Cell competition: How to eliminate your neighbours

Development (Cambridge)

Volumn 141, Issue 5, 2014, Pages 988-1000

  Amoyel, Marc ^a   Bach, Erika A ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Losers; Minute; Myc; Super competition; Winners

Indexed keywords

APOPTOSIS; LOSERS; MINUTE; MYC; SUPER-COMPETITION; WINNERS;

ANIMALS; CELL COMMUNICATION; DROSOPHILA; DROSOPHILA PROTEINS; SIGNAL TRANSDUCTION;

EID: 84894086619     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.079129     Document Type: Review

References (128)

1. Abrams, J. M. (2002). Competition and compensation: coupled to death in development and cancer. Cell 110, 403-406.
2. Abrams, J. M., White, K., Fessler, L. I. and Steller, H. (1993). Programmed cell death during Drosophila embryogenesis. Development 117, 29-43.
3. Agrawal, N., Kango, M., Mishra, A. and Sinha, P. (1995). Neoplastic transformation and aberrant cell-cell interactions in genetic mosaics of lethal(2)giant larvae (lgl), a tumor suppressor gene of Drosophila. Dev. Biol. 172, 218-229.
4. Ballesteros-Arias, L., Saavedra, V. and Morata, G. (2013). Cell competition may function either as tumour-suppressing or as tumour-stimulating factor in Drosophila. Oncogene (in press). doi: 10.1038/onc.2013.407.
5. Bergmann, A., Agapite, J., McCall, K. and Steller, H. (1998). The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95, 331-341.
6. Bilder, D. (2004). Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 18, 1909-1925.
7. Böhni, R., Riesgo-Escovar, J., Oldham, S., Brogiolo, W., Stocker, H., Andruss, B. F., Beckingham, K. and Hafen, E. (1999). Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97, 865-875.
8. Bondar, T. and Medzhitov, R. (2010). p53-mediated hematopoietic stem and progenitor cell competition. Cell Stem Cell 6, 309-322.
9. Brumby, A. M. and Richardson, H. E. (2003). scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J. 22, 5769-5779.
10. Burke, R. and Basler, K. (1996). Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing. Development 122, 2261-2269.
11. Chen, C. L., Gajewski, K. M., Hamaratoglu, F., Bossuyt, W., Sansores-Garcia, L., Tao, C. and Halder, G. (2010). The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc. Natl. Acad. Sci. USA 107, 15810-15815.
12. Chen, C. L., Schroeder, M. C., Kango-Singh, M., Tao, C. and Halder, G. (2012). Tumor suppression by cell competition through regulation of the Hippo pathway. Proc. Natl. Acad. Sci. USA 109, 484-489.
13. Clavería, C., Giovinazzo, G., Sierra, R. and Torres, M. (2013). Myc-driven endogenous cell competition in the early mammalian embryo. Nature 500, 39-44.
14. Cordero, J. B., Macagno, J. P., Stefanatos, R. K., Strathdee, K. E., Cagan, R. L. and Vidal, M. (2010). Oncogenic Ras diverts a host TNF tumor suppressor activity into tumor promoter. Dev. Cell 18, 999-1011.
15. Crick, F. H. and Lawrence, P. A. (1975). Compartments and polyclones in insect development. Science 189, 340-347.
16. de la Cova, C., Abril, M., Bellosta, P., Gallant, P. and Johnston, L. A. (2004). Drosophila myc regulates organ size by inducing cell competition. Cell 117, 107-116.
17. de Navascués, J., Perdigoto, C. N., Bian, Y., Schneider, M. H., Bardin, A. J., Martínez-Arias, A. and Simons, B. D. (2012). Drosophila midgut homeostasis involves neutral competition between symmetrically dividing intestinal stem cells. EMBO J. 31, 2473-2485.
18. Dejosez, M., Ura, H., Brandt, V. L. and Zwaka, T. P. (2013). Safeguards for cell cooperation in mouse embryogenesis shown by genome-wide cheater screen. Science 341, 1511-1514.
19. Diaz-Benjumea, F. J. and Hafen, E. (1994). The sevenless signalling cassette mediates Drosophila EGF receptor function during epidermal development. Development 120, 569-578.
