Tyrosine phosphorylation of nuclear-membrane protein emerin by Src, Abl and other kinases

Journal of Cell Science

Volumn 122, Issue 20, 2009, Pages 3780-3790

  Tifft, Kathryn E ^a   Bradbury, Katherine A ^a   Wilson, Katherine L ^a  

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

Author keywords

Abl; Barrier to autointegration factor(BAF); Breast cancer; Cardiomyopathy; Emerin; Emery Dreifuss muscular dystrophy; Her2; Laminopathy; LEM domain; Neuromuscular junction; Nuclear envelope; Src

Indexed keywords

ABELSON KINASE; BARRIER TO AUTOINTEGRATION FACTOR; EMERIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; PHENYLALANINE; PHOSPHOTRANSFERASE; PROTEIN TYROSINE KINASE; RECOMBINANT PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; GENE MUTATION; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MUTANT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; HELA CELLS; HUMANS; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NIH 3T3 CELLS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PHOSPHOTYROSINE; PROTO-ONCOGENE PROTEINS C-ABL; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 70350418612     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.048397     Document Type: Article

References (106)

1. Ahern, C. A., Zhang, J. F., Wookalis, M. J. and Horn, R. (2005). Modulation of the cardiac sodium channel NaV1.5 by Fyn, a Src family tyrosine kinase. Circ. Res. 96, 991-998.
2. Amanchy, R., Kalume, D. E., Iwahori, A., Zhong, J. and Pandey, A. (2005). Phosphoproteome analysis of HeLa cells using stable isotope labeling with amino acids in cell culture (SILAC). J. Proteome Res. 4, 1661-1671.
3. Andrechek, E. R., Hardy, W. R., Girgis-Gabardo, A. A., Perry, R. L., Butler, R., Graham, F. L., Kahn, R. C., Rudnicki, M. A. and Muller, W. J. (2002). ErbB2 is required for muscle spindle and myoblast cell survival. Mol. Cell. Biol. 22, 4714-4722.
4. Apel, E. D., Lewis, R. M., Grady, R. M. and Sanes, J. R. (2000). Syne-1, a dystrophin-and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction. J. Biol. Chem. 275, 31986-31995.
5. Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C. J., McLauchlan, H., Klevernic, I., Arthur, J. S., Alessi, D. R. and Cohen, P. (2007). The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408, 297-315.
6. Bengtsson, L. and Wilson, K. L. (2004). Multiple and surprising new functions for emerin, a nuclear membrane protein. Curr. Opin. Cell Biol. 16, 73-79.
7. 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.
8. Bose, R., Molina, H., Patterson, A. S., Bitok, J. K., Periaswamy, B., Bader, J. S., Pandey, A. and Cole, P. A. (2006). Phosphoproteomic analysis of Her2/neu signaling and inhibition. Proc. Natl. Acad. Sci. USA 103, 9773-9778.
9. Boulven, I., Robin, P., Desmyter, C., Harbon, S. and Leiber, D. (2002). Differential involvement of Src family kinases in pervanadate-mediated responses in rat myometrial cells. Cell. Signal. 14, 341-349.
10. Brill, L. M., Salomon, A. R., Ficarro, S. B., Mukherji, M., Stettler-Gill, M. and Peters, E. C. (2004). Robust phosphoproteomic profiling of tyrosine phosphorylation sites from human T cells using immobilized metal affinity chromatography and tandem mass spectrometry. Anal. Chem. 76, 2763-2772.
11. Browe, D. M. and Baumgarten, C. M. (2003). Stretch of beta 1 integrin activates an outwardly rectifying chloride current via FAK and Src in rabbit ventricular myocytes. J. Gen. Physiol. 122, 689-702.
12. 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.
13. Cantin, G. T., Yi, W., Lu, B., Park, S. K., Xu, T., Lee, J. D. and Yates, J. R., 3rd (2008). Combining protein-based IMAC, peptide-based IMAC, and MudPIT for efficient phosphoproteomic analysis. J. Proteome Res. 7, 1346-1351.
