Lamin A/C speckles mediate spatial organization of splicing factor compartments and RNA polymerase II transcription

Journal of Cell Biology

Volumn 159, Issue 5, 2002, Pages 783-793

  Kumaran, R Ileng ^a,b   Muralikrishna, Bhattiprolu ^a   Parnaik, Veena K ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Lamin A; Nuclear lamina; Nuclear organization; RNA polymerase II transcription; Splicing factor compartments

Indexed keywords

LAMIN A; LAMIN C; RNA POLYMERASE II;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ARTICLE; AXONAL INJURY; CELL COMPARTMENTALIZATION; CELL CYCLE S PHASE; CHROMATIN STRUCTURE; CYTOARCHITECTURE; DNA REPLICATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; RNA SPLICING; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION;

AMANITINS; ANTIBODIES, MONOCLONAL; CELL COMPARTMENTATION; CELL NUCLEUS; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; DOWN-REGULATION; HELA CELLS; HUMANS; KINETICS; LAMIN TYPE A; NUCLEAR PROTEINS; NUCLEIC ACID SYNTHESIS INHIBITORS; RECOMBINANT PROTEINS; RNA POLYMERASE II; RNA SPLICING; TRANSCRIPTION, GENETIC; TUMOR CELLS, CULTURED;

EID: 0037049554     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200204149     Document Type: Article

References (69)