20. Doggett, K., Grusche, F. A., Richardson, H. E. and Brumby, A. M. (2011). 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. 11, 57.
21. Duman-Scheel, M., Johnston, L. A. and Du, W. (2004). Repression of dMyc expression by Wingless promotes Rbf-induced G1 arrest in the presumptive Drosophila wing margin. Proc. Natl. Acad. Sci. USA 101, 3857-3862.
22. Etchegaray, J. I., Timmons, A. K., Klein, A. P., Pritchett, T. L., Welch, E., Meehan, T. L., Li, C. and McCall, K. (2012). Draper acts through the JNK pathway to control synchronous engulfment of dying germline cells by follicular epithelial cells. Development 139, 4029-4039.
23. Franc, N. C., Heitzler, P., Ezekowitz, R. A. and White, K. (1999). Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284, 1991-1994.
24. Froldi, F., Ziosi, M., Garoia, F., Pession, A., Grzeschik, N. A., Bellosta, P., Strand, D., Richardson, H. E., Pession, A. and Grifoni, D. (2010). The lethal giant larvae tumour suppressor mutation requires dMyc oncoprotein to promote clonal malignancy. BMC Biol. 8, 33.
25. Garcia-Bellido, A. and Merriam, J. R. (1971). Parameters of the wing imaginal disc development of Drosophila melanogaster. Dev. Biol. 24, 61-87.
26. Garcia-Bellido, A., Ripoll, P. and Morata, G. (1973). Developmental compartmentalisation of the wing disk of Drosophila. Nat. New Biol. 245, 251-253.
27. Garcia-Bellido, A., Ripoll, P. and Morata, G. (1976). Developmental compartmentalization in the dorsal mesothoracic disc of Drosophila. Dev. Biol. 48, 132-147.
28. Gateff, E. (1978). Malignant neoplasms of genetic origin in Drosophila melanogaster. Science 200, 1448-1459.
29. Gibson, M. C. and Perrimon, N. (2005). Extrusion and death of DPP/BMP-compromised epithelial cells in the developing Drosophila wing. Science 307, 1785-1789.
30. Giraldez, A. J. and Cohen, S. M. (2003). Wingless and Notch signaling provide cell survival cues and control cell proliferation during wing development. Development 130, 6533-6543.
31. Golic, K. G. (1991). Site-specific recombination between homologous chromosomes in Drosophila. Science 252, 958-961.
32. Grewal, S. S., Li, L., Orian, A., Eisenman, R. N. and Edgar, B. A. (2005). Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nat. Cell Biol. 7, 295-302.
33. Griffiths, D. F., Davies, S. J., Williams, D., Williams, G. T. and Williams, E. D. (1988). Demonstration of somatic mutation and colonic crypt clonality by X-linked enzyme histochemistry. Nature 333, 461-463.
34. Grzeschik, N. A., Amin, N., Secombe, J., Brumby, A. M. and Richardson, H. E. (2007). Abnormalities in cell proliferation and apico-basal cell polarity are separable in Drosophila lgl mutant clones in the developing eye. Dev. Biol. 311, 106-123.
35. Grzeschik, N. A., Parsons, L. M., Allott, M. L., Harvey, K. F. and Richardson, H. E. (2010). Lgl, aPKC, and Crumbs regulate the Salvador/Warts/Hippo pathway through two distinct mechanisms. Curr. Biol. 20, 573-581.
36. Hafezi, Y., Bosch, J. A. and Hariharan, I. K. (2012). Differences in levels of the transmembrane protein Crumbs can influence cell survival at clonal boundaries. Dev. Biol. 368, 358-369.
37. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129.
38. Herz, H. M., Chen, Z., Scherr, H., Lackey, M., Bolduc, C. and Bergmann, A. (2006). vps25 mosaics display non-autonomous cell survival and overgrowth, and autonomous apoptosis. Development 133, 1871-1880.
39. Huang, J., Wu, S., Barrera, J., Matthews, K. and Pan, D. (2005). The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homolog of YAP. Cell 122, 421-434.
40. Igaki, T. (2009). Correcting developmental errors by apoptosis: lessons from Drosophila JNK signaling. Apoptosis 14, 1021-1028.
