Review: Nuclear lamins - Structural proteins with fundamental functions

Journal of Structural Biology

Volumn 129, Issue 2-3, 2000, Pages 313-323

  Gruenbaum, Yosef ^a   Wilson, Katherine L ^b   Harel, Amnon ^a   Goldberg, Michal ^a   Cohen, Merav ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

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

Author keywords

Apoptosis; Chromatin; DNA replication; Emerin; LAP1; LAP2; LBR; Man1; Muscular dystrophy; Nuclear envelope; Nuclear lamina; Otefin; UNC 84; YA

Indexed keywords

LAMIN; NUCLEAR PROTEIN;

APOPTOSIS; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CHROMATIN STRUCTURE; DNA REPLICATION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

EID: 0033925932     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.2000.4216     Document Type: Article

References (135)

1. Alsheimer M., von Glasenapp E., Hock R., Benavente R. Architecture of the nuclear periphery of rat pachytene spermatocytes: Distribution of nuclear envelope proteins in relation to synaptonemal complex attachment sites. Mol. Biol. Cell. 10:1999;1235-1245.
2. Anjum R., Khar A. Caspase-mediated apoptosis in AK-5 tumor cells: A cell-free study using peptide inhibitors and antisense strategy. Exp. Cell Res. 236:1997;371-377.
3. Antoku K., Liu Z., Johnson D. E. Inhibition of caspase proteases by CrmA enhances the resistance of human leukemic cells to multiple chemotherapeutic agents. Leukemia. 11:1997;1665-1672.
4. Berger R., Theodor L., Shoham J., Gokkel E., Brok-Simoni F., Avraham K. B., Copeland N. G., Jenkins N. A., Rechavi G., Simon A. J. The characterization and localization of the mouse thymopoietin/lamina-associated polypeptide 2 gene and its alternatively spliced products. Genome Res. 6:1996;361-370.
5. Bione S., Maestrini E., Rivella S., Mancini M., Regis S., Romeo G., Toniolo D. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat. Genet. 8:1994;323-327.
6. Bonne G., Di Barletta M. R., Varnous S., Becane H. M., Hammouda E. H., Merlini L., Muntoni F., Greenberg C. R., Gary F., Urtizberea J. A., Duboc D., Fardeau M., Toniolo D., Schwartz K. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet. 21:1999;285-288.
7. Bossie C. A., Sanders M. M. A cDNA from Drosophila melanogaster encodes a lamin C-like intermediate filament protein. J. Cell Sci. 104:1993;1263-1272.
8. Bridger J. M., Kill I. R., O'Farrell M., Hutchison C. J. Internal lamin structures within G1 nuclei of human dermal fibroblasts. J. Cell Sci. 104:1993;297-306.
9. Brito J., Biamonti G., Caporali R., Montecucco C. Autoantibodies to human nuclear lamin B2 protein. Epitope specificity in different autoimmune diseases. J. Immunol. 153:1994;2268-2277.
10. Broers J. L., Machiels B. M., Kuijpers H. J., Smedts F. R., Raymond Y., Ramaekers F. C. A- and B-type lamins are differentially expressed in normal human tissues. Histochem. Cell Biol. 107:1997;505-517.
11. Broers J. L., Machiels B. M., van Eys G. J., Kuijpers H. J., Manders E. M., van Driel R., Ramaekers F. C. Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J. Cell Sci. 112:1999;3463-3475.
12. Buendia B., Santa-Maria A., Courvalin J. C. Caspase-dependent proteolysis of integral and peripheral proteins of nuclear membranes and nuclear pore complex proteins during apoptosis. J. Cell Sci. 112:1999;1743-1753.
13. Cao H., Hegele R. Nuclear lamin A/C R482Q mutation in Canadian kindreds with Dunningan-type familial partial lipodystrophy. Hum. Mol. Genet. 9:2000;109-112.
14. Courvalin J. C., Chaudhary N., Danon F., Brouet J. C., Lassoued K. Characterization of human autoantibodies specific for lamin A. Biol. Cell. 69:1990a;93-97.
15. Courvalin J. C., Lassoued K., Bartnik E., Blobel G., Wozniak R. W. The 210-kD nuclear envelope polypeptide recognized by human autoantibodies in biliary cirrhosis is the major glycoprotein of the nuclear pore. J. Clin. Invest. 86:1990b;279-285.
