Expression of Drosophila lamin C is developmentally regulated: analogies with vertebrate A-type lamins.

Vertebrate nuclear lamins form a multigene family with developmentally controlled expression. In contrast, invertebrates have long been thought to contain only a single lamin, which in Drosophila is the well-characterized lamin Dm0. Recently, however, a Drosophila cDNA clone (pG-IF) has been identified that codes for an intermediate filament protein which harbors a nuclear localization signal but lacks a carboxy-terminal CAAX motif. Based on these data the putative protein encoded by pG-IF was tentatively called Drosophila lamin C. To address whether the pG-IF encoded protein is expressed and whether it encodes a cytoplasmic intermediate filament protein or a nuclear lamin we raised antibodies against the recombinant pG-IF protein. The antibodies decorate the nuclear envelope in Drosophila Kc tissue culture cells as well as in salivary and accessory glands demonstrating that pG-IF encodes a nuclear lamin (lamin C). Antibody decoration, in situ hybridization, western and northern blotting studies show that lamin C is acquired late in embryogenesis. In contrast, lamin Dm0 is constitutively expressed. Lamin C is first detected in late stage 12 embryos in oenocytes, hindgut and posterior spiracles and subsequently also in other differentiated tissues. In third instar larvae lamins C and Dm0 are coexpressed in all tissues tested. Thus, Drosophila has two lamins: lamin Dm0, containing a CaaX motif, is expressed throughout, while lamin C, lacking a CaaX motif, is expressed only later in development. Expression of Drosophila lamin C is similar to that of vertebrate lamin A (plus C), which loses its CaaX motif during incorporation into the lamina.

[1]  E. Nigg.  Assembly-disassembly of the nuclear lamina. , 1992 .

[2]  S. Nilsson.  The Alimentary Canal , 1983 .

[3]  C. Allis,et al.  Mass isolation of pole cells from Drosophila melanogaster. , 1977, Developmental biology.

[4]  C. Lehner,et al.  Biogenesis of the nuclear lamina: in vivo synthesis and processing of nuclear protein precursors. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[5]  G. Blobel,et al.  The nuclear envelope lamina is reversibly depolymerized during mitosis , 1980, Cell.

[6]  K. Weber,et al.  A nuclear lamin of the nematode Caenorhabditis elegans with unusual structural features; cDNA cloning and gene organization. , 1993, European journal of cell biology.

[7]  S. Clarke,et al.  Protein isoprenylation and methylation at carboxyl-terminal cysteine residues. , 1992, Annual review of biochemistry.

[8]  V. Hartenstein,et al.  The Pattern of Embryonic Cell Divisions , 1985 .

[9]  S. Georgatos,et al.  Type B lamins remain associated with the integral nuclear envelope protein p58 during mitosis: implications for nuclear reassembly. , 1994, The EMBO journal.

[10]  P. Fisher,et al.  Identification, developmental regulation, and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryos: application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots , 1984, The Journal of cell biology.

[11]  P. Traub,et al.  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 , 1989, FEBS letters.

[12]  R. Lutz,et al.  The prenylation of proteins , 1992, Bioessays.

[13]  A. Kupfer,et al.  The processing pathway of prelamin A. , 1994, Journal of cell science.

[14]  A. Whalen,et al.  Developmental regulation of Drosophila DNA topoisomerase II , 1991, The Journal of cell biology.

[15]  C. Stewart,et al.  Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B , 1987, Cell.

[16]  L. Jong,et al.  Binding of matrix attachment regions to lamin B1 , 1992, Cell.

[17]  G. Dessev,et al.  The oocyte lamin persists as a single major component of the nuclear lamina during embryonic development of the surf clam. , 1990, The International journal of developmental biology.

[18]  U. Plessmann,et al.  Cytoplasmic intermediate filament proteins of invertebrates are closer to nuclear lamins than are vertebrate intermediate filament proteins; sequence characterization of two muscle proteins of a nematode. , 1989, The EMBO journal.

[19]  E. Nigg.  Assembly-disassembly of the nuclear lamina , 1992, Current Biology.

[20]  K. Hasel,et al.  The alpha‐helical rod domain of human lamins A and C contains a chromatin binding site. , 1993, The EMBO journal.

