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Article ; Online: Four-dimensional quantitative analysis of cell plate development using lattice light sheet microscopy identifies robust transition points between growth phases.

Sinclair, Rosalie / Wang, Minmin / Jawaid, Muhammad Zaki / Longkumer, Toshisangba / Aaron, Jesse / Rossetti, Blair / Wait, Eric / McDonald, Kent / Cox, Daniel / Heddleston, John / Wilkop, Thomas / Drakakaki, Georgia

Journal of experimental botany

2024

Abstract: Cell plate formation during cytokinesis entails multiple stages occurring concurrently and requiring orchestrated vesicle delivery, membrane remodeling, and timely polysaccharide deposition, such as callose. Understanding such a dynamic process requires ... ...

Abstract	Cell plate formation during cytokinesis entails multiple stages occurring concurrently and requiring orchestrated vesicle delivery, membrane remodeling, and timely polysaccharide deposition, such as callose. Understanding such a dynamic process requires dissection in time and space; this has been a major hurdle in studying cytokinesis. Using lattice light sheet microscopy (LLSM) we studied cell plate development in four dimensions, through the behavior of the cytokinesis specific GTPase YFP-RABA2a vesicles. We monitored the entire length of cell plate development, from its first emergence, with the aid of YFP-RABA2a, both in the presence and absence of cytokinetic callose. By developing a robust cytokinetic vesicle volume analysis pipeline, we identified distinct behavioral patterns, allowing the identification of three easily trackable, cell plate developmental phases. Notably, the phase transition between phase I and phase II is striking, indicating a switch from membrane accumulation to the recycling of excess membrane material. We interrogated the role of callose using pharmacological inhibition with LLSM and electron microscopy. Loss of callose inhibited the phase transitions, establishing the critical role and timing of the polysaccharide deposition in cell plate expansion and maturation. This study exemplifies the power of combining LLSM with quantitative analysis to decode and untangle such a complex process.
Language	English
Publishing date	2024-03-04
Publishing country	England
Document type	Journal Article
ZDB-ID	2976-2
ISSN	1460-2431 ; 0022-0957
ISSN (online)	1460-2431
ISSN	0022-0957
DOI	10.1093/jxb/erae091
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Article ; Online: Frontline Science: Dynamic cellular and subcellular features of migrating leukocytes revealed by in vivo lattice lightsheet microscopy.

Manley, Harriet R / Potter, David L / Heddleston, John M / Chew, Teng-Leong / Keightley, M Cristina / Lieschke, Graham J

Journal of leukocyte biology

2020 Volume 108, Issue 2, Page(s) 455–468

Abstract: Neutrophil and macrophage (Mϕ) migration underpin the inflammatory response. However, the fast velocity, multidirectional instantaneous movement, and plastic, ever-changing shape of phagocytes confound high-resolution intravital imaging. Lattice ... ...

Abstract	Neutrophil and macrophage (Mϕ) migration underpin the inflammatory response. However, the fast velocity, multidirectional instantaneous movement, and plastic, ever-changing shape of phagocytes confound high-resolution intravital imaging. Lattice lightsheet microscopy (LLSM) captures highly dynamic cell morphology at exceptional spatiotemporal resolution. We demonstrate the first extensive application of LLSM to leukocytes in vivo, utilizing optically transparent zebrafish, leukocyte-specific reporter lines that highlighted subcellular structure, and a wounding assay for leukocyte migration. LLSM revealed details of migrating leukocyte morphology, and permitted intricate, volumetric interrogation of highly dynamic activities within their native physiological setting. Very thin, recurrent uropod extensions must now be considered a characteristic feature of migrating neutrophils. LLSM resolved trailing uropod extensions, demonstrating their surprising length, and permitting quantitative assessment of cytoskeletal contributions to their evanescent form. Imaging leukocytes in blood vessel microenvironments at LLSM's spatiotemporal resolution displayed blood-flow-induced neutrophil dynamics and demonstrated unexpected leukocyte-endothelial interactions such as leukocyte-induced endothelial deformation against the intravascular pressure. LLSM of phagocytosis and cell death provided subcellular insights and uncovered novel behaviors. Collectively, we provide high-resolution LLSM examples of leukocyte structures (filopodia lamellipodia, uropod extensions, vesicles), and activities (interstitial and intravascular migration, leukocyte rolling, phagocytosis, cell death, and cytoplasmic ballooning). Application of LLSM to intravital leukocyte imaging sets the stage for transformative studies into the cellular and subcellular complexities of phagocyte biology.
MeSH term(s)	Animals ; Animals, Genetically Modified ; Biomarkers ; Cell Adhesion ; Cell Death ; Chemotaxis, Leukocyte/physiology ; Endothelium, Vascular/metabolism ; Fluorescent Antibody Technique ; Intravital Microscopy/methods ; Leukocytes/cytology ; Leukocytes/physiology ; Macrophages/cytology ; Macrophages/physiology ; Models, Biological ; Neutrophils/cytology ; Neutrophils/physiology ; Phagocytosis ; Zebrafish
Chemical Substances	Biomarkers
Language	English
Publishing date	2020-04-23
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	605722-6
ISSN	1938-3673 ; 0741-5400
ISSN (online)	1938-3673
ISSN	0741-5400
DOI	10.1002/JLB.3HI0120-589R
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Article ; Online: Quantifying Molecular Dynamics within Complex Cellular Morphologies using LLSM-FRAP.

