Emerin caps the pointed end of actin filaments: Evidence for an actin cortical network at the nuclear inner membrane

PLoS Biology

Volumn 2, Issue 9, 2004, Pages

  Holaska, James M ^a   Kowalski, Amy K ^a   Wilson, Katherine L ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

EMERIN; F ACTIN; GELSOLIN; ACTIN; MEMBRANE PROTEIN; NUCLEAR PROTEIN; THYMOPOIETIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; BINDING AFFINITY; BINDING SITE; CAPPING PHENOMENON; CELL NUCLEUS MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; AFFINITY CHROMATOGRAPHY; CELL MEMBRANE; CELL NUCLEUS; CHEMISTRY; GENETIC TRANSCRIPTION; HELA CELL; METABOLISM; MICROFILAMENT; MUSCULAR DYSTROPHY; PATHOLOGY;

ACTINS; BINDING SITES; CELL MEMBRANE; CELL NUCLEUS; CHROMATOGRAPHY, AFFINITY; GELSOLIN; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROFILAMENTS; MUSCULAR DYSTROPHIES; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PROTEIN BINDING; THYMOPOIETINS; TRANSCRIPTION, GENETIC;

EID: 19344378383     PISSN: 15449173     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pbio.0020231     Document Type: Article

References (67)

1. Amann KJ, Pollard TD (2001) The Arp2/3 complex nucleates actin filament branches from the sides of preexisting filaments. Nat Cell Biol 3: 306-310.
2. Bengtsson L, Wilson KL (2004) Multiple and surprising new functions for emerin, a nuclear membrane protein. Curr Opin Cell Biol 16: 73-79.
3. Bennett V, Baines AJ (2001) Spectrin and ankyrin-based pathways: Metazoan inventions for integrating cells into tissues. Physiol Rev 81: 1353-1392.
4. Bettinger BT, Gilbert DM, Amberg DC (2004) Opinion: Actin up in the nucleus. Nat Cell Biol 5: 410-415.
5. Bione S, Small K, Aksmanovic VM, D'Urso M, Ciccodicola A, et al. (1995) Identification of new mutations in the Emery-Dreifuss muscular dystrophy gene and evidence for genetic heterogeneity of the disease. Hum Mol Genet 4: 1859-1863.
6. Blanchoin L, Pollard TD, Mullins RD (2000) Interactions of ADF/cofilin, Arp2/3 complex, capping protein and profilin in remodeling of branched actin filament networks. Curr Biol 10: 1273-1282.
7. Bonne GYR, Beroud C, Boriani G, Brown S, de Visser M, et al. (2003) 108th ENMC International Workshop, 3rd Workshop of the MYOCLUSTER project: EUROMEN, 7th International Emery-Dreifuss Muscular Dystrophy (EDMD) Workshop, 13-15 September 2002, Naarden, The Netherlands. Neuromuscul Disord 13: 508-515.
8. Burke B, Stewart CL (2002) Life at the edge: The nuclear envelope and human disease. Nat Rev Mol Cell Biol 3: 575-585.
9. Burtnick LD, Robinson RC, Choe S (2001) Structure and function of gelsolin. Results Probl Cell Differ 32: 201-211.
10. Clark TG, Rosenbaum JL (1979) An actin filament matrix in hand-isolated nuclei of X. laevis oocytes. Cell 18: 1101-1108.
11. Clements L, Manilal S, Love DR, Morris GE (2000) Direct interaction between emerin and lamin A. Biochem Biophys Res Commun 267: 709-714.
12. Cohen M, Lee KK, Wilson KL, Gruenbaum Y (2001) Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina. Trends Biochem Sci 26: 41-47.
13. Cooper JA, Schafer DA (2000) Control of actin assembly and disassembly at filament ends. Curr Opin Cell Biol 12: 97-103.
14. Dahl KN, Kahn SM, Wilson KL, Discher DE (2004) The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J Cell Sci In press.
15. Dechat T, Vlcek S, Foisner R (2000) Review: Lamina-associated polypeptide 2 isoforms and related proteins in cell cycle-dependent nuclear structure dynamics. J Struct Biol 129: 335-345.
16. Delaunay J (2002) Molecular basis of red cell membrane disorders. Acta Haematol 108: 210-218.
17. Djinovic-Carugo K, Gautel M, Ylanne J, Young P (2002) The spectrin repeat: A structural platform for cytoskeletal protein assemblies. FEBS Lett 513: 119-123.
18. dos Remedios CG, Chhabra D, Kekic M, Dedova IV, Tsubakihara M, et al. (2003) Actin binding proteins: Regulation of cytoskeletal microfilaments. Physiol Rev 83: 433-473.
