FACS Purification and Transcriptome Analysis of Drosophila Neural Stem Cells Reveals a Role for Klumpfuss in Self-Renewal

Cell Reports

Volumn 2, Issue 2, 2012, Pages 407-418

  Berger, Christian ^a,d   Harzer, Heike ^a   Burkard, Thomas R ^a   Steinmann, Jonas ^a   van der Horst, Suzanne ^a   Laurenson, Anne Sophie ^c   Novatchkova, Maria ^a,b   Reichert, Heinrich ^c   Knoblich, Juergen A ^a  

^a INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c UNIVERSITY OF BASEL   (Switzerland)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

KLUMPFUSS PROTEIN; MESSENGER RNA; NOTCH RECEPTOR; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN TUMOR; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL RENEWAL; CELL TYPE; CHROMATIN; CONTROLLED STUDY; DROSOPHILA; EMBRYO; FLUORESCENCE ACTIVATED CELL SORTING; GENE OVEREXPRESSION; GROWTH REGULATION; INVERTEBRATE; NEURAL STEM CELL; NEUROBIOLOGY; NEUROBLAST; NONHUMAN; PROTEIN FUNCTION; RNA INTERFERENCE; RNA SEQUENCE; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; NEURAL STEM CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

INVERTEBRATA;

EID: 84865761331     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.07.008     Document Type: Article

References (61)

