Regulation of cell growth by Notch signaling and its differential requirement in normal vs. tumor-forming stem cells in Drosophila

Genes and Development

Volumn 25, Issue 24, 2011, Pages 2644-2658

  Song, Yan ^a   Lu, Bingwei ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer stem cell; Cell growth; eIF4E; Neural stem cell; Notch

Indexed keywords

INITIATION FACTOR 4E; NOTCH RECEPTOR; ONCOPROTEIN; PROTEIN D MYC; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CANCER STEM CELL; CELL DEDIFFERENTIATION; CELL GROWTH; CELL RENEWAL; CELL SIZE; DROSOPHILA; FEEDBACK SYSTEM; GROWTH RATE; GROWTH REGULATION; NEUROBLAST; NONHUMAN; OVARY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL; UPREGULATION;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SIZE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; NEOPLASTIC STEM CELLS; NEURAL STEM CELLS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84155197399     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.171959.111     Document Type: Article

References (81)

1. Almeida MS, Bray SJ. 2005. Regulation of post-embryonic neuroblasts by Drosophila Grainyhead. Mech Dev 122: 1282-1293.
2. Arabi A, Wu S, Ridderstrale K, Bierhoff H, Shiue C, Fatyol K, Fahlen S, Hydbring P, Soderberg O, Grummt I, et al. 2005. c-Myc associates with ribosomal DNA and activates RNA polymerase I transcription. Nat Cell Biol 7: 303-310.
3. Assouline S, Culjkovic B, Cocolakis E, Rousseau C, Beslu N, Amri A, Caplan S, Leber B, Roy DC, Miller WH Jr, et al. 2009. Molecular targeting of the oncogene eIF4E in acute myeloid leukemia (AML): A proof-of-principle clinical trial with ribavirin. Blood 114: 257-260.
4. Bailey AM, Posakony JW. 1995. Suppressor of hairless directly activates transcription of enhancer of split complex genes in response to Notch receptor activity. Genes Dev 9: 2609-2622.
5. Bello B, Reichert H, Hirth F. 2006. The brain tumor gene negatively regulates neural progenitor cell proliferation in the larval central brain of Drosophila. Development 133: 2639-2648.
6. Bello BC, Izergina N, Caussinus E, Reichert H. 2008. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev 3: 5. doi: 1186/1749-8104-3-5.
7. Berdnik D, Torok T, Gonzalez-Gaitan M, Knoblich JA. 2002. The endocytic protein a-Adaptin is required for numbmediated asymmetric cell division in Drosophila. Dev Cell 3: 221-231.
8. Betschinger J, Mechtler K, Knoblich JA. 2006. Asymmetric segregation of the tumor suppressor brat regulates selfrenewal in Drosophila neural stem cells. Cell 124: 1241-1253.
9. Boone JQ, Doe CQ. 2008. Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev Neurobiol 68: 1185-1195.
10. Bowman SK, Rolland V, Betschinger J, Kinsey KA, Emery G, Knoblich JA. 2008. The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev Cell 14: 535-546.
11. Cabernard C, Doe CQ. 2009. Apical/basal spindle orientation is required for neuroblast homeostasis and neuronal differentiation in Drosophila. Dev Cell 17: 134-141.
12. Clarke MF, Fuller M. 2006. Stem cells and cancer: Two faces of eve. Cell 124: 1111-1115.
13. Curley MD, Therrien VA, Cummings CL, Sergent PA, Koulouris CR, Friel AM, Roberts DJ, Seiden MV, Scadden DT, Rueda BR, et al. 2009. CD133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells 27: 2875-2883.
14. Fichelson P, Moch C, Ivanovitch K, Martin C, Sidor CM, Lepesant JA, Bellaiche Y, Huynh JR. 2009. Live-imaging of single stem cells within their niche reveals that a U3snoRNP component segregates asymmetrically and is required for self-renewal in Drosophila. Nat Cell Biol 11: 685-693.