14. Chen, Q. Q., Chen, X. Y., Jiang, Y. Y. and Liu, J. (2005). Identification of novel nuclear localization signal within the ErbB-2 protein. Cell Res. 15, 504-510.
15. Clements, L., Manilal, S., Love, D. R. and Morris, G. E. (2000). Direct interaction between emerin and lamin A. Biochem. Biophys. Res. Commun. 267, 709-714.
16. Crone, S. A., Zhao, Y. Y., Fan, L., Gu, Y., Minamisawa, S., Liu, Y., Peterson, K. L., Chen, J., Kahn, R., Condorelli, G. et al. (2002). ErbB2 is essential in the prevention of dilated cardiomyopathy. Nat. Med. 8, 459-465.
17. D'Angelo, M. A. and Hetzer, M. W. (2006). The role of the nuclear envelope in cellular organization. Cell Mol. Life Sci. 63, 316-332.
18. Daub, H., Olsen, J. V., Bairlein, M., Gnad, F., Oppermann, F. S., Korner, R., Greff, Z., Keri, G., Stemmann, O. and Mann, M. (2008). Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell 31, 438-448.
19. David-Pfeuty, T. and Nouvian-Dooghe, Y. (1995). Highly specific antibody to Rous sarcoma virus src gene product recognizes nuclear and nucleolar antigens in human cells. J. Virol. 69, 1699-1713.
20. David-Pfeuty, T., Bagrodia, S. and Shalloway, D. (1993). Differential localization patterns of myristoylated and nonmyristoylated c-Src proteins in interphase and mitotic c-Src overexpresser cells. J. Cell Sci. 105 613-628.
21. Ellis, J. A., Craxton, M., Yates, J. R. and Kendrick Jones, J. (1998). Aberrant intracellular targeting and cell cycle-dependent phosphorylation of emerin contribute to the Emery-Dreifuss muscular dystrophy phenotype. J. Cell Sci. 111, 781-792.
22. Fairley, E., Kendrick-Jones, J. and Ellis, J. (1999). The Emery-Dreifuss muscular dystrophy phenotype arises from aberrant targeting and binding of emerin at the inner nuclear membrane. J. Cell Sci. 112, 2571-2582.
23. Falcone, G., Ciuffini, L., Gauzzi, M. C., Provenzano, C., Strano, S., Gallo, R., Castellani, L. and Alema, S. (2003). v-Src inhibits myogenic differentiation by interfering with the regulatory network of muscle-specific transcriptional activators at multiple levels. Oncogene 22, 8302-8315.
24. Fantus, I. G., Kadota, S., Deragon, G., Foster, B. and Posner, B. I. (1989). Pervanadate [peroxide(s) of vanadate] mimics insulin action in rat adipocytes via activation of the insulin receptor tyrosine kinase. Biochemistry 28, 8864-8871.
25. 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.
26. Frame, M. C. (2002). Src in cancer: deregulation and consequences for cell behaviour. Biochim. Biophys. Acta 1602, 114-130.
27. Furukawa, K. (1999). LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J. Cell Sci. 112, 2485-2492.
28. Gant, T. M., Harris, C. A. and Wilson, K. L. (1999). Roles of LAP2 proteins in nuclear assembly and DNA replication: truncated LAP2β proteins alter lamina assembly, envelope formation, nuclear size, and DNA replication efficiency in Xenopus laevis extracts. J. Cell Biol. 144, 1083-1096.
29. Grady, R. M., Starr, D. A., Ackerman, G. L., Sanes, J. R. and Han, M. (2005). Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc. Natl. Acad. Sci. USA 102, 4359-4364.
30. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K. and Wilson, K. L. (2005). The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6, 21-31.
31. Guo, A., Villen, J., Kornhauser, J., Lee, K. A., Stokes, M. P., Rikova, K., Possemato, A., Nardone, J., Innocenti, G., Wetzel, R. et al. (2008). Signaling networks assembled by oncogenic EGFR and c-Met. Proc. Natl. Acad. Sci. USA 105, 692-697.
32. 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.
