Nuclear Envelope Dynamics in Drosophila Pronuclear Formation and in Embryos
As in other animals, the nuclear envelope in Drosophila has three basic subparts: the nuclear membranes, a lamina just beneath the membrane layer, and nuclear pores that rivet the nuclear membranes and permit nucleo-cytoplasmic transport.
There are two nuclear membranes, each a lipid bilayer containing characteristic proteins. The outer nuclear membrane is continuous with the endoplasmic reticulum. The inner nuclear membrane contains proteins that can associate with lamin and/or chromatin. The Drosophila genome predicts genes for relatives of several proteins known to be in the inner membranes of vertebrates or nematodes. These include otefin, a LEM protein, which has been shown to be a constituent of the Drosophila inner nuclear membrane, and predicted counterparts of two other LEM proteins (emerin and MAN-1) as well as nurim, the lamin B receptor (LBR), and unc-84
The Drosophila nuclear lamina contains proteins related to those in other animal nuclear laminas. In particular, its major constituent is intermediate-filament proteins of the lamin family. As in most higher animals, Drosophila has lamins of two subtypes: A-type and B-type. However, its suite of lamins is simpler than that in vertebrates. Drosophila has a single gene for a B-type lamin called lamin Dm0.8 Lamin Dm0 derivatives (called, collectively, lamin Dm, below) are present in the nuclear envelopes of nearly all Drosophila cells and, this protein is essential for full viability. Fertility of Drosophila females also demands sufficient levels of lamin Dm0 derivatives in the female germ line.15 The B-type lamin undergoes posttranslational modifications, including phosphorylations that convert it from a soluble form (Dmmit) to nuclear forms that can make polymeric fibers in the lamina (Dm1, Dm2).11,16Drosophila's single A-type lamin (“lamin C”,17–19) analogous to the vertebrate situation, is found only in certain cell types; in Drosophila these are a subset of differentiated cells. Drosophila nuclear laminas in early embryos include at least one protein without a vertebrate counterpart—the Young Arrest (“YA”) protein,1,20 a novel hydrophilic nuclear lamina component that is essential for embryonic development to initiate (see below). Made only during oogenesis (though excluded from nuclei at this time21,22), YA is found only in the nuclei of young (cleavage stage) embryos;1,20 after this time it is not detected in any Drosophila cells, except for developing oocytes.
Drosophila nuclear envelopes also contain pore complexes whose components are relatives of those of vertebrate nuclear pores: including nup154, gp210, a Tpr homologue, myosin-like proteins and a predicted nup153 homologue with RNA binding activity. Components of the nuclear import/export system, including importin family members and an exportin homologue, have also been found in Drosophila.
Cell cycle dynamics: In at least some, and possibly all,Drosophila cells, nuclear envelopes do not completely break down during mitosis. This was first shown for cleavage stage Drosophila embryos, in an elegant electron microscopy study; subsequent investigators extended this finding by documenting the behaviors of specific nuclear envelope, or envelope-associated, proteins during the cell cycles in embryos. The envelopes of interphase nuclei in embryos are continuous around the nuclei. By prometaphase, the envelopes are seen to be open at the spindle poles. A second membrane layer, paralleling the nuclear membranes and, like them, open at the spindle poles, begins to form around the original nuclear envelope. Nuclear pores dissociate from the nuclear membranes beginning in prophase. In metaphase, the nuclear lamina largely dissociates: most of its lamin Dm disappears from the nuclear periphery5 and YA also becomes undetectable at the nuclear periphery. However, the fenestrated, double “spindle envelope” remains, still open at the poles. Chromosomes segregate on the spindle within this envelope. At telophase, lamin Dm, otefin and nuclear pore proteins begin to be detected in the nuclear envelopes, and the second membrane layer disappears. At the end of telophase in early embryos, the YA protein becomes detectable at the nuclear periphery, suggesting that it assembles into the nuclear envelope after lamin Dm.1 These nuclear envelope dynamics may be characteristic of all Drosophila nuclei: spindle envelopes of similar appearance to those reported by Stafstrom and Staehelin40 have also been seen in spermatogenic cells41and in cultured Drosophila cells.
