Loss of Rab5 drives non-autonomous cell proliferation through TNF and Ras signaling in Drosophila

Developmental Biology

Volumn 395, Issue 1, 2014, Pages 19-28

  Takino, Kyoko ^a,b   Ohsawa, Shizue ^a   Igaki, Tatsushi ^a,c  

^a KYOTO UNIVERSITY   (Japan)

^b KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Cell cell interaction; Drosophila; Rab5; Tissue growth regulation; Tumorigenesis

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR; JANUS KINASE; PROTEIN CDC42; PROTEIN UPD; RAB PROTEIN; RAS PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CDC42 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; EIGER PROTEIN, DROSOPHILA; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; HPO PROTEIN, DROSOPHILA; MEMBRANE PROTEIN; OS PROTEIN, DROSOPHILA; PROTEIN SERINE THREONINE KINASE; RAB5 PROTEIN, DROSOPHILA; SIGNAL PEPTIDE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; ENZYME ACTIVITY; EPITHELIUM; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; CONFOCAL MICROSCOPY; DROSOPHILA MELANOGASTER; EYE; GENETICS; HUMAN; IMAGINAL DISC; METABOLISM; MUTATION; RNA INTERFERENCE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; GREEN FLUORESCENT PROTEINS; GTP-BINDING PROTEINS; HUMANS; IMAGINAL DISCS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MODELS, GENETIC; MUTATION; PROTEIN-SERINE-THREONINE KINASES; RAB5 GTP-BINDING PROTEINS; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84907523462     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.09.003     Document Type: Article

References (52)

