A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells

Journal of Cell Biology

Volumn 196, Issue 6, 2012, Pages 801-810

  Roux, Kyle J ^a,b   Kim, Dae In ^a,b   Raida, Manfred ^c   Burke, Brian ^d  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c Agency for Science   (Singapore)

^d INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTIN; HYBRID PROTEIN; INTERMEDIATE FILAMENT PROTEIN; LAMIN A; LIGASE; PROTEIN SLAP 75; UNCLASSIFIED DRUG;

ARTICLE; BIOTINYLATION; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; ENZYME SUBSTRATE; ESCHERICHIA COLI; FEMALE; HELA CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MAMMAL CELL; MASS SPECTROMETRY; MICROENVIRONMENT; NUCLEAR LAMINA; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS; WESTERN BLOTTING;

ANIMALS; BINDING SITES; BIOTIN; BIOTINYLATION; CARBON-NITROGEN LIGASES; ESCHERICHIA COLI PROTEINS; HEK293 CELLS; HUMANS; LAMININ; PROTEIN INTERACTION MAPPING; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS;

ESCHERICHIA COLI; EUKARYOTA; MAMMALIA;

EID: 84860270506     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201112098     Document Type: Article

References (61)

1. Aaronson, R.P., and G. Blobel. 1975. Isolation of nuclear pore complexes in association with a lamina. Proc. Natl. Acad. Sci. USA. 72:1007-1011. http://dx.doi.org/10.1073/pnas.72.3.1007
2. Al-Haboubi, T., D.K. Shumaker, J. Köser, M. Wehnert, and B. Fahrenkrog. 2011. Distinct association of the nuclear pore protein Nup153 with A- and B-type lamins. Nucleus. 2:500-509. http://dx.doi.org/10.4161/nucl.2.5.17913
3. Beckett, D., E. Kovaleva, and P.J. Schatz. 1999. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Sci. 8:921-929. http://dx.doi.org/10.1110/ps.8.4.921
4. Bione, S., E. Maestrini, S. Rivella, M. Mancini, S. Regis, G. Romeo, and D. Toniolo. 1994. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat. Genet. 8:323-327. http://dx.doi.org/10.1038/ng1294-323
5. Bodoor, K., S. Shaikh, D. Salina, W.H. Raharjo, R. Bastos, M. Lohka, and B. Burke. 1999. Sequential recruitment of NPC proteins to the nuclear periphery at the end of mitosis. J. Cell Sci. 112:2253-2264.
6. Bonne, G., M.R. Di Barletta, S. Varnous, H.M. Bécane, E.H. Hammouda, L. Merlini, F. Muntoni, C.R. Greenberg, F. Gary, J.A. Urtizberea, et al. 1999. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet. 21:285-288. http://dx.doi.org/10.1038/6799
7. Bonne, G., E. Mercuri, A. Muchir, A. Urtizberea, H.M. Bécane, D. Recan, L. Merlini, M. Wehnert, R. Boor, U. Reuner, et al. 2000. Clinical and molecular genetic spectrum of autosomal dominant Emery-Dreifuss muscular dystrophy due to mutations of the lamin A/C gene. Ann. Neurol. 48:170-180. http://dx.doi.org/10.1002/1531-8249(200008)48:2<170::AID-ANA6>3.0.CO;2-J
8. Broers, J.L., B.M. Machiels, G.J. van Eys, H.J. Kuijpers, E.M. Manders, R. van Driel, and F.C. Ramaekers. 1999. Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J. Cell Sci. 112:3463-3475.
9. Burke, B., and K.J. Roux. 2009. Nuclei take a position: managing nuclear location. Dev. Cell. 17:587-597. http://dx.doi.org/10.1016/j.devcel.2009.10.018
10. Castano, E., V.V. Philimonenko, M. Kahle, J. Fukalová, A. Kalendová, S. Yildirim, R. Dzijak, H. Dingová-Krásna, and P. Hozák. 2010. Actin complexes in the cell nucleus: new stones in an old field. Histochem. Cell Biol. 133:607-626. http://dx.doi.org/10.1007/s00418-010-0701-2
11. Chapman-Smith, A., and J.E. Cronan Jr. 1999. Molecular biology of biotin attachment to proteins. J. Nutr. 129(2S, Suppl):477S-484S.
12. Choi-Rhee, E., H. Schulman, and J.E. Cronan. 2004. Promiscuous protein biotinylation by Escherichia coli biotin protein ligase. Protein Sci. 13:3043-3050. http://dx.doi.org/10.1110/ps.04911804
