Several novel nuclear envelope transmembrane proteins identified in skeletal muscle have cytoskeletal associations

Molecular and Cellular Proteomics

Volumn 10, Issue 1, 2011, Pages

  Wilkie, Gavin S ^a   Korfali, Nadia ^a   Swanson, Selene K ^b   Malik, Poonam ^a   Srsen, Vlastimil ^a   Batrakou, Dzmitry G ^a   De Las Heras, Jose ^a   Zuleger, Nikolaj ^a   Kerr, Alastair R W ^a   Florens, Laurence ^b   Schirmer, Eric C ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PROTEOME; NUCLEAR PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS MEMBRANE; CYTOSKELETON; HUMAN; INTERPHASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; ANIMAL; ANTIBODY SPECIFICITY; CELL FRACTIONATION; CELL LINE; CHEMISTRY; CYTOLOGY; DNA MICROARRAY; MASS SPECTROMETRY; METABOLISM; REPRODUCIBILITY; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

RATTUS;

ANIMALS; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL LINE; CYTOSKELETON; HUMANS; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICE; MUSCLE, SKELETAL; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS;

EID: 78651112186     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.003129     Document Type: Article

References (73)

1. Prunuske, A. J., and Ullman, K. S. (2006) The nuclear envelope: form and reformation. Curr. Opin. Cell Biol. 18, 108-116
2. Suntharalingam, M., and Wente, S. R. (2003) Peering through the pore: nuclear pore complex structure, assembly, and function. Dev. Cell 4, 775-789
3. Callan, H. G., and Tomlin, S. G. (1950) Experimental studies on amphibian oocyte nuclei. I. Investigation of the structure of the nuclear membrane by means of the electron microscope. Proc. R. Soc. Lond. B Biol. Sci. 137, 367-378
4. Schirmer, E. C., and Foisner, R. (2007) Proteins that associate with lamins: many faces, many functions. Exp. Cell Res. 313, 2167-2179
5. Stewart, C. L., Roux, K. J., and Burke, B. (2007) Blurring the boundary: the nuclear envelope extends its reach. Science 318, 1408-1412
6. Worman, H. J., and Bonne, G. (2007) "Laminopathies": a wide spectrum of human diseases. Exp. Cell Res. 313, 2121-2133
7. Dorner, D., Gotzmann, J., and Foisner, R. (2007) Nucleoplasmic lamins and their interaction partners, LAP2alpha, Rb, and BAF, in transcriptional regulation. FEBS J. 274, 1362-1373 (Pubitemid 46333746)
8. Lenz-Böhme, B., Wismar, J., Fuchs, S., Reifegerste, R., Buchner, E., Betz, H., and Schmitt, B. (1997) 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. 137, 1001-1016
9. Liu, J., Rolef Ben-Shahar, T., Riemer, D., Treinin, M., Spann, P., Weber, K., Fire, A., and Gruenbaum, Y. (2000) Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol. Biol. Cell 11, 3937-3947
10. Lammerding, J., Schulze, P. C., Takahashi, T., Kozlov, S., Sullivan, T., Kamm, R. D., Stewart, C. L., and Lee, R. T. (2004) Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Investig. 113, 370-378
11. Schirmer, E. C., Guan, T., and Gerace, L. (2001) Involvement of the lamin rod domain in heterotypic lamin interactions important for nuclear organization. J. Cell Biol. 153, 479-489
12. Olins, A. L., Herrmann, H., Lichter, P., Kratzmeier, M., Doenecke, D., and Olins, D. E. (2001) Nuclear envelope and chromatin compositional differences comparing undifferentiated and retinoic acid- and phorbol ester-treated HL-60 cells. Exp. Cell Res. 268, 115-127
13. Schirmer, E. C., and Gerace, L. (2004) The stability of the nuclear lamina polymer changes with the composition of lamin subtypes according to their individual binding strengths. J. Biol. Chem. 279, 42811-42817
14. Lammerding, J., Fong, L. G., Ji, J. Y., Reue, K., Stewart, C. L., Young, S. G., and Lee, R. T. (2006) Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem. 281, 25768-25780
15. Crisp, M., Liu, Q., Roux, K., Rattner, J. B., Shanahan, C., Burke, B., Stahl, P. D., and Hodzic, D. (2006) Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172, 41-53 (Pubitemid 43042628)