19. Dreger CK, Konig AR, Spring H, Lichter P, Herrmann H (2002) Investigation of nuclear architecture with a domain-presenting expression system. J Struct Biol 140: 100-115.
20. Emery AE (2000) Emery-Dreifuss muscular dystrophy - A 40 year retrospective. Neuromuscul Disord 10: 228-232.
21. Fairley E, Kendrick-Jones J, 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.
22. Fidzianska A, Hausmanowa-Petrusewicz I (2003) Architectural abnormalities in muscle nuclei: Ultrastructural differences between Xlinked and autosomal dominant forms of EDMD. J Neurol Sci 210: 47-51.
23. Forero C, Wasserman M (2000) Isolation and identification of actinbinding proteins in Plasmodium falciparum by affinity chromatography. Mem Inst Oswaldo Cruz 95: 329-337.
24. Fowler VM (1997) Capping actin filament growth: Tropomodulin in muscle and nonmuscle cells. Soc Gen Physiol Ser 52: 79-89.
25. Fowler VM, Greenfield NJ, Moyer J (2003) Tropomodulin contains two actin filament pointed end-capping domains. J Biol Chem 278: 40000-40009.
26. Gonsior SM, Platz S, Buchmeier S, Scheer U, Jockusch BM, et al. (1999) Conformational difference between nuclear and cytoplasmic actin as detected by a monoclonal antibody. J Cell Sci 112: 797-809.
27. Gruenbaum Y, Lee KK, Liu J, Cohen M, Wilson KL (2002) The expression, lamin-dependent localization and RNAi depletion phenotype for emerin in C. elegans. J Cell Sci 115: 923-929.
28. Haraguchi T, Koujin T, Segura-Totten M, Lee KK, Matsuoka Y, et al. (2001) BAF is required for emerin assembly into the reforming nuclear envelope. J Cell Sci 114: 4575-4585.
29. Haraguchi T, Holaska JM, Yamane M, Wilson KL, 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.
30. Holaska JM, Wilson KL, Mansharamani M (2002) The nuclear envelope, lamins and nuclear assembly. Curr Opin Cell Biol 14: 357-364.
31. Holaska J, Lee K, Kowalski A, Wilson K (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.
32. Johnson BR, Nitta R, Frock RL, Mounkes L, Barbie DA, et al. (2004) Atype nuclear lamins regulate retinoblastoma protein function by promoting correct subnuclear localization and providing protection from proteasomal degradation. Proc Natl Acad Sci U S A 101: 9677-9682.
33. Krauss SW, Heald R, Lee G, Nunomura W, Gimm JA, et al. (2002) Two distinct domains of protein 4.1 critical for assembly of functional nuclei in vitro. J Biol Chem 277: 44339-44346.
34. Lattanzi G, Cenni V, Marmiroli S, Capanni C, Mattioli E, et al. (2003) Association of emerin with nuclear and cytoplasmic actin is regulated in differentiating myoblasts. Biochem Biophys Res Commun 303: 764-770.
35. Lee KK, Wilson KL (2004) All in the family: Evidence for four new LEMdomain proteins Lem2 (NET-25), Lem3, Lem4 and Lem5 in the human genome. In: Hutchinson C, Bryant J, Evans D, editors. Communication and gene regulation at the nuclear envelope. Oxford (United Kingdom): BIOS Scientific. In press.
36. Lee KK, Gruenbaum Y, Spann P, Liu J, Wilson KL (2000) C. elegans nuclear envelope proteins emerin, MAN1, lamin, and nucleoporins reveal unique timing of nuclear envelope breakdown during mitosis. Mol Biol Cell 11: 3089-3099.
37. Lee KK, Haraguchi T, Lee RS, Koujin T, Hiraoka Y, et al. (2001) Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J Cell Sci 114: 4567-4573.
38. Lin F, Blake DL, Callebaut I, Skerjanc IS, Holmer L, et al. (2000) MAN1, an inner nuclear membrane protein that shares the LEM domain with lamina-associated polypeptide 2 and emerin. J Biol Chem 275: 4840-4847.
39. Manilal S, Nguyen TM, Sewry CA, Morris GE (1996) The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein. Hum Mol Genet 5: 801-808.
40. Markiewicz EDT, Foisner R, Quinlan RA, Hutchison CJ (2002) Lamin A/C binding protein LAP2alpha is required for nuclear anchorage of retinoblastoma protein. Mol Biol Cell 13: 4401-4413.
41. McMahon LW, Walsh CE, Lambert MW (1999) Human alpha spectrin II and the Fanconi anemia proteins FANCA and FANCC interact to form a nuclear complex. J Biol Chem 274: 32904-32908.