41. Igaki, T., Pagliarini, R. A. and Xu, T. (2006). Loss of cell polarity drives tumor growth and invasion through JNK activation in Drosophila. Curr. Biol. 16, 1139-1146.
42. Igaki, T., Pastor-Pareja, J. C., Aonuma, H., Miura, M. and Xu, T. (2009). Intrinsic tumor suppression and epithelial maintenance by endocytic activation of Eiger/TNF signaling in Drosophila. Dev. Cell 16, 458-465.
43. Issigonis, M., Tulina, N., de Cuevas, M., Brawley, C., Sandler, L. and Matunis, E. (2009). JAK-STAT signal inhibition regulates competition in the Drosophila testis stem cell niche. Science 326, 153-156.
44. Jin, Z., Kirilly, D., Weng, C., Kawase, E., Song, X., Smith, S., Schwartz, J. and Xie, T. (2008). Differentiation-defective stem cells outcompete normal stem cells for niche occupancy in the Drosophila ovary. Cell Stem Cell 2, 39-49.
45. Johnston, L. A. and Sanders, A. L. (2003). Wingless promotes cell survival but constrains growth during Drosophila wing development. Nat. Cell Biol. 5, 827-833.
46. Johnston, L. A., Prober, D. A., Edgar, B. A., Eisenman, R. N. and Gallant, P. (1999). Drosophila myc regulates cellular growth during development. Cell 98, 779-790.
47. Karim, F. D. and Rubin, G. M. (1998). Ectopic expression of activated Ras1 induces hyperplastic growth and increased cell death in Drosophila imaginal tissues. Development 125, 1-9.
48. Khare, A. and Shaulsky, G. (2006). First among equals: competition between genetically identical cells. Nat. Rev. Genet. 7, 577-584.
49. Klein, A. M. and Simons, B. D. (2011). Universal patterns of stem cell fate in cycling adult tissues. Development 138, 3103-3111.
50. Kurada, P. and White, K. (1998). Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95, 319-329.
51. Leong, G. R., Goulding, K. R., Amin, N., Richardson, H. E. and Brumby, A. M. (2009). Scribble mutants promote aPKC and JNK-dependent epithelial neoplasia independently of Crumbs. BMC Biol. 7, 62.
52. Li, W. and Baker, N. E. (2007). Engulfment is required for cell competition. Cell 129, 1215-1225.
53. Li, W., Kale, A. and Baker, N. E. (2009). Oriented cell division as a response to cell death and cell competition. Curr. Biol. 19, 1821-1826.
54. Ling, C., Zheng, Y., Yin, F., Yu, J., Huang, J., Hong, Y., Wu, S. and Pan, D. (2010). The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates Hippo signaling by binding to Expanded. Proc. Natl. Acad. Sci. USA 107, 10532-10537.
55. Lolo, F. N., Casas-Tintó, S. and Moreno, E. (2012). Cell competition time line: winners kill losers, which are extruded and engulfed by hemocytes. Cell Rep. 2, 526-539.
56. Lolo, F. N., Casas Tintó, S. and Moreno, E. (2013). How winner cells cause the demise of loser cells: cell competition causes apoptosis of suboptimal cells: their dregs are removed by hemocytes, thus preserving tissue homeostasis. BioEssays 35, 348-353.
57. Lopez-Garcia, C., Klein, A. M., Simons, B. D. and Winton, D. J. (2010). Intestinal stem cell replacement follows a pattern of neutral drift. Science 330, 822-825.
58. Lu, H. and Bilder, D. (2005). Endocytic control of epithelial polarity and proliferation in Drosophila. Nat. Cell Biol. 7, 1232-1239.
59. Marinari, E., Mehonic, A., Curran, S., Gale, J., Duke, T. and Baum, B. (2012). Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 484, 542-545.
60. Martín, F. A., Herrera, S. C. and Morata, G. (2009a). Cell competition, growth and size control in the Drosophila wing imaginal disc. Development 136, 3747-3756.
61. Martín, F. A., Peréz-Garijo, A. and Morata, G. (2009b). Apoptosis in Drosophila: compensatory proliferation and undead cells. Int. J. Dev. Biol. 53, 1341-1347.
