Aneuploidy-induced delaminating cells drive tumorigenesis in Drosophila epithelia

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 50, 2012, Pages 20549-20554

  Dekanty, Andrés ^a   Barrio, Lara ^a   Muzzopappa, Mariana ^a   Auer, Herbert ^a   Milán, Marco ^a,b  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; STRESS ACTIVATED PROTEIN KINASE; CADHERIN; DROSOPHILA PROTEIN; P53 PROTEIN, DROSOPHILA; SHOTGUN PROTEIN, DROSOPHILA;

ADULT; ANEUPLOIDY; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BASEMENT MEMBRANE; CARCINOGENESIS; CELL POLARITY; CELL POPULATION; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVATION; EPITHELIUM CELL; FEMALE; GENETICS; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; EXPERIMENTAL NEOPLASM; GENOME; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANEUPLOIDY; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CADHERINS; CELL POLARITY; CHROMOSOMAL INSTABILITY; DROSOPHILA; DROSOPHILA PROTEINS; EPITHELIAL CELLS; GENOME, INSECT; HUMANS; MAP KINASE SIGNALING SYSTEM; MODELS, BIOLOGICAL; NEOPLASMS, EXPERIMENTAL; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84874412079     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206675109     Document Type: Article

References (35)

1. von Hansemann D (1890) Ueber asymmetrische Zelltheilung in epithel Krebsen und deren biologische Bedeutung [On the asymmetrical cell division in epithelial cancers and its biological significance]. Virchow’s Arch Path Anat 119:299. German.
2. Boveri T (1914) Zur Frage der Entstehung Maligner Tumoren [Origin of malignant tumors]. (Gustav Fisher, Jena), pp 1–64. German.
3. Negrini S, Gorgoulis VG, Halazonetis TD (2010) Genomic instability — an evolving hallmark of cancer. Nat Rev Mol Cell Biol 11(3):220–228.
4. Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8(5):379–393.
5. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461(7267):1071–1078.
6. Branzei D, Foiani M (2010) Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 11(3):208–219.
7. Castellanos E, Dominguez P, Gonzalez C (2008) Centrosome dysfunction in Drosophila neural stem cells causes tumors that are not due to genome instability. Curr Biol 18(16):1209–1214.
8. Holland AJ, Cleveland DW (2009) Boveri revisited: Chromosomal instability, aneuploidy and tumorigenesis. Nat Rev Mol Cell Biol 10(7):478–487.
9. Li M, et al. (2010) The ATM-p53 pathway suppresses aneuploidy-induced tumorigenesis. Proc Natl Acad Sci USA 107(32):14188–14193.
10. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: The next generation. Cell 144 (5):646–674.
11. Pagliarini RA, Xu T (2003) A genetic screen in Drosophila for metastatic behavior. Science 302(5648):1227–1231.
12. Brumby AM, Richardson HE (2005) Using Drosophila melanogaster to map human cancer pathways. Nat Rev Cancer 5(8):626–639.
13. Davoli T, de Lange T (2011) The causes and consequences of polyploidy in normal development and cancer. Annu Rev Cell Dev Biol 27:585–610.
14. McNamee LM, Brodsky MH (2009) p53-independent apoptosis limits DNA damage-induced aneuploidy. Genetics 182(2):423–435.
15. Burds AA, Lutum AS, Sorger PK (2005) Generating chromosome instability through the simultaneous deletion of Mad2 and p53. Proc Natl Acad Sci USA 102(32): 11296–11301.
16. Thompson SL, Compton DA (2010) Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J Cell Biol 188(3):369–381.
17. Brodsky MH, et al. (2000) Drosophila p53 binds a damage response element at the reaper locus. Cell 101(1):103–113.
18. Uhlirova M, Bohmann D (2006) JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J 25(22):5294–5304.
19. Hay BA, Wolff T, Rubin GM (1994) Expression of baculovirus P35 prevents cell death in Drosophila. Development 120(8):2121–2129.
20. Pacquelet A, Rørth P (2005) Regulatory mechanisms required for DE-cadherin function in cell migration and other types of adhesion. J Cell Biol 170(5):803–812.
21. Srivastava A, Pastor-Pareja JC, Igaki T, Pagliarini R, Xu T (2007) Basement membrane remodeling is essential for Drosophila disc eversion and tumor invasion. Proc Natl Acad Sci USA 104(8):2721–2726.
22. Martín-Blanco E, et al. (1998) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 12(4):557–570.
23. Pérez-Garijo A, Martín FA, Morata G (2004) Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila. Development 131(22):5591–5598.
24. Smith-Bolton RK, Worley MI, Kanda H, Hariharan IK (2009) Regenerative growth in Drosophila imaginal discs is regulated by Wingless and Myc. Dev Cell 16(6):797–809.
25. Ryoo HD, Gorenc T, Steller H (2004) Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev Cell 7(4): 491–501.
26. Schubiger M, Sustar A, Schubiger G (2010) Regeneration and transdetermination: The role of wingless and its regulation. Dev Biol 347(2):315–324.
27. Baker NE (1987) Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: The spatial distribution of a transcript in embryos. EMBO J 6(6): 1765–1773.
28. Warner SJ, Yashiro H, Longmore GD (2010) The Cdc42/Par6/aPKC polarity complex regulates apoptosis-induced compensatory proliferation in epithelia. Curr Biol 20(8): 677–686.
29. Brumby AM, Richardson HE (2003) scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J 22(21):5769–5779.
30. Igaki T, Pagliarini RA, Xu T (2006) Loss of cell polarity drives tumor growth and invasion through JNK activation in Drosophila. Curr Biol 16(11):1139–1146.
31. Igaki T, Pastor-Pareja JC, Aonuma H, Miura M, Xu T (2009) Intrinsic tumor suppression and epithelial maintenance by endocytic activation of Eiger/TNF signaling in Drosophila. Dev Cell 16(3):458–465.
32. Baena-Lopez LA, Franch-Marro X, Vincent JP (2009) Wingless promotes proliferative growth in a gradient-independent manner. Sci Signal 2(91):ra60.
33. Green MM, Shepherd SH (1979) Genetic instability in Drosophila melanogaster: The induction of specific chromosome 2 deletions by MR elements. Genetics 92(3): 823–832.
34. Sheltzer JM, Torres EM, Dunham MJ, Amon A (2012) Transcriptional consequences of aneuploidy. Proc Natl Acad Sci USA 109(31):12644–12649.
35. Torres EM, et al. (2010) Identification of aneuploidy-tolerating mutations. Cell 143(1): 71–83.