What is drosophila telling us about cancer?

Cancer and Metastasis Reviews

Volumn 18, Issue 2, 1999, Pages 295-311

  De Lorenzo, Cécilia ^a   Mechler, Bernard M ^b   Bryant, Peter J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Cancer; Cytoskeleton; Dlg; Drosophila; Lgl; Tumour suppressor gene

Indexed keywords

CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOSKELETON; DROSOPHILA; GENE ACTIVATION; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GENES, TUMOR SUPPRESSOR; GUANYLATE KINASE; HUMANS; INSECT PROTEINS; NEOPLASMS; NUCLEOSIDE-PHOSPHATE KINASE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 0033392230     PISSN: 01677659     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006381526008     Document Type: Review

References (104)

1. Vanderploeg HA, Fahnenstiel GL, Omair M, Jude DJ, Rizki TM: Tumors in freshwater zooplankton.ftp://ftp.glerl.noaa.gov/publications, 1999
2. Currie GA: Oncogenes and oncogenesis. Clin Oncol 10: 97-101, 1984
3. Boveri T: The origin of malignant tumors. William & Williams, Baltimore, 1929
4. Anders F: Tumor formation in platyfish-swordtail hybrids as a problem in gene regulation. Experientia 23: 1-10, 1967
5. 4. Amer Zool 7: 760, 1967
6. Harris H, Miller OJ, Klein G, Worst P, Tachibana: Suppression of malignancy by cell fusion. Nature 223: 363-368, 1969
7. Saxon PJ, Srivatsan ES, Stanbridge EJ: Introduction of human chromosome 11 via microcell transfer controls tumorigenic expression of HeLa cells. EMBO J 5: 3461-3466, 1986
8. Knudson Jr AG: Mutations and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci USA 68: 820-823, 1971
9. Cavenee WK, Dryja TP, Phillips RA, Benedict WF, Godbout R, Gallie BL, Murphree AL, Strong LC, White RL: Expression of recessive alleles by chromosomal mechanisms in retinoblastoma. Nature 305: 779-784, 1983
10. Friend SH, Bernards R, Rogelj S, Weinberg RA, Rapaport JM, Albert DM, Dryja TP: A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma. Nature 323: 643-646, 1986
11. Watson KL, Justice RW, Bryant PJ: Drosophila in cancer research: the first fifty tumor suppressor genes. J Cell Sci Suppl 18: 19-33, 1994
12. Gateff E: Tumor suppressor and overgrowth suppressor genes of Drosophila melanogaster. Developmental aspects. Int J Dev Biol 4: 565-590, 1994
13. Woods DF, Bryant PJ: Molecular cloning of the lethal(1)discs large-1 oncogene of Drosophila. Develop Biol 134: 222-235, 1989
14. Hadorn E: Developmental Genetics and Lethal Factors. Methuen, New York, 1961
15. Woods DF, Hough C, Peel D, Callaini G, Bryant PJ: Dlg protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J Cell Biol 134: 1469-1482, 1996
16. Gateff E, Schneiderman HA: Neoplasms in mutant and cultured wild-type tissues of Drosophila. Natl Cancer Inst Monogr 31: 365-397, 1969
17. Gateff E: Malignant neoplasms of genetic origin in Drosophila melanogaster. Science 200: 1448-1459, 1978
18. Gateff EA, Schneiderman HA: Developmental capacities of benign and malignant neoplasms of Drosophila. Roux's Arch Develop Biol 176: 23-65, 1974
19. Gateff E, Schneiderman HA: Neoplasms in mutant and cultured wild-type tissues of Drosophila. Nat Cancer Inst Monogr 31: 365-397, 1969
20. Woodhouse E, Hersperger E, Shearn A: Growth, metastasis, and invasiveness of Drosophila tumors caused by mutations in specific tumor suppressor genes. Dev Genes Evol 207: 542-550, 1998
21. Call KM, Glaser T, Ito CY, Buckler AJ, Haber DA, Rose EA, Kral A, Yeger H, Lewis WH, Jones C, Housman DE: Isolation and characterization of a zinc-finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell 60: 509-520, 1990
22. Gessler M, Poustka A, Cavenee W, Neve RL, Orkin SH, Bruns GAP: Homozygous deletion in Wilms tumours of a zinc-finger gene identified by chromosome jumping. Nature 343: 774-778, 1990
23. Pelletier J, Bruening W, Kashtan CE, Mauer SM, Manivel JC, Striegel JE, Houghton DC, Junien C, Habib R, Fouser L: Germline mutations in the Wilms' tumor suppressor gene are associated with abnormal urogenital development in Denys-Drash syndrome. Cell 67: 437-447, 1991
