Unique and shared functions of nuclear lamina LEM domain proteins in Drosophila

Genetics

Volumn 197, Issue 2, 2014, Pages 653-665

  Barton, Lacy J ^a   Wilmington, Shameika R ^b   Martin, Melinda J ^a   Skopec, Hannah M ^a   Lovander, Kaylee E ^a   Pinto, Belinda S ^c   Geyer, Pamela K ^a  

^a UNIVERSITY OF IOWA   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARRIER TO AUTOINTEGRATION FACTOR; BOCKSBEUTEL PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; MAN1 PROTEIN, DROSOPHILA; MEMBRANE PROTEIN; NUCLEAR PROTEIN; OTEFIN;

ARTICLE; DROSOPHILA; DROSOPHILA MELANOGASTER; MUTANT; NONHUMAN; NUCLEAR LAMINA; NULL ALLELE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; EMBRYOLOGY; FEMALE; FORELIMB; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MUTATION; OVARY; PROTEIN TERTIARY STRUCTURE;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MEMBRANE PROTEINS; MUTATION; NUCLEAR LAMINA; NUCLEAR PROTEINS; OVARY; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; WINGS, ANIMAL;

EID: 84902481610     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.162941     Document Type: Article

References (50)

1. Ashery-Padan, R., N. Ulitzur, A. Arbel, M. Goldberg, A. M. Weiss et al., 1997a Localization and posttranslational modificationsof otefin, a protein required for vesicle attachment to chromatin, during Drosophila melanogaster development. Mol. Cell. Biol. 17: 4114-4123.
2. Ashery-Padan, R., A. M. Weiss, N. Feinstein, and Y. Gruenbaum, 1997b Distinct regions specify the targeting of otefin to the nucleoplasmic side of the nuclear envelope. J. Biol. Chem. 272: 2493-2499.
3. Barkan, R., A. J. Zahand, K. Sharabi, A. T. Lamm, N. Feinstein et al., 2012 Ce-emerin and LEM-2: essential roles in Caenorhabditis elegans development, muscle function, and mitosis. Mol. Biol. Cell 23: 543-552.
4. Barton, L. J., B. S. Pinto, L. L. Wallrath, and P. K. Geyer, 2013 The Drosophila nuclear lamina protein otefin is required for germ line stem cell survival. Dev. Cell 25: 645-654.
5. Baxley, R. M., A. A. Soshnev, D. E. Koryakov, I. F. Zhimulev, and P. K. Geyer, 2011 The role of the Suppressor of Hairy-wing insulator protein in Drosophila oogenesis. Dev. Biol. 356: 398-410.
6. Berk, J. M., K. E. Tifft, and K. L. Wilson, 2013 The nuclear enve lope LEM-domain protein emerin. Nucleus 4: 298-314
7. Brachner, A., J. Braun, M. Ghodgaonkar, D. Castor, L. Zlopasa et al., 2012 The endonuclease Ankle1 requires its LEM and GIY-YIG motifs for DNA cleavage in vivo. J. Cell Sci. 125: 1048-1057
8. Budnik, V., Y. Zhong, and C. F. Wu, 1990 Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J. Neurosci. 10: 3754-3768.
9. Buszczak, M., S. Paterno, D. Lighthouse, J. Bachman, J. Planck et al., 2007 The carnegie protein trap library: a versatile tool for Drosophila developmental studies. Genetics 175: 1505 1531.
10. Cai, M., Y. Huang, R. Ghirlando, K. L. Wilson, R. Craigie et al., 2001 Solution structure of the constant region of nuclear en-velope protein LAP2 reveals two LEM-domain structures: one binds BAF and the other binds DNA. EMBO J. 20: 4399-4407
11. Chen, S., S. Wang, and T. Xie, 2011 Restricting self-renewal sig-nals within the stem cell niche: multiple levels of control. Curr. Opin. Genet. Dev. 21: 684-689.
12. Chintapalli, V. R., J. Wang, and J. A. Dow, 2007 Using FlyAtlas to identify better Drosophila melanogaster models of human dis-ease. Nat. Genet. 39: 715-720.
13. Dialynas, G., K. M. Flannery, L. N. Zirbel, P. L. Nagy, K. D. Mathews et al., 2012 LMNA variants cause cytoplasmic distribution of nuclear pore proteins in Drosophila and human muscle. Hum. Mol. Genet. 21: 1544-1556.