16. Starr, D. A., and Fischer, J. A. (2005) KASH 'n Karry: the KASH domain family of cargo-specific cytoskeletal adaptor proteins. BioEssays 27, 1136-1146
17. Starr, D. A., and Han, M. (2002) Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 298, 406-409
18. Bonne, G., Di Barletta, M. R., Varnous, S., Bécane, H. M., Hammouda, E. H., Merlini, L., Muntoni, F., Greenberg, C. R., Gary, F., Urtizberea, J. A., Duboc, D., Fardeau, M., Toniolo, D., and Schwartz, K. (1999) Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet. 21, 285-288 (Pubitemid 29124935)
19. Raffaele Di Barletta, M., Ricci, E., Galluzzi, G., Tonali, P., Mora, M., Morandi, L., Romorini, A., Voit, T., Orstavik, K. H., Merlini, L., Trevisan, C., Biancalana, V., Housmanowa-Petrusewicz, I., Bione, S., Ricotti, R., Schwartz, K., Bonne, G., and Toniolo, D. (2000) Different mutations in the LMNA gene cause autosomal dominant and autosomal recessive Emery-Dreifuss muscular dystrophy. Am. J. Hum. Genet. 66, 1407-1412 (Pubitemid 30468795)
20. Muchir, A., Bonne, G., van der Kooi, A. J., van Meegen, M., Baas, F., Bolhuis, P. A., de Visser, M., and Schwartz, K. (2000) Identification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances (LGMD1B). Hum. Mol. Genet 9, 1453-1459
21. Fatkin, D., MacRae, C., Sasaki, T., Wolff, M. R., Porcu, M., Frenneaux, M., Atherton, J., Vidaillet, H. J., Jr., Spudich, S., De Girolami, U., Seidman, J. G., Seidman, C., Muntoni, F., Müehle, G., Johnson, W., and McDonough, B. (1999) Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease. N. Engl. J. Med. 341, 1715-1724
22. 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
23. 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., Wheeler, M. A., Ellis, J. A., Skepper, J. N., Vorgerd, M., Schlotter-Weigel, B., Weissberg, P. L., Roberts, R. G., Wehnert, M., and Shanahan, C. M. (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
24. Wilhelmsen, K., Litjens, S. H., Kuikman, I., Tshimbalanga, N., Janssen, H., van den Bout, I., Raymond, K., and Sonnenberg, A. (2005) Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J. Cell Biol. 171, 799-810
25. 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
26. Schirmer, E. C., Florens, L., Guan, T., Yates, J. R., 3rd, and Gerace, L. (2003) Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 301, 1380-1382
27. Dreger, M., Bengtsson, L., Schöneberg, T., Otto, H., and Hucho, F. (2001) Nuclear envelope proteomics: novel integral membrane proteins of the inner nuclear membrane. Proc. Natl. Acad. Sci. U.S.A. 98, 11943-11948 (Pubitemid 32959806)
28. Korfali, N., Wilkie, G. S., Swanson, S. K., Srsen, V., Batrakou, D. G., Fairley, E. A., Malik, P., Zuleger, N., Goncharevich, A., de Las Heras, J., Kelly, D. A., Kerr, A. R., Florens, L., and Schirmer, E. C. (September 13, 2010) The leukocyte nuclear envelope proteome varies with cell activation and contains novel transmembrane proteins that affect genome architecture. Mol. Cell. Proteomics 10.1074/mcp.M110.002915
29. Su, A. I., Cooke, M. P., Ching, K. A., Hakak, Y., Walker, J. R., Wiltshire, T., Orth, A. P., Vega, R. G., Sapinoso, L. M., Moqrich, A., Patapoutian, A., Hampton, G. M., Schultz, P. G., and Hogenesch, J. B. (2002) Large-scale analysis of the human and mouse transcriptomes. Proc. Natl. Acad. Sci. U.S.A. 99, 4465-4470
30. Buch, C., Lindberg, R., Figueroa, R., Gudise, S., Onischenko, E., and Hallberg, E. (2009) An integral protein of the inner nuclear membrane localizes to the mitotic spindle in mammalian cells. J. Cell Sci. 122, 2100-2107
31. Wilkie, G. S., and Schirmer, E. C. (2008) Purification of nuclei and preparation of nuclear envelopes from skeletal muscle. Methods Mol. Biol. 463, 23-41
32. Hahn, C. G., and Covault, J. (1990) Isolation of transcriptionally active nuclei from striated muscle using Percoll density gradients. Anal. Biochem. 190, 193-197
33. Florens, L., Korfali, N., and Schirmer, E. C. (2008) Subcellular fractionation and proteomics of nuclear envelopes. Methods Mol. Biol. 432, 117-137