16. Courvalin J. C., Lassoued K., Worman H. J., Blobel G. Identification and characterization of autoantibodies against the nuclear envelope lamin B receptor from patients with primary biliary cirrhosis. J. Exp. Med. 172:1990c;961-967.
17. Courvalin J. C., Worman H. J. Nuclear envelope protein autoantibodies in primary biliary cirrhosis. Semin. Liver Dis. 17:1997;79-90.
18. Dreifuss F. H., Hogan G. R. Survival in X-chromosomal muscular dystrophy. Neurology. 11:1961;734-737.
19. Duband-Goulet I., Courvalin J. C., Buendia B. LBR, a chromatin and lamin binding protein from the inner nuclear membrane, is proteolyzed at late stages of apoptosis. J. Cell Sci. 111:1998;1441-1451.
20. Ellis D. J., Jenkins H., Whitfield W. G., Hutchison C. J. 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. 110:1997;2507-2518.
21. Ellis J. A., Craxton M., Yates J. R., Kendrick Jones J. Aberrant intracellular targeting and cell cycle-dependent phosphorylation of emerin contribute to the Emery-Dreifuss muscular dystrophy phenotype. J. Cell Sci. 111:1998;781-792.
22. Emery A. E. H., Dreifuss F. E. Unusual type of benign X-linked muscular dystrophy. J. Neurol. Neurosurg. Psychiatry. 29:1955;338-342.
23. Foisner R., Gerace L. Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell. 73:1993;1267-1279.
24. Fraser A. G., McCarthy N. J., Evan G. I. drICE is an essential caspase Lin required for apoptotic activity in Drosophila cells. EMBO J. 16:1997;6192-6199.
25. Furukawa K. LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J. Cell Sci. 112:1999;2485-2492.
26. Furukawa K., Hotta Y. cDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO J. 12:1993;97-106.
27. Furukawa K., Inagaki H., Hotta Y. Identification and cloning of an mRNA coding for a germ cell-specific A-type lamin in mice. Exp. Cell Res. 212:1994;426-430.
28. Gant T. M., Harris C. A., Wilson K. L. 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. 144:1999;1083-1096.
29. Gant T. M., Wilson K. L. Nuclear assembly. Annu. Rev. Cell Dev. Biol. 13:1997;669-695.
30. Gerace L., Bloom A., Blobel G. Immunocytochemical localization of the major polypeptides of the nuclear pore complex-lamina fraction: Interphase and mitotic distribution. J. Cell Biol. 79:1978;546-566.
31. Gerace L., Burke B. Functional organization of the nuclear envelope. Annu. Rev. Cell Biol. 4:1988;335-374.
32. Goldberg M., Harel A., Brandeis M., Rechsteiner T., Richmond T. J., Weiss A. M., Gruenbaum Y. The tail domain of lamin Dm0 binds histones H2A and H2B. Proc. Natl. Acad. Sci. USA. 96:1999;2852-2857.
33. Goldberg, M., Harel, A., and Gruenbaum, Y. (1999) The nuclear lamina: Molecular organization and interaction with chromatin, Crit. Rev. Eukaryotic Gene Expr.9, 285-293.
34. Goldberg M., Jenkins H., Allen T., Whitfield W. G., Hutchison C. J. Xenopus lamin B3 has a direct role in the assembly of a replication competent nucleus: Evidence from cell-free egg extracts. J. Cell. Sci. 108:1995;3451-3461.
35. Goldberg M., Lu H., Stuurman N., Ashery Padan R., Weiss A. M., Yu J., Bhattacharyya D., Fisher P. A., Gruenbaum Y., Wolfner M. F. Interactions among Drosophila nuclear envelope proteins lamin, otefin, and YA. Mol. Cell. Biol. 18:1998;4315-4323.
36. Goldberg, M, Nili, E, Cojocaru, G, Tzur, Y. B, Berger, R, Brandies, M, Rechavi, G, Gruenbaum, Y, and, Simon, A. J. (2000), Functional organization of the nuclear lamina, in, Boulikas, T. (Ed.), Textbook of Gene Therapy and Molecular Biology: From Basic Mechanism to Clinical Applications, Vol, 4, in press.
37. Goldman A. E., Moir R. D., Montag L. M., Stewart M., Goldman R. D. Pathway of incorporation of microinjected lamin A into the nuclear envelope. J. Cell Biol. 119:1992;725-735.
