Expression of lamina proteins Lamin and Kugelkern suppresses stem cell proliferation

References

• Gruenbaum Y, Foisner R. Lamins: Nuclear intermediate filament proteins with fundamental functions in nuclear mechanics and genome regulation. Annu Rev Biochem. 2015;84:150306093657004-164. doi:10.1146/annurev-biochem-060614-034115.
   Web of Science ®Google Scholar
• Dittmer TA, Misteli T. The lamin protein family. Genome Biol. 2011;12:222. doi:10.1186/gb-2011-12-5-222.
   PubMed Web of Science ®Google Scholar
• Gonzalo S, Kreienkamp R, Askjaer P. Hutchinson-gilford progeria syndrome: A premature aging disease caused by LMNA gene mutations. Ageing Res Rev. 2017;33:18–29. doi:10.1016/j.arr.2016.06.007.
   PubMed Web of Science ®Google Scholar
• Dialynas G, Speese S, Budnik V, et al. The role of Drosophila Lamin C in muscle function and gene expression. Development. 2010;137:3067–77. doi:10.1242/dev.048231.
   PubMed Web of Science ®Google Scholar
• Uchino R, Nonaka Y-K, Horigome T, et al. Loss of Drosophila A-type lamin C initially causes tendon abnormality including disintegration of cytoskeleton and nuclear lamina in muscular defects. Dev Biol. 2013;373:216–27. doi:10.1016/j.ydbio.2012.08.001.
   PubMed Web of Science ®Google Scholar
• Lenz-Böhme B, Wismar J, Fuchs S, et al. Insertional mutation of the Drosophila nuclear lamin Dm0 gene results in defective nuclear envelopes, clustering of nuclear pore complexes, and accumulation of annulate lamellae. J Cell Biol. 1997;137:1001–16. doi:10.1083/jcb.137.5.1001.
   PubMed Web of Science ®Google Scholar
• Brandt A, Papagiannouli F, Wagner N, et al. Developmental control of nuclear size and shape by Kugelkern and Kurzkern. Curr Biol. 2006;16:543–52. doi:10.1016/j.cub.2006.01.051.
   PubMed Web of Science ®Google Scholar
• Brandt A, Krohne G, Grosshans J. The farnesylated nuclear proteins KUGELKERN and LAMIN B promote aging-like phenotypes in Drosophila flies. Aging Cell. 2008;7:541–51. doi:10.1111/j.1474-9726.2008.00406.x.
   PubMed Web of Science ®Google Scholar
• Polychronidou M, Hellwig A, Grosshans J. Farnesylated nuclear proteins Kugelkern and lamin Dm0 affect nuclear morphology by directly interacting with the nuclear membrane. Mol Biol Cell. 2010;21:3409–20. doi:10.1091/mbc.E10-03-0230.
   PubMed Web of Science ®Google Scholar
• Espada J, Varela I, Flores I, et al. Nuclear envelope defects cause stem cell dysfunction in premature-aging mice. J Cell Biol. 2008;181:27–35. doi:10.1083/jcb.200801096.
   PubMed Web of Science ®Google Scholar
• Rosengardten Y, McKenna T, Grochová D, et al. Stem cell depletion in Hutchinson-Gilford progeria syndrome. Aging Cell. 2011;10:1011–20. doi:10.1111/j.1474-9726.2011.00743.x.
   PubMed Web of Science ®Google Scholar
• Xie T, Spradling AC. A niche maintaining germ line stem cells in the Drosophila ovary. Science. 2000;290:328–30. doi:10.1126/science.290.5490.328.
   PubMed Web of Science ®Google Scholar
• Tulina N, Matunis E. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science. 2001;294:2546–9. doi:10.1126/science.1066700.
   PubMed Web of Science ®Google Scholar
• Kiger AA, Jones DL, Schulz C, et al. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science. 2001;294:2542–5. doi:10.1126/science.1066707.
   PubMed Web of Science ®Google Scholar
• Micchelli CA, Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature. 2006;439:475–9. doi:10.1038/nature04371.
   PubMed Web of Science ®Google Scholar
• Ohlstein B, Spradling A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature. 2006;439:470–4. doi:10.1038/nature04333.
   PubMed Web of Science ®Google Scholar
• Kohlmaier A, Fassnacht C, Jin Y, et al. Src kinase function controls progenitor cell pools during regeneration and tumor onset in the Drosophila intestine. Oncogene. 2015;34:2371–84. doi:10.1038/onc.2014.163.