Colin-York, Huw / Heddleston, John / Wait, Eric / Karedla, Narain / deSantis, Michael / Khuon, Satya / Chew, Teng-Leong / Sbalzarini, Ivo F / Fritzsche, Marco

Small methods

2022 Volume 6, Issue 6, Page(s) e2200149

Abstract: Quantifying molecular dynamics within the context of complex cellular morphologies is essential toward understanding the inner workings and function of cells. Fluorescence recovery after photobleaching (FRAP) is one of the most broadly applied techniques ...

Abstract	Quantifying molecular dynamics within the context of complex cellular morphologies is essential toward understanding the inner workings and function of cells. Fluorescence recovery after photobleaching (FRAP) is one of the most broadly applied techniques to measure the reaction diffusion dynamics of molecules in living cells. FRAP measurements typically restrict themselves to single-plane image acquisition within a subcellular-sized region of interest due to the limited temporal resolution and undesirable photobleaching induced by 3D fluorescence confocal or widefield microscopy. Here, an experimental and computational pipeline combining lattice light sheet microscopy, FRAP, and numerical simulations, offering rapid and minimally invasive quantification of molecular dynamics with respect to 3D cell morphology is presented. Having the opportunity to accurately measure and interpret the dynamics of molecules in 3D with respect to cell morphology has the potential to reveal unprecedented insights into the function of living cells.
MeSH term(s)	Diffusion ; Fluorescence Recovery After Photobleaching/methods ; Molecular Dynamics Simulation ; Photobleaching
Language	English
Publishing date	2022-03-28
Publishing country	Germany
Document type	Journal Article
ISSN	2366-9608
ISSN (online)	2366-9608
DOI	10.1002/smtd.202200149
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Article ; Online: An actin-based protrusion originating from a podosome-enriched region initiates macrophage fusion.

Faust, James J / Balabiyev, Arnat / Heddleston, John M / Podolnikova, Nataly P / Baluch, D Page / Chew, Teng-Leong / Ugarova, Tatiana P

Molecular biology of the cell

2019 Volume 30, Issue 17, Page(s) 2254–2267

Abstract: Macrophage fusion resulting in the formation of multinucleated giant cells occurs in a variety of chronic inflammatory diseases, yet the mechanism responsible for initiating this process is unknown. Here, we used live cell imaging to show that actin- ... ...

Abstract	Macrophage fusion resulting in the formation of multinucleated giant cells occurs in a variety of chronic inflammatory diseases, yet the mechanism responsible for initiating this process is unknown. Here, we used live cell imaging to show that actin-based protrusions at the leading edge initiate macrophage fusion. Phase-contrast video microscopy demonstrated that in the majority of events, short protrusions (∼3 µm) between two closely apposed cells initiated fusion, but occasionally we observed long protrusions (∼12 µm). Using macrophages isolated from LifeAct mice and imaging with lattice light sheet microscopy, we further found that fusion-competent protrusions formed at sites enriched in podosomes. Inducing fusion in mixed populations of GFP- and mRFP-LifeAct macrophages showed rapid spatial overlap between GFP and RFP signal at the site of fusion. Cytochalasin B strongly reduced fusion and when rare fusion events occurred, protrusions were not observed. Fusion of macrophages deficient in Wiskott-Aldrich syndrome protein and Cdc42, key molecules involved in the formation of actin-based protrusions and podosomes, was also impaired both in vitro and in vivo. Finally, inhibiting the activity of the Arp2/3 complex decreased fusion and podosome formation. Together these data suggest that an actin-based protrusion formed at the leading edge initiates macrophage fusion.
MeSH term(s)	Actin-Related Protein 2-3 Complex/metabolism ; Actins/metabolism ; Animals ; Cell Communication ; Cell Movement ; Cytochalasin B/metabolism ; Female ; Macrophages/metabolism ; Male ; Membrane Fusion/physiology ; Mice ; Mice, Inbred C57BL ; Microscopy, Fluorescence/methods ; Podosomes/metabolism ; Wiskott-Aldrich Syndrome Protein/metabolism ; cdc42 GTP-Binding Protein/metabolism
Chemical Substances	Actin-Related Protein 2-3 Complex ; Actins ; Wiskott-Aldrich Syndrome Protein ; Cytochalasin B (3CHI920QS7) ; cdc42 GTP-Binding Protein (EC 3.6.5.2)
Language	English
Publishing date	2019-06-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1098979-1
ISSN	1939-4586 ; 1059-1524
ISSN (online)	1939-4586
ISSN	1059-1524
DOI	10.1091/mbc.E19-01-0009
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Zs.A 2853: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Actin cables and comet tails organize mitochondrial networks in mitosis.