15. Fuller MT, Spradling AC. 2007. Male and female Drosophila germline stem cells: Two versions of immortality. Science 316: 402-404.
16. Gao X, Pan D. 2001. TSC1 and TSC2 tumor suppressors antagonize insulin signaling in cell growth. Genes Dev 15: 1383-1392.
17. Gilboa L, Lehmann R. 2004. How different is Venus from Mars? The genetics of germ-line stem cells in Drosophila females and males. Development 131: 4895-4905.
18. Grandori C, Gomez-Roman N, Felton-Edkins ZA, Ngouenet C, Galloway DA, Eisenman RN, White RJ. 2005. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat Cell Biol 7: 311-318.
19. Grewal SS, Li L, Orian A, Eisenman RN, Edgar BA. 2005. Mycdependent regulation of ribosomal RNA synthesis during Drosophila development. Nat Cell Biol 7: 295-302.
20. Harrison H, Farnie G, Howell SJ, Rock RE, Stylianou S, Brennan KR, Bundred NJ, Clarke RB. 2010. Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res 70: 709-718.
21. Hernandez G, Altmann M, Sierra JM, Urlaub H, Diez del Corral R, Schwartz P, Rivera-Pomar R. 2005. Functional analysis of seven genes encoding eight translation initiation factor 4E (eIF4E) isoforms in Drosophila. Mech Dev 122: 529-543.
22. Hu Y, Fortini ME. 2003. Different cofactor activities in g-secretase assembly: Evidence for a nicastrin-Aph-1 subcomplex. J Cell Biol 161: 685-690.
23. Hutterer A, Knoblich JA. 2005. Numb and a-Adaptin regulate Sanpodo endocytosis to specify cell fate in Drosophila external sensory organs. EMBO Rep 6: 836-842.
24. Izergina N, Balmer J, Bello B, Reichert H. 2009. Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural Dev 4: 44. doi: 10.1186/1749-8104-4-44.
25. Kai T, Spradling A. 2004. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428: 564-569.
26. Kai T, Williams D, Spradling AC. 2005. The expression profile of purified Drosophila germline stem cells. Dev Biol 283: 486-502.
27. Kentsis A, Topisirovic I, Culjkovic B, Shao L, Borden KL. 2004. Ribavirin suppresses eIF4E-mediated oncogenic transformation by physical mimicry of the 7-methyl guanosine mRNA cap. Proc Natl Acad Sci 101: 18105-18110.
28. Kirilly D, Xie T. 2007. The Drosophila ovary: An active stem cell community. Cell Res 17: 15-25.
29. Kohlmaier A, Edgar BA. 2008. Proliferative control in Drosophila stem cells. Curr Opin Cell Biol 20: 699-706.
30. Krejci A, Bray S. 2007. Notch activation stimulates transient and selective binding of Su(H)/CSL to target enhancers. Genes Dev 21: 1322-1327.
31. Krejci A, Bernard F, Housden BE, Collins S, Bray SJ. 2009. Direct response to Notch activation: Signaling crosstalk and incoherent logic. Sci Signal 2: ra1. doi: 10.1126/scisignal.2000140.
32. Lazaris-Karatzas A, Montine KS, Sonenberg N. 1990. Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 59 cap. Nature 345: 544-547.
33. Lee T, Luo L. 2001. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci 24: 251-254.
34. Lee CY, Robinson KJ, Doe CQ. 2006a. Lgl, Pins and aPKC regulate neuroblast self-renewal versus differentiation. Nature 439: 594-598.
35. Lee CY, Wilkinson BD, Siegrist SE, Wharton RP, Doe CQ. 2006b. Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast self-renewal. Dev Cell 10: 441-449.
36. Lin H. 1997. The tao of stem cells in the germline. Annu Rev Genet 31: 455-491.
37. Lin H, Yue L, Spradling AC. 1994. The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120: 947-956.
38. Lin CJ, Cencic R, Mills JR, Robert F, Pelletier J. 2008. c-Myc and eIF4F are components of a feedforward loop that links transcription and translation. Cancer Res 68: 5326-5334.