62. Marusyk, A., Porter, C. C., Zaberezhnyy, V. and DeGregori, J. (2010). Irradiation selects for p53-deficient hematopoietic progenitors. PLoS Biol. 8, e1000324.
63. 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. (2007). The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol. 8, R216.
64. Menéndez, J., Pérez-Garijo, A., Calleja, M. and Morata, G. (2010). A tumorsuppressing mechanism in Drosophila involving cell competition and the Hippo pathway. Proc. Natl. Acad. Sci. USA 107, 14651-14656.
65. Menut, L., Vaccari, T., Dionne, H., Hill, J., Wu, G. and Bilder, D. (2007). A mosaic genetic screen for Drosophila neoplastic tumor suppressor genes based on defective pupation. Genetics 177, 1667-1677.
66. Merino, M. M., Rhiner, C., Portela, M. and Moreno, E. (2013). 'Fitness fingerprints' mediate physiological culling of unwanted neurons in Drosophila. Curr. Biol. 23, 1300-1309.
67. Micklem, H. S., Clarke, C. M., Evans, E. P. and Ford, C. E. (1968). Fate of chromosome-marked mouse bone marrow cells tranfused into normal syngeneic recipients. Transplantation 6, 299-302.
68. Moberg, K. H., Schelble, S., Burdick, S. K. and Hariharan, I. K. (2005). Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev. Cell 9, 699-710.
69. Morata, G. and Ripoll, P. (1975). Minutes: mutants of drosophila autonomously affecting cell division rate. Dev. Biol. 42, 211-221.
70. Moreno, E. and Basler, K. (2004). dMyc transforms cells into super-competitors. Cell 117, 117-129.
71. Moreno, E., Basler, K. and Morata, G. (2002). Cells compete for decapentaplegic survival factor to prevent apoptosis in Drosophila wing development. Nature 416, 755-759.
72. Neto-Silva, R. M., de Beco, S. and Johnston, L. A. (2010). Evidence for a growthstabilizing regulatory feedback mechanism between Myc and Yorkie, the Drosophila homolog of Yap. Dev. Cell 19, 507-520.
73. Neufeld, T. P., de la Cruz, A. F., Johnston, L. A. and Edgar, B. A. (1998). Coordination of growth and cell division in the Drosophila wing. Cell 93, 1183-1193.
74. Newsome, T. P., Asling, B. and Dickson, B. J. (2000). Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851-860.
75. Norman, M., Wisniewska, K. A., Lawrenson, K., Garcia-Miranda, P., Tada, M., Kajita, M., Mano, H., Ishikawa, S., Ikegawa, M., Shimada, T. et al. (2012). Loss of Scribble causes cell competition in mammalian cells. J. Cell Sci. 125, 59-66.
76. Nystul, T. and Spradling, A. (2007). An epithelial niche in the Drosophila ovary undergoes long-range stem cell replacement. Cell Stem Cell 1, 277-285.
77. Oertel, M., Menthena, A., Dabeva, M. D. and Shafritz, D. A. (2006). Cell competition leads to a high level of normal liver reconstitution by transplanted fetal liver stem/progenitor cells. Gastroenterology 130, 507-520, quiz 590.
78. Ohsawa, S., Sugimura, K., Takino, K., Xu, T., Miyawaki, A. and Igaki, T. (2011). Elimination of oncogenic neighbors by JNK-mediated engulfment in Drosophila. Dev. Cell 20, 315-328.
79. Oliver, E. R., Saunders, T. L., Tarlé, S. A. and Glaser, T. (2004). Ribosomal protein L24 defect in belly spot and tail (Bst), a mouse Minute. Development 131, 3907-3920.
80. Pagliarini, R. A. and Xu, T. (2003). A genetic screen in Drosophila for metastatic behavior. Science 302, 1227-1231.
81. Pan, D. (2010). The hippo signaling pathway in development and cancer. Dev. Cell 19, 491-505.
82. Pastor-Pareja, J. C., Wu, M. and Xu, T. (2008). An innate immune response of blood cells to tumors and tissue damage in Drosophila. Dis. Model. Mech. 1, 144-154.