1. Beyer, A.L., N. Yvonne, and Y.N. Osheim. 1988. Splice site selection, rate of splicing, and alternative splicing on nascent transcripts. Genes Dev. 2:754-765.
2. Bohmann, K., J.A. Ferreira, and A.I. Lamond. 1995. Mutational analysis of p80 coilin indicates a functional interaction between coiled bodies and the nucleolus. J. Cell Biol. 131:817-831.
3. Bonne, G., M.R. Di Barletta, S. Varnous, H.M. Becane, E.H. Hammonda, 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.
4. Bregman, D.B., L. Du, S. van der Zee, and S.L. Warren. 1995. Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129:287-298.
5. Bridget, J.M., I.R. Kill, M. O'Farrell, and C.J. Hutchison. 1993. Internal lamin structures within G1 nuclei of human dermal fibroblasts. J. Cell Sci. 104: 297-306.
6. 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.
7. Burley, S.K., and R.G. Roeder. 1996. Biochemistry and structural biology of transcription factor IID (TFIID). Annu. Rev. Biochem. 65:769-799.
8. Cao, H., and R.A. Hegele. 2000. Nuclear lamin A/C R482Q mutation in Canadian kindreds with Dunnigan-type familial partial lipodystrophy. Hum. Mol. Genet. 9:109-112.
9. Carmo-Fonseca, M., R. Pepperkok, M.T. Carvalho, and A.I. Lamond. 1992. Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 sn-RNPs in coiled bodies. J. Cell Biol. 117:1-14.
10. Chen, D., C.S. Hinkley, R.W. Henry, and S. Huang. 2002. TBP dynamics in living human cells. Mol. Biol. Cell. 13:276-284.
11. Clements, L., S. Manilal, D.R. Love, and G.E. Morris. 2000. Direct interaction between emerin and lamin A. Biochem. Biophys. Res. Commun. 267:709-714.
12. Cmarko, D., P.J. Verschure, T.E. Marrin, M.E. Dahmus, S. Krause, X.D. Fu, R. van Driel, and S. Fakan. 1999. Ultrastructural analysis of transcription and splicing in the cell nucleus after bromo-UTP microinjection. Mol. Biol. Cell. 10:211-223.
13. Colwill, K., T. Pawson, B. Andrews, J. Prasad, J.L. Manley, J.C. Bell, and P.I. Duncan. 1996. The Clk/Sry protein kinase phosphorylates splicing factors and regulates their intranuclear distribution. EMBO J. 15:265-275.
14. Davis, L.I., and G. Blobel. 1986. Identification and characterization of a nuclear pore complex protein. Cell. 45:699-709.
15. De Conto, F., E. Pilotti, S.V. Razin, F. Ferraglia, G. Gérand, C. Arcangeletti, and K. Scherrer. 2000. In mouse myoblasts nuclear prosomes are associated with the nuclear matrix and accumulate preferentially in the perinucleolar areas. J. Cell Sci. 113:2399-2407.
16. De Sandre-Giovannoli, A., M. Chaouch, S. Kozlov, J. Vallat, M. Tazir, N. Kassouri, P. Szepetowski, T. Hammadouche, A. Vandenberghe, C.L. Stewart, et al. 2002. Homozygous defects in LMNA, encoding lamin A/C nuclear envelope proteins, cause autosomal recessive axonal neuropathy in human (Charcot-Marie-Tooth disorder type 2) and mouse. Am. J. Hum. Genet. 70:726-736.
17. Dechat, T., B. Korbei, O.A. Vaughan, S. Vicek, C.J. Hutchison, and R. Foisnet. 2000. Intranuclear lamina-associated polypeptide 2α binds A-type lamins. J. Cell Sci. 113:3473-3484.
18. Dyer, J.A., I.R. Kill, G. Pugh, R.A. Quinlan, E.B. Lane, and C.J. Hutchison. 1997. Cell cycle changes in A-type lamin associations detected in human dermal fibroblasts using monoclonal antibodies. Chromosome Res. 5:383-394.
19. Ellis, D.J., H. Jenkins, W.G.F. Whitfield, and C.J. Hutchison. 1997. GST-lamin fusion proteins act as dominant negative mutants in Xenopus egg extract and reveal the function of the lamina in DNA replication. J. Cell Sci. 110:2507-2518.
20. Fabrizio, P., B. Laggerbauer, J. Lauber, W.S. Lane, and R. Lührmann. 1997. An evolutionarily conserved U5 snRNP-specific protein is a GTP-binding factor closely related to the ribosomal translocase EF-2. EMBO J. 16:4092-4106.
21. Fakan, S. 1994. Perichromatin fibrils are in situ forms of nascent transcripts. Trends Cell Biol. 4:86-90.
22. Fakan, S., and E. Puvion. 1980. The ultrastructural visualization of nucleolar and extranucleolar RNA synthesis and distribution. Int. Rev. Cytol. 65:255-299.