33. Haraguchi, T., Holaska, J. M., Yamane, M., Koujin, T., Hashiguchi, N., Mori, C., Wilson, K. L. and Hiraoka, Y. (2004). Emerin binding to Btf, a death-promoting transcriptional repressor, is disrupted by a missense mutation that causes Emery-Dreifuss muscular dystrophy. Eur. J. Biochem. 271, 1035-1045.
34. Hirano, Y., Segawa, M., Ouchi, F. S., Yamakawa, Y., Furukawa, K., Takeyasu, K. and Horigome, T. (2005). Dissociation of emerin from barrier-to-autointegration factor is regulated through mitotic phosphorylation of emerin in a Xenopus egg cell-free system. J. Biol. Chem. 280, 39925-39933.
35. 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.
36. Holaska, J. M., Lee, K. K., Kowalski, A. K. and Wilson, K. L. (2003). Transcriptional repressor germ cell-less (GCL) and barrier to autointegration factor (BAF) compete for binding to emerin in vitro. J. Biol. Chem. 278, 6969-6975.
37. 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.
38. Holaska, J. M., Rais-Bahrami, S. and Wilson, K. L. (2006). Lmo7 is an emerin-binding protein that regulates the transcription of emerin and many other muscle-relevant genes. Hum. Mol. Genet. 15, 3459-3472.
39. Huyer, G., Liu, S., Kelly, J., Moffat, J., Payette, P., Kennedy, B., Tsaprailis, G., Gresser, M. J. and Ramachandran, C. (1997). Mechanism of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate. J. Biol. Chem. 272, 843-851.
40. Ikeda, K., Nakayama, Y., Togashi, Y., Obata, Y., Kuga, T., Kasahara, K., Fukumoto, Y. and Yamaguchi, N. (2008). Nuclear localization of Lyn tyrosine kinase mediated by inhibition of its kinase activity. Exp. Cell Res. 314, 3392-3404.
41. Kim, H., Chan, R., Dankort, D. L., Zuo, D., Najoukas, M., Park, M. and Muller, W. J. (2005). The c-Src tyrosine kinase associates with the catalytic domain of ErbB-2: implications for ErbB-2 mediated signaling and transformation. Oncogene 24, 7599-7607.
42. Kim, Y. R., Cha, H. Y., Lim, K., Hwang, B. D., Hoe, K. L., Namgung, U. and Park, S. K. (2003). Activation of epidermal growth factor receptor is responsible for pervanadate-induced phospholipase D activation. Exp. Mol. Med. 35, 118-124.
43. 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.
44. Laprise, P., Poirier, E. M., Vezina, A., Rivard, N. and Vachon, P. H. (2002). Merosin-integrin promotion of skeletal myofiber cell survival: differentiation state-distinct involvement of p60Fyn tyrosine kinase and p38alpha stress-activated MAP kinase. J. Cell Physiol. 191, 69-81.
45. Leach, N., Bjerke, S. L., Christensen, D. K., Bouchard, J. M., Mou, F., Park, R., Baines, J., Haraguchi, T. and Roller, R. J. (2007). Emerin is hyperphosphorylated and redistributed in herpes simplex virus type 1-infected cells in a manner dependent on both UL34 and US3. J. Virol. 81, 10792-10803.
46. 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.
47. Leu, M., Bellmunt, E., Schwander, M., Farinas, I., Brenner, H. R. and Muller, U. (2003). Erbb2 regulates neuromuscular synapse formation and is essential for muscle spindle development. Development 130, 2291-2301.
48. Lilien, J. and Balsamo, J. (2005). The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of beta-catenin. Curr. Opin. Cell Biol. 17, 459-465.
49. Lin, W., Sanchez, H. B., Deerinck, T., Morris, J. K., Ellisman, M. and Lee, K. F. (2000). Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proc. Natl. Acad. Sci. USA 97, 1299-1304.
50. Luo, Y., Yang, C., Jin, C., Wang, F. and McKeehan, W. L. (2009). Novel phosphotyrosine targets of FGFR2IIIb signaling. Cell. Signal. 21, 1370-1378.
51. Mansharamani, M. and Wilson, K. L. (2005). Direct binding of nuclear membrane protein MAN1 to emerin in vitro and two modes of binding to barrier-to-autointegration factor. J. Biol. Chem. 280, 13863-13870.