38. Gotzmann J., Foisner R. Lamins and lamin-binding proteins in functional chromatin organization. Crit. Rev. Eukaryotic Gene Expr. 9:1999;257-265.
39. Gruenbaum Y., Landesman Y., Drees B., Bare J. W., Saumweber H., Paddy M. R., Sedat J. W., Smith D. E., Benton B. M., Fisher P. A. Drosophila nuclear lamin precursor Dm0 is translated from either of two developmentally regulated mRNA species apparently encoded by a single gene. J. Cell Biol. 106:1988;585-596.
40. Guilly M. N., Danon F., Brouet J. C., Bornens M., Courvalin J. C. Autoantibodies to nuclear lamin B in a patient with thrombopenia. Eur. J. Cell Biol. 43:1987;266-272.
41. Harel A., Goldberg M., Ulitzur N., Gruenbaum Y. Structural organization and biological roles of the nuclear lamina. Boulikas T. Textbook of Gene Therapy and Molecular Biology: From Basic Mechanism to Clinical Applications. 1998;529-542.
42. Harris C. A., Andryuk P. J., Cline S. W., Mathew S., Siekierka J. J., Goldstein G. Structure and mapping of the human thymopoietin (TMPO) gene and relationship of human TMPO beta to rat lamin-associated polypeptide 2. Genomics. 28:1995;198-205.
43. Hengartner M. O., Horvitz H. R. Programmed cell death in Caenorhabditis elegans. Curr. Opin. Genet. Dev. 4:1994;581-586.
44. Hetts S. W. To die or not to die: An overview of apoptosis and its role in disease. J. Am. Med. Assoc. 279:1998;300-307.
45. Hill C., Roberts Thomson P., Pollard A., Gillis D., Kirkham B. Clinical associations of anti-lamin autoantibodies. Aust. N. Z. J. Med. 26:1996;162-166.
46. Holmer L., Pezhman A., Worman H. J. The human lamin B receptor/sterol reductase multigene family. Genomics. 54:1998;469-476.
47. Hozak P., Sasseville A. M., Raymond Y., Cook P. R. Lamin proteins form an internal nucleoskeleton as well as a peripheral lamina in human cells. J. Cell Sci. 108:1995;635-644.
48. Hutchison C. J., Bridger J. M., Cox L. S., Kill I. R. Weaving a pattern from disparate threads: Lamin function in nuclear assembly and DNA replication. J. Cell Sci. 107:1994;3259-3269.
49. Hutchison C. J., Brill D., Cox R., Gilbert J., Kill I., Ford C. C. DNA replication and cell cycle control in Xenopus egg extracts. J. Cell Sci. Suppl. 12:1989;197-212.
50. Jenkins H., Holman T., Lyon C., Lane B., Stick R., Hutchison C. Nuclei that lack a lamina accumulate karyophilic proteins and assemble a nuclear matrix. J. Cell Sci. 106:1993;275-285.
51. Kaufmann S. H. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: A cautionary note. Cancer Res. 49:1989;5870-5878.
52. Kawahara A., Enari M., Talanian R. V., Wong W. W., Nagata S. Fas-induced DNA fragmentation and proteolysis of nuclear proteins. Genes Cells. 3:1998;297-306.
53. Kidd V. J. Proteolytic activities that mediate apoptosis. Annu. Rev. Physiol. 60:1998;533-573.
54. Kluck R. M., Martin S. J., Hoffman B. M., Zhou J. S., Green D. R., Newmeyer D. D. Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO J. 16:1997;4639-4649.
55. Konstantinov K., Foisner R., Byrd D., Liu F. T., Tsai W. M., Wiik A., Gerace L. Integral membrane proteins associated with the nuclear lamina are novel autoimmune antigens of the nuclear envelope. Clin. Immunol. Immunopathol. 74:1995;89-99.
56. Konstantinov K., von Mikecz A., Buchwald D., Jones J., Gerace L., Tan E. M. Autoantibodies to nuclear envelope antigens in chronic fatigue syndrome. J. Clin. Invest. 98:1996;1888-1896.
57. Lassoued K., Brenard R., Degos F., Courvalin J. C., Andre C., Danon F., Brouet J. C., Zine E. A. Y., Degott C., Zafrani S. Antinuclear antibodies directed to a 200-kilodalton polypeptide of the nuclear envelope in primary biliary cirrhosis. A clinical and immunological study of a series of 150 patients with primary biliary cirrhosis. Gastroenterology. 99:1990;181-186.