23. Fackan, D., C. MacRae, T. Sasaki, M.R. Wolff, M. Porcu, M. Frenneaux, J. Atherton, H.J. Vidaillet, Jr., S. Spudich, U. De Girolami, et al. 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.
24. Fu, X.D., and T. Maniatis. 1990. Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature. 343:437-441.
25. Gant, T.M., and K.L. Wilson. 1997. Nuclear assembly. Annu. Rev. Cell Dev. Biol. 13:669-695.
26. Gerace, L., and R. Foisner. 1994. Integral membrane proteins and dynamic organization of the nuclear envelope. Trends Cell Biol. 4:127-131.
27. Goldman, A.E., R.D. Moir, M. Montag-Lowy, M. Stewert, and R.D. Goldman. 1992. Pathway of incorporation of microinjected lamin A into the nuclear envelope. J. Cell Biol. 119:725-735.
28. Hamid, Q.A., S. Fatima, S. Thanumalayan, and V.K. Parnaik. 1996. Activation of the lamin A gene during rat liver development. FEBS Lett. 392:137-142.
29. Hendzel, M.J., F. Boisvert, and D.P. Bazett-Jones. 1999. Direct visualization of a protein nuclear architecture. Mol. Biol. Cell. 10:2051-2062.
30. Hirose, Y., and J.L. Manley. 2000. RNA polymerase II and the integration of nuclear events. Genes Dev. 14:1415-1429.
31. Hozak, P., A.M.-J. Sasseville, Y. Raymond, and P.R. Cook. 1995. Lamin proteins form an internal nucleoskeleton as well as a peripheral lamina in human cells. J. Cell Sci. 108:635-644.
32. Izumi, M., O.A. Vaughan, C.J. Hutchison, and D.M. Gilbert. 2000. Head and/or CaaX domain deletions of lamin proteins disrupt preformed lamin A and C but not lamin B structure in mammalian cells. Mol. Biol. Cell. 11:4323-4337.
33. Jackson, D.A., A.B. Hassan, R.J. Errington, and P.R. Cook. 1993. Visualization of focal sites of transcription within human nuclei. EMBO J. 12:1059-1065.
34. Jagatheesan, G., S. Thanumalayan, B. Muralikrishna, N. Rangaraj, A.A. Karande, and V.K. Parnaik. 1999. Colocalization of intranuclear lamin foci with RNA splicing factors. J. Cell Sci. 112:4651-4661.
35. Kimura, H., Y. Tao, R.G. Roeder, and P.R. Cook. 1999. Quantitation of RNA polymerase II and its transcription factors in a HeLa cell: Little soluble holoenzyme but significant amounts of polymerases attached to the nuclear substructure. Mol. Cell. Biol. 19:5383-5392.
36. Ko, T.K., E. Kelly, and J. Pines. 2001. CrkRS: A novel conserved Cdc2-related protein kinase that colocalizes with SC35 speckles. J. Cell Sci. 114:2591-2603.
37. Kruhlak, M.J., M.A. Lever, W. Fischle, E. Verdin, D.P. Bazett-Jones, and M.J. Hendzel. 2000. Reduced mobility of the alternate splicing factor (ASF) through the nucleoplasm and steady state speckle compartments. J. Cell Biol. 150:41-51.
38. Kues, T., A. Dickmanns, R. Lührmann, R. Peters, and U. Kubitscheck. 2001. High intranuclear mobility and dynamic clustering of the splicing factor U1 snRNP observed by single particle tracking. Proc. Natl. Acad. Sci. USA. 98: 12021-12026.
39. Lamond, A.I., and W.C. Earnshaw. 1998. Structure and function in the nucleus. Science. 280:547-553.
40. Mintz, P.J., S.D. Patterson, A.F. Neuwald, C.S. Spahr, and D.L. Spector. 1999. Purification and biochemical characterization of interchromatin granule clusters. EMBO J. 18:4308-4320.
41. Misteli, T. 2001. The concept of self-organization in cellular architecture. J. Cell Biol. 155:181-185.
42. Misteli, T., J.F. Caceres, and D.L. Spector. 1997. The dynamics of a pre-mRNA splicing factor in living cells. Nature. 387:523-527.
43. Misteli, T., J.F. Caceres, J.Q. Clement, A.R. Krainer, M.F. Wilkinson, and D.L. Spector. 1998. Serine phosphorylation of SR proteins is required for their recruitment to sites of transcription in vivo. J. Cell Biol. 143:297-307.
44. Moir, R.D., M. Montag-Lowy, and R.D. Goldman. 1994. Dynamic properties of nuclear lamins: Lamin B is associated with sites of DNA replication. J. Cell Biol. 125:1201-1212.
45. Moir, R.D., T.P. Spann, H. Herrmann, and R.D. Goldman. 2000a. Disruption of nuclear lamin organization blocks the elongation phase of DNA replication. J. Cell Biol. 149:1179-1192.
46. Moir, R.D., M. Yoon, S. Khuon, and R.D. Goldman. 2000b. Nuclear lamins A and B1: Different pathways of assembly during nuclear envelope formation in living cells. J. Cell Biol. 151:1155-1168.