1. Almeida M.S., Bray S.J. Regulation of post-embryonic neuroblasts by Drosophila Grainyhead. Mech. Dev. 2005, 122:1282-1293.
2. Arbouzova N.I., Bach E.A., Zeidler M.P. Ken & barbie selectively regulates the expression of a subset of Jak/STAT pathway target genes. Curr. Biol. 2006, 16:80-88.
3. Barolo S., Carver L.A., Posakony J.W. GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques 2000, 29. 726, 728, 730, 732.
4. Bello B., Reichert H., Hirth F. The brain tumor gene negatively regulates neural progenitor cell proliferation in the larval central brain of Drosophila. Development 2006, 133:2639-2648.
5. Bello B.C., Izergina N., Caussinus E., Reichert H. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev. 2008, 3:5.
6. Betschinger J., Mechtler K., Knoblich J.A. Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 2006, 124:1241-1253.
7. Boone J.Q., Doe C.Q. Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev. Neurobiol. 2008, 68:1185-1195.
8. Bowman S.K., Rolland V., Betschinger J., Kinsey K.A., Emery G., Knoblich J.A. The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev. Cell 2008, 14:535-546.
9. Bryant Z., Subrahmanyan L., Tworoger M., LaTray L., Liu C.R., Li M.J., van den Engh G., Ruohola-Baker H. Characterization of differentially expressed genes in purified Drosophila follicle cells: toward a general strategy for cell type-specific developmental analysis. Proc. Natl. Acad. Sci. USA 1999, 96:5559-5564.
10. Calvi B.R., Lilly M.A. Fluorescent BrdU labeling and nuclear flow sorting of the Drosophila ovary. Methods Mol. Biol. 2004, 247:203-213.
11. Carney T.D., Miller M.R., Robinson K.J., Bayraktar O.A., Osterhout J.A., Doe C.Q. Functional genomics identifies neural stem cell sub-type expression profiles and genes regulating neuroblast homeostasis. Dev. Biol. 2012, 361:137-146.
12. Caussinus E., Gonzalez C. Induction of tumor growth by altered stem-cell asymmetric division in Drosophila melanogaster. Nat. Genet. 2005, 37:1125-1129.
13. Cenci C., Gould A.P. Drosophila Grainyhead specifies late programmes of neural proliferation by regulating the mitotic activity and Hox-dependent apoptosis of neuroblasts. Development 2005, 132:3835-3845.
14. Ceron J., Tejedor F.J., Moya F. A primary cell culture of Drosophila postembryonic larval neuroblasts to study cell cycle and asymmetric division. Eur. J. Cell Biol. 2006, 85:567-575.
15. Chia W., Somers W.G., Wang H. Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis. J. Cell Biol. 2008, 180:267-272.
16. Chintapalli V.R., Wang J., Dow J.A. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 2007, 39:715-720.
17. Choksi S.P., Southall T.D., Bossing T., Edoff K., de Wit E., Fischer B.E., van Steensel B., Micklem G., Brand A.H. Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev. Cell 2006, 11:775-789.
18. Cumberledge S., Krasnow M.A. Preparation and analysis of pure cell populations from Drosophila. Methods Cell Biol. 1994, 44:143-159.
19. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
20. Doe C.Q. Neural stem cells: balancing self-renewal with differentiation. Development 2008, 135:1575-1587.
21. Faith J.J., Hayete B., Thaden J.T., Mogno I., Wierzbowski J., Cottarel G., Kasif S., Collins J.J., Gardner T.S. Large-scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLoS Biol. 2007, 5:e8.
22. Gonzalez C. Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nat. Rev. Genet. 2007, 8:462-472.
23. González-Gaitán M., Jäckle H. Role of Drosophila α-adaptin in presynaptic vesicle recycling. Cell 1997, 88:767-776.
24. Haley B., Hendrix D., Trang V., Levine M. A simplified miRNA-based gene silencing method for Drosophila melanogaster. Dev. Biol. 2008, 321:482-490.
25. Hart Y., Antebi Y.E., Mayo A.E., Friedman N., Alon U. Design principles of cell circuits with paradoxical components. Proc. Natl. Acad. Sci. USA 2012, 109:8346-8351.
26. Hilgers V., Perry M.W., Hendrix D., Stark A., Levine M., Haley B. Neural-specific elongation of 3' UTRs during Drosophila development. Proc. Natl. Acad. Sci. USA 2011, 108:15864-15869.
27. Izergina N., Balmer J., Bello B., Reichert H. Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural Dev. 2009, 4:44.
28. Jaiswal H., Conz C., Otto H., Wölfle T., Fitzke E., Mayer M.P., Rospert S. The chaperone network connected to human ribosome-associated complex. Mol. Cell. Biol. 2011, 31:1160-1173.
29. Kai T., Williams D., Spradling A.C. The expression profile of purified Drosophila germline stem cells. Dev. Biol. 2005, 283:486-502.
30. Klein T., Campos-Ortega J.A. klumpfuss, a Drosophila gene encoding a member of the EGR family of transcription factors, is involved in bristle and leg development. Development 1997, 124:3123-3134.
31. Knoblich J.A. Mechanisms of asymmetric stem cell division. Cell 2008, 132:583-597.
32. Knoblich J.A. Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 2010, 11:849-860.