34. Wu, C. C., MacCoss, M. J., Howell, K. E., and Yates, J. R., 3rd (2003) A method for the comprehensive proteomic analysis of membrane proteins. Nat. Biotechnol. 21, 532-538
35. Florens, L., and Washburn, M. P. (2006) Proteomic analysis by multidimensional protein identification technology. Methods Mol. Biol. 328, 159-175
36. McDonald, W. H., Tabb, D. L., Sadygov, R. G., MacCoss, M. J., Venable, J., Graumann, J., Johnson, J. R., Cociorva, D., and Yates, J. R., 3rd (2004) MS1, MS2, and SQT-three unified, compact, and easily parsed file formats for the storage of shotgun proteomic spectra and identifications. Rapid Commun. Mass. Spectrom. 18, 2162-2168
37. Venable, J. D., Dong, M. Q., Wohlschlegel, J., Dillin, A., and Yates, J. R. (2004) Automated approach for quantitative analysis of complex peptide mixtures from tandem mass spectra. Nat. Methods 1, 39-45
38. Eng, J. K., McCormack, A. L., and Yates, J. R., 3rd (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989
39. Tabb, D. L., McDonald, W. H., and Yates, J. R., 3rd (2002) DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26
40. Zybailov, B. L., Florens, L., and Washburn, M. P. (2007) Quantitative shotgun proteomics using a protease with broad specificity and normalized spectral abundance factors. Mol. Biosyst. 3, 354-360
41. Florens, L., Carozza, M. J., Swanson, S. K., Fournier, M., Coleman, M. K., Workman, J. L., and Washburn, M. P. (2006) Analyzing chromatin remodeling complexes using shotgun proteomics and normalized spectral abundance factors. Methods 40, 303-311 (Pubitemid 44709624)
42. Paoletti, A. C., Parmely, T. J., Tomomori-Sato, C., Sato, S., Zhu, D., Conaway, R. C., Conaway, J. W., Florens, L., and Washburn, M. P. (2006) Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors. Proc. Natl. Acad. Sci. U.S.A. 103, 18928-18933
43. Zybailov, B., Mosley, A. L., Sardiu, M. E., Coleman, M. K., Florens, L., and Washburn, M. P. (2006) Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 5, 2339-2347
44. Zhang, Y., Wen, Z., Washburn, M. P., and Florens, L. (2010) Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins. Anal. Chem. 82, 2272-2281
45. Flicek, P., Aken, B. L., Beal, K., Ballester, B., Caccamo, M., Chen, Y., Clarke, L., Coates, G., Cunningham, F., Cutts, T., Down, T., Dyer, S. C., Eyre, T., Fitzgerald, S., Fernandez-Banet, J., Gräf, S., Haider, S., Hammond, M., Holland, R., Howe, K. L., Howe, K., Johnson, N., Jenkinson, A., Kähäri, A., Keefe, D., Kokocinski, F., Kulesha, E., Lawson, D., Longden, I., Megy, K., Meidl, P., Overduin, B., Parker, A., Pritchard, B., Prlic, A., Rice, S., Rios, D., Schuster, M., Sealy, I., Slater, G., Smedley, D., Spudich, G., Trevanion, S., Vilella, A. J., Vogel, J., White, S., Wood, M., Birney, E., Cox, T., Curwen, V., Durbin, R., Fernandez-Suarez, X. M., Herrero, J., Hubbard, T. J., Kasprzyk, A., Proctor, G., Smith, J., Ureta-Vidal, A., and Searle, S. (2008) Ensembl 2008. Nucleic Acids Res. 36, D707-D714
46. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580
47. Carbon, S., Ireland, A., Mungall, C. J., Shu, S., Marshall, B., and Lewis, S. (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25, 288-289
48. Wu, C., Orozco, C., Boyer, J., Leglise, M., Goodale, J., Batalov, S., Hodge, C. L., Haase, J., Janes, J., Huss, J. W., 3rd, and Su, A. I. (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 10, R130
49. Mootha, V. K., Bunkenborg, J., Olsen, J. V., Hjerrild, M., Wisniewski, J. R., Stahl, E., Bolouri, M. S., Ray, H. N., Sihag, S., Kamal, M., Patterson, N., Lander, E. S., and Mann, M. (2003) Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115, 629-640
50. 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
51. Hodzic, D. M., Yeater, D. B., Bengtsson, L., Otto, H., and Stahl, P. D. (2004) Sun2 is a novel mammalian inner nuclear membrane protein. J. Biol. Chem. 279, 25805-25812
52. Manilal, S., Nguyen, T. M., Sewry, C. A., and Morris, G. E. (1996) The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein. Hum. Mol. Genet. 5, 801-808
