Activities of the nuclear envelope in the salivary glands of Drosophila

Abstract

Morphological data are presented concerning the single-membrane-bound vesicles ("oval bodies") associated with the nuclear envelopes of larval salivary gland cells of Drosophila. Data are also presented concerning the existence of cytoplasmic annulate lamellae in these same cells. The mode of formation of these structures, as well as the relationships between them and with other cytoplasmic organelles are described. The possible functional significance of these phenomena is discussed.

Cytoplasmic Capes Are Nuclear Envelope Intrusions That Are Enriched in Endosomal Proteins and Depend upon βH-Spectrin and Annexin B9

“…Within this space we see occasional single-membrane bound vesicles as well as non-membrane bound granules (Figure 3A,D and Movie S3). The regions proximal to the nuclear boundary contains a large number of single membrane-bound vesicles separated from the nucleoplasm by an additional single membrane indicating that these are vesicles in the perinuclear space as previously described [17]. These regions are often associated with out-foldings of the outer nuclear membrane.…”

“…These structures seem to be substantially bigger in the large, highly polytenized nuclei of the salivary gland. Subsequent ultrastructural analysis (see below) indicates that these structures are the same as ‘cytoplasmic capes’ [17] and so this term will be used hereinafter.…”

“…Cytoplasmic organelles have been seen in cytoplasmic capes [17], [25] and the discovery that multiple endosomal markers are present in cytoplasmic capes suggests both that endosomes are present in these structures and that protein sorting is occurring at this location. If this is true, then the concentration of mSpitz in cytoplasmic capes may have functional importance not detected by our assays.…”

“…The capes we describe were originally identified as sites of budding of the inner nuclear membrane to form vesicles in the perinuclear lumen (perinuclear vesicles) and of possible export of RNA to the cytoplasm [17], [25]. Recent confirmation of the latter notion has identified what appear to be the same structures as sites of a non-nuclear pore mRNA export pathway [22], and it has been speculated that this process is a normal manifestation of the nuclear egress pathway used by intranuclear viruses [29], [30].…”

“…While the presence of the C-terminal fragment of the Frizzled 2 receptor, which regulates RNP formation in muscle cells, in what looks like a Lamin C-positive cape in salivary glands [22] leads us to believe that the structures we have characterized will prove to be associated with RNP export, this has yet to be shown. Some of the original studies identifying cytoplasmic capes noted that these greatly increase in abundance in the mid to late third instar [17], [31], and it will be interesting to see if the assembly of these structures responds to ecdysone or other signaling molecules during larval development.…”