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PMID: 19047152 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

ODC1 is a critical determinant of MYCN oncogenesis and a therapeutic target in neuroblastoma.

Cancer research ·Vol. 68 ·No. 23 ·2008-12-01 ·Pages 9735-45

Hogarty MD, Norris MD, Davis K, Liu X, Evageliou NF, Hayes CS, Pawel B, Guo R, Zhao H, Sekyere E, Keating J, Thomas W, Cheng NC, Murray J, Smith J, Sutton R, Venn N, London WB, Buxton A, Gilmour SK, Marshall GM, Haber M

Abstract

Neuroblastoma is a frequently lethal childhood tumor in which MYC gene deregulation, commonly as MYCN amplification, portends poor outcome. Identifying the requisite biopathways downstream of MYC may provide therapeutic opportunities. We used transcriptome analyses to show that MYCN-amplified neuroblastomas have coordinately deregulated myriad polyamine enzymes (including ODC1, SRM, SMS, AMD1, OAZ2, and SMOX) to enhance polyamine biosynthesis. High-risk tumors without MYCN amplification also overexpress ODC1, the rate-limiting enzyme in polyamine biosynthesis, when compared with lower-risk tumors, suggesting that this pathway may be pivotal. Indeed, elevated ODC1 (independent of MYCN amplification) was associated with reduced survival in a large independent neuroblastoma cohort. As polyamines are essential for cell survival and linked to cancer progression, we studied polyamine antagonism to test for metabolic dependence on this pathway in neuroblastoma. The Odc inhibitor alpha-difluoromethylornithine (DFMO) inhibited neuroblast proliferation in vitro and suppressed oncogenesis in vivo. DFMO treatment of neuroblastoma-prone genetically engineered mice (TH-MYCN) extended tumor latency and survival in homozygous mice and prevented oncogenesis in hemizygous mice. In the latter, transient Odc ablation permanently prevented tumor onset consistent with a time-limited window for embryonal tumor initiation. Importantly, we show that DFMO augments antitumor efficacy of conventional cytotoxics in vivo. This work implicates polyamine biosynthesis as an arbiter of MYCN oncogenesis and shows initial efficacy for polyamine depletion strategies in neuroblastoma, a strategy that may have utility for this and other MYC-driven embryonal tumors.