47. Muralikrishna, B., J. Dhawan, N. Rangaraj, and V.K. Parnaik. 2001. Distinct changes in intranuclear lamin A/C organization during myoblast differentiation. J. Cell Sci. 114:4001-4011.
48. Nakayasu, H., and K. Ueda. 1984. Small nuclear RNA-protein complex anchors on the actin filaments in bovine lymphocyte nuclear matrix. Cell Struct. Funct. 9:317-325.
49. Nickerson, J.A. 2001. Experimental observations of a nuclear matrix. J. Cell Sci. 114:463-474.
50. O'Keefe, R.T., A. Mayeda, C.I. Sadowski, A.R. Krainer, and D.L. Spector. 1994. Disruption of pre-mRNA splicing in vivo results in reorganization of splicing factors. J. Cell Biol. 124:249-260.
51. Östlund, C., G. Bonne, K. Schwartz, and H. Worman. 2001. Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J. Cell Sci. 114:4435-4445.
52. Ozaki, T., M. Saijo, K. Murakanu, H. Enomoto, Y. Taya, and S. Sakiyama. 1994. Complex formation between lamin A and the retinoblastoma gene product: Identification of the domain on lamin A required for its interaction. Oncogene. 9:2649-2653.
53. Pederson, T. 2000. Half a century of the nuclear matrix. Mol. Biol. Cell. 11:799-805.
54. Phair, R.D., and T. Misteli. 2000. High mobility of proteins in the mammalian cell nucleus. Nature. 404:604-609.
55. Pugh, G.E., P.J. Coates, F.B. Lane, Y. Raymond, and R.A. Quinlan. 1997. Distinct nuclear assembly pathways for lamins A and C lead to their increase during quiescence in Swiss 3T3 cells. J. Cell Sci. 110:2483-2493.
56. Raharjo, W.H., P. Enarson, T. Sullivan, C.L. Stewart, and B. Burke. 2001. Nuclear envelope defects associated with LMNA mutations cause dilated cardiomyopathy and Emery-Dreifuss muscular dystrophy. J. Cell Sci. 114:4447-4457.
57. Sacco-Bubulya, P., and D.L. Spector. 2002. Disassembly of interchromatin granule clusters alters the coordination of transcription and pre-mRNA splicing. J. Cell Biol. 156:425-436.
58. Shackleton, S., D.J. Lloyd, S.N.J. Jackson, R. Evans, M.F. Niermeijer, B.M. Singh, H. Schmidt, G. Brabant, S. Kumar, P.N. Durrington, et al. 2000. LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nat. Genet. 24: 153-156.
59. Smith, K.P., P.T. Moen, K.L. Wydner, J.R. Coleman, and J.B. Lawrence. 1999. Processing of endogenous pre-mRNAs in association with SC-35 domains is gene specific. J. Cell Biol. 144:617-629.
60. Spann, T.P., R.D. Moir, A.E. Goldman, R. Stick, and R.D. Goldman. 1997. Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J. Cell Biol. 136:1201-1212.
61. Spann, T.P., A.E. Goldman, C. Wang, S. Huang, and R.D. Goldman. 2002. Alteration of nuclear lamin organization inhibits RNA polymerase II-dependent transcription. J. Cell Biol. 156:603-608.
62. Spector, D.L. 1993. Macromolecular domains within the cell nucleus. Annu. Rev. Cell Biol. 9:265-315.
63. Stein, G.S., A.J. van Wijnen, J.L. Stein, J.B. Lian, M. Montecino, J.Y. Choi, K. Zaidi, and A. Javed. 2000. Intranuclear trafficking of transcription factors: Implications for biological control. J. Cell Sci. 113:2527-2533.
64. Stuurman, N., S. Heins, and U. Aebi. 1998. Nuclear lamins: Their structure, assembly and interactions. J. Struct. Biol. 122:42-66.
65. Taniura, H., C. Glass, and L. Gerace. 1995. A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J. Cell Biol. 131: 33-44.
66. Vigouroux, C., M. Auclair, E. Dubosclard, M. Pouchelet, S. Lepanse, J. Capeau, J.C. Courvalin, and B. Buendia. 2001. Nuclear disorganization in fibroblasts from lipodystrophic patients with heterozygous R482Q/W mutations in the lamin A/C gene. J. Cell Sci. 114:4459-4468.
67. Wansink, D.G., W. Schul, I. van der Kraan, B. van Steensel, R. van Driel, and L. de Jong. 1993. Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J. Cell Biol. 122:283-293.
68. Wei, X., S. Somanathan, J. Samarabandu, and R. Berezney. 1999. Three-dimensional visualization of transcription sites and their association with splicing factor-rich nuclear specldes. J. Cell Biol. 146:543-558.
69. Wilson, K.L. 2000. The nuclear envelope, muscular dystrophy and gene expression. Trends Cell Biol. 10:125-129.