Drosophila Myc: A master regulator of cellular performance

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1849, Issue 5, 2015, Pages 570-581

  Grifoni, Daniela ^a   Bellosta, Paola ^b  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Cancer; Cell competition; Cell growth; Metabolism; MYC

Indexed keywords

BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; MAX PROTEIN, HUMAN; MXD1 PROTEIN, HUMAN; MYC PROTEIN; REPRESSOR PROTEIN;

ANIMAL; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC; REPRESSOR PROTEINS;

EID: 84930818360     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.06.021     Document Type: Review

References (174)

1. Vennstrom B., Sheiness D., Zabielski J., Bishop J.M. Isolation and characterization of c-myc, a cellular homolog of the oncogene (v-myc) of avian myelocytomatosis virus strain 29. J. Virol. 1982, 42(3):773-779.
2. Gallant P., Shiio Y., Cheng P.F., Parkhurst S.M., Eisenman R.N. Myc and Max homologs in Drosophila. Science 1996, 274(5292):1523-1527.
3. Bridges C. Drosophila melanogaster: legend for symbols, mutants, valuations. Drosophila Inf. Serv. 1935, 3:5-19.
4. Schreiber-Agus N., Stein D., Chen K., Goltz J.S., Stevens L., DePinho R.A. Drosophila Myc is oncogenic in mammalian cells and plays a role in the diminutive phenotype. Proc. Natl. Acad. Sci. U. S. A. 1997, 94(4):1235-1240.
5. Bellosta P., Gallant P. Myc function in Drosophila. Genes Cancer 2010, 1(6):542-546.
6. Gallant P. Myc function in Drosophila. Cold Spring Harb. Perspect. Med. 2013, 3(10):a014324.
7. de la Cova C., Johnston L.A. Myc in model organisms: a view from the flyroom. Semin. Cancer Biol. 2006, 16(4):303-312.
8. Schwinkendorf D., Gallant P. The conserved Myc box 2 and Myc box 3 regions are important, but not essential, for Myc function in vivo. Gene 2009, 436(1-2):90-100.
9. Galletti M., Riccardo S., Parisi F., Lora C., Saqcena M.K., Rivas L., Wong B., Serra A., Serras F., Grifoni D., et al. Identification of domains responsible for ubiquitin-dependent degradation of dMyc by glycogen synthase kinase 3beta and casein kinase 1 kinases. Mol. Cell. Biol. 2009, 29(12):3424-3434.
10. Loo L.W., Secombe J., Little J.T., Carlos L.S., Yost C., Cheng P.F., Flynn E.M., Edgar B.A., Eisenman R.N. The transcriptional repressor dMnt is a regulator of growth in Drosophila melanogaster. Mol. Cell. Biol. 2005, 25(16):7078-7091.
11. Ayer D.E., Lawrence Q.A., Eisenman R.N. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell 1995, 80(5):767-776.
12. Schreiber-Agus N., Chin L., Chen K., Torres R., Rao G., Guida P., Skoultchi A.I., DePinho R.A. An amino-terminal domain of Mxi1 mediates anti-Myc oncogenic activity and interacts with a homolog of the yeast transcriptional repressor SIN3. Cell 1995, 80(5):777-786.
13. Pierce S.B., Yost C., Anderson S.A., Flynn E.M., Delrow J., Eisenman R.N. Drosophila growth and development in the absence of dMyc and dMnt. Dev. Biol. 2008, 315(2):303-316.
14. Steiger D., Furrer M., Schwinkendorf D., Gallant P. Max-independent functions of Myc in Drosophila melanogaster. Nat. Genet. 2008, 40(9):1084-1091.
15. Trumpp A., Refaeli Y., Oskarsson T., Gasser S., Murphy M., Martin G.R., Bishop J.M. c-Myc regulates mammalian body size by controlling cell number but not cell size. Nature 2001, 414(6865):768-773.
16. Benassayag C., Montero L., Colombie N., Gallant P., Cribbs D., Morello D. Human c-Myc isoforms differentially regulate cell growth and apoptosis in Drosophila melanogaster. Mol. Cell. Biol. 2005, 25(22):9897-9909.
17. O'Shea J.M., Ayer D.E. Coordination of nutrient availability and utilization by MAX- and MLX-centered transcription networks. Cold Spring Harb. Perspect. Med. 2013, 3(9):a014258.
18. Billin A.N., Ayer D.E. The Mlx network: evidence for a parallel Max-like transcriptional network that regulates energy metabolism. Curr. Top. Microbiol. Immunol. 2006, 302:255-278.
19. Johnston L.A., Prober D.A., Edgar B.A., Eisenman R.N., Gallant P. Drosophila myc regulates cellular growth during development. Cell 1999, 98(6):779-790.