MeSH Terms
Animals Antineoplastic Combined Chemotherapy Protocols/pharmacology Biogenic Polyamines/biosynthesis Cell Growth Processes/physiology Cell Line, Tumor Child Cisplatin/administration & dosage,pharmacology Comparative Genomic Hybridization Drug Synergism Eflornithine/administration & dosage,pharmacology Gene Amplification Gene Expression Profiling Genes, myc Humans Mice Mice, Transgenic N-Myc Proto-Oncogene Protein Neuroblastoma/drug therapy,enzymology,genetics,metabolism Nuclear Proteins/genetics Oncogene Proteins/genetics Ornithine Decarboxylase/biosynthesis,genetics
Chemicals
Biogenic Polyamines MYCN protein, human N-Myc Proto-Oncogene Protein Nuclear Proteins Oncogene Proteins Ornithine Decarboxylase Cisplatin Eflornithine
Authors & Affiliations
22 authors, click to expand affiliations / ORCID
Hogarty Michael D
Division of Oncology, The Children's Hospital of Philadelphia, Department of Pediatrics, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-4318, USA. hogartym@email.chop.edu
Norris Murray D
Davis Kimberly
Liu Xueyuan
Evageliou Nicholas F
Hayes Candace S
Pawel Bruce
Guo Rong
Zhao Huaqing
Sekyere Eric
Keating Joanna
Thomas Wayne
Cheng Ngan Ching
Murray Jayne
Smith Janice
Sutton Rosemary
Venn Nicola
London Wendy B
Buxton Allen
Gilmour Susan K
Marshall Glenn M
Haber Michelle
References (46)
46 references, click to expand
  1. Regulation of S-adenosylmethionine decarboxylase activity in rat liver and prostate.
    J Biol Chem. 1985 Aug 15;260(17):9583-8 PMID: 3926770
  2. Effects of MYCN antisense oligonucleotide administration on tumorigenesis in a murine model of neuroblastoma.
    J Natl Cancer Inst. 2003 Sep 17;95(18):1394-403 PMID: 13130115
  3. Mechanisms of embryonal tumor initiation: distinct roles for MycN expression and MYCN amplification.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12664-9 PMID: 15314226
  4. Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas.
    N Engl J Med. 1985 Oct 31;313(18):1111-6 PMID: 4047115
  5. Association of high-level MRP1 expression with poor clinical outcome in a large prospective study of primary neuroblastoma.
    J Clin Oncol. 2006 Apr 1;24(10):1546-53 PMID: 16575006
  6. Targeted expression of MYCN causes neuroblastoma in transgenic mice.
    EMBO J. 1997 Jun 2;16(11):2985-95 PMID: 9214616
  7. Integrative genomics identifies distinct molecular classes of neuroblastoma and shows that multiple genes are targeted by regional alterations in DNA copy number.
    Cancer Res. 2006 Jun 15;66(12):6050-62 PMID: 16778177
  8. Development of difluoromethylornithine (DFMO) as a chemoprevention agent.
    Clin Cancer Res. 1999 May;5(5):945-51 PMID: 10353725
  9. Malignant progression and blockade of angiogenesis in a murine transgenic model of neuroblastoma.
    Cancer Res. 2007 Oct 1;67(19):9435-42 PMID: 17909053
  10. 1-Mb resolution array-based comparative genomic hybridization using a BAC clone set optimized for cancer gene analysis.
    Genome Res. 2004 Jan;14(1):179-87 PMID: 14672980
  11. High-risk neuroblastoma treated with tandem autologous peripheral-blood stem cell-supported transplantation: long-term survival update.
    J Clin Oncol. 2006 Jun 20;24(18):2891-6 PMID: 16782928
  12. Coordinate changes of polyamine metabolism regulatory proteins during the cell cycle of normal human dermal fibroblasts.
    FEBS Lett. 1999 Mar 5;446(1):18-22 PMID: 10100606
  13. Expression of a MYCN-interacting isoform of the tumor suppressor BIN1 is reduced in neuroblastomas with unfavorable biological features.
    Clin Cancer Res. 2003 Aug 15;9(9):3345-55 PMID: 12960121
  14. Polyamines and cancer: old molecules, new understanding.
    Nat Rev Cancer. 2004 Oct;4(10):781-92 PMID: 15510159
  15. Prolonged N-myc protein half-life in a neuroblastoma cell line lacking N-myc amplification.
    Oncogene. 1990 Dec;5(12):1821-7 PMID: 2284101
  16. Neuroblastomas have distinct genomic DNA profiles that predict clinical phenotype and regional gene expression.
    Genes Chromosomes Cancer. 2007 Oct;46(10):936-49 PMID: 17647283
  17. Coamplification of DDX1 correlates with an improved survival probability in children with MYCN-amplified human neuroblastoma.
    J Clin Oncol. 2004 Jul 1;22(13):2681-90 PMID: 15226335
  18. Transposition and amplification of oncogene-related sequences in human neuroblastomas.
    Cell. 1983 Dec;35(2 Pt 1):359-67 PMID: 6197179
  19. Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage.
    Science. 1984 Jun 8;224(4653):1121-4 PMID: 6719137
  20. Ornithine decarboxylase activity is critical for cell transformation.
    Nature. 1992 Nov 26;360(6402):355-8 PMID: 1280331