24. Gnarra JR, Ward JM, Porter FD, Wagner JR, Devor DE, Grinberg A, Emmert-Buck MR, Westphal H, Klausner RD, Linehan WM: Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice. Proc Natl Acad Sci USA 94: 9102-9107, 1997
25. Graana X, Garriga J, Mayol X: Role of the retinoblastoma protein family, pRB, p107 and p130 in the negative control of cell growth. Oncogene 17: 3365-3383, 1998
26. Clarke AR, Maandag ER, Van Roon M, Van der Lugt NMT, Van der Valk M, Hooper ML, Berns A, Te Riele H: Requirement for a functional Rb-1 gene in murine development. Nature 359: 328-330, 1992
27. Lee EYHP, Chang C-Y, Hu N, Wang Y-CJ, Lai C-C, Herrup K, Lee W-H, Bradley A: Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359: 288, 1992
28. Hakem R, De la Pompa JL, Sirard C, Mo R, Woo M, Hakem A, Wakeham A, Potter J, Reitmair A, Billia F, Firpo E, Hui CC, Roberts J, Rossant J, Mak TW: The tumor suppressor gene Brcal is required for embryonic cellular proliferation in the mouse. Cell 85: 1009-1023, 1996
29. Liu CY, Flesken-Nikitin A, Li S, Zeng Y, Lee WH: Inactivation of the mouse Brca1 gene leads to failure in the morphogenesis of the egg cylinder in early postimplantation development. Genes Dev 10: 1835-1843, 1996
30. Ludwig T, Chapman DL, Papaioannou VE, Efstratiadis A: Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brcal, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev 11: 1226-1241, 1997
31. Hanratty WP: Isolation and characterization of temperature-sensitive lethal (2) giant larva alleles. II. Temperature-sensitive expression of the imaginal disc neoplasm. Roux's Arch Develop Biol 193: 98-107, 1984
32. Manfruelli P, Arquier N, Hanratty WP, Sémériva M: The tumor suppressor gene, lethal(2)giant larvae (I(2)gl), is required for cell shape change of epithelial cells during Drosophila development. Develop 122: 2283-2294, 1996
33. Szabad J, Jursnich VA, Bryant PJ: Requirement for cell-proliferation control genes in Drosophila oogenesis. Genetics 127: 525-533, 1991
34. Baek KH, Hanratty WP: The lethal (2) giant larva (1(2)gl), a recessive oncogene, is required during embryonic and post-embryonic development in Drosophila. Cancer Lett 111: 233-238, 1997.
35. De Lorenzo C, Strand D, Mechler BM: Requirement of the Drosophila l(2)gl function for survival of the germline cells and organization of the follicle cells in a columnar epithelium during oogenesis. Int J Dev Biol 43: 207-221, 1999
36. Agrawal N, Kango M, Mishra A, Sinha P: Neoplastic transformation and aberrant cell-cell interactions in genetic mosaics of lethal(2)giant larvae lgl, a tumor suppressor gene of Drosophila. Develop Biol 172: 218-229, 1995
37. Mukherjee A, Lakhotia SC, Roy JK: l(2)gl gene regulates late expression of segment polarity genes in Drosophila. Mech Dev 51: 227-234, 1995
38. Farkas R, Mechler BM: The timing of Drosophila salivary gland apoptosis displays an l(2)gl gene dose response. Cell Death Diff 1999 (in press)
39. Perrimon N: The maternal effect of lethal(1)discs-large-1: a recessive oncogene of Drosophila melanogaster. Develop Biol 127: 392-407, 1998
40. Goode S, Perrimon N: Inhibition of patterned cell shape change and cell invasion by Discs large during Drosophila oogenesis. Genes Develop 11: 2532-2544, 1997
41. Mechler BM, McGinnis W, Gehring WJ: Molecular cloning of lethal(2)giant larvae, a recessive oncogene of Drosophila melanogaster. EMBO J 4: 1551-1557, 1985
42. Jacob L, Opper M, Metzroth B, Phannavong B, Mechler BM: Structure of the l(2)gl gene of Drosophila and delimitation of its tumor suppressor domain. Cell 50: 215-225, 1987
43. Merz R, Schmidt M, Torok I, Protin U, Schuler G, Walther HP, Krieg F, Gross M, Strand D, Mechler BM: Molecular action of the l(2)gl tumor suppressor gene of Drosophila melanogaster. Environ Health Perspect 88: 163-167, 1990