33. Knoblich J.A., Jan L.Y., Jan Y.N. The N terminus of the Drosophila Numb protein directs membrane association and actin-dependent asymmetric localization. Proc. Natl. Acad. Sci. USA 1997, 94:13005-13010.
34. Lee T., Luo L. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 2001, 24:251-254.
35. Lee C.Y., Robinson K.J., Doe C.Q. Lgl, Pins and aPKC regulate neuroblast self-renewal versus differentiation. Nature 2006, 439:594-598.
36. Lee C.Y., Wilkinson B.D., Siegrist S.E., Wharton R.P., Doe C.Q. Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast self-renewal. Dev. Cell 2006, 10:441-449.
37. Lin S., Lai S.L., Yu H.H., Chihara T., Luo L., Lee T. Lineage-specific effects of Notch/Numb signaling in post-embryonic development of the Drosophila brain. Development 2010, 137:43-51.
38. Marei H.E., Althani A., Afifi N., Michetti F., Pescatori M., Pallini R., Casalbore P., Cenciarelli C., Schwartz P., Ahmed A.E. Gene expression profiling of embryonic human neural stem cells and dopaminergic neurons from adult human substantia nigra. PLoS ONE 2011, 6:e28420.
39. Miller M.R., Robinson K.J., Cleary M.D., Doe C.Q. TU-tagging: cell type-specific RNA isolation from intact complex tissues. Nat. Methods 2009, 6:439-441.
40. Neufeld T.P., de la Cruz A.F., Johnston L.A., Edgar B.A. Coordination of growth and cell division in the Drosophila wing. Cell 1998, 93:1183-1193.
41. Neumüller R.A., Richter C., Fischer A., Novatchkova M., Neumüller K.G., Knoblich J.A. Genome-wide analysis of self-renewal in Drosophila neural stem cells by transgenic RNAi. Cell Stem Cell 2011, 8:580-593.
42. 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, 17:1101-1114.
43. Otto H., Conz C., Maier P., Wölfle T., Suzuki C.K., Jenö P., Rücknagel P., Stahl J., Rospert S. The chaperones MPP11 and Hsp70L1 form the mammalian ribosome-associated complex. Proc. Natl. Acad. Sci. USA 2005, 102:10064-10069.
44. Reichert H. Drosophila neural stem cells: cell cycle control of self-renewal, differentiation, and termination in brain development. Results Probl. Cell Differ. 2011, 53:529-546.
45. Roberts A., Trapnell C., Donaghey J., Rinn J.L., Pachter L. Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol. 2011, 12:R22.
46. San-Juán B.P., Baonza A. The bHLH factor deadpan is a direct target of Notch signaling and regulates neuroblast self-renewal in Drosophila. Dev. Biol. 2011, 352:70-82.
47. Shigenobu S., Arita K., Kitadate Y., Noda C., Kobayashi S. Isolation of germline cells from Drosophila embryos by flow cytometry. Dev. Growth Differ. 2006, 48:49-57.
48. Slack C., Somers W.G., Sousa-Nunes R., Chia W., Overton P.M. A mosaic genetic screen for novel mutations affecting Drosophila neuroblast divisions. BMC Genet. 2006, 7:33.
49. Smibert P., Miura P., Westholm J.O., Shenker S., May G., Duff M.O., Zhang D., Eads B.D., Carlson J., Brown J.B., et al. Global patterns of tissue-specific alternative polyadenylation in Drosophila. Cell Rep 2012, 1:277-289.
50. Song H., Goetze S., Bischof J., Spichiger-Haeusermann C., Kuster M., Brunner E., Basler K. Coop functions as a corepressor of Pangolin and antagonizes Wingless signaling. Genes Dev. 2010, 24:881-886.
51. Song Y., Lu B. Regulation of cell growth by Notch signaling and its differential requirement in normal vs. tumor-forming stem cells in Drosophila. Genes Dev. 2011, 25:2644-2658.
52. Sonoda J., Wharton R.P. Drosophila Brain Tumor is a translational repressor. Genes Dev. 2001, 15:762-773.
53. Sousa-Nunes R., Chia W., Somers W.G. Protein phosphatase 4 mediates localization of the Miranda complex during Drosophila neuroblast asymmetric divisions. Genes Dev. 2009, 23:359-372.
54. Srivastava M., Pollard H.B. Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J. 1999, 13:1911-1922.
55. Thiel G., Cibelli G. Regulation of life and death by the zinc finger transcription factor Egr-1. J. Cell. Physiol. 2002, 193:287-292.
56. Tirouvanziam R., Davidson C.J., Lipsick J.S., Herzenberg L.A. Fluorescence-activated cell sorting (FACS) of Drosophila hemocytes reveals important functional similarities to mammalian leukocytes. Proc. Natl. Acad. Sci. USA 2004, 101:2912-2917.
57. Trapnell C., Williams B.A., Pertea G., Mortazavi A., Kwan G., van Baren M.J., Salzberg S.L., Wold B.J., Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28:511-515.
58. Weng M., Golden K.L., Lee C.Y. dFezf/Earmuff maintains the restricted developmental potential of intermediate neural progenitors in Drosophila. Dev. Cell 2010, 18:126-135.
59. Zacharioudaki E., Magadi S.S., Delidakis C. bHLH-O proteins are crucial for Drosophila neuroblast self-renewal and mediate Notch-induced overproliferation. Development 2012, 139:1258-1269.
60. Zhu S., Lin S., Kao C.F., Awasaki T., Chiang A.S., Lee T. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 2006, 127:409-422.
61. Zhu S., Barshow S., Wildonger J., Jan L.Y., Jan Y.N. Ets transcription factor Pointed promotes the generation of intermediate neural progenitors in Drosophila larval brains. Proc. Natl. Acad. Sci. USA 2011, 108:20615-20620.