Developmental context determines latency of MYC-induced tumorigenesis

PLoS Biology

Volumn 2, Issue 11, 2004, Pages

  Beer, Shelly ^a   Zetterberg, Anders ^b   Ihrie, Rebecca A ^a   McTaggart, Ryan A ^c   Yang, Qiwei ^a   Bradon, Nicole ^a   Arvanitis, Constadina ^a   Attardi, Laura D ^a   Feng, Sandy ^c   Ruebner, Boris ^d   Cardiff, Robert D ^d   Felsher, Dean W ^a  

^a STANFORD UNIVERSITY   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROTEIN P53; TETRACYCLINE; KI 67 ANTIGEN; MYC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DIVISION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DNA REPLICATION; EMBRYO; GENE ACTIVATION; GENE EXPRESSION; GENE OVEREXPRESSION; LATENT PERIOD; LIVER CELL; MITOSIS; MOUSE; NEOPLASM; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE MYC; SOMATIC CELL; TRANSGENE; TRANSGENIC MOUSE; ALLELE; ANIMAL; APOPTOSIS; BIOSYNTHESIS; CANCER INVASION; CANCER TRANSPLANTATION; CELL NUCLEUS; CELL SEPARATION; CYTOLOGY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; HETEROZYGOTE; LIVER; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; NORTHERN BLOTTING; PATHOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

MURINAE; MUS MUSCULUS;

ALLELES; ANIMALS; APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL DIVISION; CELL NUCLEUS; CELL PROLIFERATION; CELL SEPARATION; DNA REPLICATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTES; HETEROZYGOTE; KI-67 ANTIGEN; LIVER; MICE; MICE, SCID; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; NEOPLASMS; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS C-MYC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 20044394527     PISSN: 15449173     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pbio.0020332     Document Type: Article

References (69)