[21]  J. Hartwig,et al.  The CaaX motif of lamin A functions in conjunction with the nuclear localization signal to target assembly to the nuclear envelope , 1989, Cell.

[22]  M. Sanders,et al.  A cDNA from Drosophila melanogaster encodes a lamin C-like intermediate filament protein. , 1993, Journal of cell science.

[23]  K. Weber,et al.  Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. , 1989, Development.

[24]  H. Worman,et al.  Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. , 1993, The Journal of biological chemistry.

[25]  J. Sedat,et al.  Localization of antigenic determinants in whole Drosophila embryos. , 1983, Developmental biology.

[26]  M. Peter,et al.  Ectopic expression of an A-type lamin does not interfere with differentiation of lamin A-negative embryonal carcinoma cells. , 1991, Journal of cell science.

[27]  I. Waizenegger,et al.  The conserved carboxy-terminal cysteine of nuclear lamins is essential for lamin association with the nuclear envelope , 1989, The Journal of cell biology.

[28]  U. Aebi,et al.  The nuclear lamina is a meshwork of intermediate-type filaments , 1986, Nature.

[29]  V. Foe,et al.  Mitotic domains reveal early commitment of cells in Drosophila embryos. , 1989, Development.

[30]  C. Hutchison,et al.  The role of lamin LIII in nuclear assembly and DNA replication, in cell-free extracts of Xenopus eggs. , 1991, Journal of cell science.

[31]  S. Janicki,et al.  Determinants for intracellular sorting of cytoplasmic and nuclear intermediate filaments , 1994, The Journal of cell biology.

[32]  P. Fisher,et al.  Interconversion of Drosophila nuclear lamin isoforms during oogenesis, early embryogenesis, and upon entry of cultured cells into mitosis , 1989, The Journal of cell biology.

[33]  Y. Gruenbaum,et al.  Biosynthesis and interconversion of Drosophila nuclear lamin isoforms during normal growth and in response to heat shock , 1987, The Journal of cell biology.

[34]  K. Wilson,et al.  A lamin-independent pathway for nuclear envelope assembly , 1990, The Journal of cell biology.

[35]  K Weber,et al.  Intermediate filaments: structure, dynamics, function, and disease. , 1994, Annual review of biochemistry.

[36]  F. McKeon,et al.  Mutations in the nuclear lamin proteins resulting in their aberrant assembly in the cytoplasm. , 1988, The EMBO journal.

[37]  R. Goldman,et al.  Dynamic properties of nuclear lamins: lamin B is associated with sites of DNA replication , 1994, The Journal of cell biology.

[38]  C. Lehner,et al.  A second higher vertebrate B-type lamin. cDNA sequence determination and in vitro processing of chicken lamin B2. , 1989, Journal of molecular biology.

[39]  G. Krohne,et al.  Interaction of Xenopus lamins A and LII with chromatin in vitro mediated by a sequence element in the carboxyterminal domain. , 1991, Experimental cell research.

[40]  J. Sedat,et al.  Drosophila nuclear lamin precursor Dm0 is translated from either of two developmentally regulated mRNA species apparently encoded by a single gene [published erratum appears in J Cell Biol 1988 Jun;106(6):2225] , 1988, Journal of Cell Biology.

[41]  C. Lehner,et al.  Differential expression of nuclear lamin proteins during chicken development , 1987, The Journal of cell biology.

[42]  K. Weber,et al.  The organization of the gene for Drosophila lamin C: limited homology with vertebrate lamin genes and lack of homology versus the Drosophila lamin Dmo gene. , 1994, European journal of cell biology.

[43]  E. Nigg,et al.  The role of isoprenylation in membrane attachment of nuclear lamins. A single point mutation prevents proteolytic cleavage of the lamin A precursor and confers membrane binding properties. , 1994, Journal of cell science.

[44]  E. Nigg,et al.  The CaaX motif is required for isoprenylation, carboxyl methylation, and nuclear membrane association of lamin B2 , 1991, The Journal of cell biology.

[45]  V. Hartenstein.  Atlas of Drosophila development , 1993 .

[46]  C. Lehner,et al.  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 endoplasmic reticulum , 1988, The Journal of cell biology.

[47]  R. Goldman,et al.  Lamin dynamics. , 1993, Current opinion in cell biology.

[48]  E. Nigg,et al.  The nuclear envelope. , 1989, Current opinion in cell biology.