Loss of function of the<i>Drosophila</i>Ninein-related centrosomal protein Bsg25D causes mitotic defects and impairs embryonic development

Kowanda, Michelle; Bergalet, Julie; Wieczorek, Michał W.; Brouhard, Gary J.; Lécuyer, Éric; Lasko, Paul

doi:10.1242/bio.019638

Cited by 27 publications

(43 citation statements)

References 77 publications

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“…We examined the distribution of Bsg25D / ninein ( nin ) mRNA with smFISH. Nin is a pericentrosomal protein ( Kowanda et al, 2016 ; Zheng et al, 2016 ) and nin mRNA localizes near centrosomes in syncytial embryos ( Lécuyer et al, 2007 ). In NC 11 and NC 12 embryos, nin mRNA appeared evenly dispersed within the cytosol, similar to gapdh ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Quantitative analysis of subcellular distributions with an open-source, object-based tool

Ryder

Lerit

2020

Biology Open

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The subcellular localization of objects, such as organelles, proteins, or other molecules, instructs cellular form and function. Understanding the underlying spatial relationships between objects through colocalization analysis of microscopy images is a fundamental approach used to inform biological mechanisms. We generated an automated and customizable computational tool, the SubcellularDistribution pipeline, to facilitate object-based image analysis from 3D fluorescence microcopy images. To test the utility of the SubcellularDistribution pipeline, we examined the subcellular distribution of mRNA relative to centrosomes within syncytial Drosophila embryos. Centrosomes are microtubule-organizing centers, and RNA enrichments at centrosomes are of emerging importance. Our open-source and freely available software detected RNA distributions comparably to commercially available image analysis software. The SubcellularDistribution pipeline is designed to guide the user through the complete process of preparing image analysis data for publication, from image segmentation and data processing to visualization.

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Section: Resultsmentioning

confidence: 99%

Quantitative analysis of subcellular distributions with an open-source, object-based tool

Ryder

Lerit

2020

Biology Open

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“…The γ-TuRC-tethering protein NEDD1 is one potential candidate involved in microtubule anchoring at centrosomes as it can tether minus ends to ectopic locations . Another protein frequently implicated in minus-end anchoring at both centrosomes and non-centrosomal sites is ninein (Goldspink et al, 2017;Kowanda et al, 2016;Mogensen et al, 2000;Wang et al, 2015); however, it is unclear whether ninein can recognize γ-TuRCbound or -free microtubule minus ends.…”

Section: Microtubule Minus-end Anchoring To Subcellular Structuresmentioning

confidence: 99%

Microtubule minus-end regulation at a glance

Akhmanova

Steinmetz

2019

Journal of Cell Science

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Microtubules are cytoskeletal filaments essential for numerous aspects of cell physiology. They are polarized polymeric tubes with a fast growing plus end and a slow growing minus end. In this Cell Science at a Glance article and the accompanying poster, we review the current knowledge on the dynamics and organization of microtubule minus ends. Several factors, including the γ-tubulin ring complex, CAMSAP/Patronin, ASPM/Asp, SPIRAL2 (in plants) and the KANSL complex recognize microtubule minus ends and regulate their nucleation, stability and interactions with partners, such as microtubule severing enzymes, microtubule depolymerases and protein scaffolds. Together with minus-end-directed motors, these microtubule minus-end targeting proteins (−TIPs) also control the formation of microtubule-organizing centers, such as centrosomes and spindle poles, and mediate microtubule attachment to cellular membrane structures, including the cell cortex, Golgi complex and the cell nucleus. Structural and functional studies are starting to reveal the molecular mechanisms by which dynamic −TIP networks control microtubule minus ends.

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“…While Nin's molecular mechanisms of action are not well understood, the conserved N-terminal domain of Drosophila Nin can associate directly with MTs (Kowanda et al, 2016). Nin localizes to Drosophila muscle and wing ncMTOCs (Zheng et al, 2016) and to the apparent ncMTOC in oocytes (Kowanda et al, 2016). We found that Nin localized to the fat body perinuclear ncMTOC ( Figure 19A).…”

Section: Patronin Cooperates With Ninein To Organize the Fat Body Ncmmentioning

confidence: 64%

“…Nin is a MT minus-end protein with anchoring function at the centriole subdistal appendages in mammals (Mogensen et al, 2000;Delgehyr et al, 2005), but Nin also has ncMTOC roles in mammals, Drosophila and C. elegans (Mogensen et al, 2000;Wang et al, 2015b;Zheng et al, 2016;Goldspink et al, 2017). While Nin's molecular mechanisms of action are not well understood, the conserved N-terminal domain of Drosophila Nin can associate directly with MTs (Kowanda et al, 2016). Nin localizes to Drosophila muscle and wing ncMTOCs (Zheng et al, 2016) and to the apparent ncMTOC in oocytes (Kowanda et al, 2016).…”

Section: Patronin Cooperates With Ninein To Organize the Fat Body Ncmmentioning

confidence: 99%

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

Zheng¹,

Buchwalter²,

Zheng³

et al. 2019

Preprint

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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 noncentrosomal MTs and does so independently of the widespread MT nucleation factor g-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. Highlights• A novel perinuclear MTOC in differentiated fat body cells • The predominant nucleator, g-tubulin, is not required at the fat body ncMTOC • Msp300/Nesprin organizes the ncMTOC at the nuclear surface by recruiting Patronin/CAMSAP and the spectraplakin Shot • Patronin cooperates with Ninein to control MT assembly at the fat body ncMTOC by recruiting Msps • Msps, a MT polymerase, is essential for radial MT elongation from the fat body ncMTOC • Patronin and Msps associate • The ncMTOC and radial MTs, but not actin, control nuclear positioning in the fat body • The fat body MTOC controls retrograde endocytic trafficking to regulate plasma membrane growth and secretion of basement membrane proteins Here we report the discovery of an ncMTOC that is assembled on the surface of nuclei in Drosophila larval fat body cells, a differentiated cell type that has critical secretory functions and serves the metabolic needs of the organism. Assembly of this perinuclear ncMTOC requires the Msp300/Nesprin (nuclear envelope spectrin repeat protein) as a primary organizer/anchor. Msp300 recruits Patronin, which functions redundantly with Ninein for MT assembly at the ncMTOC. Patronin and Ninein cooperate to recruit Msps, which is essential for the elongation of MTs from the fat body ncMTOC. Recruitment of Msps and MT assembly at the ncMTOC are independent of g-tubulin. Functionally, this ncMTOC is necessary for: 1) the regulation of nuclear positioning, 2) controlling plasma membrane growth by facilitating dynein/Rab5-mediated retrograde endosomal trafficking of excess plasma membrane, and 3) the secretion of collagen IV and other basement membrane (BM) proteins. Together, this study identifies a unique perinuclear ncMTOC with novel MT assembly mechanisms that controls physiological roles of fat body cells by supporting nuclear positioning and vital secretory functions of fat body cells.

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Loss of function of theDrosophilaNinein-related centrosomal protein Bsg25D causes mitotic defects and impairs embryonic development

Cited by 27 publications

References 77 publications

Quantitative analysis of subcellular distributions with an open-source, object-based tool

Quantitative analysis of subcellular distributions with an open-source, object-based tool

Microtubule minus-end regulation at a glance

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

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