A perinuclear microtubule-organizing center controls nuclear positioning and basement membrane secretion

Abstract

Non-centrosomal microtubule-organizing centers (ncMTOCs) have a variety of roles presumed to serve the diverse functions of the range of cell types in which they are found. ncMTOCs are diverse in their composition, subcellular localization, and function. Here we report a novel perinuclear MTOC in Drosophila fat body cells that is anchored by Msp300/Nesprin at the cytoplasmic surface of the nucleus. Msp300 recruits the MT minus-end protein Patronin/CAMSAP, which functions redundantly with Ninein to further recruit the MT polymerase Msps/XMAP215 to assemble non-centrosomal MTs and does so independently of the widespread MT nucleation factor{gamma} -tubulin. Functionally, the fat body ncMTOC and the radial MT arrays it organizes is essential for nuclear positioning and for secretion of basement membrane components via retrograde dynein-dependent endosomal trafficking that restricts plasma membrane growth. Together, this study identifies a perinuclear ncMTOC with unique architecture and MT regulation properties that serves vital functions. HighlightsO_LIA novel perinuclear MTOC in differentiated fat body cells C_LIO_LIThe predominant nucleator,{gamma} -tubulin, is not required at the fat body ncMTOC C_LIO_LIMsp300/Nesprin organizes the ncMTOC at the nuclear surface by recruiting Patronin/CAMSAP and the spectraplakin Shot C_LIO_LIPatronin cooperates with Ninein to control MT assembly at the fat body ncMTOC by recruiting Msps C_LIO_LIMsps, a MT polymerase, is essential for radial MT elongation from the fat body ncMTOC C_LIO_LIPatronin and Msps associate C_LIO_LIThe ncMTOC and radial MTs, but not actin, control nuclear positioning in the fat body C_LIO_LIThe fat body MTOC controls retrograde endocytic trafficking to regulate plasma membrane growth and secretion of basement membrane proteins C_LI O_FIG O_LINKSMALLFIG WIDTH=175 HEIGHT=200 SRC="FIGDIR/small/888065v1_ufig1.gif" ALT="Figure 1"> View larger version (43K): org.highwire.dtl.DTLVardef@19822feorg.highwire.dtl.DTLVardef@1216914org.highwire.dtl.DTLVardef@79d0d7org.highwire.dtl.DTLVardef@17dd8a0_HPS_FORMAT_FIGEXP M_FIG C_FIG