Journal of Cell Science, Vol 108, Issue 10 3189-3198, Copyright © 1995 by Company of Biologists

JOURNAL ARTICLES

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

D Riemer, N Stuurman, M Berrios, C Hunter, PA Fisher and K Weber
Max-Planck-Institute for Biophysical Chemistry, Department of Biochemistry, Goettingen, FRG.

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.

This article has been cited by other articles:

				T. Dechat, K. Pfleghaar, K. Sengupta, T. Shimi, D. K. Shumaker, L. Solimando, and R. D. Goldman Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin Genes & Dev., April 1, 2008; 22(7): 832 - 853. [Abstract] [Full Text] [PDF]

				K. A. Clark, J. M. Bland, and M. C. Beckerle The Drosophila muscle LIM protein, Mlp84B, cooperates with D-titin to maintain muscle structural integrity J. Cell Sci., June 15, 2007; 120(12): 2066 - 2077. [Abstract] [Full Text] [PDF]

				X. Bao, W. Zhang, R. Krencik, H. Deng, Y. Wang, J. Girton, J. Johansen, and K. M. Johansen The JIL-1 kinase interacts with lamin Dm0 and regulates nuclear lamina morphology of Drosophila nurse cells J. Cell Sci., November 1, 2005; 118(21): 5079 - 5087. [Abstract] [Full Text] [PDF]

				S. R. Schulze, B. Curio-Penny, Y. Li, R. A. Imani, L. Rydberg, P. K. Geyer, and L. L. Wallrath Molecular Genetic Analysis of the Nested Drosophila melanogaster Lamin C Gene Genetics, September 1, 2005; 171(1): 185 - 196. [Abstract] [Full Text] [PDF]

				J. Molnar, Z. Ujfaludi, S. F. T. Fong, J. A. Bollinger, G. Waro, B. Fogelgren, D. M. Dooley, M. Mink, and K. Csiszar Drosophila Lysyl Oxidases Dmloxl-1 and Dmloxl-2 Are Differentially Expressed and the Active DmLOXL-1 Influences Gene Expression and Development J. Biol. Chem., June 17, 2005; 280(24): 22977 - 22985. [Abstract] [Full Text] [PDF]

				K. Patterson, A. B. Molofsky, C. Robinson, S. Acosta, C. Cater, and J. A. Fischer The Functions of Klarsicht and Nuclear Lamin in Developmentally Regulated Nuclear Migrations of Photoreceptor Cells in the Drosophila Eye Mol. Biol. Cell, February 1, 2004; 15(2): 600 - 610. [Abstract] [Full Text] [PDF]

				K. Furukawa, S. Sugiyama, S. Osouda, H. Goto, M. Inagaki, T. Horigome, S. Omata, M. McConnell, P. A. Fisher, and Y. Nishida Barrier-to-autointegration factor plays crucial roles in cell cycle progression and nuclear organization in Drosophila J. Cell Sci., September 15, 2003; 116(18): 3811 - 3823. [Abstract] [Full Text] [PDF]

				S. S. Mani, R. Rajagopal, A. B. Garfinkel, X. Fan, and M. F. Wolfner A hydrophilic lamin-binding domain from the Drosophila YA protein can target proteins to the nuclear envelope J. Cell Sci., May 15, 2003; 116(10): 2067 - 2072. [Abstract] [Full Text] [PDF]

				Y. Gruenbaum, K. K. Lee, J. Liu, M. Cohen, and K. L. Wilson The expression, lamin-dependent localization and RNAi depletion phenotype for emerin in C. elegans J. Cell Sci., January 3, 2002; 115(5): 923 - 929. [Abstract] [Full Text] [PDF]

				D Lourim and G Krohne Chromatin binding and polymerization of the endogenous Xenopus egg lamins: the opposing effects of glycogen and ATP J. Cell Sci., June 14, 1999; 111(24): 3675 - 3686. [Abstract] [PDF]

				J. Broers, B. Machiels, G. van Eys, H. Kuijpers, E. Manders, R van Driel, and F. Ramaekers Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins J. Cell Sci., January 10, 1999; 112(20): 3463 - 3475. [Abstract] [PDF]

				M. Goldberg, H. Lu, N. Stuurman, R. Ashery-Padan, A. M. Weiss, J. Yu, D. Bhattacharyya, P. A. Fisher, Y. Gruenbaum, and M. F. Wolfner Interactions among Drosophila Nuclear Envelope Proteins Lamin, Otefin, and YA Mol. Cell. Biol., July 1, 1998; 18(7): 4315 - 4323. [Abstract] [Full Text]

				D Riemer and K Weber Common and variant properties of intermediate filament proteins from lower chordates and vertebrates; two proteins from the tunicate Styela and the identification of a type III homologue J. Cell Sci., January 10, 1998; 111(19): 2967 - 2975. [Abstract] [PDF]

				R Rzepecki, S. Bogachev, E Kokoza, N Stuurman, and P. Fisher In vivo association of lamins with nucleic acids in Drosophila melanogaster J. Cell Sci., January 1, 1998; 111(1): 121 - 129. [Abstract] [PDF]

				B. Lenz-Bohme, J. Wismar, S. Fuchs, R. Reifegerste, E. Buchner, H. Betz, and B. Schmitt Insertional Mutation of the Drosophila Nuclear Lamin Dm0 Gene Results in Defective Nuclear Envelopes, Clustering of Nuclear Pore Complexes, and Accumulation of Annulate Lamellae J. Cell Biol., June 2, 1997; 137(5): 1001 - 1016. [Abstract] [Full Text] [PDF]

				M Klapper, K Exner, A Kempf, C Gehrig, N Stuurman, P. Fisher, and G Krohne Assembly of A- and B-type lamins studied in vivo with the baculovirus system J. Cell Sci., January 10, 1997; 110(20): 2519 - 2532. [Abstract] [PDF]

				G Zimowska, J. Aris, and M. Paddy A Drosophila Tpr protein homolog is localized both in the extrachromosomal channel network and to nuclear pore complexes J. Cell Sci., January 4, 1997; 110(8): 927 - 944. [Abstract] [PDF]

				J. Lopez and M. Wolfner The developmentally regulated Drosophila embryonic nuclear lamina protein 'Young Arrest' (fs(1)Ya) is capable of associating with chromatin J. Cell Sci., January 3, 1997; 110(5): 643 - 651. [Abstract] [PDF]