14. Dittrich, C. M., K. Kratz, A. Sendoel, Y. Gruenbaum, J. Jiricny et al., 2012 LEM-3: a LEM domain containing nuclease involved in the DNA damage response in C. elegans. PLoS ONE 7: e24555.
15. Furukawa, K., S. Sugiyama, S. Osouda, H. Goto, M. Inagaki et al., 2003 Barrier-to-autointegration factor plays crucial roles in cell cycle progression and nuclear organization in Drosophila. J. Cell Sci. 116: 3811-3823.
16. Gonzalez, Y., A. Saito, and S. Sazer, 2012 Fission yeast Lem2 and Man1 perform fundamental functions of the animal cell nuclear lamina. Nucleus 3: 60-76.
17. Gruenbaum, Y., K. K. Lee, J. Liu, M. Cohen, and K. L. Wilson, 2002 The expression, lamin-dependent localization and RNAi depletion phenotype for emerin in C. elegans. J. Cell Sci. 115: 923-929.
18. Harris, R. E., and H. L. Ashe, 2011 Cease and desist: modulating short-range Dpp signalling in the stem-cell niche. EMBO Rep. 12: 519-526.
19. Hendzel, M. J., Y. Wei, M. A. Mancini, A. Van Hooser, T. Ranalli et al., 1997 Mitosis-specific phosphorylation of histone H3 ini tiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348-360.
20. Huber, M. D., T. Guan, and L. Gerace, 2009 Overlapping functions of nuclear envelope proteins NET25 (Lem2) and emerin in reg ulation of extracellular signal-regulated kinase signaling in myo blast differentiation. Mol. Cell. Biol. 29: 5718-5728.
21. Jiang, X., L. Xia, D. Chen, Y. Yang, H. Huang et al., 2008 Otefin, a nuclear membrane protein, determines the fate of germline stem cells in Drosophila via interaction with Smad complexes. Dev. Cell 14: 494-506.
22. Korfali, N., G. S. Wilkie, S. K. Swanson, V. Srsen, D. G. Batrakou et al., 2010 The leukocyte nuclear envelope proteome varies with cell activation and contains novel transmembrane proteins that affect genome architecture. Mol. Cell. Proteomics 9: 2571 2585.
23. Laguri, C., B. Gilquin, N. Wolff, R. Romi-Lebrun, K. Courchay et al., 2001 Structural characterization of the LEM motif common to three human inner nuclear membrane proteins. Structure 9: 503-511.
24. Lee, K. K., and K. L. Wilson, 2004 All in the family: evidence for four new LEM-domain proteins Lem2 (NET-25), Lem3, Lem4 and Lem5 in the human genome. Symp. Soc. Exp. Biol. 56: 329-339.
25. Lin, F., D. L. Blake, I. Callebaut, I. S. Skerjanc, L. Holmer et al., 2000 MAN1, an inner nuclear membrane protein that shares the LEM domain with lamina-associated polypeptide 2 and emerin. J. Biol. Chem. 275: 4840-4847.
26. Lin, H., L. Yue, and A. C. Spradling, 1994 The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120: 947-956
27. Liu, J., K. K. Lee, M. Segura-Totten, E. Neufeld, K. L. Wilson et al., 2003 MAN1 and emerin have overlapping function(s) essen tial for chromosome segregation and cell division in Caenorhab ditis elegans. Proc. Natl. Acad. Sci. USA 100: 4598-4603.
28. Livak, K. J., and T. D. Schmittgen, 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)). Method. Methods 25: 402-408.
29. Losick, V. P., L. X. Morris, D. T. Fox, and A. Spradling, 2011 Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev. Cell 21: 159-171.
30. Malik, P., N. Korfali, V. Srsen, V. Lazou, D. G. Batrakou et al., 2010 Cell-specific and lamin-dependent targeting of novel transmembrane proteins in the nuclear envelope. Cell. Mol. Life Sci. 67: 1353-1369.
31. Mansharamani, M., and K. L. Wilson, 2005 Direct binding of nu-clear membrane protein MAN1 to emerin in vitro and two modes of binding to barrier-to-autointegration factor. J. Biol. Chem. 280: 13863-13870.