20. Pierce S.B., Yost C., Britton J.S., Loo L.W., Flynn E.M., Edgar B.A., Eisenman R.N. dMyc is required for larval growth and endoreplication in Drosophila. Development 2004, 131(10):2317-2327.
21. de la Cova C., Abril M., Bellosta P., Gallant P., Johnston L.A. Drosophila myc regulates organ size by inducing cell competition. Cell 2004, 117(1):107-116.
22. Orian A., van Steensel B., Delrow J., Bussemaker H.J., Li L., Sawado T., Williams E., Loo L.W., Cowley S.M., Yost C., et al. Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev. 2003, 17(9):1101-1114.
23. Hulf T., Bellosta P., Furrer M., Steiger D., Svensson D., Barbour A., Gallant P. Whole-genome analysis reveals a strong positional bias of conserved dMyc-dependent E-boxes. Mol. Cell. Biol. 2005, 25(9):3401-3410.
24. Grewal S.S., Li L., Orian A., Eisenman R.N., Edgar B.A. Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nat. Cell Biol. 2005, 7(3):295-302.
25. Bellosta P., Hulf T., Balla Diop S., Usseglio F., Pradel J., Aragnol D., Gallant P. Myc interacts genetically with Tip48/Reptin and Tip49/Pontin to control growth and proliferation during Drosophila development. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(33):11799-11804.
26. Patel J.H., Loboda A.P., Showe M.K., Showe L.C., McMahon S.B. Analysis of genomic targets reveals complex functions of MYC. Nat. Rev. Cancer 2004, 4(7):562-568.
27. Dang C.V., O'Donnell K.A., Zeller K.I., Nguyen T., Osthus R.C., Li F. The c-Myc target gene network. Semin. Cancer Biol. 2006, 16(4):253-264.
28. Zaffran S., Chartier A., Gallant P., Astier M., Arquier N., Doherty D., Gratecos D., Semeriva M. A Drosophila RNA helicase gene, pitchoune, is required for cell growth and proliferation and is a potential target of d-Myc. Development 1998, 125(18):3571-3584.
29. Perrin L., Benassayag C., Morello D., Pradel J., Montagne J. Modulo is a target of Myc selectively required for growth of proliferative cells in Drosophila. Mech. Dev. 2003, 120(6):645-655.
30. Greasley P.J., Bonnard C., Amati B. Myc induces the nucleolin and BN51 genes: possible implications in ribosome biogenesis. Nucleic Acids Res. 2000, 28(2):446-453.
31. Grandori C., Gomez-Roman N., Felton-Edkins Z.A., Ngouenet C., Galloway D.A., Eisenman R.N., White R.J. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat. Cell Biol. 2005, 7(3):311-318.
32. Marshall L., Rideout E.J., Grewal S.S. Nutrient/TOR-dependent regulation of RNA polymerase III controls tissue and organismal growth in Drosophila. EMBO J. 2012, 31(8):1916-1930.
33. Wood M.A., McMahon S.B., Cole M.D. An ATPase/helicase complex is an essential cofactor for oncogenic transformation by c-Myc. Mol. Cell 2000, 5(2):321-330.
34. Grigoletto A., Lestienne P., Rosenbaum J. The multifaceted proteins Reptin and Pontin as major players in cancer. Biochim. Biophys. Acta 2011, 1815(2):147-157.
35. Etard C., Gradl D., Kunz M., Eilers M., Wedlich D. Pontin and Reptin regulate cell proliferation in early Xenopus embryos in collaboration with c-Myc and Miz-1. Mech. Dev. 2005, 122(4):545-556.
36. Secombe J., Li L., Carlos L., Eisenman R.N. The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev. 2007, 21(5):537-551.
37. Grewal S.S. Insulin/TOR signaling in growth and homeostasis: a view from the fly world. Int. J. Biochem. Cell Biol. 2009, 41(5):1006-1010.
38. Montagne J., Stewart M.J., Stocker H., Hafen E., Kozma S.C., Thomas G. Drosophila S6 kinase: a regulator of cell size. Science 1999, 285(5436):2126-2129.
39. Oldham S., Montagne J., Radimerski T., Thomas G., Hafen E. Genetic and biochemical characterization of dTOR, the Drosophila homolog of the target of rapamycin. Genes Dev. 2000, 14(21):2689-2694.
40. Zhang H., Stallock J.P., Ng J.C., Reinhard C., Neufeld T.P. Regulation of cellular growth by the Drosophila target of rapamycin dTOR. Genes Dev. 2000, 14(21):2712-2724.
