The molecular basis of emerin-emerin and emerin-BAF interactions

Journal of Cell Science

Volumn 127, Issue 18, 2014, Pages 3956-3969

  Berk, Jason M ^a,d   Simon, Dan N ^a,e   Jenkins Houk, Clifton R ^a   Westerbeck, Jason W ^a   Wilson, Katherine L ^a   Carlson, Cathrine R ^b,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OSLO   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d YALE UNIVERSITY   (United States)

^e ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Barrier to autointegration factor; Emerin; Emery Dreifuss muscular dystrophy; Lamin; LEM domain; Nestor Guillermo progeria; Nuclear envelope; Nuclear lamina; Nucleoskeleton

Indexed keywords

BARRIER TO AUTOINTEGRATION FACTOR; EMERIN; LAMIN; LAMIN A; BANF1 PROTEIN, HUMAN; DNA BINDING PROTEIN; MEMBRANE PROTEIN; NUCLEAR PROTEIN; PROTEIN BINDING;

ARTICLE; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; PEPTIDE ANALYSIS; PHENOTYPE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; AMINO ACID SEQUENCE; CHEMISTRY; DIMERIZATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEAR LAMINA; PROTEIN MOTIF;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; DIMERIZATION; DNA-BINDING PROTEINS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR LAMINA; NUCLEAR PROTEINS; PROTEIN BINDING;

EID: 84907048397     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.148247     Document Type: Article

References (54)