13. Crisp, M., Q. Liu, K. Roux, J.B. Rattner, C. Shanahan, B. Burke, P.D. Stahl, and D. Hodzic. 2006. Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172:41-53. http://dx.doi.org/10.1083/jcb.200509124
14. Cronan, J.E. 2005. Targeted and proximity-dependent promiscuous protein biotinylation by a mutant Escherichia coli biotin protein ligase. J. Nutr. Biochem. 16:416-418. http://dx.doi.org/10.1016/j.jnutbio.2005.03.017
15. Daigle, N., J. Beaudouin, L. Hartnell, G. Imreh, E. Hallberg, J. Lippincott-Schwartz, and J. Ellenberg. 2001. Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J. Cell Biol. 154:71-84. http://dx.doi.org/10.1083/jcb.200101089
16. Dechat, T., B. Korbei, O.A. Vaughan, S. Vlcek, C.J. Hutchison, and R. Foisner. 2000. Lamina-associated polypeptide 2alpha binds intranuclear A-type lamins. J. Cell Sci. 113:3473-3484.
17. Dwyer, N., and G. Blobel. 1976. A modified procedure for the isolation of a pore complex-lamina fraction from rat liver nuclei. J. Cell Biol. 70:581-591. http://dx.doi.org/10.1083/jcb.70.3.581
18. Foisner, R., and L. Gerace. 1993. Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell. 73:1267-1279. http://dx.doi.org/10.1016/0092-8674(93)90355-T
19. Gerace, L., and M.D. Huber. 2012. Nuclear lamina at the crossroads of the cytoplasm and nucleus. J. Struct. Biol. 177:24-31. http://dx.doi.org/10.1016/j.jsb.2011.11.007
20. Goldman, R.D., Y. Gruenbaum, R.D. Moir, D.K. Shumaker, and T.P. Spann. 2002. Nuclear lamins: building blocks of nuclear architecture. Genes Dev. 16:533-547. http://dx.doi.org/10.1101/gad.960502
21. Green, N.M. 1963. Avidin. 1. The Use of (14-C)Biotin for Kinetic Studies and for Assay. Biochem. J. 89:585-591.
22. Guan, T., R.H. Kehlenbach, E.C. Schirmer, A. Kehlenbach, F. Fan, B.E. Clurman, N. Arnheim, and L. Gerace. 2000. Nup50, a nucleoplasmically oriented nucleoporin with a role in nuclear protein export. Mol. Cell. Biol. 20:5619-5630. http://dx.doi.org/10.1128/MCB.20.15.5619-5630.2000
23. Gudise, S., R.A. Figueroa, R. Lindberg, V. Larsson, and E. Hallberg. 2011. Samp1 is functionally associated with the LINC complex and A-type lamina networks. J. Cell Sci. 124:2077-2085. http://dx.doi.org/10.1242/jcs.078923
24. Gueneau, L., A.T. Bertrand, J.P. Jais, M.A. Salih, T. Stojkovic, M. Wehnert, M. Hoeltzenbein, S. Spuler, S. Saitoh, A. Verschueren, et al. 2009. Mutations of the FHL1 gene cause Emery-Dreifuss muscular dystrophy. Am. J. Hum. Genet. 85:338-353. http://dx.doi.org/10.1016/j.ajhg.2009.07.015
25. Hase, M.E., and V.C. Cordes. 2003. Direct interaction with nup153 mediates binding of Tpr to the periphery of the nuclear pore complex. Mol. Biol. Cell. 14:1923-1940. http://dx.doi.org/10.1091/mbc.E02-09-0620
26. Holaska, J.M., and K.L. Wilson. 2006. Multiple roles for emerin: implications for Emery-Dreifuss muscular dystrophy. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 288:676-680.
27. Holaska, J.M., K.K. Lee, A.K. Kowalski, and K.L. Wilson. 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. http://dx.doi.org/10.1074/jbc.M208811200
28. Horton, H., I. McMorrow, and B. Burke. 1992. Independent expression and assembly properties of heterologous lamins A and C in murine embryonal carcinomas. Eur. J. Cell Biol. 57:172-183.
29. Krull, S., J. Thyberg, B. Björkroth, H.R. Rackwitz, and V.C. Cordes. 2004. Nucleoporins as components of the nuclear pore complex core structure and Tpr as the architectural element of the nuclear basket. Mol. Biol. Cell. 15:4261-4277. http://dx.doi.org/10.1091/mbc.E04-03-0165