41. Ikeya T., Galic M., Belawat P., Nairz K., Hafen E. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr. Biol. 2002, 12(15):1293-1300.
42. Bohni R., Riesgo-Escovar J., Oldham S., Brogiolo W., Stocker H., Andruss B.F., Beckingham K., Hafen E. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 1999, 97(7):865-875.
43. Li L., Edgar B.A., Grewal S.S. Nutritional control of gene expression in Drosophila larvae via TOR, Myc and a novel cis-regulatory element. BMC Cell Biol. 2010, 11:7.
44. Prober D.A., Edgar B.A. Interactions between Ras1, dMyc, and dPI3K signaling in the developing Drosophila wing. Genes Dev. 2002, 16(17):2286-2299.
45. Parisi F., Riccardo S., Daniel M., Saqcena M., Kundu N., Pession A., Grifoni D., Stocker H., Tabak E., Bellosta P. Drosophila insulin and target of rapamycin (TOR) pathways regulate GSK3 beta activity to control Myc stability and determine Myc expression in vivo. BMC Biol. 2011, 9:65.
46. Moberg K.H., Mukherjee A., Veraksa A., Artavanis-Tsakonas S., Hariharan I.K. The Drosophila F box protein archipelago regulates dMyc protein levels in vivo. Curr. Biol. 2004, 14(11):965-974.
47. Arnold H.K., Zhang X., Daniel C.J., Tibbitts D., Escamilla-Powers J., Farrell A., Tokarz S., Morgan C., Sears R.C. The Axin1 scaffold protein promotes formation of a degradation complex for c-Myc. EMBO J. 2009, 28(5):500-512.
48. Rennoll S.A., Konsavage W.M., Yochum G.S. Nuclear AXIN2 represses MYC gene expression. Biochem. Biophys. Res. Commun. 2014, 443(1):217-222.
49. Myant K., Sansom O.J. Wnt/Myc interactions in intestinal cancer: partners in crime. Exp. Cell Res. 2011, 317(19):2725-2731.
50. Osthus R.C., Shim H., Kim S., Li Q., Reddy R., Mukherjee M., Xu Y., Wonsey D., Lee L.A., Dang C.V. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J. Biol. Chem. 2000, 275(29):21797-21800.
51. Wise D.R., DeBerardinis R.J., Mancuso A., Sayed N., Zhang X.Y., Pfeiffer H.K., Nissim I., Daikhin E., Yudkoff M., McMahon S.B., et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(48):18782-18787.
52. Yuneva M.O., Fan T.W., Allen T.D., Higashi R.M., Ferraris D.V., Tsukamoto T., Mates J.M., Alonso F.J., Wang C., Seo Y., et al. The metabolic profile of tumors depends on both the responsible genetic lesion and tissue type. Cell Metab. 2012, 15(2):157-170.
53. Le A., Lane A.N., Hamaker M., Bose S., Gouw A., Barbi J., Tsukamoto T., Rojas C.J., Slusher B.S., Zhang H., et al. Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab. 2012, 15(1):110-121.
54. Teleman A.A., Hietakangas V., Sayadian A.C., Cohen S.M. Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metab. 2008, 7(1):21-32.
55. Parisi F., Riccardo S., Zola S., Lora C., Grifoni D., Brown L.M., Bellosta P. dMyc expression in the fat body affects DILP2 release and increases the expression of the fat desaturase Desat1 resulting in organismal growth. Dev. Biol. 2013, 379(1):64-75.
56. Andersen D.S., Colombani J., Leopold P. Coordination of organ growth: principles and outstanding questions from the world of insects. Trends Cell Biol. 2013, 23(7):336-344.
57. Demontis F., Perrimon N. Integration of Insulin receptor/Foxo signaling and dMyc activity during muscle growth regulates body size in Drosophila. Development 2009, 136(6):983-993.
58. Horikawa S., Sakata K., Hatanaka M., Tsukada K. Expression of c-myc oncogene in rat liver by a dietary manipulation. Biochem. Biophys. Res. Commun. 1986, 140(2):574-580.
59. Kim J.W., Fletcher D.L., Campion D.R., Gaskins H.R., Dean R. Effect of dietary manipulation on c-myc RNA expression in adipose tissue, muscle and liver of broiler chickens. Biochem. Biophys. Res. Commun. 1991, 180(1):1-7.
60. Geminard C., Rulifson E.J., Leopold P. Remote control of insulin secretion by fat cells in Drosophila. Cell Metab. 2009, 10(3):199-207.
61. Delanoue R., Slaidina M., Leopold P. The steroid hormone ecdysone controls systemic growth by repressing dMyc function in Drosophila fat cells. Dev. Cell 2010, 18(6):1012-1021.