39. Liu N, Han H, Lasko P. 2009. Vasa promotes Drosophila germline stem cell differentiation by activating mei-P26 translation by directly interacting with a (U)-rich motif in its 39 UTR. Genes Dev 23: 2742-2752.
40. Liu HK, Wang Y, Belz T, Bock D, Takacs A, Radlwimmer B, Barbus S, Reifenberger G, Lichter P, Schutz G. 2010. The nuclear receptor tailless induces long-term neural stem cell expansion and brain tumor initiation. Genes Dev 24: 683-695.
41. Lobo NA, Shimono Y, Qian D, Clarke MF. 2007. The biology of cancer stem cells. Annu Rev Cell Dev Biol 23: 675-699.
42. Luo D, Renault VM, Rando TA. 2005. The regulation of Notch signaling in muscle stem cell activation and postnatal myogenesis. Semin Cell Dev Biol 16: 612-622.
43. Maines JZ, Stevens LM, Tong X, Stein D. 2004. Drosophila dMyc is required for ovary cell growth and endoreplication. Development 131: 775-786.
44. Mamane Y, Petroulakis E, Rong L, Yoshida K, Ler LW, Sonenberg N. 2004. eIF4E-from translation to transformation. Oncogene 23: 3172-3179.
45. Maurange C, Cheng L, Gould AP. 2008. Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell 133: 891-902.
46. Miron M, Verdu J, Lachance PE, Birnbaum MJ, Lasko PF, Sonenberg N. 2001. The translational inhibitor 4E-BP is an effector of PI(3)K/Akt signalling and cell growth in Drosophila. Nat Cell Biol 3: 596-601.
47. Mitchell NC, Johanson TM, Cranna NJ, Er AL, Richardson HE, Hannan RD, Quinn LM. 2010. Hfp inhibits Drosophila myc transcription and cell growth in a TFIIH/Hay-dependent manner. Development 137: 2875-2884.
48. Mizutani K, Yoon K, Dang L, Tokunaga A, Gaiano N. 2007. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449: 351-355.
49. Neumuller RA, Knoblich JA. 2009. Wicked views on stem cell news. Nat Cell Biol 11: 678-679.
50. Neumuller RA, Betschinger J, Fischer A, Bushati N, Poernbacher I, Mechtler K, Cohen SM, Knoblich JA. 2008. Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature 454: 241-245.
51. Ohlstein B, Spradling A. 2007. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 315: 988-992.
52. Page SL, McKim KS, Deneen B, Van Hook TL, Hawley RS. 2000. Genetic studies of mei-P26 reveal a link between the processes that control germ cell proliferation in both sexes and those that control meiotic exchange in Drosophila. Genetics 155: 1757-1772.
53. Palacios IM, St Johnston D. 2002. Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development 129: 5473-5485.
54. Pardal R, Clarke MF, Morrison SJ. 2003. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3: 895-902.
55. Passegue E, Jamieson CH, Ailles LE, Weissman IL. 2003. Normal and leukemic hematopoiesis: Are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proc Natl Acad Sc 100: 11842-11849.
56. Pfeiffer BD, Jenett A, Hammonds AS, Ngo TT, Misra S, Murphy C, Scully A, Carlson JW, Wan KH, Laverty TR, et al. 2008. Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci 105: 9715-9720.
57. Potter CJ, Huang H, Xu T. 2001. Drosophila Tsc1 functions with Tsc2 to antagonize insulin signaling in regulating cell growth, cell proliferation, and organ size. Cell 105: 357-368.
58. Reya T, Morrison SJ, Clarke MF, Weissman IL. 2001. Stem cells, cancer, and cancer stem cells. Nature 414: 105-111.
59. Rhiner C, Diaz B, Portela M, Poyatos JF, Fernandez-Ruiz I, Lopez-Gay JM, Gerlitz O, Moreno E. 2009. Persistent competition among stem cells and their daughters in the Drosophila ovary germline niche. Development 136: 995-1006.