1. Amendola, M. and van Steensel, B. (2014). Mechanisms and dynamics of nuclear lamina-genome interactions. Curr. Opin. Cell Biol. 28, 61-68.
2. Bar, D. Z., Davidovich, M., Lamm, A. T., Zer, H., Wilson, K. L. and Gruenbaum, Y. (2014). BAF-1 mobility is regulated by environmental stresses. Mol. Biol. Cell 25, 1127-1136.
3. Barkan, R., Zahand, A. J., Sharabi, K., Lamm, A. T., Feinstein, N., Haithcock, E., Wilson, K. L., Liu, J. and Gruenbaum, Y. (2012). Ce-emerin and LEM-2: essential roles in Caenorhabditis elegans development, muscle function, and mitosis. Mol. Biol. Cell 23, 543-552.
4. Berk, J. M., Maitra, S., Dawdy, A. W., Shabanowitz, J., Hunt, D. F. and Wilson, K. L. (2013a). O-Linked b-N-acetylglucosamine (O-GlcNAc) regulates emerin binding to barrier to autointegration factor (BAF) in a chromatin- and lamin Benriched ''niche''. J. Biol. Chem. 288, 30192-30209.
5. Berk, J. M., Tifft, K. E. and Wilson, K. L. (2013b). The nuclear envelope LEMdomain protein emerin. Nucleus 4, 298-314.
6. Bione, S., Maestrini, E., Rivella, S., Mancini, M., Regis, S., Romeo, G. and Toniolo, D. (1994). Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat. Genet. 8, 323-327.
7. Burke, B. and Stewart, C. L. (2013). The nuclear lamins: flexibility in function. Nat. Rev. Mol. Cell Biol. 14, 13-24.
8. Cai, M., Huang, Y., Suh, J. Y., Louis, J. M., Ghirlando, R., Craigie, R. and Clore, G. M. (2007). Solution NMR structure of the barrier-to-autointegration factor- Emerin complex. J. Biol. Chem. 282, 14525-14535.
9. Cartegni, L., di Barletta, M. R., Barresi, R., Squarzoni, S., Sabatelli, P., Maraldi, N., Mora, M., Di Blasi, C., Cornelio, F., Merlini, L. et al. (1997). Heart-specific localization of emerin: new insights into Emery-Dreifuss muscular dystrophy. Hum. Mol. Genet. 6, 2257-2264.
10. Chang, W., Folker, E. S., Worman, H. J. and Gundersen, G. G. (2013). Emerin organizes actin flow for nuclear movement and centrosome orientation in migrating fibroblasts. Mol. Biol. Cell 24, 3869-3880.
11. Cozzetto, D. and Jones, D. T. (2013). The contribution of intrinsic disorder prediction to the elucidation of protein function. Curr. Opin. Struct. Biol. 23, 467-472.
12. Demmerle, J., Koch, A. J. and Holaska, J. M. (2012). The nuclear envelope protein emerin binds directly to histone deacetylase 3 (HDAC3) and activates HDAC3 activity. J. Biol. Chem. 287, 22080-22088.
13. Dittrich, C. M., Kratz, K., Sendoel, A., Gruenbaum, Y., Jiricny, J. and Hengartner, M. O. (2012). LEM-3 - A LEM domain containing nuclease involved in the DNA damage response in C. elegans. PLoS ONE 7, e24555.
14. Emery, A. E. and Dreifuss, F. E. (1966). Unusual type of benign x-linked muscular dystrophy. J. Neurol. Neurosurg. Psychiatry 29, 338-342
15. Foisner, R. and Gerace, L. (1993). Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73, 1267-1279.
16. Guilluy, C., Osborne, L. D., Van Landeghem, L., Sharek, L., Superfine, R., Garcia- Mata, R. and Burridge, K. (2014). Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat. Cell Biol. 16, 376-381.
17. Haque, F., Mazzeo, D., Patel, J. T., Smallwood, D. T., Ellis, J. A., Shanahan, C. M. and Shackleton, S. (2010). Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes. J. Biol. Chem. 285, 3487-3498.
18. Haraguchi, T., Koujin, T., Segura-Totten, M., Lee, K. K., Matsuoka, Y., Yoneda, Y., Wilson, K. L. and Hiraoka, Y. (2001). BAF is required for emerin assembly into the reforming nuclear envelope. J. Cell Sci. 114, 4575-4585.
19. Ho, C. Y., Jaalouk, D. E., Vartiainen, M. K. and Lammerding, J. (2013). Lamin A/ C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature 497, 507-511.
20. Holaska, J. M. and Wilson, K. L. (2007). An emerin ''proteome'': purification of distinct emerin-containing complexes from HeLa cells suggests molecular basis for diverse roles including gene regulation, mRNA splicing, signaling, mechanosensing, and nuclear architecture. Biochemistry 46, 8897-8908.
21. Holaska, J. M., Kowalski, A. K. and Wilson, K. L. (2004). Emerin caps the pointed end of actin filaments: evidence for an actin cortical network at the nuclear inner membrane. PLoS Biol. 2, e231.
22. Holaska, J. M., Rais-Bahrami, S. and Wilson, K. L. (2006). Lmo7 is an emerinbinding protein that regulates the transcription of emerin and many other muscle-relevant genes. Hum. Mol. Genet. 15, 3459-3472.
23. Huber, M. D., Guan, T. and Gerace, L. (2009). Overlapping functions of nuclear envelope proteins NET25 (Lem2) and emerin in regulation of extracellular signal-regulated kinase signaling in myoblast differentiation. Mol. Cell. Biol. 29, 5718-5728.
24. Iakoucheva, L. M., Brown, C. J., Lawson, J. D., Obradovic´, Z. and Dunker, A. K. (2002). Intrinsic disorder in cell-signaling and cancer-associated proteins. J. Mol. Biol. 323, 573-584.
25. Lammerding, J., Hsiao, J., Schulze, P. C., Kozlov, S., Stewart, C. L. and Lee, R. T. (2005). Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J. Cell Biol. 170, 781-791.
26. Lazarus, M. B., Nam, Y., Jiang, J., Sliz, P. and Walker, S. (2011). Structure of human O-GlcNAc transferase and its complex with a peptide substrate. Nature 469, 564-567.
27. Lee, K. K., Haraguchi, T., Lee, R. S., Koujin, T., Hiraoka, Y. and Wilson, K. L. (2001). Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J. Cell Sci. 114, 4567-4573.