62. de la Cova C., Senoo-Matsuda N., Ziosi M., Wu D.C., Bellosta P., Quinzii C.M., Johnston L.A. Supercompetitor status of Drosophila Myc cells requires p53 as a fitness sensor to reprogram metabolism and promote viability. Cell Metab. 2014, 19(3):470-483.
63. Parisi F., Riccardo S., Zola S., Lora C., Grifoni D., Brown L.M., Bellosta P. dMyc expression in the fat body affects DILP2 release and increases the expression of the fat desaturase Desat1 resulting in organismal growth. Dev. Biol. 2013, 379(1):64-75.
64. Valera A., Pujol A., Gregori X., Riu E., Visa J., Bosch F. Evidence from transgenic mice that myc regulates hepatic glycolysis. FASEB J. 1995, 9(11):1067-1078.
65. Riu E., Bosch F., Valera A. Prevention of diabetic alterations in transgenic mice overexpressing Myc in the liver. Proc. Natl. Acad. Sci. U. S. A. 1996, 93(5):2198-2202.
66. Menendez J.A., Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat. Rev. Cancer 2007, 7(10):763-777.
67. Igal R.A. Stearoyl-CoA desaturase-1: a novel key player in the mechanisms of cell proliferation, programmed cell death and transformation to cancer. Carcinogenesis 2010, 31(9):1509-1515.
68. Scaglia N., Chisholm J.W., Igal R.A. Inhibition of stearoylCoA desaturase-1 inactivates acetyl-CoA carboxylase and impairs proliferation in cancer cells: role of AMPK. PLoS One 2009, 4(8):e6812.
69. Mauvoisin D., Mounier C. Hormonal and nutritional regulation of SCD1 gene expression. Biochimie 2011, 93(1):78-86.
70. Zheng Y., Eilertsen K.J., Ge L., Zhang L., Sundberg J.P., Prouty S.M., Stenn K.S., Parimoo S. Scd1 is expressed in sebaceous glands and is disrupted in the asebia mouse. Nat. Genet. 1999, 23(3):268-270.
71. Ntambi J.M., Miyazaki M., Stoehr J.P., Lan H., Kendziorski C.M., Yandell B.S., Song Y., Cohen P., Friedman J.M., Attie A.D. Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(17):11482-11486.
72. Kohler K., Brunner E., Guan X.L., Boucke K., Greber U.F., Mohanty S., Barth J.M., Wenk M.R., Hafen E. A combined proteomic and genetic analysis identifies a role for the lipid desaturase Desat1 in starvation-induced autophagy in Drosophila. Autophagy 2009, 5(7).
73. Uyeda K., Repa J.J. Carbohydrate response element binding protein, ChREBP, a transcription factor coupling hepatic glucose utilization and lipid synthesis. Cell Metab. 2006, 4(2):107-110.
74. Billin A.N., Eilers A.L., Coulter K.L., Logan J.S., Ayer D.E. MondoA, a novel basic helix-loop-helix-leucine zipper transcriptional activator that constitutes a positive branch of a max-like network. Mol. Cell. Biol. 2000, 20(23):8845-8854.
75. Kaadige M.R., Looper R.E., Kamalanaadhan S., Ayer D.E. Glutamine-dependent anapleurosis dictates glucose uptake and cell growth by regulating MondoA transcriptional activity. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(35):14878-14883.
76. Martin J.F., Hersperger E., Simcox A. Shearn A: minidiscs encodes a putative amino acid transporter subunit required non-autonomously for imaginal cell proliferation. Mech. Dev. 2000, 92(2):155-167.
77. Mackenzie B., Erickson J.D. Sodium-coupled neutral amino acid (System N/A) transporters of the SLC38 gene family. Pflugers Arch. 2004, 447(5):784-795.
78. Nicklin P., Bergman P., Zhang B., Triantafellow E., Wang H., Nyfeler B., Yang H., Hild M., Kung C., Wilson C., et al. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 2009, 136(3):521-534.
79. van der Vos K.E., Eliasson P., Proikas-Cezanne T., Vervoort S.J., van Boxtel R., Putker M., van Zutphen I.J., Mauthe M., Zellmer S., Pals C., et al. Modulation of glutamine metabolism by the PI(3)K-PKB-FOXO network regulates autophagy. Nat. Cell Biol. 2012, 14(8):829-837.
80. Thao D.T., Seto H., Yamaguchi M. Drosophila Myc is required for normal DREF gene expression. Exp. Cell Res. 2008, 314(1):184-192.
81. Killip L.E., Grewal S.S. DREF is required for cell and organismal growth in Drosophila and functions downstream of the nutrition/TOR pathway. Dev. Biol. 2012, 371(2):191-202.
