Cellular Logistics: Unraveling the Interplay Between Microtubule Organization and Intracellular Transport

Burute, Mithila; Kapitein, Lukas C.

doi:10.1146/annurev-cellbio-100818-125149

Cited by 72 publications

(66 citation statements)

References 189 publications

(238 reference statements)

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“…We suggested that conduits could span across the cell to mediate the comparison. No such conduits have been identified but they could be microtubules or other organelles ( Burute and Kapitein, 2019 ).…”

Section: Resultsmentioning

confidence: 99%

Planar cell polarity in the larval epidermis ofDrosophilaand the role of microtubules

Pietra

Lawrence

et al. 2020

Preprint

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10We investigate the mechanisms of planar cell polarity (PCP) in the larval epidermis of 11 Drosophila. Measurements of the amount of Dachsous across the segment find a peak 12 located near the rear of the anterior compartment. Localisation of Dachs and 13 orientation of ectopic denticles reveal the polarity of every cell in the segment. We 14 discuss how well these findings evidence a zigzag gradient model of Dachsous activity. 15 Several groups have proposed that Dachsous and Fat fix the direction of PCP via 16 oriented microtubules that transport PCP proteins to one side of the cell. We test this 17 proposition in the larval cells and find that most microtubules grow perpendicularly 18 to the axis of PCP. We find no significant bias in the polarity of those microtubules 19 aligned close to that axis. We also reexamine published data from the pupal abdomen 20 and fail to find evidence supporting the hypothesis that microtubular orientation 21 draws the arrow of PCP. 22As cells construct embryos and organs they need access to vectorial information that 24 informs them, for example, which way to migrate, divide, extend axons or how to 25 orient protrusions. In Drosophila there are (at least) two conserved genetic systems 26 Page 2 of 32 that generate vectorial information, and here we are concerned with only one of those, 27 the Dachsous/Fat system. Dachsous (Ds) and Fat (Ft) are large atypical cadherin 28 molecules that form heterodimeric bridges from cell to cell that help build planar cell 29 polarity (PCP) in one cell and also convey polarity between cells (Ma et al., 2003; 30 Matakatsu and Blair, 2004; Casal et al., 2006; Lawrence and Casal, 2018). The 31 activity of Ft is increased and Ds is reduced when they are phosphorylated by a third 32 molecule, Four-jointed (Fj), a Golgi-based kinase (Ishikawa et al., 2008; Brittle et al., 33 2010; Simon et al., 2010). The distribution of Ds, Ft and Fj and the interaction 34 between these molecules together determine what we describe as "Ds activity", by 35 which we mean the propensity of Ds on one cell to bind to Ft in the neighbouring cell. 36 Experiments suggest that, using the disposition and orientation of Ds-Ft bridges, each 37 cell compares the Ds activity of its two neighbours and points its denticles towards the 38 neighbour with the higher Ds activity. In this way, the local slopes in a landscape of Ds 39 activity determine polarities of all the cells (Casal et al., 2002; see Lawrence and 40 Casal, 2018 for more explanation). 41 A model: the ventral epidermis of the Drosophila larva 42Each segment of the larva is divided by cell lineage into an anterior (A) and a 43 posterior (P) compartment. In the ventral epidermis, a limited region of the segment 44 makes rows of thorny denticles that are polarised in an almost invariant pattern, while 45 the larger part of each segment makes no denticles and therefore its polarity is not 46 known (Figure 1-figure supplement 1). The Ds/Ft system is alone effective in 47 48 the "core" or Stan/Fz system (Casal et ...

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Section: Resultsmentioning

confidence: 99%

Planar cell polarity in the larval epidermis ofDrosophilaand the role of microtubules

Pietra

Lawrence

et al. 2020

Preprint

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“…Besides chromosome segregation, microtubule organization is pivotal for a large number of cellular processes. This includes the regulation of cell shape by interacting with actin and actomyosin [50,51] and intracellular transport by acting as transport routes for a magnitude of cargo such as mRNA, protein and vesicles [52,53]. Furthermore, microtubules are involved in: (1) Formation of primary cilia [54] as well as motile cilia contributing to cell movement [55] or the generation of liquid flow [56].…”

Section: Control Of Microtubule Functionmentioning

confidence: 99%

Microtubule Organization in Striated Muscle Cells

Becker

Leone

Engel

2020

Cells

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Distinctly organized microtubule networks contribute to the function of differentiated cell types such as neurons, epithelial cells, skeletal myotubes, and cardiomyocytes. In striated (i.e., skeletal and cardiac) muscle cells, the nuclear envelope acts as the dominant microtubule-organizing center (MTOC) and the function of the centrosome—the canonical MTOC of mammalian cells—is attenuated, a common feature of differentiated cell types. We summarize the mechanisms known to underlie MTOC formation at the nuclear envelope, discuss the significance of the nuclear envelope MTOC for muscle function and cell cycle progression, and outline potential mechanisms of centrosome attenuation.

