The drosophila nuclear lamina protein otefin is required for germline stem cell survival

Developmental Cell

Volumn 25, Issue 6, 2013, Pages 645-654

  Barton, LacyJ ^a   Pinto, BelindaS ^a   Wallrath, LoriL ^a   Geyer, PamelaK ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAM PROTEIN; DROSOPHILA PROTEIN; NUCLEAR PROTEIN; OTEFIN; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; GENE REPRESSION; GENETIC TRANSCRIPTION; GERM CELL; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; GERM-LINE MUTATION; MEMBRANE PROTEINS; NUCLEAR LAMINA; NUCLEAR PROTEINS; PHENOTYPE; STEM CELLS;

EID: 84879537669     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.05.023     Document Type: Article

References (54)

1. Ashery-Padan R., Ulitzur N., Arbel A., Goldberg M., Weiss A.M., Maus N., Fisher P.A., Gruenbaum Y. Localization and posttranslational modifications of otefin, a protein required for vesicle attachment to chromatin, during Drosophila melanogaster development. Mol. Cell. Biol. 1997, 17:4114-4123.
2. Bakay M., Wang Z., Melcon G., Schiltz L., Xuan J., Zhao P., Sartorelli V., Seo J., Pegoraro E., Angelini C., et al. Nuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration. Brain 2006, 129:996-1013.
3. Bakhrat A., Pritchett T., Peretz G., McCall K., Abdu U. Drosophila Chk2 and p53 proteins induce stage-specific cell death independently during oogenesis. Apoptosis 2010, 15:1425-1434.
4. Baxley R.M., Soshnev A.A., Koryakov D.E., Zhimulev I.F., Geyer P.K. The role of the Suppressor of Hairy-wing insulator protein in Drosophila oogenesis. Dev. Biol. 2011, 356:398-410.
5. Cai M., Huang Y., Ghirlando R., Wilson K.L., Craigie R., Clore G.M. Solution structure of the constant region of nuclear envelope protein LAP2 reveals two LEM-domain structures: one binds BAF and the other binds DNA. EMBO J. 2001, 20:4399-4407.
6. Chen D., McKearin D. Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr. Biol. 2003, 13:1786-1791.
7. Chen D., McKearin D.M. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 2003, 130:1159-1170.
8. Chen S., Wang S., Xie T. Restricting self-renewal signals within the stem cell niche: multiple levels of control. Curr. Opin. Genet. Dev. 2011, 21:684-689.
9. Dansereau D.A., Lasko P. The development of germline stem cells in Drosophila. Methods Mol. Biol. 2008, 450:3-26.
10. Forbes A.J., Spradling A.C., Ingham P.W., Lin H. The role of segment polarity genes during early oogenesis in Drosophila. Development 1996, 122:3283-3294.
11. Geyer P.K., Vitalini M.W., Wallrath L.L. Nuclear organization: taking a position on gene expression. Curr. Opin. Cell Biol. 2011, 23:354-359.
12. Gilboa L., Lehmann R. Repression of primordial germ cell differentiation parallels germ line stem cell maintenance. Curr. Biol. 2004, 14:981-986.
13. Habermann K., Mirgorodskaya E., Gobom J., Lehmann V., Müller H., Blümlein K., Deery M.J., Czogiel I., Erdmann C., Ralser M., et al. Functional analysis of centrosomal kinase substrates in Drosophila melanogaster reveals a new function of the nuclear envelope component otefin in cell cycle progression. Mol. Cell. Biol. 2012, 32:3554-3569.
14. Hanyu-Nakamura K., Kobayashi S., Nakamura A. Germ cell-autonomous Wunen2 is required for germline development in Drosophila embryos. Development 2004, 131:4545-4553.