82. Rideout E.J., Marshall L., Grewal S.S. Drosophila RNA polymerase III repressor Maf1 controls body size and developmental timing by modulating tRNAiMet synthesis and systemic insulin signaling. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(4):1139-1144.
83. Rajan A., Perrimon N. Drosophila cytokine unpaired 2 regulates physiological homeostasis by remotely controlling insulin secretion. Cell 2012, 151(1):123-137.
84. Smith-Bolton R.K., Worley M.I., Kanda H., Hariharan I.K. Regenerative growth in Drosophila imaginal discs is regulated by Wingless and Myc. Dev. Cell 2009, 16(6):797-809.
85. Ren F., Shi Q., Chen Y., Jiang A., Ip Y.T., Jiang H., Jiang J. Drosophila Myc integrates multiple signaling pathways to regulate intestinal stem cell proliferation during midgut regeneration. Cell Res. 2013, 23(9):1133-1146.
86. Kamoshida Y., Fujiyama-Nakamura S., Kimura S., Suzuki E., Lim J., Shiozaki-Sato Y., Kato S., Takeyama K. Ecdysone receptor (EcR) suppresses lipid accumulation in the Drosophila fat body via transcription control. Biochem. Biophys. Res. Commun. 2012, 421(2):203-207.
87. Montero L., Muller N., Gallant P. Induction of apoptosis by Drosophila Myc. Genesis 2008, 46(2):104-111.
88. Marino G., Niso-Santano M., Baehrecke E.H., Kroemer G. Self-consumption: the interplay of autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2014, 15(2):81-94.
89. Nagy P., Varga A., Pircs K., Hegedus K., Juhasz G. Myc-driven overgrowth requires unfolded protein response-mediated induction of autophagy and antioxidant responses in Drosophila melanogaster. PLoS Genet. 2013, 9(8):e1003664.
90. Toh P.P., Luo S., Menzies F.M., Rasko T., Wanker E.E., Rubinsztein D.C. Myc inhibition impairs autophagosome formation. Hum. Mol. Genet. 2013, 22(25):5237-5248.
91. Conacci-Sorrell M., Eisenman R.N. Post-translational control of Myc function during differentiation. Cell Cycle 2011, 10(4):604-610.
92. Conacci-Sorrell M., Ngouenet C., Anderson S., Brabletz T., Eisenman R.N. Stress-induced cleavage of Myc promotes cancer cell survival. Genes Dev. 2014, 28(7):689-707.
93. Morata G., Ripoll P. Minutes: mutants of Drosophila autonomously affecting cell division rate. Dev. Biol. 1975, 42(2):211-221.
94. Marygold S.J., Roote J., Reuter G., Lambertsson A., Ashburner M., Millburn G.H., Harrison P.M., Yu Z., Kenmochi N., Kaufman T.C., et al. The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol. 2007, 8(10):R216.
95. Blair S.S. Genetic mosaic techniques for studying Drosophila development. Development 2003, 130(21):5065-5072.
96. Bryant P.J., Simpson P. Intrinsic and extrinsic control of growth in developing organs. Q. Rev. Biol. 1984, 59(4):387-415.
97. Garcia-Bellido A. The cellular and genetic bases of organ size and shape in Drosophila. Int. J. Dev. Biol. 2009, 53(8-10):1291-1303.
98. Garcia-Bellido A., Ripoll P., Morata G. Developmental compartmentalisation of the wing disk of Drosophila. Nat. New Biol. 1973, 245(147):251-253.
99. Simpson P., Morata G. Differential mitotic rates and patterns of growth in compartments in the Drosophila wing. Dev. Biol. 1981, 85(2):299-308.
100. Oliver E.R., Saunders T.L., Tarle S.A., Glaser T. Ribosomal protein L24 defect in belly spot and tail (Bst), a mouse Minute. Development 2004, 131(16):3907-3920.
101. Nellen D., Burke R., Struhl G., Basler K. Direct and long-range action of a DPP morphogen gradient. Cell 1996, 85(3):357-368.
102. Wilson P.A., Lagna G., Suzuki A., Hemmati-Brivanlou A. Concentration-dependent patterning of the Xenopus ectoderm by BMP4 and its signal transducer Smad1. Development 1997, 124(16):3177-3184.
103. Almirantis Y., Papageorgiou S. Modes of morphogen cooperation for limb formation in vertebrates and insects. J. Theor. Biol. 1999, 199(3):235-242.
104. 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(14):1263-1268.
105. Li W., Baker N.E. Engulfment is required for cell competition. Cell 2007, 129(6):1215-1225.
106. Moreno E., Basler K., Morata G. Cells compete for decapentaplegic survival factor to prevent apoptosis in Drosophila wing development. Nature 2002, 416(6882):755-759.