1. Abou-Elella A, Gramlich T, Fritsch C, Gansler T (1996) c-myc amplification in hepatocellular carcinoma predicts unfavorable prognosis. Mod Pathol 9: 95-98.
2. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, et al. (1985) The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533-538.
3. Artandi SE, Chang S, Lee SL, Alson S, Gottlieb GJ, et al. (2000) Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406: 641-645.
4. Blyth K, Stewart M, Bell M, James C, Evan G, et al. (2000) Sensitivity to myc-induced apoptosis is retained in spontaneous and transplanted lymphomas of CD2-mycER mice. Oncogene 19: 773-782.
5. Boige V, Laurent-Puig P, Fouchet P, Flejou JF, Monges G, et al. (1997) Concerted nonsyntenic allelic losses in hyperploid hepatocellular carcinoma as determined by a high-resolution allelotype. Cancer Res 57: 1986-1990.
6. Buetow KH, Murray JC, Israel JL, London WT, Smith M, et al. (1989) Loss of heterozygosity suggests tumor suppressor gene responsible for primary hepatocellular carcinoma. Proc Natl Acad Sci U S A 86: 8852-8856.
7. Bumgardner GL, Matas AJ, Chen S, Cahill D, Cunningham TR, et al. (1990) Comparison of in vivo and in vitro immune response to purified hepatocytes. Transplantation 49: 429-436.
8. Cerni C, Mougneau E, Zerlin M, Julius M, Marcu KB, et al. (1986) c-myc and functionally related oncogenes induce both high rates of sister chromatid exchange and abnormal karyotypes in rat fibroblasts. Curr Top Microbiol Immunol 132: 193-201.
9. Chang MH, Chen PJ, Chen JY, Lai MY, Hsu HC, et al. (1991) Hepatitis B virus integration in hepatitis B virus-related hepatocellular carcinoma in childhood. Hepatology 13: 316-320.
10. Chang MH, Chen CJ, Lai MS, Hsu HM, Wu TC, et al. (1997) Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. Taiwan Childhood Hepatoma Study Group. N Engl J Med 336: 1855-1859.
11. Chernova OB, Chernov MV, Ishizaka Y, Agarwal ML, Stark GR (1998) MYC abrogates p53-mediated cell cycle arrest in N-(phosphonacetyl)-L-aspartate- treated cells, permitting CAD gene amplification. Mol Cell Biol 18: 536-545.
12. Dang CV (1999) c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol Cell Biol 19: 1-11.
13. De Miglio MR, Simile MM, Muroni MR, Pusceddu S, Calvisi D, et al. (1999) Correlation of c-myc overexpression and amplification with progression of preneoplastic liver lesions to malignancy in the poorly susceptible Wistar rat strain. Mol Carcinog 25: 21-29.
14. Dimri GP, Itahana K, Acosta M, Campisi J (2000) Regulation of a senescence checkpoint response by the E2F1 transcription factor and p14 (ARF) tumor suppressor. Mol Cell Biol 20: 273-285.
15. el-Deiry WS (1998) Regulation of p53 downstream genes. Semin Cancer Biol 8: 345-357.
16. Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, et al. (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell 69: 119-128.
17. Felsher DW (2003) Cancer revoked: Oncogenes as therapeutic targets. Nat Rev Cancer 3: 375-380.
18. Felsher DW, Bishop JM (1999a) Transient excess of MYC activity can elicit genomic instability and tumorigenesis. Proc Natl Acad Sci U S A 96: 3940-3944.
19. Felsher DW, Bishop JM (1999b) Reversible tumorigenesis by MYC in hematopoietic lineages. Mol Cell 4: 199-207.
20. Felsher DW, Zetterberg A, Zhu J, Tlsty T, Bishop JM (2000) Overexpression of MYC causes p53-dependent G2 arrest of normal fibroblasts. Proc Natl Acad Sci U S A 97: 10544-10548.
21. Fourel G, Trepo C, Bougueleret L, Henglein B, Ponzetto A, et al. (1990) Frequent activation of N-myc genes by hepadnavirus insertion in woodchuck liver tumours. Nature 347: 294-298.
22. Gandarillas A, Davies D, Blanchard JM (2000) Normal and c-Myc-promoted human keratinocyte differentiation both occur via a novel cell cycle involving cellular growth and endoreplication. Oncogene 19: 3278-3289.
23. Grandori C, Cowley SM, James LP, Eisenman RN (2000) The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu Rev Cell Dev Biol 16: 653-699.
24. Greaves MF (1986) Differentiation-linked leukemogenesis in lymphocytes. Science 234: 697-704.
25. Iritani BM, Eisenman RN (1999) c-Myc enhances protein synthesis and cell size during B lymphocyte development. Proc Natl Acad Sci U S A 96: 13180-13185.
26. Jain M, Arvanitis C, Chu K, Dewey W, Leonhardt E, et al. (2002) Sustained loss of a neoplastic phenotype by brief inactivation of MYC. Science 297: 102-104.
27. Johnston LA, Prober DA, Edgar BA, Eisenman RN, Gallant P (1999) Drosophila myc regulates cellular growth during development. Cell 98: 779-790.
28. Karlsson A, Giuriato S, Tang F, Fung-Weier J, Levan G, et al. (2003) Genomically complex lymphomas undergo sustained tumor regression upon MYC inactivation unless they acquire novel chromosomal translocations. Blood 101: 2797-2803.
29. Kawate S, Fukusato T, Ohwada S, Watanuki A, Morishita Y (1999) Amplification of c-myc in hepatocellular carcinoma: Correlation with clinicopathologic features, proliferative activity and p53 overexpression. Oncology 57: 157-163.
30. Kim S, Li Q, Dang CV, Lee LA (2000) Induction of ribosomal genes and hepatocyte hypertrophy by adenovirus-mediated expression of c-Myc in vivo. Proc Natl Acad Sci U S A 97: 11198-11202.
31. Kistner A, Gossen M, Zimmermann F, Jerecic J, Ullmer C, et al. (1996) Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice. Proc Natl Acad Sci U S A 93: 10933-10938.
32. Klein G, Klein E (1986) Conditioned tumorigenicity of activated oncogenes. Cancer Res 46: 3211-3224.
33. Klocke R, Bartels T, Jennings G, Brand K, Halter R, et al. (2001) Lack of p53 accelerates hepatocarcinogenesis in transgenic mice constitutively overexpressing c-myc in the liver. FASEB J 15: 1404-1406.