As in other animals, the nuclear envelope in Drosophila has three basic subparts: the nuclear membranes, a lamina just beneath the membrane layer, and nuclear pores that rivet the nuclear membranes and permit nucleo-cytoplasmic transport.
There are two nuclear membranes, each a lipid bilayer containing characteristic proteins. The outer nuclear membrane is continuous with the endoplasmic reticulum. The inner nuclear membrane contains proteins that can associate with lamin and/or chromatin. The Drosophila genome predicts genes for relatives of several proteins known to be in the inner membranes of vertebrates or nematodes. These include otefin, a LEM protein, which has been shown to be a constituent of the Drosophila inner nuclear membrane, and predicted counterparts of two other LEM proteins (emerin and MAN-1) as well as nurim, the lamin B receptor (LBR), and unc-84
The Drosophila nuclear lamina contains proteins related to those in other animal nuclear laminas. In particular, its major constituent is intermediate-filament proteins of the lamin family. As in most higher animals, Drosophila has lamins of two subtypes: A-type and B-type. However, its suite of lamins is simpler than that in vertebrates. Drosophila has a single gene for a B-type lamin called lamin Dm0.8 Lamin Dm0 derivatives (called, collectively, lamin Dm, below) are present in the nuclear envelopes of nearly all Drosophila cells and, this protein is essential for full viability. Fertility of Drosophila females also demands sufficient levels of lamin Dm0 derivatives in the female germ line.15 The B-type lamin undergoes posttranslational modifications, including phosphorylations that convert it from a soluble form (Dmmit) to nuclear forms that can make polymeric fibers in the lamina (Dm1, Dm2).11,16Drosophila's single A-type lamin (“lamin C”,17–19) analogous to the vertebrate situation, is found only in certain cell types; in Drosophila these are a subset of differentiated cells. Drosophila nuclear laminas in early embryos include at least one protein without a vertebrate counterpart—the Young Arrest (“YA”) protein,1,20 a novel hydrophilic nuclear lamina component that is essential for embryonic development to initiate (see below). Made only during oogenesis (though excluded from nuclei at this time21,22), YA is found only in the nuclei of young (cleavage stage) embryos;1,20 after this time it is not detected in any Drosophila cells, except for developing oocytes.
Drosophila nuclear envelopes also contain pore complexes whose components are relatives of those of vertebrate nuclear pores: including nup154, gp210, a Tpr homologue, myosin-like proteins and a predicted nup153 homologue with RNA binding activity. Components of the nuclear import/export system, including importin family members and an exportin homologue, have also been found in Drosophila.
Cell cycle dynamics: In at least some, and possibly all,Drosophila cells, nuclear envelopes do not completely break down during mitosis. This was first shown for cleavage stage Drosophila embryos, in an elegant electron microscopy study; subsequent investigators extended this finding by documenting the behaviors of specific nuclear envelope, or envelope-associated, proteins during the cell cycles in embryos. The envelopes of interphase nuclei in embryos are continuous around the nuclei. By prometaphase, the envelopes are seen to be open at the spindle poles. A second membrane layer, paralleling the nuclear membranes and, like them, open at the spindle poles, begins to form around the original nuclear envelope. Nuclear pores dissociate from the nuclear membranes beginning in prophase. In metaphase, the nuclear lamina largely dissociates: most of its lamin Dm disappears from the nuclear periphery5 and YA also becomes undetectable at the nuclear periphery. However, the fenestrated, double “spindle envelope” remains, still open at the poles. Chromosomes segregate on the spindle within this envelope. At telophase, lamin Dm, otefin and nuclear pore proteins begin to be detected in the nuclear envelopes, and the second membrane layer disappears. At the end of telophase in early embryos, the YA protein becomes detectable at the nuclear periphery, suggesting that it assembles into the nuclear envelope after lamin Dm.1 These nuclear envelope dynamics may be characteristic of all Drosophila nuclei: spindle envelopes of similar appearance to those reported by Stafstrom and Staehelin40 have also been seen in spermatogenic cells41and in cultured Drosophila cells.