107. Martin F.A., Herrera S.C., Morata G. Cell competition, growth and size control in the Drosophila wing imaginal disc. Development 2009, 136(22):3747-3756.
108. Moreno E., Basler K. dMyc transforms cells into super-competitors. Cell 2004, 117(1):117-129.
109. Senoo-Matsuda N., Johnston L.A. Soluble factors mediate competitive and cooperative interactions between cells expressing different levels of Drosophila Myc. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(47):18543-18548.
110. Entchev E.V., Schwabedissen A., Gonzalez-Gaitan M. Gradient formation of the TGF-beta homolog Dpp. Cell 2000, 103(6):981-991.
111. Ziv O., Suissa Y., Neuman H., Dinur T., Geuking P., Rhiner C., Portela M., Lolo F., Moreno E., Gerlitz O. The co-regulator dNAB interacts with Brinker to eliminate cells with reduced Dpp signaling. Development 2009, 136(7):1137-1145.
112. Rhiner C., Diaz B., Portela M., Poyatos J.F., Fernandez-Ruiz I., Lopez-Gay J.M., Gerlitz O., Moreno E. Persistent competition among stem cells and their daughters in the Drosophila ovary germline niche. Development 2009, 136(6):995-1006.
113. Xie T., Spradling A.C. A niche maintaining germ line stem cells in the Drosophila ovary. Science 2000, 290(5490):328-330.
114. Chen D., McKearin D. Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr. Biol. 2003, 13(20):1786-1791.
115. Jin Z., Kirilly D., Weng C., Kawase E., Song X., Smith S., Schwartz J., Xie T. Differentiation-defective stem cells outcompete normal stem cells for niche occupancy in the Drosophila ovary. Cell Stem Cell 2008, 2(1):39-49.
116. Claveria C., Giovinazzo G., Sierra R., Torres M. Myc-driven endogenous cell competition in the early mammalian embryo. Nature 2013, 500(7460):39-44.
117. Sancho M., Di-Gregorio A., George N., Pozzi S., Sanchez J.M., Pernaute B., Rodriguez T.A. Competitive interactions eliminate unfit embryonic stem cells at the onset of differentiation. Dev. Cell 2013, 26(1):19-30.
118. Vincent J.P., Kolahgar G., Gagliardi M., Piddini E. Steep differences in wingless signaling trigger Myc-independent competitive cell interactions. Dev. Cell 2011, 21(2):366-374.
119. Arbouzova N.I., Zeidler M.P. JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Development 2006, 133(14):2605-2616.
120. Rodrigues A.B., Zoranovic T., Ayala-Camargo A., Grewal S., Reyes-Robles T., Krasny M., Wu D.C., Johnston L.A., Bach E.A. Activated STAT regulates growth and induces competitive interactions independently of Myc, Yorkie, Wingless and ribosome biogenesis. Development 2012, 139(21):4051-4061.
121. Rhiner C., Lopez-Gay J.M., Soldini D., Casas-Tinto S., Martin F.A., Lombardia L., Moreno E. Flower forms an extracellular code that reveals the fitness of a cell to its neighbors in Drosophila. Dev. Cell 2010, 18(6):985-998.
122. Merino M.M., Rhiner C., Portela M., Moreno E. "Fitness fingerprints" mediate physiological culling of unwanted neurons in Drosophila. Curr. Biol. 2013, 23(14):1300-1309.
123. Tamori Y., Deng W.M. Tissue repair through cell competition and compensatory cellular hypertrophy in postmitotic epithelia. Dev. Cell 2013, 25(4):350-363.
124. Portela M., Casas-Tinto S., Rhiner C., Lopez-Gay J.M., Dominguez O., Soldini D., Moreno E. Drosophila SPARC is a self-protective signal expressed by loser cells during cell competition. Dev. Cell 2010, 19(4):562-573.
125. Martinek N., Shahab J., Saathoff M., Ringuette M. Haemocyte-derived SPARC is required for collagen-IV-dependent stability of basal laminae in Drosophila embryos. J. Cell Sci. 2008, 121(Pt 10):1671-1680.
126. Dang C.V. c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol. Cell. Biol. 1999, 19(1):1-11.
127. Lolo F.N., Casas-Tinto S., Moreno E. Cell competition time line: winners kill losers, which are extruded and engulfed by hemocytes. Cell Rep. 2012, 2(3):526-539.
128. Bissell M.J., Radisky D. Putting tumours in context. Nat. Rev. Cancer 2001, 1(1):46-54.
129. Laconi E., Doratiotto S., Vineis P. The microenvironments of multistage carcinogenesis. Semin. Cancer Biol. 2008, 18(5):322-329.