15. Haraguchi T., Holaska J.M., Yamane M., Koujin T., Hashiguchi N., Mori C., Wilson K.L., Hiraoka Y. Emerin binding to Btf, a death-promoting transcriptional repressor, is disrupted by a missense mutation that causes Emery-Dreifuss muscular dystrophy. Eur. J. Biochem. 2004, 271:1035-1045.
16. Harris R.E., Ashe H.L. Cease and desist: modulating short-range Dpp signalling in the stem-cell niche. EMBO Rep. 2011, 12:519-526.
17. Higuchi Y., Hongou M., Ozawa K., Kokawa H., Masaki M. Afamily of Emery-Dreifuss muscular dystrophy with extreme difference in severity. Pediatr. Neurol. 2005, 32:358-360.
18. Holaska J.M., Lee K.K., Kowalski A.K., Wilson K.L. Transcriptional repressor germ cell-less (GCL) and barrier to autointegration factor (BAF) compete for binding to emerin invitro. J.Biol. Chem. 2003, 278:6969-6975.
19. Jiang X., Xia L., Chen D., Yang Y., Huang H., Yang L., Zhao Q., Shen L., Wang J., Chen D. Otefin, a nuclear membrane protein, determines the fate of germline stem cells in Drosophila via interaction with Smadcomplexes. Dev. Cell 2008, 14:494-506.
20. Kai T., Spradling A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 2004, 428:564-569.
21. Lasko P.F., Ashburner M. The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 1988, 335:611-617.
22. Lin H., Yue L., Spradling A.C. The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 1994, 120:947-956.
23. Lin F., Morrison J.M., Wu W., Worman H.J. MAN1, an integral protein of the inner nuclear membrane, binds Smad2 and Smad3 and antagonizes transforming growth factor-beta signaling. Hum. Mol. Genet. 2005, 14:437-445.
24. Lin F., Blake D.L., Callebaut I., Skerjanc I.S., Holmer L., McBurney M.W., Paulin-Levasseur M., Worman H.J. MAN1, an inner nuclear membrane protein that shares the LEM domain with lamina-associated polypeptide 2 and emerin. J.Biol. Chem. 2000, 275:4840-4847.
25. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
26. Losick V.P., Morris L.X., Fox D.T., Spradling A. Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev. Cell 2011, 21:159-171.
27. Mansharamani M., Wilson K.L. Direct binding of nuclear membrane protein MAN1 to emerin invitro and two modes of binding to barrier-to-autointegration factor. J.Biol. Chem. 2005, 280:13863-13870.
28. Maraldi N.M., Capanni C., Cenni V., Fini M., Lattanzi G. Laminopathies and lamin-associated signaling pathways. J.Cell. Biochem. 2011, 112:979-992.
29. Markiewicz E., Tilgner K., Barker N., van de Wetering M., Clevers H., Dorobek M., Hausmanowa-Petrusewicz I., Ramaekers F.C., Broers J.L., Blankesteijn W.M., et al. The inner nuclear membrane protein emerin regulates beta-catenin activity by restricting its accumulation in the nucleus. EMBO J. 2006, 25:3275-3285.
30. McKearin D.M., Spradling A.C. bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev. 1990, 4(12B):2242-2251.
31. Melcon G., Kozlov S., Cutler D.A., Sullivan T., Hernandez L., Zhao P., Mitchell S., Nader G., Bakay M., Rottman J.N., et al. Loss of emerin at the nuclear envelope disrupts the Rb1/E2F and MyoD pathways during muscle regeneration. Hum. Mol. Genet. 2006, 15:637-651.
32. Mercuri E., Poppe M., Quinlivan R., Messina S., Kinali M., Demay L., Bourke J., Richard P., Sewry C., Pike M., et al. Extreme variability of phenotype in patients with an identical missense mutation in the lamin A/C gene: from congenital onset with severe phenotype to milder classic Emery-Dreifuss variant. Arch. Neurol. 2004, 61:690-694.
33. Meshorer E., Gruenbaum Y. Gone with the Wnt/Notch: stem cells in laminopathies, progeria, and aging. J. Cell Biol. 2008, 181:9-13.