42. Mislow JMK, Holaska JM, Kim MS, Lee KK, Segura-Totten M, et al. (2002a) Nesprin-1a self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett 525: 135-140.
43. Mislow JMK, Kim MS, Davis DB, McNally EM (2002b) Myne-1, a spectrin repeat transmembrane protein of the myocyte inner nuclear membrane, interacts with lamin A/CJ. Cell Sci 115: 61-70.
44. Mullins RD, Heuser JA, Pollard TD (1998) The interaction of Arp2/3 complex with actin: Nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci U S A 95: 6181-6186.
45. Mullins RD, Pollard TD (1999) Structure and function of the Arp2/3 complex. Curr Opin Struct Biol 9: 244-249.
46. Nagano A, Koga R, Ogawa M, Kurano Y, Kawada J, et al. (1996) Emerin deficiency at the nuclear membrane in patients with Emery-Dreifuss muscular dystrophy. Nat Genet 12: 254-259.
47. Nili E, Cojocaru GS, Kalma Y, Ginsberg D, Copeland NG, 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.
48. Nowak G, Pestic-Dragovich L, Hozak P, Philimonenko A, Simerly C, et al. (1997) Evidence for the presence of myosin I in the nucleus. J Biol Chem 272: 17176-17181.
49. Offterdinger M, Schofer C, Weispoltshammer K, Grunt TW (2002) c-erb-3: A nuclear protein in mammary epithelial cells. J Cell Biol 157: 929-939.
50. Olave IA, Reck-Peterson SL, Crabtree GR (2002) Nuclear actin and actinrelated proteins in chromatin remodeling. Annu Rev Biochem 71: 755-781.
51. Östlund C, Worman H (2003) Nuclear envelope proteins and neuromuscular diseases. Muscle Nerve 27: 393-406.
52. Pederson T, Aebi U (2002) Actin in the nucleus: What form and what for?. J Struct Biol 140: 3-9.
53. Percipalle P, Fomproix N, Kylberg K, Miralles F, Bjorkroth B, et al. (2003) An actin-ribonucleoprotein interaction is involved in transcription by RNA polymerase II. Proc Natl Acad Sci U S A 100: 6475-6480.
54. Pestic-Dragovich L, Stojiljkovic L, Philimonenko AA, Nowak G, Ke Y, et al. (2000) A myosin I isoform in the nucleus. Science 290: 337-341.
55. Rando OJ, Zhao K, Janmey P, Crabtree GR (2002) Phosphatidylinositoldependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc Natl Acad Sci U S A 99: 2824-2829.
56. Sakaki M, Koike H, Takahashi N, Sasagawa N, Tomioka S, et al. (2001) Interaction between emerin and nuclear lamins. J Biochem (Tokyo) 129: 321-327.
57. Sasseville AM, Langelier Y (1998) In vitro interaction of the carboxyterminal domain of lamin A with actin. FEBS Lett 425: 485-489.
58. Scheer U, Hinssen H, Franke WW, Jockusch BM (1984) Microinjection of actin-binding proteins and actin antibodies demonstrates involvement of nuclear actin in transcription of lampbrush chromosomes. Cell 39: 111-122.
59. Segura-Totten M, Wilson KL (2004) BAF: Roles in chromatin, nuclear structure and retrovirus integration. Trends Cell Biol 14: 261-266.
60. Segura-Totten M, Kowalski AM, Craigie R, Wilson KL (2002) Barrier-toautointegration factor: Major roles in chromatin decondensation and nuclear assembly. J Cell Biol 158: 475-485.
61. Wang X, Xu S, Rivolta C, Li LY, Peng G, et al. (2002) Barrier to autointegration factor interacts with the cone-rod homeobox and represses its transactivation function. J Biol Chem 277: 43288-43300.
62. Wilkinson FL, Holaska JM, Sharma A, Malinal SB, Holt I, et al. (2003) Emerin interacts in vitro with the splicing-associated factor, YT521-B. Eur J Biochem 270: 2459-2466.
63. Wilson KL (2000) The nuclear envelope, muscular dystrophy and gene expression. Trends Cell Biol 10: 125-129.
64. Zastrow MS, Vlcek S, Wilson KL (2004) Proteins that bind A-type lamins: Integrating isolated clues. J Cell Sci 117: 979-989.
65. Zhang Q, Skepper JN, Yang F, Davies JD, Hegyi L, et al. (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.
66. Zhen YY, Libotte T, Munck M, Noegel AA, Korenbaum E (2002) NUANCE, a giant protein connecting the nucleus and actin cytoskeleton. J Cell Sci 115: 3207-3222.
67. Zheng R, Ghirlando R, Lee MS, Mizuuchi K, Krause M, et al. (2000) Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higherorder nucleoprotein complex. Proc Natl Acad Sci U S A 97: 8997-9002.