60. Ruggero D, Montanaro L, Ma L, Xu W, Londei P, Cordon-Cardo C, Pandolfi PP. 2004. The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat Med 10: 484-486.
61. San-Juan BP, Baonza A. 2011. The bHLH factor deadpan is a direct target of Notch signaling and regulates neuroblast self-renewal in Drosophila. Dev Biol 352: 70-82.
62. Saucedo LJ, Edgar BA. 2002. Why size matters: Altering cell size. Curr Opin Genet Dev 12: 565-571.
63. Schwamborn JC, Berezikov E, Knoblich JA. 2009. The TRIMNHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136: 913-925.
64. Shen R, Weng C, Yu J, Xie T. 2009. eIF4A controls germline stem cell self-renewal by directly inhibiting BAM function in the Drosophila ovary. Proc Natl Acad Sci 106: 11623-11628.
65. Siegrist SE, Haque NS, Chen CH, Hay BA, Hariharan IK. 2010. Inactivation of both Foxo and reaper promotes long-term adult neurogenesis in Drosophila. Curr Biol 20: 643-648.
66. Singh SK, Clarke ID, Hide T, Dirks PB. 2004. Cancer stem cells in nervous system tumors. Oncogene 23: 7267-7273.
67. Skeath JB, Doe CQ. 1998. Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS. Development 125: 1857-1865.
68. Stocker H, Radimerski T, Schindelholz B, Wittwer F, Belawat P, Daram P, Breuer S, Thomas G, Hafen E. 2003. Rheb is an essential regulator of S6K in controlling cell growth in Drosophila. Nat Cell Biol 5: 559-565.
69. Sulkowski MS, Cooper C, Hunyady B, Jia J, Ogurtsov P, Peck-Radosavljevic M, Shiffman ML, Yurdaydin C, Dalgard O. 2011. Management of adverse effects of Peg-IFN and ribavirin therapy for hepatitis C. Nat Rev Gastroenterol Hepatol 8: 212-223.
70. Tapon N, Ito N, Dickson BJ, Treisman JE, Hariharan IK. 2001. The Drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation. Cell 105: 345-355.
71. Teleman AA, Hietakangas V, Sayadian AC, Cohen SM. 2008. Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metab 7: 21-32.
72. van Riggelen J, Yetil A, Felsher DW. 2010. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer 10: 301-309.
73. Varnum-Finney B, Xu L, Brashem-Stein C, Nourigat C, Flowers D, Bakkour S, Pear WS, Bernstein ID. 2000. Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat Med 6: 1278-1281.
74. Wang H, Somers GW, Bashirullah A, Heberlein U, Yu F, Chia W. 2006. Aurora-A acts as a tumor suppressor and regulates selfrenewal of Drosophila neuroblasts. Genes Dev 20: 3453-3463.
75. Wang H, Ouyang Y, Somers WG, Chia W, Lu B. 2007. Polo inhibits progenitor self-renewal and regulates Numb asymmetry by phosphorylating Pon. Nature 449: 96-100.
76. Wendel HG, Silva RL, Malina A, Mills JR, Zhu H, Ueda T, Watanabe-Fukunaga R, Fukunaga R, Teruya-Feldstein J, Pelletier J, et al. 2007. Dissecting eIF4E action in tumorigenesis. Genes Dev 21: 3232-3237.
77. Weng M, Golden KL, Lee CY. 2010. dFezf/Earmuff maintains the restricted developmental potential of intermediate neural progenitors in Drosophila. Dev Cell 18: 126-135.
78. Wirtz-Peitz F, Nishimura T, Knoblich JA. 2008. Linking cell cycle to asymmetric division: Aurora-A phosphorylates the Par complex to regulate Numb localization. Cell 135: 161-173.
79. Wodarz A, Gonzalez C. 2006. Connecting cancer to the asymmetric division of stem cells. Cell 124: 1121-1123.
80. Wong MD, Jin Z, Xie T. 2005. Molecular mechanisms of germline stem cell regulation. Annu Rev Genet 39: 173-195.
81. Yu X, Zou J, Ye Z, Hammond H, Chen G, Tokunaga A, Mali P, Li YM, Civin C, Gaiano N, et al. 2008. Notch signaling activation in human embryonic stem cells is required for embryonic, but not trophoblastic, lineage commitment. Cell Stem Cell 2: 461-471.