Skip to main content
Log in

The gene structure ofXenopus nuclear lamin A: A model for the evolution of A-type from B-type lamins by exon shuffling

  • Original Articles
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Nuclear lamins are intermediate filament (IF) type proteins that form a fibrillar network underlying the inner nuclear membrane. The existence of multiple subtypes of lamins in vertebrates has been interpreted in terms of functional specialization during cell division and differentiation. The structure of a gene encoding an A-type lamin ofXenopus laevis was analysed. Comparison with that of a B-type lamin of the same species shows remarkable conservation of the exon/intron pattern. In both genes the last exon, only 9–12 amino acids in length, encodes the complete information necessary for membrane targeting of lamins, i.e. aras-related CaaX motif. The lamin A specific extension of the tail domain is encoded by a single additional exon. The 5′ boundary of this exon coincides with the sequence divergence between human lamins A and C, for which an alternative splice mechanism had previously been suggested. Arguments are presented suggesting that B-type lamins represent the ancestral type of lamins and that A-type lamins derived there from by exon shuffling. The acquisition of the new exon might explain the different fates of A- and B-types lamins during cell division.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aebi U, Cohn J, Buhle L, Gerace L (1986) The nuclear lamina is a meshwork of intermediate filaments. Nature 323:560–564

    Google Scholar 

  • Beck LA, Hosick TJ, Sinensky M (1988) Incorporation of a product of mevalonic acid metabolism into proteins of Chinese hamster ovary cells. J Cell Biol 107:1307–1316

    Google Scholar 

  • Beck LA, Hosick TJ, Sinensky M (1990) Isoprenylation is required for the processing of the lamin A precursor. J Cell Biol 110:1489–1499

    Google Scholar 

  • Benavente R, Krohne G (1986) Involvement of nuclear lamins in postmitotic reorganization of chromatin as demonstrated by microinjection of lamin antibodies. J Cell Biol 103:1847–1854

    Google Scholar 

  • Benavente R, Krohne G, Franke WW (1985) Cell type-specific expression of nuclear lamin proteins during development ofXenopus laevis. Cell 41:177–190

    Google Scholar 

  • Bisbee CA, Baker MA, Wilson A, Hadji-Azimi I, Fischberg M (1977) Albumin phylogeny for clawed frogs (Xenopus). Science 195:785–787

    Google Scholar 

  • Blake CCF (1985) Exons and the evolution of proteins. Int Rev Cytol 93:149–185

    Google Scholar 

  • Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383

    Google Scholar 

  • Burke B (1990) On the cell-free association of lamins A and C with metaphase chromosomes. Exp Cell Res 186:169–176

    Google Scholar 

  • Burke B, Gerace L (1986) A cell free system to study reassembly of the nuclear envelope at the end of mitosis. Cell 44:639–652

    Google Scholar 

  • Capon DJ, Seeburg PH, McGrath JP, Hayflick JS, Edman U, Levinson AD, Goeddel DV (1983) Activation of Ki-ras2 gene in human colon and lung carcinomas by two different point mutations. Nature 304:507–512

    Google Scholar 

  • Dessev G, Goldman R (1990) The oocyte lamin persists as a single major component of the nuclear lamina during embryonic development of the surf clam. Int J Dev Biol 34:267–274

    Google Scholar 

  • Dodemont H, Riemer D, Weber K (1990) Structure of an invertebrate gene encoding cytoplasmic intermediate filament (IF) proteins: implications for the origin and the diversification of IF proteins. EMBO J 9:4083–4094

    Google Scholar 

  • Döring V, Stick R (1990) Gene structure of nuclear lamin LIII ofXenopus laevis; a model for the evolution of IF proteins from a lamin-like ancestor. EMBO J 9:4073–4081

    Google Scholar 

  • Farnsworth CC, Gelb MH, Glomset JA (1990) Identification of geranylgeranyl-modified proteins in HeLa cells. Science 247:320–322

    Google Scholar 

  • Fawcett DW (1966) On the occurrence of a fibrous lamina on the inner aspect of the nuclear envelope in certain cells of vertebrates. Am J Anat 119:129–146

    Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabelling DNA restriction endonuclease fragments to a high specific activity. Anal Biochem 123:13–16

    Google Scholar 

  • Fisher DZ, Chaudhary N, Blobel G (1986) cDNA sequencing of nuclear lamin A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci USA 83:6450–6454

    Google Scholar 

  • Georgatos SG, Maroulakou I, Blobel G (1989) Lamin A, lamin B and lamin B receptor analogues in yeast. J Cell Biol 108:2069–2082

    Google Scholar 

  • gerace L, Blobel G (1980) The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19:277–287

    Google Scholar 

  • Gerace L, Burke B (1988) Functional organization of the nuclear envelope. Annu Rev Cell Biol 4:335–374

    Google Scholar 

  • Gieffers C, Krohne G (1991) In vitro reconstitution of recombinant lamin A and a lamin A mutant lacking the carboxy-terminal tail. Eur J Cell Biol 55:191–199

    Google Scholar 

  • Glass JR, Gerace L (1990) Lamins A and C bind and assemble at the mitotic chromosomes. J Cell Biol 111:1047–1057

    Google Scholar 

  • Gruenbaum Y, Landesman Y, Drees B, Bare JW, Saumweber H, Paddy MR, Sedat JW, Smith DE, Benton BM, Fisher PA (1988)Drosophila nuclear lamin precursor Dmo is translated from either of two developmentally regulated mRNA species apparently encoded by a single gene. J Cell Biol 106:585–596

    Google Scholar 

  • Hancock JF, Magee AI, Childs JE, Marshall CJ (1989) All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57:1167–1177

    Google Scholar 

  • Hancock JF, Paterson H, Marshall CJ (1990) A polybasic domain or palmitoylation is required in addition to the CaaX motif to localize p21-ras to the plasma membrane. Cell 63:133–139

    Google Scholar 

  • Heitlinger E, Peter M, Häner M, Lustig A, Aebi U, Nigg EA (1991) Expression of chicken lamin B2 inEscherichia coli: characterization of its structure, assembly and molecular interactions. J Cell Biol 113:485–495

    Google Scholar 

  • Höger TH, Krohne G, Franke WW (1988) Amino acid sequence and molecular characterization of murine lamin B as deduced from cDNA clones. Eur J Cell Biol 47:283–290

    Google Scholar 

  • Höger TH, Zatloukal K, Waizenegger I, Krohne G (1990) Characterization of a second highly conserved B-type lamin present in cells previously thought to contain only a single B-type lamin. Chromosoma 99:379–390

    Google Scholar 

  • Höger TH, Krohne G, Kleinschmidt JA (1991) Interaction ofXenopus lamins A and LII with chromatin in vitro mediated by a sequence element in the carboxyterminal domain. Exp Cell Res 197:280–289

    Google Scholar 

  • Holland SK, Blake CC (1990) Proteins, exons and molecular evolution. In: Stone EM, Schwartz RJ (eds) Intervening sequences in evolution and development. Oxford University Press, Oxford, pp 10–42

    Google Scholar 

  • Holtz D, Tanaka RA, Hartwig J, McKeon F (1989) The CaaX motif of lamin A functions in conjunction with the nuclear localization signal to target assembly to the nuclear envelope. Cell 59:969–977

    Google Scholar 

  • Kamiya Y, Sakurai A, Tamura S, Takahasi N, Tsuchiya E, Abe K, Fukui S (1979) Structure of Rhodoturicine A, a peptidyl factor, inducing mating tube formation inRhodosporidium toruloides. Agric Biol Chem 43:363–369

    Google Scholar 

  • Kitten GT, Nigg EA (1991) The CaaX motif is required for isoprenylation, carboxy methylation and nuclear membrane association of lamin B2. J Cell Biol 113:13–23

    Google Scholar 

  • Krohne G, Wolin SL, McKeon F, Franke WW, Kirschner MW (1987) Nuclear lamin LI ofXenopus laevis: cDNA cloning, amino acid sequence and binding specificity of a member of the lamin B subfamily. EMBO J 6: 3801–3808