34. Ohlstein B., McKearin D. Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development 1997, 124:3651-3662.
35. Padan R., Nainudel-Epszteyn S., Goitein R., Fainsod A., Gruenbaum Y. Isolation and characterization of the Drosophila nuclear envelope otefin cDNA. J.Biol. Chem. 1990, 265:7808-7813.
36. Pan L., Chen S., Weng C., Call G., Zhu D., Tang H., Zhang N., Xie T. Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell 2007, 1:458-469.
37. Rankin J., Auer-Grumbach M., Bagg W., Colclough K., Nguyen T.D., Fenton-May J., Hattersley A., Hudson J., Jardine P., Josifova D., et al. Extreme phenotypic diversity and nonpenetrance in families with the LMNA gene mutation R644C. Am. J. Med. Genet. A. 2008, 146A:1530-1542.
38. Sahut-Barnola I., Godt D., Laski F.A., Couderc J.L. Drosophila ovary morphogenesis: analysis of terminal filament formation and identification of a gene required for this process. Dev. Biol. 1995, 170:127-135.
39. Sano H., Renault A.D., Lehmann R. Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatases Wunen and Wunen 2. J. Cell Biol. 2005, 171:675-683.
40. Schüpbach T., Wieschaus E. Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 1991, 129:1119-1136.
41. Song X., Xie T. DE-cadherin-mediated cell adhesion is essential for maintaining somatic stem cells in the Drosophila ovary. Proc. Natl. Acad. Sci. USA 2002, 99:14813-14818.
42. Song X., Zhu C.H., Doan C., Xie T. Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 2002, 296:1855-1857.
43. Song X., Wong M.D., Kawase E., Xi R., Ding B.C., McCarthy J.J., Xie T. Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 2004, 131:1353-1364.
44. Song X., Call G.B., Kirilly D., Xie T. Notch signaling controls germline stem cell niche formation in the Drosophila ovary. Development 2007, 134:1071-1080.
45. Sui L., Yang Y. Distinct effects of nuclear membrane localization on gene transcription silencing in Drosophila S2 cells and germ cells. J.Genet. Genomics 2011, 38:55-61.
46. Wagner N., Krohne G. LEM-Domain proteins: new insights into lamin-interacting proteins. Int. Rev. Cytol. 2007, 261:1-46.
47. Wagner N., Schmitt J., Krohne G. Two novel LEM-domain proteins are splice products of the annotated Drosophila melanogaster gene CG9424 (Bocksbeutel). Eur. J. Cell Biol. 2004, 82:605-616.
48. Wheeler M.A., Ellis J.A. Molecular signatures of Emery-Dreifuss muscular dystrophy. Biochem. Soc. Trans. 2008, 36:1354-1358.
49. Wilkinson F.L., Holaska J.M., Zhang Z., Sharma A., Manilal S., Holt I., Stamm S., Wilson K.L., Morris G.E. Emerin interacts invitro with the splicing-associated factor, YT521-B. Eur. J. Biochem. 2003, 270:2459-2466.
50. Willis N.D., Wilson R.G., Hutchison C.J. Lamin A: a putative colonic epithelial stem cell biomarker which identifies colorectal tumours with a more aggressive phenotype. Biochem. Soc. Trans. 2008, 36:1350-1353.
51. Wilson K.L., Foisner R. Lamin-binding Proteins. Cold Spring Harb. Perspect. Biol. 2010, 2:a000554.
52. Worman H.J., Ostlund C., Wang Y. Diseases of the nuclear envelope. Cold Spring Harb. Perspect. Biol. 2010, 2:a000760.
53. Xie T., Spradling A.C. decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 1998, 94:251-260.
54. Zheng R., Ghirlando R., Lee M.S., Mizuuchi K., Krause M., Craigie R. Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleoprotein complex. Proc. Natl. Acad. Sci. USA 2000, 97:8997-9002.