A homeostatic apical microtubule network shortens cells for epithelial folding via a basal polarity shift

Takeda, Masaya; Sami, Mustafa M.; Wang, Yu-Chiun

doi:10.1038/s41556-017-0001-3

Cited by 64 publications

(100 citation statements)

References 46 publications

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“…These are only two of the examples where our findings are likely to hold true. There are multiple other instances, whereupon maturing and differentiating epithelial cells develop an apical microtubule meshwork, including cells of mammalian airways, and even cells in culture [16,56,57]. Furthermore, the same rules are likely to apply to squamous cells, where despite having specialized apical microtubules, the cells' depth is so small, that microtubules are constrained within a thin plane similar to that in our experimental model [58,59].…”

Section: Our System Is a Particular But Generalizable Scenariomentioning

confidence: 55%

Robustness of bidirectional microtubule network self-organization

Płochocka

Davie

Bulgakova

et al. 2019

Preprint

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Robustness of biological systems is crucial for their survival, however, for many systems its origin is an open question. Here we analyze one sub-cellular level system, the microtubule cytoskeleton. Microtubules self-organize into a network, along which cellular components are delivered to their biologically relevant locations. While individual microtubule are highly dynamic with their dynamics depends on the organism environment and genetics, network sensitivity to this dynamics would result in pathologies. Combining mathematical modelling with genetic manipulations in Drosophila, we show that the microtubule self-organization indeed does not depend on dynamics of individual microtubules, and thus is robust on the tissue level. We demonstrate the origin of this robustness via a mathematical model, suggesting this being a generic mechanism.

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Section: Our System Is a Particular But Generalizable Scenariomentioning

confidence: 55%

Robustness of bidirectional microtubule network self-organization

Płochocka

Davie

Bulgakova

et al. 2019

Preprint

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“…1 C). During 105 mid-late cellularization, Patronin::GFP shifted to a more apical localization at cell 106 junctions in both the mesoderm and ectoderm ( another study at this developmental stage (Takeda et al, 2018). During gastrulation, 108 medioapical Patronin::GFP foci localized to the center of medioapical myosin patches 109 ( Fig.…”

Section: And C; 92mentioning

confidence: 86%

“…While the regulation and organization of actomyosin during apical constriction 53 has been well-studied, the organization of the microtubule cytoskeleton and its 54 importance is less well understood. In epithelia, there is evidence for different 55 microtubule functions, such as regulating assembly or position of the adherens junctions 56 (Harris and Peifer, 2005;Stehbens et al, 2006;Meng et al, 2008;Le Droguen et al, 57 2015), recruiting apical myosin (Booth et al, 2014), regulating RhoA (Rogers et al, 58 2004;Nagae et al, 2013), and providing a counter-force resisting actomyosin 59 contraction (Takeda et al, 2018;Singh et al, 2018). Importantly, studies have shown 60 that microtubules are necessary for cell shape changes, like apical constriction (Lee and 61 Harland, 2007;Booth et al, 2014).…”

Section: Introduction 17mentioning

confidence: 99%

Microtubules stabilize intercellular contractile force transmission during tissue folding

Tserunyan

Martin

2019

Preprint

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1During development, forces transmitted between cells are critical for sculpting epithelial 2 tissues. Actomyosin contractility in the middle of the cell apex (medioapical) can change 3 cell shape (e.g., apical constriction), but can also result in force transmission between 4 cells via attachments to adherens junctions. How actomyosin networks maintain 5 attachments to adherens junctions under tension is poorly understood. Here, we 6 discovered that microtubules promote actomyosin intercellular attachments in epithelia 7during Drosophila mesoderm invagination. First, we used live imaging to show a novel 8 arrangement of the microtubule cytoskeleton during apical constriction: medioapical 9Patronin (CAMSAP) foci formed by actomyosin contraction organized an apical non-10 centrosomal microtubule network. Microtubules were required for mesoderm 11 invagination but were not necessary for initiating apical contractility or adherens junction 12 assembly. Instead, microtubules promoted connections between medioapical 13 actomyosin and adherens junctions. These results delineate a role for coordination 14

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“…Patronin/CAMSAP proteins have emerged recently as key MT regulators at ncMTOCs, though their exact functional mechanisms remain elusive (Goodwin and Vale, 2010;Wang et al, 2015b;Khanal et al, 2016;Nashchekin et al, 2016;Muroyama and Lechler, 2017;Sanchez and Feldman, 2017;Wu and Akhmanova, 2017;Martin and Akhmanova, 2018;Takeda et al, 2018;Tillery et al, 2018). Patronin protects and stablizes MT minus ends by antagonizing Kinesin-13…”

Section: A New Paradigm For Mt Assembly At Mtocsmentioning

confidence: 99%

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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A homeostatic apical microtubule network shortens cells for epithelial folding via a basal polarity shift

Cited by 64 publications

References 46 publications

Robustness of bidirectional microtubule network self-organization

Robustness of bidirectional microtubule network self-organization

Microtubules stabilize intercellular contractile force transmission during tissue folding

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

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