83. Patterson, J. T. (1929). The production of mutations in somatic cells of Drosophila melanogaster by means of X-rays. J. Exp. Zool. 53, 327-372.
84. Poduri, A., Evrony, G. D., Cai, X. and Walsh, C. A. (2013). Somatic mutation, genomic variation, and neurological disease. Science 341, 1237758.
85. Portela, M., Casas-Tinto, S., Rhiner, C., López-Gay, J. M., Domínguez, O., Soldini, D. and Moreno, E. (2010). Drosophila SPARC is a self-protective signal expressed by loser cells during cell competition. Dev. Cell 19, 562-573.
86. Posakony, L. G., Raftery, L. A. and Gelbart, W. M. (1990). Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anteriorposterior compartment boundary. Mech. Dev. 33, 69-82.
87. Prober, D. A. and Edgar, B. A. (2000). Ras1 promotes cellular growth in the Drosophila wing. Cell 100, 435-446.
88. Raff, M. C. (1992). Social controls on cell survival and cell death. Nature 356, 397-400.
89. Rhiner, C., Díaz, B., Portela, M., Poyatos, J. F., Fernández-Ruiz, I., López-Gay, J. M., Gerlitz, O. and Moreno, E. (2009). Persistent competition among stem cells and their daughters in the Drosophila ovary germline niche. Development 136, 995-1006.
90. Rhiner, C., López-Gay, J. M., Soldini, D., Casas-Tinto, S., Martín, F. A., Lombardía, L. and Moreno, E. (2010). Flower forms an extracellular code that reveals the fitness of a cell to its neighbors in Drosophila. Dev. Cell 18, 985-998.
91. Richardson, E. C. and Pichaud, F. (2010). Crumbs is required to achieve proper organ size control during Drosophila head development. Development 137, 641-650.
92. Robinson, B. S., Huang, J., Hong, Y. and Moberg, K. H. (2010). Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein Expanded. Curr. Biol. 20, 582-590.
93. Rodrigues, A. B., Zoranovic, T., Ayala-Camargo, A., Grewal, S., Reyes-Robles, T., Krasny, M., Wu, D. C., Johnston, L. A. and Bach, E. A. (2012). Activated STAT regulates growth and induces competitive interactions independently of Myc, Yorkie, Wingless and ribosome biogenesis. Development 139, 4051-4061.
94. Sancho, M., Di-Gregorio, A., George, N., Pozzi, S., Sánchez, J. M., Pernaute, B. and Rodríguez, T. A. (2013). Competitive interactions eliminate unfit embryonic stem cells at the onset of differentiation. Dev. Cell 26, 19-30.
95. Santorelli, L. A., Thompson, C. R., Villegas, E., Svetz, J., Dinh, C., Parikh, A., Sucgang, R., Kuspa, A., Strassmann, J. E., Queller, D. C. et al. (2008). Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451, 1107-1110.
96. Senoo-Matsuda, N. and Johnston, L. A. (2007). Soluble factors mediate competitive and cooperative interactions between cells expressing different levels of Drosophila Myc. Proc. Natl. Acad. Sci. USA 104, 18543-18548.
97. Shen, J. and Dahmann, C. (2005). Extrusion of cells with inappropriate Dpp signaling from Drosophila wing disc epithelia. Science 307, 1789-1790.
98. Simpson, P. (1979). Parameters of cell competition in the compartments of the wing disc of Drosophila. Dev. Biol. 69, 182-193.
99. Simpson, P. and Morata, G. (1981). Differential mitotic rates and patterns of growth in compartments in the Drosophila wing. Dev. Biol. 85, 299-308.
100. Slaughter, D. P., Southwick, H. W. and Smejkal, W. (1953). Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer 6, 963-968.
101. Snippert, H. J., van der Flier, L. G., Sato, T., van Es, J. H., van den Born, M., Kroon-Veenboer, C., Barker, N., Klein, A. M., van Rheenen, J., Simons, B. D. et al. (2010). Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143, 134-144.
102. Spencer, S. L., Gaudet, S., Albeck, J. G., Burke, J. M. and Sorger, P. K. (2009). Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 459, 428-432.