34. Kountouras J, Boura P, Lygidakis NJ (2001) Liver regeneration after hepatectomy. Hepatogastroenterology 48: 556-562.
35. Lin AW, Barradas M, Stone JC, van Aelst L, Serrano M, et al. (1998) Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev 12: 3008-3019.
36. Macleod KF, Sherry N, Hannon G, Beach D, Tokino T, et al. (1995) p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev 9: 935-944.
37. Mai S, Hanley-Hyde J, Fluri M (1996) c-Myc overexpression associated DHFR gene amplification in hamster, rat, mouse and human cell lines. Oncogene 12: 277-288.
38. Mateyak MK, Obaya AJ, Adachi S, Sedivy JM (1997) Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Differ 8: 1039-1048.
39. McCormack SJ, Weaver Z, Deming S, Natarajan G, Torri J, et al. (1998) Myc/p53 interactions in transgenic mouse mammary development, tumorigenesis and chromosomal instability. Oncogene 16: 2755-2766.
40. Michalopoulos GK, DeFrances MC (1997) Liver regeneration. Science 276: 60-66.
41. Morgenbesser SD, DePinho RA (1994) Use of transgenic mice to study myc family gene function in normal mammalian development and in cancer. Semin Cancer Biol 5: 21-36.
42. Murakami H, Sanderson ND, Nagy P, Marino PA, Merlino G, et al. (1993) Transgenic mouse model for synergistic effects of nuclear oncogenes and growth factors in tumorigenesis: Interaction of c-myc and transforming growth factor alpha in hepatic oncogenesis. Cancer Res 53: 1719-1723.
43. National Toxicology Program [NTP] (1989) NTP toxicology and carcinogenesis studies of tetracycline hydrochloride (CAS no. 64-75-5) in F344/N rats and B6C3F1 mice (feed studies). Natl Toxicol Program Tech Rep Ser 344: 1-172.
44. Oppedal BR, Glomstein A, Zetterberg A (1988) Feulgen DNA values in Wilms' tumour in relation to prognosis. Pathol Res Pract 183: 756-760.
45. Oster SK, Ho CS, Soucie EL, Penn LZ (2002) The myc oncogene: MarvelouslY complex. Adv Cancer Res 84: 81-154.
46. Pelengaris S, Littlewood T, Khan M, Elia G, Evan G (1999) Reversible activation of c-myc in skin: Induction of a complex neoplastic phenotype by a single oncogenic lesion. Mol Cell 3: 565-577.
47. Pelengaris S, Rudolph B, Littlewood T (2000) Action of Myc in vivo - proliferation and apoptosis. Curr Opin Genet Dev 10: 100-105.
48. Pelengaris S, Khan M, Evan G (2002a) c-Myc: More than just a matter of life and death. Nat Rev Cancer 2: 764-776.
49. Pelengaris S, Khan M, Evan GI (2002b) Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell 109: 321-334.
50. Piao Z, Kim H, Jeon BK, Lee WJ, Park C (1997) Relationship between loss of heterozygosity of tumor suppressor genes and histologic differentiation in hepatocellular carcinoma. Cancer 80: 865-872.
51. Renard CA, Fourel G, Bralet MP, Degott C, A De La Coste A, et al. (2000) Hepatocellular carcinoma in WHV/N-myc2 transgenic mice: Oncogenic mutations of beta-catenin and synergistic effect of p53 null alleles. Oncogene 19: 2678-2686.
52. Sandgren EP, Quaife CJ, Pinkert CA, Palmiter RD, Brinster RL (1989) Oncogene-induced liver neoplasia in transgenic mice. Oncogene 4: 715-724.
53. Santoni-Rugiu E, Jensen MR, Factor VM, Thorgeirsson SS (1999) Acceleration of c-myc-induced hepatocarcinogenesis by co-expression of transforming growth factor (TGF)-alpha in transgenic mice is associated with TGF-beta1 signaling disruption. Am J Pathol 154: 1693-1700.
54. Sargent LM, Sanderson ND, Thorgeirsson SS (1996) Ploidy and karyotypic alterations associated with early events in the development of hepatocarcinogenesis in transgenic mice harboring c-Myc and transforming growth factor alpha transgenes. Cancer Res 56: 2137-2142.
55. Sargent LM, Zhou X, Keck CL, Sanderson ND, Zimonjic DB, et al. (1999) Nonrandom cytogenetic alterations in hepatocellular carcinoma from transgenic mice overexpressing c-myc and transforming growth factoralpha in the liver. Am J Pathol 154: 1047-1055.
56. Schmitt CA, McCurrach ME, de Stanchina E, Wallace-Brodeur RR, Lowe SW (1999) INK4a/ARF mutations accelerate lymphomagenesis and promote chemoresistance by disabling p53. Genes Dev 13: 2670-2677.
57. Seglen PO (1976) Preparation of isolated rat liver cells. Methods Cell Biol 13: 29-83.
58. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602.
59. Sherr CJ (1998) Tumor surveillance via the ARF-p53 pathway. Genes Dev 12: 2984-2991.
60. Spanopoulou E, Early A, Elliott J, Crispe N, Ladyman H, et al. (1989) Complex lymphoid and epithelial thymic tumours in Thy1-myc transgenic mice. Nature 342: 185-189.
61. Thorgeirsson SS, Grisham JW (2002) Molecular pathogenesis of human hepatocellular carcinoma. Nat Genet 31: 339-346.
62. Timme TL, Thompson TC (1994) Rapid allelotype analysis of p53 knockout mice. Biotechniques 17: 460, 462-463.
63. Trumpp A, Refaeli Y, Oskarsson T, Gasser S, Murphy M, et al. (2001) c-Myc regulates mammalian body size by controlling cell number but not cell size. Nature 414: 768-773.
64. Tsuda H, Zhang WD, Shimosato Y, Yokota J, Terada M, et al. (1990) Allele loss on chromosome 16 associated with progression of human hepatocellular carcinoma. Proc Natl Acad Sci U S A 87: 6791-6794.
65. Vogelstein B, Lane D, Levine AJ (2000) Surfing the p53 network. Nature 408: 307-310.
66. Wahl GM, Carr AM (2001) The evolution of diverse biological responses to DNA damage: Insights from yeast and p53. Nat Cell Biol 3: E277-E286.
67. Weiss WA, Burns MJ, Hackett C, Aldape K, Hill JR, et al. (2003) Genetic determinants of malignancy in a mouse model for oligodendroglioma. Cancer Res 63: 1589-1595.
68. Zhu J, Woods D, McMahon M, Bishop JM (1998) Senescence of human fibroblasts induced by oncogenic Raf. Genes Dev 12: 2997-3007.
69. Zindy F, Eischen CM, Randle DH, Kamijo T, Cleveland JL, et al. (1998) Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev 12: 2424-2433.