   PubMed Web of Science ®Google Scholar
• Buchon N, Broderick NA, Poidevin M, et al. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe. 2009;5:200–11. doi:10.1016/j.chom.2009.01.003.
   PubMed Web of Science ®Google Scholar
• Lin G, Xu N, Xi R. Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature. 2008;455:1119–23. doi:10.1038/nature07329.
   PubMed Web of Science ®Google Scholar
• Ohlstein B, Spradling A. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science. 2007;315:988–92. doi:10.1126/science.1136606.
   PubMed Web of Science ®Google Scholar
• Jiang H, Patel PH, Kohlmaier A, et al. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell. 2009;137:1343–55. doi:10.1016/j.cell.2009.05.014.
   PubMed Web of Science ®Google Scholar
• Biteau B, Hochmuth CE, Jasper H. JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell. 2008;3:442–55. doi:10.1016/j.stem.2008.07.024.
   PubMed Web of Science ®Google Scholar
• Biteau B, Jasper H. EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development. 2011;138:1045–55. doi:10.1242/dev.056671.
   PubMed Web of Science ®Google Scholar
• Buchon N, Broderick NA, Kuraishi T, et al. Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection. BMC Biol. 2010;8:152. doi:10.1186/1741-7007-8-152.
   PubMed Web of Science ®Google Scholar
• Shaw RL, Kohlmaier A, Polesello C, et al. The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development. 2010;137:4147–58. doi:10.1242/dev.052506.
   PubMed Web of Science ®Google Scholar
• Lin G, Xi R. Intestinal stem cell, muscular niche and Wingless signaling. Fly (Austin). 2008;2:310–2. doi:10.4161/fly.7428.
   PubMed Web of Science ®Google Scholar
• Lin G, Xu N, Xi R. Paracrine unpaired signaling through the JAK/STAT pathway controls self-renewal and lineage differentiation of drosophila intestinal stem cells. J Mol Cell Biol. 2010;2:37–49. doi:10.1093/jmcb/mjp028.
   PubMed Web of Science ®Google Scholar
• Xu N, Wang SQ, Tan D, et al. EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells. Dev Biol. 2011;354:31–43. doi:10.1016/j.ydbio.2011.03.018.
   PubMed Web of Science ®Google Scholar
• Choi NH, Lucchetta E, Ohlstein B. Nonautonomous regulation of Drosophila midgut stem cell proliferation by the insulin-signaling pathway. Proc Natl Acad Sci USA. 2011;108:18702–7. doi:10.1073/pnas.1109348108.
   PubMed Web of Science ®Google Scholar
• Stewart C, Burke B. Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell. 1987;51:383–92. doi:10.1016/0092-8674(87)90634-9.
   PubMed Web of Science ®Google Scholar
• Röber RA, Weber K, Osborn M. Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development. 1989;105:365–78.
   PubMed Web of Science ®Google Scholar
• Rober RA, Sauter H, Weber K, et al. Cells of the cellular immune and hemopoietic system of the mouse lack lamins a/c: distinction versus other somatic cells. J Cell Sci. 1990;95(4):587–598.
   PubMed Web of Science ®Google Scholar
• Zielke N, Korzelius J, van Straaten M, et al. Fly-FUCCI: A versatile tool for studying cell proliferation in complex tissues. Cell Rep. 2014;7:588–98. doi:10.1016/j.celrep.2014.03.020.
   PubMed Web of Science ®Google Scholar
• Ekas LA, Cardozo TJ, Flaherty MS, et al. Characterization of a dominant-active STAT that promotes tumorigenesis in Drosophila. Dev Biol. 2010;344:621–36. doi:10.1016/j.ydbio.2010.05.497.
   PubMed Web of Science ®Google Scholar
• Reich NC. STATs get their move on. JAKSTAT. 2013;2:e27080.
   PubMedGoogle Scholar
• Vogel MJ, Peric-Hupkes D, van Steensel B. Detection of in vivo protein-DNA interactions using DamID in mammalian cells. Nat Protoc. 2007;2:1467–78. doi:10.1038/nprot.2007.148.
   PubMed Web of Science ®Google Scholar
• Peric-Hupkes D, Meuleman W, Pagie L, et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell. 2010;38:603–13. doi:10.1016/j.molcel.2010.03.016.