58. Lassoued K., Danon F., Andre C., Courvalin J. C., Dhumeaux D. Liver diseases associated with autoantibodies directed to nuclear envelope components. Hepatology. 9:1989;911-912.
59. Lassoued K., Danon F., Brouet J. C. Human autoantibodies to lamin B receptor are also anti-idiotypic to certain anti-lamin B antibodies. Eur. J. Immunol. 21:1991;1959-1962.
60. Lassoued K., Guilly M. N., Andre C., Paintrand M., Dhumeaux D., Danon F., Brouet J. C., Courvalin J. C. Autoantibodies to 200 kD polypeptide(s) of the nuclear envelope: A new serologic marker of primary biliary cirrhosis. Clin. Exp. Immunol. 74:1988a;283-288.
61. Lassoued K., Guilly M. N., Danon F., Andre C., Dhumeaux D., Clauvel J. P., Brouet J. C., Seligmann M., Courvalin J. C. Antinuclear autoantibodies specific for lamins. Characterization and clinical significance. Ann. Intern. Med. 108:1988b;829-833.
62. Lazebnik Y. A., Cole S., Cooke C. A., Nelson W. G., Earnshaw W. C. Nuclear events of apoptosis in vitro in cell-free mitotic extracts: A model system for analysis of the active phase of apoptosis. J. Cell Biol. 123:1993;7-22.
63. Lee M. S., Craigie R. A previously unidentified host protein protects retroviral DNA from autointegration. Proc. Natl. Acad. Sci. USA. 95:1998;1528-1533.
64. Lenz-Bohme B., Wismar J., Fuchs S., Reifegerste R., Buchner E., Betz H., Schmitt B. Insertional mutation of the Drosophila nuclear lamin dm(0) gene results in defective nuclear envelopes, clustering of nuclear pore complexes, and accumulation of annulate lamellae. J. Cell Biol. 137:1997;1001-1016.
65. Lin, F., Blake, D. L., Callebaut, I., Skerjanc, I. S., Holmer, L., McBurney, M. W., Paulin-Levasseur, M., and Worman, H. J. (2000) MAN1: An inner nuclear membrane protein that shares the LEM domain with lamina associated polypeptide 2 and emerin, J. Biol. Chem.275, 4080-4087.
66. Lin H., Song K., Hutcheson G. A., Goutte C. E., Wolfner M. F. A maternally encoded nuclear envelope protein required for embryonic mitosis in Drosophila. Cold Spring Harbor Symp. Quant. Biol. 56:1991;719-727.
67. Lincz L. F. Deciphering the apoptotic pathway: All roads lead to death. Immunol. Cell Biol. 76:1998;1-19.
68. Liu J., Song K., Wolfner M. F. Mutational analyses of fs(1)Ya, an essential, developmentally regulated, nuclear envelope protein in Drosophila. Genetics. 141:1995;1473-1481.
69. Lohka M. J., Maller J. L. Induction of nuclear envelope breakdown, chromosome condensation, and spindle formation in cell-free extracts. J. Cell Biol. 101:1985;518-523.
70. Lopez J. M., Wolfner M. F. The developmentally regulated Drosophila embryonic nuclear lamina protein young arrest (fs(1)ya) is capable of associating with chromatin. J. Cell Sci. 5:1997;643-651.
71. Lourim D., Kempf A., Krohne G. Characterization and quantitation of three B-type lamins in Xenopus oocytes and eggs: Increase of lamin LI protein synthesis during meiotic maturation. J. Cell Sci. 109:1996;1775-1785.
72. Malka D., Pham B. N., Courvalin J. C., Corbic M., Pessayre D., Erlinger S. Acute hepatitis caused by alverine associated with anti-lamin A and C autoantibodies. J. Hepatol. 27:1997;399-403.
73. Malone C. J., Fixsen W. D., Horvitz H. R., Han M. UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development. 126:1999;3171-3181.
74. Mandal M., Maggirwar S. B., Sharma N., Kaufmann S. H., Sun S. C., Kumar R. Bcl-2 prevents CD95 (Fas/APO-1)-induced degradation of lamin B and poly(ADP-ribose) polymerase and restores the NF-κB signaling pathway. J. Biol. Chem. 271:1996;30354-30359.