30. Kubben, N., J.W. Voncken, J. Demmers, C. Calis, G. van Almen, Y. Pinto, and T. Misteli. 2010. Identification of differential protein interactors of lamin A and progerin. Nucleus. 1:513-525.
31. Kulman, J.D., M. Satake, and J.E. Harris. 2007. A versatile system for site-specific enzymatic biotinylation and regulated expression of proteins in cultured mammalian cells. Protein Expr. Purif. 52:320-328. http://dx.doi.org/10.1016/j.pep.2006.09.011
32. Kuroishi, T., L. Rios-Avila, V. Pestinger, S.S. Wijeratne, and J. Zempleni. 2011. Biotinylation is a natural, albeit rare, modification of human histones. Mol. Genet. Metab. 104:537-545. http://dx.doi.org/10.1016/j.ymgme.2011.08.030
33. Kwon, K., and D. Beckett. 2000. Function of a conserved sequence motif in biotin holoenzyme synthetases. Protein Sci. 9:1530-1539. http://dx.doi.org/10.1110/ps.9.8.1530
34. Kwon, K., E.D. Streaker, S. Ruparelia, and D. Beckett. 2000. Multiple disordered loops function in corepressor-induced dimerization of the biotin repressor. J. Mol. Biol. 304:821-833. http://dx.doi.org/10.1006/jmbi.2000.4249
35. Lane, M.D., K.L. Rominger, D.L. Young, and F. Lynen. 1964. The enzymatic synthesis of holotranscarboxylase from apotranscarboxylase and (+)-biotin. II. Investigation of the reaction mechanism. J. Biol. Chem. 239:2865-2871.
36. Lee, K.K., T. Haraguchi, R.S. Lee, T. Koujin, Y. Hiraoka, and K.L. Wilson. 2001. Distinct functional domains in emerin bind lamin A and DNAbridging protein BAF. J. Cell Sci. 114:4567-4573.
37. Liu, Q., N. Pante, T. Misteli, M. Elsagga, M. Crisp, D. Hodzic, B. Burke, and K.J. Roux. 2007. Functional association of Sun1 with nuclear pore complexes. J. Cell Biol. 178:785-798. http://dx.doi.org/10.1083/jcb.200704108
38. Mansharamani, M., and K.L. Wilson. 2005. Direct binding of nuclear membrane protein MAN1 to emerin in vitro and two modes of binding to barrier-toautointegration factor. J. Biol. Chem. 280:13863-13870. http://dx.doi.org/10.1074/jbc.M413020200
39. Mechold, U., C. Gilbert, and V. Ogryzko. 2005. Codon optimization of the BirA enzyme gene leads to higher expression and an improved efficiency of biotinylation of target proteins in mammalian cells. J. Biotechnol. 116:245-249. http://dx.doi.org/10.1016/j.jbiotec.2004.12.003
40. Moir, R.D., M. Yoon, S. Khuon, and R.D. Goldman. 2000. Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J. Cell Biol. 151:1155-1168. http://dx.doi.org/10.1083/jcb.151.6.1155
41. Montes de Oca, R., C.J. Shoemaker, M. Gucek, R.N. Cole, and K.L. Wilson. 2009. Barrier-to-autointegration factor proteome reveals chromatin-regulatory partners. PLoS ONE. 4:e7050. http://dx.doi.org/10.1371/journal.pone.0007050
42. Nesbeth, D., S.L. Williams, L. Chan, T. Brain, N.K. Slater, F. Farzaneh, and D. Darling. 2006. Metabolic biotinylation of lentiviral pseudotypes for scalable paramagnetic microparticle-dependent manipulation. Mol. Ther. 13:814-822. http://dx.doi.org/10.1016/j.ymthe.2005.09.016
43. Raffaele Di Barletta, M., E. Ricci, G. Galluzzi, P. Tonali, M. Mora, L. Morandi, A. Romorini, T. Voit, K.H. Orstavik, L. Merlini, et al. 2000. Different mutations in the LMNA gene cause autosomal dominant and autosomal recessive Emery-Dreifuss muscular dystrophy. Am. J. Hum. Genet. 66: 1407-1412. http://dx.doi.org/10.1086/302869
44. Rasala, B.A., C. Ramos, A. Harel, and D.J. Forbes. 2008. Capture of AT-rich chromatin by ELYS recruits POM121 and NDC1 to initiate nuclear pore assembly. Mol. Biol. Cell. 19:3982-3996. http://dx.doi.org/10.1091/mbc.E08-01-0012
45. Roux, K.J., M.L. Crisp, Q. Liu, D. Kim, S. Kozlov, C.L. Stewart, and B. Burke. 2009. Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc. Natl. Acad. Sci. USA. 106:2194-2199. http://dx.doi.org/10.1073/pnas.0808602106
