, Zhaoqi ;
Nabel, Christopher S. ;
Lewis, Caroline A. ;
Romero, Rodrigo ;
Mercer, Kim L. ;
Bhutkar, Arjun ;
Phat, Sarah ;
Myers, David T. ;
Muzumdar, Mandar Deepak ;
Westcott, Peter M. K. ;
Beytagh, Mary Clare ;
Farago, Anna F. ;
Vander Heiden, Matthew G. ;
Dyson, Nicholas J. ;
Jacks, Tyler .
SCIENCE TRANSLATIONAL MEDICINE, 2019, 11 (517)
[24]   Molecular signatures database (MSigDB) 3.0 [J].
Liberzon, Arthur ;
Subramanian, Aravind ;
Pinchback, Reid ;
Thorvaldsdottir, Helga ;
Tamayo, Pablo ;
Mesirov, Jill P. .
BIOINFORMATICS, 2011, 27 (12) :1739-1740
[25]   Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 [J].
Love, Michael I. ;
Huber, Wolfgang ;
Anders, Simon .
GENOME BIOLOGY, 2014, 15 (12)
[26]   The MYCN oncoprotein as a drug development target [J].
Lu, XH ;
Pearson, A ;
Lunec, J .
CANCER LETTERS, 2003, 197 (1-2) :125-130
[27]   DHODH-mediated ferroptosis defence is a targetable vulnerability in cancer [J].
Mao, Chao ;
Liu, Xiaoguang ;
Zhang, Yilei ;
Lei, Guang ;
Yan, Yuelong ;
Lee, Hyemin ;
Koppula, Pranavi ;
Wu, Shiqi ;
Zhuang, Li ;
Fang, Bingliang ;
Poyurovsky, Masha V. ;
Olszewski, Kellen ;
Gan, Boyi .
NATURE, 2021, 593 (7860) :586-+
[28]   Medical Progress: Recent Advances in Neuroblastoma. [J].
Maris, John M. .
NEW ENGLAND JOURNAL OF MEDICINE, 2010, 362 (23) :2202-2211
[29]   MULTICENTER PHASE-II STUDY OF BREQUINAR SODIUM IN PATIENTS WITH ADVANCED LUNG-CANCER [J].
MAROUN, J ;
RUCKDESCHEL, J ;
NATALE, R ;
MORGAN, R ;
DALLAIRE, B ;
SISK, R ;
GYVES, J .
CANCER CHEMOTHERAPY AND PHARMACOLOGY, 1993, 32 (01) :64-66
[30]   PTEN Regulates Glutamine Flux to Pyrimidine Synthesis and Sensitivity to Dihydroorotate Dehydrogenase Inhibition [J].
Mathur, Deepti ;
Stratikopoulos, Elias ;
Ozturk, Sait ;
Steinbach, Nicole ;
Pegno, Sarah ;
Schoenfeld, Sarah ;
Yong, Raymund ;
Murty, Vundavalli V. ;
Asara, John M. ;
Cantley, Lewis C. ;
Parsons, Ramon .
CANCER DISCOVERY, 2017, 7 (04) :380-390