1. L. Ballesteros-Arias, V. Saavedra, G. Morata, 2013. Cell competition may function either as tumour-suppressing or as tumour-stimulating factor in Drosophila. Oncogene.
2. Bao Y., Hata Y., Ikeda M., Withanage K. Mammalian Hippo pathway: from development to cancer and beyond. J. Biochem. 2011, 149:361-379.
3. Bergmann A., Steller H. Apoptosis, stem cells, and tissue regeneration. Sci. Signal 2010, 3:re8.
4. Bilder D. Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 2004, 18:1909-1925.
5. 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, 17:320-329.
6. Brumby A.M., Richardson H.E. Using Drosophila melanogaster to map human cancer pathways. Nat. Rev. Cancer 2005, 5:626-639.
7. Chan S.W., Lim C.J., Chen L., Chong Y.F., Huang C., Song H., Hong W. The Hippo pathway in biological control and cancer development. J. Cell Physiol. 2011, 226:928-939.
8. Chia W.J., Tang B.L. Emerging roles for Rab family GTPases in human cancer. Biochim. Biophys. Acta 2009, 1795:110-116.
9. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 2003, 3:11-22.
10. Fernandez L.A., Kenney A.M. The Hippo in the room: a new look at a key pathway in cell growth and transformation. Cell Cycle 2010, 9:2292-2299.
11. Floyd S., De Camilli P. Endocytosis proteins and cancer: a potential link?. Trends Cell Biol. 1998, 8:299-301.
12. Giebel B., Wodarz A. Tumor suppressors: control of signaling by endocytosis. Curr. Biol. 2006, 16:R91-92.
13. Halder G., Johnson R.L. Hippo signaling: growth control and beyond. Development 2011, 138:9-22.
14. Haynie J.L., Bryant P. The effects of X-rays on the proliferation dynamics of cells in the imaginal wing disc of Drosophila melanogaster. Rouxs Arch. Dev. Biol. 1977, 183:85-100.
15. Herz H.M., Chen Z., Scherr H., Lackey M., Bolduc C., Bergmann A. vps25 mosaics display non-autonomous cell survival and overgrowth, and autonomous apoptosis. Development 2006, 133:1871-1880.
16. Herz H.M., Woodfield S.E., Chen Z., Bolduc C., Bergmann A. Common and distinct genetic properties of ESCRT-II components in Drosophila. PLoS One 2009, 4:e4165.
17. 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, 21:3009-3018.
18. Igaki T., Pagliarini R.A., Xu T. Loss of cell polarity drives tumor growth and invasion through JNK activation in Drosophila. Curr. Biol. 2006, 16:1139-1146.
19. Igaki T., Pastor-Pareja J.C., Aonuma H., Miura M., Xu T. Intrinsic tumor suppression and epithelial maintenance by endocytic activation of Eiger/TNF signaling in Drosophila. Dev Cell. 2009, 16:458-465.
20. Jacks T., Weinberg R.A. Taking the study of cancer cell survival to a new dimension. Cell 2002, 111:923-925.
21. Karim F.D., Rubin G.M. Ectopic expression of activated Ras1 induces hyperplastic growth and increased cell death in Drosophila imaginal tissues. Development 1998, 125:1-9.
22. Karpowicz P., Perez J., Perrimon N. The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 2010, 137:4135-4145.
23. Kinzler K.W., Vogelstein B. Lessons from hereditary colorectal cancer. Cell 1996, 87:159-170.
24. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
25. Lu H., Bilder D. Endocytic control of epithelial polarity and proliferation in Drosophila. Nat. Cell Biol. 2005, 7:1232-1239.
26. Moberg K.H., Schelble S., Burdick S.K., Hariharan I.K. Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev. Cell 2005, 9:699-710.
27. Mollereau B., Perez-Garijo A., Bergmann A., Miura M., Gerlitz O., Ryoo H.D., Steller H., Morata G. Compensatory proliferation and apoptosis-induced proliferation: a need for clarification. Cell Death Differ. 2013, 20:181.
28. Morata G., Ripoll P. Minutes: mutants of drosophila autonomously affecting cell division rate. Dev. Biol. 1975, 42:211-221.
29. Morata G., Shlevkov E., Perez-Garijo A. Mitogenic signaling from apoptotic cells in Drosophila. Dev. Growth Differ. 2011, 53:168-176.
30. 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, 12:1263-1268.
31. Morrison H.A., Dionne H., Rusten T.E., Brech A., Fisher W.W., Pfeiffer B.D., Celniker S.E., Stenmark H., Bilder D. Regulation of early endosomal entry by the Drosophila tumor suppressors Rabenosyn and Vps45. Mol. Biol. Cell 2008, 19:4167-4176.
32. Mosesson Y., Mills G.B., Yarden Y. Derailed endocytosis: an emerging feature of cancer. Nat. Rev. Cancer 2008, 8:835-850.
33. Ohsawa S., Sato Y., Enomoto M., Nakamura M., Betsumiya A., Igaki T. Mitochondrial defect drives non-autonomous tumour progression through Hippo signalling in Drosophila. Nature 2012, 490:547-551.
34. Ohsawa S., Sugimura K., Takino K., Xu T., Miyawaki A., Igaki T. Elimination of Oncogenic Neighbors by JNK-Mediated Engulfment in Drosophila. Dev. Cell 2011, 20:315-328.
35. Pagliarini R.A., Xu T. A genetic screen in Drosophila for metastatic behavior. Science 2003, 302:1227-1231.
36. Pan D. The hippo signaling pathway in development and cancer. Dev. Cell 2010, 19:491-505.
37. Pastor-Pareja J.C., Xu T. Dissecting social cell biology and tumors using Drosophila genetics. Annu. Rev. Genet. 2013, 47:51-74.
38. Reginensi A., Scott R.P., Gregorieff A., Bagherie-Lachidan M., Chung C., Lim D.S., Pawson T., Wrana J., McNeill H. Yap- and Cdc42-dependent nephrogenesis and morphogenesis during mouse kidney development. PLoS Genet. 2013, 9:e1003380.
39. Staley B.K., Irvine K.D. Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr. Biol. 2010, 20:1580-1587.
40. 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, 350:139-151.
41. Tamori Y., Deng W.M. Cell competition and its implications for development and cancer. J. Genet. Genom. 2011, 38:483-495.
42. Thompson B.J., Mathieu J., Sung H.H., Loeser E., Rorth P., Cohen S.M. Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev Cell. 2005, 9:711-720.
43. Tomas A., Futter C.E., Eden E.R. EGF receptor trafficking: consequences for signaling and cancer. Trends Cell Biol. 2014, 24:26-34.
44. Tseng A.S., Tapon N., Kanda H., Cigizoglu S., Edelmann L., Pellock B., White K., Hariharan I.K. Capicua regulates cell proliferation downstream of the receptor tyrosine kinase/ras signaling pathway. Curr. Biol. 2007, 17:728-733.
45. Uhlirova M., Bohmann D. JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J. 2006, 25:5294-5304.
46. Vaccari T., Bilder D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell. 2005, 9:687-698.
47. Vaccari T., Rusten T.E., Menut L., Nezis I.P., Brech A., Stenmark H., Bilder D. Comparative analysis of ESCRT-I, ESCRT-II and ESCRT-III function in Drosophila by efficient isolation of ESCRT mutants. J. Cell Sci. 2009, 122:2413-2423.
48. Vincent J.P., Fletcher A.G., Baena-Lopez L.A. Mechanisms and mechanics of cell competition in epithelia. Nat. Rev. Mol. Cell Biol. 2013, 14:581-591.
49. Xu T., Rubin G.M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 1993, 117:1223-1237.
50. Zeng Q., Hong W. The emerging role of the hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 2008, 13:188-192.
51. Zhao B., Li L., Lei Q., Guan K.L. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev. 2010, 24:862-874.
52. de Beco S., Ziosi M., Johnston L.A. New frontiers in cell competition. Dev. Dyn. 2012, 241:831-841.