46. Sang, L., J.J. Miller, K.C. Corbit, R.H. Giles, M.J. Brauer, E.A. Otto, L.M. Baye, X. Wen, S.J. Scales, M. Kwong, et al. 2011. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell. 145:513-528. http://dx.doi.org/10.1016/j.cell.2011.04.019
47. Schirmer, E.C., L. Florens, T. Guan, J.R. Yates III, and L. Gerace. 2003. Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science. 301:1380-1382. http://dx.doi.org/10.1126/science.1088176
48. Segura-Totten, M., A.K. Kowalski, R. Craigie, and K.L. Wilson. 2002. Barrier-to-autointegration factor: major roles in chromatin decondensation and nuclear assembly. J. Cell Biol. 158:475-485. http://dx.doi.org/10.1083/jcb.200202019
49. Shimi, T., K. Pfleghaar, S. Kojima, C.G. Pack, I. Solovei, A.E. Goldman, S.A. Adam, D.K. Shumaker, M. Kinjo, T. Cremer, and R.D. Goldman. 2008. The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev. 22:3409-3421. http://dx.doi.org/10.1101/gad.1735208
50. Shumaker, D.K., T. Dechat, A. Kohlmaier, S.A. Adam, M.R. Bozovsky, M.R. Erdos, M. Eriksson, A.E. Goldman, S. Khuon, F.S. Collins, et al. 2006. Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc. Natl. Acad. Sci. USA. 103:8703-8708. http://dx.doi.org/10.1073/pnas.0602569103
51. Simon, D.N., and K.L. Wilson. 2011. The nucleoskeleton as a genome-associated dynamic 'network of networks'. Nat. Rev. Mol. Cell Biol. 12:695-708. http://dx.doi.org/10.1038/nrm3207
52. Streaker, E.D., and D. Beckett. 2006. Nonenzymatic biotinylation of a biotin carboxyl carrier protein: unusual reactivity of the physiological target lysine. Protein Sci. 15:1928-1935. http://dx.doi.org/10.1110/ps.062187306
53. Sukegawa, J., and G. Blobel. 1993. A nuclear pore complex protein that contains zinc finger motifs, binds DNA, and faces the nucleoplasm. Cell. 72:29-38. http://dx.doi.org/10.1016/0092-8674(93)90047-T
54. Sullivan, T., D. Escalante-Alcalde, H. Bhatt, M. Anver, N. Bhat, K. Nagashima, C.L. Stewart, and B. Burke. 1999. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 147:913-920. http://dx.doi.org/10.1083/jcb.147.5.913
55. Torrisi, M.R., and S. Bonatti. 1985. Immunocytochemical study of the partition and distribution of Sindbis virus glycoproteins in freeze-fractured membranes of infected baby hamster kidney cells. J. Cell Biol. 101:1300-1306. http://dx.doi.org/10.1083/jcb.101.4.1300
56. Torrisi, M.R., L.V. Lotti, A. Pavan, G. Migliaccio, and S. Bonatti. 1987. Free diffusion to and from the inner nuclear membrane of newly synthesized plasma membrane glycoproteins. J. Cell Biol. 104:733-737. http://dx.doi.org/10.1083/jcb.104.3.733
57. van Steensel, B., and S. Henikoff. 2000. Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase. Nat. Biotechnol. 18:424-428. http://dx.doi.org/10.1038/74487
58. Walther, T.C., M. Fornerod, H. Pickersgill, M. Goldberg, T.D. Allen, and I.W. Mattaj. 2001. The nucleoporin Nup153 is required for nuclear pore basket formation, nuclear pore complex anchoring and import of a subset of nuclear proteins. EMBO J. 20:5703-5714. http://dx.doi.org/10.1093/emboj/20.20.5703
59. Worman, H.J. 2012. Nuclear lamins and laminopathies. J. Pathol. 226:316-325. http://dx.doi.org/10.1002/path.2999
60. Worman, H.J., L.G. Fong, A. Muchir, and S.G. Young. 2009. Laminopathies and the long strange trip from basic cell biology to therapy. J. Clin. Invest. 119:1825-1836. http://dx.doi.org/10.1172/JCI37679
61. Zhang, Q., C. Bethmann, N.F. Worth, J.D. Davies, C. Wasner, A. Feuer, C.D. Ragnauth, Q. Yi, J.A. Mellad, D.T. Warren, 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. http://dx.doi.org/10.1093/hmg/ddm238