52. 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.
53. 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.
54. Mejat, A., Decostre, V., Li, J., Renou, L., Kesari, A., Hantai, D., Stewart, C. L., Xiao, X., Hoffman, E., Bonne, G. et al. (2009). Lamin A/C-mediated neuromuscular junction defects in Emery-Dreifuss muscular dystrophy. J. Cell Biol. 184, 31-44.
55. Mislow, J. M., Holaska, J. M., Kim, M. S., Lee, K. K., Segura-Totten, M., Wilson, K. L. and McNally, E. M. (2002). Nesprin-1alpha self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett. 525, 135-140.
56. Morris, G. E. and Manilal, S. (1999). Heart to heart: from nuclear proteins to Emery-Dreifuss muscular dystrophy. Hum. Mol. Genet. 8, 1847-1851.
57. Morris, J. B., Hofemeister, H. and O'Hare, P. (2007). Herpes simplex virus infection induces phosphorylation and delocalization of emerin, a key inner nuclear membrane protein. J. Virol. 81, 4429-4437.
58. Muchir, A. and Worman, H. J. (2007). Emery-Dreifuss muscular dystrophy. Curr. Neurol. Neurosci. Rep. 7, 78-83.
59. Muchir, A., Pavlidis, P., Bonne, G., Hayashi, Y. K. and Worman, H. J. (2007). Activation of MAPK in hearts of EMD null mice: similarities between mouse models of X-linked and autosomal dominant Emery Dreifuss muscular dystrophy. Hum. Mol. Genet. 16, 1884-1895.
60. Muchir A., Wu W. and Worman H. J. (2009). Reduced expression of A-type lamins and emerin activates extracellular signal-regulated kinase in cultured cells. Biochim. Biophys. Acta 1792, 75-81.
61. Muratore, K. E., Seeliger, M. A., Wang, Z., Fomina, D., Neiswinger, J., Havranek, J. J., Baker, D., Kuriyan, J. and Cole, P. A. (2009). Comparative analysis of mutant tyrosine kinase chemical rescue. Biochemistry 48, 3378-3386.
62. Negro, A., Brar, B. K. and Lee, K. F. (2004). Essential roles of Her2/erbB2 in cardiac development and function. Recent Prog. Horm. Res. 59, 1-12.
63. Nili, E., Cojocaru, G. S., Kalma, Y., Ginsberg, D., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Berger, R., Shaklai, S., Amariglio, N. et al. (2001). Nuclear membrane protein LAP2beta mediates transcriptional repression alone and together with its binding partner GCL (germ-cell-less). J. Cell Sci. 114, 3297-3307.
64. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P. and Mann, M. (2006). Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648.
65. Otto, H., Dreger, M., Bengtsson, L. and Hucho, F. (2001). Identification of tyrosine-phosphorylated proteins associated with the nuclear envelope. Eur. J. Biochem. 268, 420-428.
66. Ozcelik, C., Erdmann, B., Pilz, B., Wettschureck, N., Britsch, S., Hubner, N., Chien, K. R., Birchmeier, C. and Garratt, A. N. (2002). Conditional mutation of the ErbB2 (HER2) receptor in cardiomyocytes leads to dilated cardiomyopathy. Proc. Natl. Acad. Sci. USA 99, 8880-8885.
67. Pan, C., Gnad, F., Olsen, J. V. and Mann, M. (2008). Quantitative phosphoproteome analysis of a mouse liver cell line reveals specificity of phosphatase inhibitors. Proteomics 8, 4534-4546.
68. Ponomareva, O. N., Ma, H., Vock, V. M., Ellerton, E. L., Moody, S. E., Dakour, R., Chodosh, L. A. and Rimer, M. (2006). Defective neuromuscular synaptogenesis in mice expressing constitutively active ErbB2 in skeletal muscle fibers. Mol. Cell Neurosci. 31, 334-345.
69. Prasad, T. S., Goel, R., Kandasamy, K., Keerthikumar, S., Kumar, S., Mathivanan, S., Telikicherla, D., Raju, R., Shafreen, B., Venugopal, A. et al. (2008). Human Protein Reference Database-2009 update. Nucleic Acids Res. 37, D767-D772.
