Mutation of the gene encoding the ubiquitin activating enzyme uba1 causes tissue overgrowth in Drosophila

Fly

Volumn 1, Issue 2, 2007, Pages 95-105

  Pfleger, Cathie M ^a,b,c   Harvey, Kieran F ^a,b,d   Yan, Hua ^c   Hariharan, Iswar K ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

Compensatory proliferation; E1; Non autonomous overgrowth; Tumor suppressor; Uba1; Ube1; Ubiquitin

Indexed keywords

MAMMALIA;

DROSOPHILA PROTEIN; UBA1 PROTEIN, DROSOPHILA; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ANIMAL; ARTICLE; CELL DEATH; DROSOPHILA MELANOGASTER; EYE; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HELA CELL; HUMAN; MALE; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; CELL DEATH; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; FEMALE; HELA CELLS; HUMANS; MALE; MUTATION; PHENOTYPE; UBIQUITIN; UBIQUITIN-ACTIVATING ENZYMES;

EID: 52949084018     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: 10.4161/fly.4285     Document Type: Article

References (64)

1. Ciechanover A. The ubiquitin-proteasome proteolytic pathway. Cell 1994; 79:13-21.
2. Hochstrasser M. Protein degradation or regulation:Ub the judge. Cell 1996; 84:813-5.
3. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998; 67:425-79.
4. Scheffner M, Nuber U, Huibregtse JM. Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 1995; 373:81-3.
5. Feldman RM, Correll CC, Kaplan KB, Deshaies RJ. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 1997; 91:221-30.
6. Glotzer M, Murray AW, Kirschner MW. Cyclin is degraded by the ubiquitin pathway. Nature 1991; 349:132-7.
7. Hunt T, Luca FC, Ruderman JV. The requirements for protein synthesis and degradation, and the control of destruction of cyclins A and B in the meiotic and mitotic cell cycles of the clam embryo. J Cell Biol 1992; 116:707-24.
8. King RW, Deshaies RJ, Peters J-M, Kirschner MW. How proteolysis drives the cell cycle. Science 1996; 274:1652-59.
9. Sheaff RJ, Roberts JM. End of the line:proteolytic degradation of cyclin-dependent kinase inhibitors. Chem Biol 1996; 3:869-73.
10. Ang XL, Harper JW. Interwoven ubiquitination oscillators and control of cell cycle transitions. Sci STKE 2004; 242:pe31.
11. Sgambato A, Cittadini A, Faraglia B, Weinstein IB. 2000. Multiple functions of p27(Kip1) and its alterations in tumor cells:a review. J Cell Physiol 2000; 183:18-27.
12. Zhang HG, Wang J, Yang X, Hsu HC, Mountz JD. Regulation of apoptosis proteins in cancer cells by ubiquitin. Oncogene 2004; 23:2009-15.
13. Moberg KH, Mukerjee A, Veraksa A, Artavanis-Tsakonas S, Hariharan IK. The Drosophila F box protein Archipelago regulates dMyc protein levels in vivo. Curr Biol 2004; 14:965-74.
14. Secombe J, Pierce SB, Eisenman RN. Myc:a weapon of mass destruction. Cell 2004; 117:153-6.
15. Barnes DM. and Camplejohn RS. P53, apoptosis, and breast cancer. J Mammary Gland Biol Neoplasia 1996; 1:163-75.
16. Freedman DA, Wu L, Levine AJ. Functions of the MDM2 oncoprotein. Cell Mol Life Sci 1999; 55:96-107.
17. Vousden KH, Prives C. P53 and prognosis:new insights and further complexity. Cell 2005; 120:7-10.
18. Trotman LC, Wang X, Alimonti A, Chen Z, Teruya-Feldstein J, Yang H, Pavletich NP, Carver BS, Cordon-Cardo C, Erdjument-Bromage H, Tempst P, Chi SG, Kim HJ, Misteli T, Jiang X, Pandolfi PP. Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 2007; 12:141-56.
19. Moberg KH, Bell DW, Wahrer DC, Haber DA, Hariharan IK. Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature 2001; 413:311-6.
20. Kaelin WG Jr. The von Hippel-Lindau tumor suppressor gene and kidney cancer. Clin Cancer Res 2004; 10:6290s-5s.
21. Ohta T, Fukuda M. Ubiquitin and breast cancer. Oncogene 2004; 23:2079-88.