44. Strand D, Torok I, Kalmes A, Schmidt M, Merz R, Mechler BM: Transcriptional and translational regulation of the expression of the l(2)gl tumor suppressor gene of Drosophila melanogaster. Adv Enzyme Regul 31: 339-350, 1991
45. Strand D, Raska I, Mechler BM: The Drosophila lethal(2)giant larvae tumor suppressor protein is a component of the cytoskeleton. J Cell Biol 127: 1345-1360, 1994
46. Datta S: Control of proliferation activation in quiescent neuroblasts of the drosophila central nervous system. Develop 121: 1173-1182, 1995
47. Mechler BM, Torok I, Schmidt M, Opper M, Kuhn A, Merz R, Protin U: Molecular basis for the regulation of cell fate by the lethal (2) giant larvae tumor suppressor gene of Drosophila melanogaster. Ciba Found Symp 142: 166-178; discus, 1989
48. Hanratty WP: Isolation and characterisation of temperature-sensitive lethal(2) giant larva alleles. I. Mutagenesis and larval pathology. Roux's Arch Dev Biol: 193, 90-97
49. Strand D, Jakobs R, Merdes G, Neumann B, Kalmes A, Heid HW, Husmann I, Mechler BM: The Drosophila lethal(2)giant larvae tumor suppressor protein forms homo-oligomers and is associated with nonmuscle myosin II heavy chain. J Cell Biol 127: 1361-1373, 1994
50. Jakobs R, de LC, Spiess E, Strand D, Mechler BM: Homooligomerization domains in the lethal(2)giant larvae tumor suppressor protein, p127 of Drosophila. J Mol Biol 264: 484-496, 1996
51. Neumann B: Assoziation des Neucleosomeaufbauprotein 1 (NAP1) mit dem Tumorsuppressorprotein l(2)gl-p127 von Drosophila und seine mögliche Zellzyklus-abhängige Rolle bei der Zytoskelettdynamik, Ruprecht-Karls University Heidelberg. Dissertation, 1997
52. Kalmes A, Merdes G, Neumann B, Strand D, Mechler BM: A serine-kinase associated with the p127-l(2)gl tumour suppressor of Drosophila may regulate the binding of p127 to nonmuscle myosin II heavy chain and the attachment of p127 to the plasma membrane. J Cell Sci 109: 1359-1368, 1996
53. Merdes G: Das l(2)gl-Genprodukt p127 bindct an dic Schwanzdomane der schweren Kett von nichtmuskulärcm Myosin II und spiclt cinc Rolle bei der Regulation von Myosin II-Funktionen während der Embryogenese von Drosophila melanogaster, University of Heidelberg. Dissertation, 1998
54. Strand D: The tumor suppressor l(2)gl; a myosin II-binding protein family. In Maruta H, Kohama K: (eds): G Proteins, Cytoskeleton and Cancer, R.G. Landes Company, Texas USA, pp 61-78, 1998
55. Ishimi Y, Sato W, Kojima M, Sugasawa K, Hanaoka F, Yamada M: Rapid purification of nucleosome assembly protein (AP-1) and production of monoclonal antibodies against it. Cell Struct Funct 10: 373-382, 1985
56. Ishimi Y, Kikychi A: Identification and molecular cloning of yeast homolog of nucleosome assembly protein I which facilitates nucleosome assembly in vitro. J Biol Chem 266: 7025-7029, 1991
57. Simon HU, Mills GB, Kozlowski M, Hogg D, Branch D, Ishimi Y, Siminovitch KA: Molecular characterization of hNRP, a cDNA encoding a human nucleosome-assembly-protein-I-related gene product involved in the induction of cell proliferation. Biochem J 297 (Pt 2): 389-397, 1994
58. Kellogg DR, Murray AW: NAP1 acts with Cib1 to perform mitotic functions and to suppress polar bud growth in budding yeast. J Cell Biol 130: 675-685, 1995
59. Kellogg DR, Kikuchi A, Fujii-Nakata T, Turck CW, Murray AW: Members of the NAP/SET family of proteins interact specifically with B-type cyclins. J Cell Biol 130: 661-673, 1995
60. Li M, Strand D, Weid H, Neumann B, Mechler B: Casein kinase 2 binds and phosphorylates the nucleosome assembly protein-1 in Drosophila melanogaster. J Mol Biol 1999 (in press)
61. Campos-Ortega JA, Hartenstein V: The embryonic development of Drosophila melanogaster. Springer-Verlag, Berlin, New York, 1985
62. Young PE, Richman AM, Ketchum AS, Kiehart DP: Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev 7: 29-41, 1993