70. Radha, V., Nambirajan, S. and Swarup, G. (1996). Association of Lyn tyrosine kinase with the nuclear matrix and cell-cycle-dependent changes in matrix-associated tyrosine kinase activity. Eur. J. Biochem. 236, 352-359.
71. Rafalska, I., Zhang, Z., Benderska, N., Wolff, H., Hartmann, A. M., Brack-Werner, R. and Stamm, S. (2004). The intranuclear localization and function of YT521-B is regulated by tyrosine phosphorylation. Hum. Mol. Genet. 13, 1535-1549.
72. Rikova, K., Guo, A., Zeng, Q., Possemato, A., Yu, J., Haack, H., Nardone, J., Lee, K., Reeves, C., Li, Y. et al. (2007). Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131, 1190-1203.
73. Roberts, R. C., Sutherland-Smith, A. J., Wheeler, M. A., Jensen, O. N., Emerson, L. J., Spiliotis, 2nd, Tate, C. G., Kendrick-Jones, J. and Ellis, J. A. (2006). The Emery-Dreifuss muscular dystrophy associated-protein emerin is phosphorylated on serine 49 by protein kinase A. FEBS J. 273, 4562-4575.
74. Rongish, B. J. and Kinsey, W. H. (2000). Transient nuclear localization of Fyn kinase during development in zebrafish. Anat. Rec. 260, 115-123.
75. Roskoski, R., Jr (2005). Src kinase regulation by phosphorylation and dephosphorylation. Biochem. Biophys. Res. Commun. 331, 1-14.
76. Rosoff, W. J. and Swope, S. L. (2002). Role for cellular Src kinase in myoblast proliferation. J. Cell Physiol. 193, 328-339.
77. Rush, J., Moritz, A., Lee, K. A., Guo, A., Goss, V. L., Spek, E. J., Zhang, H., Zha, X. M., Polakiewicz, R. D. and Comb, M. J. (2005). Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 23, 94-101.
78. 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.
79. Schlosser, A., Amanchy, R. and Otto, H. (2006). Identification of tyrosine-phosphorylation sites in the nuclear membrane protein emerin. FEBS J. 273, 3204-3215.
80. Schroder, F., Klein, G., Frank, T., Bastein, M., Indris, S., Karck, M., Drexler, H. and Wollert, K. C. (2004). Src family tyrosine kinases inhibit single L-type: Ca2+ channel activity in human atrial myocytes. J. Mol. Cell Cardiol. 37, 735-745.
81. Seeliger, M. A., Young, M., Henderson, M. N., Pellicena, P., King, D. S., Falick, A. M. and Kuriyan, J. (2005). High yield bacterial expression of active c-Abl and c-Src tyrosine kinases. Protein Sci. 14, 3135-3139.
82. Shaul, Y. (2000). c-Abl: activation and nuclear targets. Cell Death Differ. 7, 10-16.
83. Sheffield, P., Garrard, S. and Derewenda, Z. (1999). Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Protein Expr. Purif. 15, 34-39.
84. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
85. Shu, H., Chen, S., Bi, Q., Mumby, M. and Brekken, D. L. (2004). Identification of phosphoproteins and their phosphorylation sites in the WEHI-231 B lymphoma cell line. Mol. Cell. Proteomics 3, 279-286.
86. 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.
87. Smith, K. L., Dang, C. and Seidman, A. D. (2006). Cardiac dysfunction associated with trastuzumab. Expert Opin. Drug Saf. 5, 619-629.
88. Srinivasan, D. and Plattner, R. (2006). Activation of Abl tyrosine kinases promotes invasion of aggressive breast cancer cells. Cancer Res. 66, 5648-5655.
89. Stein, A. B., Tang, X. L., Guo, Y., Xuan, Y. T., Dawn, B. and Bolli, R. (2004). Delayed adaptation of the heart to stress: late preconditioning. Stroke 35, 2676-2679.