28. Liu, J., Lee, K. K., Segura-Totten, M., Neufeld, E., Wilson, K. L. and Gruenbaum, Y. (2003). MAN1 and emerin have overlapping function(s) essential for chromosome segregation and cell division in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 100, 4598-4603.
29. Margalit, A., Brachner, A., Gotzmann, J., Foisner, R. and Gruenbaum, Y. (2007). Barrier-to-autointegration factor-a BAFfling little protein. Trends Cell Biol. 17, 202-208.
30. 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. (2006). The inner nuclear membrane protein emerin regulates beta-catenin activity by restricting its accumulation in the nucleus. EMBO J. 25, 3275-3285.
31. Me´ndez-Lo´ pez, I. and Worman, H. J. (2012). Inner nuclear membrane proteins: impact on human disease. Chromosoma 121, 153-167.
32. Meyerzon, M., Fridolfsson, H. N., Ly, N., McNally, F. J. and Starr, D. A. (2009). UNC-83 is a nuclear-specific cargo adaptor for kinesin-1-mediated nuclear migration. Development 136, 2725-2733.
33. Mull, A., Kim, G. and Holaska, J. M. (2014). Lmo7-null mice exhibit phenotypes consistent with Emery-Dreifuss muscular dystrophy. Muscle Nerve [Epub ahead of print] doi:10.1002/mus.24286.
34. Puente, X. S., Quesada, V., Osorio, F. G., Cabanillas, R., Cadiñanos, J., Fraile, J. M., Ordo´ñez, G. R., Puente, D. A., Gutie´rrez-Ferna´ndez, A., Fanjul- Ferna´ndez, M. et al. (2011). Exome sequencing and functional analysis identifies BANF1 mutation as the cause of a hereditary progeroid syndrome. Am. J. Hum. Genet. 88, 650-656.
35. Reil, M. and Dabauvalle, M. C. (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.
36. Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J. and Dunker, A. K. (2001). Sequence complexity of disordered protein. Proteins 42, 38-48.
37. Salpingidou, G., Smertenko, A., Hausmanowa-Petrucewicz, I., Hussey, P. J. and Hutchison, C. J. (2007). A novel role for the nuclear membrane protein emerin in association of the centrosome to the outer nuclear membrane. J. Cell Biol. 178, 897-904.
38. Schreiber, K. H. and Kennedy, B. K. (2013). When lamins go bad: nuclear structure and disease. Cell 152, 1365-1375.
39. Shin, J. Y., Me´ndez-Lo´ pez, I., Wang, Y., Hays, A. P., Tanji, K., Lefkowitch, J. H., Schulze, P. C., Worman, H. J. and Dauer, W. T. (2013). Lamina-associated polypeptide-1 interacts with the muscular dystrophy protein emerin and is essential for skeletal muscle maintenance. Dev. Cell 26, 591-603.
40. Shumaker, D. K., Lee, K. K., Tanhehco, Y. C., Craigie, R. and Wilson, K. L. (2001). LAP2 binds to BAF.DNA complexes: requirement for the LEM domain and modulation by variable regions. EMBO J. 20, 1754-1764.
41. Simon, D. N. and Wilson, K. L. (2011). The nucleoskeleton as a genomeassociated dynamic 'network of networks'. Nat. Rev. Mol. Cell Biol. 12, 695-708.
42. Simon, D. N., Zastrow, M. S. and Wilson, K. L. (2010). Direct actin binding to Aand B-type lamin tails and actin filament bundling by the lamin A tail. Nucleus 1, 264-272.
43. Takemaru, K. I. and Moon, R. T. (2000). The transcriptional coactivator CBP interacts with beta-catenin to activate gene expression. J. Cell Biol. 149, 249-254.
44. Tifft, K. E., Bradbury, K. A. and Wilson, K. L. (2009). Tyrosine phosphorylation of nuclear-membrane protein emerin by Src, Abl and other kinases. J. Cell Sci. 122, 3780-3790.
45. Trinidad, J. C., Barkan, D. T., Gulledge, B. F., Thalhammer, A., Sali, A., Schoepfer, R. and Burlingame, A. L. (2012). Global identification and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse. Mol. Cell Proteomics 11, 215-229.
46. Tsuchiya, Y., Hase, A., Ogawa, M., Yorifuji, H. and Arahata, K. (1999). Distinct regions specify the nuclear membrane targeting of emerin, the responsible protein for Emery-Dreifuss muscular dystrophy. Eur. J. Biochem. 259, 859-865.
47. Uversky, V. N. (2013). A decade and a half of protein intrinsic disorder: biology still waits for physics. Protein Sci. 22, 693-724.
48. Uversky, V. N., Oldfield, C. J. and Dunker, A. K. (2008). Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu. Rev. Biophys. 37, 215-246.
49. Wagner, N. and Krohne, G. (2007). LEM-Domain proteins: new insights into lamin-interacting proteins. Int. Rev. Cytol. 261, 1-46.
50. Wanichawan, P., Louch, W. E., Hortemo, K. H., Austbø, B., Lunde, P. K., Scott, J. D., Sejersted, O. M. and Carlson, C. R. (2011). Full-length cardiac Na+/ Ca2+ exchanger 1 protein is not phosphorylated by protein kinase A. Am. J. Physiol. 300, C989-C997.
51. Wheeler, M. A., Davies, J. D., Zhang, Q., Emerson, L. J., Hunt, J., Shanahan, C. M. and Ellis, J. A. (2007). Distinct functional domains in nesprin-1alpha and nesprin-2beta bind directly to emerin and both interactions are disrupted in Xlinked Emery-Dreifuss muscular dystrophy. Exp. Cell Res. 313, 2845-2857.
52. Wheeler, M. A., Warley, A., Roberts, R. G., Ehler, E. and Ellis, J. A. (2010). Identification of an emerin-beta-catenin complex in the heart important for intercalated disc architecture and beta-catenin localisation. Cell. Mol. Life Sci. 67, 781-796.
53. Wozniak, M. A., Baker, B. M., Chen, C. S. and Wilson, K. L. (2013). The emerinbinding transcription factor Lmo7 is regulated by association with p130Cas at focal adhesions. PeerJ. 1, e134.
54. Xue, B., Dunbrack, R. L., Williams, R. W., Dunker, A. K. and Uversky, V. N. (2010). PONDR-FIT: a meta-predictor of intrinsically disordered amino acids. Biochim. Biophys. Acta 1804, 996-1010.