Moore, Andrew S / Coscia, Stephen M / Simpson, Cory L / Ortega, Fabian E / Wait, Eric C / Heddleston, John M / Nirschl, Jeffrey J / Obara, Christopher J / Guedes-Dias, Pedro / Boecker, C Alexander / Chew, Teng-Leong / Theriot, Julie A / Lippincott-Schwartz, Jennifer / Holzbaur, Erika L F

Nature

2021 Volume 591, Issue 7851, Page(s) 659–664

Abstract: Symmetric cell division requires the even partitioning of genetic information and cytoplasmic contents between daughter cells. Whereas the mechanisms coordinating the segregation of the genome are well known, the processes that ensure organelle ... ...

Abstract	Symmetric cell division requires the even partitioning of genetic information and cytoplasmic contents between daughter cells. Whereas the mechanisms coordinating the segregation of the genome are well known, the processes that ensure organelle segregation between daughter cells remain less well understood
MeSH term(s)	Actin Cytoskeleton/chemistry ; Actin Cytoskeleton/metabolism ; Actins/chemistry ; Actins/metabolism ; Animals ; Cell Division ; Cell Line ; Cytokinesis ; Endoplasmic Reticulum/metabolism ; Hippocampus/cytology ; Hippocampus/embryology ; Humans ; Mitochondria/chemistry ; Mitochondria/metabolism ; Mitosis ; Neurons ; Rats
Chemical Substances	Actins
Language	English
Publishing date	2021-03-03
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/s41586-021-03309-5
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Zs.A 26: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: FMNL2 regulates dynamics of fascin in filopodia.

Pfisterer, Karin / Levitt, James / Lawson, Campbell D / Marsh, Richard J / Heddleston, John M / Wait, Eric / Ameer-Beg, Simon Morris / Cox, Susan / Parsons, Maddy

The Journal of cell biology

2020 Volume 219, Issue 5

Abstract: Filopodia are peripheral F-actin-rich structures that enable cell sensing of the microenvironment. Fascin is an F-actin-bundling protein that plays a key role in stabilizing filopodia to support efficient adhesion and migration. Fascin is also highly up- ... ...

Abstract	Filopodia are peripheral F-actin-rich structures that enable cell sensing of the microenvironment. Fascin is an F-actin-bundling protein that plays a key role in stabilizing filopodia to support efficient adhesion and migration. Fascin is also highly up-regulated in human cancers, where it increases invasive cell behavior and correlates with poor patient prognosis. Previous studies have shown that fascin phosphorylation can regulate F-actin bundling, and that this modification can contribute to subcellular fascin localization and function. However, the factors that regulate fascin dynamics within filopodia remain poorly understood. In the current study, we used advanced live-cell imaging techniques and a fascin biosensor to demonstrate that fascin phosphorylation, localization, and binding to F-actin are highly dynamic and dependent on local cytoskeletal architecture in cells in both 2D and 3D environments. Fascin dynamics within filopodia are under the control of formins, and in particular FMNL2, that binds directly to dephosphorylated fascin. Our data provide new insight into control of fascin dynamics at the nanoscale and into the mechanisms governing rapid cytoskeletal adaptation to environmental changes. This filopodia-driven exploration stage may represent an essential regulatory step in the transition from static to migrating cancer cells.
MeSH term(s)	Actins/genetics ; Biosensing Techniques ; Carrier Proteins/genetics ; Carrier Proteins/isolation & purification ; Cell Adhesion/genetics ; Cell Movement/genetics ; Cellular Microenvironment/genetics ; Formins/genetics ; HeLa Cells ; Humans ; Microfilament Proteins/genetics ; Microfilament Proteins/isolation & purification ; Molecular Imaging ; Neoplasms/genetics ; Neoplasms/pathology ; Phosphorylation ; Protein Binding/genetics ; Pseudopodia/genetics ; Pseudopodia/metabolism
Chemical Substances	Actins ; Carrier Proteins ; FMNL2 protein, human ; Formins ; Microfilament Proteins ; fascin (146808-54-0)
Language	English
Publishing date	2020-04-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	218154-x
ISSN	1540-8140 ; 0021-9525
ISSN (online)	1540-8140
ISSN	0021-9525
DOI	10.1083/jcb.201906111
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Article ; Online: Developmentally programmed germ cell remodelling by endodermal cell cannibalism.