130. Moreno E. Is cell competition relevant to cancer?. Nat. Rev. Cancer 2008, 8(2):141-147.
131. Johnston L.A. Socializing with MYC: cell competition in development and as a model for premalignant cancer. Cold Spring Harb. Perspect. Med. 2014, 4(4).
132. Slaughter D.P., Southwick H.W., Smejkal W. Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer 1953, 6(5):963-968.
133. Braakhuis B.J., Tabor M.P., Kummer J.A., Leemans C.R., Brakenhoff R.H. A genetic explanation of Slaughter's concept of field cancerization: evidence and clinical implications. Cancer Res. 2003, 63(8):1727-1730.
134. Jaiswal G., Jaiswal S., Kumar R., Sharma A. Field cancerization: concept and clinical implications in head and neck squamous cell carcinoma. J. Exp. Ther. Oncol. 2013, 10(3):209-214.
135. Bissell M.J., Hines W.C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 2011, 17(3):320-329.
136. Vita M., Henriksson M. The Myc oncoprotein as a therapeutic target for human cancer. Semin. Cancer Biol. 2006, 16(4):318-330.
137. Sansom O.J., Meniel V.S., Muncan V., Phesse T.J., Wilkins J.A., Reed K.R., Vass J.K., Athineos D., Clevers H., Clarke A.R. Myc deletion rescues Apc deficiency in the small intestine. Nature 2007, 446(7136):676-679.
138. Petrova E., Lopez-Gay J.M., Rhiner C., Moreno E. Flower-deficient mice have reduced susceptibility to skin papilloma formation. Dis. Model Mech. 2012, 5(4):553-561.
139. Chong H.C., Tan C.K., Huang R.L., Tan N.S. Matricellular proteins: a sticky affair with cancers. J. Oncol. 2012, 2012:351089.
140. Wu J., Mlodzik M. A quest for the mechanism regulating global planar cell polarity of tissues. Trends Cell Biol. 2009, 19(7):295-305.
141. Li W., Kale A., Baker N.E. Oriented cell division as a response to cell death and cell competition. Curr. Biol. 2009, 19(21):1821-1826.
142. Muthuswamy S.K., Xue B. Cell polarity as a regulator of cancer cell behavior plasticity. Annu. Rev. Cell Dev. Biol. 2012, 28:599-625.
143. Royer C., Lu X. Epithelial cell polarity: a major gatekeeper against cancer?. Cell Death Differ. 2011, 18(9):1470-1477.
144. Grzeschik N.A., Parsons L.M., Allott M.L., Harvey K.F., Richardson H.E. Lgl, aPKC, and Crumbs regulate the Salvador/Warts/Hippo pathway through two distinct mechanisms. Curr. Biol. 2010, 20(7):573-581.
145. Robinson B.S., Huang J., Hong Y., Moberg K.H. Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein Expanded. Curr. Biol. 2010, 20(7):582-590.
146. Hafezi Y., Bosch J.A., Hariharan I.K. Differences in levels of the transmembrane protein Crumbs can influence cell survival at clonal boundaries. Dev. Biol. 2012, 368(2):358-369.
147. Froldi F., Ziosi M., Garoia F., Pession A., Grzeschik N.A., Bellosta P., Strand D., Richardson H.E., Grifoni D. The lethal giant larvae tumour suppressor mutation requires dMyc oncoprotein to promote clonal malignancy. BMC Biol. 2010, 8:33.
148. Bilder D. Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 2004, 18(16):1909-1925.
149. Hariharan I.K., Bilder D. Regulation of imaginal disc growth by tumor-suppressor genes in Drosophila. Annu. Rev. Genet. 2006, 40:335-361.
150. Yamanaka T., Ohno S. Role of Lgl/Dlg/Scribble in the regulation of epithelial junction, polarity and growth. Front. Biosci. 2008, 13:6693-6707.
151. Woodhouse E., Hersperger E., Shearn A. Growth, metastasis, and invasiveness of Drosophila tumors caused by mutations in specific tumor suppressor genes. Dev. Genes Evol. 1998, 207(8):542-550.
152. Tamori Y., Bialucha C.U., Tian A.G., Kajita M., Huang Y.C., Norman M., Harrison N., Poulton J., Ivanovitch K., Disch L., et al. Involvement of Lgl and Mahjong/VprBP in cell competition. PLoS Biol. 2010, 8(7):e1000422.
153. Norman M., Wisniewska K.A., Lawrenson K., Garcia-Miranda P., Tada M., Kajita M., Mano H., Ishikawa S., Ikegawa M., Shimada T., et al. Loss of Scribble causes cell competition in mammalian cells. J. Cell Sci. 2012, 125(Pt 1):59-66.