75. Manilal S., Nguyen T. M., Sewry C. A., Morris G. E. The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein. Hum. Mol. Genet. 5:1996;801-808.
76. Manilal S., Sewry C. A., Pereboev A., Man N., Gobbi P., Hawkes S., Love D. R., Morris G. E. Distribution of emerin and lamins in the heart and implications for Emery-Dreifuss muscular dystrophy. Hum. Mol. Genet. 8:1999;353-359.
77. Martin L., Crimaudo C., Gerace L. cDNA cloning and characterization of lamina-associated polypeptide 1C (LAP1C), an integral protein of the inner nuclear membrane. J. Biol. Chem. 270:1995;8822-8828.
78. McKeon F. Nuclear lamin proteins: Domains required for nuclear targeting, assembly, and cell-cycle-regulated dynamics. Curr. Opin. Cell Biol. 3:1991;82-86.
79. McKeon F. D., Tuffanelli E., Fukuyama, Kirschner M. W. Autoantibodies response directed against conserved determinants of nuclear envelope proteins in a patient with liniar scleroderma. Proc. Natl. Acad. Sci. USA. 80:1983;4374-4378.
80. Metzstein M. M., Stanfield G. M., Horvitz H. R. Genetics of programmed cell death in C. elegans: Past, present and future. Trends Genet. 14:1998;410-416.
81. Moir R. D., Montag L. M., Goldman R. D. Dynamic properties of nuclear lamins: Lamin B is associated with sites of DNA replication. J. Cell Biol. 125:1994;1201-1212.
82. Moir R. D., Spann T. P., Goldman R. D. The dynamic properties and possible functions of nuclear lamins. Int. Rev. Cytol. 162B:1995;141-182.
83. Morris G. E., Manilal S. Heart to heart: From nuclear proteins to Emery-Dreifuss muscular dystrophy. Hum. Mol. Genet. 8:1999;1847-1851.
84. Nagano A., Koga R., Ogawa M., Kurano Y., Kawada J., Okada R., Hayashi Y. K., Tsukahara T., Arahata K. Emerin deficiency at the nuclear membrane in patients with Emery-Dreifuss muscular dystrophy. Nat. Genet. 12:1996;254-259.
85. Neamati N., Fernandez A., Wright S., Kiefer J., McConkey D. J. Degradation of lamin B1 precedes oligonucleosomal DNA fragmentation in apoptotic thymocytes and isolated thymocyte nuclei. J. Immunol. 154:1995;3788-3795.
86. Newport J. Nuclear reconstitution in vitro: Stages of assembly around protein-free DNA. Cell. 48:1987;205-217.
87. Newport J. W., Wilson K. L., Dunphy W. G. A lamin-independent pathway for nuclear envelope assembly. J. Cell Biol. 111:1990;2247-2259.
88. Nickowitz R. E., Worman H. J. Autoantibodies from patients with primary biliary cirrhosis recognize a restricted region within the cytoplasmic tail of nuclear pore membrane glycoprotein Gp210. J. Exp. Med. 178:1993;2237-2242.
89. Nickowitz R. E., Wozniak R. W., Schaffner F., Worman H. J. Autoantibodies against integral membrane proteins of the nuclear envelope in patients with primary biliary cirrhosis. Gastroenterology. 106:1994;193-199.
90. Oberhammer F. A., Hochegger K., Froschl G., Tiefenbacher R., Pavelka M. Chromatin condensation during apoptosis is accompanied by degradation of lamin A + B, without enhanced activation of cdc2 kinase. J. Cell Biol. 126:1994;827-837.
91. Orth K., Chinnaiyan A. M., Garg M., Froelich C. J., Dixit V. M. The CED-3/ICE-like protease Mch2 is activated during apoptosis and cleaves the death substrate lamin A. J. Biol. Chem. 271:1996;16443-16446.
92. Östlund C., Ellenberg J., Hallberg E., Lippincott-Schwartz J., Worman H. J. Intracellular trafficking of emerin, the Emery-Dreifuss muscular dystrophy protein. J. Cell Sci. 112:1999;1709-1719.
93. Padan R., Nainudel E. S., Goitein R., Fainsod A., Gruenbaum Y. Isolation and characterization of the Drosophila nuclear envelope otefin cDNA. J. Biol. Chem. 265:1990;7808-7813.