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“…As noted in this report, following overexpression of NC1peptide in the testis, it induces extensive disruption of the MT-based tracks across the seminiferous epithelium, which are known to support intracellular trafficking of organelles (eg, endocytic vesicles, phagosomes, residual bodies, food vacuoles) and also motor proteins (eg, MT-dependent motor proteins dynein 1, kinesins) that support cargo transport. 78,79 For instance, in control testes, the MT-based tracks that lay perpendicular to the basement membrane have become shortened, truncated and mis-aligned and noted as early as 6 hours following NC1 overexpression. This notable defect in MT tracks thus impedes intracellular protein trafficking events, including the timely transport of organelles (eg, endocytic vesicles, residual bodies) across the seminiferous epithelium to sustain the epithelial cycle.…”

Section: F I G U R E 1 0 Overexpression Of Eb1 Blocks Nc1-mediated Dimentioning

confidence: 99%

NC1‐peptide regulates spermatogenesis through changes in cytoskeletal organization mediated by EB1

Liu

et al. 2020

FASEB j.

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are contributed equally to the completion of this work.Abbreviations: +TIP, microtubule plus (+)-end tracking protein; AJ, adherens junction; aPKC, atypical protein kinase C; Arp3, actin-related protein 3; BM, basement membrane; BTB, blood-testis barrier; Crb3, Crumbs homolog-3; DAPI, 4', 6-diamidino-2-phenylindole; Dia1, Diaphanous-related formin-1; Dlg1, Discs large 1; Dvl3, Disheveled 3; EB1, end-binding protein 1; Eps8, epidermal growth factor receptor pathway substrate 8; ES, ectoplasmic specialization; Fzd3, Frizzled 3; F12/DMEM, Ham's F12 nutrient mixture/Dulbecco's modified Eagle's medium (1:1, vol/vol); GAPDH, glyceraldehyde 3-phosphate dehydrogenase; GJ, gap junction; H&E, hematoxylin and eosin staining; IF, immunofluorescence microscopy; IgG, immunoglobulin; IP, immunoprecipitation; MAP1a, microtubule-associated protein 1a; MARK, microtubule affinity-regulatory kinase 4; MT, microtubule; mTOR, mammalian target of rapamycin; NC1 domain, non-collagenous domain 1; Pals1, protein associated with Lin-7 1; PatJ, Pals1-associated tight junction protein; Par6, partitioning-defective (Par) protein 6; rpS6, ribosomal protein S6; TJ, tight junction; ZO-1, zonula occludens-1. AbstractDuring the epithelial cycle of spermatogenesis, different sets of cellular events take place across the seminiferous epithelium in the testis. For instance, remodeling of the blood-testis barrier (BTB) that facilitates the transport of preleptotene spermatocytes across the immunological barrier and the release of sperms at spermiation take place at the opposite ends of the epithelium simultaneously at stage VIII of the epithelial cycle. These cellular events are tightly coordinated via locally produced regulatory biomolecules. Studies have shown that collagen α3 (IV) chains, a major constituent component of the basement membrane, release the non-collagenous (NC) 1 domain, a 28-kDa peptide, designated NC1-peptide, from the C-terminal region, via the action of MMP-9 (matrix metalloproteinase 9). NC1-peptide was found to be capable of inducing BTB remodeling and spermatid release across the epithelium. As such, the NC1-peptide is an endogenously produced biologically active peptide which coordinates these cellular events across the epithelium in stage VIII tubules. Herein, we used an animal model, wherein NC1-peptide cloned into the pCI-neo mammalian expression vector was overexpressed in the testis, to better understanding the molecular mechanism by which NC1-peptide regulated spermatogenic function. It was shown that NC1-peptide induced considerable downregulation on a number of cell polarity and planar cell polarity (PCP) proteins, and studies have shown these polarity and PCP proteins modulate spermatid polarity and adhesion via their effects on microtubule (MT) and F-actin cytoskeletal organization across the epithelium. More important, NC1-peptide exerted its effects by downregulating the expression of microtubule (MT) plus-end tracking protein (+TIP) called EB1 (end-binding protein 1). We cloned the full-length EB1 cDNA for its ov...

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Cellular Logistics: Unraveling the Interplay Between Microtubule Organization and Intracellular Transport

Cited by 72 publications

References 189 publications

Planar cell polarity in the larval epidermis ofDrosophilaand the role of microtubules

Planar cell polarity in the larval epidermis ofDrosophilaand the role of microtubules

Microtubule Organization in Striated Muscle Cells

NC1‐peptide regulates spermatogenesis through changes in cytoskeletal organization mediated by EB1

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