154. Halaoui R., McCaffrey L. Rewiring cell polarity signaling in cancer. Oncogene 2014 Mar 17, [Epub ahead of print]. 10.1038/onc.2014.59.
155. Brumby A., Secombe J., Horsfield J., Coombe M., Amin N., Coates D., Saint R., Richardson H. A genetic screen for dominant modifiers of a cyclin E hypomorphic mutation identifies novel regulators of S-phase entry in Drosophila. Genetics 2004, 168(1):227-251.
156. Grzeschik N.A., Amin N., Secombe J., Brumby A.M., Richardson H.E. Abnormalities in cell proliferation and apico-basal cell polarity are separable in Drosophila lgl mutant clones in the developing eye. Dev. Biol. 2007, 311(1):106-123.
157. Huang J., Wu S., Barrera J., Matthews K., Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homolog of YAP. Cell 2005, 122(3):421-434.
158. Dong J., Feldmann G., Huang J., Wu S., Zhang N., Comerford S.A., Gayyed M.F., Anders R.A., Maitra A., Pan D. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 2007, 130(6):1120-1133.
159. Halder G., Johnson R.L. Hippo signaling: growth control and beyond. Development 2011, 138(1):9-22.
160. Tyler D.M., Baker N.E. Expanded and fat regulate growth and differentiation in the Drosophila eye through multiple signaling pathways. Dev. Biol. 2007, 305(1):187-201.
161. Sun G., Irvine K.D. Regulation of Hippo signaling by Jun kinase signaling during compensatory cell proliferation and regeneration, and in neoplastic tumors. Dev. Biol. 2011, 350(1):139-151.
162. Menendez J., Perez-Garijo A., Calleja M., Morata G. A tumor-suppressing mechanism in Drosophila involving cell competition and the Hippo pathway. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(33):14651-14656.
163. Khan S.J., Bajpai A., Alam M.A., Gupta R.P., Harsh S., Pandey R.K., Goel-Bhattacharya S., Nigam A., Mishra A., Sinha P. Epithelial neoplasia in Drosophila entails switch to primitive cell states. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(24):E2163-E2172.
164. Neto-Silva R.M., de Beco S., Johnston L.A. Evidence for a growth-stabilizing regulatory feedback mechanism between Myc and Yorkie, the Drosophila homolog of Yap. Dev. Cell 2010, 19(4):507-520.
165. Ziosi M., Baena-Lopez L.A., Grifoni D., Froldi F., Pession A., Garoia F., Trotta V., Bellosta P., Cavicchi S. dMyc functions downstream of Yorkie to promote the supercompetitive behavior of hippo pathway mutant cells. PLoS Genet. 2010, 6(9):e1001140.
166. Xiao W., Wang J., Ou C., Zhang Y., Ma L., Weng W., Pan Q., Sun F. Mutual interaction between YAP and c-Myc is critical for carcinogenesis in liver cancer. Biochem. Biophys. Res. Commun. 2013, 439(2):167-172.
167. Pobbati A.V., Hong W. Emerging roles of TEAD transcription factors and its coactivators in cancers. Cancer Biol. Ther. 2013, 14(5):390-398.
168. Grifoni D., Garoia F., Bellosta P., Parisi F., De Biase D., Collina G., Strand D., Cavicchi S., Pession A. aPKCzeta cortical loading is associated with Lgl cytoplasmic release and tumor growth in Drosophila and human epithelia. Oncogene 2007, 26(40):5960-5965.
169. Betschinger J., Eisenhaber F., Knoblich J.A. Phosphorylation-induced autoinhibition regulates the cytoskeletal protein Lethal (2) giant larvae. Curr. Biol. 2005, 15(3):276-282.
170. Doggett K., Grusche F.A., Richardson H.E., Brumby A.M. Loss of the Drosophila cell polarity regulator Scribbled promotes epithelial tissue overgrowth and cooperation with oncogenic Ras-Raf through impaired Hippo pathway signaling. BMC Dev. Biol. 2011, 11:57.
171. Chen C.L., Schroeder M.C., Kango-Singh M., Tao C., Halder G. Tumor suppression by cell competition through regulation of the Hippo pathway. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(2):484-489.
172. Brumby A.M., Richardson H.E. Scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J. 2003, 22(21):5769-5779.
173. Pagliarini R.A., Xu T. A genetic screen in Drosophila for metastatic behavior. Science 2003, 302(5648):1227-1231.
174. Ballesteros-Arias L., Saavedra V., Morata G. Cell competition may function either as tumour-suppressing or as tumour-stimulating factor in Drosophila. Oncogene 2013 Oct 7, [Epub ahead of print]. 10.1038/onc.2013.407.