94. Panté N., Aebi U. Toward the molecular dissection of protein import into nuclei. Curr. Opin. Cell Biol. 8:1997;397-406.
95. Paulin Levasseur M., Blake D. L., Julien M., Rouleau L. The MAN antigens are non-lamin constituents of the nuclear lamina in vertebrate cells. Chromosoma. 104:1996;367-379.
96. Philipp T., Straub P., Durazzo M., Turkey R. H., Manns D. J. Molecular analysis of autoantigens in hepatitis. Hepatology. 22:1995;132-135.
97. Raff J. W. Nuclear migration: The missing (L)UNC. Curr. Biol. 9:1999;R708-R710.
98. Rao L., Perez D., White E. Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135:1996;1441-1455.
99. Reeves W. H., Ali S. A. Preferential use of lambda L chain in lamin B autoantibodies. J. Immunol. 143:1989;3614-3618.
100. Reeves W. H., Chaudhary N., Salerno A., Blobel G. Lamin B autoantibodies in sera of certain patients with systemic lupus erythematosus. J. Exp. Med. 165:1987;750-762.
101. Riemer D., Dodemont H., Weber K. A nuclear lamin of the nematode Caenorhabditis elegans with unusual structural features: cDNA cloning and gene organization. Eur. J. Cell Biol. 62:1993;214-223.
102. Rolls M. M., Stein P. A., Taylor S. S., Ha E., McKeon F., Rapoport T. A. A visual screen of a GFP-fusion library identifies a new type of nuclear envelope membrane protein. J. Cell Biol. 146:1999;29-44.
103. Senecal J. L., Rauch J., Grodzicky T., Raynauld J. P., Uthman I., Nava A., Guimond M., Raymond Y. Strong association of autoantibodies to human nuclear lamin B1 with lupus anticoagulant antibodies in systemic lupus erythematosus. Arthritis Rheumatism. 42:1999;1347-1353.
104. Senecal J. L., Raymond Y. Autoantibodies to major and minor nuclear lamins are not restricted to autoimmune diseases. Clin. Immunol. Immunopathol. 63:1992;115-125.
105. Shimizu T., Cao C. X., Shao R. G., Pommier Y. Lamin B phosphorylation by protein kinase c alpha and proteolysis during apoptosis in human leukemia HL60 cells. J. Biol. Chem. 273:1998;8669-8674.
106. Shimizu T., Pommier Y. Camptothecin-induced apoptosis in p53-null human leukemia HL60 cells and their isolated nuclei: Effects of the protease inhibitors Z-VAD-fmk and dichloroisocoumarin suggest an involvement of both caspases and serine proteases. Leukemia. 11:1997;1238-1244.
107. Silve S., Dupuy P. H., Ferrara P., Loison G. Human lamin B receptor exhibits sterol C14-reductase activity in Saccharomyces cerevisiae. Biochim. Biophys. Acta. 1392:1998;233-244.
108. Simos G., Maison C., Georgatos S. D. Characterization of p18, a component of the lamin B receptor complex and a new integral membrane protein of the avian erythrocyte nuclear envelope. J. Biol. Chem. 271:1996;12617-12625.
109. Smith G. K., Duch D. S., Dev I. K., Kaufmann S. H. Metabolic effects and kill of human T-cell leukemia by 5-deazaacyclotetrahydrofolate, a specific inhibitor of glycineamide ribonucleotide transformylase. Cancer Res. 52:1992;4895-4903.
110. Soullam B., Worman H. J. The amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal. J. Cell Biol. 120:1993;1093-1010.
111. Spann T. P., Moir R. D., Goldman A. E., Stick R., Goldman R. D. Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J. Cell Biol. 136:1997;1201-1212.
112. Stoffler D., Fahrenkrog B., Aebi U. The nuclear pore complex: From molecular architecture to functional dynamics. Curr. Opin. Cell Biol. 11:1999;391-401.
113. Stuurman N., Heins S., Aebi U. Nuclear lamins: Their structure, assembly, and interactions. J. Struct. Biol. 122:1998;42-66.
114. Sullivan T., Escalente-Alcalde D., Bhatt H., Anver M., Naryan B., Nagashima K., Stewart C. L., Burke B. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 147:1999;913-920.