22. Pham AD, Sauer F. Ubiquitin-activating/conjugating activity of TAFII250, a mediator of activation of gene expression in Drosophila. Science 2000; 289:2357-60.
23. Belz T, Pham AD, Beisel C, Anders N, Bogin J, Kwozynski S, Sauer F. In vitro assays to study protein ubiquitination in transcription. Methods 2002; 26:233-44.
24. Cook JC, Chock PB. Phosphorylation of ubiquitin-activating enzyme in cultured cells. Proc Natl Acad Sci USA 1995; 92:3454-7.
25. Nagai Y, Kaneda S, Nomura K, Yasuda H, Seno T, Yamao F. Ubiquitin-activating enzyme, E1, is phosphorylated in mammalian cells by the protein kinase Cdc2. J Cell Sci 1995; 108:2145-52.
26. Stephen AG, Trausch-Azar JS, Handley-Gearhart PM, Ciechanover A, Schwartz AL. Identification of a region within the ubiquitin-activating enzyme required for nuclear targeting and phosphorylation. J Biol Chem 1997; 272:10895-903.
27. Shang F, Deng G, Obin M, Wu CC, Gong X, Smith D, Laursen RA, Andley UP, Reddan JR, Taylor A. Ubiquitin-activating enzyme (E1) isoforms in lens epithelial cells:origin of translation, E2 specificity and cellular localization determined with novel site-specific antibodies. Exp Eye Res 2001; 73:827-36.
28. Kong SK, Chock PB. Protein ubiquitination is regulated by phosphorylation. An in vitro study. J Biol Chem 1992; 267:14189-92.
29. Berger J, Suzuki T, Senti KA, Stubbs J, Schaffner G, Dickson BJ. Genetic mapping with SNP markers in Drosophila. Nat Genet 2001; 29:475-81.
30. Tapon N, Ito N, Dickson BJ, Treisman JE, Hariharan IK. The Drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation. Cell 2001; 105:345-55.
31. Tapon N, Harvey KF, Bell DW, Wahrer DC, Schiripo TA, Haber DA, Hariharan IK. Salvador Promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 2002; 110:467-78.
32. Harvey KF, Pfleger CM, Hariharan IK. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 2003; 114:457-67.
33. Breitschopf K, Bengal E, Ziv T, Admon A, Ciechanover A. A novel site forubiquitination: the N-terminal residue, and not internal lysines of MyoD, is essential for conjugation and degradation of the protein. EMBO J 1998; 17:5964-73.
34. Kurada P, White K. Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 1998; 95:319-29.
35. Moreno E, Yan M, Basler K. Evolution of TNF signaling mechanisms:JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr Biol 2002; 12:1263-8.
36. Igaki T, Kanda H, Yamamoto-Goto Y, Kanuka H, Kuranaga E, Aigaki T, Miura M. Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J 2002; 21:3009-18.
37. Hay BA, Wassarman DA, Rubin GM. Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 1995; 83:1253-62.
38. Chen P, Nordstrom W, Gish B, Abrams JM. grim, a novel cell death gene in Drosophila. Genes Dev 1996; 10:1773-82.
39. White K, ME Grether, JM Abrams, L Young, K Farrell and H Steller, Genetic control of programmed cell death in Drosophila. Science 1994; 264:677-683.
40. Moberg KH, Schelble S, Burdick SK, Hariharan IK. Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev Cell 2005; 9:699-710.
41. Lee JD, Amanai K, Shearn A, Treisman JE. 2002. The ubiquitin ligase Hyperplastic discs negatively regulates hedgehog and decapentaplegic expression by independent mechanisms. Development 2002; 129:5697-706.
42. Huh, JR, Guo M, Hay B. Compensatory proliferation induced by cell death in the Drosophila wing disc requires activity of the apical cell death caspase Dronc in a nonapoptotic role. Curr Biol 2004; 14:1262-6.
43. Ryoo HD, Gorenc T, Steller H. Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev Cell 2004; 7:491-501.
44. Perez-Garijo A, Martin FA, Struhl G, Morata G. Dpp signaling and the induction of neoplastic tumors by caspase-inhibited apoptotic cells in Drosophila. Proc Natl Acad Sci U S A 2005; 102:17664-9.