90. Sui, S., Wang, J., Yang, B., Song, L., Zhang, J., Chen, M., Liu, J., Lu, Z., Cai, Y., Chen, S. et al. (2008). Phosphoproteome analysis of the human Chang liver cells using SCX and a complementary mass spectrometric strategy. Proteomics 8, 2024-2034.
91. Tan, M., Li, P., Klos, K. S., Lu, J., Lan, K. H., Nagata, Y., Fang, D., Jing, T. and Yu, D. (2005). ErbB2 promotes Src synthesis and stability: novel mechanisms of Src activation that confer breast cancer metastasis. Cancer Res. 65, 1858-1867.
92. Tan, M., Li, P., Sun, M., Yin, G. and Yu, D. (2006). Upregulation and activation of PKC alpha by ErbB2 through Src promotes breast cancer cell invasion that can be blocked by combined treatment with PKC alpha and Src inhibitors. Oncogene 25, 3286-3295.
93. Tao, W. A., Wollscheid, B., O'Brien, R., Eng, J. K., Li, X. J., Bodenmiller, B., Watts, J. D., Hood, L. and Aebersold, R. (2005). Quantitative phosphoproteome analysis using a dendrimer conjugation chemistry and tandem mass spectrometry. Nat. Methods 2, 591-598.
94. Tsai, C. F., Wang, Y. T., Chen, Y. R., Lai, C. Y., Lin, P. Y., Pan, K. T., Chen, J. Y., Khoo, K. H. and Chen, Y. J. (2008). Immobilized metal affinity chromatography revisited: pH/acid control toward high selectivity in phosphoproteomics. J. Proteome Res. 7, 4058-4069.
95. 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.
96. Vock, V. M., Ponomareva, O. N. and Rimer, M. (2008). Evidence for muscle-dependent neuromuscular synaptic site determination in mammals. J. Neurosci. 28, 3123-3130.
97. Wagner, N. and Krohne, G. (2007). LEM-domain proteins: new insights into lamin-interacting proteins. Int. Rev. Cytol. 261, 1-46.
98. Wang, S. C., Lien, H. C., Xia, W., Chen, I. F., Lo, H. W., Wang, Z., Ali-Seyed, M., Lee, D. F., Bartholomeusz, G., Ou-Yang, F. et al. (2004). Binding at and transactivation of the COX-2 promoter by nuclear tyrosine kinase receptor ErbB-2. Cancer Cell 6, 251-261.
99. 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 X-linked Emery-Dreifuss muscular dystrophy. Exp. Cell Res. 313, 2845-2857.
100. Wilkinson, F. L., Holaska, J. M., Zhang, Z., Sharma, A., Manilal, S., Holt, I., Stamm, S., Wilson, K. L. and Morris, G. E. (2003). Emerin interacts in vitro with the splicing-associated factor, YT521-B. Eur. J. Biochem. 270, 2459-2466.
101. Yang, X. L., Huang, Y. Z., Xiong, W. C. and Mei, L. (2005). Neuregulin-induced expression of the acetylcholine receptor requires endocytosis of ErbB receptors. Mol. Cell Neurosci. 28, 335-346.
102. Yarden, Y. and Sliwkowski, M. X. (2001). Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137.
103. Zhang, Q., Ragnauth, C. D., Skepper, J. N., Worth, N. F., Warren, D. T., Roberts, R. G., Weissberg, P. L., Ellis, J. A. and Shanahan, C. M. (2005). Nesprin-2 is a multi-isomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle. J. Cell Sci. 118, 673-687.
104. Zhang, Q., Bethmann, C., Worth, N. F., Davies, J. D., Wasner, C., Feuer, A., Ragnauth, C. D., Yi, Q., Mellad, J. A., Warren, D. T. et al. (2007). Nesprin-1 and -2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum. Mol. Genet. 16, 2816-2833.
105. Zhang, X., Xu, R., Zhu, B., Yang, X., Ding, X., Duan, S., Xu, T., Zhuang, Y. and Han, M. (2007). Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 134, 901-908.
106. Zhao, Y., Sudol, M., Hanafusa, H. and Krueger, J. (1992). Increased tyrosine kinase activity of c-Src during calcium-induced keratinocyte differentiation. Proc. Natl. Acad. Sci. USA 89, 8298-8302.