115. Takahashi A., Alnemri E. S., Lazebnik Y. A., Fernandes Alnemri T., Litwack G., Moir R. D., Goldman R. D., Poirier G. G., Kaufmann S. H., Earnshaw W. C. Cleavage of lamin A by Mch2 alpha but not CPP32: Multiple interleukin 1 beta-converting enzyme-related proteases with distinct substrate recognition properties are active in apoptosis. Proc. Natl. Acad. Sci. USA. 93:1996a;8395-8400.
116. Takahashi A., Musy P. Y., Martins L. M., Poirier G. G., Moyer R. W., Earnshaw W. C. CrmA/SPI-2 inhibition of an endogenous ICE-related protease responsible for lamin A cleavage and apoptotic nuclear fragmentation. J. Biol. Chem. 271:1996b;32487-32490.
117. Taniura H., Glass C., Gerace L. A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J. Cell Biol. 131:1995;33-44.
118. Thompson E. B. Apoptosis. Annu. Rev. Physiol. 60:1998;525-533.
119. Tsuchiya Y., Hase A., Ogawa M., Yorifuji H., Arahata K. Distinct regions specify the nuclear membrane targeting of emerin, the responsible protein for Emery-Dreifuss muscular dystrophy. Eur. J. Biochem. 259:1999;859-865.
120. Ucker D. S., Obermiller P. S., Eckhart W., Apgar J. R., Berger N. A., Meyers J. Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes. Mol. Cell Biol. 12:1992;3060-3069.
121. Voelkel J. C., Entingh A. J., Wold W. S., Gooding L. R., Laster S. M. Activation of intracellular proteases is an early event in TNF-induced apoptosis. J. Immunol. 154:1995;1707-1716.
122. Weaver V. M., Carson C. E., Walker P. R., Chaly N., Lach B., Raymond Y., Brown D. L., Sikorska M. Degradation of nuclear matrix and DNA cleavage in apoptotic thymocytes. J. Cell Sci. 109:1996;45-56.
123. Wesierska G. J., Hohenuer H., Hitchman E., Penner E. Anti-gp210 antibodies in sera of patients with primary biliary cirrhosis. Identification of a 64 kD fragment of gp210 as a major epitope. Antibodies Hybridomas. 7:1996a;167-174.
124. Wesierska G. J., Hohenuer H., Hitchman E., Penner E. Autoantibodies against nucleoporin p62 constitute a novel marker of primary biliary cirrhosis. Gastroenterology. 110:1996b;840-847.
125. Wesierska G. J., Penner E., Hitchman E., Sauermann G. Antibodies to nuclear lamins in autoimmune liver disease. Clin. Immunol. Immunopathol. 49:1988;107-115.
126. Wesierska G. J., Penner E., Hitchman E., Sauermann G. Antibodies to nuclear lamin proteins in liver disease. Immunol. Invest. 18:1989;365-372.
127. Wesierska G. J., Penner E., Hitchman E., Sauermann G. Antibodies to nuclear lamin C in chronic hepatitis delta virus infection. Hepatology. 12:1990;1129-1133.
128. Wilson, K. L. (2000), The nuclear envelope and disease, Trends Cell Biol, in press.
129. Worman H. J., Yuan J., Blobel G., Georgatos S. D. A lamin B receptor in the nuclear envelope. Proc. Natl. Acad. Sci. USA. 85:1988;8531-8534.
130. Wydner K. L., McNeil J. A., Lin F., Worman H. J., Lawrence J. B. Chromosomal assignment of human nuclear envelope protein genes LMNA, LMNB1, and LBR by fluorescence in situ hybridization. Genomics. 32:1996;474-478.
131. Xue D., Shaham S., Horvitz R. H. The Caenorhabditis elegans cell-death protein CED-3 is a cystein protease with substrate specificities similar to those of the human CPP32 protease. Genes Dev. 10:1996;1073-1083.
132. Yang L., Guan T., Gerace L. Lamin-binding fragment of LAP2 inhibits increase in nuclear volume during the cell cycle and progression into S phase. J. Cell Biol. 139:1997a;1077-1087.
133. Yang L., Guan T. L., Gerace L. Integral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis. J. Cell Biol. 137:1997b;1199-1210.
134. Ye Q., Callebaut I., Pezhman A., Courvalin J. C., Worman H. J. Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J. Biol. Chem. 272:1997;14983-14989.
135. Zhivotovsky B., Gahm A., Orrenius S. Two different proteases are involved in the proteolysis of lamin during apoptosis. Biochem. Biophys. Res. Commun. 233:1997;96-101.