    Google Scholar 

  • Krohne G, Waizenegger I, Höger TH (1989) The conserved carboxy-terminal cysteine of nuclear lamins is essential for lamin association with the nuclear envelope. J Cell Biol 109: 2003–2013

    Google Scholar 

  • Lebel S, Lampron C, Royal A, Raymond Y (1987) Lamins A and C appear during retinoic acid-induced differentiation of mouse embryonal carcinoma cells. J Cell Biol 105: 1099–1104

    Google Scholar 

  • Lehner CF, Kurer V, Eppenberger HM, Nigg EA (1986) The nuclear lamin protein family in higher vertebrates: Identification of quantitatively minor lamin proteins by monoclonal antibodies. J Biol Chem 261: 13293–13301

    Google Scholar 

  • Lehner CF, Stick R, Eppenberger HM, Nigg EA (1987) Differential expression of nuclear lamin proteins during chicken development. J Cell Biol 105: 577–587

    Google Scholar 

  • Loewinger L, McKeon F (1988) Mutations in the nuclear lamin proteins resulting in their aberrant assembly in the cytoplasm. EMBO J 7: 2301–2308

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Maul GG, Baglia FA, Newmeyer DD, Ohlsson-Wilhelm BM (1984) The major 67000 molecular weight protein of the clam oocyte nuclear envelope is lamin-like. J Cell Sci 67: 69–85

    Google Scholar 

  • McGrath JP, Capon DJ, Smith DH, Chen EY, Seeburg PH, Goeddel GV, Levinson AD (1983) Structure and organization of the human Ki-ras proto-oncogene and a related processed pseudogene. Nature 304: 501–506

    Google Scholar 

  • McKeon FD, Kirschner MW, Caput D (1986) Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature 319: 463–468

    Google Scholar 

  • Meier J, Campbell KHS, Ford CC, Stick R, Hutchinson CJ (1991) The role of lamin LIII in nuclear assembly and DNA replication, in cell-free extracts ofXenopus eggs. J Cell Sci 98: 271–279

    Google Scholar 

  • Moir RD, Donaldson AD, Stewart M (1991) Expression inEscherichia coli of human lamin A and C: influence of head and tail domains on assembly properties and paracrystal formation. J Cell Sci 99: 363–372

    Google Scholar 

  • Moreno Díaz de la Espina S, Barthellemy I, Cerezuela MA (1991) Isolation and ultrastructural characterization of the residual nuclear matrix in a plant cell system. Chromosoma 100: 110–117

    Google Scholar 

  • Müller WP (1974) The lampbrush chromosomes ofXenopus laevis (Daudin). Chromosoma 47: 283–296

    Google Scholar 

  • Newport JW, Wilson KL, Dunphy WG (1990) A lamin-independent pathway for nuclear envelope assembly. J Cell Biol 111: 2247–2259

    Google Scholar 

  • Osman M, Paz M, Landesman Y, Fainsod A, Gruenbaum Y (1990) Molecular analysis of theDrosophila nuclear lamin gene. Genomics 8: 217–224

    Google Scholar 

  • Padgett RA, Grabowski PJ, Konarska MM, Seiler S, Sharp PA (1986) Splicing of messenger RNA precursors. Annu Rev Biochem 55: 1119–1150

    Google Scholar 

  • Pappas GD (1956) The fine structure of the nuclear envelope ofAmoeba proteus. J Biophys Biochem Cytol 2: 431–435

    Google Scholar 

  • Paulin-Levasseur M, Scherbarth A, Traub U, Traub P (1988) Lack of lamins A and C in mammalian hemopoietic cell lines devoid of intermediate filament proteins. Eur J Cell Biol 47: 121–131

    Google Scholar 

  • Peter M, Nigg EA (1991) Ectopic expression of an A-type lamin does not interfere with differentiation of lamin-A-negative embryonal carconima cells. J Cell Sci 100: 589–598