53. Worman, H. J., Yuan, J., Blobel, G., and Georgatos, S. D. (1988) A lamin B receptor in the nuclear envelope. Proc. Natl. Acad. Sci. U.S.A. 85, 8531-8534
54. Zhang, Q., Skepper, J. N., Yang, F., Davies, J. D., Hegyi, L., Roberts, R. G., Weissberg, P. L., Ellis, J. A., and Shanahan, C. M. (2001) Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J. Cell Sci. 114, 4485-4498
55. Cartegni, L., di Barletta, M. R., Barresi, R., Squarzoni, S., Sabatelli, P., Maraldi, N., Mora, M., Di Blasi, C., Cornelio, F., Merlini, L., Villa, A., Cobianchi, F., and Toniolo, D. (1997) Heart-specific localization of emerin: new insights into Emery-Dreifuss muscular dystrophy. Hum. Mol. Genet 6, 2257-2264
56. Lattanzi, G., Ognibene, A., Sabatelli, P., Capanni, C., Toniolo, D., Columbaro, M., Santi, S., Riccio, M., Merlini, L., Maraldi, N. M., and Squarzoni, S. (2000) Emerin expression at the early stages of myogenic differentiation. Differentiation 66, 208-217
57. 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 (Pubitemid 47443314)
58. Foster, L. J., de Hoog, C. L., Zhang, Y., Zhang, Y., Xie, X., Mootha, V. K., and Mann, M. (2006) A mammalian organelle map by protein correlation profiling. Cell 125, 187-199
59. Schermelleh, L., Carlton, P. M., Haase, S., Shao, L., Winoto, L., Kner, P., Burke, B., Cardoso, M. C., Agard, D. A., Gustafsson, M. G., Leonhardt, H., and Sedat, J. W. (2008) Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320, 1332-1336
60. 2+ handling in intracellular stores. Nature 448, 78-82
61. 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
62. McAllister, R. M., Melnyk, J., Finkelstein, J. Z., Adams, E. C., Jr., and Gardner, M. B. (1969) Cultivation in vitro of cells derived from a human rhabdomyosarcoma. Cancer 24, 520-526
63. Blau, H. M., Pavlath, G. K., Hardeman, E. C., Chiu, C. P., Silberstein, L., Webster, S. G., Miller, S. C., and Webster, C. (1985) Plasticity of the differentiated state. Science 230, 758-766
64. Yaffe, D., and Saxel, O. (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270, 725-727
65. Salina, D., Bodoor, K., Eckley, D. M., Schroer, T. A., Rattner, J. B., and Burke, B. (2002) Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108, 97-107
66. King, M. C., Drivas, T. G., and Blobel, G. (2008) A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 134, 427-438
67. Ohba, T., Nakamura, M., Nishitani, H., and Nishimoto, T. (1999) Self-organization of microtubule asters induced in Xenopus egg extracts by GTP-bound Ran. Science 284, 1356-1358
68. Tsai, M. Y., Wang, S., Heidinger, J. M., Shumaker, D. K., Adam, S. A., Goldman, R. D., and Zheng, Y. (2006) A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 311, 1887-1893
69. Wiese, C., Wilde, A., Moore, M. S., Adam, S. A., Merdes, A., and Zheng, Y. (2001) Role of importin-beta in coupling Ran to downstream targets in microtubule assembly. Science 291, 653-656
70. Wilkie, G. S., and Schirmer, E. C. (2006) Guilt by association: the nuclear envelope proteome and disease. Mol. Cell. Proteomics 5, 1865-1875
71. Bespalova, I. N., Van Camp, G., Bom, S. J., Brown, D. J., Cryns, K., DeWan, A. T., Erson, A. E., Flothmann, K., Kunst, H. P., Kurnool, P., Sivakumaran, T. A., Cremers, C. W., Leal, S. M., Burmeister, M., and Lesperance, M. M. (2001) Mutations in the Wolfram syndrome 1 gene (WFS1) are a common cause of low frequency sensorineural hearing loss. Hum. Mol. Genet. 10, 2501-2508
72. Domènech, E., Gómez-Zaera, M., and Nunes, V. (2002) WFS1 mutations in Spanish patients with diabetes mellitus and deafness. Eur. J. Hum. Genet. 10, 421-426
73. Strom, T. M., Hörtnagel, K., Hofmann, S., Gekeler, F., Scharfe, C., Rabl, W., Gerbitz, K. D., and Meitinger, T. (1998) Diabetes insipidus, diabetes mellitus, optic atrophy and deafness (DIDMOAD) caused by mutations in a novel gene (wolframin) coding for a predicted transmembrane protein. Hum. Mol. Genet. 7, 2021-2028 (Pubitemid 28546409)