Dendritic spine geometry and spine apparatus organization govern the spatiotemporal dynamics of calcium

Bell, Miriam; Bartol, Tom; Sejnowski, Terrence J.; Rangamani, Padmini

doi:10.1085/jgp.201812261

Cited by 77 publications

(158 citation statements)

References 127 publications

(289 reference statements)

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“…Hence, C A varies both in the radial and angular directions, indicating that curvature and varying distances between the two membranes amplifies signaling gradients. Even though the observations here are in 2D, the effect of curvature and distance holds true in 3D as has been demonstrated by us and others 3,40,41 . Dimensional analysis of Eq.…”

Section: Resultssupporting

confidence: 59%

Cell shape regulates subcellular organelle location to control early Ca2+ signal dynamics in vascular smooth muscle cells

Calizo

Bell

Ron

et al. 2020

Sci Rep

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The shape of the cell is connected to its function; however, we do not fully understand underlying mechanisms by which global shape regulates a cell’s functional capabilities. Using theory, experiments and simulation, we investigated how physiologically relevant cell shape changes affect subcellular organization, and consequently intracellular signaling, to control information flow needed for phenotypic function. Vascular smooth muscle cells going from a proliferative and motile circular shape to a contractile fusiform shape show changes in the location of the sarcoplasmic reticulum, inter-organelle distances, and differential distribution of receptors in the plasma membrane. These factors together lead to the modulation of signals transduced by the M3 muscarinic receptor/Gq/PLCβ pathway at the plasma membrane, amplifying Ca2+ dynamics in the cytoplasm, and the nucleus resulting in phenotypic changes, as determined by increased activity of myosin light chain kinase in the cytoplasm and enhanced nuclear localization of the transcription factor NFAT. Taken together, our observations show a systems level phenomenon whereby global cell shape affects subcellular organization to modulate signaling that enables phenotypic changes.

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Section: Resultssupporting

confidence: 59%

Cell shape regulates subcellular organelle location to control early Ca2+ signal dynamics in vascular smooth muscle cells

Calizo

Bell

Ron

et al. 2020

Sci Rep

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“…Intracellular pattern formation in general is based on cycling of proteins between cytosolic and membrane/cortex-bound states; see for example the Cdc42 system in budding yeast and fission yeast (33,58), the PAR system (46,59) in C. elegans, excitable RhoA pulses in C. elegans (60), Xenopus and starfish oocytes (61), and MARCKS dynamics in many cell types (62,63). Further examples include, intracellular signaling cascades (64)(65)(66)(67) and, potentially, intercellular signaling in tissues and biofilms. Our study shows that it is essential to explicitly take the bulk-surface coupling into account when one investigates such systems.…”

Section: Discussionmentioning

confidence: 99%

Bulk-surface coupling reconciles Min-protein pattern formationin vitroandin vivo

Brauns

Pawlik

Halatek

et al. 2020

Preprint

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1 Self-organisation of Min proteins is responsible for the spatial control of cell division in Escherichia coli, and has been studied both in vivo and in vitro. Intriguingly, the protein patterns observed in these settings differ qualitatively and quantitatively. This puzzling dichotomy has not been resolved to date. Here, we experimentally show that the dynamics crucially depend on the bulk-to-surface ratio, which is vastly different between the cell geometry and traditional in vitro setups. We systematically control the bulk-to-surface ratio in vitro using laterally wide microchambers with a well-controlled bulk height. A theoretical analysis shows that in vitro patterns at low bulk height are driven by the same lateral oscillation mode as pole-to-pole oscillations in vivo. At larger bulk height, additional vertical oscillation modes set in, marking the transition to a qualitatively different in vitro regime. Our work resolves the Min system's in vivo/in vitro conundrum and provides important insights on the mechanisms underlying protein patterns in bulk-surface coupled systems.

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“…prolate) whereas they could also be stretched orthogonally (i.e. oblate) in shorter spines (Fig 2D), with a possible impact on nanoscale ion flows [78]. By contrast, there was no correlation between the position of the spine or the inter-spine distance and any of the morphological parameters we measured (S2 Fig).…”

Section: Resultsmentioning

confidence: 96%

Morphologically constrained modeling of spinous inhibition in the somato-sensory cortex

Gemin

Serna

Assendorp

et al. 2020

Preprint

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Pyramidal neurons are covered by thousands of dendritic spines receiving excitatory synaptic inputs. The ultrastructure of dendritic spines shapes signal compartmentalization but ultrastructural diversity is rarely taken into account in computational models of synaptic integration. Here, we developed a 3D correlative light-electron microscopy (3D-CLEM) approach allowing the analysis of specific populations of synapses in genetically defined neuronal types in intact brain circuits. We used it to reconstruct segments of basal dendrites of layer 2/3 pyramidal neurons of adult mouse somatosensory cortex and quantify spine ultrastructural diversity. We found that 10% of spines were dually-innervated and 38% of inhibitory synapses localize to spines. Using our morphometric data to constrain a model of synaptic signal compartmentalization, we assessed the impact of spinous versus dendritic shaft inhibition. Our results indicate that spinous inhibition is locally more efficient than shaft inhibition and that it can decouple voltage and calcium signaling, potentially impacting synaptic plasticity.

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Dendritic spine geometry and spine apparatus organization govern the spatiotemporal dynamics of calcium

Cited by 77 publications

References 127 publications

Cell shape regulates subcellular organelle location to control early Ca2+ signal dynamics in vascular smooth muscle cells

Cell shape regulates subcellular organelle location to control early Ca2+ signal dynamics in vascular smooth muscle cells

Bulk-surface coupling reconciles Min-protein pattern formationin vitroandin vivo

Morphologically constrained modeling of spinous inhibition in the somato-sensory cortex

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