    Google Scholar 

  • Peter M, Kitten GT, Lehner CF, Vorburger K, Bailer SM, Maridor G, Nigg EA (1989) Cloning and sequencing of cDNA clones encoding chicken lamins A and B1 and comparison of the primary structures of vertebrate A-and B-type lamins. J Mol Biol 208: 393–404

    Google Scholar 

  • Pollard KM, Chan EKL, Grant BJ, Sullivan KF, Tan EM, Glass CA (1990) In vitro posttranslational modification of lamin B cloned from human T-cell line. Mol Cell Biol 10: 2164–2175

    Google Scholar 

  • Reiss Y, Goldstein JL, Seabra MC, Casey PJ, Brown MS (1990) Inhibition of purified p21ras farnesyl: protein transferase by Cys-AAX tetrapeptides. Cell 62: 81–88

    Google Scholar 

  • Riedel W, Werner D (1989) Nucleotide sequence of the full-length mouse lamin C cDNA and its deduced amino-acid sequence. Biochim Biophys Acta 1008: 119–122

    Google Scholar 

  • Röber R-A, Weber K, Osborn M (1989) Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 105: 365–378

    Google Scholar 

  • Röber R-A, Gieseler RKH, Peters HJ, Weber K, Osborn M (1990) Induction of nuclear lamins A/C in macrophages in in vitro cultures of rat bone marrow precursor cells and human blood monocytes and in macrophages elicited in vivo by thioglycollate stimulation. Exp Cell Res 190: 185–194

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74: 5463–5467

    Google Scholar 

  • Shimizu K, Birnbaum D, Ruley MA, Fasano O, Suard Y, Edlund L, Taparowsky E, Goldfarb M, Wigler M (1983) Structure of the Ki-ras gene of the human lung carcinoma cell line Calu-1. Nature 304: 497–500

    Google Scholar 

  • Smith DE, Fisher PA (1984) Identification, developmental regulation and response to heat shock of two antigenically related forms of a major nuclear envelope protein inDrosophila embryos: application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots. J Cell Biol 99: 20–28

    Google Scholar 

  • Steward C, Burke B (1987) Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell 51: 383–392

    Google Scholar 

  • Stick R (1988) cDNA cloning of the developmentally regulated lamin LIII ofXenopus laevis. EMBO J 7: 3189–3197

    Google Scholar 

  • Stick R, Hausen P (1985) Changes in the nuclear lamina composition during early development ofXenopus laevis. Cell 41: 191–200

    Google Scholar 

  • Stick R, Angres B, Lehner CF, Nigg EA (1988) The fates of chicken nuclear lamin proteins during mitosis: evidence for a reversible redistribution of lamin B2 between inner nuclear membrane and elements of the endoplasmatic reticulum. J Cell Biol 107: 397–406

    Google Scholar 

  • Vorburger K, Lehner CF, Kitten G, Eppenberger HM, Nigg EA (1989) A second higher vertebrate B-type lamin: cDNA sequence determination and in vitro processing of chicken lamin B2. J Mol Biol 208: 405–415

    Google Scholar 

  • Weber K, Plessmann U, Traub P (1989) Maturation of nuclear lamin A involves a specific carboxy-terminal trimming, which removes the polyisoprenylation site from the precursor; implications for the structure of the nuclear lamina. FEBS Lett 257: 411–414

    Google Scholar 

  • Wilkie TM, Simon MI (1991) Cloning multigene families with degenerate PCR primers. Methods 2: 32–41

    Google Scholar 

  • Wolin SL, Krohne G, Kirschner MW (1987) A new lamin inXenopus somatic tissues displays strong homology to human lamin A. EMBO J 6: 3809–3818

    Google Scholar 

  • Zewe M, Höger TH, Fink T, Lichter P, Krohne G, Franke WW (1991) Gene structure and chromosomal localization of the murine lamin B2 gene. Eur J Cell Biol 56: 342–350

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

by H. Jäckle

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stick, R. The gene structure ofXenopus nuclear lamin A: A model for the evolution of A-type from B-type lamins by exon shuffling. Chromosoma 101, 566–574 (1992). https://doi.org/10.1007/BF00660316

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00660316

Keywords

Navigation