Abdu, Yusuff / Maniscalco, Chelsea / Heddleston, John M / Chew, Teng-Leong / Nance, Jeremy

Nature cell biology

2016 Volume 18, Issue 12, Page(s) 1302–1310

Abstract: Primordial germ cells (PGCs) in many species associate intimately with endodermal cells, but the significance of such interactions is largely unexplored. Here, we show that Caenorhabditis elegans PGCs form lobes that are removed and digested by ... ...

Abstract	Primordial germ cells (PGCs) in many species associate intimately with endodermal cells, but the significance of such interactions is largely unexplored. Here, we show that Caenorhabditis elegans PGCs form lobes that are removed and digested by endodermal cells, dramatically altering PGC size and mitochondrial content. We demonstrate that endodermal cells do not scavenge lobes PGCs shed, but rather, actively remove lobes from the cell body. CED-10 (Rac)-induced actin, DYN-1 (dynamin) and LST-4 (SNX9) transiently surround lobe necks and are required within endodermal cells for lobe scission, suggesting that scission occurs through a mechanism resembling vesicle endocytosis. These findings reveal an unexpected role for endoderm in altering the contents of embryonic PGCs, and define a form of developmentally programmed cell remodelling involving intercellular cannibalism. Active roles for engulfing cells have been proposed in several neuronal remodelling events, suggesting that intercellular cannibalism may be a more widespread method used to shape cells than previously thought.
MeSH term(s)	Animals ; Caenorhabditis elegans/cytology ; Caenorhabditis elegans Proteins/metabolism ; Cellular Reprogramming ; Cytophagocytosis ; Dynamins/metabolism ; Endoderm/cytology ; Germ Cells/cytology ; Germ Cells/metabolism ; Mitochondria/metabolism
Chemical Substances	Caenorhabditis elegans Proteins ; Dynamins (EC 3.6.5.5)
Language	English
Publishing date	2016-11-14
Publishing country	England
Document type	Journal Article
ZDB-ID	1474722-4
ISSN	1476-4679 ; 1465-7392
ISSN (online)	1476-4679
ISSN	1465-7392
DOI	10.1038/ncb3439
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Zs.A 5169: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Fabricating Optical-quality Glass Surfaces to Study Macrophage Fusion.

Faust, James J / Christenson, Wayne / Doudrick, Kyle / Heddleston, John / Chew, Teng-Leong / Lampe, Marko / Balabiyev, Arnat / Ros, Robert / Ugarova, Tatiana P

Journal of visualized experiments : JoVE

2018 , Issue 133

Abstract: Visualizing the formation of multinucleated giant cells (MGCs) from living specimens has been challenging due to the fact that most live imaging techniques require propagation of light through glass, but on glass macrophage fusion is a rare event. This ... ...

Abstract	Visualizing the formation of multinucleated giant cells (MGCs) from living specimens has been challenging due to the fact that most live imaging techniques require propagation of light through glass, but on glass macrophage fusion is a rare event. This protocol presents the fabrication of several optical-quality glass surfaces where adsorption of compounds containing long-chain hydrocarbons transforms glass into a fusogenic surface. First, preparation of clean glass surfaces as starting material for surface modification is described. Second, a method is provided for the adsorption of compounds containing long-chain hydrocarbons to convert non-fusogenic glass into a fusogenic substrate. Third, this protocol describes fabrication of surface micropatterns that promote a high degree of spatiotemporal control over MGC formation. Finally, fabricating glass bottom dishes is described. Examples of use of this in vitro cell system as a model to study macrophage fusion and MGC formation are shown.
MeSH term(s)	Cell Fusion/instrumentation ; Cell Fusion/methods ; Giant Cells/cytology ; Glass/chemistry ; Macrophages/cytology
Language	English
Publishing date	2018-03-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Video-Audio Media
ISSN	1940-087X
ISSN (online)	1940-087X
DOI	10.3791/56866
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Article ; Online: Software for lattice light-sheet imaging of FRET biosensors, illustrated with a new Rap1 biosensor.