  21. The ornithine decarboxylase gene is a transcriptional target of c-Myc.
    Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7804-8 PMID: 8356088
  22. Constitutively elevated levels of ornithine and polyamines in mouse epidermal papillomas.
    Carcinogenesis. 1991 Sep;12(9):1619-25 PMID: 1909938
  23. Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases.
    Nat Rev Drug Discov. 2007 May;6(5):373-90 PMID: 17464296
  24. A large scale genetic analysis of c-Myc-regulated gene expression patterns.
    J Biol Chem. 2003 Apr 4;278(14):12563-73 PMID: 12529326
  25. MYCN expression is not prognostic of adverse outcome in advanced-stage neuroblastoma with nonamplified MYCN.
    J Clin Oncol. 2000 Nov 1;18(21):3604-13 PMID: 11054433
  26. Generation of patterns from gene expression data by assigning confidence to differentially expressed genes.
    Bioinformatics. 2000 Aug;16(8):685-98 PMID: 11099255
  27. Myc targets Cks1 to provoke the suppression of p27Kip1, proliferation and lymphomagenesis.
    EMBO J. 2007 May 16;26(10):2562-74 PMID: 17464290
  28. Immunocytochemical detection of ornithine decarboxylase.
    J Histochem Cytochem. 1999 Nov;47(11):1395-404 PMID: 10544213
  29. High-resolution detection and mapping of genomic DNA alterations in neuroblastoma.
    Genes Chromosomes Cancer. 2005 Aug;43(4):390-403 PMID: 15892104
  30. Targeting ornithine decarboxylase in Myc-induced lymphomagenesis prevents tumor formation.
    Cancer Cell. 2005 May;7(5):433-44 PMID: 15894264
  31. Polyamine metabolism and its importance in neoplastic growth and a target for chemotherapy.
    Cancer Res. 1988 Feb 15;48(4):759-74 PMID: 3123052
  32. Dynamic monitoring of cytotoxicity on microelectronic sensors.
    Chem Res Toxicol. 2005 Feb;18(2):154-61 PMID: 15720119
  33. Evidence for an age cutoff greater than 365 days for neuroblastoma risk group stratification in the Children's Oncology Group.
    J Clin Oncol. 2005 Sep 20;23(27):6459-65 PMID: 16116153
  34. Deregulated Wnt/beta-catenin program in high-risk neuroblastomas without MYCN amplification.
    Oncogene. 2008 Feb 28;27(10):1478-88 PMID: 17724465
  35. Emerging concepts in targeting the polyamine metabolic pathway in epithelial cancer chemoprevention and chemotherapy.
    J Biochem. 2006 Jan;139(1):27-33 PMID: 16428316
  36. Inhibition of ornithine decarboxylase (ODC) decreases tumor vascularization and reverses spontaneous tumors in ODC/Ras transgenic mice.
    Cancer Res. 2000 Oct 15;60(20):5696-703 PMID: 11059762
  37. Transcriptional regulation and transformation by Myc proteins.
    Nat Rev Mol Cell Biol. 2005 Aug;6(8):635-45 PMID: 16064138
  38. Platinum drug effects on the expression of genes in the polyamine pathway: time-course and concentration-effect analysis based on Affymetrix gene expression profiling of A2780 ovarian carcinoma cells.
    Cancer Chemother Pharmacol. 2007 May;59(6):711-23 PMID: 17021820
  39. Genome-wide array CGH analysis of murine neuroblastoma reveals distinct genomic aberrations which parallel those in human tumors.
    Cancer Res. 2003 Sep 1;63(17):5266-73 PMID: 14500357
  40. Key role for p27Kip1, retinoblastoma protein Rb, and MYCN in polyamine inhibitor-induced G1 cell cycle arrest in MYCN-amplified human neuroblastoma cells.
    Oncogene. 2005 Aug 25;24(36):5606-18 PMID: 16007177
  41. Homozygous deletion of CDKN2A (p16INK4a/p14ARF) but not within 1p36 or at other tumor suppressor loci in neuroblastoma.
    Cancer Res. 2001 Jan 15;61(2):679-86 PMID: 11212268
  42. Analysis of genomic targets reveals complex functions of MYC.
    Nat Rev Cancer. 2004 Jul;4(7):562-8 PMID: 15229481
  43. Neuroblastoma.
    Lancet. 2007 Jun 23;369(9579):2106-20 PMID: 17586306
  44. Biologic variables in the outcome of stages I and II neuroblastoma treated with surgery as primary therapy: a children's cancer group study.
    J Clin Oncol. 2000 Jan;18(1):18-26 PMID: 10623689
  45. N-myc promotes survival and induces S-phase entry of postmitotic sympathetic neurons.
    J Neurosci. 2002 Feb 1;22(3):815-24 PMID: 11826111
  46. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children's Cancer Group.
    N Engl J Med. 1999 Oct 14;341(16):1165-73 PMID: 10519894
Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2008-12-01
Pages
9735-45
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC2596661
Subset
IM
Grants
NCI NIH HHS · CA97323 · United States
NCI NIH HHS · P01 CA097323 · United States
NCI NIH HHS · R01 CA070739-09 · United States
NCI NIH HHS · CA070739 · United States
NCI NIH HHS · R01 CA070739 · United States
NCI NIH HHS · P01 CA097323-01A10003 · United States
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