103. Steller, H. (2008). Regulation of apoptosis in Drosophila. Cell Death Differ. 15, 1132-1138.
104. Strassmann, J. E. and Queller, D. C. (2011). Evolution of cooperation and control of cheating in a social microbe. Proc. Natl. Acad. Sci. USA 108 Suppl. 2, 10855-10862.
105. Sun, G. and Irvine, K. D. (2011). Regulation of Hippo signaling by Jun kinase signaling during compensatory cell proliferation and regeneration, and in neoplastic tumors. Dev. Biol. 350, 139-151.
106. Tamori, Y. and Deng, W. M. (2013). Tissue repair through cell competition and compensatory cellular hypertrophy in postmitotic epithelia. Dev. Cell 25, 350-363.
107. 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. (2010). Involvement of Lgl and Mahjong/VprBP in cell competition. PLoS Biol. 8, e1000422.
108. Teleman, A. A. and Cohen, S. M. (2000). Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103, 971-980.
109. Tepass, U., Fessler, L. I., Aziz, A. and Hartenstein, V. (1994). Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120, 1829-1837.
110. Thompson, B. J., Mathieu, J., Sung, H. H., Loeser, E., Rørth, P. and Cohen, S. M. (2005). Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9, 711-720.
111. Tyler, D. M., Li, W., Zhuo, N., Pellock, B. and Baker, N. E. (2007). Genes affecting cell competition in Drosophila. Genetics 175, 643-657.
112. Uhlirova, M. and Bohmann, D. (2006). JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J. 25, 5294-5304.
113. Uhlirova, M., Jasper, H. and Bohmann, D. (2005). Non-cell-autonomous induction of tissue overgrowth by JNK/Ras cooperation in a Drosophila tumor model. Proc. Natl. Acad. Sci. USA 102, 13123-13128.
114. Vaccari, T. and Bilder, D. (2005). The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9, 687-698.
115. Verdu, J., Buratovich, M. A., Wilder, E. L. and Birnbaum, M. J. (1999). Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nat. Cell Biol. 1, 500-506.
116. Vincent, J. P., Kolahgar, G., Gagliardi, M. and Piddini, E. (2011). Steep differences in wingless signaling trigger Myc-independent competitive cell interactions. Dev. Cell 21, 366-374.
117. Vincent, J. P., Fletcher, A. G. and Baena-Lopez, L. A. (2013). Mechanisms and mechanics of cell competition in epithelia. Nat. Rev. Mol. Cell Biol. 14, 581-591.
118. Winton, D. J., Blount, M. A. and Ponder, B. A. (1988). A clonal marker induced by mutation in mouse intestinal epithelium. Nature 333, 463-466.
119. Woods, D. F. and Bryant, P. J. (1991). The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66, 451-464.
120. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
121. Yang, L. and Baker, N. E. (2001). Role of the EGFR/Ras/Raf pathway in specification of photoreceptor cells in the Drosophila retina. Development 128, 1183-1191.
122. Yang, L. and Baker, N. E. (2003). Cell cycle withdrawal, progression, and cell survival regulation by EGFR and its effectors in the differentiating Drosophila eye. Dev. Cell 4, 359-369.
123. 2+ channel promotes endocytosis and couples exocytosis to endocytosis. Cell 138, 947-960.
124. Zhang, Y. and Kalderon, D. (2001). Hedgehog acts as a somatic stem cell factor in the Drosophila ovary. Nature 410, 599-604.
125. Zhao, H. and Reed, R. R. (2001). X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104, 651-660.
126. Zhou, Z., Hartwieg, E. and Horvitz, H. R. (2001). CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104, 43-56.
127. Ziosi, M., Baena-López, L. A., Grifoni, D., Froldi, F., Pession, A., Garoia, F., Trotta, V., Bellosta, P., Cavicchi, S. and Pession, A. (2010). dMyc functions downstream of Yorkie to promote the supercompetitive behavior of hippo pathway mutant cells. PLoS Genet. 6, e1001140.
128. Ziv, O., Suissa, Y., Neuman, H., Dinur, T., Geuking, P., Rhiner, C., Portela, M., Lolo, F., Moreno, E. and Gerlitz, O. (2009). The co-regulator dNAB interacts with Brinker to eliminate cells with reduced Dpp signaling. Development 136, 1137-1145.