63. Noselli S: JNK signaling and morphogenesis in Drosophila. Trends.Genet 14: 33-38, 1998
64. Martinez Arias A: The development of Drosophila melanogaster. Cold Spring Harbor Press, 1993
65. Török I, Hartenstein K, Kalmes A, Schmitt R, Strand D, Mechler BM: The l(2)gl homologue of Drosophila pseudoobscura suppresses tumorigenicity in transgenic Drosophila melanogaster. Oncogene 8: 1537-1549, 1993
66. Koyama K, Fukushima Y, Inazawa J, Tomotsune D, Takahashi N, Nakamura Y: The human homologue of the murine Llglh gene (LLGL) maps within the Smith-Magenis syndrome region in 17p11.2. Cytogenet Cell Genet 72: 78-82, 1996
67. Strand D, Unger S, Corvi R, Hartenstein K, Schenkel H, Kalmes A, Merdes G, Neumann B, Krieg-Schneider F, Coy JF, Poustka A, Schwab M, Mechler BM: A human homologue of the Drosophila tumour suppressor gene l(2)gl maps to 17p11.2-12 and codes for a cytoskeletal protein that associates with nonmuscle myosin II heavy chain. Oncogene 11: 291-301, 1995
68. Wiemann, S. Tommerup N, Celis JE, Ansorge W, Leffers H: A human homologue of the Drosophila l(2)giant larvae tumour suppressor maps to 17q25-25. submission to NCBI. 1999, Electronic Citation
69. Larsson K, Bohl F, Sjostrom I, Akhtar N, Strand D, Mechler BM, Grabowski R, Adler L: The Saccharomyces cerevisiae SOP1 and SOP2 genes, which act in cation homeostasis, can be functionally substituted by the Drosophila lethal(2)giant larvae tumor suppressor gene. J Biol Chem 273: 33610-33618, 1998
70. Kagami M, Toh, Matsui Y: Sro7p, a Saccharomyces cerevisiae counterpart of the tumor suppressor l(2)gl protein, is related to myosins in function. Genetics 149: 1717-1727, 1998
71. Noirot-Timothee C, Noirot C: Septate and scalariform junctions in arthropods. Int Rev Cytol 63: 97-140, 1980
72. Woods DF, Bryant PJ: The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66: 451-464, 1991
73. Woods DF, Bryant PJ: Genetic control of cell interactions in developing Drosophila epithelia. Annu Rev Genet 26: 305-350, 1992
74. Hough C, Woods DF, Park S, Bryant PJ: Organising a functional junctional complex requires specific domains of the Drosophila MAGUK Discs large. Genes Develop 11: 3242-3253, 1996
75. Dimitratos SD, Woods DF, Bryant PJ: Camguk, Lin-2, and CASK: novel membrane-associated guanylate kinase homologs that also contain CaM kinase domains. Mech Dev 63: 127-130, 1997
76. Dimitratos SD, Wood DF, Stathakis DG, Bryant PJ: Signalling pathways are focused at specialised regions of the plasma membrane by scaffolding proteins of the MAGUK family, Bioessays 1999 (in press)
77. Lue RA, Marfatia SM, Branton D, Chishti AH: Cloning and characterization of hdlg: the human homologue of the Drosophila discs large tumor suppressor binds to protein 4.1. Proc Natl Acad Sci USA 91: 9818-9822, 1994
78. Makino K, Kuwahara H, Masuko N, Nishiyama Y, Morisaki T, Sasaki J, Nakao M, Kuwano A, Nakata M, Ushio Y, Saya H: Cloning and characterization of NE-dlg: a novel human homolog of the Drosophila discs large (dlg) tumor suppressor protein interacts with the APC protein. Oncogene 14: 2425-2433, 1997
79. Lau LF, Mammen A, Ehlers MD, Kindler S, Chung WJ, Garner CC, Huganir RL: Interaction of the N-methyl-D-aspartate receptor complex with a novel synapse-associated protein, SAP102. J Biol Chem 271: 21622-21628, 1996
80. Stathakis DC, Hoover KB, You Z, Bryant PJ: Human Post-Synaptic Density-95 (PSD95): location of the gene and possible function in non-neural as well as neural tissues. Genomics 44: 71-82, 1997
81. Cho K-O, Hunt CA, Kennedy MB: The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9: 929-942, 1992
82. Kistner U, Wenzel BM, Veh RW, Cases-Langhoff C, Garner AM, Appeltauer U, Voss B, Gundelfinger ED, Garner CC: SAP90, a rat presynaptic protein related to the product of the Drosophila tumor suppressor gene dlg-A. J Biol Chem 268: 4580-4583, 1993
83. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH: Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269: 1737-1740, 1995