O'Shaughnessy, Ellen C / Stone, Orrin J / LaFosse, Paul K / Azoitei, Mihai L / Tsygankov, Denis / Heddleston, John M / Legant, Wesley R / Wittchen, Erika S / Burridge, Keith / Elston, Timothy C / Betzig, Eric / Chew, Teng-Leong / Adalsteinsson, David / Hahn, Klaus M

The Journal of cell biology

2019 Volume 218, Issue 9, Page(s) 3153–3160

Abstract: Lattice light-sheet microscopy (LLSM) is valuable for its combination of reduced photobleaching and outstanding spatiotemporal resolution in 3D. Using LLSM to image biosensors in living cells could provide unprecedented visualization of rapid, localized ... ...

Abstract	Lattice light-sheet microscopy (LLSM) is valuable for its combination of reduced photobleaching and outstanding spatiotemporal resolution in 3D. Using LLSM to image biosensors in living cells could provide unprecedented visualization of rapid, localized changes in protein conformation or posttranslational modification. However, computational manipulations required for biosensor imaging with LLSM are challenging for many software packages. The calculations require processing large amounts of data even for simple changes such as reorientation of cell renderings or testing the effects of user-selectable settings, and lattice imaging poses unique challenges in thresholding and ratio imaging. We describe here a new software package, named ImageTank, that is specifically designed for practical imaging of biosensors using LLSM. To demonstrate its capabilities, we use a new biosensor to study the rapid 3D dynamics of the small GTPase Rap1 in vesicles and cell protrusions.
MeSH term(s)	Biosensing Techniques ; Fluorescence Resonance Energy Transfer ; Human Umbilical Vein Endothelial Cells/cytology ; Human Umbilical Vein Endothelial Cells/metabolism ; Humans ; Image Processing, Computer-Assisted ; Microscopy, Fluorescence ; Signal Transduction ; Software ; Telomere-Binding Proteins/genetics ; Telomere-Binding Proteins/metabolism
Chemical Substances	TERF2IP protein, human ; Telomere-Binding Proteins
Language	English
Publishing date	2019-08-23
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	218154-x
ISSN	1540-8140 ; 0021-9525
ISSN (online)	1540-8140
ISSN	0021-9525
DOI	10.1083/jcb.201903019
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Article ; Online: Endothelial junctional membrane protrusions serve as hotspots for neutrophil transmigration.

eLife

2021 Volume 10

Abstract: Upon inflammation, leukocytes rapidly transmigrate across the endothelium to enter the inflamed tissue. Evidence accumulates that leukocytes use preferred exit sites, alhough it is not yet clear how these hotspots in the endothelium are defined and how ... ...

Abstract	Upon inflammation, leukocytes rapidly transmigrate across the endothelium to enter the inflamed tissue. Evidence accumulates that leukocytes use preferred exit sites, alhough it is not yet clear how these hotspots in the endothelium are defined and how they are recognized by the leukocyte. Using lattice light sheet microscopy, we discovered that leukocytes prefer endothelial membrane protrusions at cell junctions for transmigration. Phenotypically, these junctional membrane protrusions are present in an asymmetric manner, meaning that one endothelial cell shows the protrusion and the adjacent one does not. Consequently, leukocytes cross the junction by migrating underneath the protruding endothelial cell. These protrusions depend on Rac1 activity and by using a photo-activatable Rac1 probe, we could artificially generate local exit-sites for leukocytes. Overall, we have discovered a new mechanism that uses local induced junctional membrane protrusions to facilitate/steer the leukocyte escape/exit from inflamed vessel walls.
MeSH term(s)	Animals ; Cell Line ; Gene Expression Regulation/physiology ; Green Fluorescent Proteins ; Human Umbilical Vein Endothelial Cells ; Humans ; Intercellular Junctions/physiology ; Male ; Mice ; Mice, Transgenic ; Microscopy, Electron, Transmission ; Muscle, Skeletal/physiology ; Muscle, Skeletal/ultrastructure ; Neutrophils/physiology
Chemical Substances	enhanced green fluorescent protein ; Green Fluorescent Proteins (147336-22-9)
Language	English
Publishing date	2021-08-25
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.66074
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