45. Pellock BJ, Buff E, White K, Hariharan IK. The Drosophila tumor suppressors Expanded and Merlin differentially regulate cell cycle exit, apoptosis, and Wingless signaling. Dev Biol 2007; 304:102-15.
46. Brumby AM, Richardson HE. scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J 2003; 22:5769-79.
47. Benhaj K, Akcali KC, Ozturk M. Redundant expression of canonical Wnt ligands in human breast cancer cell lines. Oncol Rep 2006; 15:701-7.
48. Brennan KR, Brown AM. Wnt proteins in mammary development and cancer. J Mammary Gland Biol Neoplasia 2004; 9:119-31.
49. Kirikoshi H, Katoh M. Expression and regulation of WNT10B in human cancer:up-regulation of WNT10B in MCF-7 cells by beta-estradiol and down-regulation of WNT10B in NT2 cells by retinoic acid. Int J Mol Med 2002; 10:507-11.
50. Lane TF, Leder P. Wnt-10b directs hypermorphic development and transformation in mammary glands of male and female mice. Oncogene 1997; 15:2133-44.
51. Hardiman G, Kastelein RA, Bazan JF. Isolation, characterization and chromosomal localization of human WNT10B. Cytogenet Cell Genet 1997; 77:278-82.
52. Bafico A, Liu G, Goldin L, Harris V, Aaronson SA. An autocrine mechanism for constitutive Wnt pathway activation in human cancer cells. Cancer Cell 2004; 6:497-506.
53. Li C, Guo B, Bernabeu C, Kumar S. Angiogenesis in breast cancer:the role of transforming growth factor beta and CD105. Microsc Res Tech 2001; 52:437-49.
54. Vejda S, Erlach N, Peter B, Drucker C, Rossmanith W, Pohl J, Schulte-Hermann R, Grusch M. Expression of activins C and E induces apoptosis in human and rat hepatoma cells. Carcinogenesis 2003; 24:1801-9.
55. Herzer K, Ganten TM, Schulze-Bergkamen H, Grosse-Wilde A, Koschny R, Krammer PH, Walczak H. Transforming growth factor beta can mediate apoptosis via the expression of TRAIL in human hepatoma cells. Hepatology 2005; 42:183-92.
56. McGrath JP, Jentsch S, Varshavsky A. UBA 1:an essential yeast gene encoding ubiquitin-activating enzyme. EMBO J 1991; 10:227-36.
57. Finley D, Ciechanover A, Varshavsky A. Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutant ts85. Cell 1984; 37:43-55.
58. Kulka RG, Raboy B, Schuster R, Parag HA, Diamond G, Ciechanover A, Marcus M. A Chinese hamster cell cycle mutant arrested at G2 phase has a temperature-sensitive ubiquitin-activating enzyme, E1. J Biol Chem 1988; 263:15726-31.
59. Ayusawa D, Kaneda S, Itoh Y, Yasuda H, Murakami Y, Sugasawa K, Hanaoka F, Seno T. Complementation by a cloned human ubiquitin-activating enzyme E1 of the S-phase-arrested mouse FM3A cell mutant with thermolabile E1.Cell Struct Funct 1992; 17:113-22.
60. Nishitani H, Goto H, Kaneda S, Yamao F, Seno T, Handley P, Schwartz AL, Nishimoto T. Tsbn75 and tsBN423, temperature-sensitive x-linked mutants of the BHK21 cell line, can be complemented by the ubiquitin-activating enzyme E1 cDNA. Biochem Biophys Res Commun 1992; 184:1015-21.
61. Handley-Gearhart PM, Trausch-Azar JS, Ciechanover A, Schwartz AL. Rescue of the complex temperature-sensitive phenotype of Chinese hamster ovary E36ts20 cells by expression of the human ubiquitin-activating enzyme cDNA. Biochem J 1994; 304:1015-20.
62. Pfleger CM, Kirschner MW. The KEN box:an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev 2000; 14:655-65.
63. Salvat C, Acquaviva A, Scheffner M, Robbins I, Piechaczyk M, Jariel-Encontre I. 2000. Molecular characterization of the thermosensitive E1 ubiquitin-activating enzyme cell mutant A31N-ts20. Requirements upon different levels of E1 for the ubiquitination/degradation of the various protein substrates in vivo. Eur J Biochem 2000; 267:3712-22.
64. Nouspikel T, Hanawalt PC. Impaired nucleotide excision repair upon macrophage differentiation is corrected by E1 ubiquitin-activating enzyme. Proc Natl Acad Sci USA 2006; 103:16188-93.