32. Markiewicz, E., K. Tilgner, N. Barker, M. van de Wetering, H. Clevers et al., 2006 The inner nuclear membrane protein emerin regulates beta-catenin activity by restricting its accumulation in the nucleus. EMBO J. 25: 3275-3285.
33. Montes de Oca, R., K. K. Lee, and K. L. Wilson, 2005 Binding of barrier to autointegration factor (BAF) to histone H3 and se-lected linker histones including H1.1. J. Biol. Chem. 280: 42252-42262.
34. Osada, S., S. Y. Ohmori, and M. Taira, 2003 XMAN1, an inner nuclear membrane protein, antagonizes BMP signaling by inter acting with Smad1 in Xenopus embryos. Development 130: 1783-1794.
35. Pinto, B. S., S. R. Wilmington, E. E. Hornick, L. L. Wallrath, and P. K. Geyer, 2008 Tissue-specific defects are caused by loss of the Drosophila MAN1 LEM domain protein. Genetics 180: 133-145
36. Raju, G. P., N. Dimova, P. S. Klein, and H. C. Huang, 2003 SANE, a novel LEM domain protein, regulates bone morphogenetic protein signaling through interaction with Smad1. J. Biol. Chem. 278: 428-437.
37. Reil, M., and M. C. Dabauvalle, 2013 Essential roles of LEM domain protein MAN1 during organogenesis in Xenopus laevis and overlapping functions of emerin. Eur. J. Cell Biol. 92: 280-294
38. Robertson, H. M., C. R. Preston, R. W. Phillis, D. M. Johnson-Schlitz, W. K. Benz et al., 1988 A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118: 461-470
39. Schirmer, E. C., L. Florens, T. Guan, J. R. Yates, and L. Gerace, 2003 Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 301: 1380-1382.
40. Schulze, S. R., B. Curio-Penny, Y. Li, R. A. Imani, L. Rydberg et al., 2005 Molecular genetic analysis of the nested Drosophila mel anogaster lamin C gene. Genetics 171: 185-196.
41. Schulze, S. R., B. Curio-Penny, S. Speese, G. Dialynas, D. E. Cryderman et al., 2009 A comparative study of Drosophila and human A-type lamins. PLoS ONE 4: e7564.
42. Segura-Totten, M., and K. L. Wilson, 2004 BAF: roles in chroma tin, nuclear structure and retrovirus integration. Trends Cell Biol. 14: 261-266.
43. Solovei, I., A. S. Wang, K. Thanisch, C. S. Schmidt, S. Krebs et al., 2013 LBR and lamin A/C sequentially tether peripheral het erochromatin and inversely regulate differentiation. Cell 152: 584-598.
44. Wagner, N., and G. Krohne, 2007 LEM-Domain proteins: new in sights into lamin-interacting proteins. Int. Rev. Cytol. 261: 1-46
45. Wagner, N., J. Schmitt, and G. Krohne, 2004 Two novel LEM domain proteins are splice products of the annotated Drosophila melanogaster gene CG9424 (Bocksbeutel). Eur. J. Cell Biol. 82: 605-616.
46. Wagner, N., B. Kagermeier, S. Loserth, and G. Krohne, 2006 The Drosophila melanogaster LEM-domain protein MAN1. Eur. J. Cell Biol. 85: 91-105.
47. Wagner, N., A. Weyhersmuller, A. Blauth, T. Schuhmann, M. Heckmann et al., 2010 The Drosophila LEM-domain protein MAN1 antago-nizes BMP signaling at the neuromuscular junction and the wing crossveins. Dev. Biol. 339: 1-13.
48. Wolff, N., B. Gilquin, K. Courchay, I. Callebaut, H. J. Worman et al., 2001 Structural analysis of emerin, an inner nuclear mem-brane protein mutated in X-linked Emery-Dreifuss muscular dys trophy. FEBS Lett. 501: 171-176.
49. Worman, H. J., C. Ostlund, and Y. Wang, 2010 Diseases of the nuclear envelope. Cold Spring Harb. Perspect. Biol. 2: a000760.
50. Zheng, R., R. Ghirlando, M. S. Lee, K. Mizuuchi, M. Krause et al., 2000 Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleoprotein complex. Proc. Natl. Acad. Sci. USA 97: 8997-9002.