84. + channels by interaction with a family of membrane-associated guanylate kinases. Nature 378: 85-88, 1995
85. Thomas U, Phannavong B, Muller B, Garner CC, Gundelfinger ED: Functional expression of rat synapse-associated proteins SAP97 and SAP102 in Drosophila dlg-1 mutants: effects on tumor suppression and synaptic bouton structure. Mechanisms of Development 62: 161-174, 1997
86. Willott E, Balda MS, Fanning AS, Jameson B, Van Itallie C, Anderson JM: The tight junction protein ZO-1 is homologous to the Drosophila discs-large tumor suppressor protein of septate junctions. Proc Natl Acad Sci USA 90: 7834-7838, 1993
87. Itoh M, Nagafuchi A, Yonemura S, Kitani-Yasuda T, Tsukita S: The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J Cell Biol 121: 491-502, 1993
88. Tsukita S, Itoh M, Nagafuchi A, Yonemura S: Submenbranous junctional plaque proteins include potential tumor suppressor molecules. J Cell Biol 123: 1049-1053, 1993
89. Gorry P, Vautier F, Le MV, Costet P, Daniel JY: Developmental regulation of a vertebrate homologue of the Drosophila dlg tumor suppressor gene. Int J Dev Biol Suppl 1: 295S-296S, 1996
90. Haskins J, Gu L, Wittchen ES, Hibbard J, Stevenson BR: ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J Cell Biol 141: 199-208, 1998
91. Takahisa M, Togashi S, Suzuki T, Kobayashi M, Murayama A, Kondo K, Miyake T, Ueda R: The Drosophila tamou gene, a component of the activating pathway of extra-macrochaetae expression, encodes a protein homologous to mammalian cell-cell junction-associated protein ZO-1. Genes Develop 10: 1783-1795, 1996
92. Ruff P, Speicher DW, Husain-Chishti A: Molecular identification of a major palmitoylated erythrocyte membrane protein containing the src homology 3 motif. Proc Natl Acad Sci USA 88: 6595-6599, 1991
93. Marfatia SM, Chishti AH: Human erythroid p55 is a catalytically active guanylate kinase. Mol Biol Cell 6: 1995
94. Mazoyer S, Gayther SA, Nagai MA, Smith SA, Dunning A, van Rensburg EJ, Albertsen H, White R, Ponder BAJ: A gene (DLG2) located at 17q12-q21 encodes a new homologue of the Drosophila tumor suppressor dlg-A. Genomics 28: 25-31, 1995
95. Smith SA, Holik P, Stavens J, Mazoyer S, Melis R, Williams B, White R, Albertsen H: Isolation of a gene (DLG3) encoding a second member of the discs-large family on chromosome 17q12-q21. Genomics 31: 145-150, 1996
96. Hata Y, Butz S, Südhof TC: CASK: A novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci 16: 2488-2494, 1996
97. Hoskins R, Hajnal AF, Harp SA, Kim SK: The C-elegans vulval induction gene lin-2 encodes a member of the MAGUK family of cell junction proteins. Develop 122: 97-111, 1996
98. 2+ calmodulin-dependent protein kinase (Caki) is localized in the central nervous system and implicated in walking speed. EMBO J 15: 1865-1876, 1996
99. Hoover KB, Liao SY, Bryant PJ: Loss of the tight junction MAGUK ZO-1 in breast cancer: relationship to glandular differentiation and loss of heterozygosity. Am J Pathol 153: 1767-1773, 1998
100. Takahashi K, Takahashi M, Katsube Ueda R, Yamamoto D: Direct binding between two PDZ domain protein canoe and ZO-1 and their role in regulation of the Jun N-terminal kinase pathway in Drosophila morphogenesis. Mech Dev 78:(1,2) 97-111, 1998
101. Itoh M, Nagafuchi A, Moroi S, Tsukita S: Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J Cell Biol 138: 181-192, 1997
102. Su L-K, Vogelstein B, Kinzler KW: Association of the APC tumor suppressor protein with catenins. Science 262: 1734-1737, 1993
103. Roch F, Baonza A, Martin-Blanco E, Garcia-Bellido A: Genetic interactions and cell behaviour in blistered mutants during proliferation and differentiation of the Drosophila wing. Develop 125: 1823-1832, 1998
104. Tsunoda S, Sierralta J, Sun Y, Bodner R, Suzuki E, Becker A, Socolich M, Zuker CS: A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature 388: 243-249, 1997