   PubMed Web of Science ®Google Scholar
• Guelen L, Pagie L, Brasset E, et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature. 2008;453:948–51. doi:10.1038/nature06947.
   PubMed Web of Science ®Google Scholar
• Muñoz-Alarcón A, Pavlovic M, Wismar J, et al. Characterization of lamin mutation phenotypes in Drosophila and comparison to human laminopathies. PLoS One. 2007;2:e532. doi:10.1371/journal.pone.0000532.
   PubMed Web of Science ®Google Scholar
• Osouda S, Nakamura Y, de Saint Phalle B, et al. Null mutants of Drosophila B-type lamin Dm(0) show aberrant tissue differentiation rather than obvious nuclear shape distortion or specific defects during cell proliferation. Dev Biol. 2005;284:219–32. doi:10.1016/j.ydbio.2005.05.022.
   PubMed Web of Science ®Google Scholar
• Lee JM, Jung H-J, Fong LG, et al. Do lamin B1 and lamin B2 have redundant functions? Nucleus. 2014;5:287–92. doi:10.4161/nucl.29615.
   PubMed Web of Science ®Google Scholar
• Lucchetta EM, Ohlstein B. The Drosophila midgut: a model for stem cell driven tissue regeneration. Wiley Interdiscip Rev Dev Biol. 2012;1:781–8. doi:10.1002/wdev.51.
   PubMed Web of Science ®Google Scholar
• Gramates LS, Marygold SJ, Santos GD, et al. FlyBase at 25: looking to the future. Nucleic Acids Res. 2017;45:D663–71. doi:10.1093/nar/gkw1016.
   PubMed Web of Science ®Google Scholar
• Guillemin K, Williams T, Krasnow MA. A nuclear lamin is required for cytoplasmic organization and egg polarity in Drosophila. Nat Cell Biol. 2001;3:848–51. doi:10.1038/ncb0901-848.
   PubMed Web of Science ®Google Scholar
• Prüfert K, Vogel A, Krohne G. The lamin cxxm motif promotes nuclear membrane growth. J Cell Sci. 2004;117:6105–6116. doi:10.1242/jcs.01532.
   PubMed Web of Science ®Google Scholar
• Chen H, Chen X, Zheng Y. The nuclear lamina regulates germline stem cell niche organization via modulation of EGFR signaling. Cell Stem Cell. 2013;13:73–86. doi:10.1016/j.stem.2013.05.003.
   PubMed Web of Science ®Google Scholar
• Risau W, Saumweber H, Symmons P. Monoclonal antibodies against a nuclear membrane protein of Drosophila. Localization by indirect immunofluorescence and detection of antigen using a new protein blotting procedure. Exp Cell Res. 1981;133:47–54. doi:10.1016/0014-4827(81)90355-4.
   PubMed Web of Science ®Google Scholar
• Hou XS, Melnick MB, Perrimon N. Marelle acts downstream of the Drosophila HOP/JAK kinase and encodes a protein similar to the mammalian STATs. Cell. 1996;84:411–9. doi:10.1016/S0092-8674(00)81286-6.
   PubMed Web of Science ®Google Scholar
• Zhang Y, You J, Ren W, et al. Drosophila glypicans Dally and Dally-like are essential regulators for JAK/STAT signaling and Unpaired distribution in eye development. Dev Biol. 2013;375:23–32. doi:10.1016/j.ydbio.2012.12.019.
   PubMed Web of Science ®Google Scholar
• 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;82:605–16. doi:10.1078/0171-9335-00350.
   PubMed Web of Science ®Google Scholar
• Kracklauer MP, Banks SML, Xie X, et al. Drosophila klaroid encodes a SUN domain protein required for Klarsicht localization to the nuclear envelope and nuclear migration in the eye. Fly (Austin). 2007;1:75–85. doi:10.4161/fly.4254.
   PubMed Web of Science ®Google Scholar
• Winkler F, Kriebel M, Clever M, et al. Essential Function of the Serine Hydroxymethyl Transferase (SHMT) Gene During Rapid Syncytial Cell Cycles in Drosophila. G3 (Bethesda). 2017;7:2305–14. doi:10.1534/g3.117.043133.
   PubMedGoogle Scholar
• Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–82. doi:10.1038/nmeth.2019.
   PubMed Web of Science ®Google Scholar